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Disposal and Management Solid Waste

La disposicio y manejo de los residuos solidos
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242 views162 pages

Disposal and Management Solid Waste

La disposicio y manejo de los residuos solidos
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
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Disposal and

Management of
Solid Waste
Pathogens and Diseases

Eliot Epstein
Disposal and
Management of
Solid Waste
Pathogens and Diseases
Disposal and
Management of
Solid Waste
Pathogens and Diseases

Eliot Epstein

Boca Raton London New York

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Dedication

I am dedicating this book to the people in developing


countries who need to be better informed on diseases and
their prevention and to use whatever means in their possession
to eliminate illnesses and provide better public health.
Contents
Preface.......................................................................................................................xi
Acknowledgments..................................................................................................... xv

Chapter 1 Pathogens and Diseases Associated with Disposal and


Management of Solid Waste..................................................................1
Introduction...........................................................................................1
Definitions.............................................................................................5
Sources of Pathogens in Solid Waste.................................................... 6
Infection of Humans from Solid Waste.................................................8
Summary............................................................................................. 10
References........................................................................................... 11

Chapter 2 Risk and Exposure.............................................................................. 13


Introduction......................................................................................... 13
Risk Assessment.................................................................................. 16
Hazard Assessment and Identification................................................ 17
Dose–­Response Assessment............................................................... 18
Exposure Assessment.......................................................................... 18
Risk Characterization.......................................................................... 19
References........................................................................................... 19
Suggested Reading..............................................................................20

Chapter 3 Odors as a Health Issue....................................................................... 21


Introduction......................................................................................... 21
Basic Concepts.................................................................................... 21
Odor and Health..................................................................................26
Summary............................................................................................. 28
References........................................................................................... 28

Chapter 4 Pathogens and Diseases of Solid Wastes: Municipal Solid Waste


or Garbage........................................................................................... 29
Introduction......................................................................................... 29
Pathogens and Their Diseases............................................................. 33
Vectors................................................................................................. 37
Summary............................................................................................. 38
References........................................................................................... 39

vii
viii Contents

Chapter 5 Pathogens and Diseases of Sewage Sludge, Septage, and Human


Fecal Matter........................................................................................ 41
Introduction......................................................................................... 41
Pathogens and Diseases.......................................................................44
References...........................................................................................46

Chapter 6 Pathogens in Soils............................................................................... 47


Introduction......................................................................................... 47
Bacteria................................................................................................54
Viruses................................................................................................. 57
Parasites............................................................................................... 58
Summary............................................................................................. 59
References........................................................................................... 59

Chapter 7 Geophagy and Human Pathogens in Plants........................................ 63


Introduction......................................................................................... 63
Geophagy............................................................................................ 63
Pathogens on Plants............................................................................. 67
Summary............................................................................................. 70
References........................................................................................... 70

Chapter 8 Bioaerosols.......................................................................................... 73
Introduction......................................................................................... 73
Fungi and Pathogens Commonly Found in Outdoor and Indoor
Environments...................................................................................... 76
Aspergillus fumigatus..................................................................... 79
Endotoxin.......................................................................................80
Glucans........................................................................................... 81
Actinomycetes................................................................................ 81
Mycotoxins..................................................................................... 82
References........................................................................................... 83

Chapter 9 Pathogens in Animal Waste and Manures.......................................... 87


Introduction......................................................................................... 87
Pathogens and Diseases Transmitted to Humans................................ 89
Bacteria...........................................................................................90
Viruses............................................................................................90
Parasites (Protozoans)....................................................................90
Summary............................................................................................. 93
References........................................................................................... 94

Chapter 10 Pathogens in Food and Water..............................................................97


Introduction.........................................................................................97
Foodborne Diseases............................................................................ 98
Contents ix

Waterborne Diseases......................................................................... 105


Summary........................................................................................... 109
References......................................................................................... 109

Chapter 11 Disposal and Management of Solid Waste........................................ 111


Introduction....................................................................................... 111
Landfills or Dumps........................................................................... 112
Incineration and Burning.................................................................. 112
Anaerobic Digestion.......................................................................... 113
Land Application............................................................................... 113
Composting....................................................................................... 114
Lime Stabilization............................................................................. 115
Summary........................................................................................... 115
References......................................................................................... 116
Appendix: Details of the Pathogens and Their Diseases................................... 117
Actinobacillus pleuropneumoniae.................................................... 117
Acinetobacter baumannii.................................................................. 117
Actinomyces spp................................................................................ 117
Aeromonas spp.................................................................................. 118
Ascaris lumbricoides......................................................................... 118
Bacillaceae spp.................................................................................. 119
Bacillus spp....................................................................................... 120
Bordetella spp.................................................................................... 122
Campylobacter jejuni........................................................................ 122
Cellulomonas.................................................................................... 124
Entamoeba histolytica...................................................................... 124
Enterobacteria................................................................................... 126
Escherichia coli................................................................................. 126
Klebsiella pneumonia....................................................................... 127
Micrococcus...................................................................................... 128
Mycobacterium spp........................................................................... 129
Neisseria............................................................................................ 131
Neisseria meningitidis.................................................................. 131
Neisseria gonorrhoeae................................................................. 132
Proteus spp........................................................................................ 133
Pseudomonas spp.............................................................................. 133
Salmonella spp.................................................................................. 135
Serratia plymuthica........................................................................... 137
Staphylococcus aureus...................................................................... 138
Streptococcus faecalis (Enterococcus faecalis), Streptococcus
pyogenes, and Streptococcus pneumoniae........................................ 139
Preface
Pathogens in solid waste and many of their diseases result from the disposal
and management of those same solid wastes. In developed countries, sanitation and
management of solid waste are highly controlled or regulated by local or state enti-
ties. The disposal of solid waste in developing countries is predominantly through
landfills or incineration. Environmentally safe systems such as composting are rela-
tively rare. In the United States, the exception involves human wastes after collection
and treatment that result in wastewater sludge. Land application and composting of
wastewater sludge is the preferred disposal management system in the United States.
This is not the case in many developing countries. Collection and disposal of solid
waste are poor and neglected. Human and animal wastes are often left on the surface
adjacent to residences. George (2008) points out that in India nearly 800 million per-
sons spread contagious diseases in this fashion. Even where latrines were installed,
they were not used. In developing countries, dumps and outdoor defecation can be a
major source of pathogens and bioaerosols. Not only workers are at risk but also the
general population. George (2008) indicates that in India there are between 400,000
and 1.2 million manual scavengers, who are not only affected directly by pathogens
and bioaerosols but also by pathogens and dust containing bioaerosols brought into
the home.
In developed countries, pathogens and the diseases resulting from them are
predominantly waterborne or foodborne. There have been relatively few illnesses
reported in the literature from the disposal and management of sewage sludge, biosol-
ids, or municipal solid waste (MSW). The populations most likely to be exposed are
workers. Even diseases from direct contact or exposure during wastewater treatment,
collection of MSW, or disposal of MSW are rare. Hygiene, sanitary conditions, and
the education of workers are high. However, the potential exposure to diseases by
workers can result from inhaling bioaerosols and having respiratory complications.
Bioaerosols produced during composting of sewage sludge or MSW has been a con-
cern for workers and populations residing near composting facilities. The bioaerosols
of predominant concern have been Aspergillus fumigatus and endotoxins. Numerous
studies have been conducted on this issue in the United States and United Kingdom.
In the United States, composting of sewage sludge and yard waste has increased
significantly. Today, the disposal or utilization of sewage sludge is primarily through
land application, followed by composting and landfilling. Bans from disposing of
yard material or green waste in landfills resulted in a massive growth of outdoor
windrow composting. This resulted in concern for exposure to bioaerosols for work-
ers and residents living near composting facilities. I have been involved in lawsuits by
residents against municipalities because the residents feared exposure to Aspergillus
fumigatus, a fungus predominating during composting since it survives the high
temperatures during composting.
Bioaerosols in the indoor environment have been a source of respiratory illnesses
such as asthma. Molds and mildew are found in air conditioning units, humidifiers,

xi
xii Preface

laundry rooms, plumbing leaks, and other sources of moisture. The “sick building”
syndrome has been attributed to bioaerosols.
This book devotes two chapters to bioaerosols. One chapter covers the general
aspects, including the indoor environment, bioaerosols from MSW facilities, as well
as measuring and enumerating technologies. The second chapter is devoted to com-
posting. This is not only because of the vast literature but also because composting
can represent a viable low-­cost technology to deal with the vast production of solid
waste and its disposal.
In 1931, Sir Albert Howard and Yeshwant Wad published The Waste Products of
Agriculture, addressing a composting method called the Indore method, a technique
to produce stable organic matter termed humus as a means of promoting crop growth.
Although this was applied to agricultural waste, it also had an application to solid
waste. This aspect was never endorsed. A later book, An Agricultural Testament,
indicated that the Indore method had become widespread. The organic matter and
fertility were the benefits. I describe this and other newer, low-­cost technologies. In
developing countries, composting by any means can be a viable technique for disease
prevention and control (Howard 1935).
Anaerobic digestion of human wastes as well as other wastes can be greatly
expanded, especially in developing countries. Anaerobic digestion provides meth-
ane, which can be a source of energy. The solids remaining can be used either
directly as a source of nutrients and organic matter for plant growth or composted
for further disinfection and use in horticulture, public works, and agriculture. In
India, I learned of small anaerobic digesters used in the home to provide methane
gas for cooking. In the United States, anaerobic digestion of biosolids takes place in
large expensive digesters. Methane from these facilities is used for power generation
and even power for vehicles. These expensive digesters are not a method to handle
sewage sludge in developing countries since paying off the capital investment and
operations through taxation would be prohibitive. However, I saw several inexpen-
sive anaerobic digesters used for agricultural and food waste that could be adapted
for other wastes in developing countries. According to George (2008), 15.4 million
rural households in China have biogas (methane from anaerobic digestion) for cook-
ing and other uses. She stated that Nepal has more digesters per capita than China.
Covered lagoons have also been used to produce biogas from dilute waste from ani-
mal production facilities (Bowman 2009). In Minnesota, at a food-­processing facil-
ity, I also saw a covered lagoon that produced methane.
This book describes the various pathogens that are found in solid wastes and
the diseases they produce, with emphasis on their relation to developing countries.
Sanitation is highly neglected in developing countries. More money is often spent on
arms and tribal warfare than on sanitation and food production. In Iran and Egypt,
the military controls many industries and commercial enterprises.
Besides better sanitation, hygiene and education that promotes disease preven-
tion are extremely important. This enhances prevention of waterborne and food-
borne diseases.
Preface xiii

REFERENCES
Bowman DD. 2009. Manure Pathogens. Alexandria, VA: WEF Press.
George R. 2008. The Big Necessity. New York: Metropolitan Books.
Howard A. 1935. The manufacture of humus by the Indore process. J Royal Soc Arts 74:
26–60.
Howard A. 1943. An Agricultural Testament. New York: Oxford University Press.
Howard A and Wad YD. 1931. The Waste Products of Agriculture: Their Utilization as Humus.
London: Oxford University Press.
Acknowledgments
I would like to thank my family: Esther, my wife; and my three children, Beth,
Jonathan, and Lisa, for their encouragements, suggestions, and patience. My wife
worked at the National Institutes of Health. All three of my children are involved
in human health and welfare. Beth is an occupational therapist, often working
with autistic children. Jonathan is director of surgical pathology at Johns Hopkins
Hospital and is a professor of pathology, urology, and oncology involved in work
with prostate cancer and other urological problems. Lisa works as a nutritionist for
an organization called WIC (Women, Infants, and Children). Their dedication to
human health encouraged me to pursue this direction.

xv
1 Pathogens and Diseases
Associated with Disposal
and Management
of Solid Waste

INTRODUCTION
This book covers:

• Global aspects of pathogens and diseases from solid waste


• Pathogens and diseases in various solid wastes other than hospital wastes
• Disposal and management of solid wastes in relation to diseases

Most of the scientific data available relate to foodborne and waterborne pathogens
and their diseases. This primarily involves ingestions or direct intake into the gastro­
intestinal system. With solid waste, dermal and respiratory infections and diseases
are important. Probably, as will be shown, respiratory diseases are the most impor-
tant route for diseases to workers and the public from solid waste. Pathogenic bio-
aerosols are also an important source of disease.
In developed countries, sanitation is often well developed. There is great empha-
sis on hygiene and general cleanliness. Water is treated with disinfectants such as
chlorine, or water treatment facilities filter the water. Many homes also use water
filters for the entire home, under the sink, or in closed containers.
This is not the case in developing countries. Although emphasis is placed on clean
water, there is neglect of sanitation and management and disposal of solid waste.
This is particularly true in small villages. In 1945, when I was in Cairo, Egypt,
garbage of municipal solid waste (MSW) was piled in the streets. During the 1970s,
I was invited to Milan, Italy, to suggest opportunities for management of MSW.
During my stay, there was a strike of municipal garbage collectors. Garbage gath-
ered in the streets. I am sure if water was not available or if homes could not dispose
of sewage, a great cry would have taken place, and the problems would have been
immediately solved, but disposal of MSW was of secondary importance. Few people
were concerned with vectors and their impact on human health.
In recent years, there have been numerous instances of water and food contami-
nation resulting from fouling by wild or domestic animals. In developing countries,
especially in rural areas of Africa, India, and China, human waste disposal is a

1
2 Disposal and Management of Solid Waste: Pathogens and Diseases

major concern, especially as related to health. Developing countries today account


for 85.4% of the world’s population, and an estimated 500,000 people defecate in
the open. Poor sewage conditions often lead to a host of diseases and mortality. It
is reported that poor sanitation kills 12 million people each year due to mosquito-­
borne diseases and through diseases from water contamination. The World Health
Organization (WHO) has reported that 3.4 million people die as a result of water-­
related diseases that are often the result of poor sanitation and water contamination
from raw sewage and human fecal matter. In villages and small communities, there
is a direct relation between water contamination and sewage or solid waste disposal.
Water resources such as wells and streams are downstream from where defecation
or disposal of contaminated solid waste occurs. Sanitation is nonexistent. As will be
shown, the role of vectors, especially mosquitoes, is extremely important in diseases
and human health. The effort for eradication has been concentrated on medication
and screening. Little effort is given to control the source of mosquitoes and their
breeding. This is often directly related to solid waste management. Water can accu-
mulate in numerous MSW sources such as tires, containers, discarded shoes, and so
on. Proper sanitation includes restricting runoff that carries fecal matter, providing
adequate drainage and water removal, providing adequate conditions for disposal
of human waste, and least but not less important is providing education. In The Big
Necessity, Rose George stated, “Sanitation is one of the best investments a country
can make.” Further, she asserted, “Excreta disposal is a political football, kicked
between departments” (George 2008).
In developing countries where sewer systems and treatment are unavailable, often
outdoor defecation is the predominant mode of fecal matter disposal. George (2008)
points out that in India nearly 800 million persons spread contagious diseases in this
fashion. Even where latrines were installed, they were not used.
From more than 3,500 years ago, the biblical portion of Deuteronomy 23 states,
“You shall have a shovel in addition to your weapons, and it will be that when you
sit outside, you dig with it; you shall go back and cover your excrement.” Proper
hygiene required the Israelites to defecate between 1,000 and 2,000 cubits or 1,000
to 4,000 feet away from the camp (George 2008). It was evident that they realized
then that open defecation could result in diseases.
Foodborne diseases are a major problem. Contaminated food causes approxi-
mately 1,000 reported disease outbreaks, with an estimated 48 million illnesses,
128,000 hospitalizations, and 3,000 deaths in the United States annually (Gilliss
et al. 2011). Some of these occurrences were related to solid waste, such as contami-
nation by animal manure.
Water contamination can be related to sanitation. Two early examples of
water contamination incidences are: (1) A Milwaukee, Wisconsin, outbreak with
Cryptosporidium believed to be from animal or human waste contamination. This
resulted in 100 deaths and 400,000 persons becoming ill (MacKenzie et al. 1994).
(2) Another incident occurred in Walkerton, Canada. Starting May 15, 2000, many
residents of the town of about 5,000 began to simultaneously experience purple diar-
rhea, gastrointestinal infections, and other symptoms of Escherichia coli infection.
Pathogens and Diseases Associated with Disposal of Solid Waste 3

At least 7 people died directly from drinking the water contaminated with E. coli,
and about 2,500 became ill (Krewski et al. 2002).
The major foodborne illnesses are caused by the following pathogens:

• Clostridium botulism
• Campylobacter
• Cryptosporidium
• Giardia
• E. coli O157:H7
• Listeria
• Molds
• Noroviruses
• Yersinia
• Salmonella
• Shigella
• Toxoplasma gondii
• Vibrio parahaemolyticus

WHO estimated that in 2005 alone, 1.8 million died from diarrheal diseases.
Many of these diseases were related to food and drinking water (WHO 2007). WHO
conservatively estimated that the global death toll from diarrheal diseases is from
1.7 to 2.5 million deaths per year. Most of these occur in children under five years of
age (WHO 2009). In many developing countries with poor resources, other diseases,
such as cholera, shigellosis, and typhoid, take a large toll. On February 23, 2013, the
New York Times reported that in Haiti over 2 years ending in 2012, 8,000 persons
died and 646,000 were ill from cholera as a result of poor sanitary conditions.
The principal agents of diarrheal diseases are

• Vibrio cholerae
• Salmonella spp.
• Shigella spp.
• Campylobacter spp.
• Escherichia coli strains
• Staphylococcus aureus
• Clostridium perfringens
• Clostridium difficile
• Giardia lamblia
• Cyclospora
• Cryptosporidium parvum

A number of viruses, including enteric adenovirus, astrovirus, and calicivirus,


can cause diarrhea.
Furthermore, fungal infections and airborne aspects related to fungi such as
Aspergillus, molds, and actinomycetes have increased. In the United States, asthma
affects over 25 million persons, 7 million of them children. Worldwide, it is estimated
4 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 1.1
Deaths from Several Diseases in Developing Countries
Causes of Death 1990a 2002b 2008a
Lower respiratory infections 3,894,000 2,806,000 1,050,000
Diarrheal diseases 2,865,000 1,535,000 760,000
Malaria 928,000 1,246,000 480,000
Tuberculosis 1,978,000 961,000 400,000

a World Health Organization, Media Centre. 2014. The top 10 causes of


death. May. Fact sheet 310. http://www.who.int/­mediacentre/­factsheets/​
­fs310/en/­index.html
b Parliamentary Office of Science and Technology. 2005. Post note, num-
ber 241. June.

that over 300 million people are affected. Indoor air pollution from molds or nox-
ious fumes can result in allergies and asthma (“Asthma Statistics” 2011). The lack
of hygiene, inaccessibility to soap and water, and lack of public health education
are a major source of the problem. It is estimated that correction of these aspects
could reduce diarrheal diseases by 50% (Centers for Disease Control and Prevention
[CDC] 2010).
Table  1.1 shows deaths in developing countries from several diseases. The
data were hard to obtain because of inconsistency in reporting. Lower respiratory
tract infections, diarrheal diseases, and tuberculosis decreased for the three peri-
ods reported. Malaria increased from the reported years of 1990 to 2002 and then
decreased in the reported year of 2008. Diarrheal diseases and malaria can result of
poor sanitation and solid waste disposal as indicated in Chapter 4.
Infectious diseases are the greatest killers of adults and children. They account
for 13 million deaths a year. Six diseases cause 90% of infectious disease deaths
(Brundtland 1999). With children under five years old, acute respiratory illnesses
are the leading cause of death. Lower respiratory tract infections refer to pneu-
monia, influenza, bronchitis, and bronchiolitis caused by common microbes with
worldwide distribution. Malaria is the most serious parasitic disease in the world.
Eradications are infeasible. Parasitic diseases are also a major cause of disease and
death. Protozoal parasites of African trypanosomiasis cause African sleeping sick-
ness, and American trypanosomiasis causes Chagas disease, with annual mortalities
estimated at 55,000 and 25,000, respectively. Another protozoan disease, leishmani-
asis, is highly fatal. Other causes as reported by WHO and the Centers for Disease
Control and Prevention (CDC) are: amoeba, 54,000 deaths; hookworm, 90,000
deaths; Ascaris, 60,000 deaths; schistosomiasis, 38,000 deaths; and onchocerciasis,
30,000 deaths (“How the Other Half Dies” n.d.). Although these numbers will not be
the same currently or each year, they still represent the situation in the sub-­Saharan
region of Africa and other developing countries.
Pathogens and Diseases Associated with Disposal of Solid Waste 5

DEFINITIONS
It is important to define the parameters discussed in this book. The three principal
parameters are

• Pathogens
• Diseases
• Solid waste

Stedman’s Medical Dictionary (1976) defines a pathogen as any virus, micro­organ­


ism, or other substance causing disease. It further defines an opportunistic patho-
gen as one that is capable of causing a disease when the host defense mechanism
(immunosuppression) is lowered. A disease is defined as an illness, sickness, inter-
ruption, cessation, or disorder of body functions, systems, or organs.
Solid waste includes the following:

• MSW or garbage
• Sewage sludge and biosolids (treated sewage sludge)
• Septage
• Manure
• Human excrement from domestic sources that do not have municipal dis-
posal facilities

Solid waste can consist of MSW (garbage), which may contain discards of pet
feces, contaminated tissues from humans, contaminated food waste (e.g., chicken
with Salmonella), and other contaminated sources. In the United States, most of the
MSW is landfilled. Incineration or heat recovery systems are few. There are approxi-
mately 200, mostly small, biosolid composting facilities in the United States. The
largest facility is the Inland Empire composting facility located in Chino, California.
There are few MSW composting facilities. Food waste collection and composting are
increasing. Approximately 154 municipalities are collecting food waste. On June 17,
2013, Mayor Bloomberg of New York indicated that the city will initiate food waste
composting as being done in several other cities.
In the United States, sewage sludge, the residue after anaerobic digestion, is fre-
quently applied to the land. For sewage sludge to be applied to land, it must undergo
treatment to stabilize and destroy some of the pathogen concentration. Sewage sludge
that is treated is then classified as biosolids. Lime treatment is also a method of sta-
bilizing sewage sludge prior to land application. In the United States, approximately
50% of biosolids are applied to land.
Composting of sewage sludge has grown significantly in the United States, with
one of the largest facilities handling several hundred tons per day. The state of
California has been the most progressive in utilizing composting of sewage sludge
or biosolids.
Since excellent treatment of pathogens in manure has occurred recently (Bowman
2009), Chapter 9 is devoted to this subject to update the information.
6 Disposal and Management of Solid Waste: Pathogens and Diseases

SOURCES OF PATHOGENS IN SOLID WASTE


The sources of pathogens in solid waste are

• Discarded raw food


• Diapers
• Animal and pet wastes
• Discarded medicinal items such as Band-­Aids, contaminated gauze, and
the like
• Contaminated paper towels, nose wipes, and so on
• Wastewater containing excreta and urine
• Other domestic sources not using sewage systems (e.g., outhouses, pits,
soil surfaces)
• Health care wastes
• Manure on land and runoff

Solid waste can contain pathogens such as viruses, bacteria, parasites, fungi, and
actinomycetes. As an example, Aspergillus fumigatus can infect humans directly
through the respiratory system. Airborne pathogens can land on crops and eventually
infect foods and humans. Ritter et al. (2002) stated that, on a global scale, pathogenic
contamination of drinking water poses the most significant health risk to humans.
Contaminated water resulting from leachate from landfills or other disposal meth-
ods can enter drinking water supplies in ground or surface waters. Sobsey (1978)
found enteric viruses in landfill leachate. Contaminated water can directly affect
the food supply. Pathogens can enter the soil from applications of manure and sew-
age sludge (unless disinfected by composting, heat treatments, or lime). The patho-
gens can move through the soil (e.g., via fissures, wormholes, etc.) and eventually
end in groundwater and drinking supplies (Ritter et al. 2002). Teschke et al. (2010)
indicated that studies of endemic diseases across multiple water or sewage systems
are rare.
The transmission route of pathogens from solid waste to the environment is shown
in Figure 1.1. It is evident that human exposure to pathogens from solid waste is ubiq-
uitous. A major source of diseases to children in developing countries is ingestion of
soil. This is discussed under the topic of geophagia.
The soil and its environment are depicted in Figure  1.2. Chapter  6 is entirely
devoted to pathogens in soil. The soil is a complex medium consisting of chemical,
physical, and biological parameters. Soil water affects plant growth and the biologi-
cal properties. It affects the survival of plants, as well as the microbial population.
Soil water dissolves chemicals, as well as transports them through the soil. Plant
nutrients assist in the growth of plants. The physical and chemical properties are
inert, whereas the biological properties are dynamic.
It is well known that the soil may harbor pathogenic micro­organ­isms as well
as other hazardous material (Berg, Eberl, and Hartman 2005; Baumgardner 2012).
Many of the pathogens may result from sewage sludge or biosolid application in
developed countries, whereas in developing countries solid waste, raw sewage, or
fecal matter disposal can contaminate soil. Helminths or geohelminths, such as
Pathogens and Diseases Associated with Disposal of Solid Waste 7

Pathogens in Solid Waste

Air Water Soil Crops Vectors

Food

Humans and Animals

FIGURE 1.1  The transmission route of pathogens from solid waste to humans.

Physical Biological Chemical


Properties Properties Properties

Water Bacteria pH
Soil Temperature Parasites Plant Nutrients
Soil Structure Viruses Organic Chemicals
Soil Texture Nematodes Inorganic Chemicals
Fungi
Plant Roots
Rhizosphere

FIGURE 1.2  The physical, biological, and chemical properties of soil.

roundworm (Ascaris lumbricoides), whipworm (Trichiura trichiura), hookworms


(Ancylostoma duodenale and Necator americanus), and threadworm (Strongyloides
stercoralis), can result in infection from soils (Brooker, Clements, and Bundy 2006).
WHO estimates that as many as 1 billion persons are currently infected by soil-­
transmitted helminths (WHO 2011).
Tetanus and botulism are two pathogenic organisms found in soil. The causative
organisms are Clostridium tetani and Clostridium botulinum, respectively. C. tetani
is distributed worldwide and can be found in fields, playgrounds, schoolyards,
and other locations (Baumgardner 2012; Ebisawa et al. 1986). It produces a life-­
threatening toxin affecting the muscle.
C. botulinum is also found in soil and water (Baumgardner 2012). Its toxin pro-
duces paralysis and on occasion fatal illness. The April 28, 2013, New York Times
magazine reported an unusual case of an infant apparently contaminated from soil
by the organism C. botulinum. If not for proper diagnosis, the child probably would
have died.
8 Disposal and Management of Solid Waste: Pathogens and Diseases

Soil can either directly or indirectly be detrimental to human health. This can
occur in ingestion, inhalation, and dermal absorption (Abrahams 2002). Direct inges-
tion of soil particles, geophagia (discussed further in Chapter 7), also termed pica
(e.g., pica child), meaning one who eats soil, can take place in both developed and
developing countries (George and Ndip 2011; Vermeer and Frate 1979). I am aware
of one incident that occurred when a young female child played in a sandbox where
the previous year a young boy relative played with her in the same sandbox. The boy
was from a Caribbean country, and while playing in the box, he defecated. The girl
became very ill, and after visiting several doctors and hospitals, she died. Apparently
while playing the following year, she ingested some of the contaminated sand. A
parasite was able to get into her bloodstream and eventually into the brain. Although
this incidence is rare, geophagia occurs in both developed and developing countries,
with the majority of the occurrences in developing countries (Vermeer and Frate
1979). George and Ndip (2011) reported that in rural South Africa there was a wide-
spread practice of geophagia among young girls. This subject is discussed in detail
in Chapter 7.
The potential for inhalation from the soil surface is low. However, the applica-
tion of wastes and surface dumping of trash can result in inhalation of bioaerosols
that enter the respiratory system (see Chapter 8). Aerosolization of dust can contain
numerous organisms, including bacteria and fungal spores (Sing and Sing 2010).
Coccidioidomycosis, commonly known as “valley fever,” as well as “California
fever,” “desert rheumatism,” and “San Joaquin Valley fever,” is a fungal disease
caused by Coccidioides immitis or Coccidioides posadasii and is endemic in certain
parts of Arizona, California, Nevada, New Mexico, Texas, Utah, and northwestern
Mexico (Rapini et al. 2007).
C. immitis, a fungus, resides in the soil in certain parts of the southwestern United
States, northern Mexico, and parts of Central and South America. It is dormant dur-
ing long dry spells, and then develops as a mold with long filaments that break off
into airborne spores when the rains come. The spores, known as arthroconidia, are
swept into the air by disruption of the soil, such as during construction, farming, or
an earthquake. Infection is caused by inhalation of the particles. The disease is not
transmitted from person to person. The infection ordinarily resolves, leaving the
patient with a specific immunity to reinfection. C. immitis is a dimorphic sapro-
phytic organism that grows as a mycelium in the soil and produces a spherule form
in the host organism.
Polymenakou et al. (2008) reported on the short distance of areal transport of a
dust-­borne pathogen, Neisseria meningitidis, which caused seasonal outbreaks of
bacterial infection from that organism in Africa.

INFECTION OF HUMANS FROM SOLID WASTE


There are several potential sources of human infections from solid waste. As indi-
cated, solid waste applied or deposited on soil can result in pathogen transmission
to humans.
Pathogens and Diseases Associated with Disposal of Solid Waste 9

FIGURE 1.3  Individuals sorting usable material from municipal solid waste in Wuhan,
China.

The potential sources are as follows:

• Direct contact with pathogens present in solid waste


• Aerosolization of pathogens from solid waste
• Contaminated drinking water

Pathogenic organisms can infect humans through contact and open skin wounds.
This is especially relevant to workers in jobs related to solid waste and others exposed
to solid waste, such as scavengers in dumps (see Figure 1.3).
Figure  1.3 shows an open dump I saw in Wuhan, China. These conditions are
often prevalent in developing countries in Asia and Africa. Individuals coming in
contact with trash or garbage can be infected through wounds. The individuals can
bring pathogens on their clothing and shoes to the home and infect other individuals.
Pathogens can also leach through the soil to water resources. Pathogenic bioaerosols
can be released through the air and infect the respiratory system of individuals in
the area.
The October  27, 2012, New York Times reported on the hazards from an open
landfill or dump in Bangalore, India. It stated that: “A stinking mountain of trash, the
landfill has been poisoning local waters and sickening nearby villagers. … Trash is
India’s plague.” The surface disposal of trash directly influences workers and scav-
engers. As stated in the article, as many as 15,000 waste workers can be affected.
In most developed countries, landfills require a liner to protect ground- and sur-
face waters. Under these conditions, especially since the conditions in the landfill
are under anaerobic conditions and produce methane, the survival of pathogens
10 Disposal and Management of Solid Waste: Pathogens and Diseases

is negligible. The concern for water contamination is from inorganic and organic
chemicals. There are few data on pathogen survival under lined landfill conditions
in developed countries. These conditions are not usually applicable in develop-
ing countries.
Obire and Aguda (2002) in Nigeria found large numbers of total viable aerobic
heterotrophic bacteria for the leachate from a waste dump and an adjacent stream.
The leachate counts ranged from 2.5 × 106 to 6.5 × 106 CFU/­m L, and in the stream
counts ranged from 1.2 × 106 to 1.2 × 107 CFU/­m L. The bacteria found in some
leachate and stream samples were Bacillus spp., Staphylococcus spp., Klebsiella,
and Shigella (Obire and Aguda 2002).
Flores-­Tena et al. (2007) reported that they identified 20 pathogenic or oppor-
tunistic bacteria in air, 20 from soil, and 11 from leachate in a landfill in Mexico.
Although most were enteric, some were respiratory tract pathogenic bacteria. In
leachate, the most frequent species were Acinetobacter baumannii, Bordetella spp.,
Brucella spp., and Escherichia coli var II (Flores-­Tena et al. 2007).
Aerosolization of pathogens can be from land application of sewage sludge and
biosolids (Epstein 1998a, 1998b; Dowd et al. 2000). The extent of pathogen aero-
solization depends on the type of application and weather conditions. Typically,
biosolids (i.e., treated sewage sludge) in developed countries are either applied in
a semisolid form directly to the land and followed by disking or other methods of
incorporation into the soil, or liquid biosolids may be sprayed and then disked into the
soil. Spraying will tend to disperse pathogens further than if semisolids are applied.
Windy conditions could result in greater dispersion of bioaerosols (Epstein 1998).
This is discussed further in Chapter 4. Bioaerosols may be dispersed during the com-
posting of sewage sludge or biosolids. The aerated static pile (ASP) results in much
fewer emissions of bioaerosols than the windrow method. In the windrow method,
the turning and agitation could result in significant dispersion of bioaerosols contain-
ing pathogens. Enclosed systems with proper containment and treatment of the air
will not result in emissions containing pathogenic bioaerosols (Epstein 1998b).
In many developing countries, fecal matter or raw sewage does not go through
a sewage system and is often deposited on land. This could result in dispersion or
bioaerosolization of pathogens or direct infection through contact.
In the case of incineration of sewage sludge or solid waste, the potential for patho-
gen infection is to workers. This could result from direct contact as well as inhalation
of pathogenic bioaerosols. Workers need to practice good hygienic practices, use
protective equipment, and leave clothing and shoes at the workplace.

SUMMARY
There are few data and information on pathogens in various solid wastes. The expo-
sure to pathogens from solid wastes in developed countries is primarily a concern
for workers. Respiratory and dermal modes of infection are probably the greatest
in developing countries, especially in Asia and Africa, but also are important in
Mexico and Central and South America.
Contamination of water supplies beneath dumps or in villages and small towns
that do not have proper sewage infrastructure can result in diseases in the population.
Pathogens and Diseases Associated with Disposal of Solid Waste 11

Scavengers in dumps not only expose themselves through dermal and respiratory
infections but also can bring causative elements into their homes on contaminated
shoes, sandals, bare feet, and clothing, thus exposing other members of the family.
The main objective of this book is to discuss pathogens in solid waste, provide
some of the recent available data, and provide insight into disposal options and man-
agement of solid waste to reduce infection and diseases.

REFERENCES
Abrahams PW. 2002. Soils: their implications in human health. Science Total Environ 291:
1–32.
American Academy of Allergy, Asthma, and Immunology. 2011. Asthma statistics. http://
www.aaaai.org/about-­the-­aaaai/newsroom/asthma-­statistics.aspx
Baumgardner DJ. 2012. Soil-­related bacterial and fungal infections. J Am Board Fam Med
25: 734–744.
Berg G, Eberl L, and Hartman A. 2005. The rhizosphere as a reservoir for opportunistic human
pathogenic bacteria. Environ Microbiol 7: 1673–1685.
Bolognia JL, Jorizzo JL, and Rapini RP (Eds.) 2007. Dermatology (2 volume set) 2nd edition.
London: Elsevier.
Bowman DD. 2009. Manure Pathogens. Alexandria, VA: WEF Press.
Brooker S, Clements ACA, and Bundy DAP. 2006. Global epidemiology, ecology, and control
soil-­transmitted helminths infections. Adv Parasitol 62: 221–261.
Brundtland G. 1999. Removing Obstacles to Health Development. Geneva, Switzerland:
World Health Organization.
Centers for Disease Control and Prevention (CDC). 2010. Diarrheal diseases in less developed
countries. http://www.cdc.gov/healthywater/hygiene/ldc/diarrheal_diseases.html
Dowd SE, Gerba CP, Pepper IL, and Pillai SD. 2000. Bioaerosol transport modeling and risk
assessment in relation to biosolid placement. J Environ Qual 29: 343–348.
Ebisawa I, Takayangi M, Kurata M, and Kigawa M. 1986. Density and distribution of
Clostridium tetani in the soil. Jpn J Exp Med 56: 69–74.
Epstein E. 1998a. Legal and health implications of land application of biosolids. In 12th Annual
Residuals and Biosolids Management Conference. Bellevue, WA: Water Environment
Federation, pp. 507–518.
Epstein E. 1998b. Pathogenic health aspects of land application. BioCycle 39: 62–67.
Flores-­Tena FJ, Guerrero-­Barrera AL, Alelar-­Gondzalez FJ, Ramire-­Lopez EM, and Martinez-­
Saldaria MC. 2007. Pathogenic and opportunistic Gram-­negative bacteria in soil, leach-
ate and air in San Nicolas landfill at Aguascalientes, Mexico. Rev Latinoam Microbiol
49: 25–30.
George R. 2008. The Big Necessity. New York: Metropolitan Books.
George G, and Ndip E. 2011. Prevalence of geophagia and its possible implications to health—
a study in rural South Africa. Paper presented at 2011 2nd International Conference on
Environmental Science and Development, Singapore.
Gilliss D, Cronquist A, Carter M, Tobin-­D’Angelo M, Blythe D, Smith K, Lathrop S, Birkhead
G, Cieslak P, Dunn J, Holt KG, Guzewich JJ, Henao Ol, Mahon B, Griffin P, Tauxe RV,
and Crim SM. 2011. Vital signs: incidence and trends of infection with pathogens trans-
mitted commonly through food. MMWR Morb Mortal Wkly Rep 60: 749–755.
How the other half dies. n.d. http://www.imva.org/Pages/deadtxt.htm
Krewski D, Balbus J, Butler-­Jones D, Hass C, Isaac-­Renton J, Roberts KJ, and Sinclair M.
2002. Managing health risk from drinking water—a report on the Walkerton inquiry.
J Toxicol Environ Health A 65: 1635–1823.
12 Disposal and Management of Solid Waste: Pathogens and Diseases

MacKenzie WR, Hoxie NJ, Proctor ME, Gardus MS, Blair KA, Peterson DE, Kazmierczak JJ,
Addiss DG, Fox KR, Rose JB, and Davis JP. 1994. A massive outbreak in Milwaukee of
Cryptosporidium infection transmitted through the public water supply. N Engl J Med
331: 161–167.
Polymenakou PN, Manolis M, Euripides GS, and Anastasios T. 2008. Particle size distribution
of airborne micro­organ­isms and pathogens during an intense dust event in the eastern
Mediterranean. Environ Health Prospect. 116: 292–296.
Ritter L, Solomon K, Sibley P, Hall K, Keen P, Mattu G, and Linton B. 2002. Sources, path-
ways, and relative risks of contaminants in surface water and ground water: a perspec-
tive prepared for the Walkerton inquiry. J Toxicol Environ Health A 65: 1–142.
Sing D and Sing CF. 2010. Impact of direct soil exposure from airborne dust and geophagy on
human health. Int J Environ Res Public Health 7: 1205–1223.
Sobsey MD. 1978. Field survey of enteric viruses in solid waste landfill leachates. Am J Public
Health 68: 858–864.
Teschke K, Bellack N, Shen H, Atwater J, Chu R, Koehoom M, MacNab YC, Schreier H, and
Isaac-­Renton JL. 2010. Water and sewage systems, socio-­demographics, and duration
of residence associated with endemic intestinal infectious diseases. BMC Public Health
10: 1–24.
Vermeer DE and Frate DA. 1979. Geophobia in rural Mississippi: environmental and cultural
contents and nutritional implications. Am J Clin Nutr 32: 2129–2135.
World Health Organization (WHO). 2007. Fact Sheet No. 237. http://foodhygiene2010.files.
wordpress.com/2010/06/who-food_safety_fact-sheet.pdf
World Health Organization (WHO). 2009. Diarrhoeal diseases. February 2009. http://www.
who.int/vaccine_research/disease/diarrhoeal/en/index.html
2 Risk and Exposure

INTRODUCTION
When dealing with the potential for disease caused by pathogens, it is important to
understand the risk potential. In this way, we can communicate to the individual and
the public the precautions needed. It also allows public health individuals to evaluate
and provide proper management. Risk analysis provides a framework for regulations.
There are virtually no risk assessments with respect to solid waste. For example,
what is the risk to a young person rummaging through a dump to collect items that
may be sold? Considering the prevalence of thousands of dumps in Asia and Africa
as well as in South America, what is the risk of disease for workers, scavengers, and
the public? How many persons have been infected?
Most of the risk assessments have been on food, drinking water, and chemicals. In
1993, the United States Environmental Protection Agency (USEPA) published Title
40 of the Code of Federal Regulations, Part 503. This set pollution limits for some
organic and inorganic chemicals in the disposal of sewage sludge. Included also was
a technical support document for reduction of pathogen and vector attraction. The
risk assessment used by the USEPA in 1995 and updated subsequently follows four
basic steps:

• Hazard identification: Can the identified pollutants harm human health and
the environment?
• Exposure assessment: Who is exposed, how do they become exposed, and
how much exposure occurs?
• Dose–­response evaluation: What is the likelihood of an individual develop-
ing a particular disease as the dose and exposure increase?
• Risk characterization: What is the likelihood of an adverse effect in the
population exposed to a pollutant? Risk is calculated as

Risk = Hazard × Exposure

A major criticism of the USEPA regulations was the minimum emphasis and
concern regarding exposure and potential disease from pathogens and pathogenic
substances. One problem was the lack of dose–­response relationships. Since that
time, there have been attempts to improve the risk analysis, many of these through
modeling since dose–­response information was still lacking and is difficult to obtain.
It is not the objective of this chapter to go into extensive detail. However, when
discussing pathogens, pathogenic substances, and diseases, some attention must be

13
14 Disposal and Management of Solid Waste: Pathogens and Diseases

given to the risk potential. With respect to solid waste management, three popula-
tions are of major consideration:

• Workers handling or involved in the disposal of wastes


• Populations residing near waste disposal facilities
• Scavengers

In recent years, the risk paradigm called quantitative microbiological risk assess-
ment (QMRA) has focused on exposure assessment, dose–­response analysis, and
risk characterization. The following are examples of three governmental organiza-
tions that have used QMRA:

• USEPA: Cryptosporidium risk and virus risk


• Food and Drug Administration (FDA): Listeria monocytogenes, Escherichia
coli, Vibrio parahaemolyticus, all with regard to certain foods
• United States Department of Agriculture: Clostridium perfringens,
Salmonella serotype Enteritidis and E.  coli O157:H7, also with regard
to foods

What is risk? Risk is the probability (i.e., the likelihood) of exposure and the
result that something dangerous or hazardous can occur related to human health.
In the case of potential diseases to humans resulting from the potential exposure to
pathogens, it is important to determine the conditions of exposure, the pathogens of
concern, routes of exposure, and the risk factors. This involves a risk analysis.
The three basic components of risk analysis are

• Risk assessment
• Risk communication
• Risk management

These are interrelated. However, unless one conducts or evaluates the risk assess-
ment, it is difficult to manage an unknown and therefore to communicate the conse-
quences and how to proceed in managing and controlling the potential for disease.
Although this chapter is a summary and guideline, there are several excellent
sources for those who wish to become further involved in the subject. Some refer-
ences are provided in the Suggested Reading section at the end of the chapter.
Haas (1999) presented an early framework for risk analysis illustrated in
Figure 2.1, which shows the integrated components of the risk.
In 1995, the USEPA updated and issued the current Agency-­ wide Risk
Characterization Policy (USEPA 1995). The policy calls for all risk assessments per-
formed at the USEPA to include a risk characterization to ensure that the risk assess-
ment process is transparent; it also emphasizes that risk assessments are to be clear,
reasonable, and consistent with other risk assessments of similar scope prepared
by programs across the agency. Effective risk characterization is achieved through
transparency in the risk assessment process and clarity, consistency, and reason-
ableness of the risk assessment product. Risk characterization, the last step in risk
Risk and Exposure 15

Risk Risk
Assessment Management

Risk
Characterization

FIGURE 2.1  Risk analysis framework. (From Haas, 1999. Quantitative Microbial Risk
Assessment. New York: Wiley.)

assessment, is the starting point for risk management considerations and the founda-
tion for regulatory decision making, but it is only one of several important compo-
nents in such decisions. As the last step in risk assessment, the risk characterization
identifies and highlights the noteworthy risk conclusions and related uncertainties.
Each of the environmental laws administered by the USEPA calls for consideration
of other factors at various stages in the regulatory process. As authorized by differ-
ent statutes, decision makers evaluate technical feasibility (e.g., treatability, detec-
tion limits) and economic, social, political, and legal factors as part of the analysis of
whether to regulate and, if so, to what extent. Thus, regulatory decisions are usually
based on a combination of the technical analysis used to develop the risk assessment
and information from other fields.
Recognizing that for many people the term risk assessment has wide meaning, the
National Research Council (NRC) report in 1983 on risk assessment in the federal
government distinguished between risk assessment and risk management: “Broader
uses of the term [risk assessment] than ours also embrace analysis of perceived risks,
comparisons of risks associated with different regulatory strategies, and occasion-
ally analysis of the economic and social implications of regulatory decisions func-
tions that we assign to risk management.”
In 1984, the USEPA endorsed these distinctions between risk assessment and risk
management for agency use and later relied on them in developing risk assessment
guidelines. In 1994, the NRC reviewed the agency’s approach to and use of risk
assessment and issued an extensive report on the findings. This distinction suggests
that USEPA participants in the process can be grouped into two main categories,
each with somewhat different responsibilities, based on their roles with respect to
risk assessment and risk management (USEPA 1995).
The NRC developed a standardized model for the purpose of developing a uni-
form risk assessment methodology for all federal agencies. The NRC model has
four steps: (1) risk assessment, (2) hazard assessment and identification, (3) dose–­
response assessment, and (4) exposure assessment.
16 Disposal and Management of Solid Waste: Pathogens and Diseases

RISK ASSESSMENT
Modern societies have learned to reduce the impact of disease-­causing micro­organ­
isms (pathogens) by adopting various sanitary control measures, such as farm-­
to-­fork processes in food production and treatment plants for drinking water and
waste­water. Nonetheless, our aging and more vulnerable population groups com-
bined with the emergence of drug-­resistant pathogens and enhanced global spread
of human pathogens provide a breeding ground for novel and reemerging diseases.
What is the need for risk assessment? Whenever a hazard exists, such as potential
exposure to a pathogen or pathogens in this case, it is valuable to assess the poten-
tial risk. The greater the potential risk and exposure, the more precautions are neces-
sary. As indicated, in most cases workers are the most exposed individuals. They are
exposed more frequently and often to higher amounts of the hazard.
The risk assessment process is often provided as a four-­step process:

• Hazard assessment and identification: This process identifies the pathogens and
diseases caused by them that could result in infection morbidity and mortality.
• Exposure assessment: This delineates the likelihood of an individual devel-
oping the disease as the dose and exposure increase.
• Dose–­response analysis. The relationship between the hazard quantity and
the adverse effect is explored.
• Risk characteristics: This synthesizes the previous steps to estimate the risk.

Most risk analysis has been geared to chemical hazards since these are easier
to evaluate. Furthermore, the potential of incurring a disease or infection is often
related to the number of pathogens exposed and the occurrence of exposure. For
example, dermatological exposure when there are no eruptions in the skin or fissures
that allow the pathogen to enter is less apt to result in the incurrence of a disease.
Risk assessment allows for planning, hazard identification, exposure mediation,
and prevention. Risk assessment also provides for the identification of the most likely
population that could be affected. Generally, children and aged populations are at
greater risk.
Parkin (2008) comprehensively reviewed the foundations and frameworks for
human microbial risk assessment. The author pointed out that the early concept of
risk assessment was provided by the NRC as follows: The framework is based on the
1983 NRC concept. Although this model was based on chemical risks, it was applied
to pathogens. Subsequently, in the 1990s, additional issues were identified, and it was
determined that the model based on chemical risk was not applicable to microbial
pathogens (Haas et al. 1993). The microbial risk assessment (MRA) is fundamen-
tally different from chemical risk assessment (Eisenberg 2006). Eisenberg indicated
that the chemical risk assessment to a great extent does not account for infectious
diseases and immunity issues. Furthermore, the chemical risk assessment relies on
static modeling techniques, which cannot represent dynamic processes such as dis-
ease transmission (Eisenberg 2006; Parkin 2008). The traditional risk assessment is
shown in Figure 2.2.
Risk and Exposure 17

Hazard
Identification

Risk
Dose Response Characterization
Assessment

Risk
Exposure
Assessment
Assessment

FIGURE 2.2  Traditional risk assessment framework.

Several problems with using a chemical risk analysis for pathogens or micro­
organ­isms were identified by scientists (Parkin 2008):

• Pathogens can grow, evolve into different life stages, and die off.
• Virulence, the relative power and degree of pathogenicity by organisms,
varies during a pathogen’s life cycle and between strains.
• Pathogens behave differently under different ecological and environmental
conditions, such as temperature, moisture, and media (soil).
• Pathogens may be transmitted from person to person. Chemicals are not.
• Infection and exposure differs between individuals. Immunities vary
among persons.

Subsequently, an ecological risk assessment framework was developed in North


America (USEPA 1998; Environment Canada 1996).

HAZARD ASSESSMENT AND IDENTIFICATION


Hazard assessment relates to identification of a pathogen of significance that may
cause acute or chronic illnesses in humans. Pathogenic micro­organ­isms are essen-
tially known by the scientific community. Pathogens are often referred to as primary
pathogens and secondary or opportunistic pathogens. The primary pathogens can
be bacteria, parasites, or viruses. They usually involve direct contact. With solid
waste, workers are the individuals most exposed. Good hygiene is the best preventive
measure. Epidemiological or ecological studies, including exposure routes and the
potential effects on individuals, provide information on the distribution of disease
and pathogens among persons.
The two important exposure routes are through either direct contact or bioaero-
sols. Direct routes could be ingestion, inhalation, or dermal contact. Ingestion can
come from contaminated food or water. Inhalation occurs from air pollution or
emissions of bioaerosols. Dermal contact is through direct contact with pathogen-­
contaminated material. Direct contact typically involves individuals. A good exam-
ple is the fecal-­to-­oral route.
18 Disposal and Management of Solid Waste: Pathogens and Diseases

In developing countries where sanitation and hygiene are poor, many of the dis-
eases causing morbidity and mortality occur this way. Often, in rural areas of devel-
oping countries, fecal defecation occurs outdoors, where children in particular are
exposed. Exposure can occur also when persons, especially children, come in con-
tact with solid waste either at home or in public places such as dumps. In developed
countries, exposure is broader and generally is of concern to the public as a whole.
This could be from air pollution from incineration or bioaerosol emissions from
facilities such as those involved with solid waste composting.
Another exposure route could be from groundwater pollution as a result of old
landfills that do not have liners or from animal waste, particularly in areas where
large concentrations of domestic animals are outdoors. In dealing with solid
waste exposure, consideration must be given to (1) workers and (2) the public. Worker
exposure can be either through direct contact or through bioaerosols. The public will
be exposed primarily through pathogenic bioaerosols.

DOSE–­RESPONSE ASSESSMENT
Dose–­response assessment is the process of quantitatively evaluating the health
aspect of a specific disease as a function of human exposure to that pathogen. The
relationship between the dose of the organism exposure and the incidence of adverse
health effects in the exposed population forms the basis for the quantitative dose–­
response relationship. The response of humans to exposure to a pathogen is highly
variable. The incidence of disease is dependent on a number of factors, such as viru-
lence characteristics of the pathogen, the number of cells ingested, and the general
health and immune conditions of the hosts. Generally, children and older persons
are more susceptible to a disease from a pathogen. Immunosuppressed individuals
are also more susceptible. These last individuals are much more susceptible to an
infection (e.g., from bioaerosols) than the general population. A key question when
comparing dose–­response studies is which biological responses are being measured.
In the case of pathogenic enteric bacterial infection, morbidity and mortality are the
end points (Buchanan, Smith, and Long 2000). The term infections is often defined
differently by various disciplines.
Any consideration of microbial dose–­response relations must take into account
the various modes of pathogenicity associated with different pathogenic organisms.
An understanding of how a pathogen causes a disease is critical. Three different
broad classes of pathogens are differentiated—infectious, toxico-­infectious, and
toxigenic—based on the modes of pathogenicity (Buchanan, Smith, and Long 2000).

EXPOSURE ASSESSMENT
Exposure is the frequency, duration, and intensity with which a population or per-
sons are exposed through various routes, such as inhalation, ingestion, or dermal
contact. Inhalation with regard to solid waste exposure can be through bioaerosols.
Ingestion usually involves contaminated food or water. The exposure assessment
Risk and Exposure 19

process includes the following steps: (1) characterize exposure setting, (2) identify
exposure pathways, and (3) quantify exposure.

RISK CHARACTERIZATION
Risk characterization is the final phase of risk assessment. During this phase, the like-
lihood of adverse effects occurring as a result of exposure to a stressor is evaluated.
Risk characterization contains two major steps: risk estimation and risk description.
The stressor–­response profile and the exposure profile from the analysis phase serve
as input to risk estimation. The uncertainties identified during all phases of the risk
assessment also are analyzed and summarized. The estimated risks are discussed by
considering the types and magnitude of effects anticipated, the spatial and temporal
extent of the effects, and recovery potential. Supporting information in the form of
a weight-­of-­evidence discussion also is presented during this step. The results of the
risk assessment, including the relevance of the identified risks to the original goals
of the risk assessment, then are discussed with the risk manager (EPA/630/R-92/001
Framework for Ecological Risk Assessment).

REFERENCES
Buchanan RL, Smith JI, and Long W. 2000. Microbial risk assessment: dose-­response rela-
tions and risk characterization. Int J Food Microbiol 58: 159–172.
Eisenberg JNS. 2006. Application of a Dynamic Model to Assess Microbial Health Risks
Associated with the Beneficial Uses of Biosolids: Final Report to the Water Environmental
Research Foundation. WERF Report 98-REM-1a. London: Water Environmental
Research Foundation.
Environment Canada. 1996. Ecological Risk Assessment of Priority Substances under the
Canadian Protection Act. Ottawa: Environment Canada.
Haas, C. 1999. Quantitative Microbial Risk Assessment. New York: Wiley.
Haas C, and Eisenberg JNS. 2001. Risk assessment. In Water Quality: Guidelines, Standards
and Health, ed. Bartram L, and Fewtreil J. London: World Health Organization.
Haas CN, Rose JB, Gerba C, and Regli S. 1993. Risk assessment of virus in drinking water.
Risk Anal 13: 545–662.
National Research Council (NRC). 1983. Risk Assessment in the Federal Government:
Managing the Process. Washington, DC: National Academy Press.
Parkin RT. 2008. Foundations and Frameworks for Human Microbial Risk Assessment.
Washington, DC: US Environmental Protection Agency.
US Environmental Protecton Agency (USEPA). 1993. Title 40, Code of Federal Regulations,
Part 503.
US Environmental Protection Agency (USEPA). 1995. Guidance for Risk Characterization.
Washington, DC: US Environmental Protection Agency.
US Environmental Protection Agency (USEPA). 1982, November. Technical Support
Document for Reduction of Pathogens and Vector Attraction in Sewage Sludge.
Washington, DC: USDA.
US Environmental Protection Agency (USEPA). 1995. A Guide to the Biosolids Risk
Assessments for the EPA Part 503 Rule. US Environmental Protection Agency.
Washington, DC: USDA.
20 Disposal and Management of Solid Waste: Pathogens and Diseases

US Environmental Protection Agency (USEPA). 1998. Guidelines for Ecological Risk


Assessment. Washington, DC.: Federal Register 63(93): 26846–26924.
United States Environmental Protection Agency and US Department of Agriculture (USEPA/
USDA). 2012. Microbial Risk Assessment Guideline. Washington, DC: United States
Environmental Protection Agency and US Department of Agriculture.

SUGGESTED READING
Haas CN, Rose JB, and Gerba CP. 1999. Quantitative Microbial Risk Assessment. New York:
Wiley.
Parkin RT. 2008. Foundations and Frameworks for Human Microbial Risk Assessment. Report
submitted to the US Environmental Protection Agency, Washington, DC.
US Environmental Protection Agency (USEPA) and US Department of Agriculture. 2012.
Microbial Risk Assessment Guideline. Pathogenic Microorganisms with Focus on Food
and Water. Washington, DC: Interagency Microbiological Risk Assessment Guideline
Workgroup.
World Health Organization (WHO). 2001. Water Quality, Guidelines, Standards and Health,
ed. Fewtrell L, and Bartram J. London: IWA.
3 Odors as a Health Issue

INTRODUCTION
Odors are pervasive throughout the globe. Primarily, odors are either chemical or
organic. Typically, chemical odors are the result of industrial activity, including from

• Pulp and paper mills


• Wood treatment plants
• Petroleum facilities
• Pesticide and fertilizer plants
• Incineration facilities

Organic odors usually result from

• Wastewater treatment plants


• Septage and sewage
• Composting facilities
• Landfills and open dumps
• Land application of wastes
• Animal farms, especially large concentrations of animals
• Human and animal discharge to fields, streets, and open areas
• Garbage discharged in streets

BASIC CONCEPTS
What makes some of the odors from solid waste? Odorants result from the decom-
position of organic matter, primarily containing sulfur and nitrogen. What is the
difference between an odor and an odorant? The term odor refers to the perception
experienced when one or more chemicals come in contact with receptors on olfac-
tory nerves. An odorant refers to any chemical in the air that is part of the perception
of odor (McGinley and McGinley 1999).
How are odors characterized?

• Odor quality. Odor levels are usually expressed as the ratio of dilution to
threshold (D/­T ) rather than concentration. One of the major reasons for not
characterizing the odor by concentration of specific compounds is that one
compound at low concentration can be much more effective in producing a
malodor than another compound at a high concentration.

21
22 Disposal and Management of Solid Waste: Pathogens and Diseases

6
y = 1.3426x – 0.0227
5 R2 = 0.609

Intensity
3

0
0 1 2 3 4
Log C

FIGURE 3.1  Intensity versus concentration of dimethyl sulfide.

• Odor intensity. This is the relative strength of the odor compared to a stan-
dard compound, usually butanol. It is expressed in parts per million (ppm)
of butanol. This is expressed by Steven’s law. The equation is I = kC n where
I is intensity, C is the mass concentration of the odorant I (mg/­m3) (Epstein
2011; Hooper and Cha 1988; Walker 1993; Water Environment Federation
[WEF] 2004). An example is shown in Figure 3.1. As the concentration (log
C) increases, the intensity increases.
• Odor persistence. This indicates how long the odor prevails and is an indi-
cation of the rate of dilution.
• Odor character. This is the type of odor or its offensiveness. For example,
hydrogen sulfide smells like rotten eggs, and dimethyl sulfide smells like
rotten cabbage.
• Hedonic tone. The hedonic tone is the relative pleasantness or unpleasant-
ness of an odor.

Principally, most odors are considered a nuisance. However, in the 1990s scien-
tific interest began to evaluate whether odors per se could result in health effects.
Until that time, there were few scientific papers indicating that odors may be a health
problem. In the United States, individual states regulated odors in a vague way. Most
states did not use quantifying or mathematical ways to evaluate odors.
The assessment of potential health effects as a result of odors is difficult. Some of
the reasons for these difficulties are the following:

• A small quantity of an odorant produced by a chemical well below a toxic


level can result in an obnoxious odor.
• Odor is generally considered a nuisance or as a damaging effect on the
quality of life.
• Perception of an odor as noxious is not directly linked to toxicity.
• Behavioral patterns and physiological responses can be developed as a
result of exposure to odors.
• Epidemiological studies evaluating the effect of odors on health are limited.
Odors as a Health Issue 23

QUALIFYNG ODOR

· Hedonic Tone
– Pleasant/
Medicinal
Alcohol Disinfectant
Almond
Floral
Lavender
Cinnamon Perfumy
Coconut Rose-like
Fruity
Apple Maple

·
Ammonia Menthol Cherry Melon
– Unpleasant Eucalyptus Spicy
Citrus Minty
Anesthetic Soapy Fragrant Vanilla
Very little Camphor Vinegar Herbal Cloves Orange
practical use in Chlorinous Grapes Strawberry
odor management Lemon

· Quality

– Description of
Chemical
Car exhaust Paint
Cleaning Fluid Petroleum
Creosote Plastic
Vegetable
Celery
Cucumber
Gasoline Solvent Dill
character Garlic
Grease Sulfur
Kerosene Tar Green Pepper
– Marginally useful Molasses Turpentine Nutty
for source Mothball Varnish Onion
differentiating Oil Vinyl Earthy
Ashes Mushroom Smokey
Chalk-like Musky Stale
Fishy
Grassy Musty Swampy
Amine
Mold Peat-like Woody
Dead Fish
Mouse-like Pine Yeast
Perm Solution
Offensive
Blood Manure Septic
Burnt Putrid Sewer
Decay Rancid Sour
Fecal Raw Meat Urine
Garbage Rotten Eggs Vomit

FIGURE 3.2  The quality and hedonic tone of odors.

• There are no toxicity values for use in assessing risk posed by odorants
commonly present in biosolids.
• There is no database to properly assess odorants and associated potential risks.

Figure 3.2 shows odor quality and hedonic tone.


Once an odor is detected, its effect and consequences increase with concentration
as shown in Table 3.1. Figure 3.3 shows the effect of odor concentration on eye and
nasal irritation.

TABLE 3.1
Sequence of Sensory Effects as a Result
of an Odorant Concentration
Concentration Level Effect
1 Odor detection
2 Odor recognition
3 Odor annoyance
4 Odor intolerance
5  Perceived
6  Intolerance
    7 Toxicity
24 Disposal and Management of Solid Waste: Pathogens and Diseases

4
3
2 Eye Irritation
1
0

Perceived Magnitude
4
3 Nasal Irritation
2
1
0

4 ODOR
3
2
1
0 –4
10 10–2 100 102

FIGURE 3.3  The effect of odor concentration on eye and nasal irritation.

An odor episode can lead to complaints from the public and is related to (1) odor
character, (2) odor intensity, (3) odor duration, and (4) odor frequency (McGinley and
McGinley 1999). The sensitivity and response to odors will vary in individuals. This
variation can be related to age, gender, social habits, and medical history. The medi-
cal conditions that can increase sensitivity to odors are asthma, chronic obstructive
pulmonary diseases (COPDs), mental health (e.g., depression), and hypersensitivity.
As we inhale air containing an odor, the following occurs:

• Ten percent of odors pass under the olfactory organ.


• Twenty percent pass under the epithelium during sniffing. There are 10 to
25 million olfactory cells in the epithelium.
• The mucous layer on the epithelium traps odorants that are water soluble.
• An electrical response is created that, depending on its amplitude (strength),
is sent along to the brain in the form of a pain stimulus.

The sense of smell is complex and unique in structure and organization. The
human olfactory system supplies 80% of flavor sensation during eating. However, the
olfactory system plays a major role as a defense mechanism by creating an aversion
response to malodors and irritants (McGinley and McGinley 1999). The odorant
receptors and the organization of the olfactory system are shown in Figure 3.4.
Odors are experienced differently by different people, such as whether the per-
fume of another individual is bothersome to someone in an elevator, yet the individ-
ual and others do not object to the odor. Odor can trigger memories and associations.
There are numerous factors affecting odor perception. These can include adapta-
tion, environmental exposure, age, nutritional status, mental illness, diseases, and
disorders (Chrostowski and Foster 2003). Dalton et al. (2002) indicates that there
are numerous factors, including exposure history, personality, beliefs, expectations,
social factors, and bias. The longer one is exposed to an odor, especially if its inten-
sity increases or it extends for long periods of time, the more apt one is to consider
Odors as a Health Issue 25

Olfactory
bulb

4. The signals are transmitted


Mitral to higher region of the brain.
cell
Glomerulus 3. The signals
are relayed
Bone in glomeruli.
Nasal
epithelium

Olfactory
receptor
cells 2. Olfactory receptor cells
are activated and
send electric signal.

1. Odorants bind to
receptors.
Odorant
receptor

Air with odorant molecules

FIGURE 3.4  Odorant receptors and the organization of the olfactory system. (From Cain
WS, presentation at US Composting Council’s 14th Annual Conference and Travel Show,
Albuquerque, NM, 2006, with permission.)

whether the odor can have a health effect. Perception can be an important factor.
In a study when subjects were told that an odor was hazardous, the odor was more
offensive than when told it was a natural occurrence.
The following odorants detected in biosolids and associated with wastewater
treatment were reported by the National Resources Council (NRC 2002).

Sulfur compounds
• Hydrogen sulfide
• Dimethyl sulfide
• Diphenyl sulfide
• Carbon disulfide
• Dimethyl disulfide
• Methyl mercaptan
• Ethyl mercaptan
• Propyl mercaptan
• Allyl mercaptan
• Benzyl mercaptan
• Thiocresol
• Diethyl sulfide
26 Disposal and Management of Solid Waste: Pathogens and Diseases

• Diallyl sulfide
• Butyl mercaptan
• T-­Butyl mercaptan
• Crotyl mercaptan
• Thiophenol
• Sulfur dioxide
Nitrogen compounds
• Ammonia
• Methylamine
• Dimethylamine
• Trimethylamine
• Ethylamine
• Triethylamine
• Pyridine
• Indole
• Skatole
Acids
• Acetic (ethanoic)
• Butyric (butanoic)
Aldehydes
• Acetaldehyde
• Diamines (cadaverine)
Aldehydes and ketones
• Butyraldehyde
• Formaldehyde
• Isobutyraldehyde
• Isovaleraldehyde
• Acetone
• Butanone

ODOR AND HEALTH


In my previous books, I discussed odor as related to health and provided extensive
discussions on odor management (Epstein 1997, 2011). In this book, I primarily want
to make information on the subject current. Excellent reviews were presented by
several authors (Chrostowski and Foster 2003; Johnson 2011). Readers should also
evaluate other references (Cain and Cometto-­Muniz 2004; Epstein 2011; Schiffman
and Williams 2005; Shusterman 1992).
Malodors may have negative effects on well-­being. Convened on April  15–17,
1998 to discuss odors and health, the US Environmental Protection Agency (USEPA)
and the National Institute of Deafness and Other Communication Disorders raised
greater awareness, and interest evolved on whether odor has associated health effects
(Schiffman and Williams 2005).
Odors as a Health Issue 27

Cain (1987) indicated that people associated the health or harmful effects of envi-
ronments by the presence or quality of perceived odors.
Dalton (1999) reported that many health-­related effects of exposure to odorants
are mediated not by the direct effect of odors but by cognitive association of odors
and health. In a study, Dalton found that individuals given a harmful bias reported
significantly more health symptoms on exposure to an odorant than those receiving
the same odorant but with no harmful effects indicated. Thus, the author concluded
that prejudiced odor perceptions and reactions underscore the incredible ambiguity
of odor sensation and suggested that similar nonsensory factors play a large role in
people’s everyday reactions to ambient odors. When odors are persistent, they can
result in potential health effects (Dalton 1999).
Furthermore, odor perception has been shown to affect mood, tension, stress,
depression, anger, and fatigue. These conditions could potentially lead to physiologi-
cal and biochemical changes with subsequent health effects (Bolla-­Wilson, Wilson,
and Bleeker 1988)
We can view health effects in various ways. Depending on the frequency and
extent of an odor, if one resides near an industrial source of odors, people com-
plain of headaches, nausea, stress, eye irritation, throat irritation, cough, and mood
changes. Today, these are considered health effects depending on the severity. Odor
at times has served as an exposure marker.
Figure 3.4 shows that as the odor level increases, it eventually triggers an irrita-
tion. If the odor persists, this irritation can be great and require medical treatment.
It is evident from Table 3.2 that some compounds can cause an irritating effect at
low concentrations, whereas others require much higher concentrations.
Villemure et al. (2003) reported that odors altered mood, anxiety level, and
pain unpleasantness but did not change the perception of pain intensity (Villemure,
Slotnick, and Bushnell 2003). Johnson (2011) found that odor delivery can have both
a positive and a negative impact on cognitive operations (Johnson 2011).

TABLE 3.2
Odorous Compounds and Toxicological Thresholds of Irritation
Odor Threshold Range Irritating Concentration
Chemical (mg/­m3) (mg/­m3)
Acetic acid 2.5–250  25
Acetone 47–1613 475
Acetaldehyde 0.0002–4.1  90
Ammonia 0.026–40  72
Hydrogen sulfide 0.0007–0.014  14
Methyl ethyl ketone 0.74–147 590

Source: Modified from Chrostowski PC, and Foster MS. 2003. Odor perception and
health effects. WEFTEC 2003 Workshop on the Status of Biosolids Recycling
in the United States, Los Angeles, October.
28 Disposal and Management of Solid Waste: Pathogens and Diseases

SUMMARY
The term odor refers to the perception experienced when one or more chemicals come
in contact with receptors on olfactory nerves. An odorant refers to any chemical in
the air that is part of the perception of odor. While odors are generally perceived as
nuisances, if they persist or intensify, they can be an irritant, cause headaches, and
especially affect people with respiratory conditions such as asthma, emphysema, and
COPD. These are health concerns.

REFERENCES
Bolla-­Wilson K, Wilson RJ, and Bleeker ML. 1988. Conditions of physical symptoms after
neurotoxic exposure. J Occup Med 30: 684–686.
Cain WS. 1987. Indoor air as a source of annoyance. In Environmental Annoyance,
Characterization, Measurement and Control, ed. Koelega HS. Amsterdam: Elsevier.
Cain WS and Cometto-­Muiz JE. 2004. Health Effects of Biosolid Odors: A Review. Alexandria,
VA: Water Environment Research Foundation.
Chrostowski PC, and Foster MS. 2003. Odor perception and health effects. Presented at the
WEFTEC 2003 Workshop on the Status of Biosolids Recycling in the United States,
Los Angeles, October.
Dalton P. 1999. Cognitive influence on health symptoms from acute chemical exposure.
Health Physiol. 18: 579–590.
Dalton P et al. 2002. Gender-specific induction of enhanced sensitivity to odors. Nat Neurosci
5(3): 199–200.
Epstein E. 1997. The Science of Composting. Lancaster, PA: Technomic.
Epstein E, ed. 2011. Industrial Composting: Environmental Engineering and Facilities
Management. Boca Raton, FL: CRC Press.
Hooper JE and Cha S. 1988. Odor Perception and Its Measurement. East Hartford, CT: TRC
Environmental Consultants.
Johnson AJ. 2011. Cognitive facilitation following intentional odor exposure. Sensors 11:
5469–5488.
McGinley MA and McGinley CM. 1999. The “gray line” between odor nuisance and health
effects. Proceedings of Air and Waste Management Association, 92nd Annual Meeting
and Exhibition, St. Louis, MO.
National Research Council, July 2002. Biosolids Applied to Land: Advancing Standards and
Practices. Washington, DC: National Academies Press.
Schiffman SS, Walker JM, Dalton P, Lorig TS, Rajmer JH, Shusterman D, and Williams CM.
2000. Potential health effects of odors from animal operations, wastewater treatment,
and recycling of byproducts. J Agromed 7: 7–81.
Schiffman SS and Williams CM. 2005. Science of odor as a potential health issue. J Environ
Quality 34: 129–138.
Shusterman D. 1992. Critical review: the health significance of environmental odor pollution.
Arch Environ Health 47: 76–87.
Villemure CS, Slotnick BM, and Bushnell MC. 2003. Effects of odor on pain perception:
deciphering the role of emotion and attention. Pain 106: 101–108.
Walker JM. 1993. Control of composting odors. In Hoitink HAJ and Keener HM, eds.
Science and Engineering of Composting: Design, Environmental, Microbiological, and
Utilization Aspects. Columbus, OH: Ohio State University.
Water Environment Federation (WEF). 2004. Control of Odors and Emissions from Wastewater
Treatment Plants. WEF Manual of Practice 25. Alexandria, VA.: Water Environment
Federation.
4 Pathogens and Diseases
of Solid Wastes
Municipal Solid
Waste or Garbage

INTRODUCTION
Unfortunately, little data exist on pathogens in municipal solid waste (MSW), dumps,
and the handling of garbage, although the World Health Organization (WHO) does
provide data and information available on the Internet. By reviewing the method of
how MSW and garbage is handled globally, the lack of data is apparent. In 1983,
Althaus et al. (Althaus, Sauerwald, and Schrammeck 1983; Collins and Kennedy
1992) examined wastes from hospitals and municipal garbage dumps and found that
household wastes often contained more pathogens than hospital wastes.
In the United States, MSW is typically either landfilled or incinerated. Data
from the United States Environmental Protection Agency (USEPA) are shown in
Figures  4.1 and 4.2. In 2010, approximately 250 million tons of MSW were pro-
duced. Since 1960, MSW generation increased. In 2010, the generation rates were
reduced. Generation per person remained at the same level from 1990 to 2010. The
percentage of generated recycled material increased since 1985 to an average of 25%.
In some states, it is much higher. There are several reasons for these trends. Many
communities mandate recycling with a minimum separation of paper from glass
and plastics and do not allow disposal of yard waste in landfills. The use of garbage
disposals in the home reduces food waste removal. For many years, New York City
prohibited garbage disposals in homes. More recently, this restriction was lifted,
resulting in more liquid and greater biological oxygen demand (BOD) going into
wastewater treatment plants and production of more sewage sludge. But, it preserved
landfill space at the Staten Island landfill.
In the United States, most MSW goes to landfills. In recent years, regulations
required that landfills be lined, and often the methane gas produced is collected
and used. Earlier landfills were not lined; therefore, leachate could move through
the media and contaminate groundwater or drinking water. How long the liners will
remain intact is a controversial question.
Incineration is also a major method of handling MSW. However, in the United
States, incineration is not as prominent as in Europe. Land is more available in the
United States. Furthermore, many communities oppose incineration since they are

29
30 Disposal and Management of Solid Waste: Pathogens and Diseases

300 10
Total MSW generation
Per capita generation 9
252.7 249.9
250 242.5

Per Capita Generation (pounds/person/day)


8
Total MSW Generation (million tons)

217.3
208.3
7
200
166.3 6
151.6
150 5
127.8
121.1 4.57 4.72 4.67
4.52 4.43 4
104.4
100 88.1 3.83
3.66
3.25 3.25 3
2.96
2.68
2
50
1

0 0
1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010

FIGURE 4.1  MSW generation rates in the United States.

90 50
85.1
Total MSW recycling 79.9
80 Percent recycling 45

69.5 40
70
Total MSW Recycling (million tons)

Percent of Generation Recycling

35
60
55.8 34.1%
31.6% 30
50
28.6%
25
25.7%
40
33.2 20
30
16.0% 15
10.1%
20 9.6%
10
6.6% 7.3%
6.4% 6.2% 16.7
10 14.5
5
8.0 9.3
5.6 6.5
0 0
1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010

FIGURE 4.2  MSW recycling rates in the United States.


Pathogens and Diseases of Solid Wastes 31

concerned with air pollution. It is difficult to permit an incinerator even if it uses


heat recovery.
More recently in the United States and Canada, interest has been raised and effort
has been made to recover energy. Many states and municipalities conduct recycling
of paper, plastics, and glass. Cardboard is often recycled to Asia for reuse. Paper
was recycled for production of pulp and new recycled paper. Glass is recycled, and
attempts are also made to use crushed glass as a road surface material. The food
industry recognized that placing food in dark glass containers was better for pres-
ervation. However, the public prefers to see the product; hence, clear glass is used.
The separation of glass into clear and colored elements is more labor intensive.
But overall, separation techniques are improving. Metal recovery occurs through
magnets for ferrous metals, and aluminum is collected using eddy current tech-
niques. Air separation is used for lightweight material.
Aluminum, ferrous metals, plastics, and paper are all separated in a facility that I
designed in Hong Kong. This was more expensive than landfilling the waste. Some
grocery stores require consumers to bring recycled bags to reduce the distribution
of plastic. Several grocery stores in the United States give consumers the option of
plastic or paper bags. A few communities are planning or currently avoiding the use
of plastic bags. In Hong Kong, Tuesday was a day free of plastic containers.
Attempts at composting or anaerobic digestion met with little success in the
United States. In Europe, anaerobic digestion of source-­separated MSW is used a
bit more. In the United States and Canada, there is considerable composting of pro-
cessed sewage sludge, termed biosolids. There is considerable composting of yard
material since many states ban it from going into landfills. Recently, there is an
increase in composting of food waste, primarily from large generators.
In Europe, land is at a premium. There is more emphasis on waste reduction,
reuse, and recycling. For whatever cannot be recycled or reused, incineration is the
optimal disposal method.
The public is most unlikely to be exposed directly to bioaerosols, diseases, and
illnesses from MSW that is disposed of in landfills or incinerators.
Considering this situation in the United States, there is little interest in investigat-
ing the role of pathogens and their diseases in MSW. It is most likely that worker
health is of greater importance. Good hygienic practices are important. Smoking
or eating while working without disinfection can result in gastrointestinal diseases.
Inhalation of bioaerosols is probably of greater importance than ingestion as the
bioaerosols will infect the respiratory system.
The situation in developing countries is very different. The disposal of solid waste
is haphazard and often ends in dumps, where scavengers attempt to find marketable
material. In these cases, not only workers collecting the waste but also scavengers
and their families are exposed.
In 1976, at the request of the United Nations Development Programs (UNDP), I
went to Aden in Yemen to investigate the feasibility of composting solid waste by a
German technology to be financed by the UNDP. The facility was to be designed by
the United Nations Industrial Developing Organization (UNIDO). Although Aden
was the most developed city in Yemen as a result of the previous presence of the
32 Disposal and Management of Solid Waste: Pathogens and Diseases

British, its infrastructure was primarily for wastewater. The German technology was
not recommended because Yemeni personnel were not trained to maintain such a
facility once the foreign professionals left. It was pointed out to the South Yemen
government that similar plants in Morocco and Egypt were not in use and were not
constructed correctly. It turned out that even these countries, which were much more
advanced than Yemen, were not capable of maintaining the facilities.
The issue of collection and disposal is another solid waste problem I have seen in
the Middle East and Asian countries. Garbage often left in streets for a considerable
amount of time exposes children and other residents to pathogens and pathogenic
bioaerosols. In Chapter 1, a dump in Wuhan, China, shown in Figure 1.3, is exem-
plary of conditions prevalent throughout Asia, Africa, Mexico, and other Central
and South American countries. Workers, scavengers, and the public are at risk of
exposure and conditions present a threat to public health, especially since hygiene is
not well practiced and disinfectants are scarcely available.
In Egypt, a country of 80 million persons, 75% of the solid waste is generated
in urban areas. It is estimated that by 2025, MSW will reach 33 million tons per
year. Eight percent of the solid waste is sent to a compost plant, and the rest is dis-
posed in dumps in open spaces, presenting a major health risk to the public (Khatib
2011; Collins and Kennedy 1992). Similarly, this situation exists in many Asian and
African countries.
What are the health impacts of solid waste? Unless MSW is properly disposed,
when discarded, especially for organic wastes, decomposition occurs that creates
favorable conditions for the survival and growth of pathogens. Wastes harboring
pathogens can be diapers, clothes containing fecal matter, blood, animal flesh, body
fluids, soiled rags, and wastes that attract flies, rats, and other vectors and creatures.
The most vulnerable persons are handlers and workers, as well as children and pick-
ers frequenting dumps.
When dumps are located adjacent to bodies of water that serve as a source of
drinking water, the additional potential from water contaminated with pathogens
exposes the local population. Frequently, dumps or waste disposal sites are located
upstream of wells and sources of drinking water.
The occupational hazards related to disposal and handling of solid waste are
as follows:

• Infections
• Skin and blood infections obtained from direct contact with wastes and
open wounds
• Eye infections from exposure to dust
• Respiratory infections from exposure to pathogenic bioaerosols
• Infections and diseases passed on through vectors
• Chronic diseases
• Infections from medical wastes discharged as part of solid waste
• Exposure from industrial discharge of chemicals (not covered in this book)
• Accidents, such as infected wounds from exposure of ruptured skin or
burns from methane gas explosions at landfill sites
Pathogens and Diseases of Solid Wastes 33

FIGURE 4.3  Scavengers at a dump in Wuhan, China.

Health risks from waste are caused by numerous factors, including the following:

• The composition and type of raw waste


• The decomposition of the waste and its release, leading to the environmen-
tal potential for diseases or infection (e.g., dust, attraction to vectors)
• Occupational risks related to handling and processing of the waste
• Disposal of wastes

Dumps in developing countries are a source of recyclable material. In developed


countries, recycling usually takes place at the source or at a mechanized recycling
center. An example is Palm Beach County, Florida. In dumps in developing coun-
tries, often children and women are involved in rummaging through the material,
hence creating a greater risk of exposure. Furthermore, the lack of proper hygiene
increases the exposure of the individuals and their families. Most likely, workers
in dumps such as shown in Figure 4.3 do not change clothes when arriving home
or traveling. I even saw a child in a baby carriage waiting while the mother scav-
enged the dump. Both the workers and the scavengers are contaminated directly or
through bioaerosols.

PATHOGENS AND THEIR DISEASES


A pathogen is an organism capable of causing disease. It can be a virus, bacteria,
micro­organ­isms, fungi, or actinomycetes. Often, they are classified as primary and
secondary pathogens. Primary pathogens can invade and infect a healthy person.
The young and aged are the most vulnerable. Secondary pathogens primarily invade
and infect a debilitated person or an individual on immunosuppressant medication.
Good examples are diabetics, especially those with type I diabetes, but those with
type II can also be affected. The immune system of these individuals is depressed,
and they are more subject to infections. How many organisms are needed to cause
an infection was addressed in the discussion of risk assessment, especially dose–­
response relationships or infective dose.
34 Disposal and Management of Solid Waste: Pathogens and Diseases

The significant aspect of diseases resulting from poor sanitation is illustrated by


the bubonic or pneumonic plague in 1994 in Surat, India. Several hundred thousand
people fled the city. This represented 25% of the population of about 1.5 million.
Approximately 6,000 persons became ill, and 56 died. The cost to the economy of
India was estimated at $600 million. Vectors were a significant factor in the spread
of the disease.
As indicated, the leachate from landfills in developed countries currently is con-
tained by liners. There is also a requirement to cover the waste disposed daily. This
prevents the spread of diseases, especially pathogenic bioaerosols. Previously, land-
fills were essentially soil-­covered dumps. The leachate may enter groundwater, a
source of drinking water. Engelbrecht and Amihor (1975) found several pathogens
in landfill leachate: Staphylococcus aureus, Streptococcus pyogenes, Streptococcus
faecalis, Streptococcus durans, Streptococcus pneumonia, Klebsiella pneumoniae,
various Salmonella serovars, as well as Proteus spp. and coliform bacilli.
Pourcher et al. (2001) identified aerobic cellulolytic bacteria in both 1- and 5-year-­
old refuse samples from a French landfill site. The organisms ranged from 1.1 × 106
to 2.3 × 108 CFU (colony-­forming units) (g.dry wt) –1. The predominant groups found
were Bacillaceae, Cellulomonas, Microbacterium, and Lactobacillus.
Adeyeba and Akinbo (2002) found a high degree of contamination of solid
waste dump sites with bacterial and parasitic agents. The organisms found were
Ascaris lumbricoides, Entamoeba histolytica, hookworm/­strongyle, Ascaris suum,
Ascaris vitulorum, Strongyloides papillosus, Schistosoma suis, and Dicrocoelium
dendriticum. Some of these infect humans (see Table  4.1); others infect domestic
animals. Some of the bacterial organisms were Klebsiella species, Escherichia coli,
Proteus species, streptococci, and other Gram-­positive micro­organ­isms.
Bioaerosols were also detected in airborne dust. They included endotoxins and
fungi. Danuta et al. (2004) measured the air quality in offices of municipal landfills.
They used a six-­stage Anderson sampler and found that the concentration of bacterial
aerosols ranged from 1 × 103 to 7.3 × 104 CFU/­m3. Outdoors, the range was similar.
The fungal units, which could be more significant from a respiratory aspect, ranged
from 2.3 × 102 to 7.3 × 103 indoors and 2.0 × 102 to 1.2 × 104 CFU/­m3. The implica-
tion to public and worker health was discussed (Danuta et al. 2004). Bioaerosols are
discussed in detail in Chapter 8.
There are many sources of pathogens from solid waste that can affect humans,
primarily

• Soil: human wastes, solid wastes, animal wastes


• Air: human wastes, solid waste, animal wastes
• Water for bathing and drinking: human wastes, animal wastes
• Plants: solid waste, domestic and wild animal wastes
• Domestic animals: contaminate soil, directly contaminate humans
• Wild animals: plants, soil

Achudume and Olawale (2007) collected and enumerated pathogens from four
different dumping sites (solid waste sources). Their results showed the presence of
bacterial species, including Pseudomonas, Micrococcus, Actinomyces, Neisseria,
Pathogens and Diseases of Solid Wastes 35

TABLE 4.1
Human Pathogens of Significance Reported in the Cited Literature
Organism Disease
Acinetobacter Gram-­negative bacteria; cause pneumonia, urinary tract infections, meningitis
baumannii
Actinobacillus Parasites or pathogens in mammals, birds, and reptiles
pleuropneumoniae
Actinomyces spp. Gram-­positive bacillus; causes infection in dental procedures and oral abscesses
Agents: A. israelii, A. gerencseriae, A. naeslundii, A. odontolyticus, A. viscosus,
A. meyer, and Propionibacterium propionicum
Normal flora of mouth, gut, genital tract
Aeromonas spp. In humans and marine animals
Aeromonas hydrophila, Aeromonas caviae, Aeromonas sobria cause
gastroenteritis
Ascaris Cause bloody sputum, cough, fever, abdominal pain, infection
lumbricoides
Bacillus spp. Genus of Gram-­positive bacilli
B. anthracis causes anthrax; B. cereus causes a foodborne illness
Bacillaceae spp. A family of bacteria that includes the genera Bacillus and Clostridium, which are
generally rod shaped, Gram negative, and spore producing; endotoxin
Bordetella spp. Species are B. bronchiseptica, B. pertussis, and B. parapertussis
Cause whooping cough, respiratory infections
Cellulomonas spp. Cause infective endocarditis and osteomyelitis
Enterobacteria Gram-­negative bacteria that include many of the more familiar pathogens, such
as Salmonella, Escherichia coli, Yersinia pestis, Klebsiella, and Shigella
Entamoeba Causes amebiasis, acute colitis, bloody diarrhea, abdominal pain
histolytica
Escherichia coli Causes digestive tract infections
var. II
Klebsiella Causes infections, including pneumonia, bloodstream infections, wound or
pneumonia surgical site infections, and meningitis
Microbacterium Genus includes pathogens known to cause serious diseases in mammals,
spp. including tuberculosis (Mycobacterium tuberculosis) and leprosy
(Mycobacterium leprae)
Micrococcus May be involved in other infections, including recurrent bacteremia, septic
shock, septic arthritis, endocarditis, meningitis, cavitating pneumonia
(in immunosuppressed patients)
Neisseria Two are pathogens, N. meningitides and N. gonorrhea; often cause asymptomatic
infections
Pasteurella Primarily causes a respiratory infection in sheep and goats
haemolytica
Proteus spp. P. vulgaris, P. mirabilis, and P. penneri: opportunistic human pathogens
Proteus includes pathogens responsible for many human urinary tract infections
P. mirabilis causes wound and urinary tract infections
Pseudomonas spp. Pseudomonas aeruginosa increasingly recognized as an emerging opportunistic
pathogen of clinical relevance
(Continued)
36 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 4.1 (Continued)
Human Pathogens of Significance Reported in the Cited Literature
Organism Disease
Salmonella spp. Acute symptoms: Nausea, vomiting, abdominal cramps, diarrhea, fever,
headache
Chronic consequences
Salmonellosis is infection of the intestines
Serratia plymuthica Are not common source of infection; nosocomial septicemia has been reported
Staphylococcus Found on the skin and respiratory system; causes skin infection (e.g., boils),
aureus respiratory disease, food poisoning
Streptococcus Can cause endocarditis and bacteremia, urinary tract infections, meningitis, and
faecalis other infections in humans
Streptococcus Is the cause of many important human diseases, ranging from mild superficial
pyogenes skin infections to life-­threatening systemic diseases
Infections typically begin in the throat or skin
Streptococcus Major cause of pneumonia
pneumoniae

Sources: Major sources: Food and Drug Administration (FDA). 2012. Bad bug book—foodborne
pathogenic micro­ organ­
isms and natural toxins handbook. http://www.fda.gov/­ food/­
foodsafety/­foodborneillness/­foodborneillnessfoodbornepathogensnaturaltoxins/­badbugbook/­
default.htm; Centers for Disease Control and Prevention (CDC). 2012. Diseases and
conditions. http://www.cdc.gov/­diseasesconditions.

Bacillus, and Klebsiella. In later work, Achudume and Olawale (2010) showed that
Klebsiella pneumoniae, Pseudomonas aeruginosa, and other nonfermenting hetero-
trophic microbes were identified in soil underlying urban waste sites in southwest-
ern Nigeria.
A study by Shantha, Sarayu, and Sandhya (2009) in India evaluated bioaero-
sols from a municipal dumping ground. Depending on the time of the year, the
range of bioaerosols was from nil to 106 CFU/­m3. In most cases, the values were
higher than 106. Bacteria in the air were Salmonella spp., Klebsiella pneumoniae,
Enterobacteria, and Pseudomonas spp. Any of these can result in human disease. It
is interesting that with the more recent emphasis on endotoxins and Aspergillus spe-
cies, these were not enumerated.
Flores-­Tena et al. (2007) evaluated the air, soil, and leachate in the San Nicolas
landfill in Mexico. The authors indicated that landfills are the most common meth-
ods of MSW disposal in major Mexican cities. No information was provided on
the design of the landfills and their mode of operation, which have a significant
effect on both the leachate and the air. They isolated 39 pathogenic and opportu-
nistic Gram-­negative bacteria. Ten were pathogenic, 17 were opportunistic, and 2
were plant pathogens. The means of the total bacterial count in soil, leachate, and air
samples were 3.0 × 108 CFU/­g, 1.5 × 106 CFU/­m L, and 4.4 × 103 CFU/­m3, respec-
tively. The organisms found in leachate were Actinobacillus pleuropneumoniae,
Bordetella spp., Escherichia coli var. II, and Acinetobacter baumannii. Airborne
Pathogens and Diseases of Solid Wastes 37

bacteria represented 19 species. Pasteurella haemolytica was isolated in all the air
samples. Other species detected were Serratia plymuthica and Aeromonas. There
were many other species found, but in smaller amounts.
One of the most comprehensive studies on occupational and environmental health
issues of solid waste management was a report written by Cointreau (2006). The data
describe infectious diseases, respiratory infections, and cancer. Some of the diseases
were from foodborne pathogens, and others were from vectors.
The data presented clearly indicate the lack of recent information on dumps, espe-
cially in developing countries. Most of the data describe findings of primary patho-
gens. Totally lacking is information on bioaerosols, especially Aspergillus fumigatus,
molds, and endotoxin. Asthma has been on the increase, even in developed countries.
This, to some extent, can be attributed to molds and other bioaerosols.

VECTORS
One of the most important aspects of open landfills, dumps, or MSW left in streets is
the issue of vectors. Vectors are difficult to control, particularly in developing coun-
tries where slums occur, dumps exist, and there is poor sanitation. Solid waste manage-
ment is key to vector control. Probably the most well-­known attempt at vector control
is mosquito eradication. Major diseases through vectors are indicated in Table 4.2.
At the beginning of the twentieth century, vector-­borne diseases were a significant
global health problem (Gubler 2008), and are still a major health problem in devel-
oping countries. Vector-­borne disease describes an illness caused by an infectious
microbe that is usually transmitted to people. However, vertebrates, including foxes,
raccoons, skunks, and dogs, which can all transmit the rabies virus to humans via a
bite, can also act as vectors. Arthropods account for over 85% of all known animal
species, and they are the most important disease vectors. They can infect animals as
well as humans. More than 600 different viruses are transmitted by arthropods. The
most common vectors are flies, mosquitoes, ticks, lice, fleas, and bugs. Mosquitoes,
which primarily transmit parasitic and viral diseases, are the most important arthro-
pod vectors (Gubler 2008). This is especially true in Africa and Asia, where there
has been a major effort to eradicate mosquitoes.
The disease agent (e.g., virus and bacteria) is normally found in a reservoir that
can be an animal or a physical environment (e.g., soil). Children are at particular risk
from vectors. The diseases transmitted by vectors could be viral (e.g., yellow fever,
dengue fever, encephalitis); bacterial, such as Rickettsia typhi and Yersinia species;
and parasitic, either helminths or protozoa. Uncollected waste containing stagnant
water breeds mosquitoes. Containers, used tires, and similar items will retain water
after a rain and are excellent breeding grounds for mosquitoes. It is estimated that
50 to 100 million cases of dengue fever occur each year.
Ahmed (2011) reported on vectors of pathogens from selected refuse dumps in
northern Nigeria. The vectors found were the cockroach (Periplaneta americana),
dung beetles (Canthon pilularius), housefly (Musca domestica), black garbage fly
(Ophyra leucostoma), stable fly (Stomoxys calcitrans), latrine fly (Fannia scalaris),
and other species of the Diptera order. The cockroach is known to feed on fecal
38 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 4.2
Major Diseases through Vectors
Disease/
­Disease Agent Illness Vector Reference
Yellow fever Febrile illness, severe liver Mosquito CDC 2011
disease
Dengue Febrile illness, severe Mosquito; transmitting CDC 2011
musculoskeletal pain four serotypes of Taber’s Cyclopedic
flavivirus Medical Dictionary
Encephalitis Flu-­like symptoms, headache, Mosquito Mayo Clinic (2011)
seizures, inflammation of the
brain
Yersinia Y. pestis causes plague Rodents Sherris Medical
Microbiology (Ryan
and Ray 2004)
Rickettsia Murine typhus: fever, headache, Fleas CDC 2009
typhi chills nausea, vomiting

Note: CDC = Centers for Disease Control and Prevention.

matter and transmit such diseases as amoebiasis caused by Entamoeba histolytica,


giardiasis, and Toxoplasma gondii.
The two species of beetles are known to transmit Toxoplasma gondii and
Cryptosporidium parvum. The housefly is known to transmit protozoan parasites and
bacteria, such as Salmonella, Shigella, Campylobacter, Escherichia, Enterococcus,
Chlamydia, and other species that produce diseases (Ahmed 2011). The black gar-
bage flies, although not a direct human vector, contaminated food, causing such
infections as polio, typhoid fever, dysentery, and food poisoning. The stable fly is
known to harbor a variety of pathogens that cause diseases in humans. Several of the
other species found can also cause diseases in humans (Ahmed 2011). The article did
not report on direct infections from these vectors on diseases. Essentially, it reported
on vectors found in Nigerian dumps that could be responsible for human diseases
attributed to uncollected waste.

SUMMARY
Municipal solid waste, often referred to as garbage or household waste to differenti-
ate it from industrial wastes, contains pathogens from numerous sources, such as
diapers, spoiled food, contaminated clothing, and other material. These may include
body fluids and blood, facial tissues, animal and human wastes, and other sources.
In developed countries, most MSW is either landfilled or incinerated. In the
United States, over 50% is landfilled, whereas in Europe the majority is incinerated.
Landfills are regulated to reduce or prohibit groundwater contamination, and daily
landfill cover reduces the dispersion and dissemination of pathogenic bioaerosols.
Pathogens and Diseases of Solid Wastes 39

Recycling, reuse, source separation, and mechanical separation are increasing but
often depend on markets for such items as paper, cardboard, glass, and plastics.
In developing nations and emerging industrial nations with large populations,
much of the MSW ends up in uncontrolled dumps. These sites are open, and scav-
engers roam them to seek reusable and resalable items. Consequently, workers or
scavengers are exposed to pathogens, resulting in diseases. Not only are the individu-
als exposed, but also they bring pathogens into the home and public places on their
clothing and shoes. Furthermore, MSW is often left in streets and not removed for
days, harboring vectors.
Dumps are major sources of vectors such as rats, mosquitoes, and other arthro-
pods. These are major transmitters of diseases. Mosquitoes proliferate in standing
water, often found in containers or used rubber tires. Dengue fever, resulting in mil-
lions of cases of fever and mortality, especially in children, occurs annually.
Dumps that are located near bodies of drinking water (e.g., streams) contaminate
the water, resulting in gastrointestinal diseases. Open dumps are a source of patho-
genic bioaerosols, resulting in respiratory diseases in handlers, workers, and persons
separating recyclable or reusable items.
The change in demographics and increased urbanization puts additional cost
on disposal and proper treatment of MSW in developing countries. In places like
India, large families live in crowded conditions, resulting in transmission of diseases
among family members.

REFERENCES
Achudume AC and Olawale JT. 2007. Microbial pathogens of public health significance in
waste dumps and common sites. J Environ Biol 28: 151–154.
Achudume AC and Olawale JT. 2010. Enumeration and identification of Gram-negative bacte-
ria present in soil underlying urban waste-­sites in southwestern Nigeria. J Environ Biol
31: 643–648.
Adeyeba OA and Akinbo JA. 2002. Pathogenic intestinal parasites and bacterial agents in solid
waste. East Afr Med J 79: 604–610.
Ahmed AB. 2011. Insect vectors of pathogens in selected undisposed refuse dumps in Kaduna
Town, northern Nigeria. Sci World J 6: 21–26.
Althaus H, Sauerwald M, and Schrammeck E. 1983. Waste from hospitals and sanatoria.
Zentralbl Bakteriol Mikrobiol Hyg B 178: 1–29.
Centers for Disease Control and Prevention (CDC). 2009. Outbreak of Rickettsia typhi
infection—Austin, Texas, 2008. http://www,cdc.gov/mmwr/preview/mmwrhl/
mm5845a4.htm
Centers for Disease Control and Prevention (CDC). 2011. Yellow fever. http://www.cdc.gov/
yellowfever/
Centers for Disease Control and Prevention (CDC). 2012. Diseases and conditions. http://
www.cdc.gov/diseasesconditions
Cointreau S. 2006. Occupational and Environmental Health Issues of Solid Waste. Washington,
DC: International Bank for Reconstruction and Development/World Bank.
Collins GH and Kennedy DA. 1992. The microbial hazards of municipal and clinical wastes.
J Appl Bacteriol 73: 1–6.
Danuta OL, Krzysztof U, Wlazlo A, and Pastuszka JS. 2004. Microbial air quality in offices at
municipal landfills. J Occup Environ Hyg 1: 62–68.
40 Disposal and Management of Solid Waste: Pathogens and Diseases

Engelbrecht RS and Amirhor P. 1975. Inactivation of Enteric Bacteria and Viruses in Sanitary
Landfill Leachate. Urbana, IL: University of Illinois, Department of Civil Engineering.
Federal Communication Commission. Ntisl BB 234.
Flores-­Tena FJ, Guerrero-­Barrera AL, Avelar-­Gonzalez FJ, Ramirez-­Lopez EM, and Martinez-­
Saldana MC. 2007. Pathogenic and opportunistic Gram-­negative bacteria in soil, leach-
ate and air in San Nicolas landfill at Aquascalientes, Mexico. Rev Latinoam Microbiol
49: 25–30.
Food and Drug Administration (FDA). 2012. Bad bug book—foodborne pathogenic micro­
organ­i sms and natural toxins handbook. http://www.fda.gov/food/foodsafety/
foodborneillness/foodborneillnessfoodbornepathogensnaturaltoxins/badbugbook/
default.htm
Gubler DJ. 2008. The global threat of emergent/reemergent vector-­borne diseases. http://www.
ncbi.nlm.nih.gov/books/NBK52945/
Khatib IA. 2011. Municipal solid waste management in developing countries: future chal-
lenges and possible opportunities. In Integrated Waste Management, Vol. 2, ed. Kumar
S. Rijeke, Croatia: INTECH.
Mayo C. 2011. Encephalitis. http://www,mayoclinic.com/health/encepholitis/DS00226
Pourcher A, Sutra L, Hebe I, Moguedet G, Bollet C, Simoneau P, and Gardan L. 2001.
Enumeration and characterization of cellulolytic bacteria from refuse of a landfill.
FEMS Microbiol Ecol 34: 229–241.
Ryan KJ and Ray CG, eds. 2004. Sherris Medical Microbiology. New York: McGraw Hill.
Shantha R, Sarayu K, and Sandhya S. 2009. Molecular identification of air micro­organ­isms
from municipal dumping ground. World Appl Sci J 7: 689–692.
Taber’s Cyclopedic Medical Dictionary, 22nd edition. Philadelphia, PA: FA Davis Co.
5 Pathogens and
Diseases of Sewage
Sludge, Septage, and
Human Fecal Matter

INTRODUCTION
The collection, disposal, and management of human wastes greatly affect the poten-
tial for diseases from pathogens discharged with these wastes (Table 5.1). In devel-
oped countries, humans generally discharge fecal matter through toilets into sewage
systems or septic systems. The object of the sewer system is to separate the solids
from liquids and to disinfect these components before their discharge into the envi-
ronment. A generalized sewage treatment system is shown in Figure 5.1.
Although this is a general process flow, there are several variations, all with the
same objectives. The objectives are to produce a clean and disinfected effluent and
usable solids, termed biosolids. During the beginning of the process, large objects
such as rags, rocks, and sand may cause damage to pumps and other aspects of the
process. These are removed and sent to a landfill. A few facilities operate an incinera-
tor, and the ash is landfilled. Following these first two steps, the influent is treated in
the primary treatment. This is also a physical process designed to further separate
the liquid from solids. The solids are termed primary sludge and later combined with
sludge produced by secondary treatment, which is a biological treatment. The effluent
is relatively clean, but since it can contain pathogens, it requires disinfection. Since
many compounds are soluble in water, they may be present in the effluent, and if there
is a need to discharge the effluent into a pristine body of water, further treatment may
be needed, called tertiary treatment. This was originally designed to remove nitro-
gen and phosphorus. However, we more recently learned that effluent might contain
organic compounds that could have an impact on the environment. These compounds,
such as surfactants, are more difficult and expensive to remove. The disinfected efflu-
ent is sometimes used to irrigate golf courses or other public works.
The solids are usually thickened and often are placed into sealed tanks called
digesters. During digestion, which is an anaerobic process, methane or biogas is
produced. This may be burned or reused to produce power for use in the waste­
water facility. Biosolids is a term given to processed sewage sludge. The main rea-
son for the use of the term is that the term sludge is often used without prefacing it
with the word sewage, so it can be misleading. For example, the medical profession
uses sludge for blockage of the intestinal system. The term biosolids is specific. The

41
42 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 5.1
Some Bacteria Found in Wastewater, Sludge, and Biosolids and On-­Site Soil
Transmission Systems and the Diseases They Transmit
Bacteria Disease
Salmonella spp. (approximately 1,700 types) Salmonellosis
Gastroenteritis
Salmonella typhi Typhoid fever
Mycobacterium spp. Tuberculosis, leprosy
Shigella spp. Dysentery
Yersinia spp. Gastroenteritis
Vibrio cholerae Cholera
Campylobacter jejuni Gastroenteritis
Escherichia coli (pathogenic strains) Gastroenteritis
Helicobacter pylori Duodenal and gastric ulcers
Yersinia enterocolitica Diarrhea (watery or bloody), fever
Aeromonas hydrophila Gastroenteritis, cellulitis, myonecrosis, eczema
Leptospira Kidney damage, meningitis, liver failure, respiratory
stress, death
Brucella Brucellosis, fever, headache, fatigue, anorexia

Viruses
Enteroviruses
  Hepatitis A Infectious hepatitis, liver disease
  Hepatitis E Liver inflammation
 Reoviruses Respiratory and gastrointestinal infections
 Rotaviruses Diarrhea, vomiting, abdominal pain, fever
 Adenoviruses Respiratory infections
Caliciviruses
 Norwalk
 Snow

biosolids, produced after anaerobic digestion, are usually dewatered. These biosol-
ids are reused as a fertilizer in land application. Land application immediately after
digestion may be used directly through either spraying or spreading. Prior to land
application, the biosolids must be stabilized to avoid odors and further reduce patho-
gens. Stabilization can be achieved by composting, alkaline treatment, or heat drying.
Biosolids management is regulated by the federal government in a set of regulations
termed 40 CFR 503 (Epstein 1997, 2003; National Research Council [NRC] 2002).
A septic system (on-­site disposal system, OSDS) is used where a wastewater col-
lection system is not available. In communities where a sewage treatment plant and
a collection system are not available, individual homes or several homes combined
would have a septic system. The septic system would consist of a tank that receives
household wastes from sinks, bathtubs, and toilets. The tank is designed to allow
Pathogens and Diseases of Sewage Sludge, Septage, and Human Fecal Matter 43

Wastewater Influent
Collection Grit
Pump
System Removal
Station

Rocks
Screenings Sand
Landfill
Incineration

Primary Secondary Effluent Discharge


Sedimentation Treatment Disinfection to Water
Courses

Recycle
Primary Secondary Liquid or Reuse
Sludge Sludge

Solids Sludge Solid Biosolids


Thickening Digestion Dewatering Treatment

Biogas Reuse
Incineration
Landfill Land Application
Composting
Alkaline stabilization
Heat drying
Other

FIGURE 5.1  Generalized sewage treatment system.

solids to settle to the bottom. These solids need to be pumped out periodically. When
the tank is full, the liquid portion is passed through perforated pipes into the soil.
Fortunately, if the system is designed properly and the soil conditions are right, the
pathogens will not survive or reach groundwater. In the United States, approximately
20% of the population in 1998 used septic systems (Meschke and Sobsey 1999).
Contamination of groundwater can occur when a system fails and is implicated in up
to 40% of groundwater-­attributed outbreaks (Cogger 1988).
In developing countries, collection and treatment systems or septic systems are not
available or used. Consequently, fecal matter is often discharged outdoors, not even
into a pit or outhouse. Children or adults are exposed to these pathogens, and dis-
eases occur. Fecal-­to-­oral contamination is common. Disease prevention is difficult.
Furthermore, as was pointed out, vectors such as flies and mosquitoes can transmit
diseases from this source.
Diarrheal stool specimens have been used to identify microbial pathogens.
Therefore, the discharge of fecal matter from children with diarrhea can result
in infections.
44 Disposal and Management of Solid Waste: Pathogens and Diseases

PATHOGENS AND DISEASES


Wastewater contains pathogens from human and animal wastes discharged into the
sewer system. In addition, surface runoff will contain animal and avian pathogens.
Human fecal matter discharged on soil surfaces, as commonly occurs in develop-
ing countries, can directly contaminate individuals or drinking water supplies.
Pathogens in runoff can enter bathing waters as well and infect humans.
Global and regional conditions can also affect the type and numbers of certain
pathogens. The mobility of our society, ease of travel, and influx of individuals from
developing countries, especially from semitropical and tropical regions, increase the
likelihood of both numbers and types of parasites entering wastewater. Increased
numbers of pathogens with disease resistance as a result of mutation and the improper
use of antibiotics are becoming evident. Infections with Escherichia coli O157H7
and Helicobacter pylori and mad cow disease (bovine spongiform encephalopathy,
BSE) are more prevalent, and not much is known about their reduction or elimina-
tion during wastewater treatment. The survival of human immunodeficiency virus
(HIV) and other pathogens in wastewater has been studied and reported (Casson
1992; Chauret, Springthorpe, and Sattar 1999; Epstein 2003).
Food contamination occurs more frequently. Each year, 48 million people in the
United States become sick from contaminated food. Common contaminating cul-
prits include bacteria, parasites, and viruses. Symptoms range from mild to serious,
including

• Upset stomach
• Abdominal cramps
• Nausea and vomiting
• Diarrhea
• Fever
• Dehydration

Harmful bacteria are the most common cause of foodborne illness. Foods may
have some bacteria on them when you buy them. Raw meat may become contami-
nated during slaughter. Fruits and vegetables may become contaminated when they
grow or are processed (MedlinePlus, nih.gov).
Each year, more than 9 million foodborne illnesses are estimated to be caused by
major pathogens acquired in the United States. Using data from outbreak-­associated
illnesses for 1998–2008, we estimated annual US foodborne illnesses, hospitaliza-
tions, and deaths attributable to each of 17 food commodities. We attributed 46% of
illnesses to produce and found that more deaths were attributed to poultry than to
any other commodity (Painter et al. 2013).
Pathogens can be grouped into two major categories. Primary pathogens can
invade and infect healthy humans. Secondary pathogens invade and infect debilitated
or immunosuppressed individuals. The important human enteric microbial pathogens in
on-­site soil transmission systems are shown in Table 5.2 (Meschke and Sobsey 1999).
Pathogens and Diseases of Sewage Sludge, Septage, and Human Fecal Matter 45

TABLE 5.2
Important Human Enteric Microbial Pathogens
• Bacteria • Protozoan
• Salmonella spp. • Cryptosporidium parvum
• Campylobacter spp. • Cyclospora cayetanensis
• Escherichia coli • Giardia lamblia
• Helicobacter pylori • Entamoeba histolytica
• Aeromonas hydrophila • Balantidium coli
• Yersinia enterocolitica • Microsporidia
• Vibrio cholerae • Toxoplasma gondii
• Brucella leptospira • Helminth
• Mycobacteria spp. • Ancylostoma duodenale
• Shigella spp. • Ascaris lumbricoides
• Viruses • Enterobius vermicularis
• Enteroviruses • Necator americanus
−− Polio • Strongyloides stercoralis
−− Echos • Trichuris trichiura
• Hepatitis A virus • Enteric viruses
• Hepatitis V virus • Protozoa
• Reoviruses • Helminths
• Rotaviruses • Nematodes (roundworms)
• Adenoviruses • Cestodes (tapeworms)
• Caliciviruses
−− Norwalk
−− Snow

Source: Modified from Meschke JS and Sobsey MD. 1999. Microbial pathogens and
on-­site soil treatment systems. http://.ces.bcsu.edu/­plymouth/­septic/98meschke.
html

Examples of secondary pathogens are

• Klebsiella sp.
• Listeria
• Molds
• Fungi
• Aspergillus fumigatus
• Penicillium
• Actinomycetes
• Endotoxin
46 Disposal and Management of Solid Waste: Pathogens and Diseases

REFERENCES
Casson LW. 1992. HIV survivability in wastewater. Water Environ Res 64: 213.
Chauret C, Springthorpe S, and Sattar S. 1999. Fate of Cryptosporidium oocysts, Giardia cysts
and microbial indicators during wastewater treatment and anaerobic sludge digestion.
Can J Microbiol 45(3): 257–262.
Cogger, C. 1988. On-­site septic systems: the risk of groundwater contamination. J Environ
Health 51(1), 12–16.
Epstein E. 1997. The Science of Composting. Lancaster, PA: Technomic.
Epstein E. 2003. Land Application of Sewage Sludge and Biosolids. Boca Raton, FL: CRC
Press.
MedlinePlus. nih.gov Foodborne illnesses, foodborne diseases. Atlanta, GA: Centers for Disease
Control and Prevention.
Meschke JS and Sobsey MD. 1999. Microbial pathogens and on-­site soil treatment systems.
http://.ces.bcsu.edu/plymouth/septic/98meschke.html.
National Research Council (NRC). 2002. Biosolids Applied to Land. Washington, DC:
National Research Council of the National Academies Press.
Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, and Griffin PM. 2013.
Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by
using outbreak data, United States. 1998–2008. Emerg Infect Dis 19(3): 407–415.
6 Pathogens in Soils

INTRODUCTION
The importance of the role of pathogens in soil depends greatly on the method of
collection and treatment of human waste materials. The potential health impacts
to populations greatly depends on the availability of infrastructure to remove and
treat human wastes, potential for contact with human wastes, control and prohibi-
tion of vectors to transmit diseases, and education related to the avoidance of dis-
ease potential.
The early literature regarding the persistence and movement of pathogens dealt
with land application of sewage, effluent, or low-­solids sewage sludge (Sepp 1971).
This literature indicated that the use of raw sewage could result in animal or human
health infections (Bicknell 1972; Dunlop, Twedt, and Wang 1951; Dunlop and Wang
1961). Currently, the practice of applying untreated sewage or sewage sludge is pro-
hibited in the United States, Canada, and Europe. The United States Environmental
Protection Agency (USEPA) 503 regulations allow land application of biosolids
(treated sewage sludge) as either class A or class B material. Class A treatments are
intended to significantly reduce pathogens to virtually nondetected limits. Class B
treatments allow land application with crop restrictions and a regulated concentra-
tion of fecal coliforms (see Epstein 1997). With all the regulations and efforts by
agencies such as the US federal government, there are still numerous incidences of
foodborne and waterborne diseases. From 1990 to 2003, produce caused the most
foodborne disease in the United States. In England and Wales, 6.4% and 10.1% of
all disease outbreaks with a known food vehicle occurred from 1993 to 1998 and
1999 to 2000, respectively. Some of the foodborne diseases could be the result of
soil contamination (Brandl 2006).
The survival of pathogens in soils depends on the pathogen surviving the waste-
water treatment processes and biosolids treatment, method of land application,
defecation on soil surfaces, soil conditions, and environmental conditions. In large
communities, many of the biosolids processes can result in effective disinfection,
and the application of these biosolids does not represent a health hazard. Public
perception may be significantly negative so that applying biosolids to the land for
certain food chain crops must be avoided. Figure 6.1 shows the potential routes of
pathogen transmission to humans and animals. Food chain crops that are cooked or
processed would have no potential for infection. These would include crops for oil
(soybeans, sunflower, and canola) or canned foods. Food crops that would not come
in contact with biosolids, such as fruit trees (citrus, nut, pears, apples, etc.), would
also not harbor pathogens and would not be a potential source of infection. Non-­food

47
48 Disposal and Management of Solid Waste: Pathogens and Diseases

Wastewater
or
biosolids

Pathogen present Pathogen

absent

air
Soil crop

(Aerosolized)

Movement Runoff Food or feed Non-food

through Chain
Eaten Cooked
soil forest, fiber Inhalation

raw or processed

Ground Surface

water water
Ingestion

Drinking water

Potential for infection


No or very little potential for infection

FIGURE 6.1  Potential routes of pathogen transmission to humans and animals.

chain crops such as fiber (cotton) or forest would also not present a hazard to humans
or animals.
Although class B biosolids can contain pathogens, the USEPA provided site
restrictions to preclude potential impacts to human and animal health and environ-
mental consequences. These site restrictions were based on the potential survival of
pathogens in the environment.
When low-­solid biosolids are applied by spraying on land, there is the potential for
pathogens to be aerosolized. Workers in particular may be subjected to these patho-
gens and become infected. Contamination of water resources, especially drinking
water, can result from the movement of pathogens through the soil or in runoff into
surface waters.
Pathogens in Soils 49

Since pathogens survive the wastewater treatment processes (primary and sec-
ondary treatment), land application of sewage sludge directly from these processes
needs to be avoided or restricted to land management systems that would have mini-
mal potential for environmental contamination or health hazards to humans and
animals. Further treatment, such as digestion, composting, alkaline stabilization, or
heat drying, increases the opportunities for land application. Composted products
can be used as soil-­conditioning materials for agricultural and horticultural applica-
tions, such as landscaping, nurseries, parks, public work projects, and home gardens;
alkaline-­stabilized biosolids can be used as lime products and soil amendments for
agriculture and horticultural practices, such as turf production and certain public
works projects; and heat-­dried materials are often used as substitutes for chemi-
cal fertilizers.
Pathogen survival in soils depends on several factors:

• Climatic and microclimate effects


• Soil physical properties
• Soil chemical properties
• Soil biological properties, especially antagonistic microbial populations

The survival of pathogens in soils and their potential movement through soils to
groundwater depends on several edaphic and climatic factors. The most important
are soil moisture, pH, temperature, organic matter, soil texture, soil permeability,
sunlight, and antagonistic microflora.
Exposure to sunlight and ultraviolet light will destroy pathogens on soil surfaces.
Desiccation and temperature will destroy organisms on the soil surface. Physical
properties of soil such as soil moisture, soil temperature, organic matter, and ionic
strength can affect pathogen survival and movement through soils.
Rudolfs, Falk, and Ragotzkie (1950) summarized the literature prior to 1950 on
the occurrence and survival of enteric, pathogenic, and relative organisms in soil,
water, sewage, sludges, and vegetation. They concluded from the early literature sur-
vey that the following soil factors affect the survival of pathogenic micro­organ­isms:

• Type of organism: Escherichia coli, Eberthella typhosa, and Mycobacterium


tuberculosis appear to be most resistant.
• Soil moisture content: Longevity is greater in moist soils. High soil
moisture-­holding capacity increases longevity.
• Soil pH: Neutral soils favor longevity.
• Organic matter: The type and amount of organic matter may serve as food
and energy sources to sustain or allow bacteria to increase.
• The presence of other micro­organ­isms reduces the presence or concentra-
tion of pathogenic organisms.
• Temperature: There is longer survival at low temperatures.

Other literature reviews were provided by Dunlop (1968) and Sepp (1971). Gerba,
Wallis, and Melnick (1975) reviewed the literature prior to 1975 and substantiated the
50 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 6.1
Survival of Bacteria in Soils
Organism Soil Temperature (°C) Survival Time (Days)
Salmonella spp. Soil — 15–7280
Salmonella serotype Soil Summer sun <28
Typhimurium
Salmonella serotype Soil Summer shade <70
Typhimurium
Salmonella typhi Soil — 1–120
Salmonella typhi Sandy soil 16–17 <29 to <58
Salmonella typhi Soil moist — <80
Salmonella typhi Soil dry — <24
Tubercle bacilli Soil — >189
Leptospira Soil — 15–43
Coliform Soil surface — 38
Streptococcus spp. Soil — 35–63
Fecal streptococci Soil — 26–77

Source: Modified from Rudolfs W, Falk LL, and Ragotzkie RA. 1950. Literature review
of the occurrence and survival of enteric pathogenic, and relative organisms in
soil, water, sewage, and sludge and on vegetation. Sewage Indust Wastes 22:
1261–1281.

TABLE 6.2
Survival Time for Some Bacteria in Soil
Temperature
Bacteria Soil Moisture (°C) Survival
Streptococci Loam ? ? 9–11 weeks
Streptococci Sandy loam ? ? 5–6 weeks
Salmonella typhi Various soils ? 22 2–400 days
Bovine tubercle bacilli Soil and dung ? ? Less than 178 days
Leptospires Varied Varied Summer 12 hours to 15 days

Source: Modified from Feachem JB, Bradley DJ, Garelick H, and Mara DD. 1980. Appropriate
Technology for Water Supply and Sanitation. Washington, DC: World Bank.

soil factors of Rudolfs, Falk, and Ragotzkie (1950). They indicated that sunlight also
reduced survival time on soil surfaces. The early data on the survival of pathogens
in soil are shown in Table 6.1 as provided by Rudolfs, Falk, and Ragotzkie (1950).
Tables 6.1 and 6.2 provide early data on the survival of some pathogens in soils.
One of the most comprehensive early reviews on the persistence of pathogens in
soil was conducted by Feachem et al. (1980). Some of his data are shown in Tables 6.3
to 6.6, which provide information on pathogen persistence in soils. Table 6.3 shows
Pathogens in Soils 51

TABLE 6.3
Survival of Enteroviruses in Soil
Moisture Temperature Days of Survival
Soil Type pH (%) (°C) (Less than)
Sterile, sandy 7.5 10–20  3–10 130–170
10–20 18–23  90–110
5.0 10–20  3–10 110–150
10–20 18–23 40–90
Nonsterile, sandy 7.5 10–20  3–10 110–170
10–20 18–23  40–110
5.0  0–20  3–10  90–150
10–20 18–23 25–60
Sterile, loamy 7.5 10–20  3–10  70–150
10–20 18–23  70–110
5.0 10–20  3–10  90–150
10–20 18–23 25–60
Nonsterile, loamy 7.5 10–20  3–10 110–150
10–20 18–23  70–110
5.0 10–20  3–10  90–130
10–20 18–23 25–60
Nonsterile, sandy 7.5 10–20 18–23 15–25

Source: Data from Feachem JB, Bradley DJ, Garelick H, and Mara DD.
1980. Appropriate Technology for Water Supply and Sanitation.
Washington, DC: World Bank.

the survival of enteroviruses, the majority of which do not survive more than 150 days
in soil. (Feachem et al. 1980). Table 6.4 shows that although parasites in soil rarely
survive for a few weeks, hookworms may survive up to six months.
Reddy, Khaleel, and Overcash (1981) provided a comprehensive review of the
behavior and transport of microbial pathogens and indicator organisms in soils
treated with organic wastes. They also concluded that the most important factors
affecting the die-­off rate were temperature, moisture, pH, and method of waste
application. Die-­off doubled for temperature increases of 10°C and increased for
decreases in soil moisture. Retention of micro­organ­isms increased with an increase
in clay content of the soil. Table  6.6 shows the average die-­off rate constants for
selected indicator organisms and pathogens.
The decay die-­off rates for Salmonella serotype Typhimurium and fecal coliform
were in the range that Reddy et al. (1981) had shown. The Shigella sonnei decay
coefficient rates were lower. Evans et al. (1995), with column studies, found that
S. sonnei and fecal coliforms survived longer on average than Salmonella serotype
Typhimurium. Casson (1996) also conducted a laboratory study and showed that two
log reductions were found after 10 to 20 days. Decay rates ranged between 0.08 log
per day and 0.4 log per day.
52 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 6.4
Survival Time for Some Parasitic Worms in Soil
Worm Soil Moisture Temperature (°C) Survival
Hookworm Sand ? Room temperature Less than
larvae 4 months
Soil ? Open shade, Sumatra Less than
6 months
Soil Moist Dense shade 9–11 weeks
Moderate shade 6–7.5 weeks
Sunlight 5–10 days
Soil Water covered Varied 10–43 days
Soil Moist 0 Less than 1 week
16 14–17.5 weeks
27 9–11 weeks
35 Less than 3 weeks
40 Less than 1 week
Hookworm ova Heated soil with Water covered 15–27 9% survival after
(eggs) night soil 2 weeks
Unheated soil Water covered 15–27 3% survival after
with night soil 2 weeks
Roundworm ova Sandy, shade 25–36 31% dead after
54 days
Sandy, sun 24–38 99% dead after
15 days
Loam, shade 25–36 3.5% dead after
21 days
Loam, sun 24–38 4% dead after
21 days
Clay, shade 25–36 2% dead after
21 days
Clay, sun 24–38 12% dead after
21 days
Humus, shade 25–36 1.5% dead after
22 days
Clay, shade 22–35 More than 90 days
Sandy, shade 22–35 Less than 90 days

Source: Modified from Feachem JB, Bradley DJ, Garelick H, and Mara DD. 1980. Appropriate
Technology for Water Supply and Sanitation. Washington, DC: World Bank.
Note: Data from other scientists are shown in Table 6.5.
Pathogens in Soils 53

TABLE 6.5
Survival of Some Viruses in Soil
Application Temperature Survival
Organism Soil System (°C) Time (Days) Reference

Poliovirus Sand dunes


(dry)

Poliovirus Effluent 31
type 1
33 >40 days Palfi 1972

30 Reduced by Moore,
4 logs in Sagic, and
30 days Sorber 1978

Poliovirus 1 Secondary Winter 89 days


effluent Summer 11 days

Activated Winter 96 days Tierney,


sewage Summer 7 days Sullivan,
sludge and Larkin
1977

Coxsackievirus Sandy soil Dewatered Winter 23 weeks


and clay Anaerobically
digested

TABLE 6.6
Die-­off Rate Constants (Day–1) for Selected Indicator Organisms
and Pathogens in a Soil-­Water-­Plant System
Standard Coefficient
Deviation of Variation No. of
Organism Average Maximum Minimum ± (%) Observations
Escherichia coli 0.92 6.39 0.15 0.64 179 26
Fecal coliforms 1.53 9.10 0.07 4.35 283 46
Fecal streptococci 0.37 3.87 0.05 0.69 188 34
Salmonella spp. 1.33 6.93 0.21 1.70 128 16
Shigella spp. 0.68 0.62 0.74 0.06   9  3
Staphylococcus spp. 0.16 0.17 0.14 0.02  14  2
Viruses 1.45 3.69 0.04 1.44  99 11

Source: After Reddy KR, Khaleel R, and Overcash MR. 1981. Behavior and transport of microbial
pathogens and indicator organisms in soils treated with organic wastes. J Environ Qual 10(3):
255–266.
54 Disposal and Management of Solid Waste: Pathogens and Diseases

BACTERIA
Shortly after the discovery of Eberthella typhosa as the causative organism for
typhoid, attempts were made to determine its survival in soils (Rudolfs, Falk, and
Ragotzkie 1950). Melick (1917) reported that E. typhosa survived from 29 to 58 days
depending on the soil type. In a sandy soil, survival lasted for 74 days. Kliger (1921)
indicated that moist alkaline conditions in soils were most favorable for the survival
of pathogens. Beard (1938, 1940) reported that soil water-­holding capacity, tempera-
ture, precipitation, sunlight, soil pH, and soil organic matter all affected the survival
of typhoid bacillus. The data showed that the survival of Salmonella typhosa was
greatest in soils during the rainy season. In sand, where drying is more rapid, the
organism survived for a short time, between 4 and 7  days; however, in soils that
retained moisture, the organism persisted for longer than 42 days.
Van Dorsal, Geldreich, and Clarke (1967) found that there was a greater die-­off
rate for Escherichia coli and Streptococcus faecalis in soil plots exposed to the sun
than for those in the shade. The authors also reported that 90% of fecal coliforms
in the soil were reduced in 3.3  days in the summer and 13.4  days in the winter.
Bacteria can move through soils to great depths. Romero (1970) reported that after
2 days, fecal coliforms and fecal streptococci organisms were observed to travel over
500 m (1,500 ft) after the application of tertiary treated wastewater. This movement
occurred in coarse gravel. Several other early authors reported that bacteria could
move through soils to depths ranging from less than 1 to 830 m. The lower soil depths
were in sand, sandy gravel, and gravel. The majority of the studies have shown that
the movement of bacteria in soils is restricted to less than 30 ft and should not per-
colate into groundwater (Butler, Orlob, and McGauhey 1954; McGauhey and Krone
1967). These studies have been primarily through the use of wastewater or biosolids
at low concentrations. Pathogens in dewatered or high-­biosolid material applied to
land will not likely leach out and move through the surface soil to groundwater. The
application of dewatered biosolids on the movement of bacteria is markedly differ-
ent from that for wastewater. Surface application, including tilling or incorporating
biosolids into the upper 15 cm (6 in.), greatly reduces the survival of bacteria and
movement. Andrews, Mawer, and Matthews (1983) found that when biosolids were
injected into the soil, 90% were inactivated after 17 days in the winter and 3.7 days
in the summer.
Sorber and Moore (1986) reviewed the literature prior to 1986 and concluded that
quantitative data describing pathogen survival or transport in biosolids-­amended soil
were extremely limited. Their data are shown in Table 6.7.
Generally, some salmonellae bacteria and indicator organisms survived for sev-
eral weeks. Median die-­off rates for indicator bacteria, fecal coliforms, fecal strep-
tococci, and total coliforms were less than those observed for Salmonella. The
literature review presented by Sorber and Moore (1986) showed that, with one excep-
tion, there was a 90% reduction in Salmonella within 3  weeks of biosolid appli-
cation. These studies were conducted with both indigenous and seeded organisms
(Andrews, Mawer, and Matthews 1983; Jones et al. 1983; Kenner, Dotson, and Smith
1971; Larkin et al. 1978). These authors indicated that seeded Salmonella organisms
often showed higher persistence. They suggested that could be the result of very high
TABLE 6.7
Survival of Several Microorganisms in Soil
Die-­off Rate: T90a Days Die-­off rate: T99b Days
Depth
Pathogens in Soils

Organism (cm) Minimum Maximum Median Observationsc Minimum Maximum Median Observations
Salmonella 0–5  6  61 12 11 11  45  22  8
5–15  4  22 15  8  7  45  30  6
Fecal streptococci 0–5  7  28 17 10 14  63  24  8
5–15 NAd NA NA NA NA NA NA NA
Fecal coliforms 0–5  7  84 25 19 12 165  60 16
5–15  4  49 16 10  9  56  32  9
Total coliforms 0–5 16 170 40  7 28 350 155  4
5–15 35  70 42  3 NA NA NA NA
Viruses 0–5 <1  30  3  9  2  52   6  6
5–15 30  56 30  3 60 100  60  3
Parasites 0–5 17 270 77 11 68 500  81  5
5–15 NA NA NA NA NA NA NA NA

Source: From Sorber CA, and Moore BE. 1986. Survival and transport of pathogens in sludge-­amended soil. In Proceedings of the National
Conference on Municipal Treatment Plant Sludge Management. Orlando, FL: Information Transfer, 25–32.
a T = 90% reduction within the days indicated.
90
b T = 99% reduction within the days indicated.
99
c Obser., observations.

d NA, data not available.


55
56 Disposal and Management of Solid Waste: Pathogens and Diseases

concentrations, 106 to 109 per liter, that were land applied. In field studies, indigenous
Salmonella generally persisted for less than 2 months, with few positive recoveries
reported for as long as 3 to 5 months. Strauch, Konig, and Evers (1981) evaluated
the survival of seeded salmonellae in biosolids applied to forestland. The soils were
sand and marl. The average temperature was 8.3°C, and average precipitation was
739 mm. Salmonellae survived from 270 to 640  days. Watson (1980), in a study
in England, found that organic matter, pH, temperature, and the physical state of
the organism affected salmonellae survival when digested biosolids were applied to
land. Salmonellae concentrations dropped from 100 million to zero in 42 to 49 days.
The sieving effect of soil, which is affected by particle size, texture (i.e., clay vs.
sand), and adsorption, can greatly reduce bacterial movement. Alexander et al. (1991)
studied the factors affecting the movement of bacteria through soil. They measured
sorption partition coefficient, hydrophobicity, net surface electrostatic charge, zeta
potential, cell size, encapsulation, and flagellation of the cells using 19 different bac-
terial strains. The results indicated that adsorption greatly contributed to the reten-
tion of bacteria and that bacterial movement through aquifer sand was enhanced by
reducing the ionic strength of the in-­flowing solution. Cell density and flow velocity
also affected bacterial movement. The data indicated that the potential for bacte-
rial contamination of groundwater from the application of biosolids was minimal.
Studies inoculating bacteria in sterile and nonsterile soil showed that pathogens were
suppressed by the presence of other soil organisms. Bryanskaya (1966) showed that
actinomycetes suppressed the growth of salmonellae and dysentery bacilli.
Pepper et al. (1993) conducted both laboratory and field studies using total
coliforms, fecal coliforms, and fecal streptococci organisms. They found that soil
moisture, soil temperature, and soil texture affected the survival of these indica-
tor organisms. Survival of organisms increased with increasing soil moisture and
clay content and decreased with increasing soil temperature. Under field conditions
when soil moisture increased as a result of rainfall, regrowth of indicator organ-
isms occurred.
Although concentrations of fecal coliforms, fecal streptococci, and salmonel-
lae decreased through an extended hot, dry summer period and were not detected,
repopulation occurred after precipitation (Gibbs et al., 1997). The authors indicated
that despite apparent die-­off of salmonellae, land to which biosolids have been
applied may be subject to salmonella repopulation. Management needs to take this
into account to protect public health.
Land application of biosolids can result in runoff and potential contamination
of surface waters. This would be especially true if the biosolids were not incorpo-
rated into the soil prior to rainfall (Evans et al. 1995). Land application of biosolids
to highly porous soils following significant amounts of precipitation could result
in some movement of pathogenic organisms for several meters. However, unless
the groundwater levels are very shallow, there is little potential for contamination
of groundwater. Biosolid application modifies soil properties, which increases the
retention and removal of pathogens. Increased organic matter will decrease water
percolation and increase water retention in sandy or gravelly soils. Biosolid appli-
cation modifies pH, which could affect bacterial survival. This is especially true
if the pH is increased through liming. The increased organic matter from biosolid
Pathogens in Soils 57

application enhances the indigenous microbial population, which could result in


pathogen inactivation.

VIRUSES
Data on virus movement in soil from the application of biosolids are meager.
However, considerable information is available as a result of effluent application to
land. Application of viruses in effluents offers much greater potential for movement
through soils and therefore represents much worse scenarios. Movement with a liq-
uid medium is more rapid than by leaching from a solid matrix. Furthermore, viruses
are adsorbed on the solid surfaces and less apt to leach. The organic matter in bio-
solids would also affect the adsorption of viruses. Survival and movement of viruses
through soil are greatly affected by soil properties. Viruses generally do not survive
long outside their hosts. They contain a nucleic acid core surrounded by proteins.
Viruses are electrically charged colloidal particles and thus are capable of adsorbing
onto soil surfaces. Many studies utilized bacteriophages as models. A bacteriophage
is a virus with specific affinity for bacteria (Stedman’s 1977).
The early studies of adsorption of viruses onto soil surfaces were reviewed by
Bitton (1975). Drewry and Eliassen (1968) studied virus retention in soils and con-
cluded that virus adsorption was affected by the soil–­water system pH. Carlson et al.
(1968) studied the adsorption of bacteriophage T2 and type 1 poliovirus to kaolinite,
montmorillonite, and illite clays. The type and concentration of cations present in
soil water affected sorption of viruses under similar ionic conditions. Kaolinite and
montmorillonite adsorbed the same amount of viruses. Illite required twice as much
salt to attain the same binding capacity. These authors concluded that the surface
exchange capacity determined by the surface density and clay particle geometry was
important in the adsorption process. Adsorption is more rapid at a lower pH.
Bagdasaryan (1964) reported that enteroviruses survived in loamy and sandy loam
soils for prolonged times. The adsorption of viruses to soil may prolong their sur-
vival (Gerba, Wallis, and Melnick 1975). Tierney, Sullivan, and Larkin (1977) also
found that poliovirus 1 viruses inoculated in raw and activated sludge survived in
soils for up to 96 days in the winter. Damgaard-­Larsen et al. (1977) found that it took
23 weeks during a normal Danish winter to inactivate 106 TCID50/g of coxsackie-
virus B3. Under warm, humid Florida conditions, Farrah, Scheuerman, and Bitton
(1981) reported a 2 log10 drop in titer of indigenous viruses in biosolids-­amended soil.
Gerba (1983) indicated that virus inactivation occurred in the top few centimeters of
soil where drying and radiation forces were greatest. Bitton, Pancorbo, and Farrah
(1984) evaluated virus transport and survival after land application of biosolids.
Viral strains of poliovirus type 1 and echovirus type 1 were mixed with anaerobi-
cally and aerobically digested biosolids, applied to the soil, and mixed with the top
2.5 cm of soil. Neither the poliovirus nor echovirus was detectable in soil after being
exposed for 8 days to dry fall weather conditions. Under summer weather conditions
in Florida, poliovirus was detectable in the soil for 35 days.
Generally, viruses are adsorbed on clays, and the adsorption capacity increased
with clay content, cation exchange capacity, specific surface, and organic matter. It
has been shown that virus adsorption in natural soils follows the Freundlich isotherm:
58 Disposal and Management of Solid Waste: Pathogens and Diseases

q = KFC1/n

where q is the amount of virus (PFU/­g of soil); C is the concentration of the virus
at equilibrium (in PFU/­m L solution); KF is the Freundlich constant determined by
the y-­axis intercept from a plot of q versus log C; and 1/n is the slope of the line as
determined by the plot.
Burge and Enkiri (1978) showed that the amount of virus adsorbed by five soils
was linearly related to the square root of time. There was a high negative correlation
with pH, as would be expected due to their amphoteric nature. The lower the soil
pH was, the more positively charged the virus particles were.
Viruses are removed from percolating water by adsorption on soil particles.
Lance (1977) found that poliovirus type 1 essentially remained in the top 5 cm.
Other factors are soil type, iron oxides, pH, cations, and virus type. Gilbert, Gerba,
et al. (1976) reported that human bacterial and viral pathogens are largely removed
as sewage effluent percolates through the soil. The viruses measured included polio,
echo 15, coxsackie B4, reovirus 1 and 2, and undetermined types. The bacterial
indicators and bacterial pathogens were fecal coliforms, fecal streptococci, and
Salmonella spp. Gilbert, Rice, et al. (1976) also reported that human viral pathogens
do not move through soil into groundwater. Lue-­Hing, Sedita, and Rao (1979) did
not find any evidence of viral contamination of runoff, surface water, or groundwater
at the Fulton County, Georgia, biosolids application site. Although the adsorption of
viruses to clays precludes their movement to groundwater, Shaub et al. (1975) have
shown that adsorbed viruses were still infectious.
Straub, Pepper, and Gerba (1992) measured the inactivation rate (k = log–10 reduc-
tion per day) of poliovirus type 1 and bacteriophages MS2 and PRD-1, in a labora-
tory study using two desert soils. Biosolids were added to a Brazito sandy loam and
Pima clay loam. They found that, under constant moisture and temperature, tem-
perature and soil texture were the most important factors controlling inactivation. As
the temperature increased from 15°C to 40°C, the inactivation rate for poliovirus and
bacteriophage MS2 increased, whereas for the bacteriophage PRD-1 a significant
increase in inactivation occurred only at 40°C. Clay soils afforded more protection
to all three viruses than sandy soils. Reduction in moisture content to less than 5%
completely inactivated all three viruses within 7 days at 15°C. Thus, a combination
of moisture reduction and high temperature is effective in virus inactivation. These
studies under laboratory conditions using soil columns and constant parameters can
provide indication of possible trends but should not be taken as definitive behavior of
organisms in the environment. Soils undergo fluctuations in moisture and tempera-
ture. These fluctuations, especially desiccation and high surface temperatures, will
destroy pathogens.

PARASITES
Sorber and Moore (1986) reported that parasites persisted the longest of most organ-
isms in soils. Gerba (1983) indicated that air, desiccation, and sunlight will result
in rapid die-­off. Protozoan cysts are highly sensitive to drying and are expected to
survive for only a few days in most soils. Entamoeba histolytica has been reported
Pathogens in Soils 59

to survive 18–24 hours in dry soil and 42–72 hours in moist soil (Kowal 1982).
Helminth eggs and larvae can survive in soil for longer periods. Under favorable con-
ditions of moisture, temperature, and sunlight, Ascaris, Trichuris, and Toxocara can
remain viable and infective for several years (Little 1980). Ascaris eggs can survive
up to 7 years in soil (Sepp 1971). However, Strauch, Konig, and Evers (1981) reported
that Ascaris eggs are dependent on a host for survival and thus died fairly quickly in
both winter and summer when seeded biosolids were applied to forestland. In the East
Bay Municipal Utility District (EBMUD, Oakland, California) study, 12.9% of the
soil samples contained viable helminth ova 3 years after biosolid application (Theis,
Bolton, and Storm 1978). Feachem et al. (1950) reported that hookworms can survive
for up to 6 months. Babaeva (1966) indicated that Taenia could survive from several
days to 7 months.

SUMMARY
Although the data on pathogen survival in soils are highly variable, it is evident that
most pathogens do not survive in soils for a great length of time. The soil environ-
ment is generally hostile to pathogens. Desiccation, soil temperature, and pH affect
their survival. Decreases in soil moisture have resulted in a greater pathogen die-­off
rate. Increases in soil temperature increase the die-­off rate of pathogens. Soil acidity
also lowers the rate of pathogen survival. Organic matter and clay affect retention,
especially of viruses. Generally, most pathogens are retained in the upper 5 to 15 cm
of the soil. The data show that bacteria and viruses do not survive in soils for exten-
sive periods. Thus, the potential for bacteria and viruses to move through soils to
groundwater is low. Parasites are larger and heavier than bacteria and viruses and do
not readily move through soils.
Most of the early studies concerned pathogens in sewage sludge, biosolids, and
wastewater. Since most biosolids applications are immediately incorporated into the
soil, the potential for contamination of surface runoff is minimal. The low survivabil-
ity of pathogens in soils also reduces the potential for surface water contamination.
Today, most biosolids are incorporated into the soil before a crop is planted. An
exception is pastures, where liquid biosolids may be applied to an existing crop.
Pathogens survive on plants for short periods of time as they are exposed to sunlight
and ultraviolet light. Desiccation is also a major factor that reduces their survival.
The major danger to humans from soils in the food chain occurs primarily in
developing countries where sanitation is poor. Human excrement is deposited in the
field, often above water resources such as wells or streams.

REFERENCES
Alexander M, Wagenet RJ, Baveye RC, Gannon JT, Mingelgrin U, and Tan Y. 1991. Movement
of Bacteria through Soil and Aquifer Sand. EPA/600/S2–91/010. Ada, OK: US
Environmental Protection Agency, Robert S. Kerr Environmental Laboratory.
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7 Geophagy and Human
Pathogens in Plants

INTRODUCTION
In Chapter 6, I discussed the pathogens in soil and their impact on human health.
This chapter presents another aspect of human health related to soils: geophagy.
Geophagy is the deliberate ingestion of soil; the practice of consuming earthy or
soil-­like substances. Another term often used is pica (Izugbara 2003). Pica differs
from geophagy in that it is less specific because it connotes the ingestion and appetite
for largely nonnutritive substances. The Centers for Disease Control and Prevention
(CDC), a unit of the National Institutes of Health, defines soil pica as eating 500 mg
to more than 50 g of soil per day.
Soil and plants as related to pathogens and human health are interrelated. There
are different variations of pica. Pica children in poor neighborhoods may ingest a soil
near their residence. This soil, for example, could be contaminated by lead as a result
of earlier lead-­based paints or from tetraethyl lead-­enhanced gasoline (Sing and Sing
2010). As an example, a young mother in Massachusetts received an old home when
her grandmother died. The mother scraped the old paint from the home and refin-
ished cabinets in the kitchen. Both her child and her dog came down with lead poi-
soning. Both had to undergo chelation, an unpleasant procedure. Removing the soil
surrounding the house was also extremely expensive as Massachusetts required that
the contaminated soil removed be sent to a hazardous waste site. The alternative was
to bind the lead with organic matter and phosphorus and to find a place on the home
grounds that was free of lead, which then became the child’s playground.

GEOPHAGY
Geophagy has been recorded in every region of the world and is reported as a patho-
logical condition by those in the medical profession (Reid 1992). It is most preva-
lent in the world’s poorest regions (Abrahams 1997; Abrahams and Parsons 1997).
Although there are some nutritional aspects to soil ingestion or geophagy, the purpose
of this section is to point out the potential health hazards, excluding nonpathogens.
Generally, pregnant women and children are the greatest consumers (Callahan
2003). Childhood geophagy routinely involves topsoil (upper 15 cm). Geophagy has
both positive and negative aspects. The positive aspects most reported in the litera-
ture refer to nutritional benefits. The practice has been observed in many cultures,
primarily in pregnant women (Njiru, Elchalal, and Paltiel 2011; Sing and Sing 2010).
Sing and Sing indicate that colloidal clays are consumed for antidiarrheal properties,
and that geophagy is practiced for nutritive substances where normal diets do not

63
64 Disposal and Management of Solid Waste: Pathogens and Diseases

have the full benefits of vegetative nutrients. Another aspect is the provision of cal-
cium, which is also associated with low supply in certain regions (Sing and Sing
2010). In Bangladesh, where there is a high concentration of arsenic in drinking
water, an additional source of arsenic could be soil ingestion. Further, baked clay,
which is ingested, may also contain cadmium and lead as well as arsenic (Al-­Rmalli
et al. 2010).
One aspect that has been pointed out is cultural (Izugbara 2003).
The practice is primarily among children of both sexes, school-­aged children,
teenage mothers, and women. There are few studies in this regard. A summary of a
study involving pregnant women in southeastern Nigeria is shown in Table 7.1. The
study of geophagy was conducted by the University of Uyo and Abia State University
in Nigeria. Table 7.2 shows the frequency of geophagy and types of soil consumed.

TABLE 7.1
Sociodemographic Characteristics
of Southeastern Nigeria Pregnant
Persons Associated with Geophagy
Pregnant Percentage
Age (years)
  Less than 30 31.3
 31–40 42.1
  41 and older 27
Highest level of education
  No formal education 33.3
  Primary (1–6 years) 49.6
 Secondary 14.6
  Beyond 14 years of age 2.5
Marital status
 Single 2.5
 Married 90
Religion
 Catholic 39.6
 Protestant 58.3
 Other 2.1
Occupation
 Housekeeper 89.6
 Farmer 97.5
  Petty trader (businesswomen) 82.5

Source: Modified from Izugbara CO. 2003. The


cultural context of geophagy among
pregnant and lactating Ngwa women of
southeastern Nigeria. Afr Anthropol 10:
180–199.
Geophagy and Human Pathogens in Plants 65

TABLE 7.2
Frequency of Geophagy and Types
of Soil Consumed
Frequency of Soil Eaten Percentage
Eats soil at least once per day 78.3
Eats soil less than seven times per week 15
Does not eat soil at all 67
Types of soil eaten
 Clay 93
  Soil from gullies and paths 27
  Walls of huts 59.6
  Soil from cooking mounds 65.4
  Termite mounds 64.2

Source: Modified from Izugbara CO. 2003. The cul-


tural context of geophagy among pregnant and
lactating Ngwa women of southeastern
Nigeria. Afr Anthropol 10: 180–199.

Although this was a sociodemographic study, two aspects would have been interest-
ing: the chemical content of the clay/­soil and any frequency of infection from para-
sites and other bacteria or viruses.
Another aspect as a result of ingesting soil, especially in developing countries,
is the risk from soil contaminated by human and animal feces containing parasites.
Two children at two different locations were infected with raccoon roundworm
(Baylisascaris procyonis) as a result of ingesting soil (Callahan 2003; CDC 2002).
Although most of the recent literature on geophagy is from incidences in develop-
ing countries, Flynt’s Dixie’s Forgotten People: The South’s Poor Whites indicates
that geophagy was common among poor whites (Flynt 2004). The CDC indicates
that the most common infection in the United States is associated with parasitic
infection caused by Toxocara canis, and the most common route of infection is con-
tact with soil contaminated with cat and dog feces. The parasite can remain in the
soil for years (Callahan 2003).
Vermeer and Frate (1979) reported on an investigation of the black population
in rural Holmes County in Mississippi. They found that geophagy occurred among
57% of women and 16% of children of both sexes but was not found among male
adults or adolescents. The data did not correlate with hunger, anemia, or parasitic
problems (Vermeer and Frate 1979). Geophagy has also been associated with min-
eral deficiency. In a study in Turkey, iron and zinc deficiencies were found among
Turkish children and women in villages (Cavdar et al. 1983). Several symptoms were
observed, including anemia, growth retardation, and hypogonadism. Hooda et al.
(2002) evaluated five geophagic materials from Uganda, Tanzania, Turkey, and India
with mineral nutrient concentrations and conditions similar to the gastrointestinal
tract. They reported that while calcareous geophagic materials may supplement
66 Disposal and Management of Solid Waste: Pathogens and Diseases

calcium, geophagy could result in iron and zinc deficiency. Dreyer, Chaushev, and
Gledhill (2004) indicate that the local African population believed that ingestion of
soil benefits pregnant women suffering from iron deficiency.
The predominant literature regarding geophagy relates to human infections from
organisms. As would be expected, infections from geophagy related to diseases are
more common in developing countries. In 1998, Geissler et al., in a study of 204
children aged 10–18 in western Kenya, found infections by the helminth Ascaris
lumbricoides, Trichuris trichiura, and Schistosoma mansoni. There were significant
associations between geophagy and infection intensity with Ascaris lumbricoides
and Trichuris trichiura (Geissler et al. 1998).
There were also significant associations between geophagy and Ascaris lumbri-
coides and not hookworm, Trichuris trichiura, and Strongyloides stercoralis and
high microbial viable counts (maximum 120,000 CFU/­g) (Kutalek et al. 2010).
Similar results were reported by Kawai et al. (2009).
One aspect rarely reported is the relation of airborne dust and geophagy to human
health. Airborne dust can carry not only spores but also fungi, endotoxins, bacteria,
and a large variety of micro­organ­isms. Sing and Sing (2010) point out the difficulty
in studying dust components. Data from several US areas as well as Mali, Israel,
Virgin Islands, and Korea are shown in Table 7.3. Although not enumerated, amounts
of bacteria in dusts were high. Undoubtedly, several of the bacteria could have been
pathogenic. Dust containing fungal spores could increase asthmatic symptoms and
can affect respiratory conditions.
It is evident that supplemental multivitamins given to residents in villages of
developing countries can overcome some of the health aspects resulting from infec-
tions due to geophagy that are much more costly and difficult to eradicate. This
action must be coupled with education and appropriate sanitary conditions.

TABLE 7.3
Bacterial and Fungal Concentrations in Dust Storms
Fungal Fungal
Bacterial Bacteria in Concentrations Concentrations
Sample Background Dust in Background in Dust
Location Dust Source (CFU/­m3) (CFU/­m3) (CFU/­m3) (CFU/­m3)
Kansas Kansas <10 2,880–42,735 Not detected Not detected
Junction Texas <450 >1,544 Not applicable Not applicable
Mali Sahara/­Sahil 200–1,100 720–15,700 0–130 80–370
Israel Sahara 79–108 694–995 31–115 205–226
US Virgin Sahara/­Sahil 0–100 90–350 0–60 30–60
Islands
Korea Gobi/­ 105–1,930 225–8,212 100–8,510 336–6,992
Taklamakanm

Source: Modified from Sing D, and Sing CF. 2010. Impact of direct soil exposure from airborne dust and
geophagy on human health. Int J Environ Res Public Health 7: 1205–1223.
Note: CFU/­m3, colony-­forming units per cubic meter.
Geophagy and Human Pathogens in Plants 67

PATHOGENS ON PLANTS
Soil, plants, and human pathogens are interrelated. Normally, we associate human
diseases from pathogens and plants as the result of contamination. Contamination
can be caused by improper worker sanitation as well as contamination of produce
from wild or domestic animals or contaminated wastewater. Workers with proper
education and incentives can be taught to identify potential sources of contamina-
tion. Wild and domestic animals entering a produce field can contaminate the pro-
duce through defecation. The improper use of manures that have not been sterilized
(e.g., compost that has not reached 55°C) can also be a source of contamination.
In many cases, the soil becomes contaminated, resulting in contamination of the
food produced.
However, earlier data (Table 7.4) show that once human pathogens infect plants,
they can survive for long periods of time. More recently, it has been shown that there
is a relationship between human pathogens and the rhizosphere. Organisms associ-
ated with plants can be fungi, bacteria, and viruses.
In recent years, there have been numerous incidents of foodborne diseases as a
result of contamination of food crops. This could be the result of pathogen survival
in soils and contaminating crops. Manure, which often is untreated for destruction
of pathogens, could result in contamination as could irrigation waters. There was
also an indication that wild animals entering food-­growing fields could result in con-
tamination of crops. A schematic in Figure 7.1 shows the factors that can contribute
to the contamination of plants (fruits and vegetables) with human enteric pathogens
in the field (Brandl 2006). Brandl indicated that the first step in the contamination
of the aerial portion of the plant is attachment. The author provided an excellent
review. There are several potential sources of contamination of field-­grown fruits

TABLE 7.4
Survival of Pathogens or Indicator Organisms on Plants
Organism Plant Survival Time References
Poliovirus 1 Lettuce 23 days Tierney, Sullivan, and
Radish Larkin 1977
Coliforms Tomatoes 35 days Englebrecht 1978
  Salmonella typhi Vegetables 7–53 days Englebrecht 1978
  Salmonella typhi Vegetables and fruit <1–68 days Parsons et al. 1975
  Shigella spp. Vegetables 2–10 days Parsons et al. 1975
  Shigella spp. Tomatoes 2–7 days Englebrecht 1978
  Vibrio cholerae Vegetables 2 days Englebrecht 1978
  Tubercle bacilli Radish 90 days Englebrecht 1978
  Tubercle bacilli Grass 10–49 days Parsons et al. 1975
  Entamoeba histolytica Vegetables 3 days Englebrecht 1978
  Entamoeba histolytica Vegetables <1–3 days Parsons et al. 1975
  Taenia saginata eggs Pasture 90–365 days Englebrecht 1978
Enteroviruses Vegetables and fruits 4–6 days Parsons et al. 1975
68 Disposal and Management of Solid Waste: Pathogens and Diseases

Untreated manure Bioaerosols


and human wastes Contaminated irrigation water
and flood water

Insect vectors

Animal and human feces

Plants Contaminated seeds

Fungi, protozoa, nematodes and vectors in soil to plant and root

FIGURE 7.1  Pathway of plant contamination by human pathogens.

and vegetables. The application of untreated (raw) manure to fields can result in
enteric pathogens in the fields (Solomon, Brandl, and Mandrell 2006). Thus, the use
of untreated or unstabilized manure can result in the contamination of food crops.
Furthermore, organisms from a manure pile or field where manure has been applied
can contaminate irrigated water or bodies of water used for swimming or drinking.
This also applies to free-­roaming domestic or wild animals, whose fecal matter can
contaminate food or water resources. Many immigrant workers do not have proper
sanitation conditions or knowledge regarding the importance of sanitation and can
transmit disease to other workers or members of the family as well as the crops
harvested. Escherichia coli O157:H7 and other enteric bacteria can contaminate the
surface of edible plants both pre- and postharvest (Aruscavage, Miller, and LeJeune
2006). There are other reported incidents of pathogenic bacteria and viruses that can
attach to fruits and vegetables. These soil organisms have been Listeria monocyto-
genes and Clostridium botulinum.
According to earlier reports, Rudolfs, Falk, and Ragotzkie (1950) and Bryan
(1977) indicated that pathogens do not penetrate into fruits or vegetables unless their
skin is broken. Bryan reviewed the early literature on the survival of pathogens on
crops. Pathogen survival on fruits and vegetables exposed to sunlight and drying
would be short. The survival on subsurface crops such as potatoes and beets would
be similar to those in soil (Gerba 1983).
Crops whose edible portion does not come in contact with the soil or biosolids are
less apt to be contaminated. This is the basis for the Part 503 regulations concerning
class B biosolids used for land application. Table 6.6 provides information on the
survival of indicator organisms and pathogens on plants.
Kowal (1982) indicated that survival times of several bacterial pathogens ranged
from less than 1  day to 6  weeks. Virus survival on the surface of aerial crops
would be expected to be shorter than in soil because of exposure to deleterious
Geophagy and Human Pathogens in Plants 69

environmental effects, especially sunlight, high temperatures, drying, and wash-


ing off by rainfall (Kowal 1982). Gerba (1983) indicated that the intact surfaces of
vegetables are probably impenetrable for viruses. Parasites have been reported to
survive on plant surfaces for months. Sepp (1971) reported that Ascaris ova were
destroyed in 27–35 days on vegetable surfaces during dry summer weather by desic-
cation. In a study by Ohio University and the Ohio Farm Bureau federation in Ohio
(US Environmental Protection Agency [USEPA] 1985), soil and forage samples were
collected for parasitic ova and larvae on three farms. Samples were taken from pas-
ture lands treated with biosolids and untreated pasture lands. The analysis was done
before biosolid application and 7, 14, and 28 days following application. The study
concluded that the risk of parasite transmission to animals from land with applied
biosolids was indistinguishable from farms without such application.
Gagliardi and Karns (2002) studied the persistence of E. coli O157:H7 in fallow
and manured soil and plants. They reported that the bacteria persisted for 25–41 days
on rye roots and for 47–96 days on alfalfa roots. Islam et al. (2005) found that they
survived for 154–196 days on carrots and onions. Walker et al. (2004) indicated that
Pseudomonas aeruginosa, an opportunistic human pathogen, is capable of infecting
sweet basil and Arabidopsis.
The antimicrobial activity of some medicinal plant extracts have been shown to
inhibit antibacterial activity against Bacillus subtilis, E.  coli, Pseudomonas fluo-
rescens, Staphylococcus aureus, Xanthomonas axonopodis pv. malvacearum, and
Aspergillus flavus (Mahesh and Satish 2008). As plants are continuously in contact
with micro­organ­isms (i.e., bacteria, fungi, and viruses), they can accumulate anti­
microbial secondary metabolites (Gonzalez-­Lamothe et al. 2009).
It is evident from the literature that the survival rate of pathogens on plants is
short. Desiccation, temperature, and ultraviolet light are the most important fac-
tors in destroying pathogens on plants. Thus, the risk for humans consuming foods
grown where biosolids have been applied to the land is even lower since most of the
biosolids are incorporated into the soil and do not come in contact with edible food
crops. The risk to humans from pathogens in biosolids that are applied to nonedible
crops, forestry, and fruit trees is essentially nil.
Aruscavage, Miller, and LeJeune (2006) state that pathogens on edible plants
present a significant potential source of human illness. Even though some patho-
gens do not survive on plant surfaces or are removed by washing, a significant por-
tion of enteric pathogens can remain in association with fresh produce (Aruscavage,
Miller, and LeJeune 2006). As these authors report, contrary to conventional wis-
dom, Escherichia coli and Salmonella survive outside the animal host. Often, irri-
gation water was insufficient to remove micro­organ­isms (Brandl 2006). In 2006,
increased foodborne disease outbreaks in the United States were due primarily to
E.  coli O157:H7, Listeria monocytogenes, Salmonella serotype Enteritidis, and
Clostridium botulinum (CDC 2009). It is not known how the opportunistic fungal
pathogen Cryptococcus can complete its sexual cycle in association with plants (Xue
et al. 2007).
Tyler and Triplett (2008) showed in laboratory studies that enteric human patho-
gens such as Salmonella and E. coli O157:H7 can enter plants. Plant defenses can
regulate the extent of entry.
70 Disposal and Management of Solid Waste: Pathogens and Diseases

The removal of enteric pathogens during washing and sanitizing may not be
effective if the organism is localized on subsurface sites on leafy green plant tissue
(Hirneisen, Sharma, and Kniel 2012). Akhtyamova (2013a, 2013b) also indicated
that members of the family Enterobacteriaceae, including pathogenic Salmonella
and Shigella strains, Vibrio cholerae, and Pseudomonas aeruginosa were found in
plants or inside plants.
The survival time of several pathogenic or indicator organisms on plants are
shown in Table 7.4. Most did not survive for long periods. However, tubercle bacilli
did survive for 90 days.
It is evident that the contamination and survival of human pathogenic organisms
on plants can result in human diseases. This can be minimized by good hygienic
practices and the decontamination of fruits and vegetables by washing.

SUMMARY
This chapter covered two topics related to Chapter 6, Pathogens in Soil. In this chap-
ter, one of the less-­known areas was geophagy—the deliberate ingestion of soil.
There are two aspects to this condition. Ingestion of soil can be beneficial through
the addition of minerals such as calcium, iron, and zinc and deleterious by ingestion
of human pathogens.
Earlier literature indicates that geophagy occurred in poor and less-­developed
countries as a nutritive measure that provided iron, calcium, and zinc to pregnant
mothers and children. What was ignored was the harboring of human pathogens in
the soil as a result of human defecation. In many villages in developing countries,
children and adults defecate outside the home and do not properly discharge their
feces. Subsequently, children ingesting contaminated soil will ingest pathogens,
resulting in illnesses such as diarrhea.
This chapter also discussed pathogens on plants, which is further elaborated in
the chapter on foodborne pathogens and diseases. Pathogens on plants generally do
not survive for long periods of time because of exposure to ultraviolet light, tempera-
ture, and desiccation. However, where food crops are produced, the short harvest
period and further contamination of other plants can result in human health issues.

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8 Bioaerosols

INTRODUCTION
Bioaerosols can contain living organisms, including bacteria, viruses, fungi, acti-
nomycetes, arthropods, and protozoa. They can also contain microbial products
such as endotoxin, microbial enzymes, β-1(3)-glucans, and mycotoxins (American
Conference of Governmental Industrial Hygienists [ACGIH] 1999). Many of the bio-
aerosols are ubiquitous in both indoor and outdoor environments. The sources can be
soil, plants, organic matter, animals, and humans.
Polymemkou (2012) indicates that the atmosphere has been one of the latest fron-
tiers of biological exploration. Humans can obtain pathogens by inhalation of patho-
genic airborne particles transmitted by other humans. Table  8.1 lists some of the
diseases transmitted by humans and caused by inhalation. There are several other
diseases that can result from inhalation of particles, as shown in Table 8.2.
The US Department of Defense has indicated that military personnel serving
in camps located in southwestern Asia and Afghanistan have complained of expo-
sure to dust in the air containing particles from fecal matter. These particles can
result in eye and nasal irritation and other respiratory discomfort and health aspects.
Furthermore, inadvertent contact with fecal matter and poor hygiene can result in
severe infections.
Occupational exposure to bioaerosols occurs in numerous agricultural industries,
as well as nonfarming practices. These can include the following:

• Activities related to animal manure


• Animal feeding activities
• Composting
• Pulp and paper industry
• Horticultural industry (e.g., greenhouses, landscaping, turf and sod production)
• Zoological activities
• Public works activities
• Veterinary activities

One aspect related to air pollution is asthma. Asthma is characterized by chronic


inflammation of the airways. Breathing becomes difficult. An attack of asthma
results in constricted and swollen airways filled with mucus. It is a complex condition.
Numerous molecular immune system pathways are being explored. More details are

73
74 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 8.1
Some Important Inhaled Diseases
and Their Organisms
Disease Pathogen
Chicken pox Varicella
Flu Influenza
Measles Rubeola
German measles Rubella
Mumps Mumps
Smallpox Variola
Whooping cough Bordetella pertussis
Meningitis Neisseria
Diphtheria Corynebacterium diphtheriae
Pneumonia Mycoplasma pneumoniae
Tuberculosis Mycobacterium tuberculosis

Source: Modified from Deacon, date not available.

TABLE 8.2
Some Pathogens Not as Prevalent in the Air
Disease Organism Source
Psittacosis Chlamydia psittaci Bird fecal particles
Legionnaires’ disease Legionella pneumophila Air conditioning systems
Acute allergic alveolitis Fungal and actinomycetes spores Decomposing organic matter
Aspergillosis Aspergillus fumigatus and Composting, decomposing organic
Aspergillus niger matter
Histoplasmosis Histoplasma capsulatum Fungal spores from bird and bat fecal
matter
Coccidioidomycosis Coccidioides immitis Spores in dust

Source: Modified from Deacon L, Parkhurst L, Liu J, Gewq GH, Hayes ET, Jackson S, Longhurst J,
Longhurst P, Pollard S, and Tyrrel S. 2009. Environ Health 8: 51–59.

available in a recent article (Maxmen 2011). There are numerous conditions related
to air quality resulting in asthma. These can be the following:

• Sulfur dioxide as a result of burning coal and crude oil.


• Ground-­level ozone as a component of smog. This can trigger asthma. It is
a major problem in cities with pollution from cars and trucks.
• Particulate matter, which is the result of numerous pollutants, such as dust,
soot, fly ash, diesel exhaust particles, wood smoke, and aerosols.
• Nitrogen oxide, which is emitted from automobile tailpipes and power plants.
Bioaerosols 75

The World Health Organization (WHO) indicated in 2013 that some 234 million
persons suffer from asthma. It is the most common chronic disease among children.
Most asthma-­related deaths occur in low- and lower-income countries. The strongest
risk factors are inhaled substances and particles that may produce allergic reactions
or irritation to the airways (WHO 2013). There are numerous factors that trigger
asthma. These can include

• Dust
• Mites
• Pollen and molds
• Tobacco smoke
• Chemical irritants in the workplace
• Air pollution

Other factors can be psychological or related to air temperature and even certain
medications. Although the role of human pathogens has not been cited as a direct
source, bioaerosols can increase asthmatic conditions.
Bioaerosols are found both indoors and outdoors. Many occupations are in greater
contact with bioaerosols; therefore, these workers are more vulnerable to the respira-
tory effects. The most noted such workers are

• Farmers involved with animal manure, animal feedstock, grain, hay, and
silo material
• Composters and others involved with decaying organic matter and yard
materials
• Workers dealing with municipal solid waste
• Workers involved with biosolids, especially in closed environments
• Workers in the pulp and paper industry, wood products, and lumber
• Employees in the horticultural industry, especially greenhouses, and in
landscaping, turf, and sod production
• Workers in zoological gardens
• Public work employees in parks and recreational facilities
• Veterinarians

Sources of indoor bioaerosols have been identified as follows (Cox and Wathes
1995):

• Cooling towers
• Building exhausts
• Humidification systems
• Homes
• Hospitals
• “Sick buildings”
• Laboratories
76 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 8.3
Fungal and Bacterial Concentrations in Several Industries
Industry Fungi (CFU/­m2) Bacteria (CFU/­m2)
Agricultural harvesting and storage 103–109 102–103
Animal facilities 102–108 103–105
Composting 102–107 103–107
Manufacturing technology 102–106 102–106
Sawmill 104–108 10–103
Wastewater treatment (activated sludge) 10–103 102–106

Source: Modified from Prasad M, van der Werf P, and Brickman A. 2004. Bioaerosols
and composting—a literature evaluation. Composting Association of Ireland.
http://www.cre.ie/­docs/­cre_bioaerosol_aug2004.pdf (accessed February 18,
2011).

Table 8.3 provides some data on concentration of fungi and bacteria in the air of
several industries.

FUNGI AND PATHOGENS COMMONLY FOUND


IN OUTDOOR AND INDOOR ENVIRONMENTS
The outdoor environment is the principal source of bioaerosols in the indoor envi-
ronment. The main environmental areas are the natural environment; agricultural
activities; wastewater treatment facilities; and solid waste activities, including han-
dling, collection, and disposal.
Many of the indoor airborne fungi were identified by Levetin (n.d.). Some of these
are listed next:

• Acremonium: Common species, found in soil, decaying vegetation and food


sources. Several species have been associated with human diseases, such as
meningitis, midline granuloma, and infections.
• Alternaria: Common outdoor fungus. Many times, it has been considered
the second-­most-­common mold spore genus. Numerous infections have
been reported. Lesions have been related to immunosuppressant conditions.
The spores are highly allergenic.
• Aspergillus spp.: The environmental source is plant debris, decaying veg-
etation, organic matter, and soil. It is also found in household dust and
construction material. There are over 185 species, and many cause oppor-
tunistic infections in humans. One species, Aspergillus fumigatus, has been
considered a ubiquitous organism in the environment. There are many dif-
ferent species of Aspergillus, but the most common species are Aspergillus
fumigatus and Aspergillus flavus. Other species are Aspergillus terreus,
Aspergillus nidulans, and Aspergillus niger.
Bioaerosols 77

• Basidiospores: Spores produced by mushrooms, puffballs, shelf fungi,


rusts, smuts, and many other fungi.
• Chaetomium: It is a genus of fungi. As a mold, it is found outdoors in the air
and in soil and plant debris. It can produce an infection in humans.
• Cladosporium: It is a fungal genus found both indoors and outdoors. It is a
weak plant pathogen. Indoors, it can be found in carpets and wallpaper. It is
not known to be a serious human pathogen.
• Curvularia: It is an outdoor fungus or mold and a facultative pathogen of
many plant species.
• Drechslera: An outdoor fungus whose species are often plant pathogens.
• Epicoccum: A saprophyte occurring both indoors and outdoors. It is essen-
tially a plant pathogen.
• Fusarium: A common saprophyte in the soil and a plant pathogen. Some
species produce mycotoxins in cereal crops that can affect human and ani-
mal health if they enter the food chain.
• Myrothecium: Soil fungus that can produce mycotoxins.
• Paecilomyces: It is a fungus occurring both indoors and outdoors and can
form mycotoxins.
• Penicillium: It is a common fungal genus. It is found both indoors and out-
doors. Some species can produce mycotoxins.

There are many other fungi that produce spores. Although they are in the outdoor
air, they can also be found indoors in moist environments. Fungal molds are often
found in water-­damaged homes (Fabian et al. 2005).
Pathogenic fungi and their environmental sources are shown in Table 8.4.
Candida spp., Aspergillus spp., and Cryptococcus neoformans are the most com-
mon pathogenic fungi. Candida spp. constitute the third to fourth most common
cause of bloodstream infections occurring in hospitals or infirmaries (Walsh et al.
2004). Rhodes (2006) stated that Aspergillus fumigatus is the leading mold patho-
gen among immunocompromised patients, especially those who have had bone mar-
row and solid organ transplantation. Cryptococcus neoformans is the most common
cause of fungal-­related mortality in patients with human immunodeficiency virus
(HIV) (Walsh et al. 2004). Walsh et al. indicate that Fusarium spp., Scedosporium
spp., Trichoderma spp., Zygomycetes, Penicillium marneffei, and Trichosporons
spp. are the most significant emerging fungi. Immunocompromised patients are
the most vulnerable. One important issue is the presence of bioaerosols in hospi-
tal rooms (McGinnis et al. 2009).
Bioaerosol infections in hospitals have been reported (Nobel and Clayton 1963;
Burge 2008; Mullins, Harvey, and Seaton 1976; Rodenhuis et al. 1984; Bodey and
Vartibvarian 1989; Arnow et al. 1978; Summerbell, Krajden, and Kane 1989; Burton
et al. 1972; Hopkins, Webber, and Rubin 1989). These and subsequent reports showed
that nosocomial infections or secondary infections may be acquired from hospitals
during treatment (Ekhaise, Ighosewe, and Ajakpori 2008). Ekhaise et al. reported
on the concentration of bioaerosols in various hospital departments. The bacterial
population ranged from 3.0 to 76 CFU/­m3. The highest levels were in the accident
and emergency ward. The fungal population ranged from 6.0 to 44.7 CFU/­m3. The
78 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 8.4
Some Pathogenic Fungi and Their Environmental Sources
Environmental
Fungus Disease Source Reference
Aspergillus spp. Allergic Soil, plant debris, Latgé 1999; Epstein 2011;
bronchopulmonary organic matter, Kwon-­Chung and Bennett
aspergillosis; compost air 1992
colonization; tissue
invasion; toxicosis
Candida spp. Candidiasis; Gastrointestinal tract; Dagnani, Solomkin, and
Candida albicans opportunistic mycosis; leaves, flowers, soil, Anaissie 2003; Epstein
bloodstream infection water 2011; www.doctorfungus.
org. 2006
Cryptococcus Cryptococcosis Soil contamination Viviani, Tortorano, and
neoformans from avian excreta; Ajello 2003; Epstein
pigeon droppings 2011; www.doctorfungus.
org. 2006
Fusarium spp. Plant pathogen; Soil; decaying Dagnani, Kiwan, and
Fusarium solani keratomycosis; vegetation; air Anaissie 2003; Epstein
mycetoma; 2011; www.doctorfungus.
onychomycosis; org. 2006
mycotoxicosis
Penicillium spp. Penicilliosis; Soil; decaying www.doctorfungus.org.
Penicillium pulmonary infection vegetation; air 2006; Kwon-­Chung and
marneffei Bennett 1992; Epstein
2011
Scedosporium spp. Sinusitis; brain abscess; Soil; polluted water; Epstein 2011; Kwon-­Chung
meningitis; fungus compost and Bennett 1992;
ball; endocarditis Dagnani, Kiwan, and
Anaissie 2003)
Trichoderma spp. Peritonitis; infections in Soil; plant material; www.doctorfungus.org.
immunocompromised common house 2006; Kwon-­Chung and
individuals mold; decaying Bennett 1992; www.
vegetation; wood doctorfungus.org. 2006;
Epstein 2011
Trichosporon Trichosponosis; Soil; water; birds; Kwon-­Chung and Bennett
infections mammals; mouth; 1992; www.doctorfungus.
skin; nails; org. 2006; Epstein 2011;
vegetables Maenza 2003
Zygomycetes Zygomycosis; Decaying vegetables; Dromer and McGinnis
mucormycosis; fruits; soil and 2003; Epstein 2011;
opportunistic infection animal excreta Kwon-­Chung and Bennett
1992
Bioaerosols 79

predominant organisms were Staphylococcus aureus, Staphylococcus epidermis,


Escherichia coli, Bacillus spp., and Proteus mirabilis. The fungal species were
Aspergillus spp., Penicillium spp., Mucor spp., Candida spp., and Verticillium spp.
(Ekhaise, Ighosewe, and Ajakpori 2008).
Rocha et al. (2012), in Venezuela, reported on bioaerosols in a general hospital.
They found that the nephrology surgery room, sterilization room, and neonatal room
had bacterial and fungal contamination. The densities of micro­organ­isms ranged
from 1 to 222 CFU/­m3. Bacterial contamination revealed 14 genera and 8 species
of micro­organ­isms. Staphylococcus was the most frequent bacteria. Aspergillus and
Penicillium spp. were the most common fungus species among 12 genera and 5 spe-
cies (Rocha et al. 2012). There have been numerous other references (Augustowska
and Dutkiewicz 2006; Nourmoradi et al. 2012; Roberts et al. 2006; Qudiesat et al.
2009). In an article, Fletcher et al. (n.d.) provided information on the importance of
bioaerosols in relation to hospital infections, their dispersal, potential micro­organ­isms
involved, methods of monitoring bioaerosols, and the control of nosocomial infec-
tions using ultraviolet (UV) germicidal irradiation.
There is considerable literature on the health effects of bioaerosols in the indoor
environment (Burge 1990; Verhoeff and Burge 1997; Epstein 1997). Mandal and
Brandl (2011) pointed out that the presence of human beings performing various
activities, such as walking, talking, coughing, sneezing, washing, and toilet flush-
ing, can release airborne biological particles into the air. Furthermore, plants, food
material, house dust, pets, textiles, carpets, wood material, and furniture stuffing can
occasionally release various fungal spores into the air (Mandal and Brandl 2011).
Following flooding, there can be a higher concentration of bioaerosols (Fabian
et al. 2005).
Bioaerosols are ubiquitous; consequently, in any indoor working environment
where there is moisture there may be the potential for molds, fungi, and other bio-
aerosols. Several industries have reported on the presence of bioaerosols, often caus-
ing illnesses in workers. Examples are agriculture, swine, or pig farming (Radon
et al. 2002; Masclaux et al. 2013; Basinas et al. 2013); livestock (Dungan 2010); and
greenhouses (Madsen et al. 2013). Bioaerosols are found in hospital environments as
well (Fletcher et al. 2006; Drew et al. 2006).
Bioaerosols from composting operations are of great concern. The composting
industry in the United States has increased considerably over the past few years due
to the ban on landfilling green material. In addition, there is an interest and activity
in composting food waste and biosolids (processed sewage sludge), the latter often
done in enclosed facilities to reduce the public’s exposure to bioaerosols. Workers
need to be protected. In the United Kingdom, compost production in 2000–2001
increased from 1 million tonnes to 3.4 million tonnes by 2005–2006 and is expected
to grow. The bioaerosols of interest include Aspergillus fumigatus, endotoxin, glu-
cans, thermophilic actinomycetes, and mycotoxins.

Aspergillus fumigatus
Aspergillus fumigatus occurs worldwide. It has the ability to degrade cellulose and
is found in high numbers (Swan et al. 2003, p. 543). It has been associated with the
80 Disposal and Management of Solid Waste: Pathogens and Diseases

outdoors (grass, hay, birds’ nests and bird droppings, cattle and horse manure, for-
est litter, wood chips) (Passman 1980) and indoors (refrigerators, bathroom walls,
basements, bedding, house dust). It is of greatest importance in composting and is
produced in abundance. It is heat tolerant, surviving composting temperatures, and
the spores are easily dispersed in the air and are very small so they can easily reach
the lung. It is one of the few fungi that can survive human temperatures.
Aspergillus fumigatus grows rapidly at temperatures between 30°C and 52°C and
as high as 55°C (Latgé 1999). The fungal spores typically range from 2 to 50 µm. A.
fumigatus is found in many environments other than composting, and its large pres-
ence has a low risk of allergic response for healthy individuals (Drew et al. 2009).
However, it is a fungus that can cause allergies and is an opportunistic pathogen
that can affect immunocompromised individuals (Swan et al. 2003). It is essential
in recycling carbon and nitrogen. It is estimated that all humans will inhale at least
several hundred A. fumigatus spores per day without harm (Swan et al. 2003). It can
also produce mycotoxins, which are low-molecular-weight toxic secondary metabo-
lites that can cause acute or chronic disease in vertebrate animals, with effects rang-
ing from neurotoxicity, to carcinogenicity, and to teratogenicity (Swan et al. 2003).
Although we inhale hundreds of spores daily, we are not infected with the organism.
Inhalation of conidia by immunocompromised and immunocompetent individuals
can have an adverse effect (Latgé 1999).

Endotoxin
An endotoxin is a lipopolysaccharide (LPS) that is part of the cell wall of Gram-­
negative bacteria. Rylander and Jacobs (1994) indicate that endotoxins are made
of complex LPS compounds that consist of polysaccharide chains connected by a
core oligosaccharide to a lipid part. Endotoxins are relatively heat stable. They are
released into the environment during cell growth and after the cell dies, when the
integrity of the cell wall is ruptured (Bradley 1979). They are present in the cavities
and intestinal tracts of humans and animals (Swan et al. 2003).
Endotoxin is toxic to humans and animals. Endotoxin can cause fever and short-­
term illness, with flu-­like symptoms, myalgia, and malaise. Inhaled endotoxins
increase the activity of macrophages, which leads to a series of inflammatory condi-
tions (Rylander 2002; Swan et al. 2003; Epstein 2011. Rylander (2002) indicates that
internalization of endotoxin in macrophages and endothelial cells results in local
production of inflammatory cytokines. The result is the migration of inflammatory
cells into the lung and the penetration of cytokines into the blood. These lead to
inflammation, toxic pneumonia, and systemic symptoms.
Endotoxins present in organic dust have been implicated in toxic pneumonia
and organic dust toxic syndrome (Rylander et al. 1989; Rylander and Jacobs 1994;
National Institute for Occupational Safety and Health [NIOSH] 2002). Chronic
exposure to endotoxin has been linked to work-­related symptoms, such as inflam-
mation leading to chronic bronchitis, chronic obstructive pulmonary disease, and
reduced lung function (Jacobs et al. 1997).
Bioaerosols 81

There have been studies of Dutch compost workers that reported excess acute and
subchronic nonimmune inflammation in the upper airways, presumably by exposure
to endotoxin (Douwes et al. 2003; Drew et al. 2009; Deacon et al. 2009). Endotoxin
was not detected in upwind samples but was consistently detected in on-­site samples.
Concentrations of endotoxin were consistently higher during composting activities
compared to periods of no activity. Downwind measurements showed a pattern of
peaks and troughs, suggesting complex dispersal dynamics. Quantities of endotoxin
measured on site were consistently below 50 EU/m3, which the Netherlands suggest
as a threshold level for occupational exposure. Cytokine release levels were minimal
at concentrations less than 50 EU/­m3 (Deacon 2009). There are no data indicating
carcinogenic, mutagenic, or reproductive effects from exposure to endotoxins.

Glucans
(1–3)β-­D-glucan is a polyglucose compound in the cell walls of fungi, some bacte-
ria, and plants. It is a potential inflammatory agent that induces nonspecific inflam-
matory reactions and may also be a respiratory immunomodulatory agent. It may
be involved in contributing to the inflammatory response, resulting in respiratory
symptoms and adverse lung function effects in response to inhalation of bioaerosols
(Swan et al. 2003). It has been found in green waste composting activities and has
been proposed as a nonspecific indicator of fungal exposure.
In a study in the Netherlands, an association was found between peak flow
variability and (1–3)β-­D-glucan levels and house dust among children (Douwes
et al. 2000).
Noncellulosic β-­ glucans are recognized as potent immunological activators.
Chen and Seviour (2007) report that they are used in China and Japan in clinics.
They further report that the literature suggests β-­glucans are effective in treating
cancer, a range of microbial infections, hypercholesterolemia, and diabetes and
appear to stimulate the immune system (Chen and Seviour 2007). Akramiene et al.
(2007) indicate that β-­glucans can prevent oncogenesis due to a protective effect
against potent genotoxic carcinogens. β-­Glucans act on several immune receptors,
including dectin-1, complement receptor (CR3), and TLR-2/6, and trigger a group of
immune cells, including macrophages, neutrophils, monocytes, natural killer cells,
and dendritic cells (Chan, Chan, and Sze 2009). Vetvicka and Vetvickova (2010)
tested 16 different glucans to evaluate whether individual glucans were similarly
active against each of the tested biological properties or if each glucan effected dif-
ferent reactions. No direct connection between sources and immunological activities
were found.

Actinomycetes
Actinomycetes are one of the most diverse groups of filamentous bacteria. They are a
subgroup of actinobacteria, which are Gram-­positive organisms. They include many
familiar and important bacteria, such as Mycobacterium, which causes tuberculosis
82 Disposal and Management of Solid Waste: Pathogens and Diseases

and leprosy. Another bacterium, Corynebacterium, can be found in the mucosa and
normal skin flora of humans. Streptomyces is a source of numerous antibiotics and
are the organisms producing the characteristics of freshly turned soil that are essen-
tial in the composting process (Burge 2008). Nocardia asteroids are actinomycetes
that are common in soil and can cause a respiratory infection.
Thermophilic actinomycetes are the most common cause of hypersensitive pneu-
monitis (e.g., farmer’s lung), which results from exposure to hay that has been colo-
nized with thermophilic actinomycetes. They are common in soil and water. The
odor associated with fresh soil is attributed to a volatile organic compound, geosmin,
produced by actinomycetes.
Actinomycetes are a major component of bioaerosols emitted during compost-
ing (Lacey and Dutkiewicz 1994; Taha et al. 2007). Several, such as Nocardia spp.,
Streptomyces spp., Thermoactinomyces vulgaris, Thermoactinomyces sacchari,
Thermomonospora curvata, and Thermomonospora spp. have been identified in
composting material (Lacey 1973; Palmisano and Barlaz 1996). Mesophilic acti-
nomycetes grow at temperatures of 20°C to 50°C, whereas thermophilic actinomy-
cetes thrive at 30°C to 60°C with short chains of spherical spores 0.7–1.3 µm in
diameter (Taha et al. 2007). Thermophilic actinomycetes such as Streptomyces spp.,
Thermomonospora spp., and Thermoactinomyces vulgaris can tolerate temperatures
in the range of 40°C to 50°C and are found even at 65°C. They prefer moist, highly
aerobic, and neutral or slightly alkaline pH conditions (Lacey 1973; Palmisano and
Barlaz 1996).
Actinomycetes offer the most promising synthesizers of many industrial and
commercially meaningful metabolites (Nawani et al. 2013).
Prolonged inhalation of these bioaerosols is linked to adverse health effects
(Douwes et al. 2003), including allergic alveolitis and other respiratory effects
(Millner 1982; Lacey and Crook 1988; (Lacey and Dutkiewicz 1994; Herr et al.
2003) in which inflammation of the lung is believed to be caused by glycopeptides
and protein allergens caused by spores (e.g., farmer’s lung disease) (Edwards 1972.).
Actinomycetes spores are more difficult to aerosolize than fungal spores because
of their smaller size (Reponen et al. 1997, 1998).

Mycotoxins
A mycotoxin is a toxic secondary metabolite produced by organisms of the fungi
kingdom, commonly known as molds. The term mycotoxin is usually reserved for
the toxic chemical products produced by fungi that readily colonize crops. One mold
species may produce many different mycotoxins, and the same mycotoxins may be
produced by several species (“Mycotoxins” n.d.).
Mycotoxins can appear in the food chain as a result of fungal infection of crops,
either by being eaten directly by humans or by use as livestock feed.
Mycotoxins greatly resist decomposition or being broken down in digestion, so
they remain in the food chain in meat and dairy products. Even temperature treat-
ments, such as cooking and freezing, do not destroy some mycotoxins.
Mycotoxins are small, approximately 0.1 μm. Toxic mold will produce mycotox-
ins, which are airborne and cause respiratory problems.
Bioaerosols 83

Stachybotrys (toxic black mold) is associated with poor air quality, resulting often
from water-­damaged conditions. Exposure to the mycotoxins present in Stachybotrys
chartarum or Stachybotrys atra can have a wide range of effects. Depending on the
length of exposure and volume of spores inhaled or ingested, symptoms can manifest
as chronic fatigue or headaches; fever; irritation to the eyes, mucous membranes of
the mouth, nose, and throat; sneezing; rashes; and chronic coughing. In severe cases
of exposure or cases exacerbated by allergic reaction, symptoms can be extreme,
including nausea, vomiting, and bleeding in the lungs and nose (“Stachybotrys”
n.d.). Recently, there has been heightened concern regarding exposure to a specific
type of mold commonly referred to as black or toxic mold. However, currently there
is no conclusive scientific evidence linking the inhalation of black mold spores or
any type of mold in the indoor environment to any illness other than allergy symp-
toms. The term toxic is inaccurate. Some indoor molds are capable of producing
extremely potent toxins (mycotoxins) that are lipid soluble and readily absorbed by
the intestinal lining, airways, and skin. These agents, usually contained in the fungal
spores, have toxic effects, ranging from short-­term irritation to immunosuppression
and cancer. Among the indoor mycotoxin-­producing species of molds are Fusarium,
Trichoderma, and, although less commonly isolated, Stachybotrys atra (also known
as S. chartarum, black mold). There is almost a complete lack of information on
specific human responses to well-­defined exposures to mold contaminants. There is
currently no proven method to measure the type or amount of mold to which a person
is exposed since common symptoms associated with mold exposure are nonspecific.
Molds are present everywhere in the environment, particularly where there is mois-
ture (e.g., under sinks), and responses to exposure vary greatly among individuals.
Molds often cause allergic symptoms. The concentration at which molds have an
impact on human health is unknown (Robbins et al. 2000).

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9 Pathogens in Animal
Waste and Manures

INTRODUCTION
In 2009, the Water Environment Federation published a book, Manure Pathogens,
edited by Dr. Dwight D. Bowman. This chapter updates the information presented in
that book (Bowman 2009). The pathways of sources and transmission of pathogens
from animals to humans are shown in Figure 9.1. If manure is not treated to destroy
pathogens, then they can survive in the environment for a long time. Table 9.1 illus-
trates the survival times of several pathogens in the environment.
More than 85% of the world’s fecal wastes are from domestic animals, such as
poultry, cattle, sheep, and pigs. These animals harbor zoonotic pathogens. Diseases
passed from animals to humans are called zoonoses. These pathogens can enter
the environment and infect humans. Primarily, this environmental contamination
is through runoff. However, as indicated previously in this book, unless the wastes
are incorporated into the ground, there could be leaching and movement to drinking
water resources. Little information exists on health effects associated with exposure
to this potential hazard to human health.
Olson (2001) reported that six prevalent enteric pathogens were found in cattle,
pigs, and poultry (Table 9.2). Thus, manures from these animals could harbor these
organisms and, if in contact with humans, cause serious illnesses.
One of the major criteria for potential infection to humans from pathogens is their
infective dose. This refers to the number of pathogens required to infect a host or the
number of organisms required to cause a disease. With humans, this is highly vari-
able. Factors such as age, individual immune conditions, route of infection, and route
of transmission (inhalation, dermal absorption, ingestion) are some of the important
ones. The US Food and Drug Administration, in their Bad Bug Book (2013), indicates
that the infective dose values should be viewed with caution for the following reasons:

• Often, they are extrapolated from epidemiological investigations.


• They were obtained by human feeding studies of healthy, young adult volunteers.
• They are best estimates based on a limited database from outbreaks.
• They are worst-­case estimates.
• There are several variables that cannot be directly used to assess risks.

The following are some of the variables:


Variables with regard to micro­organ­isms:
• Variability of gene expression of multiple pathogenic mechanisms
• Potential for damage or stress of the micro­organ­ism

87
88 Disposal and Management of Solid Waste: Pathogens and Diseases

Land Application
Manure Bioaerosols
Crops

Treatment
Direct
Composting Animals
Contact
Lime Stabilization

Wastewater Runoff
Biosolids Treatment Water–Ground
Surface

FIGURE 9.1  Pathways of sources and transmission of pathogens from animals to humans.

TABLE 9.1
Survival of Several Animal Pathogens in the Environment
Pathogens Soil Cattle Manure Grass
Listeria 2 weeks to 4 years 128 days
Escherichia coli 1 month to 1 year 10 days to 3 months 99 days
Cryptosporidium 1 month to 1 year 4 weeks to 1 year 30 days
Salmonella 2 weeks to 1 month 4 weeks to 6 months 63 days
Campylobacter 1 month 1week to 8 weeks

Source: Wisconsin—Farm Safety Fact Sheet, University of Wisconsin, Madison.

TABLE 9.2
Prevalent Enteric Pathogens
Pathogen Cattle (%) Pigs (%) Poultry (%)
Salmonella spp.  0–13  0–38  10–100
Escherichia coli 0157:H7 16  0.4   1.3
Campylobacter jejuni  1  2 100
Yersinia enterocolitica <1 18   0
Giardia lamblia 10–100  1–20   0
Cryptosporidium spp.  1–100  0–10   0
Pathogens in Animal Waste and Manures 89

• Interaction of organism with food solvent and environment


• The organism’s susceptibility to pH
• The organism’s immunological uniqueness
• Interactions with other organisms
Variables with regard to the host:
• Age
• General health
• Pregnancy
• Medication: over the counter or prescription
• Metabolic disorders
• Alcoholism, cirrhosis (progressive disease of the liver), hemochromato-
sis (a disease of older men with excessive iron intake)
• Malignancy
• Amount of food consumed
• Gastric acidity variation
• Genetic disturbances
• Nutritional status
• Immune competence
• Surgical history
• Occupation

The following are some infective dose data:

• Shigella and Giardia: approximately 10 cells to start an infection (Leggett,


Cornwallis, and West 2012)
• Vibrio cholera and Staphylococcus: 103 to 108 cells to start an infection
(Leggett, Cornwallis, and West 2012)
• Salmonella and strains of Escherichia coli: 105 or more organisms (Kothary
and Babu 2001)
• Toxigenic Vibrio cholerae (01 and 0139 serotypes): 104 organisms (Kothary
and Babu 2001)
• Cryptosporidium jejuni: Infective dose as low as 500 organisms (Kothary
and Babu 2001)
• Cryptosporidium parvum: 10 oocysts (Kothary and Babu 2001)
• Entamoeba coli: One cyst (Kothary and Babu 2001)
• Escherichia coli: Approximately 10 cells (Schmid-­Hempel and Frank 2007)
• Variola (smallpox virus): One virus particle (Nicas et al. 2004)

PATHOGENS AND DISEASES TRANSMITTED TO HUMANS


The pathogens transmitted from animals to humans can be bacteria, viruses, and
parasites. More than 150 pathogens can cause zoonotic infections (Jensen 2011).
Some of the most important ones are discussed next.
90 Disposal and Management of Solid Waste: Pathogens and Diseases

Bacteria
• Escherichia coli: Pathogenic strains cause enteritis, peritonitis, or cystitis.
• Salmonella spp.: Some species are pathogenic in animals and humans.
They can cause food poisoning.
• Leptospira spp.: These bacteria can cause leptospirosis, a fever that is the
world’s most common disease transmitted to people from animals. The
infection is commonly transmitted to humans by allowing water that has
been contaminated by animal urine to come in contact with unhealed
breaks in the skin, the eyes, or the mucous membranes.
• Aeromonas: Some species are pathogenic. Two major diseases associ-
ated with Aeromonas are gastroenteritis and wound infections, with or
without bacteremia.
• Listeria monocytogenes: One species can cause meningitis; encephalitis;
septicemia; endocarditis; abortion; abscesses; and lesions. It is often fatal.
• Yersinia enterocolitica: Contamination from feces occurs. Symptoms may
include watery or bloody diarrhea and fever.
• Vibrio spp.: Vibrio cholerae is the cause of cholera; Vibrio sputorum causes
diseases of the mouth.
• Campylobacter spp.: These species can result in campylobacteriosis, a
common cause of food poisoning.
• Hydrophilia (pathogenic strains): Aeromonas hydrophila can cause
gastroenteritis.

Viruses
• Hepatitis E (swine): This has resemblance to the human hepatitis E virus
and its ability to infect nonhuman primates.
• Rotaviruses: Rotavirus is a virus that causes gastroenteritis (inflammation
of the stomach and intestines). It can cause diarrhea, vomiting, fever, and
abdominal pain. Rotavirus is the most common cause of severe gastroen-
teritis in infants and young children.
• Adenoviruses: These are associated with respiratory infections of children,
conjunctivitis, and pneumonia.
• Caliciviruses (certain strains): Influenza viruses (orthomyxoviruses),
Norwalk virus, and other caliciviruses produce infections that cause acute
diarrhea and vomiting (gastroenteritis), abdominal cramps, myalgia, mal-
aise, headache, nausea, and low-­grade fever.

Parasites (Protozoans)
• Cryptosporidium parvum: This is one of several protozoa species that cause
cryptosporidiosis, a parasitic disease of the human intestinal tract.
Pathogens in Animal Waste and Manures 91

• Giardia lamblia: This is a parasite of the small intestinal tract. It inter-


feres with the absorption of fats and produces flatulence, steatorrhea, and
acute discomfort.
• Balantidium coli: A parasitic ciliate, it is a cause of colitis similar to ame-
bic dysentery.

It has been reported that potentially harmful pathogens, including verocytoxi-


genic Escherichia coli (VTEC) are shed in animal manures, and there is growing
concern in many countries about the number of sporadic and outbreak cases of
VTEC attributable to direct contact with fecal material either as a result of handling
contaminated soil in fields or ingestion of produce grown in contaminated manures
or slurries. VTEC has been detected in the feces of ruminant and nonruminant
farmed animals, wild animals, domestic pets, and birds. This pathogen appears to be
well adapted to survive in animal wastes and can persist for extended periods, rang-
ing from several weeks to many months. Because of this persistence, these animal
manure materials are important as potential vehicles for transmission within farm
animals, fresh food, and the wider environment.
The application of raw manure to crops to be eaten raw needs to be avoided.
Several treatments are available to disinfect manure. The most economical ones
for farmers or other producers of manure are composting and lime stabilization.
Depending on location (i.e., with respect to residences or others affected by odors
or noise), composting may be done in an enclosed facility or outdoors. The com-
mon composting methods are windrowing, passive aeration, or aerated static piles.
Windrow composting is typically conducted outdoors and unless using fabric covers
can result in severe odors (see Figure 9.1).
Passive aeration is the least expensive, but there is little experience and confirma-
tion regarding pathogen disinfection. The aerated static pile, originally developed by
the US Department of Agriculture, has been primarily used with sewage sludge or
biosolids. The data on disinfection is extensive and well documented.
In the past, farmers piled manure for several months or years, and since there
is a relationship between length of time and disinfection, considerable die-­off of
pathogens occurred. However, this process required considerable space and often
offended nearby residences. Unlike municipalities that have considerable resources,
farmers have limited finances.
The survival of several pathogens found in animal fecal wastes are shown in
Table 9.3. In water, the optimum temperature was 5°C for all the organisms reported.
In the soil, cold temperatures also enhanced survival. The surprise was the survival
time for the compost. Apparently, this compost did not reach 55°C, as required by
both Canadian and US regulations for sewage sludge or biosolids. As expected, sur-
vival was low on dry surfaces. It was not specified if the dry surfaces were in the
winter or summer.
92

TABLE 9.3
Survival of Pathogens Found in Animal Fecal Wastes
Duration of Survival
Yersinia Escherichia coli
Material Temperature Giardia Cryptosporidium Salmonella Campylobacter enterolitica O157:H7
Water Frozen >1 day >1 year >6 months 2–8 weeks >1 year >300 days
5°C 11 weeks >1 year >6 months 12 days >1 year >300 days
30°C 2 weeks 10 weeks >6 months 4 days 10 days 84 days
Soil Frozen <1 day >1 year >12 weeks 2–8 weeks >1 year >300 days
5°C 7 weeks 8 weeks 12–28 weeks 2 weeks >1 year 100 days
30°C 2 weeks 4 weeks 4 weeks 1 week 10 days 2 days
Cattle feces Frozen <1 day >1 year >6 months 2–8 weeks >1 year >100 days
5°C 1 week 8 week 12–28 weeks 1–3 weeks 30–100 days >100 days
30°C 1 week 4 week 4 weeks 1 week 10–30 days 10 days
Slurry 1 year >1 year 13–75 days >112 days 12–28 days 10–100 days
Compost 2 week 4 week 7–14 days 7 days 7 days 7 days
Dry surfaces 1 day 1 day 1–7 days 1 day 1 day 1 day

Source: Olson ME. 2001. Human and animal pathogens in manure. Paper presented at Livestock Options for the Future, National Conference,
Winnipeg, Canada. June 2001.
Disposal and Management of Solid Waste: Pathogens and Diseases
Pathogens in Animal Waste and Manures 93

The Ontario Ministry of Agriculture and Food stated:


Using proper composting procedures can drastically reduce the number of pathogens
in manure. One of the parameters identified in many composting procedures is to
maintain temperature above 55°C for at least 3 days when using aerated or in-­vessel
systems. In windrow systems, the core of the windrow may reach these temperatures,
but surface zones and near the base of the windrow will have lower temperatures.
Turning or mixing the windrow will introduce oxygen to the windrow and quickly
increase temperatures in the earlier stages of composting. Turning with equipment that
moves material from the surface to the core of the windrow will expose more materi-
als to higher temperatures. Repeated turnings are necessary to ensure all materials are
exposed to at least 3 consecutive days of high temperature.
It is generally recommended that windrows maintain a core temperature of 55°C
for 15 days with at least 5 turnings. Due to the need for proper mixing and consistent
high temperatures, pathogen reduction in windrow composting has sometimes been
found to be less consistent than when using well-­managed, aerated static pile or in-­
vessel systems.
Some organisms are more difficult to kill than others and temperatures must be
regularly monitored to ensure that appropriate temperatures are maintained. Proper
moisture levels (50%–60%), optimum C:N ratios (25:1–30:1) and appropriate aeration
or turnings are all factors to ensure the conditions are optimum to reach and maintain
the necessary temperatures. Records should be kept for temperatures, compost condi-
tions, C:N ratio, moisture, and the date/­time of turnings. (Martin 2005)

Campylobacter was found to survive at temperatures of raw and cooked poultry


samples, although its optimum temperature ranged between 37°C and 42°C. A study
by Haddad et al. (2009) found that long-­term survival of Campylobacter jejuni at low
temperatures is dependent on polynucleotide phosphorylase activity. It is therefore
possible that other pathogens can have characteristics that allow them to survive
under nonoptimal conditions in the environment.
In a review, Guan and Holley (2003) indicated that survival of pathogens in soil,
manure, and water indicated significant variability in resistance to environmental
challenges. Generally, pathogens survive longer in the environment at cooler temper-
atures, but differences were reported for both liquids and solid manure. Temperatures
ranging from 25°C to 90°C destroyed pathogens.
In the developed countries, the major concern is contamination of the water sup-
plies. Effective low-­cost treatment such as composting would significantly destroy
animal pathogens. Incorporating animal waste to a depth of at least 6 inches (plow
zone) will greatly reduce contamination by runoff.
In developing countries, especially in small villages, animal waste could be com-
posted or, if untreated, should not be used to grow food chain crops. These crops
could be nuts, cotton, fruit trees, and others. If it is needed or desired to use untreated
animal manures on food chain crops, it would be best to apply them to fields that
would not be used for weeks or even a year.

SUMMARY
Manure Pathogens (Bowman 2009) is an excellent book on the subject of animal
manures. Animal wastes can harbor pathogens that can harm humans and cause
94 Disposal and Management of Solid Waste: Pathogens and Diseases

diseases and illnesses. Diseases passed from animals to humans are called zoono-
ses. More than 85% of the world’s fecal wastes are from domestic animals, such as
poultry, cattle, sheep, and pigs.
The largest waterborne disease outbreak in US history occurred in 1993 in
Milwaukee, Wisconsin, when over 400,000 people became ill with diarrhea when the
parasite Cryptosporidium was found in the city’s drinking water supply (Brunkard
et al. 2011). This was thought to be the result of manure shed by cattle that resulted
in runoff that contaminated the water supply. Another incident attributed to animal
waste contamination occurred on May 11, 2000, when many people of a community of
about 5,000 people began to simultaneously experience bloody diarrhea, gastrointesti-
nal infections, and other symptoms of E. coli O157:H7 and Cryptosporidium infection.
Two thousand persons became ill, and seven died (Holme, 2003; Clark et al. 2003).
The survival time of pathogens in animal wastes can extend for a year of more
depending on the temperature of the waste, the type of waste, and the organism. The
pathogens transmitted from animals to humans can be bacteria, viruses, and parasites.
More than 150 pathogens can cause zoonotic infections. Treatments that raise the
temperature of the waste to over 55°C are effective in destroying animal pathogens.

REFERENCES
Bowman DD. 2009. Manure Pathogens. Alexandria, VA: WEF Press.
Brunkard JM, Ailes E, Roberts VA, Hill V, Hilborn ED, Craun GF, Rajasingham A, Kahler A,
Garrison L, Hicks L, Carpenter J, Wade TJ, Beach MJ, and Yoder JS. 2011. Surveillance
for Waterborne Disease Outbreaks Associated with Drinking Water—United States,
2007–2008. Atlanta, GA: CDC.
Clark CG, Rafiq Ahmed LP, Woodward DL, Melito PL, Rodgers FG, Jamieson F,
Ciebin B, Li A, and Ellis A. 2003. Characterization of waterborne outbreak–­associated
Campylobacter jejuni, Walkerton, Ontario. Emerg Infect Dis 9: 1232–1241.
Guan TY and Holley RA. 2003. Pathogen survival in swine manure environments and trans-
mission of human enteric illnesses—a review. J Environ Qual 32: 383–392.
Haddad N, Burns CM, Bolla JM, Pre’vost H, Fe’de’right M, Drider D, and Cappelier JM.
2009. Long-­term survival of Campylobacter jejuni at low temperatures is dependent on
polynucleotide phosphorylase activity. Appl Env Microbiol 75: 7310–7318.
Holme R. 2003. Drinking water contamination in Walkerton, Ontario: positive identification.
Water Sci Technol 47: 1–6.
Jensen J. 2011. Foodborne Disease in the United States. http://vbs.psu.edu/extension/
resources/pdf/presentations/pathogens.pdf
Kothary MH and Babu US. 2001. Infective dose of foodborne pathogens in volunteers: a
review. J Food Safety 21: 149–268.
Leggett HC, Cornwallis CK, and West SA. 2012. Mechanisms of pathogenesis, infective dose
and virulence in human parasites. PLoS Pathog 8(2): e1002512. doi:10.1371/journal.
ppat.1002512
Martin H. 2005. Agricultural Composting Basics. http://www.omafra.gov.ca/english/engineer/
facts/05-021.pdf
Nicas M, Hubbard AE, Jones RM, and Reingold AL. 2004. The infectious dose of Variola
(small pox) virus. Appl Biosafety 9: 118–127.
Olson ME. 2001. Human and animal pathogens in manure. Paper presented at Livestock
Options for the Future, National Conference, Winnipeg, Canada. June 2001.
Pathogens in Animal Waste and Manures 95

Schmid-­Hempel P and Frank SA. 2007. Pathogenesis, virulence and infective dose. PLoS
Pathog 3: e147.
US Food and Drug Administration. 2013. Bad Bug Book. Handbook of Foodborne Microorganisms
and Natural Toxins. 2nd ed. http://www.fda.gov/food/foodborneillnesscontaminants/
causesofillnessbadbugbook/default.htm
Wisconsin Farm Safety Fact Sheet. Madison, WI: University of Wisconsin.
10 Pathogens in Food
and Water

INTRODUCTION
This chapter includes both foodborne and waterborne pathogens together because
of their relationship. These two need to be managed together to be effective in con-
trolling diseases and human exposure. Food produced can be exposed to pathogens
through the soil, water, and air. The soil can harbor pathogens, which can be trans-
mitted to roots and to plants. Some of these pathogens are introduced to the soil
through the application of manure, contaminated water, or aerosols.
Water is a key ingredient of foodstuffs, and contamination can occur from vari-
ous sources. Irrigated contaminated water resulting from both domestic and wildlife
excreta can contaminate crops. The World Health Organization (WHO) indicates
that human exposure to pathogens from food and water as a result of wastewater
reuse in the irrigation of vegetables and fruits resulted in disease outbreaks (WHO
2003). WHO suggests that the use of a common approach for characterization of
microbial hazards in food and water will result in greater understanding, which can
effectively reduce disease risk and improve public health.
Education and hygiene can significantly result in reducing foodborne and water-
borne diseases. This primarily will be effective in developed countries. The popula-
tion of developed countries tends to have a higher degree of education. Both parents
and children are taught the importance of washing hands after using the toilet and
prior to eating. Unfortunately, this is not the case in developing countries.
In developing countries, access to infrastructure, flush toilets, clean water, and
other sources related to hygiene are not available. The lack of availability of these
facilities can result in fecal-­to-­oral contamination.
There are numerous factors that affect the potential for a pathogen to cause a
disease (WHO, 2003). These can include

• The pathogen’s properties and characteristics (e.g., ability to survive and


multiply in food and water)
• The pathogen’s phenotypic and genetic characteristics
• Host specificity: tolerance is generally lower for the young and elderly
• Infection mode
• Antimicrobial resistance
• Environmental conditions: heat, drought

A pathogen’s properties and characteristics have been discussed in other chap-


ters. Survival and persistence rates vary with the organism and type of waste and
its treatment.

97
98 Disposal and Management of Solid Waste: Pathogens and Diseases

Host-­related factors are important and can influence the likelihood of infection.
These can affect the probability and severity of disease (WHO 2003). These can
include

• Age: Children and the elderly are more susceptible and may have greater
difficulty fighting diseases.
• The general health of the individual: In many cases, this can be related to
nutrition and the availability of medical care and its implementation.
• The immune status of the individual: Today, in developed countries, immu-
nization can be significant.
• Exposure.
• Nutritional status.
• Demographic conditions: Poverty, social, cultural, and religious impacts.

An antimicrobial is defined as an agent or agents that kill organisms or inhibit


their growth. These agents could be natural or man-­made. Natural antimicrobial
agents found in soil and compost inhibit waste-­related pathogens. One organism well
known for resistance to antibiotics is methicillin-­resistant Staphylococcus aureus
(MRSA) bacteria. There is evidence of a connection of antimicrobial-­resistant human
infections to foodborne pathogens of animal origin (Swartz 2002). Salmonella,
Campylobacter, and Escherichia coli O157:H7 have been shown to be antimicrobial
resistant (Swartz 2002).
Climate change and other environmental conditions, such as surface heat, ultra-
violet light, or dryness, can effectively reduce or eliminate pathogens. These condi-
tions can be significant in destroying pathogens in agriculture and food production.

FOODBORNE DISEASES
The foodborne diseases listed under this topic are the most common in the United
States and developing countries. Foodborne diseases usually manifest in gastrointes-
tinal problems such as diarrhea and vomiting with the potential for fever. Symptoms
could be caused by toxins as a result of the growth of the pathogen in foods or
by gastrointestinal infection (Bates, Hoffman, and Morris 2011). According to the
University of Florida, symptoms from preformed toxins can generally have a fairly
rapid onset. Often, the effect does not show up for several hours, or it takes a day or
two for symptoms to appear. Diseases caused by bacteria and viruses tend to show
up more rapidly, whereas those as a result of protozoa are slower.
Some of the more common foodborne pathogens, according to the Iowa State
University Food Safety Project, the US Food and Drug Administration (FDA) (2014),
and Epstein (2011), are the following:

• Bacillus cereus: It is responsible for a minority of foodborne illnesses


(2%–5%), causing severe nausea, abdominal discomfort, vomiting, and
diarrhea. Bacillus foodborne illnesses occur due to survival of the bacterial
endospores when food is improperly cooked.
Pathogens in Food and Water 99

• Campylobacter jejuni: This bacterium is the most common cause of diar-


rhea in the United States. The highest rate is found in children under the
age of 1 year. Unborn babies and infants are more susceptible on exposure
to this organism. The sources are raw milk; contaminated water; raw and
undercooked meat, poultry, or shellfish; and eggs. The incubation period
is generally 2 to 5 days after eating contaminated food and lasts for 7 to
10 days.
• Clostridium botulinum: This bacterium produces a toxin that causes bot-
ulism, resulting in muscular paralysis. Honey can contain Clostridium
botulinum spores. Sources can be home-­canned products, meat and sea-
food products, and herbal cooking oils. The symptoms are dry mouth, dou-
ble vision, muscular paralysis, respiratory failure, nausea, vomiting, and
diarrhea. Botulism can be fatal and requires immediate medical attention.
The incubation period is usually from 4 to 36 hours after eating contami-
nated food. The recovery period can extend from a week to a full year.
Cooking food properly is imperative.
• Clostridium perfringens: This produces heat-­stable spores that prevail in
undercooked foods and foods left unrefrigerated and at room temperature.
The sources are meat and meat products. The symptoms are abdominal
pain and diarrhea with occasional vomiting and nausea.
• Cryptosporidium parvum: This protozoan causes illness from contami-
nated water, fecal-­to-­oral contamination, and raw and undercooked foods.
Sources of contamination are water, milk, contaminated food, and person-­
to-­person transmission. The incubation period is usually 2 to 10  days.
Symptoms consist of diarrhea, gastrointestinal cramps, and loss of appetite.
Prevention can be achieved with good hygiene and boiling potentially con-
taminated water.
• Pathogenic Escherichia coli, O157:H7: Deadly toxins can be produced. The
symptoms are hemorrhagic colitis. Sources are raw or undercooked meat,
raw milk, unpasteurized juice, and contaminated water. The symptoms are
severe cramps, hemorrhagic colitis, and bloody or nonbloody diarrhea. The
incubation period is usually 3 to 4 days and may last from 5 to 8 days.
• Listeria monocytogenes: Illness or death in pregnant women, fetuses, and
newborns may occur. The sources are meat, seafood, poultry, and unpas-
teurized dairy or dairy products. The symptoms are fever, muscle aches,
headaches, nausea, vomiting, diarrhea, meningitis, and miscarriages. The
incubation period can be from as little as 2 days to 3 weeks. Sanitary and
hygiene practices are important.
• Giardia lamblia: This is a protozoan parasite. The disease is termed giardi-
asis. The symptoms are watery stool, diarrhea, stomach cramps, and lactose
intolerance. The protozoan is found in soil water and foods that have been
contaminated with the feces of animals or infected humans. Good hygiene
and sanitization are preventive measures.
• Norovirus (Norwalk, Norwalk-­like): This virus can cause nausea, vomit-
ing, diarrhea, fever, and abdominal cramps. The sources are shellfish, oys-
ters, salads, frosting, and person-­to-­person contamination. The incubation
100 Disposal and Management of Solid Waste: Pathogens and Diseases

period is usually 24 to 48 hours but can occur as early as 12 hours and can
last for 12 to 60 hours.
• Salmonella serotype Enteritidis: This Salmonella causes salmonellosis.
Contamination can be from eggs, poultry, meat, or milk products. The
symptoms can be diarrhea, fever, vomiting, nausea, and abdominal cramps.
The incubation period is usually 12 to 72 hours after ingesting contami-
nated food and can last for 4 to 7 days.
• Shigella: Shigella is a bacterium that results from poor hygiene, water
contaminated by human feces, and unsanitary food handling. It can cause
dysentery. The sources can be salads, raw vegetables, dairy products,
raw oysters, ground beef, and poultry. The incubation period is 12 to
60 hours, but often is as long as 7 days. The duration of illness is usually
5 to 7 days.
• Staphylococcus aureus: The bacterium is found on the skin and in nasal pas-
sages. As a result of poor hygiene and sanitation, it can be transferred from
person to person. Sources can be dairy products, raw meats, poultry, and
humans. Following surgical operations, it has caused infection. The symp-
toms are abdominal cramps, nausea, vomiting, and diarrhea. Symptoms
can appear within 30 minutes to 8 hours after ingesting contaminated food.
The duration of infection is usually 24 to 48 hours.
• Vibrio cholerae: The bacterium is found in estuary environments. It can
result in death. The primary sources are raw and undercooked seafood as
well as contaminated water and food. Potential symptoms are diarrhea,
vomiting, and leg cramps. The incubation period can occur from 5 to 6 days
following intake of contaminated food. The duration is usually 7 days.
• Vibrio parahaemolyticus: This bacterium resides in saltwater and can
cause gastroenteritis. The sources can be raw or undercooked fish or shell-
fish. The symptoms can be fever, nausea, vomiting, headache, chills, and
stomach cramps. The incubation period can last from 4 to 96 hours and can
last for 2.5 days following consumption of contaminated food.
• Vibrio vulnificus: This also inhabits saltwater. It can enter through an
exposed wound. The sources are raw fish and shellfish, especially oysters.
The symptoms can manifest in diarrhea, nausea, gastrointestinal pain,
fever, vomiting, chills, and in some cases sores or blisters on a person’s legs.
The incubation period is usually 16 hours after ingesting contaminated food
or exposure to contaminated water. The infection may last from 2 to 3 days.
• Yersinia enterocolitica: It is the cause of the disease yersiniosis. It can
mimic acute appendicitis. The primary sources are raw meat and seafood,
dairy and dairy products, as well as contaminated water. The predominant
symptoms are vomiting, fever, diarrhea, and stomach pain. The symptoms
can be severe in children. Symptoms may appear in 1 to 2 days after inges-
tion and last from 1 to 2 days.

Table  10.1 provides data on reported and estimated illnesses, hospitalization


rates, and case fatality rates for known foodborne bacterial pathogens in the United
Pathogens in Food and Water 101

TABLE 10.1
Reported and Estimated Illnesses, Hospitalization Rates,
and Case Fatality Rates for Known Foodborne Bacterial
Pathogens in the United States
Estimated Hospitalization Case Fatality
Pathogen Total Cases Rate Rate

Bacterial
Bacillus cereus 27,360 0.006 0.0000
Botulism 58 0.800 0.0769
Brucella spp. 1,554 0.550 0.0500
Campylobacter spp. 2,453,926 0.102 0.0010
Salmonella, nontypical 1,412,498 0.221 0.0078
Escherichia coli
 O157:H7 73,480 0.295 0.0083
 Non-­O157:H7 STEC 36,740 0.295 0.0083
 Enterotoxigenic 79,420 0.005 0.0001
  Other diarrheagenic 79,420 0.005 0.0001
Listeria monocytogenes 2,518 0.922 0.2000
Salmonella typhi 824 0.750 0.0040
Shigella spp. 448,240 0.139 0.0016
Staphylococcus
  Food poisoning 185,060 0.180 0.0002
 Foodborne 50,920 0.130 0.0000
Vibrio cholerae 54 0.340 0.0060
Vibrio vulnificus 94 0.910 0.3900
Vibrio, other 7,880 0.126 0.0250
Yersinia enterocolitica 96,368 0.242 0.0005
Clostridium perfringens 248,520 0.242 0.0005
Brucella species 1,554 0.550 0.0500
 Subtotal 5,204,934

Parasitic
Cryptosporidium parvum 300,000 0.150 0.0050
Cyclospora cayetanensis 16,264 0.020 0.0005
Giardia lamblia 2,000,000 Not available Not available
Toxoplasma gondii 225,000 Not available Not available
Trichinella spiralis 52 0.081 0.0030
 Subtotal 2,541,316

Viral
Norwalk-­like virus 23,000,000 Not available Not available
Rotavirus 3,900,000 Not available Not available

(Continued)
102 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 10.1 (Continued)
Reported and Estimated Illnesses, Hospitalization Rates,
and Case Fatality Rates for Known Foodborne Bacterial
Pathogens in the United States
Estimated Hospitalization Case Fatality
Pathogen Total Cases Rate Rate
Astrovirus 3,900,000 Not available Not available
Hepatitis A 83,391 0.130 0.0030
 Subtotal 30,883,391
   Total 38,629,641

Source: Data from Centers for Disease Control and Prevention (CDC). 1999.
CDC’s Emerging Infections Programs—1999 Surveillance Results.
Atlanta, GA: Centers for Disease Control and Prevention; Mead PS,
Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro G, Griffin PM,
and Tauxe RV. 1999. Food-­related illnesses and death in the United
States. Emerg Infect Dis 5(5): 607–625.

States. It was estimated that foodborne diseases caused approximately 76 million


illnesses, 325,000 hospitalizations, and 5,000 deaths in the United States each year
(Mead et al. 1999).
The Centers for Disease Control and Prevention (CDC) indicate that some portion
of gastrointestinal illnesses is caused by foodborne agents not yet identified (Mead
et al. 1999). Deaths are also unreported. And, Mead et al. (1999) indicated that food-­
related death information is especially difficult to obtain because pathogen-­specific
surveillance systems rarely collect information on illness outcome.
Table 10.2 provides data on cases and incidence rates of foodborne diseases each
year in the United States (Swartz 2002.). Obviously, there are many more cases
throughout the United States. Furthermore, many cases are not reported by doctors.
Note that the source of data was the CDC (1999). Surveillance occurred in eight
states (Connecticut, Georgia, Minnesota, and Oregon and selected counties in the
states of California, Maryland, New York, and Tennessee) through more than 300
clinical laboratories. The total population assessed was 25.6 million.
Table 10.3 provides data on the percentage of people hospitalized in the United
States as a result of foodborne pathogens (CDC 1999). The data were obtained from
the National Ambulatory Medical Care Survey (McCaig and Burt 1999).
The CDC (2011) indicated that foodborne illness can be prevented.
In subsequent data, the CDC indicated that there were two major groups of food-
borne illnesses. There were 31 known pathogens and several unspecified agents. The
31 known foodborne pathogens caused an estimated annual 9.4 million illnesses
(6.6–12.7 million), resulting in 1,351 (712–2,268) deaths. The unspecified number
of agents resulted in 38.4 (19.8–61.2) million estimated annual illnesses (Centers for
Disease Control and Prevention (CDC) 2011).
Pathogens in Food and Water 103

TABLE 10.2
Cases and Incidence Rates of Foodborne
Diseases Each Year in the United States
Incidence Rate
Pathogen Cases per 100,000

Bacteria
Salmonella 4,533 17.7
Campylobacter 3,794 14.8
Shigella 1,031 4.0
Escherichia coli O157:H7 530 2.0
Yersinia 163 0.6
Listeria 113 0.5
Vibrio 45 0.2
 Total 10,209

Parasites
Cryptosporidium 474 1.5
Cyclospora 14 0.04
 Total 488

Source: Swartz MM. 2002. Human diseases caused by


foodborne pathogens of animal origin. Clin
Infect Dis 34(Suppl 3): S111–S122.

TABLE 10.3
Percentage of People Hospitalized Each Year
in the United States as a Result of Infections
from Foodborne Pathogens
Percentage Percentage Hospitalized
Listeria 88
Escherichia coli O157:H7 37
Yersinia 36
Vibrio 25
Salmonella 22
Shigella 14
Campylobacter 11

Source: Centers for Disease Control and Prevention (CDC).


1999. CDC’s Emerging Infections Programs—1999
Surveillance Results. Atlanta, GA: Centers for
Disease Control and Prevention.
104 Disposal and Management of Solid Waste: Pathogens and Diseases

The top five pathogens causing the most illness annually were

• Norovirus: 5,461,731 illnesses (range 3,227,078–8,309,480)


• Salmonella (nontyphoidal): 1,027,561 (range 644,786–1,679,667)
• Clostridium perfringens: 965,958 (range 192,316–2,483,309)
• Campylobacter spp.: 845,024 (range 337,031–1,611,083)
• Staphylococcus aureus: 241,148 (range 72,341–529,417)

The top five pathogens contributing acquired foodborne illnesses resulting in esti-
mated deaths were

• Salmonella (nontyphoidal): 378 estimated deaths


• Toxoplasma gondii: 327 estimated deaths
• Listeria monocytogenes: 255
• Norovirus: 149
• Campylobacter: 76

These numbers above estimated 88% of the deaths as a result of foodborne illnesses.
Thomas et al. (2013) reported on the estimates of foodborne illnesses in Canada
for 30 specified pathogens and unspecified agents based on data from 2000 to
2010 using a population census of 2006. It was estimated that each year there were
1.6 million (1.2–2.0 million) illnesses related to 30 known pathogens and 2.4 million
(1.8–3.0 million) related to unspecified agents. The leading pathogens accounting for
90% of the illnesses were Norovirus, Clostridium perfringens, Campylobacter spp.,
and nontyphoidal Salmonella spp. These accounted for 90% of the pathogen-­specific
foodborne illnesses. At that time, approximately 1 in 8 Canadians experienced an
episode of domestically acquired foodborne illness each year in Canada (Thomas
et al. 2013).
In developing countries, the situation is more acute. In addition to the cited organ-
isms in the United States and Canada, Vibrio cholerae is a major public health con-
cern for the cholera. This results from both water and food contamination.
Other foodborne illnesses and infection have been caused by enterohemorrhagic
Escherichia coli O157:H7 and Listeria, which causes listeriosis. The illness among
infants and the elderly may be severe and even fatal.
It was indicated that there were other sources of foodborne pathogens as unspec-
ified agents. These could refer to naturally occurring toxins such as mycotoxins,
marine biotoxins, cyanogenic glycosides, and toxins produced by mushrooms.
Mycotoxins, such as aflatoxin and ochratoxin A, are found in numerous staple foods.
Prevention and control of foodborne diseases need to be achieved and reduced by
farmers, producers, and the public. Organic farmers using manure need to use prop-
erly composted materials. Other farmers need to prevent domestic and wild animals
from entering fields and contaminating crops. Where possible, fruits and vegetables
sold to the public should be washed thoroughly. Good hygienic practice must be
Pathogens in Food and Water 105

used by the public. Water supplies need to be protected from animal and human
waste contamination.

WATERBORNE DISEASES
As stated previously, many of the foodborne diseases are also related to water-
borne organisms. There are other direct and indirect diseases associated with water
courses; for example, malaria is transmitted via a bite by the female Anopheles mos-
quito. With the bite, the parasitic protozoan is introduced into the human circulatory
system. The mosquito breeds in shallow stagnant water. Most of the waterborne
diseases caused by pathogenic micro­organ­isms are transmitted from freshwater
sources. These can be bathing, swimming, drinking, and washing water. Food can
be contaminated by the water.
The major waterborne diseases occur in developing countries as the result of lack
of sanitary conditions, lack of infrastructure to remove and treat wastes, lack of or
poor hygiene, poor education, and stagnant water sources.
Table 10.4 presents waterborne pathogens confirmed by epidemiological studies
and case histories. These studies were done with healthy adult volunteers and as such
apply to only a portion of the exposed population.
Bacteria and protozoa are the predominant micro­organ­isms causing waterborne
diseases. These organisms enter the intestinal tract and then invade tissues or the cir-
culatory system. Viruses are also causes of waterborne diseases. Metazoan parasites
(e.g., roundworms or nematodes such as Dracunculus, which causes guinea worm
disease) come from swallowing water in which there are certain copepods, which
are small crustaceans found in the sea and nearly every freshwater habitat and act as
vectors for nematode Dracunculus.
Some members of the Schistosomatidae family infect individuals who have skin
contact with infected water. The disease schistosomiasis affects hundreds of mil-
lions of people worldwide.
Table 10.5 shows some waterborne infections, the agent, and the source the agent
in the water supply, and general disease symptoms. Many of the symptoms are simi-
lar (e.g., diarrhea), and the sources can be identified by specific tests. Particularly
with respect to developing countries, where proper sanitation is not available, fecal
contamination (e.g., fecal to oral) is a major source of infection. Runoff containing
fecal matter will contaminate drinking and bathing water sources.
Although the United States has one of the safest drinking water systems in the
world, there are an estimated 4 to 32 million cases of acute gastrointestinal illness
(AGI) per year from public drinking water systems. This estimate does not include
waterborne illness from nonpublic drinking water systems (e.g., private wells), rec-
reational water, or water for other uses (e.g., irrigation, medical uses, or building
water systems). The frequency of disease from all water exposures is likely higher,
but the overall prevalence of waterborne illness in the United States is unknown
(CDC 2013).
106 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 10.4
Waterborne Pathogens and Their Significance in Water Supplies
Health Persistence in Relative
Pathogen Significancea Water Suppliesb Infectivityc

Bacteria
Burkholderia pseudomallei High May multiply Low
Campylobacter jejuni, Campylobacter coli High Moderate Low
Escherichia coli: Pathogenic High Moderate Low
Escherichia coli: Enterohemorrhagic High Moderate Low
Legionella spp. High May multiply Low
Nontuberculous mycobacteria Low May multiply High
Pseudomonas aeruginosa Moderate May multiply Moderate
Salmonella typhi High Moderate Low
Other salmonellae High May multiply Low
Shigella spp. High Short Low High
Vibrio cholerae High Short to long Low
Yersinia enterocolitica High Long Low
Viruses
Adenoviruses High Long High
Enteroviruses High Long High
Astroviruses High Long High
Hepatitis A virus High Long High
Hepatitis E virus High Long High
Noroviruses High Long High
Sapoviruses High Long High
Rotavirus High Long High

Protozoa
Acanthamoeba spp. High May multiply High
Cryptosporidium parvum High Long High
Cyclospora cayetanensis High Long High
Entamoeba histolytica High Moderate High
Giardia intestinalis High Moderate High
Naegleria fowleri High May multiply Mod
Toxoplasma gondii High Long High

Helminth
Dracunculus medinensis High Moderate High
Schistosoma spp. High Moderate High

Source: World Health Organization (WHO). 2007. http://www.who.int/­water_sanitation_health/­​


gdwqrevision/­watborpath/­en
a Health significance relates to the severity of impact, including associations with outbreaks.

b Detection period for infective stage in water at 20°C; short, up to 1 week; moderate, 1 week to

1 month; long, greater than 1 month.


c From experiment with human volunteers, from epidemiological evidence and animal studies.

High mean infective dose can be 1–102 organisms or particles, moderate can be 102–104, and
low is greater than 104.
Pathogens in Food and Water 107

TABLE 10.5
Some Waterborne Infections, the Agents Involved, Source of Water Supply,
and General Disease Symptoms
Disease and Sources of Agent
Transmission Microbial Agent in Water Supply General Symptoms

Bacteria
Botulism Clostridium botulinum Contaminated water
Contaminated food Vomiting, diarrhea,
difficulty swallowing,
respiratory failure
resulting in death
Campylobacteriosis Most commonly Fecal-­contaminated High fever, dysentery
caused by drinking water symptoms
Campylobacter jejuni
Cholera Vibrio cholerae Contaminated Watery diarrhea, nausea,
drinking water vomiting, rapid pulse,
hypovolemic shock
resulting in death
Escherichia coli Certain strains Contaminated water Diarrhea, prolonged
infection dehydration
Mycobacterium Mycobacterium Exposure in Lesions on elbows, knees,
marinum swimming pools feet, and hands
Dysentery Species of Salmonella Contaminated water Feces with blood or mucus,
and Shigella, Shigella bloody vomit
dysenteriae
Legionellosis Legionella Contaminated water Influenza, pneumonia, fever,
pneumophila chills, ataxia, anorexia,
muscle aches
Leptospirosis Leptospira Animal urine-­ Flu-­like symptoms,
contaminated water meningitis, liver damage,
and renal failure
Salmonellosis Salmonella Food, contaminated Diarrhea, fever, vomiting,
water abdominal cramps
Typhoid fever Salmonella typhi Feces-­contaminated High fever, delirium,
water enlargement of spleen and
liver

Protozoa
Amoebiasis Entamoeba histolytica Sewage, Fever, abdominal pain,
contaminated diarrhea, bloating
drinking water
Cryptosporidiosis Cryptosporidium Animal manure Flu-­like symptoms, diarrhea,
parvum weight loss, nausea
Giardiasis Giardia lamblia Water contamination Diarrhea, abdominal pain,
bloating, flatulence

(Continued)
108 Disposal and Management of Solid Waste: Pathogens and Diseases

TABLE 10.5 (Continued)
Some Waterborne Infections, the Agents Involved, Source of Water Supply,
and General Disease Symptoms
Disease and Sources of Agent
Transmission Microbial Agent in Water Supply General Symptoms

Parasites
Schistosomiasis Schistosoma Water contaminated Blood in urine, fever, chills,
with certain snails rash
Dracunculiasis Dracunculus Stagnant water Rash, vomiting, diarrhea,
medinensis containing larvae asthmatic attack
Taeniasis Taenia (tapeworms) Contaminated Intestinal discomfort, weight
drinking water loss
Ascariasis Ascaris lumbricoides Feces-­contaminated Inflammation, fever, diarrhea
drinking water

Viruses
Severe acute Coronavirus Poorly treated water Fever, myalgia,
respiratory gastrointestinal discomfort,
syndrome (SARS) cough, and sore throat
Hepatitis A Hepatitis A virus Water and food Fever, fatigue, abdominal
pain, diarrhea, weight loss,
jaundice, depression

Source: Waterborne diseases. n.d. http://en.wikipedia.org/­wiki/­waterborne_diseases.

WHO states that water-­related diseases include:

• Those due to micro­organ­isms and chemicals in water people drink


• Diseases like schistosomiasis that have part of their life cycle in water
• Diseases like malaria with water-­related vectors
• Drowning and some injuries
• Others, such as legionellosis, carried by aerosols containing certain
micro­organ­isms

Obviously, not all of these result in gastrointestinal diseases. However, many of


the illnesses of children in developing countries that result in diarrhea and in many
cases death are due to gastrointestinal illness from waterborne causes. Many of these
could be prevented through good hygiene and eliminating sources (e.g., malaria).
Diarrhea occurs worldwide and causes 4% of all deaths and 5% of health loss
to disability. It is most commonly caused by gastrointestinal infections, which kill
around 2.2 million people globally each year, mostly children in developing coun-
tries. The use of water in hygiene is an important preventive measure, but contami-
nated water is also an important cause of diarrhea. Cholera and dysentery cause
severe, sometimes life-­threatening, forms of diarrhea.
Pathogens in Food and Water 109

SUMMARY
Foodborne and waterborne pathogens can contaminate individuals through food,
water, soil, and air. These pathogens result in large numbers of illnesses and deaths.
The burden to society is in the billions of dollars.
In developed countries, as a result of better hygiene, sanitation, and education,
the illnesses, hospitalizations, and death are considerably less than in developing
countries. However, the numbers and costs are still high. In developing countries,
mostly children are killed.
Water contamination can occur as a result of human and animal fecal matter. In
developing countries, especially in villages, drinking water resources are below the
deposition of human wastes.
The agricultural industry in the United States particularly needs to prevent con-
tamination by workers as well as potential contamination from runoff containing
animal waste. Many agricultural workers migrating from warm or hot climates can
infect crops, especially during harvesting. Education to prevent contamination by
workers is essential. Workers should also have adequate and clean facilities provid-
ing good hygienic practices.
The global burden, human toll, and costs could be greatly reduced by better edu-
cation, improved sanitation (especially in developing countries), and hygiene.

REFERENCES
Batz MB, Hoffman S, and Morris JG, Jr. Ranking the Risks: The 10 Pathogen-Food
Combinations with the Greatest Burden on Public Health. Gainesville, FL: University
of Florida, Emerging Pathogens Institute.
Centers for Disease Control and Prevention (CDC). 1999. CDC’s Emerging Infections
Programs—1999 Surveillance Results. Atlanta, GA: Centers for Disease Control and
Prevention.
Centers for Disease Control and Prevention (CDC). 2011. Vital signs: incidence and trends
of infection with pathogens transmitted commonly through food. MMWR Morb Mortal
Wkly Rep 60: 749–755.
Centers for Disease Control and Prevention (CDC). 2011. CDC Estimates of Foodborne
Illness in the United States. http://www.cdc.gov/foodborneburden/2011-foodborne-
estimates.html
Centers for Disease Control and Prevention (CDC). 2013. Magnitude and burden of water-
borne disease in the U.S. http://www.cdc.gov/healthywater/burden/index.html.
Epstein, E. 2011. Industrial Composting. Boca Raton, FL: CRC Press, Taylor and Francis.
Foodborne illness. n.d. http://en.wikipedia.org/wiki/Foodborne_illness
McCaig LF and Burt CW. 1999. National Hospital Ambulatory Medical Care Survey: 1999
Emergency Department Summary. Adv Data Jun 25 (320): 1–34.
Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro G, Griffin PM, and Tauxe
RV. 1999. Food-­related illnesses and death in the United States. Emerg Infect Dis 5(5):
607–625.
National Institute of Environmental Health Sciences (NIEHS). 2010. A Report Outlining the
Research Needs on the Human Effects of Climate Change. http://www.niehs.nih.gov/
health/materials/a_human_health_perspective_on_climate_change_full_report_508.pdf
110 Disposal and Management of Solid Waste: Pathogens and Diseases

Swartz MM. 2002. Human diseases caused by foodborne pathogens of animal origin. Clin
Infect Dis 34(Suppl 3): S111–S122.
Thomas MK, Murray R, Flockhart L, Pintar F, Pollari F, Fazil A, Nesbitt A, and Marshall B.
2013. Estimates of the burden of foodborne illnesses in Canada for 30 specified patho-
gens and unspecified agents, circa 2006. Foodborne Pathog Dis 10: 639–648.
US Food and Drug Administration. 2014. Food safety for moms-­to-­be: medical professionals—
foodborne pathogens. http://www.fda.gov/food/resourcesforyou/healtheducators/
ucm091681.htm
Waterborne diseases. n.d. http://en.wikipedia.org/wiki/Waterborne_disease
World Health Organization (WHO). 2003. Guidelines for Drinking Water Quality, 3rd edition.
Geneva, Switzerland: WHO.
World Health Organization (WHO). 2003. Hazard characterization for pathogens in food and
water. Microbial health risk assessment.
World Health Organization (WHO). 2007. Rolling revision of the WHO guidelines for drink-
ing-water quality. Waterborne Pathogens. http://www.who.int/water_sanitation_health/
gdwqrevision/watborpath/en
11 Disposal and
Management
of Solid Waste

INTRODUCTION
The disposal and management of solid waste will generally differ greatly in devel-
oped counties than in developing countries. This is partly the result of the absence
of infrastructure in developing countries. In developed countries, the presence of
wastewater-­handling facilities; septic systems for single homes (i.e., disposal in the
absence of sewerage); trash or garbage pickup; incineration with heat recovery; and
recycling and recovery of paper, metals, plastic, and glass are part of a regulated
and controlled infrastructure.
In many developing countries, disposal of both human wastes and solid waste is
unhygienic, resulting in proliferation of pathogens and diseases. There are opportu-
nities to reduce these conditions through low-­cost biological systems and in some
cases chemical systems.
The most opportune biological system is composting (i.e., controlled decomposi-
tion of organic wastes). In many cases, the compost can be used as an organic fertil-
izer or for plant nutrients to produce food. If lime is available, especially where soils
are acidic as in the case of humid areas, it is both an excellent disinfectant and a
source of calcium to plants.
The disposal options are

• Landfill or dumps
• Incineration or burning
• Anaerobic digestion
• Land application
• Composting
• Lime stabilization

I have separated land application and composting as two distinct entities even
though many agricultural and horticultural scientists would consider composting as
a subunit of land application. However, compost can also be used as a mulch to mini-
mize runoff and erosion, thus not directly incorporated into the soil. Furthermore,
dried compost can be used as a source of heat.

111
112 Disposal and Management of Solid Waste: Pathogens and Diseases

LANDFILLS OR DUMPS
Landfills today, especially in developing countries, are designed to reduce environ-
mental impacts, such as groundwater contamination and air pollution. Groundwater
contamination can principally result from both inorganic and organic chemical con-
taminants. Inorganic contaminants could be nitrogen and phosphorus from fertil-
izers, whereas organic contaminants could be pesticides, surfactants, lubricants, and
similar compounds.
The principal air pollution from landfills is from the discharge of the methane that
results from organic material decomposition under anaerobic conditions. Methane is
25 times the air pollutant compared to carbon dioxide. Methane is also an explosive
gas and has been known to seep into basements in nearby residences. There have
also been incidents of explosions when buildings were built on former landfills. An
example is one that occurred in the Boston, Massachusetts, area; newly developed
low-­cost housing had to be abandoned as a result of methane seepage into basements
and an explosion.
Dumps are places for indiscriminant disposal of human and other solid wastes.
They are a source of pathogens both through contamination of humans who scav-
enge the dump and via air pollution. As pointed out previously in this book, not
only are the scavengers subject to diseases but also they bring diseases into their
households and communities. Today, in addition to traditional garbage, a large
amount of electronic hardware is disposed. This can result in heavy metal and some
organic contamination.
Singh, Datta, and Nema (2007) reported that in India uncontrolled land disposal
of municipal solid waste (MSW) is common. They noted that groundwater contami-
nation is the most important source of contamination. Financial constraints are the
predominant restraint for improvements (Singh, Datta, and Nema 2007). In India
in 2007, it was reported that nearly 90% of the MSW was disposed in open dumps
and landfills, creating public health and environmental issues (Sharholy et al. 2008).
Uncontrolled dumps and landfills are also common in many other developing coun-
tries in Asia, Africa, and South America. As indicated previously, open dumps and
landfills are scavenged for usable items. However, the only possible management of
these dumps and landfills is soil covering on a daily basis. Groundwater contamina-
tion can be avoided by the use of liners. These actions then become a financial issue.

INCINERATION AND BURNING


Incineration is controlled burning in an enclosed facility. Incineration can be accom-
plished with energy recovery. Air pollution and disposal of ash can be regulated to
minimize environmental impacts. Burning of dumps can be deliberate or the result
of methane emission. Workers can initiate a fire by the careless disposal of ciga-
rettes. The United States Environmental Protection Agency (USEPA) reports that
the first incinerator was built in New York in 1885. By the middle of the twentieth
century, there were hundreds of combustion facilities. Combustion of MSW grew
in the 1980s, with more than 15% of all US MSW combusted by the early 1990s.
The majority of the nonhazardous waste incinerators was recovering energy by this
Disposal and Management of Solid Waste 113

time and had installed pollution control equipment. Following incineration, there
is still ash to be disposed. The ash is often toxic, containing heavy metals such
as vanadium, manganese, chromium, nickel, cadmium, arsenic, mercury, and lead.
There has been an attempt to use the ash for road building where it can be sealed to
prevent leaching. Alternative technologies are available or in development, such as
composting or anaerobic digestion with energy recovery, autoclaving, or mechanical
heat treatment using steam.
Incinerators are expensive and require control of emissions. However, heat
recovery is possible and may result in financial feasibility. Most likely, developing
countries would not opt for this way to manage MSW. In developed countries, espe-
cially Europe, this may be a feasible option, providing the incinerators can signifi-
cantly reduce air pollution.

ANAEROBIC DIGESTION
Anaerobic digestion is the biological decomposition of organic waste by bacteria
without oxygen. This can result in the production of combustible methane gas that
can be used for heating or operation of engines. Anaerobic digestion is common at
wastewater treatment plants in the United States, Canada, and Europe. It is not com-
mon in the use of MSW. Anaerobic digestion of solid waste is more complicated.
The material is heterogeneous, often containing metal and plastics, which are not
digested. Also, the moisture content is low; however, this can be adjusted.
Generally, anaerobic digesters in Europe and America are large and expensive
structures. However, I have seen modest, low-­cost units built from plywood and used
to decompose food waste in California and Hawaii. These could be designed in
small units for villages in developing countries and used to provide hot water and
even cooking for better hygiene. The residue can be used as a fertilizer and land
applied (see land application).
In India, inside a poor home I saw a simple animal waste anaerobic digester used
for cooking. My point is that there are opportunities in developing countries that
could provide for better methods of disposal of waste.
The efficiency of anaerobic digestion of wastes to kill human and animal patho-
gens is limited. Since anaerobic digested wastes, especially human wastes, are land
applied, the efficiency of anaerobic digestion on pathogen destruction is discussed in
the next section on the land application of wastes.

LAND APPLICATION
Direct land application of human and animal wastes has been used for many cen-
turies. Johansson et al. (2005) discussed the potential risks when spreading anaero-
bic digested residues on grass silage crops. One of the most comprehensive reviews
regarding the sources and fate of pathogens during land application of wastes was
reported by Gerba and Smith (2005). They found that more than 150 known enteric
pathogens might be present in untreated wastes. Use of untreated or raw wastes for
fertilization of food crops is not recommended. They can be used as fertilizer for trees
or crops not to be eaten by humans. There are regulations on land application of
114 Disposal and Management of Solid Waste: Pathogens and Diseases

wastes in the United States, Canada, and Europe. In the United States, the USEPA
regulation regarding the various processes that can be used to reduce pathogens
prior to land application are cited in 40 CFR 503 (processes to significantly reduce
pathogens [PSRPs]) (USEPA 1995).
Prior to land application, the waste can be disinfected using anaerobic digestion,
composting, or lime stabilization. Human wastes should not be applied near water
wells used for drinking or bathing. They should be applied downstream from human
habitation. Human wastes applied to land should be incorporated into the soil as
soon as possible. Children should not be allowed to play in the area. Workers should
change clothes prior to returning home or contacting other persons.

COMPOSTING
Composting of human wastes is being done in United States, Canada, and Europe.
Facilities range from very small to large. The two largest facilities are in California
and Canada. In developing countries, composting can be done on a very small
scale as well as for large municipalities. The technology selected depends on loca-
tion, material, land availability, power availability, human resources, and financial
resources. Location refers to proximity to homes and soil surface conditions. A com-
pacted surface may be needed if heavy equipment is used. Regardless of technology,
some type of bulking agent is required. This could be straw, grass, bagasse, shredded
wood or tree branches, nut hulls, or any other type of local material. The amount
of land required depends on the technology selected. Windrow technology would
require more land than the aerated static pile. Power is needed in the form of fuel for
equipment or electricity for blowers for the aerated pile system. Both solar and wind
power could be used for motors on blowers for the aerated pile system. No power is
needed for the system devised by Sir Albert Howard, an English botanist known for
his refinement of a traditional Indian composting system (Van Vuren 1949). A simple
method for composting human or animal wastes, also based on studies by Howard,
is shown in Figure 11.1 (Howard 1935, 1936, 1943; Epstein 1997).
For example, the aerated pile system basically only requires a blower. The piles
can be constructed by humans using shovels or a front-­end loader. Pipes to provide
the aeration range from bamboo to drainage plastic pipes or iron pipes. The aerated
pile system has been used in climates where rainfall exceeded 100 cm per month but
can be used where rainfall is much higher. The use of fabric covers allows the piles
to be constructed in virtually any climate.
Windrow composting can also be used with minimal equipment. Turning can be
accomplished by humans using shovels.
The disposal and management of various wastes is feasible by composting for
either small or large communities. In developing countries, the collection of various
wastes harmful to humans can be composted by simple processes and the residue
used as a fertilizer. If during the composting process the temperature were allowed
to reach 55°C for several days, then disinfection would occur. Pathogen destruction
is a function of time and temperature. The higher the temperature is, the less time is
needed for disinfection. Thus, in developing countries the wastes can be held in piles
for long periods of time.
Disposal and Management of Solid Waste 115

FIGURE 11.1  A simple process for composting human or animal wastes.

LIME STABILIZATION
The addition of lime can be an effective means for pathogen destruction. Most patho-
gens strive at neutral to slightly acid conditions. Bean et al. (2007) state that liming
is a cost-­effective treatment currently employed in much USEPA class B biosol-
ids production.
Lime stabilization is a simple process. Its advantages are simplicity and low cost.
The USEPA stated that the waste must reach a pH of 12 for 2 hours to be effective
in reducing pathogens. During lime treatment, ammonia, which is a disinfectant,
is released. Furthermore, heat is also produced. This combination of ammonia and
heat release can result in pathogen destruction.
For example, India has an abundance of lime primarily used for cement produc-
tion. Some of this lime could effectively be used for waste disinfection.

SUMMARY
Waste disposal is a major problem in developing countries. Solid waste production,
accumulation, and disposal are major sources of diseases.
There are several potential disposal methods:

• Landfill or dumps
• Incineration or burning
• Anaerobic digestion
• Land application
• Composting
• Lime stabilization

Landfills that are properly constructed and operated, land application, compost-
ing, and lime stabilization are the least-­expensive options. Landfills can be designed
to capture methane for heating and other uses. It is an affective disposal method for
all types of human wastes. Its limitation is that if energy is not recovered and used,
116 Disposal and Management of Solid Waste: Pathogens and Diseases

the technology results in solid waste disposal without any benefits. Furthermore, the
design must consider groundwater contamination.
Incineration with heat recovery is expensive, and air pollution is a major consid-
eration. The use of air pollution devices makes the technology even more expensive.
The technology has a primary use in developed countries that can afford it.
Certain wastes (e.g., human wastes), when land applied, are fertilizers for crops
that are not to be eaten raw. Land application is not feasible for MSW (e.g., plastics,
paper, and other materials).
Composting when temperatures reach 55°C can be effective in pathogen destruc-
tion, and the product can be used as a fertilizer and soil conditioner. However, the
technology today is primarily used for human and animal wastes. This also applies
for lime stabilization. These technologies are not suitable for MSW consisting of
plastics, metals, and other materials.
It is evident that several low-­cost and implementable technologies are available
and suitable for developing countries.

REFERENCES
Bean CL et al. 2007. Class B alkaline stabilization to achieve pathogen inactivation. Int J
Environ Res Public Health. 4(1): 53–60.
Epstein E. 1997. The Science of Composting. Lancaster, PA: Technomic.
Gerba CP, and Smith JE Jr. 2005. Sources of pathogenic micro­organ­isms and their fate during
land application of wastes. J Environ Quality 34: 42–48.
Howard A. 1935. The manufacture of humus by the Indore process. J R Soc Arts 74: 26–60.
Howard A. 1936. Manufacture of humus by the Indore process. Nature 137(3461): 363.
Howard A. 1943. An Agricultural Testament. New York: Oxford University Press.
Johansson M, Emmoth E, Salomonsson AC, and Albihm A. 2005. Potential risks when spread-
ing anaerobic digestion residues on grass silage crops—survival of bacteria, moulds and
viruses. Grass Forage Sci 60: 175–185.
Sharholy M, Ahmad K, Mahmood G, and Trivedi RC. 2008. Municipal solid waste manage-
ment in Indian cities. Waste Manage 28: 459–467.
Singh RK, Datta M, and Nema AK. 2007. Ground water contamination hazard potential rat-
ing of municipal solid waste dumps and landfills. In Proceedings of the International
Conference on Sustainable Solid Waste Management, Chennai, India, 296–303.
United States Environmental Protection Agency (USEPA). 1995. A Guide to the Biosolids Risk
Assessments for the EPA Part 503 Rule. Washington, DC: US Environmental Protection
Agency.
Van Vuren JPJ. 1949. Soil Fertility and Sewage. London: Faber and Faber.
Appendix: Details
of the Pathogens
and Their Diseases
ACTINOBACILLUS PLEUROPNEUMONIAE
Actinobacillus pleuropneumoniae causes porcine pleuropneumonia, a highly conta-
gious disease for which there is no effective vaccine. It is found in most major swine-­
producing regions. It is a pathogen in mammals, bird, and reptiles.

Sources
en.wikipedia.org/wiki/Actinobacillus_pleuropneumoniae.
http://www.ncbi.nlm.nih.gov/pubmed/11880056.

ACINETOBACTER BAUMANNII
Acinetobacter baumannii is considered one of the most difficult Gram-­negative
bacilli to control and treat. It can cause outbreaks of infection, including meningitis,
urinary infections, pneumonia, and wound infections. It is found in soil and water.
It is an opportunistic nosocomial pathogen. Therefore, it poses little risk to healthy
persons. It can live on the skin and survives for extensive periods under a variety of
environmental conditions.

Sources
Antunes LCS, Visca P, and Towner KJ. 2014. Acinetobacter baumannii: evolution of a global
pathogen. Pathog Dis doi: 10.1111/2049-632X.12125.
Maragakis LL and Perl TM. 2008. Acinetobacter baumannii: epidemiology, antimicrobial
resistance, and treatment options. Clin Infect Dis 46(8): 1254–1263.

ACTINOMYCES SPP.
Actinomycetes are a specific group of bacteria. Morphologically, they resemble
fungi because of their elongated cells that branch into filaments or hyphae.
During composting, reaching high temperatures, thermophilic and thermotoler-
ant actinomycetes are responsible for decomposition of the organic matter. In the
initial phase of composting, the intensive increase of microbial activity leads to self-­
heating of the organic material. High temperatures in composting help to kill viruses,
pathogenic bacteria (e.g., coliforms), parasites, and weed seeds. Actinomycetes live

117
118 Appendix: Details of the Pathogens and Their Diseases

predominantly aerobically; that is, they need oxygen for their metabolism. Aeration
during composting is therefore important. During the composting process, the acti-
nomycetes degrade natural substances such as chitin or cellulose.
Some thermophilic and thermotolerant actinomycetes are found to be responsible
for allergic symptoms in the respiratory tract (e.g., “extrinsic allergic alveolitis”).

Sources
en.wikipedia.org/wiki/Actinobacillus_pleuropneumoniae
Kokotovic B, Angen O, and Bisgaard M. 2011. Genetic diversity of Actinobacillus lignieresii
isolates from different hosts. Int J Acta Vet Scand 53(1): 6. http://www.actavetscand.
com/content/53/1/6

AEROMONAS SPP.
Species of Aeromonas are Gram-­negative, non-­spore-­forming, rod-­shaped, facul-
tatively anaerobic bacteria that occur ubiquitously and autochthonously in aquatic
environments. Aeromonas spp. are Gram-­negative rods of the family Vibrionaceae.
They are normal water inhabitants and are part of the regular flora of poikilotherm,
and homeotherm animals. They can be isolated from many foodstuffs (green veg-
etables, raw milk, ice cream, meat, and seafood).
While traveler’s diarrhea is the most common health problem of international
visitors, the major human diseases caused by Aeromonas spp. can be classified in
two principal groups: septicemia (mainly by strains of A. veronii subsp. sobria and
A. hydrophila) and gastroenteritis (any mesophilic Aeromonas spp. but principally
A. hydrophila and A. veronii). Most epidemiological studies have shown Aeromonas
spp. in stools were more often associated with diarrhea than with the carrier state;
an association with the consumption of untreated water was also conspicuous.
Acute self-­limited diarrhea is more frequent in young children and in older patients.
Chronic enterocolitis may also be observed. Fever, vomiting, and fecal leukocytes
or erythrocytes (colitis) may be present. The main putative virulence factors are
exotoxins and endotoxin (lipopolysaccharide, LPS).

Sources
Merino S, Rubitre X, Knochel S, and Tomas JM. 1995. Emerging pathogens: Aeromonas spp.
Int J Food Microbiol 28(2): 157–168.
Jordi Vila, Laboratori de Microbiologia, Institut d’Infeccions i Immunologia, Institut
d’Investigacions Biomèdiques August Pi i Sunyer, Fascultat de Medicina, Universitat de
Barcelona, Villarroel, 170; 08036 Barcelona, Spain; fax: 34.93.2279372. Opportunisitic
pathogen that can cause diarrheal diseases in otherwise healthy individuals and can
cause wound infections. Int J Food Microbiol 28: 2157–2168.

ASCARIS LUMBRICOIDES
An estimated 807–1,221 million people in the world are infected with Ascaris
lumbricoides (sometimes called just Ascaris). Ascaris, hookworm, and whipworm
are known as soil-­transmitted helminths (parasitic worms). Together, they account
Appendix: Details of the Pathogens and Their Diseases 119

for a major burden of disease worldwide. Ascariasis is now uncommon in the United
States, according to the Centers for Disease Control and Prevention.
Ascaris lives in the intestine and Ascaris eggs are passed in the feces of infected
persons. If the infected person defecates outside (near bushes, in a garden, or field)
or if the feces of an infected person are used as fertilizer, eggs are deposited on soil.
They can then mature into a form that is infective. Ascariasis is caused by ingesting
eggs. This can happen when hands or fingers that have contaminated dirt on them are
put in the mouth or by consuming vegetables or fruits that have not been carefully
cooked, washed, or peeled.
People infected with Ascaris often show no symptoms. If symptoms do occur,
they can be light and include abdominal discomfort. Heavy infections can cause
intestinal blockage and impair growth in children. Other symptoms such as cough
are due to migration of the worms through the body. Ascariasis is treatable with
medication prescribed by your health care provider.
Ascaris lumbricoides is a nematode (roundworm) that inhabits the intestines of
humans. It measures 13–35 cm in length and may live in the gut for 6–24 months.
Infection is normally from food contaminated by soil containing feces from the
worm. It is prevalent in developing countries, where there is often a combination of
poor sanitation and a host made vulnerable by malnutrition, iron-­deficiency anemia,
or impairment of growth.
If only a few worms are present, there may be no symptoms initially, but during
the migratory phase, the larvae may penetrate into the tissues and circulate around the
body via the blood and lymphatic systems, commonly to the lungs. In the lungs, the
larvae penetrate the pulmonary capillaries to enter the alveoli, from where they ascend
into the throat and descend back into the gut, where they may grow as large as 35 cm
in length.

Sources
Centers for Disease Control and Prevention, 1600 Clifton Rd., Atlanta, GA 30333. www.cdc.
gov/parasites/ascariasis 2013
Dora-Laskey A et al. 2012. Ascaris Lumbricoides-Medscape Reference. http://emedicine.
medscape.com/article/788398-overview
Patient.co.uk. http://www.patient.co.uk/doctor/ascaris-­lumbricoides

BACILLACEAE SPP.
See Bacillus spp.
Members of the family Bacillaceae produce endospores; most are Gram positive,
motile by lateral or peritrichous flagella (having flagella over the entire surface) or
nonmotile, and aerobic, facultative, or anaerobic.
The genus Bacillus, of the family Bacillaceae, consists of a heterogeneous group
of Gram-­positive, heterotrophic, aerobic or facultative anaerobic bacilli with the abil-
ity to form environmentally resistant, metabolically inert spores. These soil-­borne
organisms are ubiquitous throughout the world and occupy surprisingly diverse
environments. Within this large genus, the B. cereus sensu lato group consists of six
species, based on classical microbial taxonomy: B. anthracis (Ba), B. cereus (Bc),
120 Appendix: Details of the Pathogens and Their Diseases

B. mycoides, B. pseudomycoides, B. thuringiensis (Bt), and B. weihenstephanensis.


However, newer molecular phylogenies and comparative genome sequencing suggests
that these organisms should be classified as a single species. On the surface, this con-
clusion seems difficult to reconcile with the varied biological characteristics of these
organisms. Some Bc strains are thermophiles, while B. weihenstephanensis is psy-
chrophilic. By contrast, many members of this group are mesophiles and can be found
in a variety of locales, including soil, on plant surfaces, and in the mammalian gastro-
intestinal microflora. Some members of this group appear to be nonpathogenic, while
others cause diverse diseases, including gastroenteritis, food poisoning, endophthal-
mitis, tissue abscesses, and anthrax. Bt strains have the capacity to cause disease in
insects and possibly nematodes, while some evidence suggests that Bc strains are
part of the normal insect gut flora. Nevertheless, whole-­genome comparisons between
these organisms reveal a surprising similarity in gene content, and Han et al. (1989)
have concluded “that differential regulation [of gene content] modulates virulence
rather than simple acquisition of virulence factor genes,” a conclusion confirmed by
other studies. Consequently, we will refer to these organisms as the Bc species-­group,
to reflect the extremely close phylogenetic relationships between these organisms.

Sources
Han K et al. 1989. Synergistic activation and repression of transcription by Drosophila homeo-
box proteins. Cell 56(4): 573–583.
http://www.biomedcentral.com/1471–2164/12/430
Schmidt T, Scott EJ, and Dyer DW. 2011. Whole-­genome phylogenies of the family Bacillaceae
and expansion of the sigma factor gene family in the Bacillus cereus species-­group.
BMC Genomics 12: 430. doi:10.1186/1471-2164-12-430. http://www.biomedcentral.
com/1471–2164/12/430

BACILLUS SPP.
Bacillus cereus is a Gram-­positive, facultatively anaerobic, endospore-­forming, large
rod. These and other characteristics, including biochemical tests, are used to dif-
ferentiate and confirm the presence of B. cereus, although these characteristics are
shared with B. mycoides, B. pseudomycoides, B. thuringiensis, and B. anthracis.
Differentiation of these organisms depends on:

determination of motility (most B. cereus strains are motile)


presence of toxin crystals (B. thuringiensis)
hemolytic activity (B. cereus and others are beta-­ hemolytic, whereas
B. anthracis usually is nonhemolytic)
rhizoid growth, which is characteristic of B. cereus var. mycoides

Bacilli are an extremely diverse group of bacteria that include both the causative
agent of anthrax (Bacillus anthracis) as well as several species that synthesize impor-
tant antibiotics. In addition to medical uses, bacillus spores, due to their extreme
tolerance to both heat and disinfectants, are used to test heat sterilization tech-
niques and chemical disinfectants. Bacillus is a genus of Gram-­positive, rod-­shaped
Appendix: Details of the Pathogens and Their Diseases 121

(bacillus), bacteria and a member of the phylum Firmicutes. Bacillus species can
be obligate aerobes (oxygen reliant) or facultative anaerobes (having the ability to be
aerobic or anaerobic). They will test positive for the enzyme catalase when there has
been oxygen used or present. Ubiquitous in nature, Bacillus includes both free-­living
(nonparasitic) and parasitic pathogenic species. Under stressful environmental con-
ditions, the bacteria can produce oval endospores that are not true spores but which
the bacteria can reduce themselves to and remain in a dormant state for very long
periods. These characteristics originally defined the genus, but not all such species
are closely related, and many have been moved to other genera of Firmicutes.
Bacilli cause an array of infections, from ear infections to meningitis and uri-
nary tract infections to septicemia. Mostly, they occur as secondary infections in
immunodeficient hosts or otherwise-­compromised hosts. They may exacerbate pre-
vious infections by producing tissue-­damaging toxins or metabolites that interfere
with treatment.
The most well-­known disease caused by bacilli is anthrax, caused by Bacillus
anthracis. Anthrax has a long history with humans. It has been suggested that the fifth
and sixth plagues of Egypt recorded in the Bible (the fifth attacking animals, the sixth,
known as the plague of the boils, attacking humans) are descriptive of B. anthracis.
Bacilli are an extremely diverse group of bacteria that include both the causative agent
of anthrax (Bacillus anthracis) as well as several species that synthesize important
antibiotics. In addition to medical uses, bacillus spores, due to their extreme tolerance
to both heat and disinfectants, are used to test heat sterilization techniques and chemi-
cal disinfectants. Anthrax has more recently been brought to our attention as a pos-
sible method for bioterrorism. The recent anthrax mailings have brought acute public
attention to the issue and sparked extensive research into the devastating disease.
Anthrax is primarily a disease of herbivores, who acquire the bacterium by eating
plants with dust that contains anthrax spores. Humans contract the disease in three
different ways. Cutaneous anthrax occurs when a human comes into contact with the
spores from dust particles or a contaminated animal or carcass through a cut or abra-
sion. Cutaneous anthrax accounts for 95% of anthrax cases worldwide. During a 2- to
3-day incubation period, the spores germinate, vegetative cells multiply, and a papule
develops. Over the following days, the papule ulcerates, dries, and blackens to form the
characteristic eschar. The process is painless unless infected with another pathogen.
Gastrointestinal anthrax is contracted by ingesting contaminated meat. It occurs
in the intestinal mucosa when the organisms invade the mucosa through a preexist-
ing lesion. It progresses the same way as cutaneous anthrax. Although it is extremely
rare in developed countries, it has a very high mortality rate.
Pulmonary anthrax is the result of inhaled spores that are transported to the lymph
nodes, where they germinate and multiply. They are then taken into the bloodstream
and lymphatics, culminating in systemic arthritis, which is usually fatal.

Sources
Turnbull PCB. 1996. Bacillus. In Barons Medical Microbiology 4th edition. Galveston, TX:
University of Texas Medical Branch. http://en.wikipedia.org/wiki/Bacillus
Bacillus. Microbe Wiki. 2010. http://microbewiki.kenyon.edu/index.php/Bacillus
122 Appendix: Details of the Pathogens and Their Diseases

Turnbull PCB. Bacillus. In Medical Microbiology NCBI Bookshelf 4th edition, chapter 15.
http://www.ncbi.nlm.nih.gov/books/NBK7699
Food and Drug Administration. 2012. Bad Bug Book. Foodborne Pathogenic Microorganisms
and Natural Toxins. 2nd edition. Washington, DC: Food and Drug Administration.

BORDETELLA SPP.
Bordetella spp. are considered opportunistic pathogens. Thus, they predominantly
infect immunosuppressed and immunocompromised individuals. Several Bordetella
species have been associated with respiratory disease in humans. Bordetella pertussis
still poses an important health threat in developing countries. Although B. avium is
thought to be strictly an animal pathogen that causes tracheobronchitis in wild and
domesticated birds, infections in birds share many of the clinical and histopatho-
logic features of disease in mammals caused by B. pertussis and B. bronchiseptica.
Human cases of respiratory disease associated with B. avium have only recently
been reported in patients with cystic fibrosis.
Pertussis or whooping cough is a highly infectious respiratory disease caused by
Bordetella pertussis. In vaccinating countries, infants, adolescents, and adults are
relevant patient groups.
Whooping cough is a major cause of infant and childhood mortality. The World
Health Organization (WHO) reported about 16 million pertussis cases worldwide in
2008, with 95% of cases occurring in developing countries, and more than 100,000
children died from this disease. Pertussis remains endemic despite the introduction
of a vaccination program in 1974. During 2003–2007, there were 43,482 cases or
an incidence of 4.1 per 100,000 people reported from 20 European countries. In the
United States, the incidence of pertussis also increased from 3.53 in year 2007 to
5.54 per 100,000 in year 2009. Although pertussis is always classified as a disease
of infants and children, an increasing number of cases in the adolescent and adult
groups were also observed.

Sources
Emerging Infectious Diseases 15(1), January 2009.
Jusot V, Aberrane S, Ale F, Laouali B, Moussa I, Alio SA, Adehossi E, Collard JM, and Grais
RF. 2014. Prevalence of Bordetella infection in a hospital setting in Niamey, Niger.
J Trop Pediatr 60(3): 223–230.
Ting TX, Hashim R, Ahmad N, and Abdullah KH. 2013. Detection of Bordetella pertus-
sis from clinical samples by culture and end-­point PCR in Malaysian patients. Int J
Bacteriol 2013, Article ID 324136. http://dx.doi.org/10.1155/2013/324136

CAMPYLOBACTER JEJUNI
Campylobacter is one of the most common causes of diarrheal illness in the United
States. Most cases occur as isolated, sporadic events, not as part of recognized out-
breaks. Active surveillance through the Foodborne Diseases Active Surveillance
Network (FoodNet) indicates that about 14 cases are diagnosed each year for each
100,000 persons in the population. Many more cases go undiagnosed or unreported,
Appendix: Details of the Pathogens and Their Diseases 123

and campylobacteriosis is estimated to affect over 1.3 million persons every year.
Campylobacteriosis occurs much more frequently in the summer months than in the
winter. The organism is isolated from infants and young adults more frequently than
from persons in other age groups and from males more frequently than females.
It is a non-­spore-­forming, Gram-­negative rod with a curved to S-­shaped morphol-
ogy. Many strains display motility, which is associated with the presence of a flagel-
lum at one or both of the polar ends of this bacterium.
Members of the Campylobacter genus are microaerophilic, that is, they grow
at lower-­than-­atmospheric oxygen concentrations. Most grow optimally at oxygen
concentrations from 3% to 5%. Thus, these bacteria generally are fairly fragile in the
ambient environment and somewhat difficult to culture in the laboratory. Additional
conditions to which C. jejuni are susceptible include drying, heating, freezing, disin-
fectants, and acidic conditions.
Other Campylobacter species, such as C. coli and C. fetus, also cause foodborne
diseases in humans; however, more than 80% of Campylobacter infections are
caused by C. jejuni. Campylobacter coli and C. jejuni cause similar disease symp-
toms. Campylobacter fetus infections often are associated with animal contact or
consumption of contaminated foods and beverages and are especially problematic
for fetuses and neonates, in whom the mortality rate may be up to 70%.
Campylobacteriosis is an infectious disease caused by bacteria of the genus
Campylobacter. Most people who become ill with campylobacteriosis get diarrhea,
cramping, abdominal pain, and fever within 2 to 5 days after exposure to the organ-
ism. The diarrhea may be bloody and can be accompanied by nausea and vomiting.
The illness typically lasts about 1  week. Some infected persons do not have any
symptoms. In persons with compromised immune systems, Campylobacter occa-
sionally spreads to the bloodstream and causes a serious life-­threatening infection.
It does not commonly cause death. It has been estimated that approximately
76 persons with Campylobacter infections die each year.
Campylobacter jejuni is commonly found in animal feces. Campylobacter is the
most common bacterial cause of diarrhea in the United States; over 2 million cases
are reported each year. Although Campylobacter does not commonly cause death,
it is estimated that approximately 100 persons with Campylobacter infections die
each year.
In general, the infective dose, the minimum number of ingested Campylobacter
cells that can cause infection, is thought to be about 10,000. However, in trials, as
few as 500 ingested Campylobacter cells led to disease, not necessarily death, in
volunteers. Differences in infectious dose likely can be attributed to several fac-
tors, such as the type of contaminated food consumed and the general health of the
exposed person.
The incubation period, from time of exposure to onset of symptoms, generally is
2 to 5 days.
A small percentage of patients develop complications that may be severe. These
include bacteremia and infection of various organ systems, such as meningitis, hepa-
titis, cholecystitis, and pancreatitis. An estimated 1.5 cases of bacteremia occur for
every 1,000 cases of gastroenteritis. Infections also may lead, although rarely, to
miscarriage or neonatal sepsis.
124 Appendix: Details of the Pathogens and Their Diseases

Autoimmune disorders are another potential long-­term complication associated


with campylobacteriosis, for example, Guillain-­Barré syndrome (GBS). One case of
GBS is estimated to develop per 2,000 C. jejuni infections, typically 2 to 3 weeks
postinfection. Not all cases of GBS appear to be associated with campylobacteriosis,
but it is the factor most commonly identified prior to development of GBS. Various
studies have shown that up to 40% of GBS patients first had a Campylobacter infec-
tion. It is believed that antigens present on C. jejuni are similar to those in certain
nervous tissues in humans, leading to the autoimmune reaction. Reactive arthritis is
another potential long-­term autoimmune complication. It can be triggered by various
kinds of infections and occurs in about 2% of C. jejuni gastroenteritis cases.
Hemolytic uremic syndrome and recurrent colitis following C. jejuni infection
also have been documented.
The major symptoms are fever, diarrhea, abdominal cramps, and vomiting. The
stool may be watery or sticky and may contain blood (sometimes occult, i.e., not dis-
cernible to the naked eye) and fecal leukocytes (white cells). Other symptoms often
present include abdominal pain, nausea, headache, and muscle pain.
Most cases of campylobacteriosis are self-­limiting. The disease typically lasts
from 2 to 10 days.

Sources
http://www.cdc.gov/pulsenet/pathogens/campylobacter.html
Centers for Disease Control and Prevention (CDC).
Division of Foodborne, Waterborne, and Environmental Diseases (DFWED).
Food and Drug Administration. 2012. Bad Bug Book. Foodborne Pathogenic Microorganisms
and Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.
National Center for Emerging and Zoonotic Infectious Diseases (NCEZID).

CELLULOMONAS
Cellulomonas is a genus of Gram-­positive rod-­shaped bacteria. One of its main dis-
tinguishing features is the ability to degrade cellulose using enzymes such as endo-
glucanase and exoglucanase. The species are members of the Actinobacteria group.
Cellulomonas spp. are often believed to be of low virulence. There are only a few
reports of human infections.

Sources
Glazer AN, and Nikaido H. 2007. Microbial Biotechnology. 2nd ed. Cambridge, UK:
Cambridge University Press.
Madigan MT, Martinko JM, Dunlap PV, and Clark DP. 2009. Brock Biology of Microorganisms.
12th ed. San Francisco: Pearson.

ENTAMOEBA HISTOLYTICA
Entamoeba histolytica is a single-­cell anaerobic protozoan parasite responsible for a
disease called amoebiasis. It occurs usually in the large intestine and causes internal
Appendix: Details of the Pathogens and Their Diseases 125

inflammation, as its name suggests (histo = tissue, lytic = destroying). Worldwide,


50 million people are infected, mostly in tropical countries in areas of poor sanita-
tion. In industrialized countries, most of the infected patients are immigrants, insti-
tutionalized people, and those who have recently visited developing countries.
Inside humans, Entamoeba histolytica lives and multiplies as a trophozoite.
Trophozoites are oblong and about 15–20 µm in length. To infect other humans, they
encyst and exit the body. The life cycle of Entamoeba histolytica does not require
any intermediate host. Mature cysts (spherical, 12–15 µm in diameter) are passed in
the feces of an infected human. Another human can become infected by ingesting
them in fecally contaminated water, food, or hands. If the cysts survive the acidic
stomach, they transform back into trophozoites in the small intestine. Trophozoites
migrate to the large intestine, where they live and multiply by binary fission. Both
cysts and trophozoites are sometimes present in the feces. Cysts are usually found in
firm stool, whereas trophozoites are found in loose stool. Only cysts can survive lon-
ger periods (up to many weeks outside the host) and infect other humans. If tropho-
zoites are ingested, they are killed by the gastric acid of the stomach. Occasionally,
trophozoites might be transmitted during sexual intercourse.
Severe infections inflame the mucosa of the large intestine, causing amoebic dys-
entery. The parasites can also penetrate the intestinal wall and travel to organs such
as the liver via the bloodstream, causing extraintestinal amoebiasis. Symptoms of
these more severe infections include

• anemia
• appendicitis (inflammation of the appendix)
• bloody diarrhea
• fatigue
• fever
• gas (flatulence)
• genital and skin lesions
• intermittent constipation
• liver abscesses (can lead to death if not treated)
• malnutrition
• painful defecation (passage of the stool)
• peritonitis (inflammation of the peritoneum, which is the thin membrane
that lines the abdominal wall)
• pleuropulmonary abscesses
• stomachache
• stomach cramping
• toxic megacolon (dilated colon)
• weight loss

Sources
Food and Drug Administration. 2012. Bad Bug Book. Foodborne Pathogenic Microorganisms
and Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.
http://www.parasitesinhumans.org/entamoeba-­histolytica-­amoebiasis.html
126 Appendix: Details of the Pathogens and Their Diseases

ENTEROBACTERIA
Enterobacteriaceae is a large family of Gram-­ negative bacteria that includes,
along with many harmless symbionts, many of the more familiar pathogens, such
as Salmonella, Escherichia coli, Yersinia pestis, Klebsiella, and Shigella. Other
disease-­causing bacteria in this family include Proteus, Enterobacter, Serratia,
and Citrobacter.
Note: Individual pathogens of this family are discussed separately.

ESCHERICHIA COLI
Escherichia coli (E. coli) bacteria normally live in the intestines of people and ani-
mals. Most E.  coli are harmless and actually are an important part of a healthy
human intestinal tract. However, some E.  coli are pathogenic, meaning they can
cause illness, either diarrhea or illness outside the intestinal tract. The types of
E. coli that can cause diarrhea can be transmitted through contaminated water or
food or through contact with animals or persons.
Currently, there are four recognized classes of enterovirulent E. coli (collectively
referred to as the EEC group) that cause gastroenteritis in humans. Among these
is the enterohemorrhagic (EHEC) strain designated E.  coli O157:H7. E.  coli is a
normal inhabitant of the intestines of all animals, including humans. When aerobic
culture methods are used, E. coli is the dominant species found in feces. Normally,
E. coli serves a useful function in the body by suppressing the growth of harmful
bacterial species and by synthesizing appreciable amounts of vitamins. A minority
of E. coli strains are capable of causing human illness by several different mecha-
nisms. E. coli serotype O157:H7 is a rare variety of E. coli that produces large quan-
tities of one or more related, potent toxins that cause severe damage to the lining of
the intestine. These toxins (verotoxin [VT], shiga-­like toxin] are closely related or
identical to the toxin produced by Shigella dysenteriae.
E. coli consists of a diverse group of bacteria. Pathogenic E. coli strains are cate-
gorized into pathotypes. Six pathotypes are associated with diarrhea and collectively
are referred to as diarrheagenic E. coli.

• Shiga toxin-­producing E.  coli (STEC): STEC may also be referred to as


verocytotoxin-­producing E.  coli (VTEC) or EHEC. This pathotype is the
one most commonly heard about in the news in association with foodborne
outbreaks.
• Enterotoxigenic E. coli (ETEC)
• Enteropathogenic E. coli (EPEC)
• Enteroaggregative E. coli (EAEC)
• Enteroinvasive E. coli (EIEC)
• Diffusely adherent E. coli (DAEC)

Some kinds of E. coli cause disease by making a toxin called Shiga toxin. The
bacteria that make these toxins are called Shiga toxin-­producing E. coli, or STEC for
Appendix: Details of the Pathogens and Their Diseases 127

short. You might hear these bacteria called verocytotoxic E. coli (VTEC) or entero-
hemorrhagic E. coli (EHEC); these all refer generally to the same group of bacteria.
The strain of Shiga toxin-­producing E. coli O104:H4 that caused a large outbreak in
Europe in 2011 was frequently referred to as EHEC. The most commonly identified
STEC in North America is E. coli O157:H7 (often shortened to E. coli O157 or even
just O157). When you hear news reports about outbreaks of “E. coli” infections, they
are usually talking about E. coli O157.
In addition to E. coli O157, many other kinds (called serogroups) of STEC cause
disease. Other E. coli serogroups in the STEC group, including E. coli O145, are
sometimes called “non-­O157 STECs.” Currently, there are limited public health sur-
veillance data on the occurrence of non-­O157 STECs, including STEC O145; many
STEC O145 infections may go undiagnosed or unreported.
Compared with STEC O157 infections, identification of non-­O157 STEC infec-
tions is more complex. First, clinical laboratories must test stool samples for the
presence of Shiga toxins. Then, the positive samples must be sent to public health
laboratories to look for non-­O157 STEC. Clinical laboratories typically cannot iden-
tify non-­O157 STEC. Other non-­O157 STEC serogroups that often cause illness
in people in the United States include O26, O111, and O103. Some types of STEC
frequently cause severe disease, including bloody diarrhea and hemolytic uremic
syndrome (HUS), which is a type of kidney disease.

Sources
Centers for Disease Control and Prevention. http://www.cdc.gov/ecoli/general/index.html​?​
s_cid=cs_002
Food and Drug Administration. 2012. Bad Bug Book. Foodborne Pathogenic Microorganisms
and Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.

KLEBSIELLA PNEUMONIA
Klebsiella pneumoniae is a Gram-­ negative, nonmotile, encapsulated, lactose-­
fermenting, facultative anaerobic, rod-­shaped bacterium. Although found in the
normal flora of the mouth, skin, and intestines, it can cause destructive changes
to human lungs if aspirated. In the clinical setting, it is the most significant mem-
ber of the Klebsiella genus of Enterobacteriaceae. Klebsiella oxytoca and Klebsiella
rhinoscleromatis have also been demonstrated in human clinical specimens. In
recent years, klebsiellae have become important pathogens in nosocomial infections.
It naturally occurs in the soil, and about 30% of strains can fix nitrogen in anaero-
bic conditions [2]. As a free-­living diazotroph, its nitrogen fixation system has been
much studied and is of agricultural interest, as K. pneumoniae has been demon-
strated to increase crop yields in agricultural conditions.
K. pneumoniae can cause destructive changes to human lungs via inflammation
and hemorrhage, with cell death (necrosis) that sometimes produces a thick, bloody,
mucoid sputum (currant jelly sputum). These bacteria gain access typically after a
person aspirates colonizing oropharyngeal microbes into the lower respiratory tract.
128 Appendix: Details of the Pathogens and Their Diseases

As a general rule, Klebsiella infections are seen mostly in people with a weakened
immune system. Most often, illness affects middle-­aged and older men with debili-
tating diseases. This patient population is believed to have impaired respiratory host
defenses, including persons with diabetes, alcoholism, malignancy, liver disease,
chronic obstructive pulmonary diseases (COPDs), glucocorticoid therapy, renal fail-
ure, and certain occupational exposures (such as paper mill workers). Many of these
infections are obtained when a person is in the hospital (a nosocomial infection) for
some other reason. Feces are the most significant source of patient infection, fol-
lowed by contact with contaminated instruments.
The most common infection caused by Klebsiella bacteria outside the hospital
is pneumonia, typically in the form of bronchopneumonia and bronchitis. These
patients have an increased tendency to develop lung abscess, cavitation, empyema,
and pleural adhesions. It has a high death rate of about 50%, even with antimicro-
bial therapy. The mortality rate can be nearly 100% for persons with alcoholism
and bacteremia.
In addition, K. pneumoniae has long been recognized as a possible cause of
community-­ acquired pneumonia. Over the past two decades, K. pneumoniae
has been an exceedingly rare cause of community-­acquired pneumonia in North
America, Europe, and Australia. Yet, it remains an important cause of severe
community-­acquired pneumonia in Asia and Africa. In these regions, patients also
have the classic risk factor of alcoholism.

Sources
http://en.wikipedia.org/wiki/Klebsiella_pneumoniae
Yu VL, Hansen DS, Ko WC, Sagnimeni A, Klugman KP, von Gottberg A, et al. 2007. Virulence
characteristics of Klebsiella and clinical manifestations of K. pneumoniae bloodstream
infections. Emerg Infect Dis http://wwwnc.cdc.gov/eid/article/13/7/07–0187.htm.

MICROCOCCUS
Micrococcus is a genus of spherical bacteria in the family Micrococcaceae that is
widely disseminated in nature. Micrococci are microbiologically characterized as
Gram-­positive cocci, 0.5 to 3.5 μm in diameter.
Micrococci are usually not pathogenic. They are normal inhabitants of the human
body and may even be essential in keeping the balance among the various microbial
flora of the skin. Some species are found in the dust of the air (M. roseus), in soil
(M. denitrificans), in marine waters (M. colpogenes), and on the skin or in skin glands
or skin-­gland secretions of vertebrates (M. flavus). Those species found in milk, such
as M. luteus, M. varians, and M. freudenreichii, are sometimes referred to as milk
micrococci and can result in spoilage of milk production.
Micrococci have been isolated from human skin, animal and dairy products, and
beer. They are found in many other places in the environment, including water, dust,
and soil. Micrococcus luteus on human skin transforms compounds in sweat into
compounds with an unpleasant odor. Micrococci can grow well in environments with
Appendix: Details of the Pathogens and Their Diseases 129

little water or high-­salt concentrations. Most are mesophiles; some, like Micrococcus
antarcticus (found in Antarctica), are psychrophiles.
Though not a spore former, Micrococcus cells can survive for an extended period
of time. It has been indicated that the survival time can be thousands of years.
Micrococcus is generally thought to be a saprotrophic or commensal organism,
although it can be an opportunistic pathogen, particularly in hosts with compromised
immune systems, such as patients with human immunodeficiency virus (HIV). It can
be difficult to identify Micrococcus as the cause of an infection since the organism
is normally present in skin microflora, and the genus is seldom linked to disease. In
rare cases, death of immunocompromised patients has occurred from pulmonary
infections caused by Micrococcus. Micrococci may be involved in other infections,
including recurrent bacteremia, septic shock, septic arthritis, endocarditis, meningi-
tis, and cavitating pneumonia (immunosuppressed patients).

Sources
Encyclopedia Britannica. http://www.britannica.com/EBchecked/topic/380299/Micrococcus.
http://en.wikipedia.org/wiki/Micrococcus

MYCOBACTERIUM SPP.
Mycobacteria are widespread in nature, but the primary sources are water, soil,
cows, and gastrointestinal tracts of animals. Mycobacterium bovis is pathogenic for
cattle and some other animals but also has been shown to be infectious to humans
and therefore is a pathogen of concern to humans. Mycobacterium species are con-
sidered hardy because of their unique cell walls, which enable them to survive long
exposures to chemical disinfectants, including acids, alkalis, and detergents, and
because they are able to resist lysis by antibiotics. Mycobacterium bovis can survive
in the environment for several months in cold, dark, moist conditions and for up to
332 days at a temperature range of 12°C to 24°C.
Mycobacterium bovis, also referred to as Mycobacterium tuberculosis var. bovis,
is a Gram-­positive, aerobic, nonmotile, straight or slightly curved, rod-­shaped bac-
terium that lacks an outer cell membrane. It does not have spores or capsules and is
classified as an acid-­fast bacterium because in staining procedures its lipid-­rich cell
wall resists decolorization by acids.
Some other species of the genus Mycobacterium include M. tuberculosis,
M. leprae, M. africanum, M. avium, and M. microti. Members of the Mycobacterium
tuberculosis complex, which includes M. tuberculosis and M. bovis, are the causative
agents of human and animal tuberculosis. Mycobacterium bovis is a causative agent
of foodborne human tuberculosis (although it may also be transmitted via the air-
borne route if it subsequently infects the lungs and results in active disease).
Mycobacterium bovis causes tuberculosis in cattle and is considered a zoonotic
disease that also affects humans. Human tuberculosis caused by this organism is now
rare in the United States because of milk pasteurization and culling of infected cattle.
130 Appendix: Details of the Pathogens and Their Diseases

Death can result if the infection is left untreated. The Centers for Disease Control
and Prevention (CDC) recently reported that an estimated three deaths (mean) are
associated with M. bovis annually in the United States.
The infective dose of Mycobacterium bovis in cattle could be as low as 1 CFU
(6–10 organisms), while the precise infective dose for humans is still unknown; it is
suggested to be on the order of tens to millions of organisms.
Symptoms generally appear months to years after initial infection. Some infected
persons do not show any signs of the disease.
Ingestion of food contaminated with M. bovis can result in infection of the gastro-
intestinal tract or other parts of the body, for example, the lungs or the lymph nodes.
The disease may result in death if untreated.
Typical symptoms include fever, night sweats, fatigue, loss of appetite, and weight
loss. Other symptoms depend on the part of the body affected, for example, chronic
cough, blood-stained sputum, or chest pain, if the lungs are affected, or diarrhea,
abdominal pain, and swelling, if the gastrointestinal tract is affected. Infections in
humans also may be asymptomatic.
Duration of illness depends on the immune status of the infected person.
Symptoms could last for months or years, which necessitates a longer treatment
period. Individuals with symptoms of lung involvement should avoid public settings
until told by their health care providers that they are no longer a risk to others.
The route of entry is mostly through ingestion (oral). Inhalation and direct contact
with mucous membranes or broken skin, although not common, are also potential
routes of exposure.
Regarding the pathway, M. bovis can be taken up by alveolar macrophages in
the lung, especially if transmission is by the aerosol route (pulmonary tuberculosis).
From there, it is carried to the lymph nodes, where the organism can migrate to
other organs. M. bovis can multiply in these cells and in interstitial spaces, lead-
ing to formation of tubercle lesions. Gastrointestinal tuberculosis also causes the
associated lymph nodes to form tubercles, although the organism may not spread to
other organs.
An example occurred in March 2004 when a US-­born boy aged 15 months in New
York City died of peritoneal tuberculosis caused by Mycobacterium bovis infection.
M. bovis, a bacterial species of the M. tuberculosis complex, is a pathogen that pri-
marily infects cattle. However, humans also can become infected, most commonly
through consumption of unpasteurized milk products from infected cows. In indus-
trialized nations, human tuberculosis caused by M. bovis is rare because of milk
pasteurization and culling of infected cattle herds. This report summarizes an ongo-
ing, multiagency investigation that has identified 35 cases of human M. bovis infec-
tion in New York City. Preliminary findings indicate that fresh cheese (e.g., queso
fresco) brought to New York City from Mexico was a likely source of infection. No
evidence of human-­to-­human transmission has been found. Products from unpas-
teurized cow’s milk have been associated with certain infectious diseases and carry
the risk of transmitting M. bovis if imported from countries where the bacterium is
Appendix: Details of the Pathogens and Their Diseases 131

common in cattle. All persons should avoid consuming products from unpasteurized
cow’s milk.

Sources
Centers for Disease Control and Prevention. Human tuberculosis caused by Mycobacterium
bovis—New York City, 2001–2004. 2005. MMWR Morb Mortal Wkly Rep 54(24):
605–608.
Food and Drug Administration. 2012. Bad Bug Book. Foodborne Pathogenic Microorganisms
and Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.

NEISSERIA
Neisseria is a large genus of bacteria that colonize the mucosal surfaces of many
animals. Of the 11 species that colonize humans, only 2 are pathogens, N. meningitidis
and N. gonorrhoeae. Most gonococcal infections are asymptomatic and self-­
resolving, and epidemic strains of the meningococcus may be carried in more than
95% of a population where systemic disease occurs at less than 1% prevalence.
Neisseria species are Gram-­negative bacteria included among the proteobacteria,
a large group of Gram-­negative forms.
There are several species of Neisseria that are important pathogens. These are
discussed separately.
Approximately 2,500 to 3,500 cases of N. meningitidis infection occur annually
in the United States, with a case rate of about 1 in 100,000. Children younger than
5 years are at greatest risk, followed by teenagers of high school age. Rates in sub-­
Saharan Africa can be as high as 1 in 1,000 to 1 in 100.

Neisseria meningitidis
Neisseria meningitidis, often referred to as meningococcus, is a bacterium that can
cause meningitis and other forms of meningococcal disease, such as meningococ-
cemia, a life-­threatening sepsis. Neisseria meningitidis is a major cause of illness
and death during childhood in industrialized countries and has been responsible for
epidemics in Africa and in Asia. The bacteria are round and are often joined in pairs.
They are Gram negative since they have outer and inner membranes with a thin
layer of peptidoglycan between. Cultures of the bacteria test positive for the enzyme
cytochrome c oxidase. It exists as normal flora (nonpathogenic) in the nasopharynx
of up to 5%–15% of adults. It causes the only form of bacterial meningitis known to
occur epidemically.
Meningococcus is spread through the exchange of saliva and other respiratory
secretions during activities like coughing, sneezing, kissing, and chewing on toys.
It infects the host cell by sticking to it, mainly with long thin extensions called pili
and the surface-­exposed proteins Opa and Opc. Although it initially produces gen-
eral symptoms like fatigue, it can rapidly progress from fever, headache, and neck
132 Appendix: Details of the Pathogens and Their Diseases

stiffness to coma and death. The symptoms of meningitis are easily confused with
those caused by other organisms, such as Hemophilus influenzae and Streptococcus
pneumoniae. Death occurs in approximately 10% of cases [5]. Those with impaired
immunity may be at particular risk of meningococcus (e.g., those with nephrotic
syndrome or splenectomy; vaccines are given in cases of removed or nonfunction-
ing spleens).

Neisseria gonorrhoeae
Neisseria gonorrhoeae infections are acquired by sexual contact and usually affect
the mucous membranes of the urethra in males and the endocervix and urethra in
females, although the infection may disseminate to a variety of tissues. The patho-
genic mechanism involves the attachment of the bacterium to nonciliated epithelial
cells via pili and the production of lipopolysaccharide endotoxin. Similarly, the lipo-
polysaccharide of Neisseria meningitidis is highly toxic, and it has an additional
virulence factor in the form of its antiphagocytic capsule. Both pathogens produce
immunoglobulin A proteases, which promote virulence. Many normal individu-
als may harbor Neisseria meningitidis in the upper respiratory tract, but Neisseria
gonorrhoeae is never part of the normal flora and is only found after sexual contact
with an infected person (or direct contact, in the case of infections in the newborn).
Infection of the genitals can result in a purulent (or pus-­like) discharge from the
genitals, which may be foul smelling. Symptoms may include inflammation, redness,
swelling, and dysuria.
Neisseria gonorrhoeae can also cause conjunctivitis, pharyngitis, proctitis or ure-
thritis, prostatitis, and orchitis.
Conjunctivitis is common in neonates (newborns), and silver nitrate or antibiotics
are often applied to their eyes as a preventive measure against gonorrhoea. Neonatal
gonorrheal conjunctivitis is contracted when the infant is exposed to N. gonorrhoeae
in the birth canal and can lead to corneal scarring or perforation, resulting in blind-
ness in the neonate.
Disseminated N. gonorrhoeae infections can occur, resulting in endocarditis, men-
ingitis, or gonococcal dermatitis-­arthritis syndrome. Dermatitis-­arthritis syndrome
presents with arthralgia, tenosynovitis, and painless nonpruritic (nonitchy) dermatitis.
Infection of the genitals in females with N. gonorrhoeae can result in pelvic
inflammatory disease if left untreated, which can result in infertility. Pelvic inflam-
matory disease results if N. gonorrhoeae travels into the pelvic peritoneum (via the
cervix, endometrium, and fallopian tubes). Infertility is caused by inflammation and
scarring of the fallopian tube. Infertility is a risk to 10% to 20% of the females
infected with N. gonorrhoeae.
The prevalence of gonorrhea (Neisseria gonorrheae) in the United States and
abroad, especially in underdeveloped and developing countries, has decreased in the
last two decades. Recently, though, higher rates of infection have been reported due
to the increase of antimicrobial-­resistant gonococci.
Appendix: Details of the Pathogens and Their Diseases 133

Sources
http://biology.kenyon.edu/slonc/bio38/stancikd_02/What_is_Neisseria_gonorrhoeae.html.
http://en.wikipedia.org/wiki/Neisseria_meningitidis#Epidemiology.
Todar’s Online Textbook. http://textbookofbacteriology.net/neisseria.html.

PROTEUS SPP.
Proteus is a genus of Gram-­negative proteobacteria. Proteus bacilli are widely distrib-
uted in nature as saprophytes, being found in decomposing animal matter, in sewage,
in manure soil, and in human and animal feces. They are opportunistic pathogens,
commonly responsible for urinary and septic infections, often nosocomially.
Three species—P. vulgaris, P. mirabilis, and P. penneri—are opportunistic human
pathogens. Proteus includes pathogens responsible for many human urinary tract
infections. P. mirabilis causes wound and urinary tract infections. Most strains of
P. mirabilis are sensitive to ampicillin and cephalosporins. P. vulgaris is not sensi-
tive to these antibiotics. However, this organism is isolated less often in the labo-
ratory and usually only targets immunosuppressed individuals. P. vulgaris occurs
naturally in the intestines of humans and a wide variety of animals and in manure,
soil, and polluted waters. P. mirabilis, once attached to the urinary tract, infects the
kidney more commonly than Escherichia coli. P. mirabilis is often found as a free-­
living organism in soil and water.
About 10%–15% of kidney stones are struvite stones, caused by alkalization of
the urine by the action of the urease enzyme (which splits urea into ammonia and
carbon dioxide) of Proteus (and other) bacterial species.

Sources
http://en.wikipedia.org/wiki/Proteus_(bacterium)

PSEUDOMONAS SPP.
Pseudomonas infections are caused by any of several types of the Gram-­negative
Pseudomonas bacteria, especially Pseudomonas aeruginosa. Infections range from
mild external ones (affecting the ear or hair follicles) to serious internal infections
(affecting the lungs, bloodstream, or heart).
Pseudomonas bacteria, including Pseudomonas aeruginosa, are present through-
out the world in soil and water. These bacteria favor moist areas, such as sinks,
toilets, inadequately chlorinated swimming pools and hot tubs, and outdated or inac-
tivated antiseptic solutions. These bacteria may temporarily reside in the skin, ears,
and intestine of healthy people.
Pseudomonas aeruginosa infections range from minor external infections to
serious, life-­threatening disorders. Infections occur more often and tend to be more
severe in people who
134 Appendix: Details of the Pathogens and Their Diseases

• Are weakened (debilitated) by certain severe disorders


• Have diabetes or cystic fibrosis
• Are hospitalized
• Have a disorder that weakens the immune system, such as human immuno-
deficiency virus (HIV) infection
• Take drugs that suppress the immune system, such as those used to treat
cancer or to prevent rejection of transplanted organs

These bacteria can infect the blood, skin, bones, ears, eyes, urinary tract, heart
valves, and lungs, as well as wounds (such as burns, injuries, or wounds made dur-
ing surgery). Use of medical devices, such as catheters inserted into the bladder or a
vein, breathing tubes, and mechanical ventilators, increases the risk of Pseudomonas
aeruginosa infections. These infections are commonly acquired in hospitals.
P. aeruginosa is a rod-­shaped organism that can be found in soil, water, plants,
and animals. Because it rarely causes disease in healthy persons but infects those
who are already sick or who have weakened immune systems, it is called an opportu-
nistic pathogen. Opportunistic pathogens are organisms that do not ordinarily cause
disease but multiply freely in persons whose immune systems are weakened by ill-
ness or medication. Such persons are said to be immunocompromised. Patients with
acquired immunodeficiency syndrome (AIDS) have an increased risk of developing
serious Pseudomonas infections. Hospitalized patients are another high-­risk group
because P. aeruginosa is often found in hospitals. Infections that can be acquired in
the hospital are sometimes called nosocomial diseases.

• Heart and blood. P. aeruginosa is the fourth-­most-­common cause of bacte-


rial infections of the blood (bacteremia). Bacteremia is common in patients
with blood cancer and patients who have Pseudomonas infections else-
where in the body. P. aeruginosa infects the heart valves of intravenous
drug abusers and persons with artificial heart valves.
• Bones and joints. Pseudomonas infections in these parts of the body can
result from injury, the spread of infection from other body tissues, or bac-
teremia. Persons at risk for Pseudomonas infections of the bones and joints
include diabetics, intravenous drug abusers, and bone surgery patients.
• Central nervous system. P. aeruginosa can cause inflammation of the tis-
sues covering the brain and spinal cord (meningitis) and brain abscesses.
These infections may result from brain injury or surgery, the spread of
infection from other parts of the body, or bacteremia.
• Eye and ear. P. aeruginosa can cause infections in the external ear canal—
so-­called swimmer’s ear—that usually disappear without treatment. The
bacterium can cause a more serious ear infection in elderly patients, possibly
leading to hearing problems, facial paralysis, or even death. Pseudomonas
infections of the eye usually follow an injury. They can cause ulcers of the
cornea that may cause rapid tissue destruction and eventual blindness. The
risk factors for Pseudomonas eye infections include wearing soft extended-­
wear contact lenses; using topical corticosteroid eye medications; being in
Appendix: Details of the Pathogens and Their Diseases 135

a coma; having extensive burns; undergoing treatment in an intensive care


unit; and having a tracheostomy or endotracheal tube.
• Urinary tract. Urinary tract infections can be caused by catheterization,
medical instruments, and surgery.
• Lung. Risk factors for P. aeruginosa pneumonia include cystic fibrosis;
chronic lung disease; immunocompromised condition; being on antibiotic
therapy or a respirator; and congestive heart failure. Patients with cystic
fibrosis often develop Pseudomonas infections as children and suffer recur-
rent attacks of pneumonia.
• Skin and soft tissue. Even healthy persons can develop a Pseudomonas skin
rash following exposure to the bacterium in contaminated hot tubs, water
parks, whirlpools, or spas. This skin disorder is called Pseudomonas or
“hot tub” folliculitis and is often confused with chickenpox. Severe skin
infection may occur in patients with P. aeruginosa bacteremia. The bacte-
rium is the second-­most-­common cause of burn wound infections in hospi-
talized patients.

Sources
The Free Dictionary.
http://medical-­dictionary.thefreedictionary.com/Pseudomonas+Infections
http://www.merckmanuals.com/home/infections/bacterial_infections/pseudomonas_​
infections.html

SALMONELLA SPP.
Salmonella is a motile, non-­spore-­forming, Gram-­negative, rod-­shaped bacterium in
the family Enterobacteriaceae and the tribe Salmonellae. Nonmotile variants include
S. gallinarum and S. pullorum. The genus Salmonella is divided into two species
that can cause illness in humans:

Salmonella enterica
Salmonella bongori

Salmonella enterica, which is of the greatest public health concern, is comprised


of six subspecies:

Salmonella enterica subsp. enterica (I)


Salmonella enterica subsp. salamae (II)
Salmonella enterica subsp. arizonae (IIIa)
Salmonella enterica subsp. diarizonae (IIIb)
Salmonella enterica subsp. houtenae (IV)
Salmonella enterica subsp. indica (VI)

Salmonella is further subdivided into serotypes based on the Kaufmann–­White


typing scheme first published in 1934, which differentiates Salmonella strains by their
136 Appendix: Details of the Pathogens and Their Diseases

surface and flagellar antigenic properties. Salmonella spp. are commonly referred to
by their serotype names. For example, Salmonella enterica subsp. enterica is fur-
ther divided into numerous serotypes, including Salmonella serotype Enteritidis and
Salmonella serotype Typhimurium, which are common in the United States. (Note
that species names are italicized, but serotype names are not.) When Kaufmann first
proposed the scheme, 44 serotypes had been discovered. As of 2007, the number of
serotypes discovered was 2,579.
Salmonella spp. are bacteria that cause one of the most common forms of food
poisoning worldwide. There are over 2,500 different types of Salmonella spp., but
they all produce a similar clinical picture to other forms of infective gastroenteritis.
Salmonellosis is an infection with bacteria called Salmonella. Salmonella germs
have been known to cause illness for over 100 years. They were discovered by an
American scientist named Salmon, for whom they are named.
Most persons infected with Salmonella develop diarrhea, fever, and abdominal
cramps 12 to 72 hours after infection. The illness usually lasts 4 to 7 days, and most
persons recover without treatment. However, in some persons, the diarrhea may be
so severe that the patient needs to be hospitalized. In these patients, the Salmonella
infection may spread from the intestines to the bloodstream and then to other body
sites and can cause death unless the person is treated promptly with antibiotics. The
elderly, infants, and those with impaired immune systems are more likely to have a
severe illness.
Every year, approximately 42,000 cases of salmonellosis are reported in the
United States. Because many milder cases are not diagnosed or reported, the actual
number of infections may be 29 or more times greater. There are many different
kinds of Salmonella bacteria. Salmonella serotype Typhimurium and Salmonella
serotype Enteritidis are the most common in the United States. Salmonellosis is
more common in the summer than winter.
Children are the most likely to get salmonellosis. The rate of diagnosed infec-
tions in children less than 5 years old is higher than the rate in all other persons.
Young children, the elderly, and the immunocompromised are the most likely to
have severe infections. It is estimated that approximately 400 persons die each year
with acute salmonellosis.
Salmonella causes two kinds of illness:

Gastrointestinal illness causes nausea, vomiting, diarrhea, cramps, and fever,


with symptoms generally lasting a couple of days and tapering off within
a week. In otherwise-­healthy people, the symptoms usually go away by
themselves, but long-term arthritis may develop.
Typhoidal illness causes high fever, diarrhea or constipation, aches, headache,
lethargy (drowsiness or sluggishness), and sometimes a rash. It is a very
serious condition; up to 10% of people who do not receive treatment may
die. Many kinds of food can become contaminated with the first type, from
meats and eggs to fruits and vegetables, and even dry foods, like spices
and raw tree nuts. The typhoidal illness usually is associated with sewage-
contaminated drinking water or crops irrigated with sewage-contaminated
Appendix: Details of the Pathogens and Their Diseases 137

water. Some pets, like turtles and other reptiles and chicks, can carry
Salmonella, which can spread to anything that comes into contact with
the pet. For example, a pet owner can, through unwashed hands, contami-
nate foods or even his or her own face with Salmonella. This bacterium is
hard to wash off food, even with soapy water, so important measures for
preventing foodborne illness from Salmonella include thorough cooking,
hand washing, keeping raw foods separated from cooked foods, and keep-
ing foods at the correct temperature (refrigerate foods at 40°F or below). In
people with weak immune systems, Salmonella can spread to other organs
and cause very serious illness.

Sources
Centers for Disease Control and Prevention (CDC). http://www.cdc.gov/salmonella/general/
Food and Drug Administration. 2012. Bad Bug Book. Foodborne Pathogenic Microorganisms
and Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.
Patient.co.uk. http://www.patient.co.uk/doctor/salmonella-­gastroenteritis

SERRATIA PLYMUTHICA
Serratia is a genus of Gram-­negative, facultatively anaerobic, rod-­shaped bacteria
of the Enterobacteriaceae family. The most common species in the genus, Serratia
marcescens, is normally the only pathogen and usually causes nosocomial infec-
tions. However, rare strains of Serratia plymuthica, S. erratia liquefaciens, Serratia
rubidaea, and Serratia odoriferae have caused diseases through infection.
In the hospital, Serratia species tend to colonize the respiratory and urinary
tracts, rather than the gastrointestinal tract, in adults.
Serratia infection is responsible for about 2% of nosocomial infections of the
bloodstream, lower respiratory tract, urinary tract, surgical wounds, and skin and
soft tissues in adult patients. Outbreaks of S. marcescens meningitis, wound infec-
tions, and arthritis have occurred in pediatric wards.
Serratia infection has caused endocarditis and osteomyelitis in people addicted
to heroin.
Cases of Serratia arthritis have been reported in outpatients receiving intra-­
articular injections.
Serratia marcescens is ubiquitous. It is commonly found in soil, water, plants, and
animals. It is widely present in nonpotable water in underdeveloped countries due to
poor chlorination.
Serratia marcescens is an opportunistic pathogen that causes nosocomial infec-
tions. It is resistant to many antibiotics traditionally used to treat bacterial infections,
such as penicillin and ampicillin.

Sources
http://en.wikipedia.org/wiki/Serratia
https://microbewiki.kenyon.edu/index.php/Serratia_marcescens
138 Appendix: Details of the Pathogens and Their Diseases

STAPHYLOCOCCUS AUREUS
Staphylococcus aureus (staph) is a type of bacteria that about 30% of people carry
in their noses. Most of the time, staph does not cause any harm; however, sometimes
staph causes infections. In health care settings, these infections can be serious or
fatal, including

• Bacteremia or sepsis when bacteria spread to the bloodstream


• Pneumonia, which predominantly affects people with underlying lung dis-
ease, including those on mechanical ventilators
• Endocarditis (infection of the heart valves), which can lead to heart failure
or stroke
• Osteomyelitis (bone infection), which can be caused by staph bacteria trav-
eling in the bloodstream or put there by direct contact, such as following
trauma (puncture wound of foot or intravenous drug abuse)

Staph bacteria can also become resistant to certain antibiotics. These drug-­
resistant staph infections include those cased by methicillin-­resistant Staphylococcus
aureus (MRSA), vancomycin-­intermediate Staphylococcus aureus (VISA), and
vancomycin-­resistant Staphylococcus aureus (VRSA).
Staphylococcal species are Gram-­positive, nonmotile, catalase-­positive, small,
spherical bacteria (cocci), which, on microscopic examination, appear in pairs, short
chains, or bunched in grape-­like clusters. Staphylococci are ubiquitous and impos-
sible to eradicate from the environment. Many of the 32 species and subspecies in the
genus Staphylococcus are potentially found in foods due to environmental, human,
and animal contamination.
Several staphylococcal species, including both coagulase-­negative and coagulase-­
positive strains, have the ability to produce highly heat-­stable enterotoxins that cause
gastroenteritis in humans. S. aureus is the etiologic agent predominantly associated
with staphylococcal food poisoning.
S. aureus is a versatile human pathogen capable of causing staphylococcal food
poisoning, toxic shock syndrome, pneumonia, postoperative wound infection, and
nosocomial bacteremia.
S. aureus produces a variety of extracellular products, many of which act as viru-
lence factors. Staphylococcal enterotoxins can act as superantigens capable of stimu-
lating an elevated percentage of T cells.
S. aureus is one of the most resistant non-­spore-­forming human pathogens and can
survive for extended periods in a dry state. Staphylococci are mesophilic. S. aureus
growth, in general, ranges from 7°C to 47.8°C, with 35°C the optimum temperature
for growth. The growth pH range is between 4.5 and 9.3, with an optimum between
7.0 and 7.5. Staphylococci are atypical in that they are able to grow at low levels
of water activity. For the most part, strains of S. aureus are highly tolerant to salts
and sugars.
This bacterium, often called “staph” for short, can cause food poisoning. It is
common in the environment and can be found in soil, water, and air and on everyday
objects and surfaces. It can live in humans and animals. Staphylococcus aureus is
Appendix: Details of the Pathogens and Their Diseases 139

found in foods and can make toxins (enterotoxins) that might not be destroyed by
cooking, although the bacterium itself can be destroyed by heat. These toxins can
cause nausea, stomach cramps, vomiting, and diarrhea. In more severe cases, the
toxins may cause loss of body fluid (dehydration), headache, muscle cramps, and
temporary changes in blood pressure and heart rate. The illness usually is intense
but normally lasts from just a few hours to a day. The toxins are fast-acting; they
cause symptoms within 1 to 7 hours after contaminated food is eaten. Follow basic
food safety tips to help protect yourself from this illness. Outbreaks often have
been linked to foods that require a lot of handling when they are being processed
or prepared or were not kept at proper refrigerator temperature (40°F or below). To
help protect yourself, it is especially important to wash your hands well when han-
dling food, properly clean your cooking equipment and surfaces, keep your cooked
foods from touching raw foods or unclean equipment or surfaces, and keep foods
refrigerated at 40°F or below. Examples of foods that have been linked to this type
of food poisoning include meat and meat products; poultry and egg products; salads,
such as egg, tuna, chicken, potato, and macaroni; bakery products, such as cream-
filled pastries, cream pies, and chocolate éclairs; sandwich fillings; and milk and
dairy products. Good hygienic practices are essential.

Sources
Centers for Disease Control and Prevention (CDC). http://www.cdc.gov/hai/organisms/staph.
html
Food and Drug Administration. Bad Bug Book. Foodborne Pathogenic Microorganisms and
Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.

STREPTOCOCCUS FAECALIS (ENTEROCOCCUS


FAECALIS), STREPTOCOCCUS PYOGENES,
AND STREPTOCOCCUS PNEUMONIAE
Enterococcus faecalis, formerly classified as part of the group D Streptococcus
system, is a Gram-­positive, commensal bacterium inhabiting the gastrointestinal
tracts of humans and other mammals. Like other species in the genus Enterococcus,
E. faecalis can cause life-­threatening infections in humans, especially in the nosoco-
mial (hospital) environment, where the naturally high levels of antibiotic resistance
found in E. faecalis contribute to its pathogenicity.
Streptococcus A is not a major cause of foodborne illness, although serious com-
plications occasionally develop if foodborne illness does occur. Streptococci can be
found on the skin; the mucous membranes of the mouth, respiratory, alimentary, and
genitourinary tracts of human and animals; and in some plants, soil, and bodies of
dirty water. They are opportunistic pathogens. Optimum incubation temperature is
usually 37°C, with relatively wide variations among species.
The genus Streptococcus is comprised of Gram-­positive, catalase-­negative, micro-
aerophilic cocci that are nonmotile and occur in chains or pairs, and in long chains
in broth culture. Cells are normally spherical, ovoid, and less than 2 μm in diameter.
140 Appendix: Details of the Pathogens and Their Diseases

E. faecalis has frequently been found in root canal-­treated teeth in prevalence


values ranging from 30% to 90% of the cases. Root canal-­treated teeth are about
nine times more likely to harbor E. faecalis than cases of primary infections.
E. faecalis can cause endocarditis and bacteremia, urinary tract infections, men-
ingitis, and other infections in humans. Several virulence factors are thought to
contribute to E. faecalis infections. A plasmid-­encoded hemolysin, called the cyto-
lysin, is important for pathogenesis in animal models of infection, and the cytolysin
in combination with high-­level gentamicin resistance is associated with a fivefold
increase in risk of death in human bacteremia patients. A plasmid-­encoded fac-
tor called aggregation substance is also important for virulence in animal models
of infection.
In otherwise-­healthy people, most cases of foodborne Streptococcus infection
are relatively mild. In patients who develop invasive disease (most likely to occur in
people with underlying health issues, such as those who are immunocompromised),
the death rate is estimated at 13%.
Contaminated food is one way you can be infected with Streptococcus, the bacte-
rium that causes it. Streptococcus is not a leading cause of illness from food, but the
illness that it does cause can develop into more serious problems.
Some people infected with foodborne Streptococcus have no symptoms, but those
who do will start to have them in about 1 to 3 days after eating contaminated food.
They may start with red, sore throat (with or without white patches); painful swal-
lowing; high fever; nausea; vomiting; headache; discomfort; and runny nose. The
symptoms usually go away in about 4 days. However, 2 or 3 weeks afterward, some
people develop scarlet fever, which includes a rash, or rheumatic fever, which can
harm the heart and other parts of the body; or, Streptococcus could spread to other
organs and cause serious illness or death. Children 5 to 15 years old and people with
weak immune systems are more likely than others to develop the serious forms of the
illness. Infected food handlers are thought to be the main way food is contaminated
with Streptococcus. In most cases, the food was left at room temperature for too long
a time.
The infectious dose for group A Streptococcus probably is fewer than 1,000
organisms.
Some foodborne Streptococcus group A infections are asymptomatic. Most man-
ifest as pharyngitis (and are commonly referred to as “strep throat”). Although they
may be painful and uncomfortable, they usually are relatively mild. However, the
infection may also result in complications, such as tonsillitis, scarlet fever, rheumatic
fever, and septicemic infections. The symptoms are sore, inflamed throat, on which
there are white patches.
Streptococcus pneumoniae is a bacterium commonly found in the nose and
throat. The bacterium can sometimes cause severe illness in children, the elderly,
and other people with weakened immune systems. Streptococcus pneumoniae is
the most common cause of middle-ear infections, sepsis (blood infection) in chil-
dren, and pneumonia in immunocompromised individuals and the elderly. It can
also cause meningitis (inflammation of the coverings of the brain and spinal cord) or
sinus infections. It is considered invasive when it is found in the blood, spinal fluid,
or other normally sterile sites (sites where it is not commonly found).
Appendix: Details of the Pathogens and Their Diseases 141

Streptococcus pneumoniae causes an acute bacterial infection. The bacterium,


also called pneumococcus, was first isolated by Pasteur in 1881 from the saliva of a
patient with rabies.
Most S. pneumoniae serotypes have been shown to cause serious disease, but only
a few serotypes produce the majority of pneumococcal infections. The 10 most com-
mon serotypes are estimated to account for about 62% of invasive disease worldwide.

Sources
http://en.wikipedia.org/wiki/Enterococcus_faecalis#Pathogenesis
Food and Drug Administration. Bad Bug Book. Foodborne Pathogenic Microorganisms and
Natural Toxins. 2nd ed. Washington, DC: Food and Drug Administration.
Iowa Department of Public Health. http://www.idph.state.ia.us/Cade/DiseaseIndex.aspx​?​­disease​
=Streptococcus%20pneumoniae
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