Special Supplement to the Journal of Food Science

CHAPTER VI
Control of Food Safety Hazards During
Cold-Smoked Fish Processing
MICHAEL L. JAHNCKE ADN DANIEL HERMAN

Scope when it arrives at the smoking facility. On the positive side, farm-

T his section describes a general process of cold smoking fin

fish (see also Appendix A) from the fishing vessel to the con-
sumer. It was not the intention of the panel for this section to be
raised fish that are fed with a controlled diet, such as processed
feed pellets, and reared in closed systems with purified or treat-
ed water have been shown to be free of parasites (Angot and
a Hazard Analysis Critical Control Point (HACCP) plan. This sec- Brasseur 1993). Due to the amount of variation in water quality
tion is limited to the following significant concerns: pathogenic and conditions for farm-raised fish, a processor must consult
bacteria, production of biogenic amines, and parasites. Other with the supplier and not assume that the aquaculture product
chemical or physical hazards are not included. Each step of this is parasite free.
general process is analyzed in terms of identifying potential haz- The quality of the water should be one of the factors that de-
ards, control points, and processing parameters when scientifi- termine the stringency of harvest and postharvest treatments.
cally substantiated. Verification of the processing parameters is Processors of cold-smoked fish should be concerned with the mi-
included in Appendix C. It is beyond the scope of this document crobiological quality of the primary product they receive from
to capture all of the wide variety of cold-smoking methods. suppliers since product from contaminated sources may not be
Therefore, differences from the cold-smoking process described appropriate for production of cold-smoked products. In general,
here may require a different analysis and evaluation. See Ap- good sanitation procedures should be applied throughout har-
pendix D for survey data received from cold-smoked processor vest, transportation, storage, and postharvest handling.
respondents. Appendix B describes some of the most common Transportation of the fish from harvest or processing to the
vessel practices. This chapter addresses some recommendations cold-smoking facility is another area of concern. Fish can be
by the Association of Food and Drug Officials (AFDO 1991). It is transported frozen or refrigerated (typically iced and thus cooled
noteworthy to clarify, however, that although developed by ex- to 0 °C (32 °F). Basic sanitation practices and temperature con-
perts and widely used, these recommendations have not neces- trols need to be in place in transportation vehicles and contain-
sarily been scientifically evaluated. ers. Temperature should be monitored at all times during trans-
portation and storage before processing, especially if the fish is
1. Receiving being frozen to control parasites or belongs to a scombrotoxin-
1.1. Background and support information susceptible fish.
Hazards posed by fish and fish products vary and depend on In the United States, direct treatment of finfish to reduce mi-
the fish environment, both while the fish was alive and after it crobial load is permitted after harvest and before processing.
was caught. For example, a wild-caught, scombrotoxin-suscepti- Chlorine solution dips (Eklund and others 1993), which require
ble fish that has been kept for some time in the water or on a intense management to avoid recontamination, have been re-
boat before being iced or frozen can have elevated toxic levels of placed by chlorine solution rinses or sprays that are followed by a
biogenic amines. Vessel practices would help prevent biogenic rinse with potable water. Although it has been suggested that
amine development in scombrotoxin-susceptible species. Waters rinsing of the fish is important to reduce numbers of pathogenic
where fish are harvested may contain bacteria or spores that may microorganisms, no data on the effect of this procedure could be
be pathogenic to humans (Clostridium botulinum or Listeria found in the scientific literature.
monocytogenes). Fish also may come in contact with pathogenic In summary, efforts directed to reduce or minimize microbial
microorganisms during harvesting, handling on board, and off- load on fish destined for cold smoking must be initiated as early
loading and transportation to a smoking facility. Rinsing wild- in the production cycle as practical. The most critical interven-
caught fish with potable water (not environmental surface water) tions, however, are those directed to prevent growth of specific
may aid in reducing L. monocytogenes in certain areas during cer- bacteria that may eventually lead to health hazards. At all times,
tain seasons. Additionally, wild-caught fish may carry parasites from harvest through receiving, Good Manufacturing Practices
that could be infectious to humans. (GMPs), Good Hygienic Practices (GHPs), appropriate sanitation
Aquaculture provides a year-round supply of fresh fish and a procedures (that is, Sanitation Standard Operating Procedures,
significant amount of raw material for cold-smoked fish proces- [SSOPs]), and control of the product temperature should be ap-
sors. In general, aquaculture has the potential to be a highly con- plied. After harvest, the fish should be cooled as soon as practi-
trolled and hygienic operation at the initial harvesting and han- cally possible and maintained at a temperature below 40 °F
dling step, particularly in the case of salmon. The microbial flora (4.4 °C) until processed. Ideally, fish is stored at 32 °F (0 °C) in
present on aquacultured fish is affected by water quality and ice. The use of temperature-recording devices is highly recom-
feed composition. Water quality can range from that in raceways mended.
or tanks fed by microbe-free spring water, well water, ozone-
treated water, and ultraviolet light-treated water, to that in mud 1.2. Potential hazards
ponds purposely enriched with untreated human or animal Incoming fish may harbor parasites. Scombrotoxin-suscepti-
waste. Hence, regardless of whether a fish has been wild-caught ble fish may have been temperature-abused and contain unsafe
or farm-raised, it may carry various types of pathogenic bacteria levels of biogenic amines. Additionally, fish may be contaminat-

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Processing Parameters Needed to Control Pathogens in Cold-smoked Fish

ed with C. botulinum or L. monocytogenes. Table VI–1. Approximate Safe Shelf Life of Scrombrotoxin-Forming
Species at Various Storage Temperatures (FDA 1998)

1.3. Control point Safe shelf life (d) Safe shelf life (d) with
Product temperature with Rapid C delayed cooling
Receiving is a control point for aquacultured and wild-caught
fish. For scombrotoxin-susceptible fish, receiving is a control 0 °F (–17.8 °C) No limit No limit
32 °F (0 °C) 14 8
point to screen for harmful, unsafe levels of biogenic amines. If 38 °F (3.3 °C) 10 7
the product is received frozen and there are no other freezing 40° F (4.4° C) 7 5
steps in the process, this is a control point for parasites. 50 °F (10 °C) 3 0
70 °F (21.1 °C) 0 0
90 °F (32.2 °C) 0 0
1.4. Processing parameters
If scombrotoxin-susceptible fish are received directly from
the harvest vessel, all lots should be accompanied by documen-
tation certifying proper time and temperature handling of the
fish. Refrigerated scombrotoxin-susceptible fish should be re-
ceived at an internal temperature of 40 °F (4.4 °C) or less. Table point for parasites or there is no other freezing step later in the
VI-1 shows the estimated shelf life of scrombrotoxin-forming process.
species at various storage temperatures. In addition to the time
and temperature parameters, analytical testing for histamines 2.4 Processing parameters
should be done periodically on samples of edible fish flesh (FDA Refrigerated fish should be stored so that their internal tem-
guidance limits the histamine level to 50 ppm). A recent report perature is less than 40 °F (4.4 °C). For freezing, a number of time
on Hawaiian fishery (Kaneko 2000) concluded that odors of de- and temperature combinations have been recommended, such
composition were reliable indicators of biogenic amines risk and as holding the fish at –10 °F (–23 °C) for 60 h, or less than –4 °F (–
that sensory evaluation is an effective monitoring measure. Even 20 °C) for 7 d, or –31 °F (–35 °C) internally for 15 h. For a more de-
though an experienced processor may be doing the evaluation, tailed explanation of freezing regimes, see Chapter V.
sensory analysis is a very subjective and not a quantitative moni-
toring method; therefore, a more objective method (analytical 3. Thawing, washing, and rinsing
method or temperature record) should be in place. Practically, 3.1. Background and support information
most companies use a sensory evaluation of incoming scombro- Thawing frozen raw fish is necessary to process cold-smoked
toxin-susceptible species with a maximum receiving tempera- fish. Many cold-smoked fish processors receive frozen fish, either
ture for refrigerated raw material received. If sensory analysis aquaculture-produced or wild-caught, for processing. Thawed or
points to a high biogenic amine level, analytical testing is per- fresh fish also needs to be thoroughly washed and rinsed after
formed. being received into the plant and then again after being butch-
If product is received frozen to control for parasites, a number ered and processed. For these activities, it is necessary to use
of time and temperature combinations have been recommend- cold, potable, and continuously flowing water.
ed in the United States, such as holding the fish at –10 °F (–
23 °C) for 60 h, or less than –4 °F (–20 °C) for 7 d, or –31 °F (– 3.2. Potential hazards
35 °C) internally for 15 h. For a more detailed explanation of Frozen raw fish should be thawed under sanitary conditions.
freezing regimes, see Chapter V. Although this step is short and one would not anticipate biogenic
amine production or pathogen growth, AFDO guidelines state
2. Fresh or frozen storage that frozen raw material should be thawed under temperature
2.1. Background and support information control (AFDO 1991). This step is not considered to be a control
Before smoking, fish may be stored fresh or frozen. Fresh and point but it should be performed following GMPs and GHPs.
frozen storage areas should be maintained in a clean and sani-
tary manner. Refrigerated fish should be stored so that their in- 4. Butchering and evisceration
ternal temperature minimizes the production of toxic biogenic 4.1. Background and support information
amines and the outgrowth of L. monocytogenes. Frozen storage Butchering and evisceration may occur at the smoking facility
may potentially be a control point for parasites, if there is no oth- or at the supplier’s processing plant before the raw material is
er freezing step in the process. In this case, freezing of fish to the shipped to the smoker. Many cold-smoked fish processors re-
proper internal temperature and for the proper length of time is ceive raw material in the form of fillets or other products that
necessary to kill parasites in the incoming product that would have already been completely or partially processed (eviscerat-
otherwise survive the cold-smoking process. ed, headed, gutted, and skinned). Temperature records are
needed and the product should be checked for cleanliness when
2.2. Potential hazards it is received into the processing facility.
Contamination of the raw material or outgrowth of pathogen- If fish are eviscerated or butchered at the smoking facility,
ic microorganisms may occur if the fish is not maintained in a AFDO guidelines recommend that gutting be performed “with
sanitary facility with proper refrigeration conditions. minimal disturbance of the intestinal tract contents.” The guide-
If the frozen storage is intended to be the step to kill para- lines further recommend that fish should be butchered in a room
sites, and the product is not frozen at the proper temperature for or area that is separate from the rest of the smoking and process-
the proper length of time, parasites may become a hazard in the ing facility. The fish, especially the body cavity, should be
finished product. washed and rinsed thoroughly with potable water after butcher-
ing.
2.3. Control point
If fish are stored under refrigeration, this is a control point for 4.2. Potential hazards
biogenic amines in scombrotoxin-susceptible species. If fish are This step does not present a significant or special potential
stored frozen, this could be a control point for parasites, provid- hazard and consequently is not considered to be a control point.
ed a previous freezing step has not been included as the control Nevertheless, butchering and evisceration should be done

SUPPLEMENT TO VOL. 66, NO. 7, 2001—JOURNAL OF FOOD SCIENCE S-1105

Special Supplement to the Journal of Food Science

promptly and should follow GMPs and GHPs. enough to inhibit the outgrowth and toxin formation of C. botuli-
num in the final product. Brining should be done at a salt con-
5. Washing and rinsing centration that will provide the appropriate concentration in the
See section 3 above. final product (that is, 3.5% WPS in the final product). Acidity
(pH), salt, moisture (water activity), or some combination of
6. Sorting, sizing, and salting these act in combination to inhibit Clostridia outgrowth and toxin
6.1. Background and support information formation. The salt level and refrigerated storage of the final
Salting of fish can be conducted by two different methods, product along with competing microflora can prevent the growth
brining and dry-salting. Brining is the process by which the fish of C. botulinum type E and nonproteolytic types B and F. The
is soaked or steeped (Kassem 1977) in a solution consisting of wa- reader is referred to the C. botulinum section for a review of the
ter, salt, sugar, various spices and flavorings, phosphates, and, scientific literature on this subject.
depending on the recipe and species of fish (allowed in the Unit-
ed States for sable, salmon, shad, chub, and tuna), sodium ni- 6.3. Control point
trite. Brining may also be accomplished by injecting a liquid Salting, including sizing and sorting of the fish, is a control
brine solution, usually with an automated or mechanized system point because the presence of enough salt in the fish is essential
but occasionally by hand, into the fish. In dry salting, fish are to inhibit the outgrowth of Clostridia species and to prevent the
placed directly into a salt mixture usually consisting of some vari- formation of toxins, particularly in vacuum-packaged finished
ation of the previously mentioned ingredients without the water. products. The sizing and sorting step is an integral part of proper
Brining solutions are often referred to as a percent of a totally salting in cold-smoked fish processing. Batches of fish should be
saturated salt solution and may be measured with a salometer or checked going into or being removed from the brine. Portions
other methods. A saturated brine solution is one in which no that are too thick or too large should be removed and cut to the
more salt will dissolve into the water (aqueous phase). A salome- proper size.
ter measures in degrees (100 °S), which can be thought of as
“percent saturation” of the brine solution or directly in % salt. Ta- 6.4. Processing parameters
bles and guides are available for preparing salt brines from the A number of parameters need to be considered when salting.
U.S. Sea Grant Extension Service (Hilderbrand 1973). These include: 1) a minimum salt concentration of the brine so-
Salting should be as uniform as possible, with the correct lution, usually measured at the beginning of salting; 2) a mini-
amount of salt or brine solution absorbed into the fish flesh of mum ratio of brine solution or dry salt mix to fish so that each fish
each piece. To accomplish this, the fish must be sorted by size is adequately exposed to the brine; 3) a minimum salting time to
and thickness and spread out uniformly prior to salting so they allow the salt to adequately and uniformly absorb into the fish;
will absorb the same amount of salt. Eklund pointed out that and 4) a maximum temperature of the salting. A further require-
“even under the best salting conditions, it is nearly impossible to ment is that the fish or fish portions be of a uniform thickness
obtain the predetermined concentration of salt in all samples and size so that in the given amount of time for the batch, all of
even within the same lot of fish” (Eklund 1989). For example, the portions absorb sufficient salt. As mentioned above, extra
when 50 samples from a commercial operation with a target of thick or large pieces in a batch would not be sufficiently salted,
3.5% (WPS) were tested, WPS concentrations of the final product meaning they would not have a high enough salt concentration
ranged from 2.8 % to 6.0 %, with the majority of the samples be- in the final product to inhibit Clostridia growth. Conversely, small
ing above 4.0 %. The inherent variability in this important pro- or thin pieces would be oversalted at the end of this step, com-
cess must be taken into consideration. promising the sensory characteristics. The AFDO guidelines rec-
Proper salting is essential to cold-smoked fish processing for ommend that the temperature of the brine not exceed 60 °F
three reasons: 1) it usually reduces the moisture content of the (15.5 °C) at the beginning of salting. If the salting is longer than 4
fish, affecting both texture and shelf life; 2) it imparts essential h, it is recommended that the salting be done under refrigera-
flavors; and 3) it is important as a preservative and inhibitor of tion.
microbial growth (Kassem 1977). Eklund points out that with The amount of salt, volume of the brine, weight of the fish,
cold-smoked products, the addition of sugars would provide an and duration and temperature of the process should be calculat-
advantage in that the carbohydrate source would “encourage the ed empirically by the processor. All these parameters need to be
growth of lactic acid and other spoilage bacteria and lower of the established with the objective of obtaining a final product with
product pH which can be inhibitory to C. botulinum” in the final at least 3.5% salt concentration in the water phase, if the product
product (Eklund 1989). Other researchers, however, noted that if is to be vacuum-packaged (see Packaging, section 11). No scien-
the product is vacuum-packaged and chilled, very rapid growth tific data specifically address the question of the salt concentra-
of lactic acid bacteria (Carnobacteria spp.) is observed, indepen- tion needed to inhibit C. botulinum toxin formation on air-pack-
dent of addition of carbohydrates (L. Gram 2000; personal com- aged products. Although it is believed that spoilage of aerated
munication; unreferenced). products will act as a safeguard against botulism, not enough sci-
entific evidence supports this idea (see Chapter III).
6.2. Potential hazards
Listeria monocytogenes and C. botulinum spores present on a 7. Rinsing, draining, and preparation
single fish could contaminate an entire batch within the brine so- 7.1. Background and support information
lution. To minimize microbial growth and cross-contamination, The AFDO guidelines recommend rinsing fish with fresh wa-
temperature control of the brine solution during brining is rec- ter after salting. This process, sometimes called “freshening,” in-
ommended, particularly if brining is done for more than a few volves rinsing in cold, potable water for a certain amount of time.
hours. If brine injection is used, needles can get contaminated After the rinse, the fish may be laid on a rack to begin the drying
and spread a pathogen to other fish. Fish may be underbrined if and smoking stage.
the brine solution is too diluted or if the brine soak time is too
short, potentially allowing botulinum toxin formation in the final 7.2. Potential hazards
product. Cross-contamination with pathogens that may be present on
This step is especially important in that WPS needs to be high the fish is unlikely during freshening due to rinsing with potable

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Processing Parameters Needed to Control Pathogens in Cold-smoked Fish

water. Consequently, the freshening step is not considered to be shown to have some inhibitory effect on microorganisms (Storey
a control point. 1982). Research indicates that short-term cold smoking (< 24 h,
as recommended by the AFDO guidelines [AFDO 1991]) causes a
8. Drying and cold smoking reduction rather than an increase in numbers of L. monocytoge-
8.1. Background and support information nes (see Chapter II for a review of this subject).
A number of cold-smoking procedures involve a drying stage Contribution of smoke to the inactivation of pathogens, how-
with no smoke added to the product. This can be considered a ever, is not of significant importance in the overall process (see
separate step or an initial part of the cold-smoking step. The Chapters II and III for a review of the scientific literature). Rath-
product is held at a specific temperature for a specific amount of er, the low temperatures of smoking permit the survival of a sig-
time before the smoke is introduced. The duration and tempera- nificant portion of the natural microbiological flora on the fillets.
ture of this initial drying step constitute the “art” of smoking fish. Several studies have shown that growth of L. monocytogenes in
The parameters that are considered for this initial drying compo- smoked fish is hampered by a high background microflora (Rør-
nent include the type or species of fish, its fat content, and hu- vik and others 1991). It is a common belief that the natural flora
midity. If the humidity is high, the fish will tend to be wetter will spoil the fish prior to botulinum toxin formation in cases of
longer and the drying step must be adjusted accordingly. Smoke temperature abuse of air-packaged or unpackaged cold-smoked
should be applied before a pellicle (dried skin-like layer) forms fish. On the contrary, vacuum packaging or modified atmosphere
on the outside of the fish fillets. If a pellicle forms first, the effec- packaging (MAP) inhibits the growth of the natural flora so the
tiveness of the smoke is markedly reduced. The goal is to have rate of spoilage under temperature-abuse conditions is lower
the surface of the fish portions a little “tacky” so the smoke can and toxin production may occur before spoilage. Consequently,
be absorbed (R. Martin 2000; personal communication; unrefer- relying on the competition from the naturally occurring back-
enced). ground flora or on spoilage organisms to restrict C. botulinum is
There is a variety of literature on the smoking of fish and sea- not a reliable and reproducible method of controlling toxin for-
food products (Gilbert and Knowles 1975; Storey 1982). Variations mation.
include temperature, time, humidity, types of control (from a
thermometer hanging in the smokehouse to sophisticated micro- 8.3. Control point
processor feedback-controlled systems), types of smoke used The cold-smoking step is a control point for C. botulinum
(natural, generated, or liquid), and the design and types of growth and toxin production and for L. monocytogenes growth.
smokehouses or kilns. Usually, fish are laid or arranged uniform- Although cold smoking will not completely eliminate either the
ly (that is, on racks) to prevent contact, ensuring that the por- microorganisms or the spores of concern, inadequate tempera-
tions receive a uniform exposure to the smoke and drying. ture and time control could exacerbate the hazards. Conse-
Traditional smokehouses or kilns allow natural airflow or con- quently, it is important to control the temperature and time dur-
vection, and their use requires a lot of expertise. Modern smoke- ing smoking so that the background microflora is not eliminated.
houses or kilns control the airflow mechanically or electrically.
Many also have refrigeration units; temperature monitors and 9. Cooling
controls; and microprocessor control systems that can regulate 9.1. Background and support information
smoke exposure, humidity, drying, and temperature. This per- Cold-smoked fish products must be rapidly cooled to mini-
mits strict control of the complex smoking operation. Wood smoke mize possible growth of L. monocytogenes and bacteria capable of
can be generated by burning wood or, more commonly, by heat- producing biogenic amines in the products.
ing sawdust or small wood chips. Wood that has been treated
with chemicals or preservatives should not be used for smoking. 9.2. Potential hazards
A wide variety of woods has been used for smoking, including Formation of biogenic amines is possible if scombrotoxin-sus-
oak, hickory, mahogany, pine, whitewood, cherry, apple, alder, ceptible species are used in the cold-smoking process. Also, low
mesquite, beech, birch, and maple to impart various flavors and levels of biogenic amines have been found in nonscombrotoxin-
colors. Some of the “original Scottish processes used smoldering susceptible species such as cold-smoked salmon (Gram and
peat or moss” (Storey 1982). According to some authorities, wood Huss 2000). Formation of amines in cold-smoked fish products
smoke is generally comprised of two components: the visible during vacuum-packed storage may be caused by lactic acid bac-
“tarry droplets” and the invisible gaseous or vaporous compo- teria, which have the ability to form biogenic amines (Leisner
nent (Storey 1982). Chemically, wood smoke contains hundreds and others 1994). The primary amine-producing bacteria are
of compounds, including a number of phenolic substances and species of Enterobacteriaceae, which typically are associated with
volatile acids (Storey 1982; Gilbert and Knowles 1975). Liquid temperature-abuse before packing. Rapid cooling of the product
smoke products, which are produced by condensing the wood is important to reduce the growth rate of bacteria capable of
smoke in some fashion, are generally available. From a culinary forming biogenic amines.
perspective, the purpose of the smoking step in cold-smoked Other potential hazards include pathogen growth and cross
fish processing is to add flavor components and modify the taste contamination of the cold- smoked product with pathogens. List-
and texture of the fish. eria monocytogenes can survive the salting and cold-smoking pro-
cess and will grow at refrigerator temperatures (Ben-Embarak
8.2. Potential hazards and Huss 1992; Hudson and Mott 1993; Rørvik and others 1991).
Cold-smoked fish is defined as a product in which the fish Thus, although complete assurance that L. monocytogenes is ab-
flesh proteins show incomplete coagulation. Practitioners cite a sent from cold-smoked fish products is not possible (Anonymous
range of temperatures as the upper-bound limit of cold smoking, 1995; FAO 1999; Gram and Huss 2000), its numbers on the fin-
but the true defining limit is to leave the fish proteins partially ished product may be kept low by rapid cooling of the cold-
undenatured or uncoagulated. smoked product, following strict GMPs, and implementing and
Although it is natural to assume that the product being adhering to appropriate SSOPs.
smoked gets hot from exposure to the smoke and is thus cooked,
cold smoking is not a cooking step due to the low temperatures 9.3. Control point
involved. In some instances the addition of smoke has been Cooling is a control point for scombrotoxin-susceptible spe-

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Special Supplement to the Journal of Food Science

cies. In addition, proper cooling will prevent or minimize growth sition so it differs from air; and 3) Vacuum Packaging (VAC) re-
of pathogenic bacteria, including L. monocytogenes. moves the air from a package and seals it so a near-perfect vacu-
um remains inside the package. For fatty fish species, packaging
9.4. Processing parameters that excludes oxygen is preferred to prevent rancidity caused by
The AFDO guidelines state that all finished product must be oxidation of lipids.
cooled to a temperature of 50 °F (10 °C) or less within 3 h after The United States seafood industry uses a variety of films
cooking and further cooled to a temperature of 38 °F (3.3 °C) or and packages to protect the product and extend the shelf life of
below within 12 h after cooking. The New York State guidelines cold-smoked fish products. Packaging protects and preserves
are similar to the AFDO guidelines except that the product must foods, providing an additional mechanism for marketing prod-
be cooled to a temperature of 50 °F (10 °C) or less within 5 h after ucts by improving shelf life, convenience, freshness, and quality
cooking (Corby 1991). (Lord 2000). These packaging materials include vacuum bags
It should be noted, however, that these temperature guide- and flexible pouches, vacuum shrink barrier bags and films, vac-
lines are under discussion as to their validity and applicability uum multilayer bags, thermoformed and rollstock laminates, ox-
for the cold-smoked fish processing industry. Additional research ygen-permeable shrink bags, film overwraps, rigid sheeting,
is needed at this step to determine scientifically based tempera- films for semirigid packages, and preformed trays. The types of
ture requirements at the cooling step. packaging and film-permeability characteristics depend on the
intended use and nature of the product. Packages can be de-
10. Slicing and cutting signed to control film permeability to adjust oxygen, carbon diox-
10.1. Background and support information ide, and moisture levels. Such information can be used to help
High priority must be given to the slicing and cutting step to extend product distribution shelf life without odor buildup with-
help control possible recontamination or cross-contamination of in the package.
the cold-smoked fish product with pathogens. Clean, sanitary Other parameters being equal, gas permeability characteris-
food contact surfaces are essential. A processor should have well tics of the film will determine the microflora that survives in a
designed and comprehensive SSOPs and must follow GMPs to packaged product. Therefore, gas permeability is an important
control contamination of the cold-smoked fish product at this parameter and should be taken into account when doing re-
step. The development and verification of effective sanitation search and making decisions on food safety issues. Specifica-
and cleaning programs will help reduce the prevalence of L. tions for gas permeability, however, are product- and use-specific
monocytogenes on the slicing and cutting equipment and in the and are usually established at ambient temperatures under
general processing environment. Such programs will help reduce moderate humidity conditions (that is, 23 °C and 50% R.H.) us-
contamination of the cold-smoked fish product. Recent studies ing a variety of testing and verification methods. These various
have shown that one potential source of L. monocytogenes in testing conditions make it difficult to compare gas transmission
cold-smoked salmon is the slicer, where specific DNA types can rates between films. In addition, film permeability rates also
occupy a niche for extended periods of time (Fonnesbech Vogel, change when the film is stretched or when it contacts the prod-
Ojeniyi, Ahrens and others 2001). uct. Data are also limited on gas-transmission rates of films at
As Eklund and others (1993, 1995) suggested, in addition, to product-chill temperatures (Robertson 1993).
inactivating the bacterium on the incoming raw product and in-
hibiting growth of survivors in the final product, processors 11.1.1. Pathogens
should strictly follow GMPs to prevent recontamination of L. Temperatures used in the preparation of cold-smoked fish
monocytogenes during processing. Because the source of L. are inadequate to eliminate C. botulinum spores; thus, other
monocytogenes may be other than the incoming product, follow- controls such as temperature and NaCl must be included to en-
ing GMPs is currently the most important measure to minimize L. sure its safety. Numerous studies address the formation of botu-
monocytogenes presence in the final product. lism toxin under vacuum. A few of the studies are done with
fresh, hot-smoked fish and cold-smoked fish.
10.2. Potential hazards Eklund (1992) conducted studies on growth of C. botulinum
Potential hazards during slicing and cutting include possible and subsequent toxin formation in hot-smoked fish packaged in
cross-contamination of the cold-smoked product with pathogens an oxygen-permeable film (1.5 ml polyethylene; oxygen trans-
such as L. monocytogenes. mission 7195 cc/m2/24 h at 760 mm Hg 23 ° C and 0% R.H.; CO2
transmission 22858 cc/m2/24 h) and under vacuum in an oxy-
10.3. Control point gen-impermeable film (108 cc/m2/24 h; CO2 transmission 526
The slicing and cutting step is not a control point but is an ex- cc/m2/24 h) (Table VI-2). He reported that higher concentrations
tremely important processing operation. Strict adherence to of NaCl were required to inhibit toxin formation by C. botulinum
SSOPs and GMPs to control cross contamination of product with in O2-impermeable films compared with O2-permeable films.
pathogens is essential; in particular, effective SSOPs can be used In addition, under temperature-abuse conditions, toxin for-
to minimize or prevent cross-contamination with L. monocytoge- mation can occur in VAC- or MAP-products before or at the same
nes. time as spoilage (Eklund 1992). Although the studies were con-
ducted at 25 °C (77 °F), Eklund reported that concentrations of
11. Packaging and labeling NaCl, the combination of NaCl and nitrite, or other preservatives
11.1. Background and support information needed to inhibit C. botulinum were similar for growth and toxin
Reduced Oxygen Packaging (ROP) is defined as any packag- formation at 25 °C (77 °F) as at 10 °C (50 °F). Toxin formation,
ing procedure that results in a reduced oxygen level in a sealed however, was dramatically delayed at 10 °C compared with 25 °C.
package (FDA 1999). Furthermore, the Food Code defines the We should emphasize, though, that these studies were per-
following: 1) Controlled Atmosphere Packaging (CAP) is the formed on hot-smoked fish, which are different microbiologically
packaging of a product in a modified atmosphere followed by from cold-smoked fish.
maintaining subsequent control of that atmosphere; 2) Modified Dufresne and others (2000) recently completed studies on
Atmosphere Packaging (MAP) is the packaging of a product in an the effect of packaging film permeability and storage tempera-
atmosphere that had a one-time modification of gaseous compo- tures on C. botulinum type E growth and toxin formation in cold-

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Processing Parameters Needed to Control Pathogens in Cold-smoked Fish
Table VI-2. Toxin production by Clostridium botulinum type E (103 Table VI-3. Challenge studies with Clostridium botulinum type E
spores/100 g) in hot-process whitefish steaks vacuum-packaged in spores (102/g) on cold-smoked trout fillets with 1.7% NaCl (WPS)
O2-permeable (7195 cc/m2/24 h), or O2-impermeable (108 cc/m2/24 h) packaged in films of different oxygen transmission rates and stored
films (adapted from Eklund 1992) at 4 °C
Quantity of C. botulinum toxin Oxygen trans-
formed (MLD50/g) mission rate Sensory shelf
cc/m2/d/atm life1 based Nr of toxic samples at
Storage time, Water phase Oxygen- Oxygen- @ 24 °C, 0% R.H. on odor (d) each sampling interval (d) 2
d at 25 °C salt (%) permeable film impermeable film
7 14 21 28
3 1.8 50 2500
2.6 0 500 12 ~28 0 0 0 0
3.4 0 5 2950 ~28 0 0 0 0
4920 ~22 0 0 0 0
5 1.8 250 50000 10040 ~18 0 0 0 0
2.8 0 2500
1 Time (d) to reach a score of 3.5 on a hedonic scale of 1 to 7. (7 = Extremely desirable, 1 =
3.5 0 0
Extremely undesirable)
2 Trypsinized extract (in duplicate)
7 1.8 2500 50000
2.8 0 5000 Dufresne and others 2000
3.5 0 50
Table VI-4. Challenge studies with Clostridium. botulinum type E
spores (102/g) on cold-smoked trout fillets with 1.7% NaCl (WPS),
packaged in films of different oxygen transmission rates and stored
at 8 °C

smoked and hot-smoked trout products. Summaries of her find- Oxygen trans-
mission rate Sensory shelf
ings on cold-smoked fish are contained in Tables VI–3–5. cc/m2/d/atm life1 based Nr of toxic samples at
In Dufresne’s studies, product shelf life for cold-smoked trout @ 24 °C, 0% R.H. on odor (d) each sampling interval (d) 2
ranged from 18 to 28 d at storage temperatures of 4 °C (39 °F) 7 14 21 28
with no toxin formed in any sample (Table VI–3). At 8 °C (46 °F) 12 ~14 0 0 0 0
(Table VI–4), cold-smoked trout packaged in films with oxygen 2950 ~13 0 0 0 0
transmission rate (OTR) of 10040 cc/m 2/24 h spoiled at 6 d of 4920 ~16 0 0 0 1
storage, and toxin formation occurred at 28 d of storage. Spoilage 10040 ~6 0 0 0 1
1 Time (d) to reach a score of 3.5 on a hedonic scale of 1 to 7. (7 = Extremely desirable, 1 =
occurred at 16 d, and toxigenisis occurred by 28 d in cold-smoked Extremely undesirable)
trout packaged in films with OTRs of 4920cc/m2/24 h (Dufresne 2 Trypsinized extract (in duplicate)
Dufresne and others 2000
and others 2000). Spoilage of products packaged in films with
OTRs of 12 and 2950 cc/m2/24 h occurred at 13 to 14 d, but there
Table VI-5. Challenge studies with Clostridium botulinum type E
was no toxin formation by 28 d of storage. It should be empha- spores (102/g) on cold-smoked trout fillets with 1.7% NaCl (WPS),
sized that packages with high OTRs were toxic after 28 d, whereas packaged in films of different oxygen transmission rates and stored
packages with low OTRs were not toxic. at 12 °C
At 12 °C (54 °F) (Table VI–5), spoilage in smoked trout pack- Oxygen trans-
aged in film with OTRs of 12, 2950, and 4920 cc/m2/24 h occurred mission rate Sensory shelf
between 11 and 12 d with toxin formation by 14 d of storage. cc/m2/d/atm life1 based Nr of toxic samples at
@ 24 °C, 0% R.H. on odor (d) each sampling interval (d) 2
Cold-smoked trout packaged in films with an OTR of 10040
cc/m2/24 h spoiled at 6 d of storage, and toxin formation occurred 7 14 21 28
by 14 d of storage (Dufresne and others 2000). From Dufresne’s 12 ~11 0 1 2 1
2950 ~12 0 1 2 2
data it would seem that at abuse temperatures (8 to 12 °C) spoil- 4920 ~11 0 1 2 2
age may proceed toxin production, particularly when packaged 10040 ~6 0 1 2 2
in high O2 permeable films. Spoilage may help prevent the con- 1 Time (d) to reach a score of 3.5 on a hedonic scale of 1 to 7. (7 = Extremely desirable, 1 =
sumption of toxic fish, but it cannot be relied upon solely as a Extremely undesirable)
2 Trypsinized extract (in duplicate)
control to prevent foodborne botulism. Dufresne and others 2000
These studies illustrate the need for additional research to
identify the processing conditions and characteristics that must
be present for a product to be considered air-packaged. Results
from these studies suggest that film with OTRs of 7195 cc/m2/24
h or greater could be considered air-packaged. Additional re- um nitrite (NaNO2) could be used to inhibit L. monocytogenes in
search on O2 and CO2 film permeability characteristics is needed cold-smoked fish. Pelroy and others (1994b) reported that
to better define these parameters. Nevertheless, storage of NaNO2 enhanced the inhibitory effect of NaCl on L. monocytoge-
smoked trout at 4 °C or 8 °C or less resulted in no toxin formation nes at refrigeration temperatures, when the inoculum was low
prior to spoilage in the cold-smoked product, regardless of film and the storage temperature was 5 °C. This inhibitory effect de-
OTRs (Dufresne and others 2000; Eklund 1984, 1992). creased as the storage temperature increased to 10 °C and the
Listeria monocytogenes is another pathogen of concern in cold- inoculum level increased. These results emphasized the impor-
smoked fish. Studies indicate that L. monocytogenes grows well tance of reducing or eliminating L. monocytogenes and adequate
on the finished cold-smoked product at refrigerated tempera- refrigeration during all stages of storage or cold-smoked fish
tures (Farber 1991). Peterson and others (1993) reported that products.
vacuum-packaging initially suppressed growth of L. monocytoge-
nes by 10 to 100 fold in samples with 3% or 5% WPS. Neither 3% 11.1.2. U.S. packaging and labeling requirements
nor 5% water-phase salt by itself, however, sufficed to prevent The botulism outbreaks from hot-smoked fish during the
the growth of L. monocytogenes in vacuum-packaged or O2-per- 1960s were caused by a combination of inadequate processing of
meable film-packaged, cold-processed salmon during prolonged the products, WPS concentration in most cases less than 1%, and
storage at 5 °C (41 °F) or 10 °C (50 °F). The authors suggested gross temperature-abuse during distribution (Eklund 1992). It is
that in addition to NaCl, other inhibitors such as smoke and sodi- interesting to note that although WPS guidelines are part of state

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Special Supplement to the Journal of Food Science

regulations in New York, Michigan, and Minnesota, current U.S. bel information is also important in reducing the growth rate of L.
HACCP guidelines do not recommend specific WPS concentra- monocytogenes, although temperature will not prevent its
tions for cold-smoked fish. growth. A warning label for populations at high risk of developing
Current AFDO guidelines (followed by New York, Michigan, listeriosis may be considered for cold-smoked fish and other
and Minnesota) recommend that cold-smoked products contain ready-to eat foods in the risk category. Such a label could indi-
a WPS level of at least 2.5% for air-packaged fish; or a minimum cate that these products may constitute a health hazard to im-
WPS level of 3.5% for vacuum- or modified atmosphere-pack- munocompromised individuals and pregnant women.
aged fish; or a combination of at least 3% WPS and a nitrite level
of 100 to 200 ppm. Each container of processed fish must contain 11.4. Processing parameters
identification indicating where the product was packaged, the All finished products should be labeled to advise on refrigera-
year and day packed, and the period during which the product tion temperatures and storage time. This panel concluded that,
was packaged. Packing codes shall be changed with sufficient with the appropriate salt concentrations (that is, 3.5% WPS), the
frequency to allow identification of lots during sale and distribu- product should be refrigerated at 40 °F (4.4 °C) or less for no
tion. The label should also state the need for refrigerated storage more than 5 wk (for a detailed discussion on this subject, see the
(AFDO 1991). As mentioned in the scope section of this chapter, Chapter III). This would mean the final product needs to main-
although developed by experts and widely used, these recom- tain that temperature during storage, distribution, retail, and
mendations have not necessarily been scientifically evaluated. home storage and that the recommended maximum time from
Adequate refrigeration is the most important factor for the safe manufacture to consumption is 5 wk. Frozen product must also
distribution of smoked fish products and has been recommend- be labeled to indicate that the “product shall remain frozen until
ed in multiple occasions (Eklund 1992; Eklund and others 1982; it is thawed at refrigeration temperatures.”
Eklund and others 1988; Pelroy and others 1982).
12. Storage and distribution
11.1.3. Canadian packaging and labeling 12.1. Background and support information
requirements Cold-smoked fish products can be stored refrigerated or fro-
The Canadian document “Food and Drugs Act and Regula- zen. Companies may freeze and hold the product in frozen stor-
tions” states under Division 21 (B.21.025.) that no person shall age for 1 to 2 wk prior to distribution and shipment. This is done
sell marine and fresh water animals, or marine and fresh water primarily for inventory control. Other companies simply refriger-
animal products, that are packed in a container that has been ate products and distribute and ship them as soon as possible. In
sealed to exclude air and that are smoked or to which liquid addition, cold-smoked products are also distributed via over-
smoke or flavour or liquid smoke flavour concentrate has been night carriers and government postal services.
added, unless (a) the container has been heat-processed after Kalish (1991) conducted audits of temperature readings at
sealing at a temperature and for a time sufficient to destroy all more than 50 major warehouses and distribution centers. She re-
spores of the species Clostridium botulinum; (b) the contents of ported that most warehouses and distribution centers main-
the container contain not less than nine percent salt, as deter- tained refrigeration temperatures within the recommended tem-
mined by official method PO-38, Determination of Salt in perature range (0 to 3.3 °C, 32 to 38 °F), although a few (number
Smoked Fish, dated March 15, 1985; (c) the contents of the con- not specified) were as high as 10 °C (50 °F). The rotation of prod-
tainer are customarily cooked before eating; or (d) the contents uct in warehouses and distribution centers was good (Kalish
of the container are frozen and the principle display panel of the 1991).
label of the container carries the statement “Keep Frozen Prior to
Use” in the same size types used for the common name of the 12.2. Potential hazards
contents of the container (Health Canada 1994). Potential hazards during refrigerated storage and distribu-
The Canadian government, however, allows refrigerated stor- tion include pathogens such as L. monocytogenes or C. botulinum
age of smoked products if they are packaged in containers with and botulin toxin formation on the finished product. In addition,
an oxygen permeability equal to or greater than 2000-cc/m2/24 h biogenic amine formation is possible if scombrotoxin forming
at 24 °C at 1 atm. These products must also be stored at 4 °C or species are used for the cold-smoking process. Frozen storage is
less and should have a label that states shelf life must not exceed not considered a control point, since pathogens will not grow and
14 d from the date of packaging. Processors and retailers should biogenic amine will not form during storage.
record the type of film used and its permeability characteristics
(Health Canada 1994). 12.3. Control point
Both storage and distribution are control points for biogenic
11.2. Potential hazards amine formation in both aerobic-packaged and ROP cold-
Hazards that may arise from the time of final product manu- smoked scombrotoxin susceptible species. Storage and distribu-
facture to the time of consumption within the product packaging tion are also control point for C. botulinum growth and toxin for-
include growth of pathogens such as L. monocytogenes or C. botu- mation in cold-smoked products. Although chill temperature
linum and production of botulin toxin on the finished product. In during storage and distribution will also reduce the growth rate
addition, biogenic amine formation is possible if scombrotoxin- of L. monocytogenes, it will not prevent its growth.
susceptible species are used for the cold-smoking process.
12.4. Processing parameters
11.3. Control point Cold-smoked fish should be stored and distributed at storage
The packaging and labeling step is not considered a control temperatures of less than 40 °F (4.4 °C) or frozen. Studies indi-
point, since it is not possible to label safety into a product. Never- cate that storage at 4 °C (39 °F) or less resulted in no botulin toxin
theless, label information identifying appropriate storage tem- formation prior to spoilage in cold-smoked products at salt levels
peratures and time for safety is critical to control biogenic amine of 1.7% WPS (Dufresne and others 2000) (for a more detailed dis-
formation in scombrotoxin-susceptible species, as well as C. bot- cussion see Chapter III). Those temperatures will also reduce the
ulinum growth and toxin formation in cold-smoked products, es- growth of scombrotoxin forming species and of L. monocytogenes.
pecially if packaged in a reduced-oxygen environment. This la- Frozen storage and distribution is not considered a control point,

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Processing Parameters Needed to Control Pathogens in Cold-smoked Fish

as pathogens will not grow and biogenic amines will not form monly reported food preparation practice that contributed to
during frozen storage. foodborne disease was improper holding temperature; the sec-
ond most commonly reported practice was inadequate cooking
13 Retail of food (MMWR 2000).
13.1. Background and support information Beard (1991) reported that out of 14 home refrigerators and
The Food Code provides criteria that must be met by the 11 freezers, only 7 refrigerators and 1 freezer had thermometers.
HACCP plans of operators that handle ROP products (FDA 1999). Refrigerator temperatures ranged from 0 to 13 °C (32 to 55 °F).
(Note: the Food Code is a voluntary recommendation from the The panel recommends labeling frozen products with thawing
FDA and is not codified in all states). The Food Code prohibits instructions and storing the thawed product below 40 °F (4.4 ° C).
products from being packaged in ROP at the retail level and re-
quires maintenance of adequate refrigeration during the entire 14.2. Potential hazards
shelf life of the product. Nevertheless, temperature-abuse does Potential hazards at its consumer stage include pathogens
occur during retail storage. Studies have shown that at the retail such as L. monocytogenes or C. botulinum, or botulin toxin forma-
level, product rotation procedures were inadequate, as sales of tion on the finished product. In addition, biogenic amine forma-
product dictated product rotation frequency (Kalish 1991). tion is possible if scombrotoxin susceptible species are used for
Approximately 2000 retail stores, including back-room storage the cold-smoking process.
facilities and chill cases, were checked. Kalish reported that only
37% of refrigerated foods were stored within the 32 to 38 °F (0 to 14.3. Control point
3.3 °C) range. Products were also found stacked on the floor with- The refrigerator of the consumer is a control point to control
out any refrigeration, and the temperature of many refrigerated biogenic amine formation in both air-packaged and ROP cold-
cases was 44 °F (6.7 °C) with some as high as 56 °F (13.3 °C) (Kal- smoked scombrotoxin-susceptible species and to control C. botu-
ish 1991). linum growth and toxin formation in cold-smoked products. Low
temperature will also reduce the rate of growth of L. monocytoge-
13.2. Potential hazards nes, although it will not prevent its growth.
Potential hazards during all retail operations include patho-
gens such as L. monocytogenes or C. botulinum on the finished 14.4. Processing parameters
product. In addition, biogenic amine formation is possible if Cold-smoked fish should be stored at storage temperatures
scombrotoxin-susceptible species are used for the cold-smoking of < 40 °F (4.4 °C). Studies indicate that storage at 4 °C or less re-
process. sulted in no botulin toxin formation prior to spoilage in cold-
smoked products at salt levels of 1.7% WPS (Dufresne and others
13.3. Control point 2000) (for a more detailed discussion see section 11 of this chap-
Temperature and time control at all retail operations are con- ter and Chapter III). Those temperatures will also reduce the
trol points to control biogenic amine formation in both air-pack- growth of scombrotoxin-forming species and L. monocytogenes.
aged and ROP cold-smoked scombrotoxin-susceptible species
and to control C. botulinum growth and toxin formation in cold- References
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