Barbosa et al.

, J Vet Sci Med Diagn 2017, 6:4

DOI: 10.4172/2325-9590.1000237 Journal of
Veterinary Science &
Medical Diagnosis
Research Article a SciTechnol journal

management system. In this context, it is common to find between 5

Identification of and 10 species of helminths and high levels of infection in free-range
reared pigs [1-3]. However, in “technified” and industrial pig farming
Macracanthorhynchus systems, this scenario is no longer observed due to the adoption of a

Hirudinaceus, Stephanurus series of preventive hygienic-health measures [4,5].

Brazil is the fourth largest producer and exporter of pork in the
Dentatus and Trichuris Suis in world [6]; however, the production of pigs in free-range systems is still
a common reality in rural and riverine areas of the country, especially
Native Pigs on Marajó Island in specific ecosystems such as the Mato Grosso and Mato Grosso do
José Diomedes Barbosa1*, Jenevaldo Barbosa da Silva2,
Sul Pantanal regions, the Maranhão lowlands and Marajó Island. Pigs
Alessandra dos Santos Belo Reis1, Henrique dos Anjos raised in free-range systems in the country are generally managed
Bomjardim1, David Driemeier3, Felipe Masiero Salvarani1, Cairo without the use of anthelmintics, food supplementation, vaccination
Henrique Sousa de Oliveira4, Carlos Magno Chaves Oliveira1, or routine veterinary medical follow-up, in a purely extractive system.
Marilene de Farias Brito5 Thus, although the epidemiology of the major diseases in these pigs is
not known, high levels of helminth infection are expected at all stages
of production.
Abstract
The objective of this work was to describe the necropsy findings
Technification of pig farming in recent decades has led to a
significant reduction in the occurrence of helminth parasitism.
and to identify the main species of helminths and the microscopic
However, the production of pigs in free-range systems is still a changes caused by helminths in pigs farmed in an extensive
common reality in rural areas of Brazil, such as Marajó Island, in the production system on Marajó Island, State of Pará, Brazil.
State of Pará, a Brazilian Amazonian biome. Therefore, the present
work describes the main parasitological and anatomopathological Materials and Methods
findings of six pigs in a sample of 23, of different age groups,
A clinical examination of 23 pigs of both sexes, ranging from
raised under free-range conditions on native pastures on Marajó
Island. During slaughter, the presence of Stephanurus dentatus in five months to two years of age, was conducted extensively on native
the ureters and renal pelvis, Macracanthorhynchus hirudinaceus pastures, belonging to small properties located in the municipality of
in the small intestine and Trichuris suis in the cecum and colon Cachoeira do Arari, Marajó Island, State of Pará, Brazil. Data on the
was detected in these six pigs. The histopathology results showed nutritional status, origin and clinical history of all pigs were organized
different types of lesions, including mild granulomatous infiltrates in individual records.
in the lymph nodes, granulomatous inflammation and brown
pigment in the tonsils, hyperkeratosis in the esophagus and non- Of the 23 pigs in the sample, six were slaughtered by the property
glandular stomach, lung with dark pigment in the bronchioles and owners, in the places of origin, for household consumption. For the
intra-alveolar macrophages, as well as squamous metaplasia of the study, the animals were identified as one to six, being five females (four
peribronchial glands, hemosiderosis in the spleen, liver with marked two-year-old pigs and one six-month-old pig) and a seven-month-old
extramedullary hematopoiesis, mild hepatitis and abscess caused male pig. From the six pigs, fragments of injured organs were collected
by parasitic migration with eosinophils, intestinal edema and and fixed in 10% formalin and then sent for histopathological analysis
neuronal lipofuscinosis in the spinal cord. From these findings, it can in the Veterinary Pathology Sector of the Federal University of Rio
be inferred that free-range pigs on Marajó Island are susceptible to
Grande do Sul. Endoparasites were collected and stored in individual
helminths, reflecting the high degree of environmental contamination
in which these animals are reared, and that such ecosystems can
labeled jars with 70% ethanol fixative solution for later classification
function as reservoirs of these agents. Helminth infections lead to at the Veterinary Medicine Institute of the Federal University of Pará.
losses in pig farming in the Amazon biome, showing the importance The parasite load was classified as absent, mild, moderate or
of the strategic control of these parasites.
marked, according to the number of parasites found. The same
Keywords: criterion was adopted to classify the intensity of the macroscopic
findings, according to the severity of the lesions, as absent, mild,
Helminths; Pig farming; Amazon; Parasitism; Pathology
moderate or marked.

Introduction Results
High occurrence and intensity of gastrointestinal helminth The pigs evaluated according to the history provided by the farmers
infection has been a strong trend in pig herds kept under a traditional were raised in a free-range system (Figures 1 and 2), together with other
animal species (cattle, horses, buffalo, sheep and chickens), without
adequate nutritional and health management, and had never received
*Corresponding author: José Diomedes Barbosa Neto, Instituto de Medicina
treatment against ecto and endoparasites or mineral supplementation.
Veterinária, Campus de Castanhal, Universidade Federal do Pará, Rodovia BR-
316 km 61, 68741-740, Castanhal, PA, Brazil, Telephone: +9137211686 ; Fax: The animals fed on carcasses, insects and native grass. Clinical
+9137211686; E-mail: diomedes@ufpa.br examination showed retarded growth and poor nutritional status. The
Received: August 23, 2017 Accepted: September 08, 2017 Published: two young pigs that were slaughtered were found mired next to puddles
September 12, 2017 of still water, with obvious weakness and malnutrition.

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Technology and Medicine
Citation: Barbosa JD, Silva JB, Reis ASB, Bomjardim HA, Driemeier D, et al. (2017) Identification of Macracanthorhynchus Hirudinaceus, Stephanurus
Dentatus and Trichuris Suis in Native Pigs on Marajó Island. J Vet Sci Med Diagn 6:4.

doi: 10.4172/2325-9590.1000237

Macroscopic alterations were observed, such as small areas of

calcification in the lung, nodules adjacent to the ureters, bladder and
kidneys, which presented a whitish caseous mass when sectioned

Table 1: Parasite load in slaughtered pigs on Marajó Island, Pará.

Identification S. dentatus M. hirudinaceus T. suis
Pig 1 +++ +++ ++
Pig 2 ++ - ++
Pig 3 ++ - -
Pig 4 - ++ -
Pig 5 +++ ++ -
Pig 6 - - ++
Parasite load: absent = -, mild = +, moderate = ++, marked = +++

Table 2: Macroscopic findings in slaughtered pigs on Marajó Island, Pará.

Identification S. dentatus M. hirudinaceus T. suis
Figure 1: Native pigs, reared on a free-range system on Marajó Island, Pig 1 +++ ++ -
Pará, with parasitic infection and poor nutritional status. Pig 2 ++ - -
Pig 3 ++ - -
Pig 4 - ++ -
Pig 5 +++ + -
Pig 6 - - -
Lesion: absent = -, mild = +, moderate = ++, marked = +++

Figure 2: Native pigs with parasitic infection and poor nutritional status,
reared on a free-range system on Marajó Island, Pará, found mired.

Tables 1 and 2 describe the parasite load and macroscopic Figure 3: Macracanthorhynchus hirudinaceus infection nodules (arrows) in
findings of the six pigs from a sample of 23 animals from Marajó the intestinal serosa, also called “blackberry spots”.
Island.
At slaughtering, it was observed that 50% (3/6) of the animals
(Pigs 1, 4 and 5) had small nodules in the serosa of the small intestine
(Figure 3) and that the mesenteric lymph nodes were enlarged. In the
intestinal lumens of the same pigs, 30 helminths on average, with sizes
ranging from 2 to 30 cm in length, were found attached to the mucosa
(Figures 3-5), and the nodules found in the serosa coincided with
the point of proboscis attachment of the parasitic worms. In some
segments of the small intestine, dilatation and partial obstruction of
the intestine (Figure 6) were observed due to infestation of worms
in the lumen; this parasite was identified as Macracanthorhynchus
hirudinaceus (Figures 3 and 6).
Additionally, during the necropsy analysis, a high parasite load
of Stephanurus dentatus nematodes on the ureters and renal pelvis
(Figures 7 and 8) was observed in 66.6% (4/6) of the animals (Pigs
1, 2, 3 and 5). Abscesses were observed on the ureter wall (Figure 9), Figure 4: Macracanthorhynchus hirudinaceus with proboscis attached
renal pelvis (Figure 10), renal capsule, bladder, liver and lung. One of to the mucosa of the small intestine, with a thick, long and transversely
wrinkled body.
the animals (Pig 5) presented lesions caused by parasitic migration.

Volume 6 • Issue 4 • 1000237 • Page 2 of 5 •

Citation: Barbosa JD, Silva JB, Reis ASB, Bomjardim HA, Driemeier D, et al. (2017) Identification of Macracanthorhynchus Hirudinaceus, Stephanurus
Dentatus and Trichuris Suis in Native Pigs on Marajó Island. J Vet Sci Med Diagn 6:4.

doi: 10.4172/2325-9590.1000237

The main histopathological findings of pigs with M. hirudinaceus

were edema and mixed infiltrate in the small intestine mucosa and
lymph nodes with mild macrophage infiltrate. In the pigs with
Stephanurus dentatus, ureter with nematodes, abscess in the wall
of the ureter, cystic area in the adrenal gland and abscesses in the
kidneys were observed. In the liver, mild, moderate and marked
hepatocellular swelling, abscess caused by parasitic migration
with eosinophils, marked extramedullary hematopoiesis and mild
hepatitis were observed. In the tonsils, lymphoid hyperplasia, the

Figure 5: Details of Figure 4 and evidence of the fixation of the proboscis

of the parasites to the mucosa of the small intestine.

Figure 8: Specimens of Stephanurus dentatus.

Figure 6: Several worms attached to the mucosa, causing dilatation and

partial obstruction of the small intestine

Figure 9: Abscess in the lumen of the pig ureter.

Figure 7: Presence of nematodes in the renal pelvis of the pig.

(Figures 9 and 10), liver slightly yellow with small abscesses, edema
in the mucous membranes of the stomach and intestine, enlarged
mesenteric lymph nodes, abscesses in the renal capsule, and a whitish
mass near the kidney and renal pelvis.
Trichuris suis was found in the cecum and colon of 50% (3/6) of
the animals (Pigs 1, 2 and 6). There were no significant macroscopic
lesions related to this parasite, and the histopathological findings
of the pigs with Trichuris suis were restricted to mild edema in the
large intestine, with mixed infiltrate in the mucosa, macrophages and
hemosiderin.
Table 3 shows the histopathological lesions observed in each of
the six animals sampled on Marajó Island, with lesions detected in
Figure 10: Abscess in the renal pelvis of the pig.
various organs and tissues.

Volume 6 • Issue 4 • 1000237 • Page 3 of 5 •

Citation: Barbosa JD, Silva JB, Reis ASB, Bomjardim HA, Driemeier D, et al. (2017) Identification of Macracanthorhynchus Hirudinaceus, Stephanurus
Dentatus and Trichuris Suis in Native Pigs on Marajó Island. J Vet Sci Med Diagn 6:4.

doi: 10.4172/2325-9590.1000237

Table 3: Histological findings in pigs slaughtered on Marajó Island, Pará.

Identification Description of the main lesions observed under microscopy
Liver with mild hepatocellular swelling, tonsils with lymphoid hyperplasia and macrophages with dark pigment, ureter with parasites and formation
Pig 1 of abscess; mild edema in the submucosa of the large intestine. Small intestine, glandular stomach, heart, brain, cerebellum and lung without
histopathological changes.
Submucosal edema and mixed infiltrate in the large intestine, mild macrophage infiltration in the lymph nodes, liver with moderate hepatocellular
Pig 2
swelling. Duodenum, heart, kidney, lung, brain, cerebellum, spinal cord and spleen without histopathological changes.
Mild granulomatous infiltrate in the lymph nodes, hyperkeratosis in the non-glandular stomach, large intestine with mixed infiltrate in the mucosa, with
mild edema, macrophages and hemosiderin; ureter with nematodes, cystic area in the adrenal gland, granulomatous inflammation area and brown
Pig 3 pigment in the tonsils, neuronal lipofuscinosis in the spinal cord, hemosiderosis in the spleen, lung with dark pigment in the bronchioles and intra-
alveolar macrophages. Glandular stomach, thyroid, bladder, small intestine, cerebral cortex, esophagus, kidney, heart, liver and pancreas without
histopathological changes.
Lung with hypertrophy of muscles of bronchioles, nematode parasites in bronchial lumen, squamous metaplasia of peribronchial glands; liver with
marked extramedullary hematopoiesis, mild hepatitis and abscess caused by parasitic migration with eosinophils; lymph nodes with mild macrophage
Pig 4
infiltration in follicular centers, with microabscesses and granulomatous infiltrate. Cerebellum, brain, heart, tonsil, adrenal, glandular stomach and
kidneys without histopathological changes.
Abscess on the wall of the ureter; macrophages with dark pigment and microabscesses in the tonsils; abscess with large numbers of eosinophils and
Pig 5 marked hepatocellular swelling in the liver; abscess in the kidney; spleen with hemosiderosis. Adrenal, pancreas, lung, brain, cerebellum, salivary
gland, duodenum, small intestine and bladder without histopathological changes.
Edema in the large intestine, mild hyperkeratosis in the esophagus, macrophage infiltrate in the small intestine mucosa, hydropic degeneration with
Pig 6 inclusion body and neutrophil infiltrate in the non-glandular stomach, hemosiderosis in the spleen, microabscess in the tonsil. Heart, kidney, brain and
spinal cord without histopathological changes.

presence of macrophages with dark pigment, microabscesses, areas of infective larvae and act as intermediate hosts. Swine are infected when
granulomatous inflammation and brown pigment were observed. In they ingest an infected larva or beetle. The attachment of the larva to
the lymph nodes, mild macrophage infiltrate with microabscesses and the wall of the small intestine produces nodules that are also called
mild granulomatous infiltrate occurred. In the lungs, dark pigment in “blackberry spots”. Severe infestations by M. hirudinaceus decelerate
the bronchioles and intra-alveolar macrophages, bronchial muscle growth and cause weight loss [9,10], as observed in the animals in this
hypertrophy, parasites in the bronchial lumen, squamous metaplasia study, which had poor nutritional status. Infections can also result in
of the peribronchial glands, hemosiderosis in the spleen and neuronal perforation of the intestinal wall and peritonitis [9-11]. On Marajó
lipofuscinosis in the spinal cord were observed. Island, adverse environmental conditions, such as floods where land
is flooded and muddy, and food shortages are other factors that may
Discussion have contributed to animal weight loss and may also have increased
The results of the present work show the challenges that proliferation and transmission of the parasite by ingestion of the
helminths pose to small producers who raise free-range pigs. beetle that transmits that helminth. High parasite loads of these
Although pig helminths are rare in industrial farms today, this helminths can be observed in periods of high temperature, especially
disease still causes severe losses in family farms in various tropical in tropical and subtropical regions, a condition compatible with that
regions [7]. The macroscopic and histopathological findings of this of the Marajó Island biome. According to Radostits et al. [9] and
study described pigs with a high helminth parasite load, a fact that is Souza et al. [10], nodules in the serosa of the small intestine, known
not commonly observed in other regions of the world, even those in as “blackberry spots”, are common findings in necropsies of pigs
which pigs are reared in an intensive free-range system (SISCAL). In infested with M. hirudinaceus; these nodules occur due to the fixation
the present study, the helminths found were Stephanurus dentatus, of the spiny rings of the helminth proboscis in the intestinal mucosa.
Macracanthorhynchus hirudinaceus and Trichuris suis. Histological examination revealed edema and mixed infiltrate in the
mucosa of the small intestine, findings similar to those of Souza et
The industrialization of Brazilian pig production in the last decades al. [10]. Stephanurus dentatus, of the Stephanuridae family, is a stout
has limited the occurrence of most species of helminths; however, pig parasite that is approximately 2 mm by 40 mm long, found in the
production in free-range systems, which are more rustic, without any hepatic, renal and perirenal tissues, axial musculature and spinal
hygienic-health and food control, is still a common reality in rural canal of pigs and, sometimes, cattle. The buccal cavity is cup-shaped
areas of Brazil. This is especially true in biomes such as Marajó Island, and is directed straightforward, with 6 to 10 triangular teeth at its
the Maranhão lowlands and the Mato Grosso and Mato Grosso do base. The gut is convoluted, the spicules are equal and short, and the
Sul Pantanal regions. According to Costa et al. [8], this parasitic bursa is reduced [12]. This parasite is a problem in countries with a
disease is not common in “technified” production systems and occurs hot climate [13]. The evolutionary cycle may be direct or may involve
only in animals raised in SISCAL or extensive production systems, as worms as facultative intermediate hosts. Infection occurs by ingestion
on Marajó Island. or skin penetration of third-stage larvae or by oral ingestion of
Macracanthorhynchus hirudinaceus is a round acanthocephalan infected worms that act as paratenic hosts [12]. Stephanurus dentatus
parasite with a body and a proboscis formed by retractile spiny is a less prevalent helminth because it has a long life cycle and its cycle
rings by which it attaches to the wall of the small intestine of its has been disrupted by the industrialization of pig production in most
host; its evolutionary cycle is indirect. The worm has a thick, long of the world. This helminth has a prepatent period ranging from nine
and transversely wrinkled body and no digestive tract; nutrients are to 16 months. A large number of eggs are eliminated along with the
absorbed through the integument. Males measure approximately urine. In the environment, third-stage infective larvae may develop
10 cm, and females are up to 35 cm in length; females release within a few days. Marajó Island has the peculiarity of presenting
numerous highly resistant, long-lasting eggs that are infective to high temperatures and large marsh areas for a long period of the year,
pigs only after development for two to three months inside beetles. which may represent an ecological benefit for maintenance of the
The coprophagous beetles of the Scarabaeidae family are carriers of parasite in the environment because the paratenic host, earthworms

Volume 6 • Issue 4 • 1000237 • Page 4 of 5 •

Citation: Barbosa JD, Silva JB, Reis ASB, Bomjardim HA, Driemeier D, et al. (2017) Identification of Macracanthorhynchus Hirudinaceus, Stephanurus
Dentatus and Trichuris Suis in Native Pigs on Marajó Island. J Vet Sci Med Diagn 6:4.

doi: 10.4172/2325-9590.1000237

have affinity for moist soils. The macroscopic findings observed in the Acknowledgements
pigs of the present study are in agreement with those of Bowman et al. We thank the Coordination for the Improvement of Higher Level of Education
[12], who reported the formation of abscesses in the liver due to the Personnel (CAPES) foundation and the National Council of Technological and
erratic, destructive migration of the larvae of Stephanurus dentatus to Scientific Development (CNPq) for their financial support.
this organ, which the larvae migrate through for four to nine months. References
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9. Bowman DD (2010) Georgis – Parasitologia veterinária. Rio de Janeiro.
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Conclusions 13. Mcgavin MD (2009) Zachary J. F. Bases da Patologia em Veterinária. (4th

edn), Elsevier, Netherlands.
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on Marajó Island, are generally managed without the use of
15. Larsen MN, Roepstorff A (1999) Seasonal variation in development and
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16. Grant Maxie (2016) Jubb, Kennedy & Palmer’s Pathology of Domestic
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anthelmintics available on the market, these environments function
as a genetic reservoir of sensitive worms. Thus, in the near future,
with the spread of anti-helminth resistance throughout the world,
these areas will become refuges of sensitive worms for studies and Author Affiliation Top
tests of anthelmintics that work in populations of animals still non- 1
Instituto de Medicina Veterinária, Campus de Castanhal, Universidade
resistant. Thus, it is necessary to know the occurrence of the main Federal do Pará, Rodovia BR-316 km 61, 68741-740, Castanhal, PA, Brazil
helminths in these regions of Brazil to formulate adequate control 2
Instituto de Ciências Agrárias, Universidade Federal dos Vales do
strategies. In this type of parasitism, control strategies for free-range Jequitinhonha e Mucuri, Avenida Vereador João Narciso 1380, 38610-000,
pigs should be based on the adoption of management techniques that Unaí, MG, Brazil
aim to interrupt the helminth cycle, which are aided by the strategic- Escola de Medicina Veterinária da Universidade Federal do Rio Grande do
3

tactical use of anthelmintics. Sul, Av. Bento Gonçalves 9090, Porto Alegre, RS, Brazil
Setor de Medicina Veterinária Preventiva, Escola de Veterinária e Zootecnia,
4

Conflict of interest statement Universidade Federal de Goiás, Campus Samambaia 74690900, Goiânia,
GO, Brazil
None of the authors of this work has a financial or personal relationship
with other people or organizations that could inappropriately influence or bias the
5
Instituto de Medicina Veterinária, Universidade Federal Rural de Rio de
content of the paper. Janeiro, Br 465, Km 7, 23890-000, Seropédica, RJ, Brazil

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