Anaerobe 33 (2015) 14e17

Contents lists available at ScienceDirect

Anaerobe
journal homepage: www.elsevier.com/locate/anaerobe

Mini-review

Clostridium perfringens: A review of enteric diseases in dogs, cats and

wild animals

vio Silveira Silva*, Francisco Carlos Faria Lobato
Rodrigo Ota
^nio Carlos Avenue, 6627, 31 270-901 Belo Horizonte, MG, Brazil
Veterinary School, Universidade Federal de Minas Gerais (UFMG), Anto

a r t i c l e i n f o a b s t r a c t

Article history: Clostridium perfringens is a gram-positive anaerobic bacillus that is commonly part of the microbiota of
Received 21 July 2014 humans and animals. It is considered a common enteric pathogen, but the pathogenesis and the pre-
Received in revised form disposing factors of the disease commonly differ between host species. Thus, specific research is
18 January 2015
necessary to understand the role of this pathogen, how to diagnose it, and which control measures are
Accepted 21 January 2015
Available online 30 January 2015
applicable. The aim of this paper is to review the current knowledge of C. perfringens infections in dogs,
cats and wild animals.
© 2015 Elsevier Ltd. All rights reserved.
Keywords:
Diarrhea
Canine
Cats
Feline
Dogs
Enteritis

1. Introduction we review the most recent advances in the understanding of

C. perfringens enteric disease in dogs, cats and wild species.
Clostridia produce the highest number of toxins of any type of
bacteria. Among Clostridium species, Clostridium perfringens is the
2. Dogs and cats
largest toxin producer and also the most widespread, being found
as part of the microbiota of animals and humans and in the soil.
The role of C. perfringens type A as an enteropathogen in dogs
This bacterium is a gram-positive anaerobic bacillus that is classi-
and cats is not fully understood, but it is suspected to be associated
fied into five types according to the production of four major toxins:
with anything from mild, self-limiting diarrhea to rapidly fatal
alpha (a), beta (b), epsilon (ε) and iota (i). In addition to the major
necrohemorrhagic enteritis [7e14]. Most studies indicate that
toxins, it can produce more than 15 other known toxins. Some of
C. perfringens is a primary enteropathogen, but some authors also
these additional virulence factors, including enterotoxin, necrotic
suggest that it could act as an opportunistic agent in dogs and cats.
enteritis B-like toxin (NetB) and beta-2 toxin, have received more
Disruption of the normal microbiota, such as a sudden change to a
attention than others due to their role in the pathogenesis of
high protein diet, or enteric infection by other pathogens, such as
C. perfringens-associated disease (CPAD) in humans and animals
parvovirus, are considered predisposing factors [15,16].
[1,2].
C. perfringens type A is the most common genotype in dogs and cats,
C. perfringens is recognized as one of the most important causes
and 10e30% of the isolated strains are also positive for beta-2 toxin
of foodborne disease in humans, and it is also commonly involved
gene (cpb2). The enterotoxin gene (cpe) is also common in canine
in human and animal cases of gas gangrene [3,4]. In veterinary
and feline C. perfringens strains. No reports of strains positive for
medicine, C. perfringens is responsible for several, mostly enteric,
necrotic enteritis-like B toxin gene (netB) from cats and dogs have
diseases. In the last few years, significant progress in the under-
been published [17].
standing of C. perfringens in animals has been achieved [5,6]. Here,
In addition to type A, it is believed that C. perfringens type C can
also be responsible for acute fatal hemorrhagic enteritis in dogs and
cats; however, there have been no case reports in the literature
* Corresponding author. until now [10].
E-mail address: rodrigo.otaviosilva@gmail.com (R.O.S. Silva). Diagnosis of C. perfringens type A-associated diarrhea in dogs is

http://dx.doi.org/10.1016/j.anaerobe.2015.01.006
1075-9964/© 2015 Elsevier Ltd. All rights reserved.
 R.O.S. Silva, F.C.F. Lobato / Anaerobe 33 (2015) 14e17
very difficult because the clinical signs cannot be differentiated
from enteritis caused by other enteropathogens. Additionally,
C. perfringens type A is a normal inhabitant of the canine intestine,
so isolation of this microorganism is not diagnostic [17]. A corre-
lation between the presence of CPE in feces and diarrhea in recent
studies suggests that the detection of this toxin in stool samples
could be useful to diagnose CPAD in dogs [10,11,18]. However, the
specificity and sensitivity of most enzyme immunoassays (EIA) for
the detection of CPE in dog stool samples is unknown [10].
Isolation of the bacteria followed by detection of the enterotoxin
gene (cpe) by PCR was also suggested and supported by studies that
reported that detection of cpe is correlated with the occurrence of
diarrhea in dogs [8,11,19]. In summary, (1) despite this commonly
reported association, there is no confirmatory study about the role
of the enterotoxin of C. perfringens in dogs; (2) both enterotoxin and
isolates positive for the cpe gene can be found in healthy dogs, so
these methods could suggest that C. perfringens is involved, but
they are not confirmatory. A more robust diagnosis could be ach-
ieved by the exclusion of other potential enteropathogens and the
detection of enterotoxin followed by the isolation of a cpe-positive
C. perfringens strain [10]. In addition, if death occurs, visualization
of a large number of clostridia-like bacilli on the mucosal surfaces
and associated with the lesions could add more confidence to the
final diagnosis of CPAD [14,20,21].
It is important to note that, in contrast with dogs, studies have
failed to show an association between diarrhea and the detection of
enterotoxin in stool samples or detection of cpe in C. perfringens
strains isolated from cats [16,22]. Thus, the diagnosis should be
based only on the isolation of C. perfringens (positive or negative for
cpe) in conjunction with the absence of other enteropathogens.
A presumptive diagnosis of C. perfringens type C diarrhea can be
determined by the association of clinical signs (bloody diarrhea,
commonly in young animals) with isolation of the agent, which is
not commonly part of the feline microbiota. A confirmatory diag-
nosis would require the detection of beta toxin in stool samples or
in intestinal contents [10].
The most commonly recommended drugs for the treatment of
C. perfringens infection in dogs are metronidazole and tylosin,
although amoxicillin, tetracycline, erythromycin and cephalexin
are also used. Studies regarding the susceptibility of C. perfringens
isolates from dogs showed that most C. perfringens isolates are
strongly susceptible to metronidazole, but resistance to macrolides
and tetracyclines is common [23,24].
Future studies might focus on the pathogenesis and diagnosis of
C. perfringens infection in dogs. Despite the known association
between diarrheic dogs and detection of enterotoxin or cpe in
C. perfringens isolates, few studies, such as those employing animal
models or examining molecular differences among canine
C. perfringens cpe positive strains, have been conducted to under-
stand the true role of this toxin in canine diarrhea.
3. Wild animals
Knowledge about C. perfringens as a cause of enteric disease in
wild animals is extremely limited mainly because of the difficulty in
accessing fecal samples from these species, which makes studies of
diseased and healthy animals rare. Another complicating factor is
that most accessible animals are in captivity, which might interfere
directly with the microbiota composition. Thus, for most wild
species, knowledge is limited to a few case reports, and the role of
this microorganism as a pathogen or even as part of the normal
microbiota is still poorly understood.
There are reports of single cases or outbreaks of necrotic en-
teritis (NE) caused by C. perfringens type A with elevated mortality
in several wild avian species such as swans, capercaillies, white
15
storks, crows, geese, western bluebirds, lories, lorikeets, and
bobwhite quail [25e33]. C. perfringens type C was also reported but
seems to be uncommon [34]. The lesions are similar to those
described for NE in poultry, including confluent mucosal necrosis
restricted to the small intestine along with hepatitis and chol-
angiohepatitis. In addition to the common macroscopic lesions, the
diagnosis is made by an association between histology, isolation of
C. perfringens type A and the absence of other enteropathogens
[26,30,35].
The main predisposing factors are not well understood for wild
avian species and, in contrast with broiler chicken, coccidian
infection is not commonly associated with NE in most reports
[25e34]. It is also important to note that the netB gene, which has
been associated with NE in broiler chickens, has not been detected
in C. perfringens isolates from wild avian species to date. Similar to
broiler chickens, the beta-2 toxin gene (cpb2) and enterotoxin (cpe)
can be found, but these genes do not seem important for the
pathogenesis of NE in wild avian species [36].
In contrast with domestic avian species, it seems that
C. perfringens is not commonly isolated from healthy wild birds.
Silva et al. [36] reported an isolation rate of 5.6% in a study of
Ramphastidae, Tinamidae and Cracidae species in Brazil, raising the
hypothesis that C. perfringens might not be part of the normal
microbiota in these species. However, there are marked anatomical
differences in the intestinal tract and also in the habits of each avian
species, and therefore, specific studies are needed to better un-
derstand the role of this bacterium in wild avian species.
Regarding wild carnivores, C. perfringens type A is commonly
isolated from healthy animals, and the strains can also be positive
for cpb2 and cpe genes [37]. However, as there was no balance
between diarrheic and healthy animals, no conclusions could be
made regarding the importance of these additional virulence fac-
tors in C. perfringens isolated from wild carnivore species. Recently,
Zhang et al. [38] reported the death of a Siberian tiger (Panthera
tigris altaica) and a lion (Panthera leo) due to hemorrhagic entero-
colitis associated with C. perfringens type A. Both developed
depression, anorexia and bloody diarrhea, which quickly led to
death. Neither the cpe nor cbp2 genes were found in the
C. perfringens isolates from the animals. A similar case was also
reported in an Amur tiger (Panthera pardus orientalis) by Neiffer
[39]; however, in addition to the isolation of the microorganism,
the authors also detected the enterotoxin in its feces. In both re-
ports, the source of infection and the predisposing factors were not
confirmed, but the authors suggested that the supply of partially
thawed chicken meat could have contributed to the development of
disease in these three animals [38,39].
Another interesting recent report in wild felines is a suspected
case of neurotoxicity due to C. perfringens type B in a tiger (P. tigris)
[40]. In this case, the tiger was referred with acute onset of severe
abnormal consciousness with a suspected diffuse forebrain lesion.
C. perfringens type B was found in high numbers in the feces in the
absence of other infections, vascular lesions or metabolic abnor-
malities. The animal recovered after antibiotic therapy against the
C. perfringens infection.
C. perfringens type A cpb2-positive strains were also reported to
be associated with cases of necrotic and hemorrhagic enteritis in
Asiatic black bears (Selenarctos thibetanus) and pygmy hogs (Sus
salvanius) in Italy and India, respectively [41,42]. In both cases, the
animals developed acute hemorrhagic enteritis, which led to death.
Cpb2-positive C. perfringens type A was obtained from the intestine
in the absence of other enteropathogens. C. perfringens type A
infection was also reported in ferrets suggested as one of the most
common causes of death in free-living seals (Phoca vitulina) in
Germany, but there is limited data about the predisposing factors or
laboratory diagnosis in these two reports [43,44]. In simians, in
16 R.O.S. Silva, F.C.F. Lobato / Anaerobe 33 (2015) 14e17
addition to case reports [46], there are some studies showing that
this microorganism could be responsible for foodborne diarrhea
and acute gastric dilatation in these animals [46,47]. Anyway,
similar to almost all wild species, there is no recognized method to
differentiate C perfringens strains that are causing infection from
strains that are only part of the microbiota. In light of this, the
diagnostic is still based in an association between histological le-
sions, isolation of C. perfringens and absence of other enter-
opathogens [45,48].
There are a few case reports of C. perfringens type C infection in
wild species. Carvalho et al. [49] reported an outbreak in four young
captive collared (Pecari tajacu) and three white-lipped (Tayassu
pecari) peccaries in Brazil. The animals showed lethargy and
inappetence followed by sudden death within 24 h of the beginning
of clinical signs. In addition to typical post mortem findings and
isolation of C. perfringens type C, the diagnosis was confirmed by
detection of beta-toxin from the intestinal contents. The authors
suggested that the ingestion of a feed containing sweet potato was
an important predisposing factor in this outbreak [49]. Sweet po-
tato is a potent trypsin inhibitor, and it is well known as a predis-
posing factor of type C infection in humans [50].
There are few reports about the antimicrobial susceptibility of
C. perfringens isolates from wild animals. In studies with isolates
from wild carnivores and wild avian species, Silva et al. [36,37]
reported that these isolates were widely susceptible to florfenicol,
metronidazole, penicillin and vancomycin, but some strains were
resistant to erythromycin, tylosin and oxytetracycline.
Conflict of interest
The authors declare that they have no conflicts of interest.
Acknowledgments
This work was supported by funds from Fapemig, Capes, CNPq,
INCT and PRPq-UFMG.
References
[1] W.H. Welch, G.H.F. Nuttall, A gas producing bacillus (Bacillus aerogenes cap-
sulatus, Nov. Spec.) capable of rapid development in the blood vessels after
death, Bull. Johns Hopkins Bull. 1982 3 (1892) 81e91.
[2] M.R. Popoff, P. Bouvet, Genetic characteristics of toxigenic Clostridia and toxin
gene evolution, Toxicon 75 (2013) 63e89.
[3] F.A. Uzal, J.G. Songer, Diagnosis of Clostridium perfringens intestinal infections
in sheep and goats, J. Vet. Diag. Invest. 20 (2008) 253e265.
[4] D. Taylor, Clostridial infections, in: B.E. Straw, S. D'Allaire, W.L. Mengeling,
D. Taylor (Eds.), Diseases of Swine, Iowa State University Press, Ames, IA, 1999,
pp. 395e412.
[5] K. Miyamoto, J. Li, B.A. McClane, Enterotoxigenic Clostridium perfringens:
detection and identification, Microbes Environ. 27 (2012) 343e349.
[6] F.A. Uzal, J.C. Freedman, A. Shrestha, J.R. Theoret, J. Garcia, M.M. Awad,
V. Adams, R.J. Moore, J.I. Rood, B.A. McClane, Towards an understanding of the
role of Clostridium perfringens toxins in human and animal disease, Future
Microbiol. 9 (2014) 361e377.
[7] M.R. Goldstein, S.A. Kruth, A.M. Bersenas, M.K. Holowaychuk, J.S. Weese,
Detection and characterization of Clostridium perfringens in the feces of
healthy and diarrheic dogs, Can. J. Vet. Res. 76 (2012) 161e165.
[8] R.O.S. Silva, R.L.R. Santos, P.S. Pires, L.C. Pereira, S.T. Pereira, M.C. Duarte,
R.A. Assis, F.C.F. Lobato, Detection of toxins A/B and isolation of Clostridium
difficile and Clostridium perfringens from dogs in Brazil, Braz. J. Microbiol. 44
(2013) 133e137.
[9] S.M. el-Sanousi, M.O. el-Shazly, A. al-Dughyem, A.A. Gameel, An outbreak of
enterotoxaemia in cats, Zentralbl. Veterinarmed. B 39 (1992) 403e409.
[10] J.S. Weese, Bacterial enteritis in dogs and cats: diagnosis, therapy, and zoo-
notic potential, Vet. Clin. North Am. Small Anim. Pract. 41 (2011) 287e309.
[11] J.S. Weese, H.R. Staempfli, J.F. Prescott, S.A. Kruth, S.J. Greenwood, H.E. Weese,
The roles of Clostridium difficile and enterotoxigenic Clostridium perfringens in
diarrhea in dogs, J. Vet. Intern. Med. 15 (2001) 374e378.
[12] J.S. Weese, S.J. Greenwood, H.R. Staempfli, Recurrent diarrhea associated with
enterotoxigenic Clostridium perfringens in 2 dogs, Can. Vet. J. 42 (2001)
292e294.
[13] S. Unterer, K. Busch, M. Leipig, W. Hermanns, G. Wolf, R.K. Straubinger,
R.S. Mueller, K. Hartmann, Endoscopically visualized lesions, histologic find-
ings, and bacterial invasion in the gastrointestinal mucosa of dogs with acute
hemorrhagic diarrhea syndrome, J. Vet. Intern. Med. 28 (2014) 52e58.
[14] B.J. Schlegel, T. Van Dreumel, D. Slavi
c, J.F. Prescott, Clostridium perfringens
type A fatal acute hemorrhagic gastroenteritis in a dog, Can. Vet. J. 53 (2012)
555e557.
[15] J. Turk, W. Fales, M. Miller, L. Pace, J. Fischer, G. Johnson, J. Kreeger,
S. Turnquist, L. Pittman, A. Rottinghaus, Enteric Clostridium perfringens infec-
tion associated with parvoviral enteritis in dogs: 74 cases (1987e1990), J. Am.
Vet. Med. Assoc. 200 (1992) 991e994.
[16] S.J. Sabshin, J.K. Levy, T. Tupler, S.J. Tucker, E.C. Greiner, C.M. Leutenegger,
Enteropathogens identified in cats entering a Florida animal shelter with
normal feces or diarrhea, J. Am. Vet. Med. Assoc. 241 (2012) 331e337.
[17] J.S. Suchodolski, M.E. Markel, J.F. Garcia-Mazcorro, S. Unterer, R.M. Heilmann,
S.E. Dowd, P. Kachroo, I. Ivanov, Y. Minamoto, E.M. Dillman, J.M. Steiner,
A.K. Cook, L. Toresson, The fecal microbiome in dogs with acute diarrhea and
idiopathic inflammatory bowel disease, PLoS One 7 (2012) e51907.
[18] S.L. Marks, E.J. Kather, P.H. Kass, A.C. Melli, Genotypic and phenotypic char-
acterization of Clostridium perfringens and Clostridium difficile in diarrheic and
healthy dogs, J. Vet. Intern. Med. 16 (2002) 533e540.
[19] T. Tupler, J.K. Levy, S.J. Sabshin, S.J. Tucker, E.C. Greiner, C.M. Leutenegger,
Enteropathogens identified in dogs entering a Florida animal shelter with
normal feces or diarrhea, J. Am. Vet. Med. Assoc. 241 (2012) 338e343.
[20] J.F. Prescott, J.A. Johnson, J.M. Patterson, W.S. Bulmer, Haemorrhagic gastro-
enteritis in the dog associated with Clostridium welchii, Vet. Rec. 103 (1978)
116e117.
[21] J. Sasaki, M. Goryo, M. Asahina, M. Makara, S. Shishido, K. Okada, Hemorrhagic
enteritis associated with Clostridium perfringens type A in a dog, J. Vet. Med.
Sci. 61 (1999) 175e177.
[22] E.V. Queen, S.L. Marks, T.B. Farver, Prevalence of selected bacterial and para-
sitic agents in feces from diarrheic and healthy control cats from Northern
California, J. Vet. Intern. Med. 26 (2012) 54e60.
[23] S.L. Marks, E.J. Kather, Antimicrobial susceptibilities of canine Clostridium
difficile and Clostridium perfringens isolates to commonly utilized antimicro-
bial drugs, Vet. Microbiol. 94 (2003 Jun 24) 39e45.
[24] S. Gobeli, C. Berset, I. Burgener, V. Perreten, Antimicrobial susceptibility of
canine Clostridium perfringens strains from Switzerland, Schweiz Arch. Tier-
heilkd 154 (2012) 247e250.
[25] H.L. Shivaprasad, F. Uzal, R. Kokka, D.J. Fisher, B.A. McClane, A.G. Songer, Ul-
cerative enteritis-like disease associated with Clostridium perfringens type A in
bobwhite quail (Colinus virginianus), Avian Dis. 52 (2008) 635e640.
[26] G. Wobeser, D.J. Rainnie, Epizootic necrotic enteritis in wild geese, J. Wildl.
Dis. 23 (1987) 376e385.
[27] Y. Asaoka, T. Yanai, H. Hirayama, Y. Une, E. Saito, H. Sakai, M. Goryo,
H. Fukushi, T. Masegi, Fatal necrotic enteritis associated with Clostridium
perfringens in wild crows (Corvus macrorhynchos), Avian Pathol. 33 (2004)
19e24.
[28] D. O'Toole, K. Mills, R. Ellis, R. Farr, M. Davis, Clostridial enteritis in red lories
(Eos bornea), J. Vet. Diag. Invest 5 (1993) 111e113.
[29] G. Stuve, M. Hofshagen, G. Holt, Necrotizing lesions in the intestine, gizzard,
and liver in captive capercaillies (Tetrao urogallus) associated with Clostridium
perfringens, J. Wildl. Dis. 28 (1992) 598e602.
[30] M. Pizarro, U. Ho € fle, A. Rodríguez-Bertos, M. Gonza
lez-Huecas, M. Castan ~ o,
Ulcerative enteritis (quail disease) in lories, Avian Dis. 49 (4) (2005) 606e608.
[31] G. Pritchard, H. Ainsworth, M. Brown, J.P. Duff, Suspected necrotic enteritis in
wild swans, Vet. Rec. 154 (2004) 480, 10.
[32] P. Boujon, M. Henzi, J.-H. Penseyres, L. Belloy, Enterotoxaemia involving b2-
toxigenic Clostridium perfringens in a white stork (Ciconia ciconia), Veteri-
nary Rec. 156 (23) (2005) 746e747.
[33] R.J.1 Bildfell, E.K. Eltzroth, J.G. Songer, Enteritis as a cause of mortality in the
western bluebird (Sialia mexicana), Avian Dis. 45 (2001) 760e763.
[34] S. McOrist, R.L. Reece, Clostridial enteritis in free-living lorikeets (Tricho-
glossus spp.), Avian Pathol. 21 (1992) 503e507.
[35] K.K. Cooper, J.G. Songer, F.A. Uzal, Diagnosing clostridial enteric disease in
poultry, J. Vet. Diag. Invest 25 (2013) 314e327.
[36] R.O.S. Silva, C.A. Oliveira Junior, F.C. Ferreira Junior, M.V.R. Marques,
N.R.S. Martins, F.C.F. Lobato, Genotyping and antimicrobial susceptibility of
Clostridium perfringens isolated from Tinamidae, Cracidae and Ramphastidae
species in Brazil, Cie ^ncia Rural. 44 (2014) 486e491.
[37] R.O.S. Silva, E.P.T. Teixeira, M.L. D'Elia, F.C.F. Lobato, Clostridium difficile and
C. perfringens from wild carnivore species in Brazil, Anaerobe 28 (2014)
207e211.
[38] Y. Zhang, Z. Hou, J. Ma, Hemorrhagic enterocolitis and death in two felines
(Panthera tigris altaica and Panthera leo) associated with Clostridium per-
fringens type A, J. Zoo. Wildl. Med. 43 (2012) 394e396.
[39] D.L. Neiffer, Clostridium perfringens enterotoxicosis in two Amur leopards
(Panthera pardus orientalis), J. Zoo. Wildl. Med. 32 (2001) 134e135.
[40] O. Zeira, C. Briola, M. Konar, M.P. Dumas, M.A. Wrzosek, V. Papa, Suspected
neurotoxicity due to Clostridium perfringens type B in a tiger (Panthera tigris),
J. Zoo. Wildl. Med. 43 (2012) 666e669.
[41] G. Greco, A. Madio, V. Martella, M. Campolo, M. Corrente, D. Buonavoglia,
C. Buonavoglia, Enterotoxemia associated with beta2 toxin-producing Clos-
tridium perfringens type A in two Asiatic black bears (Selenarctos thibetanus),
J. Vet. Diag. Invest. 17 (2005) 186e189.
[42] B.R. Shome, R. Shome, K.M. Bujarbaruah, A. Das, H. Rahman, G.D. Sharma,
 R.O.S. Silva, F.C.F. Lobato / Anaerobe 33 (2015) 14e17
B.K. Dutta, Investigation of haemorrhagic enteritis in pygmy hogs (Sus sal-
vanius) from India, Rev. Sci. Techno. 29 (2010) 687e693.
[43] U. Siebert, P. Wohlsein, K. Lehnert, W. Baumga €rtner, Pathological findings in
harbour seals (Phoca vitulina): 1996-2005, J. Comp. Pathol. 137 (2007) 47e58.
[44] F.Y.1 Schulman, R.J. Montali, P.J. Hauer, Gastroenteritis associated with Clos-
tridium perfringens type A in black-footed ferrets (Mustela nigripes), Vet.
Pathol. 30 (1993) 308e310.
[45] G.N. Nikolaou, M.J. Kik, A.J. van Asten, A. Gro € ne, Beta2-toxin of Clostridium
perfringens in a hamadryas baboon (Papio hamadryas) with enteritis, J. Zoo.
Wildl. Med. 40 (2009) 806e808.
[46] T. Uemura, G. Sakaguchi, T. Ito, K. Okazawa, S. Sakai, Experimental diarrhea in
cynomolgus monkeys by oral administration with Clostridium perfringens type
A viable cells or enterotoxin, Jpn. J. Med. Sci. Biol. 28 (1975) 165e177.
17
[47] Z.K. Stasilevich, E.K. Dzhikidze, V.A. Kalashnikova, O.A. Sultanova, Role of
anaerobic bacteria in simian enteric diseases, Bull. Exp. Biol. Med. 156 (2013)
248e251.
[48] B.T. Bennett, L. Cuasay, T.J. Welsh, F.Z. Beluhan, L. Schofield, Acute gastric
dilatation in monkeys: a microbiologic study of gastric contents, blood and
feed, Lab. Anim. Sci. 30 (1980) 241e244.
[49] M.A. de Carvalho, P.S. Santos, S.S. Nogueira, F. Lessa, A. Almeida Vdos,
N.F. Leça-Júnior, F.M. Salvarani, F.C. Lobato, S.L. Nogueira-Filho, Necrotic en-
teritis in collared (Pecari tajacu) and white-lipped (Tayassu pecari) peccaries,
J. Zoo. Wildl. Med. 42 (2011) 732e734.
[50] G. Lawrence, The pathogenesis of pig-bel in Papua New Guinea, P. N. G. Med. J.
48 (1979) 39e49.