Suggested Citation: Siqueira, L. R.; Martins-Panizzutti, M.H.; Muniz-Pereira, L.C.; Magalhães-Pinto, R. 2009. Macro lesiones
inducidas por nematodos de Bothrops jararaca y Bothrops alternatus en brasil con dos nuevos registros.
Neotropical Helminthology, vol. 3, nº 1, pp. 29-34.
Resumen
Palabras clave: Bothrops spp. - Brasil - Nematodos - Patologia - Serpientes.
Resultados de exámenes de heces han sido comparados a los obtenidos durante necropsias de serpientes
infectadas con helmintos. Muestras de heces de ejemplares de Bothrops jararaca e B. alternatus fueron
investigadas y tres animales fueron positivos para huevos durante los exámenes: un caso representando
parásitos autóctonos de serpientes, otro relativo a especies introducidas accidentalmente junto con ratones
naturalmente infectados que son ofrecidos como alimentación para las serpientes y otro con la asociación de
ambos. Resultados de las necropsias de los mismos ejemplares indican la presencia de los nematodos
Ophidascaris travassosi Vaz, 1938, Kalicephalus costatus (Rudolphi, 1819), K. inermis Molin, 1861,
Kalicephalus sp. y Acanthorhabdias acanthorhabdias Pereira, 1927. Las especies Bothrops jararaca es un
nuevo registro de huésped para Ophidascaris travassosi y Bothrops alternatus para A. acanthorhabdias; los
resultados con relación a lesiones macroscópicas inducidas por los nematodos son presentados.
Key words: Bothrops spp. - Brazil - Nematodes - Pathology - Snakes.
Abstract
Results of fecal examinations have been compared with those obtained during necropsies of snakes infected
with helminths. Stool samples from specimens of Bothrops jararaca and B. alternatus were investigated and
three animals were positive for eggs during coprological screenings: one case representing authochtonous
snake parasites, other related to species accidentally introduced together with naturally infected mice snakes
fed on, and another with the association of both. Necropsies of those same specimens, showed the presence of
the nematodes Ophidascaris travassosi Vaz, 1938, Kalicephalus costatus (Rudolphi, 1819), K. inermis
Molin, 1861, Kalicephalus sp. and Acanthorhabdias acanthorhabdias Pereira, 1927. Bothrops jararaca is a
new host record for O. travassosi and Bothrops alternatus for A. acanthorhabdias; the gross pathological
lesions induced by the nematodes are reported.
1Laboratório de Helmintos Parasitos de Vertebrados, Departamento de Helmintologia, Instituto Oswaldo Cruz, Av. Brasil, 4365, 21045-900 Rio
de Janeiro, Rio de Janeiro, Brasil.
2Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) fellowship
3Instituto de Biologia do Exército (IBEx), Rua Francisco Manuel, 102, 20911-270, Rio de Janeiro, RJ
4 Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) research fellow
Neotrop. Helminthol., 3(1), 2009
2009 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
29
GROSS LESIONS INDUCED BY NEMATODES OF BOTHROPS JARARACA AND
BOTHROPS ALTERNATUS IN BRAZIL WITH TWO NEW RECORDS
MACRO LESIONES INDUCIDAS POR NEMATODOS DE BOTHROPS JARARACA Y
BOTHROPS ALTERNATUS EN BRASIL CON DOS NUEVOS REGISTROS
1,2, 3 1 1, 4*
Liege Renata Siqueira Marcia Helena Martins Panizzutti , Luís C. Muniz-Pereira , Roberto Magalhães Pinto
INTRODUCTION
Species included in the genus Bothrops Wagler,
1824, occur in a great number, with a large
geographical distribution in the Neotropical region,
appearing from Mexico to the North of Argentina
and are absent only in Chile (Gomes & Puerto,
1993), inducing several cases of snake poisoning
in humans and animals (Souza, 2000).
In the extensive survey of nematodes of Brazilian
reptiles (Vicente et al., 1993), the data on parasites
recovered from captive snakes are very few, in
despite of their importance for the knowledge of the
helminth fauna infecting those hosts aiming at the
improvement of maintenance conditions to the
further extraction and production of antiophidic
serum.
The present investigation evaluated the prevalence
of infection by helminths in captive specimens of
Bothrops jararaca and B. alternatus, previously
obtained in wild environments, with data on new
host records for two of the nematode species
recovered during necropsies, together with
comments on the macroscopic lesions induced by
the parasites, taking into account the sensibility and
adaptation of the hosts maintained under laboratory
conditions.
Nematodes were obtained from five specimens of
Bothrops jararaca (Wied, 1824) and one of B.
alternatus (Duméril, Bibron & Duméril, 1854)
maintained in the serpentarium of the Army
Biology Institute (IBEx), Rio de Janeiro, RJ,
Brazil. Animals were captured in the wild and
further donated by volunteers from the State of Rio
de Janeiro (two specimens of B. jararaca [one
male, one female], necropsies LRS002, LRS004,
respectively, from the municipality of Resende -
22o28'08''S, 44o26'48''W, three [one male, two
females], necropsies LRS003, LRS001, LRS006,
respectively, from the municipality of Petrópolis -
22o30'18''S, 43o10'43''W, and from the State of
Minas Gerais (one female specimen of B.
alternatus) necropsy LRS005 from the
municipality of Três Corações - 21º41'49''S,
45º15'12”W . When in captivity, animals were
submitted to the same conditions of temperature,
feeding and luminosity. The maintenance
procedures adopted in the serpentarium of the IBEx
are intensive and animals are kept individually in
special plastic cages. Snakes are fed once a week,
on mice (Mus musculus L., 1758) raised in the IBEx
animal house, with a food amount corresponding to
nearly 10% of the weight of the snake. Wild
specimens maintained in the serpentarium are kept
under quarantine for adaptation and also to avoid
the transmission of pathogens to those already
screened for ecto and endoparasites. The
specimens studied here were investigated during
the quarantine period.
Stool samples were recovered and processed for
analysis in accordance with the method of Gordon
& Whitlock (Mattos Jr & Motta, 1996).
Necropsies were performed from September to
December, 2001, according to the technique of
Gomes & Puerto (1993) and helminthological
procedures followed Amato et al. (1991). Briefly,
organs were dissected in Petri dishes containing a
0.85% NaCl solution.
Nematodes were collected and fixed in hot AFA
solution [(acetic acid (2%) + formaldehyde (3%) +
70% ethanol (93%)] and processed for study
according to Muniz-Pereira & Amato (1995, 1998).
The identification of the nematodes was based on
data after Yamaguti (1961), Schad (1962), Freitas
(1968) and Vicente et al. (1993).
A couple of nematode specimens, just after their
identification were preserved as whole mounts
(Canada balsam + beechwood creosote) and other
amounts, kept as wet material in the fixative
solution.
In the present investigation, the designation
“introduced species” refers to those helminths that
commonly infect mice and accidentally
contaminated the snakes when they fed on naturally
parasitized mice and also for this reason, eggs of
introduced species were detected during
coprological examination. Representative
specimens of each studied nematode species were
deposited in the Helminthological Collection of the
Oswaldo Cruz Institute (CHIOC), Rio de Janeiro,
RJ, Brazil. NHR refers to New Host Record.
30
MATERIALS AND METHODS
Nematodes of Bothrops
Siqueira et al.
Three out of the six coprological screenings were
positive for helminth eggs. In two, eggs of
nematodes that usually infect reptilian hosts, were
observed, with one case of infection with
specimens of Kalicephalus sp. appearing alone
(LRS 004) and one with Kalicephalus sp.
associated to Ophidascaris sp. together with eggs
of the accidentally introduced species, related to
the nematodes Syphacia sp., Aspiculuris sp. and
the cestode Rodentolepis sp.[= Hymenolepis =
Vampirolepis] (LRS006); in the other positive
case, the introduced species were the only to
appear associated (LRS005); eggs of Rhabdiasidae
nematodes were absent. (Table 1). In the snakes
with mixed infections, haemorrhagic foci in the
intestinal mucosa, pulmonary and tracheal exudate
and stomatitis were observed.
Gross lesions observed in the stomach and
intestine of the parasitized snakes appeared as
ulcers associated to the penetration sites of the
nematodes that invaded the mucosa and
submucosa of the organ and the ulcers were either
active or healed. Lesions induced in the intestine of
the infected hosts by specimens of the genus
Kalicephalus consisted of haemorrhagic foci and
alterations of the mucosa in the sites of parasite
attachment. Some snakes presented a cyst in the
gall bladder, pneumonia and stomatitis. As for the
changes observed in snakes by account of
i n f e c t i o n s w i t h A c a n t h o r h a b d i a s
acanthorhabdias, they appeared as a mild mucous
pulmonary exudate; snakes parasitized with these
nematodes had been in captivity for a short period.
New host records for two species, already well
described and figured, are considered in
taxonomic summaries.
N e m a t o d a , D i a p h a n o c e p h a l o i d e a ,
Diaphanocephalidae
Kalicephalus costatus (Rudolphi, 1819)
Taxonomic summary: host: Bothrops jararaca;
site of infection: stomach; locality: municipality of
Resende, Statate of Rio de Janeiro, RJ, Brazil; size
of parasite load: 03 males, 03 females; deposited
specimens: CHIOC no.35.228 (wet material).
Kalicephalus inermis Molin, 1861
Taxonomic summary: host: Bothrops jararaca;
site of infection: intestine; locality: municipality of
Petrópolis, State of Rio de Janeiro, RJ, Brazil; size
of parasite load: 03 males, 07 females; deposited
specimens: CHIOC no. 35.227 (wet material).
Kalicephalus sp.
Taxonomic summary: host: Bothrops alternatus;
site of infection: intestine; locality: municipality of
Três Corações, State of Minas Gerais, MG, Brazil;
size of parasite load: 01 male, one female;
specimens deposited: CHIOC no. 36.233 a-b
(whole mounts).
Nematoda, Ascaridoidea, Ascarididae
Ophidascaris travassosi Vaz, 1938
Taxonomic summary: host: Bothrops jararaca
(NHR) [Pit viper]; other host: Crotalus durissus
terrificus Laurenti, 1768 [South American
rattlesnake]; site of infection: esophagus; locality:
municipality of Petrópolis, State of Rio de Janeiro,
RJ, Brazil; size of parasite load: 02 males, 04
females; deposited specimens: CHIOC no. 35.225
(wet material).
Nematoda, Rhabditoidea, Rhabdiasidae
Acanthorhabdias acanthorhabdias Pereira, 1927
(=Rhabdias labiata)
Taxonomic summary: host: Bothrops alternatus
[Crossed pit viper] (NHR); other host:
Waglerophis merremii (Wagler, 1824) (= Rhadnea
merremii) [Wagler's snake]; site of infection:
lungs; locality: municipality of Três Corações,
State of Minas Gerais, MG, Brazil; size of parasite
load: 09 females; deposited specimens: CHIOC:
no. 35.230 (wet material). Rhabdias labiata
Pereira, 1927 was proposed as a junior synonym of
A. acanthorhabdias Pereira, 1927, by Baker
(1987).
Periodical fecal screenings from captive snakes,
although considered as an important step for the
detection and control of worm burdens, is, in fact,
only an accessory tool, since a the reliable
helminth identification only occurs by means of
the necropsies. The present obtained results related
to coproscopy were not statistically considered,
since they differ from those obtained during the
recovery of worm burdens, regarding the
prevalence of infection with adult worms, since
three, out of the six, fecal samples obtained from
RESULTS
DISCUSSION
Neotrop. Helminthol., 3(1), 2009
31
with specimens of Acanthorhabdias, were more
sensible to adaptation, also presenting more severe
lesions, characterized by necrosis in the sites of
parasite attachment. Rubião (1995) and Grego et al.
(2004) referred to cases of mucous pneumonia in
specimens of B. jararaca infected with species of
Rhabdias and these alterations caused by the
parasitism with A. acanthorhabdias were also
observed during this investigation. Santos et al.
(2008), reported to similar changes in specimens of
the South American rattlesnake Crotalus durissus
terrificus parasitized with Rhabdias spp.
Granulous and caseous gastritis due to the presence
of Ophidascaris sp. worms in B. jararaca (Grego et
al., 2004) were not presently observed in snakes
harboring the ascaridid O. travassosi that appeared
with a low parasitic burden.
wild snakes were positive for helminth eggs, and of
which two showed the presence of nematodes
commonly found in snakes, namely Kalicephalus
sp. and Ophidascaris sp. (Table 1). The presence of
eggs representing species of the genera
Aspiculuris, Syphacia and Rodentolepis appearing
alone or associated to other authochtonous
nematodes of snakes, clearly indicates that those
helminths, in fact, were accidentally introduced,
since they naturally infect the mice snakes were fed
on. Conversely, necropsies confirmed that snakes
that appeared to be negative for authochtonous
helminths, on the basis of fecal examination
presented adult worm burdens, as it was observed
in the specimen of B. alternatus, LRS005, only
positive for introduced species and that was further
found to be infected, during necropsy, with males
and females of Ophidascaris travassosi and
Kalicephalus sp. Similarly, the specimen of B.
jararaca, LRS001 was negative either for
authochtonous helminths or introduced species by
fecal examination and further showed to be
harboring adult Kalicephalus sp. worms in the
intestine. Nevertheless, either unauthorized or
unnecessary necropsies are to be avoided in
serpentariums where snakes are maintained for
venom extraction procedures, only. In the present
case, the aim of the investigation was to supply
data on the helminth fauna of wild specimens of
Bothrops spp. to further support the evaluation of
anti-helminthic drugs to be administered in order
to prevent the spreading of massive infections to
the colony.
Specimens of the genus Kalicephalus, due to their
active percutaneous via of infection, present a
maximized pathogenic action, even in artificial
environments and thus, parasitized snakes with
these nematodes appeared with severe cases of
stomatitis. Significant intestinal lesions were not
observed except for discrete haemorrhagic foci
near the sites nematodes were attached.
The present data are in agreement with those of
Grego et al. (2004) that reported to the finding of
acute and caseous enteritis in specimens of B.
jararaca infected with K. inermis.
According to Fower (1986) and Frye (1991)
species of Rhabdias have a life cycle with
alternating homogonic and heterogonic phases,
also with percutaneous infections, and thus with the
increasing probability to infect captive snakes. In
despite of the low prevalence, snakes parasitized
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Siqueira et al.
32
Nematodes of Bothrops
Authochtonous
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Specimen
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LRS001 F N - - - - - -
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*Correspondence to author/ Autor para correspondencia
Roberto Magalhães Pinto
Laboratório de Helmintos Parasitos de Vertebrados,
Instituto Oswaldo Cruz Cruz.
Av. Brasil, 4365, 21040-900 Rio de Janeiro, Brasil
E-mail: rmpinto@ioc.fiocruz.br
Telefax: 55 (21) 2562-1511
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Ophidascaris sp. (Ophi.), Rhabdiasidae (Rha.), Rodentolepis sp. (Rod.), Syphacia sp. (Sypha.), Aspiculuris sp. (Aspic.), N =
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33
Siqueira et al.
34
Nematodes of Bothrops
