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Full length article
A description of parasites from Iranian snakesVahid Nasiri
a,b,*, Iraj Mobedi c, Abdolhossein Dalimi b, Abbas Zare Mirakabadi
d,Fatemeh Ghaffarifar b, Shohreh Teymurzadeh d, Gholamreza Karimi
a, Amir Abdoli b,Habibollah Paykari a
a Department of Parasitology, Razi Vaccine and Serum Research
Institute, Karaj, Alborz, Iranb Departments of Parasitology,
Faculty of Medical Sciences, Tarbiat Modares University, Tehran,
Iranc Department of Parasitology, School of Public Health, Tehran
University of Medical Sciences, Tehran, Irand Department of
Venomous Animals and Antivenom Production, Razi Vaccine and Serum
Research Institute, Karaj, Alborz, Iran
H I G H L I G H T S
These are the first data on theparasitic fauna of Iranian
terrestrialsnakes.
Little is known of the parasiticfauna of terrestrial snakes in
Iran.
This study demonstrates the highprevalence of parasites
amongIranian snakes.
G R A P H I C A L A B S T R A C T
* Corresponding author. Fax: 009826-34552194.E-mail address:
[email protected] (V. Nasiri).
http://dx.doi.org/10.1016/j.exppara.2014.09.0070014-4894/ 2014
Elsevier Inc. All rights reserved.
Experimental Parasitology 147 (2014) 715
Contents lists available at ScienceDirect
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A R T I C L E I N F O
Article history:Received 23 March 2014Received in revised form
19 September2014Accepted 24 September 2014Available online 6
October 2014
Keywords:Iranian snakesParasitic faunaIntestinal
parasitesHemoparasites
A B S T R A C T
Little is known of the parasitic fauna of terrestrial snakes in
Iran. This study aimed to evaluate the par-asitic infection rates
of snakes in Iran. A total of 87 snakes belonging to eight
different species, that werecollected between May 2012 and
September 2012 and died after the hold in captivity, under which
theywere kept for taking poisons, were examined for the presence of
gastrointestinal and blood parasites.According to our study 12
different genera of endoparasites in 64 (73.56%) of 87 examined
snakes weredetermined. Forty one snakes (47.12%) had
gastrointestinal parasites. In prepared blood smears, it wasfound
that in 23 (26.43%) of 87 examined snakes there are at least one
hemoparasite. To our knowl-edge, these are the first data on the
internal parasitic fauna of Iranian terrestrial snakes and our
findingsshow a higher prevalence of these organisms among them.
2014 Elsevier Inc. All rights reserved.
1. Introduction
More than 3500 species of snakes have been found around
theworld, less than 10% of which are venomous (Bawaskar, 2004;
Black-man and Dillon, 1992; Meenatchisundaram and Michael,
2009;Warrel, 2005). In Iran, 69 species of snakes assigned to 37
generain six families have been identified, of which 36 species are
non-venomous, 25 species are venomous and 8 species are
semi-venomous (Dehghani, 2010; Latifi, 2000; Zare Mirakabadi
andTeymurzadeh, 2008).
The class Reptilia, consisting of more than 6000 species, is
hostto a wide variety of protozoan and metazoan parasites and
virtu-ally 100% of free-ranging reptiles harbor some kind of
parasites andhowever, the presence of these organisms is not
necessarily asso-ciated with a disease state (Barnard and Upton,
1994; McFarlen, 1991).Breeding snakes in captivity, particularly in
a semi-extensive system,is an activity that exposes the animals to
the action of several para-sites (Mader, 1996). Intestinal
helminths, pentastomids, and intestinaland blood protozoa are
common endoparasites of captive or wildreptiles that these animals
may serve as definitive, intermediate,accidental or paratenic hosts
(Frye, 1991; Greiner and Mader, 2006;Hernandez-divers, 2006;
Jackson and Cooper, 1981; Macarthur et al.,2004). The prevalence of
parasites with a monoxenic cycle is higherthan that of
heteroxenic-cycle parasites, since the latter require
anintermediate host to complete their cycle (Rey, 2001). The
trans-mission of monoxenic-cycle parasites is favored by the
physical andorganic conditions of the captivity, thus a snake can
contaminateother animals or even reinfect itself with its own
feces. In addition,the captivity conditions or the related stress
may be responsible forthe acquisition or increase of the parasitic
infection (Klingenberg,1993). The result of this parasitism is
competition with the host animalfor food, removal of tissue and
fluid, blocking of lymph and bloodvessels, edema, ulcerations,
necrosis, and anemia (Barnard, 1983;Frank, 1981; Frye, 1991;
Marcus, 1981).
Although a considerable species of reptiles are present in
Iransecosystems, there is not enough information about the
parasitic faunaof reptiles and their role in transmission of
veterinary and zoonoticdisease (Youssefi et al., 2013). In a
research in Iran, a Natrix natrixsnake was found to be infected
with the worm that belong to thegenus Ophiotaenia (Youssefi et al.,
2010). In a case report study, myiasisdue to Musca domestica was
described in a Pseudocerastes persicussnake and a lesion was found
on its body where 14 live larvae of M.domestica was removed
(Dehghani et al., 2012). An investigationshowed that 1 turtle
(Mauremys caspica caspica), 11 grass snakes(Natrix natrix) and 5
dice snakes (Natrix tessellata) have been in-fected with Telorchis
assula in Mazandaran, north of Iran (Youssefiet al., 2013). In
another research, one European glass lizard, Pseudopusapodus, and
three European grass snakes, Natrix natrix, were ex-amined for
helminths and found that Pseudopus apodus harboredone species of
Nematoda, Entomelas entomelas and N. natrix har-bored 1 species of
Digenea, Telorchis assula, 1 species of Cestoda,Ophiotaenia
europaea, and 1 species of Nematoda, Rhabdias fuscovenosa(Halajian
et al., 2013). Recently it have been reported that 18
snakes,including 9 N. natrix and 9 N. tessellata from Mazandaran
Province,north of Iran were infected with parasitic helminths
including 1 Nem-atode: Rhabdias fuscovenosa (larva), 1 Digenea:
Telorchis assula and1 Cestoda: Ophiotaenia europaea (Yossefi et
al., 2014).
In this study the parasitic fauna of native Iranian snakes that
weretaken from the wild and kept in captivity were
investigated.
2. Materials and methods
A total of 87 snakes representing eight species that were
col-lected between May 2012 and September 2012 from
variousprovinces of Iran sent to the department of Venomous Animals
andAntivenom Production, Razi Vaccine and Serum Research
Insti-tute. These parasites were kept under captivity and after
dingtransferred immediately to the Parasitology laboratory of
Razi
Table 1The taxonomic characterization of examined snakes and
number of their parasites.
Scientific name of snakes Common name Number
ofexaminedsnakes
Number ofpositivesnakes forintestinalparasitic
Number ofpositivesnakes forhemoparasites
Number ofpositivesnakes forany parasites
Pseudocerastes persicus fieldi Persian horned viper 23 10 13
23Naja oxiana Central Asian cobra 10 7 3 10Vipera albicornuta
Zigzag mountain viper 5 5 0 5Vipera lebetina obtusa West-Asian
blunt-nosed viper 20 10 6 16Vipera ursinii eriwanensis
Transcaucasian meadow viper 2 2 0 2Agkistrodon intermedius
caucasicus Caucasian pit viper 23 5 0 5Natrix natrix European grass
snake 1 1 0 1Coluber caspius gmelin Caspian whip snake 3 1 1 2Total
87 41 23 64
8 V. Nasiri et al./Experimental Parasitology 147 (2014) 715
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Fig. 1. Acanthocephalan larval detected on the intestinal wall
surface.
Fig. 2. The detected Telorchis assula from Natrix natrix.
9V. Nasiri et al./Experimental Parasitology 147 (2014) 715
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Fig. 3. The detected (A) Ophiotaenia sp. and (B) one unknown
species from Natrix natrix.
Fig. 4. The detected nematodes belong to superfamily
Rhabditoidea, Strongyloides sp. from one Vipera ursinii eriwanensis
and four Naja oxiana.
10 V. Nasiri et al./Experimental Parasitology 147 (2014) 715
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Vaccine and Serum Research Institute. The snakes body wall
wasopened by a longitudinal incision and organ surfaces,
mesenteriesof the body cavity, the lumen of the digestive tract and
the lungswere examined visually for parasites. Subsequently, the
viscera wereplaced in a Petri dish with normal physiological saline
and exam-ined for helminths under a dissecting microscope. The
recoveredhelminths were cleaned carefully and, fixed in 70% alcohol
andstained with acetocarmine. The Protozoan parasites were
identi-fied by prepared direct wet mount smears and modified
ZiehlNeelsen staining of fecal samples and examination of them
underlight microscope. The fecal samples were placed in vials with
2.5%K2Cr2O7 and 10% formalin for examination of the fecal contents
forany parasite eggs or oocysts and sporulation of any oocysts
foundin the samples.
For identification of hemoparasites, thin blood smears were
pre-pared from cardiac blood of each snake and then air dried,
fixedin absolute methanol, stained with Giemsa stain and examined
underlight microscope.
Collected parasites were deposited in the Museum of
Parasitol-ogy Department, Razi Vaccine and Serum Research
Institute, Karaj,Alborz, Iran.
Fig. 5. The detected Nematode: Ascarididae from intestine of one
Naja oxiana.
Fig. 6. The detected Eimeria sp. from one Vipera ursinii
eriwanensis and one Viperaalbicornuta.
Fig. 7. The detected Blastocystis sp. from one Vipera lebetina
obtuse.
Fig. 8. The detected Nyctotheroides sp. from one Pseudocerastes
persicus fieldi.
11V. Nasiri et al./Experimental Parasitology 147 (2014) 715
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3. Results
3.1. Intestinal parasites
3.1.1. Intestinal worm infectionTwelve different genus of
endoparasites were determined in 64
(73.56%) out of 87 examined snakes. In the majority of snakes,
two
or more species of parasites were found (see details in Table
1). Atnecropsy, an Acanthocephalan larval stage
(Centrorhynchuscorvi) was found on the outer surface of the
intestinal wallof seven snakes (2 Vipera lebetina obtuse; 2 Vipera
albicornuta; 2 Najaoxiana and 1 Coluber caspius gmelin). Local
necroses were ob-served on the intestinal wall surface of snakes
with Centrorhynchuscorvi (Fig. 1).
Fig. 9. The detected Hexamita batrachorum (Giemsa stain).
Fig. 10. Intraerythrocytic gametocytes in Naja oxiana.
12 V. Nasiri et al./Experimental Parasitology 147 (2014) 715
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An adult stage of one species of trematode (Digenea:
Telorchiidae:Telorchis assula) (Fig. 2), two species of cestoda (A:
Ophiotaenia sp.and B: one unknown species) (Fig. 3) were detected
from the in-testine of a Natrix natrix (European Grass Snake).
Adult stages of two genus of nematode were detected, includ-ing:
one belonging to the superfamily Rhabditoidea (Strongyloidessp.)
from the intestine of five snakes (one Vipera ursinii
eriwanensisand four Naja oxiana) (Fig. 4) and one that belongs to
familyAscarididae from the intestine of one Naja oxiana (Fig.
5).
3.1.2. Intestinal protozoa infectionEimeria sp. was detected in
two snakes (one Vipera ursinii
eriwanensis and one Vipera albicornuta) and in both snakes
withEimeria sp. infection, petechia was observed in the mucous
layerof the intestinal tract (Fig. 6). A large number of
Blastocystis sp. was
Fig. 11. Intraerythrocytic hemoparasites in Pseudocerastes
persicus field. (AD) Intraerythrocytic gametocytes with different
pattern of erythrocyte shape changes. (E) De-veloping schizonts in
the liver of infected snake. (F) Unknown organism from liver.
Fig. 12. Intraerythrocytic gametocytes in Coluber caspius
gmelin.
13V. Nasiri et al./Experimental Parasitology 147 (2014) 715
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detected in one snake (Vipera lebetina obtuse) (Fig. 7).
Moreover, Cili-ated protozoa (Nyctotheroides sp.) was detected in a
snake(Pseudocerastes persicus fieldi) (Fig. 8).
A large numbers of Hexamita batrachorum (a flagellate proto-zoa
belonging to Phylum Sarcomastigophora, Class Mastigophora)
wasdetected in intestinal mucosa and stool of 27 snakes (9
Pseudocerastespersicus fieldi, 8 Vipera lebetina obtuse, 3
Agkistrodon intermediuscaucasicus, 1 Vipera ursinii eriwanensis, 2
Vipera albicornuta and 4Naja oxiana) (Fig. 9). This parasite was
the most frequent organ-ism found in snakes (31.03%).
3.2. Hemoparasites
Hemoparasites were observed in 23 (26.43%) out of 87 exam-ined
snakes. Many of the infected red blood cells were distorted insize
and shape; however, some infected cells were similar touninfected
erythrocytes. We could not to see sporogonic stages,thus we could
not determine the parasites genus. Microscopic ex-amination of
Giemsa stained slides showed infection of red bloodcells of 13
Pseudocerastes persicus fieldi, 6 Vipera lebetina obtusa, 3Naja
oxiana and 1 Coluber caspius gmelin with Hemoparasites(Figs.
1013).
4. Discussion
The reptiles have important impacts on different aspects of
theirecology and thus demands deep research regarding the
influenceof these animals and their flora on people and
autochthonous animalspecies. The varieties of different pathogens
in these species are verylarge. The presence of several pathogens
in one host and stressfulsituations can have a negative influence
on the health status. Fur-thermore, there is a possibility of
pathogen transmission to human.A healthy reptile has a number of
pathogens, all kept in check bya healthy immune system and the
beneficial gut flora. When a reptileis highly stressed or under
prolonged moderate to severe stress, theimmune system falters. In
cases of improper environmental tem-peratures, starvation, or
prolonged dehydration, the beneficial gutflora die off and
organisms benign in small numbers gain ascen-dancy and start
causing problems (Rataja et al., 2011).
It is widely known that under captivity the stress to
whichanimals are submitted to can induce the settlement of several
pa-thologies, mainly those related to parasites (Leinz et al.,
1989; Santoset al., 2008; Siqueira et al., 2009) and because
parasites can reach
high infection loads in hosts in captivity, can be very
problematicand may cause the death of hosts (Klingenberg, 1993). So
for con-servation efforts involving captive breeding, an
understanding of theparasites of a particular species is crucial.
With this view, it is nec-essary to provide data on the parasitic
fauna of Iranian snakes, inorder to permit the establishment of
prophylactic procedures toproperly reduce the mortality of captive
animals.
The present study was carried out to evaluate the parasitic
in-fections in wild snakes. The study was proposed because we
observedthat, in captivity, snakes presented a high prevalence
(above 70%)of infection by different parasite species. The present
investiga-tion showed that 64 (73.56%) of 87 analyzed snakes
arrived forcaptivity already infected by at least one parasite
species. The resultsfrom this study are important for the sanitary
handling of these im-portant animals during captivity. Other
different species were alsodetected that similar parasite were
described in the previous lit-eratures (Klingenberg, 2000; Mader,
1996; Telford, 2009). In twosnakes a wide dilatation and
destruction of gastrointestinal tractwas seen and Modified
ZiehlNeelsen staining was positive forEimeria sp. The
Hemogregarines (Apicomplexa: Adeleorina) are,intraerythrocytic
protozoan parasites that infect a wide variety ofvertebrates
(Davies and Johnston, 2000; Telford, 2009) and are con-sidered
common Hemoparasites of reptiles and this was also truein our
study.
In conclusion, to our knowledge, these are the first data on
theparasitic fauna of Iranian terrestrial snakes and our findings
showa higher prevalence of these organisms among them. Control
andprevention of many parasitic diseases is associated with
breakingthe cycle of transmission, and there is no shadow of doubt
thatprecise information about diseases and their causative agents
is themajor key to control of them and thus, further precise
parasito-logical investigations are required due to the noticeable
unexploredarea of our country in order to ascend our knowledge
concerningparasites of snakes and probable zoonotic and veterinary
impor-tance of them.
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A description of parasites from Iranian snakes Introduction
Materials and methods Results Intestinal parasites Intestinal worm
infection Intestinal protozoa infection Hemoparasites Discussion
%pagenumx2333-(%by+%yrelsob+%prelead)/352ReferencesReferences