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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: v.nasiri@rvsri.ac.ir (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

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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

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Fig. 1. Acanthocephalan larval detected on the intestinal wall surface.

Fig. 2. The detected Telorchis assula from Natrix natrix.

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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.

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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.

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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

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.

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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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