J Arthropod-Borne Dis, June 2015, 9(1): 1–6 M Nateghpour et al.: Endoparasites of Wild … 1 Original Article Endoparasites of Wild Rodents in Southeastern Iran Mehdi Nateghpour 1, *Afsaneh Motevalli-Haghi 1,2, Kamran Akbarzadeh 3, Amir Ahmad Akhavan 3, Mehdi Mohebali 1, Iraj Mobedi 1, Leila Farivar 1 1Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical sciences, Tehran, Iran 2National Institute of Health Research, Tehran University of Medical sciences, Tehran, Iran 3Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical sciences, Tehran, Iran (Received 9 Dec 2012; accepted 27 Apr 2014) Abstract Background: This study was aimed to collect wild rodents for endoparasites determination in some parts of Sistan and Baluchistan Province, southeastern Iran nearby Pakistan and Afghanistan countries. Methods: A total of 100 wild rodents were captured alive with cage traps. Various samples were collected from blood and feces, also impression smear prepared from different organs. The samples were prepared by formalin-ether or stained with Giemsa, after that were examined under microscope. Results: All the caught rodents (47 Tatera indica, 44 Meriones hurriana, 5 Gerbilus nanus and 4 Meriones libycus) were studied for endoparasites emphasizing to their zoonotic aspects. Endoparasites including Spirurida, Hymenolepis diminuta, Hymenolepis nana feraterna, Trichuris trichiura, Skerjabino taenia, Trichostrongylus spp, Entamoeba muris, Chilomastix mesnili and Leishmania spp were parasitologically identified. Conclusion: Among 9 genera or species of the identified parasites at least 5 of them have zoonotic and public health importance. Keywords: Wild rodent, Endoparasite, Iran Introduction Many infectious diseases classified as zo- onotic infections can be caused by parasitic, viral and bacterial agents transmitted to hu- man by different types of animals such as rodents (Etemad 1978, Weiss et al. 2008). Ectoparasites such as fleas, lice and ticks can also transmit some infectious agents from rodents to human (Daniels and Hutchings 2001). Meerburg et al. (2009) showed a large spectrum of rodent borne pathogens. Helminth parasites are a large group of met- azoan organisms that infect vast numbers of human and livestock (Anthony 2007). Simi- larly, some protozoan zoonoses such as Tox- oplasma and Leishmania can also affect hu man and become malignant for those who are positive HIV (Alvar et al. 2008, Naqi et al. 2010). Metazoan and protozoan zoonoses are re- sponsible for a large number of morbidity and mortality of human around the world (Chai et al. 2005) and induce significant public health and socioeconomic problems. This study was conducted to collect some informative data about the rodents and rele- vant parasites in some parts of Sistan and Baluchistan Province in Iran with emphasis on finding worms and protozoan parasites which have medical importance to human. *Corresponding author: Dr Afsaneh Motevalli-Haghi, E-mail: amh.mot@gmail.com  http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 1–6 M Nateghpour et al.: Endoparasites of Wild … 2 Materials and Methods Study areas The study was performed at the Iranshahr and Nikshahr districts in Sistan and Baluchi- stan Province, southeastern Iran (Fig. 1). The weather in the districts is hot and dry in summer with usual maximum temperature of 45 ºC but temperate and low humid in winter with usual minimum temperature of 15 ºC. Six sites in each district nearby the inhabit- ant locations along the rodent's routes were randomly selected for trapping. Rodent collection A total of 100 rodents were captured alive with cage traps. The traps were collected and transfered to Iranshahr Health Research Station. Tail punctured and thin blood smears were made from all of the rodents and then the animals were anesthetized under chloroform inhalation for careful dissection and preparing impression smears of spleen, liver and lungs. One smear also was made from any papilla on the surface of ears. The smears were stained with Giemsa stain diluted in natural distilled water up to 3% for 30 min. Spots that pre- pared from dissected brains were also stained as the same method and precisely observed by light microscope with magnification of 1000. Some amounts of the gastrointestinal tract content were collected for gastrointestinal par- asites examination. Ether-chloroform method was applied to identify parasites. Both proto- zoan and helminthes parasites isolated as well as the rodents were distinguished by skilled persons using a number of valid references (Khalil and Jones 1994, David et al. 2004, Jones et al. 2004, Rodney et al. 2008). Results Four species of rodents including Tatera indica (47%), Meriones hurrianae (44%), Gerbilus nanus (5%) and M. libycus (4%) were identified. Classification of the animals was performed according to family (Cricetidae), subfamily (Gerbillinae), genus (Tatera, Meriones, Gerbilus) and species. The maxi- mum and minimum quantities belong to T. indica 47(47%) and M. libycus 4(4%) re- spectively (Table 1). The microscopic examination of gastro- intestinal tract contents revealed the presence of Spirurida spp. and Trichostrongylus eggs in seven and two T. indica respectively. The rest helminthes isolated including Hymenolepis diminuta, H. nana feraterna, Trichuris trichiura, Skerjabino taenia and Rictularia were found in adult stages. Moreover protozoan parasites, Entamoeba muris and Chilomastix mesnili were isolated from the feces. In one case of liver tis- sue Leishmania spp., was identified (Table 2). Table 1. Distribution of wild rodents caught from Iranshahr and Nikshahr districts in southeastern Iran Genus/species Iranshahr Nikshahr Total N(%) Tatera indica 38 9 47 (47) Meriones hurrianae 0 44 44 (44) Gerbilus nanus 5 0 5 (5) Meriones libycus 4 0 4 (4) Total 47 53 100 (100) http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 1–6 M Nateghpour et al.: Endoparasites of Wild … 3 Table 2. Frequency of protozoan and helminthes parasites identify captured in 100 wild Nikshahr and Iranshahr districts Rodents Parasites Wild Rodents Total Meriones libycus Meriones hurrianae Tatera indica Gerbilus nanus N (%) Hymenolepis diminuta 0 0 11 0 11 (23.4) Hymenolepis nana feraterna 0 0 8 0 8 (17.0) Spirurida spp. 0 0 7 0 7 (14.9) Trichuris trichiura 0 0 6 0 6 (12.7) Skerjabino taenia spp. 0 0 4 0 4 (8.5) Trichostrongylus 0 0 2 0 2 (4.2) Rictularia spp. 0 0 1 0 1 (2.1) Entamoeba muris 0 2 (%4.2) 2 0 4 (8.5) Chilomastix mesnili 0 3 (%6.3) 0 0 3 (6.3) Leishmania spp. 0 0 1 0 1 (2.1) Total 0 5 (%10.6) 42 0 47 (10) Fig. 1. Sistan and Baluchistan Province located at southeastern Iran : location of the study areas in the province Discussion This study was conducted to consider the endoparasites of wild rodents in some parts of southeastern Iran where located nearby western borderline of Pakistan and Afghani- stan countries. Control of zoonotic parasites depends on reliable knowledge of their life-cycles, res- ervoirs, distribution and transmission patterns in each zoogeographical situation. Many ro- dents particularly commensal species enable to take place in transmission cycle of para- sitic infections as an important reservoir (Ghadirian and Arfaa 1972, Sadighian et al. 1973, Mohebali et al. 1998, 2004, Kia et al. 2001, Mowlavi et al. 2004). Reports released by some authors about rodent borne parasitic infections from some parts of Iran made more obvious the role of rodents as reservoir of many protozoan and helminth parasites (Edrissian et al. 1975, 1976, Yaghoobi-Ershadi 1996, Mohebali 1997, Javadian et al. 1998, Sadjjadi and Massoud 1999 Kia et al. 2001, 2010). During this study four species of rodents, M. libycus, M. hurrianae, T. indica and G. nanus were identified that the most preva- lent species was T. indica with 47% (n= 47). In a zoonotic helminth study conducted in Khuzestan, a Province in southwestern Iran, T. indica was found as the most dominant species (Sadjjadi and Massoud 1999). While in another study performed by Kia et al. (2001) Rattus norvegicus was the most prev- alent rodent in Ahvaz, centre of Khuzestan Province. In the present study the samples were collected from rural areas so our results are comparable with those studies that em- http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 1–6 M Nateghpour et al.: Endoparasites of Wild … 4 phasis gerbils are dominant species in the rural areas, while in the urban areas rattus can be usually found more than gerbils. In Kamranrashani et al. study in Maraveh Tappeh, Golestan Province located in north- east of Iran a heavy burden of infectivity with helminth parasites (81.8%) was found in R. opimus (Kamranrashani et al. 2012). In our study M. hurrianae (n= 44, 44%), G. nanus (n= 5, 5%) and M. libycus (n= 4, 4%) stayed at the second to fourth ranks re- spectively after T. indica. Tatera indica bore the maximum parasitic infectivity and none of the parasites was isolated from M. libycus and G. nanus (Table 2). In a previous study performed in the leishmaniasis endemic ar- eas of Iran T. indica was accounted the main Leishmania major reservoir in Mehran dis- trict of Iran where located nearby eastern borderline of Iraq (Mohebali et al. 2004). Some promastigotes of Leishmania spp. were isolated from Phlebotomous papatasi and Ph. salehi sand flies those were collected from T. indica and M. Hurrianae burrows in Chabahar district located at the south of Iranshahr district (Kasiri and Javadian 2000). In our study Leishmania spp. was isolated from T. indica which is consistent their results. In addition, examination of gastrointesti- nal content of this rodent showed infection with Entamoeba muris. Although E. muris is assumed to be a common protozoan parasite of the most rodents, results of this study rec- orded the parasite only for T. indica and M. hurrianae with equal burden of infection. Chilomastix mesnili as the third protozoan parasitic infection in this study was found among three M. hurrianae. Although C. mesnili has been isolated from a few infected individuals, it is a common parasite among rodents and usually none pathogen for hu- man. A scientific report indicated that 0.6% of adolescent girls from two boarding schools, in southern Benin were carrier of C. mesnili at the time of study (Alaofe et al. 2008). All the identified helminth parasites were iso- lated only from T. indica in this study. These results pointed to the more activity and prevalence of T. indica and also capability of the rodent for assuming a wide variety of parasitic infections in comparison with the other captured rodents in the studied areas. Among the parasites isolated from rodents in this study, Hymenolepis diminuta, the rat tapeworm, was the most prevalent helminth species. In Kia et al. study (2010) H. diminuta was the most common parasite that could be found in different species of rodents. Some helminthes such as Trichuris trichiura, H. feraterna, Skerjabino taenia, Trichostrongylus spp., Spirurida and Rictularia spp. are infective to human and deleterious for public health (Keney et al. 1975, Mowlavi et al. 2006, 2008, Ok 2009). Infectivity of H. diminuta for human had been distinguished from long time ago in Iran (Ghadirian and Arfaa 1972). Among eight T. indica that were infected with order of Spirurida one of them was identified as adult Rictularia spp. infection but the others remained at the level of order because the infectivities were dis- tinguished only with presence of the eggs. Some studies performed in Khuzestan Prov- ince indicated presence of Rictularia spp. and Gongylonema spp. that were isolated from a number of wild rodents and carni- vores (Farahnak1998, Sadjjadi and Massoud 1999, Kia et al. 2001). Spirurida includes a great number of genera and species which all have invertebrate intermediate hosts. Both Rictularia and Gongylonema have been iso- lated from human (Urch et al. 2005, Keney et al. 1975). To our knowledge among nine genera or species of the identified parasites at least five of them have zoonotic and public health importance. Conclusion Harboring a wide variety of zoonotic par- asites by T. indica particularly when the ro- http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 1–6 M Nateghpour et al.: Endoparasites of Wild … 5 dent lives nearby the native population res- idences represents a potential risk to the health of the population. Although the in- fection of M. hurrianae was not comparable with T. indica, nevertheless the rodent can be accounted at the second potential risk to the health of human at the studied areas. Acknowledgements The authors would like to thank Prof M Rezaeian, Dr M Kazemi, Dr G Mowlavi, Mr A Shahbakhsh, Mr A Amiri, Mrs E Ghodrati- Moghaddam, Mrs F Tarighei, Mr F Damani and Mr R Sheikh for their useful coopera- tion. This study was financially supported by National Institute of Health Research, Teh- ran University of Medical Sciences. The au- thors declare that there is no conflict of in- terests. References Alaofe H, Zeeb J, Dossac R, Turgeon HB (2008) Intestinal parasitic infections in adolescent girls from two boarding schools in southern Benin. Trans Roy Soc Trop Med Hyg. 102: 653–661. Alvar J, Aparicio P, Aseffa A, Den Boer M, Can˜avate C, Dedet JP, Gradoni L, Horst RT, Lopez-Velez R, Moreno J (2008) The relationship between Leish- maniasis and AIDS: the Second 10 Years. Clin Microbiol Rev. 21(2): 334– 359. Anthony RM, Rutitzky LI, Urban JR, Stadecker MJ, Gause WC (2007) Protective immune mechanisms in helminth infection. Na- ture Rev Immunol. 7: 975–987. Chai JY, Darwin Murrell K, Lymbery AJ (2005) Fish-borne parasitic zoonoses: Status and issues. Int J Parasitol. 35: 1233–1254. Daniels MJ, Hutchings MR (2001) The re- sponse of cattle and sheep to feed con- taminated with rodent feces. Vet J. 162 (3): 211–218. David IG, Jones A, Rodney AB, (2004) Key to the Termatoda. Vol 1. CABI Pub- lishing, Wallingford, UK. Edrissian GhH, Ghorbani M, Tahvildar- Bidruni GH (1975) Meriones persicus, another probable reservoir zoonotic cutaneous leishmaniasis in Iran. Trans Roy Soc Trop Med Hyg. 69(5–6): 517–519. Edrissian GhH, Farahnag-Azad A, Neronov VM (1976) Trypanosomes of small mammals in Iran. J Wildlife Dis. 12: 497. Etemad E (1978) Mammals of Iran. Vol. I: Rodents and their Identification key. National Society of Natural Sources and Human Environment Protection Publications, Tehran. Ghadirian E, Arfaa F (1972) Human infec- tion with Hymenolepis diminuta in vil- lages of Minab, southern Iran. Int J Parasitol. 2(4): 481–482. Javadian E, Dehestani M, Nadim A, Rassi Y, Tahvildar-Bidruni GH, Seyedi-Rashti MA, Shadmehr A (1998) Confirmation of Tatera indica (Rodentia: Gerbillidae) as the main reservoir host of zoonotic cutaneous leishmaniasis in the west of Iran. Iran J Publ Health. 27(1–2): 55–60. Jones A, Rodney AB, David IG (2004) Key to the Termatoda. Vol 2. CABI Pub- lishing, Wallingford, UK. Kamranrashani B, Kia EB, Mobedi I, Mohebali M, Zarei Z, Mowlavi Gh, Hajjaran H, Abai MR, Sharifdini M, Kakooei Z, Mirjalali H, Charedar S (2012) Helminth parasites of Rhombomys opimus from Golestan Province, Northeast Iran. Iran J Parasitol. 8(1): 78–84. Kasiri H, Javadian E (2000) The natural leptomonad infection of Phlebotomous papatasi and Phlebotomous salehi in endemic foci of cutaneous Leismaniasis in Sistan and Baluchistan Province (southeast of Iran). Iran J Pub Health. 29(1–4):15–20 (In Persian). http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 1–6 M Nateghpour et al.: Endoparasites of Wild … 6 Keney M, Eveland LK, Yermakov V, Kassovny DY (1975) A case of Rictularia infec- tion of man in New York. Am J Trop Med Hyg. 24(4): 596–599. Khalil LF, Jones A, Bray RA (1994) Key to the Cestodes Parasites of Vertebrates. ISBN-13: 978-0851988795 Kia E, Shahryary-Rad E, Mohebali M, Mahmoudi M, Mobedi I, Zahabiun F, Zarei Z, Miahipoor A, Mowlavi Gh, Akhavan AA, Vatandoost H (2010) Endoparasites of rodents and their zo- onotic importance in Germi, Dashte- Mogan, Ardabil Province, Iran. Iran J Parasitol. 5(4):15–20. Kia EB, Homayoun MM, Farahnak A, Mohebali M, Shojai S (2001) Study of endoparasites of rodents and their zo- onotic importance in Ahvaz, south west Iran. Iran J Publ Health. 30(1–2): 40–52. Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for Public Health. Crit Rev Microbiol. 35(3): 221–270. Mohebali M (1997) The first report of Babesia microti in rodents captured in Meshkin-Shahr, Iran. Iran J Pub Health. 26(3–4): 83–85. Mohebali M, Poormohmmadi B, Kanani A, Hajjaran H, Edrissian GhH (1998) Rodents- Gerbillidae- Cricetidae an- other animal host of visceral Leish- maniasis in Meshkin-Shahr district, Iran. East Med Health J. 4(2): 376–274. Mohebali M, Javadian E, Yaghoobi-Ershadi MR, Akhavan A, Hajjaran H, Abaei MR (2004) Characterization of Leishmania infection in rodents from endemic ar- eas of the Islamic Republic of Iran. East Med Health J. 10(4–5). Mowlavi GhR, Kia EB, Mobedi I (2004) Natural infection of the gerbil Meriones libycus with the metacestode of taenia endothoracicus in Arak, central Iran. J Helminth. 78(3): 275–276. Mowlavi GhR, Massoud J, Gutierrez Y (2006) Human Gongylonema infection in Iran. J Helminth. 80: 425–428. Mowlavi GhR, Mobedi I, Mamishi S, Rezaeian M, Haghi Ashtiani MT, Kashi M (2008) Hymenolepis diminuta (Rodolphi 1819) infection in a child from Iran. Iran J Publ Health. 37(2): 120–122. Naqi R, Azeemuddin M, Ahsan H (2010) Cerebral toxoplasmosis in a patient with acquired immunodeficiency syndrome. J Pak Med Assoc. 60(4): 316–318. Ok KS, Kim YS, Song JH, Lee JH, Ryu SH, Moon JS, Whang DH, Lee HK (2009) Trichuris trichiura infection diagnosed by colonoscopy: case reports and review of literature. Korean J Parasitol. 47(3): 275–280. Rodney AB, David IG, Jones A (2008) Key to the Termatoda. Vol 2. CABI Pub- lishing, Wallingford, UK. Sadighian A, Arfaa F, Movafagh K (1973) Trichinella spiralis in carnivores and rodents in Isfahan, Iran. J Parasitol. 59 (6): 986. Sadjjadi SM, Massoud J (1999) Helminth parasites of wild rodents in Khuzestan Province, south west of Iran. J Vet Parasitol. 13(1): 55–56. Urch T, Albrecht BC, Büttner DW, Tannich E (2005) Human infection with Gongylonema pulchrum. Dtsch Med Wochenschr. 130(45): 2566–2568. Weiss LM (2008) Zoonotic parasitic dis- eases: Emerging issues and problems. Int J Parasitol. 38(11): 1209–1210. Yaghoobi-Ershadi MR, Akhavan AA, Mohebali M (1996) Meriones libycus and Rhombomys opimus are the main reservoir hosts in a new focus of zo- onotic cutaneous leishmaniasis in Iran. Trans Roy Soc Trop Med Hyg. 90: 503–504. http://jad.tums.ac.ir Published Online: July 16, 2014