An Investigation of Potentially Zoonotic Helminth Parasites of Allactaga elater in Sarakhs, Iran
Main Article Content
Abstract
Introduction: Rodents are the reservoir of many endoparasites and act as their intermediate or final hosts. This study aimed to assess parasitic helminths of Allactaga elater in Sarakhs, Khorasan Razavi Province, northeastern Iran.
Material and methods: From August 2017 to February 2018, 33 Allactaga elater were collected using live traps. All Allactaga elaters were euthanized, and their gastrointestinal tracts were removed and examined to identify parasitic helminths. Finally, parasites were identified using key morphological characteristics.
Results: Overall, 91% of Allactaga elaters were infected with helminths, including Syphacia obvelata (86.6%), Aspicularis tetraptera (36.6%), Trichuris spp (13.3%), Heligmosomoides polygyrus (3.3%), Hymenolepis nana (16.6%), Hymenolepis diminuta (16.6%), and Cysticercus fasciolaris (13.3%).
Conclusion: Various species of helminths were found in Allactaga elater from the studied area. These findings highlight the importance of this rodent species as a reservoir for zoonotic helminths.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Funding data
-
Ferdowsi University of Mashhad
Grant numbers 47274
References
Wilson DE and Reeder DM. Mammal species of the world: A taxonomic and geographic reference. J. Mammal. 2007; 88(3): 824-830. DOI: https://doi.org/10.1644/06-MAMM-R-422.1
Fokin IM. Jerboas. Obituary Igor Mikhailovich Fokin. Russian J Theriol. 2018; 17(2): 108-112. Available at: https://www.kmkjournals.com/ upload/PDF/RJT/17/ther17_2_108_112.pdf
Miljutin A. Trends of specialization in rodents: The five-toed jerboas, subfamily Allactaginae (Dipodoidea, Rodentia). Acta Zool Litu. 2008; 18(4): 228-239. DOI: https://doi.org/10.2478/V10043-008-0033-9
Dianat M, Aliabadian M, Darvish J, and Akbarirad S. Molecular phylogeny of the Iranian Plateau five-toed jerboa, Allactaga (Dipodidea: Rodentia), inferred from mtDNA. Mammalia. 2013; 77(1): 95-103. DOI: https://doi.org/10.1515/mammalia-2012-0011
Shenbrot GI, Sokolov VE, Heptner VG, and Kovalskaya YM. Dipodoidea. Mammals of Russia and Adjacent Regions. Moscow: Nauka Publishing House; 1995. Available at: https://www.routledge.com/Jerboas-Mammals-of-Russia-and-Adjacent-Regions/Shenbrot-Sokolov-Heptner/p/book/9781578085316#
Shenbrot G, Tsytsulina K, Batsaikhan N, Avirmed D, Tinnin D, Sukhchuluun G, et al. International Union for Conservation of Nature. 2008. Available at: IUCN Red List of Threatened Species.
Lagassé P. The Columbia encyclopedia. 6th ed. New York: Columbia UP; 2000.
Rabiee MH, Mahmoudi A, Siahsarvie R, Kryštufek B, and Mostafavi E. Rodent-borne diseases and their public health importance in Iran. PLoS Negl Trop Dis. 2018; 12(4): e0006256. DOI: https://doi.org/10.1371/journal.pntd.0006256
Sadr S, Charbgoo A, Borji H and Hajjafari A. Interactions between innate immunity system and Echinococcus granulosus: Permission for vaccine development. Series Med Sci. 2022; 3(1): 1-18. Available at: https://seriesscience.com/echinococcus-granulosus/
Lotfalizadeh N, Sadr S, Moghaddam S, Najjar MS, Khakshoor A, Simab PA, et al. The innate immunity defense against gastrointestinal nematodes: Vaccine development. Farm Anim Health Nutr. 2022; 1(2): 31-38. Available at: https://fahn.rovedar.com/ article_164201_04a5451bd9cbb5bc803e8d08b64032e3.pdf
Carmena D, Benito A, and Eraso E. The immunodiagnosis of Echinococcus multilocularis infection. Clin Microbiol Infect. 2007; 13(5): 460-475. DOI: https://doi.org/10.1111/j.1469-0691.2007.01665.x
Bartholomot G, Vuitton DA, Harraga S, Giraudoux P, Barnish G, Wang YH, et al. Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in central China. Am J Trop Med Hyg. 2002; 66(1): 23-29. DOI: https://doi.org/10.4269/AJTMH.2002.66.23
Eckert J. Predictive values and quality control of techniques for the diagnosis of Echinococcus multilocularis in definitive hosts. Acta Trop. 2003; 85(2): 157-163. DOI: https://doi.org/10.1016/S0001-706X(02)00216-4
Ito A, Romig T, and Takahashi K. Perspective on control options for Echinococcus multilocularis with particular reference to
Japan. Parasitol. 2003; 127(1): S159-S172. Available at: https://pubmed.ncbi.nlm.nih.gov/15027612/
Deplazes P, Hegglin D, Gloor S, and Romig T. Wilderness in the city: The urbanization of Echinococcus multilocularis. Trends parasitol. 2004; 20(2): 77-84. DOI: https://doi.org/10.1016/j.pt.2003.11.011
Kia EB, Homayouni MM, Farahnak A, Mohebali M, and Shojai S. Study of endoparasites of rodents and their zoonotic importance in Ahvaz, south west Iran. Iran J Public Health. 2001; 30(1-2): 49-52. Available at: https://www.sid.ir/EN/VEWSSID/J_pdf/86320011209.pdf
Moradpour N, Borji H, Darvish J, Moshaverinia A, and Mahmoudi A. Rodents helminth parasites in different region of Iran. Iran
J Parasitol. 2018; 13(2): 275-284. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6068363/
Arzamani K, Salehi M, Mobedi I, Adinezade A, Hasanpour H, Alavinia M, et al. Intestinal helminths in different species of rodents in North Khorasan Province, northeast of Iran. Iran J Parasitol. 2017; 12(2): 267-273. Available at: https://europepmc.org/article/pmc/5527038
Darvish J, Hajjar T, Moghaddam Matin M, Haddad F, and Akbary rad S. New species of five-toed jerboa (Rodentia: Dipodidae, Allactaginae) from north-east Iran. J Sci I R Iran. 2008; 19(2): 103-109. Available at: https://jsciences.ut.ac.ir/article_31883_52906f2460011db0bce41cc94f2167e3.pdf
Darvish J, Mohammadi Z, Mahmoudi A, and Siahsarvie R. Faunistic and taxonomic study of Rodents from northwestern Iran. Iran J Anim Biosystem. 2014; 10(2): 119-136. DOI: https://doi.org/10.22067/IJAB.V10I2.44285
El-Hamed A, Abd-Rabou A, and Faramawy A. Therapeutic efficacy of curcuma and pomelo loaded chitosan nanoparticles in intestinal murine trichinellosis. Egypt J Chem. 2022; 65(2): 551-564. DOI: https://doi.org/10.21608/EJCHEM.2021.102400.4750
Yanagida T, Mohammadzadeh T, Kamhawi S, Nakao M, Sadjjadi SM, Hijjawi N, et al. Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitol. Internat. 2012 1;61(4):599-603. DOI: https://doi.org/10.1016/j.parint.2012.05.014
Sazmand A, Joachim A. Parasitic diseases of camels in Iran (1931–2017)–a literature review. Parasite. 2017; 24: 21. DOI: https://doi.org/10.1051/parasite/2017024
Borhani M, Fathi S, Darabi E, Jalousian F, Simsek S, Ahmed H, et al. Echinococcoses in Iran, Turkey, and Pakistan: Old diseases in the new millennium. Clin Microbiol Rev. 2021; 34(3): e00290-20. DOI: https://doi.org/10.1128/CMR.00290-20
Zare-Bidaki M, Mobedi I, Naddaf SR, Kia EB, Mahmoudi M, Piazak N, et al. Prevalence of Echinococcus spp. infection using coproantigen ELISA among canids of Moghan Plain, Iran. Iran J Pub Health. 2009; 38(1): 112-118. Available at: https://eprints.arums.ac.ir/1047/1/Coproantigen.pdf
Borji H, Emami MR, Maleki MO, Razmi GH, Mehrjerdi HK, and Moghaddas E. Alveolar echinococcosis infection in a monkey (Ateles geoffroyi) in Mashhad, Iran. Iran J Pub Health. 2012; 41(2): 111-116. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3481672/
Pakdel N, Naem S, Rezaei F, and Chalehchaleh AA. A survey on helminthic infection in mice (Mus musculus) and rats (Rattus norvegicus and Rattus rattus) in Kermanshah, Iran. Vet Res Forum. 2013; 4(2): 105-109. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4313010/
Rasti S, Moubedi I, Dehghani R, Doroodgar A, and Arbabi M. Epidemiological evaluation of intestinal parasites of wild and domestic mice in Kashan Province in 1997. J Kashan Univ Med Sci. 2002; 5(4): 102-108. Available at: http://feyz.kaums.ac.ir/article-1-357-en.html
Gholami SH, Motavali Haghgi F, Mobedi I, and Shahabi S. Study on intestinal helminth parasites of rodents in urban and central area of Mazandaran Province. J Mazandaran Univ Med Sci. 2002; 12(35): 67-73. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6068363/
Moradpour N, Borji H, Darvish J, Moshaverinia A, Mahmoudi A. Rodents Helminth Parasites in Different Region of Iran.
Iran J Parasitol. 2018; 13(2): 275-284. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6068363/
Kia EB, Shahryary-Rad E, Mohebali M, Mahmoudi M, Mobedi I, Zahabiun F, et al. Endoparasites of rodents and their zoonotic importance in Germi, Dashte–Mogan, Ardabil Province, Iran.
Iran J Parasitol. 2010; 5(4): 15-20. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3279854/
Tanideh N, Sadjjadi SM, Mohammadzadeh T, and Mehrabani D. Helminthic infections of laboratory animals in animal house of Shiraz University of Medical Sciences and the potential risks of zoonotic infections for researchers. Iran Red Crescent Med J. 2010; 12(2): 151-157. Available at: https://pesquisa.bvsalud.org/portal/resource/pt/emr-93184
Eslami A. Veterinary helminthology. 2nd ed. Nematoda and Acanthocephala. Tehran University Publication; 1997.
Forrester DJ. Heligmosomoides polygyrus (= Nematospiroides dubius) from wild rodents of northern California: Natural infections, host specificity, and strain characteristics. J Parasitol. 1971; 57(3): 498-503. Available at: https://pubmed.ncbi.nlm.nih.gov/5090957/
GÜRLER AT, Beyhan YE, BÖLÜKBAŞ CS, Acici M, and Şinasi UM. Gastrointestinal helminths of wild rats (brown rat-Rattus norvegicus, Berkenhout 1769) in Samsun, Turkey. Ank Univ Vet Fak Derg. 2011; 58(4): 289-290. DOI: https://doi.org/10.1501/Vetfak_0000002490
Sadjjadi SM, and Massoud J. Helminth parasites of wild rodents in Khuzestan Province, south west of Iran. J Vet Parasitol. 1999; 13(1): 55-56. Available at: https://www.scienceopen.com/document?vid=dd1ca058-b2f6-48cf-82dd-8f2d0258fc57
Mowlavi GH, Mobedi I, and Mamishi S. Hymenolepis diminuta (Rudolphi, 1819) infection in a child from Iran. Iran J Public Health. 2008; 37(2): 120-121. Available at: https://www.ncbi.nlm.nih.gov/ pmc/articles/PMC7145915
Mohebali M, Rezaei H, Farahnak A, and Kanani Nootash A. A survey on parasitic fauna (helminths and ectoparasites) of the rodents in Meshkin Shahr district, North West Iran. J Fac Vet Med
Univ Tehran. 1997; 52(3): 23-25. Available at: https://www.sid.ir/en/Journal/ViewPaper.aspx?ID=58936
Ghadirian E, and Arfaa F. Human infection with Hymenolepis diminutain villages of Minab, Southern Iran. Int J Parasitol. 1972; 2(4): 481-482. DOI: https://doi.org/10.1016/0020-7519(72)90093-8
Tena D, Simón MP, Gimeno C, Pomata MT, Illescas S, Amondarain I, et al. Human infection with Hymenolepis diminuta: Case report from Spain. J Clin Microbiol. 1998; 36(8): 2375-2376. DOI: https://doi.org/10.1128/JCM.36.8.2375-2376.1998
Marangi M, Zechini B, Fileti A, Quaranta G, and Aceti A. Hymenolepis diminuta infection in a child living in the urban area of Rome, Italy. J Clin Microbiol. 2003; 41(8): 3994-3995. DOI: https://doi.org/10.1128/JCM.41.8.3994-3995.2003
Rokni MB. The present status of human helminthic diseases in Iran. Ann Trop Med Parasitol. 2008; 102(4): 283-295. DOI: https://doi.org/10.1179/136485908X300805
Rafique A, Rana SA, Khan HA, and Sohail A. Prevalence of some helminths in rodents captured from different city structures including poultry farms and human population of Faisalabad, Pakistan. Pak Vet J. 2009; 29(3): 141-144. Available at: http://www.pvj.com.pk/pdf-files/29_3/141-144.pdf
Medeiros VB. Endo and ectoparasites in conventionally maintained rodents laboratory animals. J Surg Clin Res. 2012; 3(1): 27-40. DOI: https://doi.org/10.20398/jscr.v3i1.3144
Goudarzi F, Mohtasebi S, Teimouri A, Yimam Y, Heydarian P, Sangani GS, et al. A systematic review and meta-analysis of Hymenolepis nana in human and rodent hosts in Iran: A remaining public health concern. Comp Immunol Microbiol Infect Dis. 2021; 74: 101580. DOI: https://doi.org/10.1016/j.cimid.2020.101580
Borji H, Sadeghi H, Razmi G, Pozio E, and La Rosa G. Trichinella infection in wildlife of northeast of Iran. Iran J Parasitol. 2012; 7(4): 57-61. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3537469/
Mowlavi G, Marucci G, Mobedi I, Zahabiioon F, Mirjalali H, and Pozio E. Trichinella britovi in a leopard (Panthera pardus saxicolor) in Iran. Vet Parasitol. 2009; 164(2-4): 350-352. DOI: https://doi.org/10.1016/j.vetpar.2009.05.001
Marucci G, La Rosa G, and Pozio E. Incorrect sequencing and taxon misidentification: An example in the Trichinella genus. J Helminthol. 2010; 84(3): 336-339. DOI: https://doi.org/10.1017/S0022149X10000131
Sadighian A, Arfaa F, and Movafagh K. Trichinella spiralis in carnivores and rodents in Isfahan, Iran. J Parasitol. 1973; 59(6): 986. https://pubmed.ncbi.nlm.nih.gov/4760650/
Fuehrer HP, Igel P, and Auer H. Capillaria hepatica in man—an overview of hepatic capillariosis and spurious infections. Parasitol Res. 2011; 109(4): 969-979. DOI: https://doi.org/10.1007/s00436-011-2494-1
Zarei Z, Mohebali M, Heidari Z, Davoodi J, Shabestari A, Haghi AM, et al. Helminth infections of Meriones persicus (Persian Jird), Mus musculus (House Mice) and Cricetulus migratorius (Grey Hamster): A cross-sectional study in Meshkin-Shahr district, northwest Iran.
Iran J Parasitol. 2016; 11(2): 213-220. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5236098/
Kazemi Aghdam M, Karimi A, Amanati A, Ghoroubi J, Khoddami M, Shamsian S, et al. Capillaria hepatica, A case report and review of the literatures. Arch Pediatr Infect Dis. 2015; 3(2): e19398. DOI: https://doi.org/10.5812/pedinfect.19398.
Dubey A, Bagchi A, Sharma D, Dey A, Nandy K, and Sharma R. Hepatic Capillariasis- Drug Targets. Infect disord – drug Targ. 2018; 18: 3-10. DOI: https://doi.org/10.2174/1871526517666170427124254
da Rocha EJG, Basano Sde A, Souza MM, Honda ER, Castro MB, Colodel EM, et al. Study of the prevalence of Capillaria hepatica in humans and rodents in an urban area of the city of Porto Velho, Rondônia, Brazil. Rev Inst Med Trop Sao Paulo, 2015; 57(1): 39-46. DOI: https://doi.org/10.1590/S0036-46652015000100006
Miller MA, Duignan PJ, Dodd E, Batac F, Staedler M, Tomoleoni JA, et al. Emergence of a zoonotic pathogen in a coastal marine sentinel: Capillaria hepatica (syn. Calodium hepaticum)-associated hepatitis in southern sea otters (Enhydra lutris nereis). Front Marine Sci. 2020; 7: 335. DOI: https://doi.org/10.3389/fmars.2020.00335
Misra S, Nanda P, Nandan D, and Sakhuja P. Capillaria hepatica: Report from North India. Trop Gastroenterol. 2020; 40(3): 118-121. DOI: https://doi.org/10.7869/tg.551
Singla N, Singla LD, Gupta K, and Sood NK. Pathological alterations in natural cases of Capillaria hepatica infection alone and in concurrence with Cysticercus fasciolaris in Bandicota bengalensis. J Parasit Dis. 2013; 37: 16-20. DOI: https://doi.org/10.1007/s12639-012-0121-4