Abstract
Despite the economic importance of camels, the parasites that affect them have not received adequate attention so far and molecular studies are scarce compared to other livestock. In this study, we characterized peripheral blood microfilariae in 200 healthy one-humped camels (Camelus dromedarius) from south-east Iran by microscopy and molecular tools to receive a more detailed insight into prevalence and species that affect them. Moreover, adult specimens of the filarial nematode Dipetalonema evansi were collected from the carcass of an infected animal. Microscopic examination was performed on Giemsa-stained blood smears, and blood was also spotted on Whatman FTA® cards for DNA analysis. Genomic DNA was extracted, and PCR was carried out for the detection of filaroid helminths, followed by sequence analysis of positive samples. Four samples were positive for microfilariae by microscopy, while 16 animals (8 %) were positive by PCR. Sequence analysis revealed D. evansi in all cases. Phylogenetic analysis of a cytochrome C oxidase subunit I (COI) sequence of filaroid nematodes showed that most species in a single genus cluster in the same clade; however, D. evansi and D. gracile are not monophyletic and branch rather at the base of the tree. Further studies on the life cycle of D. evansi, specifically the identification of intermediate host(s), have become feasible with the provision of the first specific COI sequences in this study.



Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Azari-Hamidian S (2007) Checklist of Iranian mosquitoes (Diptera: Culicidae). J Vector Ecol 32:235–242
Borji H, Razmi G, Parandeh S (2009) Epidemiological study on haemoparasites of dromedary (Camelus dromedarius) in Iran. J Camel Pract Res 16:217–219
Casiraghi M, Bain O, Guerrero R et al (2004) Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol 34:191–203
Chhabra MB, Gupta S (2006) Parasitic diseases of camels—an update. 2. Helminthoses. J Camel Pract Res 13:81–87
Dakkak A, Ouhelli H (1987) Helminths and helminthoses of the dromedary. A review of the literature. Rev Sci Tech Off Int Epiz 4:447–461
Determann A, Mehlhorn H, Ghaffar FA (1997) Electron microscope observations on Onchocerca ochengi and O. fasciata (Nematoda:Filarioidea). Parasitol Res 83:591–603
El Bihari S (1985) Helminths of the camel: a review. Br Vet J 141:315–326
El Harrak M, Faye B, Bengoumi M (2011) Main pathologies of camels, breeding of camels, constraints, benefits and perspectives. In: 19th Conference of the OIE Regional Commission for Africa. OIE, Kigali, pp 1–6
Elamin EA, Mohamed GE, Fadl M, Elias S, Saleem MS, Elbashir MO (1993) An outbreak of cameline filariasis in the Sudan. Br Vet J 149:195–200
Grácio AJS, Richter J, Komnenou AT, Grácio MA (2015) Onchocerciasis caused by Onchocerca lupi: an emerging zoonotic infection. Systematic review. Parasitol Res 114:2401–2413
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hodžić A, Alić A, Fuehrer H-P, Harl J, Wille-Piazzai W, Duscher GG (2015) A molecular survey of vector-borne pathogens in red foxes (Vulpes vulpes) from Bosnia and Herzegovina. Parasit Vectors 8:88
Hussein HS, Atta el Mannan AM, el Sinnary K (1988) Onchocerca armillata Railliet and Henry, 1909 and Onchocerca gutturosa (Neumann, 1910) in camels (Camelus dromedarius L.) in the Sudan. Vet Res Commun 12:475–480
Karimi A, Rahbari S, Yousefi A (2015) Blood parasites of camels from central regions of Iran: comparative evaluation of various detection techniques and serum protein components. J Adv Parasitol 2:1–4
Kataĭtseva TV (1968) Interpretation of the development cycle of the nematode Dipetalonema evansi Lewis, 1882. Dokl Akad Nauk SSSR 180:1262–1264
Koehsler M, Soleiman A, Aspöck H, AuerH WJ (2007) Onchocerca jakutensis filariasis in humans. Emerg Infect Dis 13:1749–1752
Krueger A, Fischer P, Morales-Hojas R (2007) Molecular phylogeny of the filaria genus Onchocerca with special emphasis on Afrotropical human and bovine parasites. Acta Trop 101:1–14
Lefoulon E, Bain O, Bourret J et al (2015) Shaking the tree: multi-locus sequence typing usurps current onchocercid (filarial nematode) phylogeny. PLoS Negl Trop Dis 9(11):e0004233
Lehane MJ (2005) The biology of blood-sucking in insects. Cambridge University Press, Cambridge, UK, 2nd ed., 336pp Ministry of Agriculture Jihad (2014) Annual production report. Tehran, Iran
Mowlavi G, Massoud J, Mobedi I (1997) Hydatidosis and testicular filariasis (D. evansi) in camel (C. dromedarius) in central part of Iran. Iran J Public Health 26:21–28
Nagaty HF (1947) Dipetalonema evansi (Lewis, 1882) and its microfilaria from Camelus dromedarius. Parasitology 38:86–92
Omar MS, Raoof AM (1994) Histochemical distribution of hydrolytic enzymes in adult Onchocerca fasciata (Filarioidea: Onchocercidae). Parasitol Res 80:216–222
Omar MS, Raoof AM, Al-Amari OM (1996) Onchocerca fasciata: enzyme histochemistry and tissue distribution of various dehydrogenases in the adult female worm. Parasitol Res 82:32–37
Orihel TC, Eberhard ML (1998) Zoonotic filariasis. Clin Microbiol Rev 11:366–381
Oryan A, Valinezhad A, Bahrami S (2008) Prevalence and pathology of camel filariasis in Iran. Parasitol Res 103:1125–1131
Sazmand A, Anvari Tafti MH, Hekmatimoghaddam S, Moobedi I (2013) Dipetalonema evansi infection in camels of Iran’s central area. Pak J Biol Sci 16:647–650
Schillhorn-Van-Veen TW, Bello SI, Folaranmi DO (1976) Onchocerca armillata (Railliet and Henry, 1909) from a new host, Camelus dromedari. Rev Elev Med Vet Pays Trop 29:227–228
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 10:2731–2739
Wernery U, Kinne J, Schuster RK (2014) Camelid Infectious Disorders. OIE, Paris, pp 428–430
Xia X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30:1720–1728
Acknowledgments
We thank Dr. Mehdi Hosseini (Chief of Sistan-va-Baloochestan Provincial Veterinary Organization) and Mr. Mansour Aminzadeh (Laboratory of Parasitology, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman) for their help in preparation of the samples.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Rights and permissions
About this article
Cite this article
Sazmand, A., Eigner, B., Mirzaei, M. et al. Molecular identification and phylogenetic analysis of Dipetalonema evansi (Lewis, 1882) in camels (Camelus dromedarius) of Iran. Parasitol Res 115, 1605–1610 (2016). https://doi.org/10.1007/s00436-015-4896-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4896-y


