Molecular Identification of Nematodes (Superfamily: Strongylida) Traced in Herbivores Excrement Found in Wildlife from Western Iran
-
Mohammad Reza Vafaei
,
Mohammad Safaie
,
Elham Kazemirad
,
Hamed Mirjalali
,
Zaynab Askari
,
Mehdi Mohebali
,
Gholamreza Mowlavi
Abstract
Background: In wildlife, the identification of parasitic infections should be pursued seriously in countries facing endangered species of animals in their geographical territories. We aimed to increase understanding of the possible role of wildlife herbivore reservoirs in the emergence of helminth infections in Kermanshah Province, western Iran.
Methods: Sixty-five feces from Gazelle (Gazella subgutturosa) (N = 36 samples) and wild goat (Capra aegagrus) (N = 14 samples) were investigated. The samples were microscopically examined for gastrointestinal helminth eggs, and genomic DNA was extracted from the identified eggs. The internal transcribed spacer 2 (ITS2) region of ribosomal DNA was amplified and sequenced. Phylogenetic analysis of the nucleotide sequences confirmed the species identity.
Results: The most common species circulating in the hosts were Teladorsagia circumcincta, Marshallagia spp., and Nematodirus oiratianus, all of which are reported in the wildlife in western Iran for the first time.
Conclusion: These findings emphasize the importance of continuously assessing the parasite status of wildlife and similar routine surveillance in domestic environments to detect and manage potential zoonotic parasite species.
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3. Kirk R. The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology. 2003;10(6):385-94.
4. Sorvillo F, Ash LR, Berlin OG, et al. Baylisascaris procyonis: an emerging helminthic zoonosis. Emerg Infect Dis. 2002;8(4):355-9.
5. Brooker S. Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers a review. Int J Parasitol. 2010;40(10):1137-44.
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7. Thumbi SM, de CBBM, Poole EJ, et al. Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology. 2013;140(14):1789-98.
8. Albon SD, Stien A, Irvine RJ, et al. The role of parasites in the dynamics of a reindeer population. Proc Biol Sci. 2002;269(1500):1625-32.
9. Hughes J, Albon SD, Irvine RJ, et al. Is there a cost of parasites to caribou? Parasitology. 2009;136(2):253-65.
10. Nadler SA, GP DEL. Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology. 2011;138(13):1688-709.
11. Gilabert A, Wasmuth JD. Unravelling parasitic nematode natural history using population genetics. Trends Parasitol. 2013;29(9):438-48.
12. Fadakar D, Bärmann EV, Lerp H, et al. Diversification and subspecies patterning of the goitered gazelle (Gazella subgutturosa) in Iran. Ecol Evol. 2020;10(12):5877-5891.
13. Phetla V, Chaisi M, Malatji M. Epidemiology and diversity of gastrointestinal tract helminths of wild ruminants in sub-Saharan Africa: a review. J Helminthol. 2024;98:e45.
14. Agosta SJ, Janz N, Brooks DR. How specialists can be generalists: resolving the" parasite paradox" and implications for emerging infectious disease. Zoologia (Curitiba). 2010;27:151-62.
15. Hrabok JT, Oksanen A, Nieminen M, et al. Reindeer as hosts for nematode parasites of sheep and cattle. Vet Parasitol. 2006;136(3-4):297-306.
16. McGhee MB, Nettles VF, Rollor EA, et al. Studies on cross-transmission and pathogenicity of Haemonchus contortus in white-tailed deer, domestic cattle and sheep. J Wildl Dis. 1981;17(3):353-64.
17. Ghadirian E, Arfaa F. Present status of trichostrongyliasis in Iran. Am J Trop Med Hyg. 1975;24(6 Pt 1):935-41.
18. Hosseinnezhad H, Sharifdini M, Ashrafi K, et al. Trichostrongyloid nematodes in ruminants of northern Iran: prevalence and molecular analysis. BMC Vet Res. 2021;17(1):371.
19. Craig TM. Gastrointestinal Nematodes, Diagnosis and Control. Vet Clin North Am Food Anim Pract. 2018;34(1):185-199.
20. Lichtenfels JR, Hoberg EP, Zarlenga DS. Systematics of gastrointestinal nematodes of domestic ruminants: advances between 1992 and 1995 and proposals for future research. Vet Parasitol. 1997;72(3-4):225-38.
21. Georgi JR, McCulloch CE. Diagnostic morphometry: identification of helminth eggs by discriminant analysis of morphometric data. 1988.
22. Ghasemikhah R, Sharbatkhori M, Mobedi I, et al. Sequence Analysis of the Second Internal Transcribed Spacer (ITS2) Region of rDNA for Species Identification of Trichostrongylus Nematodes Isolated From Domestic Livestock in Iran. Iran J Parasitol. 2012;7(2):40-6.
23. Ashrafi K, Sharifdini M, Heidari Z, et al. Zoonotic transmission of Teladorsagia circumcincta and Trichostrongylus species in Guilan province, northern Iran: molecular and morphological characterizations. BMC Infectious Diseases. 2020;20(1):28.
24. Karami M, Ghadirian T, Faizolahi K. The atlas of mammals of Iran: Jahad daneshgahi, kharazmi Branch; 2016.
25. Garcia LS. Diagnostic medical parasitology. Manual of commercial methods in clinical microbiology. 2001:274-305.
26. Chilton NB. The use of nuclear ribosomal DNA markers for the identification of bursate nematodes (order Strongylida) and for the diagnosis of infections. Animal Health Research Reviews. 2004;5(2):173-87.
27. Allwin B, Balakrishnan S, Kumar N, et al. Prevalence of gastrointestinal parasites in Gaur (Bosgaurus) and domestic cattle at interface zones of the Nilgiri Hills, Tamil Nadu, India. J Vet Sci Technol. 2016;7(1):1-6.
28. Van Wyk IC, Boomker J. Parasites of South African wildlife. XIX. The prevalence of helminths in some common antelopes, warthogs and a bushpig in the Limpopo province, South Africa. Onderstepoort J Vet Res. 2011;78(1):308.
29. Dhimal M, Kramer IM, Phuyal P, et al. Climate change and its association with the expansion of vectors and vector-borne diseases in the Hindu Kush Himalayan region: A systematic synthesis of the literature. Advances in Climate Change Research. 2021;12(3):421-429.
30. McFarland C, Rose Vineer H, Chesney L, et al. Tracking gastrointestinal nematode risk on cattle farms through pasture contamination mapping. Int J Parasitol. 2022;52(10):691-703.
31. Walker JG, Morgan ER. Generalists at the interface: Nematode transmission between wild and domestic ungulates. Int J Parasitol Parasites Wildl. 2014;3(3):242-250.
32. Halvarsson P, Baltrušis P, Kjellander P, Höglund J. Parasitic strongyle nemabiome communities in wild ruminants in Sweden. Parasit Vectors. 2022;15(1):341.
33. Modabbernia G, Meshgi B, Eslami A. Diversity and burden of helminthiasis in wild ruminants in Iran. J Parasit Dis. 2021;45(2):394-9.
34. Meradi S, Bentounsi B, Zouyed I, et al. The steppe species of gastrointestinal nematodes of small ruminants, with a focus on Marshallagia: climate as a key determinant. Parasite. 2011;18(3):261-9.
35. Said Y, Gharbi M, Mhadhbi M, et al. Molecular identification of parasitic nematodes (Nematoda: Strongylida) in feces of wild ruminants from Tunisia. Parasitology. 2018;145(7):901-911.
36. Barghandan T, Hajialilo E, Sharifdini M, et al. Prevalence and phylogenetic analysis of gastrointestinal helminths (Nematoda: Trichostrongylidae) in ruminant livestock of northwest Iran. Ankara Üniversitesi Veteriner Fakültesi Dergisi. 2019;67(1):65-71.
37. Nazarbeigy M, Yakhchali M, Pourahmad F. First Molecular Characterization and Seasonality of Larvae of Trichostrongylid Nematodes in Arrested Development in the Abomasum of Iranian Naturally Infected Sheep. Acta Parasitol. 2021;66(1):193-198.
38. Pestechian N, Kalani H, Faridnia R, et al. Zoonotic gastrointestinal nematodes (Trichostrongylidae) from sheep and goat in Isfahan, Iran. Acta Scientiae Veterinariae. 2014;42(1):1-6.
39. Naem S, Gorgani T, editors. Gastrointestinal parasitic infection of slaughtered sheep (Zel breed) in Fereidoonkenar city, Iran. Veterinary Research Forum; 2011: Faculty of Veterinary Medicine, Urmia University.
40. Ghadirian E, Arfaa F. First report of human infection with Haemonchus contortus, Ostertagia ostertagi, and Marshallagia marshalli (family Trichostrongylidae) in Iran. J Parasitol. 1973; 59(6):1144-5.
41. Malathi S, Shameem U, Komali M. Prevalence of gastrointestinal helminth parasites in domestic ruminants from Srikakulam district, Andhra Pradesh, India. J Parasit Dis. 2021;45(3):823-830.
42. Lyles AM, Dobson AP. Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine. 1993:315-326.
2. Hurd H. Physiological and behavioural interactions between parasites and invertebrate hosts. Adv Parasitol. 1990;29:271-318.
3. Kirk R. The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology. 2003;10(6):385-94.
4. Sorvillo F, Ash LR, Berlin OG, et al. Baylisascaris procyonis: an emerging helminthic zoonosis. Emerg Infect Dis. 2002;8(4):355-9.
5. Brooker S. Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers a review. Int J Parasitol. 2010;40(10):1137-44.
6. Steele J, Orsel K, Cuyler C, et al. Divergent parasite faunas in adjacent populations of west Greenland caribou: Natural and anthropogenic influences on diversity. Int J Parasitol Parasites Wildl. 2013;2:197-202.
7. Thumbi SM, de CBBM, Poole EJ, et al. Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology. 2013;140(14):1789-98.
8. Albon SD, Stien A, Irvine RJ, et al. The role of parasites in the dynamics of a reindeer population. Proc Biol Sci. 2002;269(1500):1625-32.
9. Hughes J, Albon SD, Irvine RJ, et al. Is there a cost of parasites to caribou? Parasitology. 2009;136(2):253-65.
10. Nadler SA, GP DEL. Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology. 2011;138(13):1688-709.
11. Gilabert A, Wasmuth JD. Unravelling parasitic nematode natural history using population genetics. Trends Parasitol. 2013;29(9):438-48.
12. Fadakar D, Bärmann EV, Lerp H, et al. Diversification and subspecies patterning of the goitered gazelle (Gazella subgutturosa) in Iran. Ecol Evol. 2020;10(12):5877-5891.
13. Phetla V, Chaisi M, Malatji M. Epidemiology and diversity of gastrointestinal tract helminths of wild ruminants in sub-Saharan Africa: a review. J Helminthol. 2024;98:e45.
14. Agosta SJ, Janz N, Brooks DR. How specialists can be generalists: resolving the" parasite paradox" and implications for emerging infectious disease. Zoologia (Curitiba). 2010;27:151-62.
15. Hrabok JT, Oksanen A, Nieminen M, et al. Reindeer as hosts for nematode parasites of sheep and cattle. Vet Parasitol. 2006;136(3-4):297-306.
16. McGhee MB, Nettles VF, Rollor EA, et al. Studies on cross-transmission and pathogenicity of Haemonchus contortus in white-tailed deer, domestic cattle and sheep. J Wildl Dis. 1981;17(3):353-64.
17. Ghadirian E, Arfaa F. Present status of trichostrongyliasis in Iran. Am J Trop Med Hyg. 1975;24(6 Pt 1):935-41.
18. Hosseinnezhad H, Sharifdini M, Ashrafi K, et al. Trichostrongyloid nematodes in ruminants of northern Iran: prevalence and molecular analysis. BMC Vet Res. 2021;17(1):371.
19. Craig TM. Gastrointestinal Nematodes, Diagnosis and Control. Vet Clin North Am Food Anim Pract. 2018;34(1):185-199.
20. Lichtenfels JR, Hoberg EP, Zarlenga DS. Systematics of gastrointestinal nematodes of domestic ruminants: advances between 1992 and 1995 and proposals for future research. Vet Parasitol. 1997;72(3-4):225-38.
21. Georgi JR, McCulloch CE. Diagnostic morphometry: identification of helminth eggs by discriminant analysis of morphometric data. 1988.
22. Ghasemikhah R, Sharbatkhori M, Mobedi I, et al. Sequence Analysis of the Second Internal Transcribed Spacer (ITS2) Region of rDNA for Species Identification of Trichostrongylus Nematodes Isolated From Domestic Livestock in Iran. Iran J Parasitol. 2012;7(2):40-6.
23. Ashrafi K, Sharifdini M, Heidari Z, et al. Zoonotic transmission of Teladorsagia circumcincta and Trichostrongylus species in Guilan province, northern Iran: molecular and morphological characterizations. BMC Infectious Diseases. 2020;20(1):28.
24. Karami M, Ghadirian T, Faizolahi K. The atlas of mammals of Iran: Jahad daneshgahi, kharazmi Branch; 2016.
25. Garcia LS. Diagnostic medical parasitology. Manual of commercial methods in clinical microbiology. 2001:274-305.
26. Chilton NB. The use of nuclear ribosomal DNA markers for the identification of bursate nematodes (order Strongylida) and for the diagnosis of infections. Animal Health Research Reviews. 2004;5(2):173-87.
27. Allwin B, Balakrishnan S, Kumar N, et al. Prevalence of gastrointestinal parasites in Gaur (Bosgaurus) and domestic cattle at interface zones of the Nilgiri Hills, Tamil Nadu, India. J Vet Sci Technol. 2016;7(1):1-6.
28. Van Wyk IC, Boomker J. Parasites of South African wildlife. XIX. The prevalence of helminths in some common antelopes, warthogs and a bushpig in the Limpopo province, South Africa. Onderstepoort J Vet Res. 2011;78(1):308.
29. Dhimal M, Kramer IM, Phuyal P, et al. Climate change and its association with the expansion of vectors and vector-borne diseases in the Hindu Kush Himalayan region: A systematic synthesis of the literature. Advances in Climate Change Research. 2021;12(3):421-429.
30. McFarland C, Rose Vineer H, Chesney L, et al. Tracking gastrointestinal nematode risk on cattle farms through pasture contamination mapping. Int J Parasitol. 2022;52(10):691-703.
31. Walker JG, Morgan ER. Generalists at the interface: Nematode transmission between wild and domestic ungulates. Int J Parasitol Parasites Wildl. 2014;3(3):242-250.
32. Halvarsson P, Baltrušis P, Kjellander P, Höglund J. Parasitic strongyle nemabiome communities in wild ruminants in Sweden. Parasit Vectors. 2022;15(1):341.
33. Modabbernia G, Meshgi B, Eslami A. Diversity and burden of helminthiasis in wild ruminants in Iran. J Parasit Dis. 2021;45(2):394-9.
34. Meradi S, Bentounsi B, Zouyed I, et al. The steppe species of gastrointestinal nematodes of small ruminants, with a focus on Marshallagia: climate as a key determinant. Parasite. 2011;18(3):261-9.
35. Said Y, Gharbi M, Mhadhbi M, et al. Molecular identification of parasitic nematodes (Nematoda: Strongylida) in feces of wild ruminants from Tunisia. Parasitology. 2018;145(7):901-911.
36. Barghandan T, Hajialilo E, Sharifdini M, et al. Prevalence and phylogenetic analysis of gastrointestinal helminths (Nematoda: Trichostrongylidae) in ruminant livestock of northwest Iran. Ankara Üniversitesi Veteriner Fakültesi Dergisi. 2019;67(1):65-71.
37. Nazarbeigy M, Yakhchali M, Pourahmad F. First Molecular Characterization and Seasonality of Larvae of Trichostrongylid Nematodes in Arrested Development in the Abomasum of Iranian Naturally Infected Sheep. Acta Parasitol. 2021;66(1):193-198.
38. Pestechian N, Kalani H, Faridnia R, et al. Zoonotic gastrointestinal nematodes (Trichostrongylidae) from sheep and goat in Isfahan, Iran. Acta Scientiae Veterinariae. 2014;42(1):1-6.
39. Naem S, Gorgani T, editors. Gastrointestinal parasitic infection of slaughtered sheep (Zel breed) in Fereidoonkenar city, Iran. Veterinary Research Forum; 2011: Faculty of Veterinary Medicine, Urmia University.
40. Ghadirian E, Arfaa F. First report of human infection with Haemonchus contortus, Ostertagia ostertagi, and Marshallagia marshalli (family Trichostrongylidae) in Iran. J Parasitol. 1973; 59(6):1144-5.
41. Malathi S, Shameem U, Komali M. Prevalence of gastrointestinal helminth parasites in domestic ruminants from Srikakulam district, Andhra Pradesh, India. J Parasit Dis. 2021;45(3):823-830.
42. Lyles AM, Dobson AP. Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine. 1993:315-326.
| Files | ||
| Issue | Vol 20 No 4 (2025) | |
| Section | Original Article(s) | |
| Keywords | ||
| Strongylida Western Iran Herbivores Parasitology | ||
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How to Cite
1.
Vafaei MR, Safaie M, Kazemirad E, Mirjalali H, Askari Z, Mohebali M, Mowlavi G. Molecular Identification of Nematodes (Superfamily: Strongylida) Traced in Herbivores Excrement Found in Wildlife from Western Iran. Iran J Parasitol. 2025;20(4):573-583.
