Prevalence and Seasonality of Adult and Arrested Larvae of Gastrointestinal Nematodes of Sheep from Mashhad City, Northeastern Iran
-
Abbas Jadidoleslami
,
Abolghasem Siyadatpanah
,
Hassan Borji
,
Mehdi Zarean
,
Lida Jarahi
,
Elham Moghaddas
,
Christine M. Budke
Abstract
Background: This study was conducted to determine the prevalence and intensity of nematode infections in sheep located in northeastern Iran from Apr 2018 to Mar 2019.
Methods: Gastrointestinal nematodes of 300 sheep were inspected. The season of slaughter, anatomic location where the parasite was located, the animal’s sex, infection prevalence and intensity were recorded. Seasonal differences in arrested larvae numbers also were assessed using Cochran's Q test.
Results: Overall, 4,331 adult nematode specimens were collected. Among the examined sheep, 53% (159/300) were infected with one or more nematode species. Among infected sheep, 42.8% were infected with a single species of nematode, 26.4% were infected with two species of nematodes, and 30.8% were infected with three or more species of nematodes. Marshallagia marshalli (13.3%) was the most common nematode recovered from the abomasums of infected sheep, while Trichostrongylus vitrinus (4.6%) was commonly recovered from the small intestines, and Trichuris ovis (25.6%) was commonly recovered from the large intestines. In total, 463 arrested larvae were found in the abomasums of 7.5% of infected sheep and 104 arrested larvae were found in the small intestines of 8.8% of infected sheep. A significantly higher numbers of arrested larvae were found in summer compared to autumn (P<0.001).
Conclusion: Intestinal parasites continue to be a problem for sheep in northeastern Iran and additional control measures need to be explored.
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2. Kamalzadeh A, Rajabbaigy M, Kiasat A. Livestock production systems and trends in livestock industry in Iran. J Agri Soc Sci, 2008; 4:183-88.
3. Padula A. Gastrointestinal nematodes of sheep and cattle: biology and control. Aust Vet J. 2011; 1(89):54-54.
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5. Sharma, D.K, Paul S, Gururaj K. Gastrointestinal Helminthic Challenges in Sheep and Goats in Afro-Asian Region: A Review. J Anim Res. 2020; 10(1):1-18.
6. Borji H., Raji AR, Naghibi AG. The comparative morphology of Marshallagia marshalli and Ostertagia occidentalis (Nematoda: Strongylida, Trichostrongylidae) by scanning electron microscopy. Parasitol Res. 2011; 108(6):1391-1395.
7. Naem S, Gorgani T. Gastrointestinal parasitic infection of slaughtered sheep (Zel breed) in Fereidoonkenar city, Iran. Vet Res Forum. 2011; 2(4):238-241
8. Moghaddar N, Afrahi A. Gastrointestinal helminthosis in sheep in Iran. J Vet Parasitol. 2008; 22(1):41-44.
9. Langrová I,Jankovská I. Arrested development of Trichostrongylus colubriformis in experimentally infected rabbits. Effect of decreasing photoperiod, low temperature and desiccation. Helminthologia. 2004; 41(2):85-90.
10. Fernández A, Fiel C, SteffanP. Study on the inductive factors of hypobiosis of Ostertagia ostertagi in cattle. Vet Parasitol. 1999; 81(4):295-307.
11. 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.
12. Rahimi Esboei B, Mobedi I, Mizani A, et al. A Seasonal Survey on the Helminths Infections of the Ruminants Slaughtered in the Abattoirs of Mazandaran Province, Northern Iran. J Hum Environ Health Promot. 2020; 6(3):142-146.
13. Acharya AS, Prakash A, Saxena P, et al. Sampling: Why and how of it. Indian Journal of Medical Specialties. 2013; 4(2):330-333.
14. Bogale M, Baniya A, DiGennaro P. Nematode identification techniques and recent advances. Plants (Basel). 2020; 9(10):1260.
15. Giangaspero M, Bahhady FA, Orita G, et al. Effect of gastrointestinal parasite and lungworm control on survivability and fertility of ewes in farm flocks in Syria. Trop Anim Health Prod. 1992; 78:594-597.
16. Roeber F, Jex AR, Gasser RB. Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance-an Australian perspective. Parasite Vector. 2013; 6:153.
17. Eslami A, Ashrafihelan J, Vahedi N. Study on the prevalence and pathology of Gongylonema pulchrum (gullet worm) of sheep from Iran. Glob Vet. 2010; 5(1):45-48.
18. Movassaghi A, Razmi G. Oesophageal and gastric gongylonemiasis in a donkey. Iran J Vet Res. 2008; 9(1):84-86.
19. Halajian A,Eslami A, Salehi M, et al. Incidence and genetic characterization of Gongylonema pulchrum in cattle slaughtered in Mazandaran Province, northern Iran. Iran J Parasitol, 2010; 5(2):10-8.
20. Eslami A, Nabavi L. Species of gastro-intestinal nematodes of sheep from Iran. Bull Soc Pathol Exot Filiales. 1976; 69(1):92-95.
21. Eslami A, Meydani M, Maleki SH, et al., Gastrointestinal nematodes of wild sheep (Ovis orientalis) from Iran. J Wildl Dis. 1979; 15(2):263-265.
22. Sazmand A, Ehsani-Barahman S, Moradi H, et al. Esophageal gongylonemosis in ruminants slaughtered in Hamedan and Babol, Iran. Journal of Zoonotic Diseases. 2020; 4(2):56-63.
23. Mowlavi G, Mikaeili E, Mobedi I, et al. A survey of dung beetles infected with larval nematodes with particular note on copris lunaris beetles as a vector for Gongylonema sp. in Iran. Korean J Parasitol. 2009;47(1):13-7.
24. Nabavi R,Eslami A , Shokrani HR, et al., Study on the prevalence, intensity and seasonal dynamics of abomasal helminths in sheep from different climatic zones of Iran. World Applied Sciences Journal. 2011; 12(4):441-445.
25. Hakimzadegan M, Khosroshahi MK. Prevalence of abomasal nematodes in slaughtered goats at industrial Urmia slaughterhouse, West Azerbaijan Province, Northwest of Iran. J Animal Poult Sci. 2013;2(4):120-124.
26. Shahbazi A, Fallah E, Koshki MHK, et al. Morphological characterization of the Trichostrongylus species isolated from sheep in Tabriz, Iran. Res Opin Anim Vet Sci. 2012;2(5):309-312.
27. Umur Ş, Yukari BA. An abattoir survey of gastro-intestinal nematodes in sheep in the Burdur region, Turkey. Turk J Vet Anim Sci. 2005; 29(5):1195-1201.
28. Pestechian N, Kalani H, Faridnia R, et al. Zoonotic gastrointestinal nematodes (Trichostrongylidae) from sheep and goat in Isfahan, Iran. Acta Sci Vet. 2014;42(1): 1-6.
29. Ghasemikhah R, Mirhendi H, Kia EB, et al. Morphological and morphometrical description of Trichostrongylus species isolated from domestic ruminants in Khuzestan province, southwest Iran. Iran J Parasitol. 2011; 6(3):82–88.
30. Gharekhani J, Gerami-Sadeghian A, Yousefi M. Parasitic helminth infections in native sheep (Mehraban) in Hamedan, Iran. J Adv Vet Anim Res. 2015;2(2):115-119.
31. Lone BA , Chishti I, Fayaz A, et al. A survey of gastrointestinal helminth parasites of slaughtered sheep and goats in Ganderbal, Kashmir. Glob Vet. 2012;8(4):338-341.
32. Bersissa K,Tigist T, Teshale S, et al. Helminths of sheep and goats in central Oromia (Ethiopia) during the dry season. J Anim Vet Adv. 2011;10(14):1845-1849.
33. Kianifard L, Naem S, Kianifard D. An Investigation on Trichuris Species in Slaughtered Goats in Urmia. Int J Livest Res. 2013; 3(2): 122-129
34. Foreyt WJ. Veterinary parasitology reference manual. John Wiley & Sons. 2013
35. Gibbs H. Mechanisms of survival of nematode parasites with emphasis on hypobiosis. Vet Parasitol. 1982;11(1):25-48.
36. Armour J, Duncan M. Arrested larval development in cattle nematodes. Parasitol Today. 1987; 3(6):171-176.
37. Michel J, Houshmand-Rad P. Arrested larval development of nematodes in sheep in southern Iran. Parasitol. 1978;77:15-18.
38. Meradi S, Cabaret J, Bentounsi B. Arrested development of abomasal trichostrongylid nematodes in lambs in a steppe environment (North-Eastern Algeria). Parasite. 2016; 23:39.
39. Giangaspero M, Bahhady FA, Orita G, et al. Summer-arrested larval development of abomasal tricostrongylids in Awassi sheep in semi-arid areas of northwest Syria. Parasitol Res. 1992;78(7):594–597.
40. McRae KM, Stear MJ, Good B, et al. The host immune response to gastrointestinal nematode infection in sheep. Parasite Immunol. 2015; 37(12):605-613.
41. Urquhart G, Armure J, Dincan JL et al. Veterinary parasitology.(2nd edn), Black Well Science. The University of Glaskow, Scotland, UK, 1996;181-188.
42. Dafur, B, Mbap ST, Tok CC, et al. Breed and environmental factors influencing prevalence of helminths in sheep. Nig J Anim Prod. 2020; 47(5):13–28.
43. El-Azazy O. Seasonal changes and inhibited development of the abomasal nematodes of sheep and goats in Saudi Arabia. Vet Parasitol. 1995; 58(1-2):91-98.
44. Blitz N, Gibbs H. Studies on the arrested development of Haemonchus contortus in sheep—I. The induction of arrested development. Int J Parasitol. 1972. 2(1): 5-12.
45. Carlsson, A.M., Irvine RJ, Wilson K, et al. Disease transmission in an extreme environment: nematode parasites infect reindeer during the Arctic winter. Int J Parasitol. 2012; 42(8):789-795.
46. El-Azazy O. Absence of hypobiosis in abomasal nematodes of sheep and goats in Egypt. Vet Parasitol. 1990; 37(1):55-60.
2. Kamalzadeh A, Rajabbaigy M, Kiasat A. Livestock production systems and trends in livestock industry in Iran. J Agri Soc Sci, 2008; 4:183-88.
3. Padula A. Gastrointestinal nematodes of sheep and cattle: biology and control. Aust Vet J. 2011; 1(89):54-54.
4. Elseadawy R.M, Alaraby MA, Abbas IE, et al. Prevalence of Trichostrongyle eggs infecting sheep and goats in Dakahlia Governorate, Egypt. J. Egypt. Soc. Parasitol. 2018; 14(2):121-136.
5. Sharma, D.K, Paul S, Gururaj K. Gastrointestinal Helminthic Challenges in Sheep and Goats in Afro-Asian Region: A Review. J Anim Res. 2020; 10(1):1-18.
6. Borji H., Raji AR, Naghibi AG. The comparative morphology of Marshallagia marshalli and Ostertagia occidentalis (Nematoda: Strongylida, Trichostrongylidae) by scanning electron microscopy. Parasitol Res. 2011; 108(6):1391-1395.
7. Naem S, Gorgani T. Gastrointestinal parasitic infection of slaughtered sheep (Zel breed) in Fereidoonkenar city, Iran. Vet Res Forum. 2011; 2(4):238-241
8. Moghaddar N, Afrahi A. Gastrointestinal helminthosis in sheep in Iran. J Vet Parasitol. 2008; 22(1):41-44.
9. Langrová I,Jankovská I. Arrested development of Trichostrongylus colubriformis in experimentally infected rabbits. Effect of decreasing photoperiod, low temperature and desiccation. Helminthologia. 2004; 41(2):85-90.
10. Fernández A, Fiel C, SteffanP. Study on the inductive factors of hypobiosis of Ostertagia ostertagi in cattle. Vet Parasitol. 1999; 81(4):295-307.
11. 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.
12. Rahimi Esboei B, Mobedi I, Mizani A, et al. A Seasonal Survey on the Helminths Infections of the Ruminants Slaughtered in the Abattoirs of Mazandaran Province, Northern Iran. J Hum Environ Health Promot. 2020; 6(3):142-146.
13. Acharya AS, Prakash A, Saxena P, et al. Sampling: Why and how of it. Indian Journal of Medical Specialties. 2013; 4(2):330-333.
14. Bogale M, Baniya A, DiGennaro P. Nematode identification techniques and recent advances. Plants (Basel). 2020; 9(10):1260.
15. Giangaspero M, Bahhady FA, Orita G, et al. Effect of gastrointestinal parasite and lungworm control on survivability and fertility of ewes in farm flocks in Syria. Trop Anim Health Prod. 1992; 78:594-597.
16. Roeber F, Jex AR, Gasser RB. Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance-an Australian perspective. Parasite Vector. 2013; 6:153.
17. Eslami A, Ashrafihelan J, Vahedi N. Study on the prevalence and pathology of Gongylonema pulchrum (gullet worm) of sheep from Iran. Glob Vet. 2010; 5(1):45-48.
18. Movassaghi A, Razmi G. Oesophageal and gastric gongylonemiasis in a donkey. Iran J Vet Res. 2008; 9(1):84-86.
19. Halajian A,Eslami A, Salehi M, et al. Incidence and genetic characterization of Gongylonema pulchrum in cattle slaughtered in Mazandaran Province, northern Iran. Iran J Parasitol, 2010; 5(2):10-8.
20. Eslami A, Nabavi L. Species of gastro-intestinal nematodes of sheep from Iran. Bull Soc Pathol Exot Filiales. 1976; 69(1):92-95.
21. Eslami A, Meydani M, Maleki SH, et al., Gastrointestinal nematodes of wild sheep (Ovis orientalis) from Iran. J Wildl Dis. 1979; 15(2):263-265.
22. Sazmand A, Ehsani-Barahman S, Moradi H, et al. Esophageal gongylonemosis in ruminants slaughtered in Hamedan and Babol, Iran. Journal of Zoonotic Diseases. 2020; 4(2):56-63.
23. Mowlavi G, Mikaeili E, Mobedi I, et al. A survey of dung beetles infected with larval nematodes with particular note on copris lunaris beetles as a vector for Gongylonema sp. in Iran. Korean J Parasitol. 2009;47(1):13-7.
24. Nabavi R,Eslami A , Shokrani HR, et al., Study on the prevalence, intensity and seasonal dynamics of abomasal helminths in sheep from different climatic zones of Iran. World Applied Sciences Journal. 2011; 12(4):441-445.
25. Hakimzadegan M, Khosroshahi MK. Prevalence of abomasal nematodes in slaughtered goats at industrial Urmia slaughterhouse, West Azerbaijan Province, Northwest of Iran. J Animal Poult Sci. 2013;2(4):120-124.
26. Shahbazi A, Fallah E, Koshki MHK, et al. Morphological characterization of the Trichostrongylus species isolated from sheep in Tabriz, Iran. Res Opin Anim Vet Sci. 2012;2(5):309-312.
27. Umur Ş, Yukari BA. An abattoir survey of gastro-intestinal nematodes in sheep in the Burdur region, Turkey. Turk J Vet Anim Sci. 2005; 29(5):1195-1201.
28. Pestechian N, Kalani H, Faridnia R, et al. Zoonotic gastrointestinal nematodes (Trichostrongylidae) from sheep and goat in Isfahan, Iran. Acta Sci Vet. 2014;42(1): 1-6.
29. Ghasemikhah R, Mirhendi H, Kia EB, et al. Morphological and morphometrical description of Trichostrongylus species isolated from domestic ruminants in Khuzestan province, southwest Iran. Iran J Parasitol. 2011; 6(3):82–88.
30. Gharekhani J, Gerami-Sadeghian A, Yousefi M. Parasitic helminth infections in native sheep (Mehraban) in Hamedan, Iran. J Adv Vet Anim Res. 2015;2(2):115-119.
31. Lone BA , Chishti I, Fayaz A, et al. A survey of gastrointestinal helminth parasites of slaughtered sheep and goats in Ganderbal, Kashmir. Glob Vet. 2012;8(4):338-341.
32. Bersissa K,Tigist T, Teshale S, et al. Helminths of sheep and goats in central Oromia (Ethiopia) during the dry season. J Anim Vet Adv. 2011;10(14):1845-1849.
33. Kianifard L, Naem S, Kianifard D. An Investigation on Trichuris Species in Slaughtered Goats in Urmia. Int J Livest Res. 2013; 3(2): 122-129
34. Foreyt WJ. Veterinary parasitology reference manual. John Wiley & Sons. 2013
35. Gibbs H. Mechanisms of survival of nematode parasites with emphasis on hypobiosis. Vet Parasitol. 1982;11(1):25-48.
36. Armour J, Duncan M. Arrested larval development in cattle nematodes. Parasitol Today. 1987; 3(6):171-176.
37. Michel J, Houshmand-Rad P. Arrested larval development of nematodes in sheep in southern Iran. Parasitol. 1978;77:15-18.
38. Meradi S, Cabaret J, Bentounsi B. Arrested development of abomasal trichostrongylid nematodes in lambs in a steppe environment (North-Eastern Algeria). Parasite. 2016; 23:39.
39. Giangaspero M, Bahhady FA, Orita G, et al. Summer-arrested larval development of abomasal tricostrongylids in Awassi sheep in semi-arid areas of northwest Syria. Parasitol Res. 1992;78(7):594–597.
40. McRae KM, Stear MJ, Good B, et al. The host immune response to gastrointestinal nematode infection in sheep. Parasite Immunol. 2015; 37(12):605-613.
41. Urquhart G, Armure J, Dincan JL et al. Veterinary parasitology.(2nd edn), Black Well Science. The University of Glaskow, Scotland, UK, 1996;181-188.
42. Dafur, B, Mbap ST, Tok CC, et al. Breed and environmental factors influencing prevalence of helminths in sheep. Nig J Anim Prod. 2020; 47(5):13–28.
43. El-Azazy O. Seasonal changes and inhibited development of the abomasal nematodes of sheep and goats in Saudi Arabia. Vet Parasitol. 1995; 58(1-2):91-98.
44. Blitz N, Gibbs H. Studies on the arrested development of Haemonchus contortus in sheep—I. The induction of arrested development. Int J Parasitol. 1972. 2(1): 5-12.
45. Carlsson, A.M., Irvine RJ, Wilson K, et al. Disease transmission in an extreme environment: nematode parasites infect reindeer during the Arctic winter. Int J Parasitol. 2012; 42(8):789-795.
46. El-Azazy O. Absence of hypobiosis in abomasal nematodes of sheep and goats in Egypt. Vet Parasitol. 1990; 37(1):55-60.
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| Issue | Vol 17 No 2 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v17i2.9539 | |
| Keywords | ||
| Sheep Gastrointestinal nematode Hypobiosis Iran | ||
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How to Cite
1.
Jadidoleslami A, Siyadatpanah A, Borji H, Zarean M, Jarahi L, Moghaddas E, Budke C. Prevalence and Seasonality of Adult and Arrested Larvae of Gastrointestinal Nematodes of Sheep from Mashhad City, Northeastern Iran. Iran J Parasitol. 2022;17(2):214-222.
