Seroprevalence and Endemic Status of Babesia ovis by Enzyme-Linked Immunosorbent Assay in East Azerbaijan Province, North-West of Iran
,
Abstract
Background: Babesia ovis, an intraerythrocytic parasite carried by ticks and one of the most common subclinical ovine illnesses, was studied to ascertain its seroprevalence and endemic status in ram and ewe populations in East Azerbaijan Province, Iran, in lambs, yearlings, and adults of over two years of age.
Methods: A total of 960 sheep from 10 cities were selected from Jan 2018 to Nov 2019. Blood samples were collected from each animal and tested for the presence of B. ovis antibodies by applying a developed enzyme-linked immunosorbent assay (ELISA) technique. Checkerboard titrations were used to determine the optimal dilution of the antigen using negative and positive control sera. To determine whether the disease is endemically stable, inoculation rates for each age group were also calculated. Correlation coefficients were calculated between age and infection rates and also between age and inoculation rates.
Results: The results revealed an average infection rate of 49.4% in East Azerbaijan Province. There was a positive correlation between the age of animals and susceptibility to infection except for lambs and yearlings, whereas there was no meaningful difference in exposure to B. ovis between rams and ewes. The negative correlation between age and inoculation rates indicates increased disease instability with age. Inoculation rate results revealed the endemically instable status of B. ovis in the studied area.
Conclusion: High prevalence rates and endemically instable status of the disease suggest demand for vaccine development and implementation of appropriate control measures for ovine babesiosis to mitigate the associated economic losses.
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2. Altay K, Dumanli N, Aktas M (2007) Mo-lecular identification, genetic diversi¬ty and distribution of Theileria and Babe¬sia species infecting small ruminants. Vet Par¬asitol. 147(1–2): 161–165.
3. Song R, Wang Q, Guo F, Liu X, Song S, Chen C, Tu C, Wureli H, Wang Y (2018) Detection of Babesia spp., Theileria spp. and Anaplasma ovis in Border Regions, northwestern China. Transbound Emerg Dis. 65(6): 1537–1544.
4. Spotin A, Dalir F, Hazratian T, Shekarchi AA, Mahami-Oskouei M, Farmani M, Dolatkhah A, Ahmadpour E (2023) Glob-al haplotype distribution of Babesia ovis inferred by 18S rRNA sequences; a phy-lo¬geographical systematic review. Mi¬crob Pathog. 181: 106179.
5. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani K, Jalilza-deh- Amin G, Golabi M, Arjmand J (2014) PCR-based detection of Babesia ovis in Rhipicephalus bursa and small rumi¬nants. J Parasitol Res. 2014: 294704.
6. Shayan P, Hooshmand E, Rahbari S, Na-bian S (2007) Determination of Rhip-iceph¬a¬lus spp. as vectors for Babesia ovis in Iran. Parasitol Res. 101(4): 1029–1033.
7. Razmi G, Pourhosseini M, Yaghfouri S, Rashidi A, Seidabadi M (2013) Molecu¬lar detection of Theileria spp. and Babe¬sia spp. in sheep and ixodid ticks from the northeast of Iran. J Parasitol. 99(1): 77–81.
8. Hurtado A, Barandika JF, Oporto B, Min-guijón E, Povedano I, García-Pérez AL (2015) Risks of suffering tick-borne dis-eases in sheep translocated to a tick in-fested area: A laboratory approach for the investigation of an outbreak. Ticks Tick Borne Dis. 6(1): 31–37.
9. Hashemi-Fesharki R (1997) Tick-borne dis-eases of sheep and goats and their re¬lated vectors in Iran. Parassitologia. 39(2): 115–117.
10. Friedhoff KT (1997) Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parassitolo-gia. 39(2): 99–109.
11. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani K, Golabi M, Arjmand J, Kazemnia A, Jalil¬zadeh G (2015) Determination of preva¬lence and risk factors of infection with Babesia ovis in small ruminants from West Azerbaijan Province, Iran by poly¬merase chain reac-tion. J Arthropod Borne Dis. 9(2): 246–252.
12. Hasheminasab SS, Moradi P, Wright I (2018) A four year epidemiological and chemotherapy survey of babesiosis and theil¬eriosis, and tick vectors in sheep, cat-tle and goats in Dehgolan, Iran. Ann Par-asitol. 64(1): 43–48.
13. Ocaido M, Muwazi RT, Opuda JA (2009) Economic impact of ticks and tick-borne diseases on cattle production systems around Lake Mburo National Park in South Western Uganda. Trop Anim Health Prod. 41(5): 731–739.
14. Yadufashije C, Habyarimana T (2019) Epi¬demiological Studies and Validity of Di¬agnostic Test. Am J Biomed Sci. 11(1): 1–14.
15. Guo S, Yuan Z, Wu G, Wang W, Ma D, Du H (2002) Epidemiology of ovine theileriosis in Ganan region, Gansu Prov-ince, China. Parasitol Res. 88(Suppl 1): S36–37.
16. Calder JA, Reddy GR, Chieves L, Court-ney CH, Littell R, Livengood JR, Norval RA, Smith C, Dame JB (1996) Monitor-ing Babesia bovis infections in cattle by using PCR-based tests. J Clin Microbiol. 34(11): 2748–2755.
17. Tumwebaze MA, Byamukama B, Tayeb-wa DS, Byaruhanga J, Angwe MK, Galon EM, Liu M, Lee SH, Ringo AE, Adjou Moumouni PF, Li J (2020) First molecu¬lar detection of Babesia ovis, Theileria spp., Anaplasma spp., and Ehrlichia ru¬mi¬nantium in Goats from Western Ugan¬da. Pathogens. 9(11): 895.
18. Aktaş M, Altay K, Dumanli N (2005) De-velopment of a polymerase chain reaction method for diagnosis of Babesia ovis in-fection in sheep and goats. Vet Parasitol. 133(4): 277–281.
19. Passos LM, Bell-Sakyi L, Brown CG (1998) Immunochemical characterization of in vitro culture-derived antigens of Babesia bovis and Babesia bigemina. Vet Parasi¬tol. 76(4): 239–249.
20. Waltisbuhl DJ, Goodger BV, Wright IG, Commins MA, Mahoney DF (1987) An enzyme linked immunosorbent assay to diagnose Babesia bovis infection in cat¬tle. Parasitol Res. 73(2): 126–131.
21. Furuta PI, Oliveira TMFDS, Teixeira MCA, Rocha AGR, Machado RZ, Tinucci-Costa M (2009) Comparison between a soluble antigen-based ELISA and IFAT in detect¬ing antibodies against Babesia canis in dogs. Rev Bras Parasitol Vet. 18(03): 41–45.
22. Bazmani A, Abolhooshyar A, Imani-Baran A, Akbari H (2018) Semi-nested poly¬mer¬ase chain reaction-based detec-tion of Babe¬sia spp. in small ruminants from north¬west of Iran. Vet World. 11(3): 268–273.
23. Habibi G, Sepahvand-Mohammadi E, Af-shari A, Bozorgi S (2020) Molecular de-tection of Theileria spp. and Babesia ovis infection in sheep in Baneh, Iran. Arch Razi Inst. 75(2): 289–296.
24. Gholamreza S, Somaieh M, Roya S, Ali-reza B, Ghazale A, Yasin B (2017) First detection of Babesia ovis in Dermacentor spp in Ardabil area, northwest of Iran. J
Vector Borne Dis. 54(3): 277–281.
25. Mahoney D, Ross D (1972) Epizooti-ological factors in the control of bovine babesiosis. Aust Vet J. 48(5): 292–298.
26. Hashemzadeh Farhang H, Nabavi L, Sey-fiabad Shapouri MR, Rahbari S, Azizi F (2006) Development of an ELISA tech-nique for the detection of Babesia ovis and serological survey of the parasite in Khouzestan Province, southern Iran. Iran J Vet Res. 7(2): 53–58.
27. Ekici OD, Sevinc F, Isik N (2012) Insta-bility of ovine babesiosis in an endemic area in Turkey. Vet Parasitol. 188(3–4): 372–375.
28. Razmi GR, Naghibi A, Aslani MR, Fathi-vand M, Dastjerdi K (2002) An epidemi-ological study on ovine babesiosis in the Mashhad suburb area, province of Khora-san, Iran. Vet Parasitol. 108(2): 109–115.
29. Ceylan O, Sevinc F (2020) Endemic insta-bility of ovine babesiosis in Turkey: A country-wide sero-epidemiological study. Vet Parasitol. 278: 109034.
30. Böse R, Jorgensen WK, Dalgliesh RJ, Friedhoff KT, de Vos AJ (1995) Current state and future trends in the diagnosis of babesiosis. Vet Parasitol. 57(1–3): 61–74.
31. Lahariya C (2016) Vaccine epidemiolo¬gy: A review. J Family Med Prim Care. 5(1): 7–15.
32. WHO (2009) State of the World's Vac-cines and Immunization. World Health Organization, UNICEF, World Bank. 3rd edition. Available at: https://apps.who.int/iris/handle/10665/44169
33. Sevinc F, Sevinc M, Ekici OD, Yildiz R, Isik N, Aydogdu U (2013) Babesia ovis infections: Detailed clinical and labora-tory observations in the pre-and post-treatment periods of 97 field cases. Vet Parasitol. 191(1–2): 35–43.
34. Hay SI (2001) The paradox of endemic stability. Trends Parasitol. 17(7): 310–310.
35. Jonsson NN, Bock RE, Jorgensen WK, Morton JM, Stear MJ (2012) Is endemic stability of tick-borne disease in cattle a useful concept? Trends Parasitol. 28(3): 85–89.
2. Altay K, Dumanli N, Aktas M (2007) Mo-lecular identification, genetic diversi¬ty and distribution of Theileria and Babe¬sia species infecting small ruminants. Vet Par¬asitol. 147(1–2): 161–165.
3. Song R, Wang Q, Guo F, Liu X, Song S, Chen C, Tu C, Wureli H, Wang Y (2018) Detection of Babesia spp., Theileria spp. and Anaplasma ovis in Border Regions, northwestern China. Transbound Emerg Dis. 65(6): 1537–1544.
4. Spotin A, Dalir F, Hazratian T, Shekarchi AA, Mahami-Oskouei M, Farmani M, Dolatkhah A, Ahmadpour E (2023) Glob-al haplotype distribution of Babesia ovis inferred by 18S rRNA sequences; a phy-lo¬geographical systematic review. Mi¬crob Pathog. 181: 106179.
5. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani K, Jalilza-deh- Amin G, Golabi M, Arjmand J (2014) PCR-based detection of Babesia ovis in Rhipicephalus bursa and small rumi¬nants. J Parasitol Res. 2014: 294704.
6. Shayan P, Hooshmand E, Rahbari S, Na-bian S (2007) Determination of Rhip-iceph¬a¬lus spp. as vectors for Babesia ovis in Iran. Parasitol Res. 101(4): 1029–1033.
7. Razmi G, Pourhosseini M, Yaghfouri S, Rashidi A, Seidabadi M (2013) Molecu¬lar detection of Theileria spp. and Babe¬sia spp. in sheep and ixodid ticks from the northeast of Iran. J Parasitol. 99(1): 77–81.
8. Hurtado A, Barandika JF, Oporto B, Min-guijón E, Povedano I, García-Pérez AL (2015) Risks of suffering tick-borne dis-eases in sheep translocated to a tick in-fested area: A laboratory approach for the investigation of an outbreak. Ticks Tick Borne Dis. 6(1): 31–37.
9. Hashemi-Fesharki R (1997) Tick-borne dis-eases of sheep and goats and their re¬lated vectors in Iran. Parassitologia. 39(2): 115–117.
10. Friedhoff KT (1997) Tick-borne diseases of sheep and goats caused by Babesia, Theileria or Anaplasma spp. Parassitolo-gia. 39(2): 99–109.
11. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani K, Golabi M, Arjmand J, Kazemnia A, Jalil¬zadeh G (2015) Determination of preva¬lence and risk factors of infection with Babesia ovis in small ruminants from West Azerbaijan Province, Iran by poly¬merase chain reac-tion. J Arthropod Borne Dis. 9(2): 246–252.
12. Hasheminasab SS, Moradi P, Wright I (2018) A four year epidemiological and chemotherapy survey of babesiosis and theil¬eriosis, and tick vectors in sheep, cat-tle and goats in Dehgolan, Iran. Ann Par-asitol. 64(1): 43–48.
13. Ocaido M, Muwazi RT, Opuda JA (2009) Economic impact of ticks and tick-borne diseases on cattle production systems around Lake Mburo National Park in South Western Uganda. Trop Anim Health Prod. 41(5): 731–739.
14. Yadufashije C, Habyarimana T (2019) Epi¬demiological Studies and Validity of Di¬agnostic Test. Am J Biomed Sci. 11(1): 1–14.
15. Guo S, Yuan Z, Wu G, Wang W, Ma D, Du H (2002) Epidemiology of ovine theileriosis in Ganan region, Gansu Prov-ince, China. Parasitol Res. 88(Suppl 1): S36–37.
16. Calder JA, Reddy GR, Chieves L, Court-ney CH, Littell R, Livengood JR, Norval RA, Smith C, Dame JB (1996) Monitor-ing Babesia bovis infections in cattle by using PCR-based tests. J Clin Microbiol. 34(11): 2748–2755.
17. Tumwebaze MA, Byamukama B, Tayeb-wa DS, Byaruhanga J, Angwe MK, Galon EM, Liu M, Lee SH, Ringo AE, Adjou Moumouni PF, Li J (2020) First molecu¬lar detection of Babesia ovis, Theileria spp., Anaplasma spp., and Ehrlichia ru¬mi¬nantium in Goats from Western Ugan¬da. Pathogens. 9(11): 895.
18. Aktaş M, Altay K, Dumanli N (2005) De-velopment of a polymerase chain reaction method for diagnosis of Babesia ovis in-fection in sheep and goats. Vet Parasitol. 133(4): 277–281.
19. Passos LM, Bell-Sakyi L, Brown CG (1998) Immunochemical characterization of in vitro culture-derived antigens of Babesia bovis and Babesia bigemina. Vet Parasi¬tol. 76(4): 239–249.
20. Waltisbuhl DJ, Goodger BV, Wright IG, Commins MA, Mahoney DF (1987) An enzyme linked immunosorbent assay to diagnose Babesia bovis infection in cat¬tle. Parasitol Res. 73(2): 126–131.
21. Furuta PI, Oliveira TMFDS, Teixeira MCA, Rocha AGR, Machado RZ, Tinucci-Costa M (2009) Comparison between a soluble antigen-based ELISA and IFAT in detect¬ing antibodies against Babesia canis in dogs. Rev Bras Parasitol Vet. 18(03): 41–45.
22. Bazmani A, Abolhooshyar A, Imani-Baran A, Akbari H (2018) Semi-nested poly¬mer¬ase chain reaction-based detec-tion of Babe¬sia spp. in small ruminants from north¬west of Iran. Vet World. 11(3): 268–273.
23. Habibi G, Sepahvand-Mohammadi E, Af-shari A, Bozorgi S (2020) Molecular de-tection of Theileria spp. and Babesia ovis infection in sheep in Baneh, Iran. Arch Razi Inst. 75(2): 289–296.
24. Gholamreza S, Somaieh M, Roya S, Ali-reza B, Ghazale A, Yasin B (2017) First detection of Babesia ovis in Dermacentor spp in Ardabil area, northwest of Iran. J
Vector Borne Dis. 54(3): 277–281.
25. Mahoney D, Ross D (1972) Epizooti-ological factors in the control of bovine babesiosis. Aust Vet J. 48(5): 292–298.
26. Hashemzadeh Farhang H, Nabavi L, Sey-fiabad Shapouri MR, Rahbari S, Azizi F (2006) Development of an ELISA tech-nique for the detection of Babesia ovis and serological survey of the parasite in Khouzestan Province, southern Iran. Iran J Vet Res. 7(2): 53–58.
27. Ekici OD, Sevinc F, Isik N (2012) Insta-bility of ovine babesiosis in an endemic area in Turkey. Vet Parasitol. 188(3–4): 372–375.
28. Razmi GR, Naghibi A, Aslani MR, Fathi-vand M, Dastjerdi K (2002) An epidemi-ological study on ovine babesiosis in the Mashhad suburb area, province of Khora-san, Iran. Vet Parasitol. 108(2): 109–115.
29. Ceylan O, Sevinc F (2020) Endemic insta-bility of ovine babesiosis in Turkey: A country-wide sero-epidemiological study. Vet Parasitol. 278: 109034.
30. Böse R, Jorgensen WK, Dalgliesh RJ, Friedhoff KT, de Vos AJ (1995) Current state and future trends in the diagnosis of babesiosis. Vet Parasitol. 57(1–3): 61–74.
31. Lahariya C (2016) Vaccine epidemiolo¬gy: A review. J Family Med Prim Care. 5(1): 7–15.
32. WHO (2009) State of the World's Vac-cines and Immunization. World Health Organization, UNICEF, World Bank. 3rd edition. Available at: https://apps.who.int/iris/handle/10665/44169
33. Sevinc F, Sevinc M, Ekici OD, Yildiz R, Isik N, Aydogdu U (2013) Babesia ovis infections: Detailed clinical and labora-tory observations in the pre-and post-treatment periods of 97 field cases. Vet Parasitol. 191(1–2): 35–43.
34. Hay SI (2001) The paradox of endemic stability. Trends Parasitol. 17(7): 310–310.
35. Jonsson NN, Bock RE, Jorgensen WK, Morton JM, Stear MJ (2012) Is endemic stability of tick-borne disease in cattle a useful concept? Trends Parasitol. 28(3): 85–89.
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| Issue | Vol 18 No 1 (2024) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v18i1.15673 | |
| Keywords | ||
| Babesia ovis Endemic status Seroepidemiolog ELISA Iran | ||
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How to Cite
1.
Hashemzadeh Farhang H, Akbari-Shahkhosravi N. Seroprevalence and Endemic Status of Babesia ovis by Enzyme-Linked Immunosorbent Assay in East Azerbaijan Province, North-West of Iran. J Arthropod Borne Dis. 2024;18(1):68–77.
