Molecular detection of Anaplasma spp. in blood and ticks collected from sheep and goat in West Azerbaijan province, Iran
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Abstract
Background and Objectives: Anaplasmosis, an ailment affecting both captive and free-ranging small ruminants, is instigated by Anaplasma spp., a tick-vectored, obligate intracellular rickettsial bacterium. Iran's ovine and caprine populations, numbering roughly 71 million, are vital to its financial structure.
Materials and Methods: This study investigated the prevalence of Anaplasma species in sheep and goats within West Azerbaijan province. Additionally, nucleic acid specimens were isolated from gathered ticks and examined for Anaplasma spp. Through polymerase chain reaction (PCR) utilizing the major surface protein gene (groEL).
Results: Anaplasma was detected in 161 (69.0%) of 919 ovine and 82 (71.3%) of 243 caprine blood DNA extracts. Subsequently, genetic material from 426 ticks comprised of Rhipicephalus sanguineus (n=146), Rhipicephalus turanicus (n=63), Hyalomma asiaticum (n=56), Hyalomma anatolicum (n=74), and Hyalomma egebtiom (n=87) was screened for A. ovis utilizing the same methodology.
Conclusion: This research not only confirmed the presence of A. ovis within Iranian sheep and goats but also implicated ticks as a possible vector for its transmission. The findings emphasize the importance of monitoring the health status of Iran's small ruminants to detect clinical manifestations of anaplasmosis and of implementing effective tick control strategies worldwide.
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2. de la Fuente J, Estrada-Peña A, Rafael M, Almazán C, Bermúdez S, Abdelbaset AE, et al. Perception of ticks and tick-borne diseases worldwide. Pathogens 2023; 12: 1258.
3. Li Y, Li J, Xieripu G, Rizk MA, Macalanda AMC, Gan L, et al. Molecular Detection of Theileria ovis, Anaplasma ovis, and Rickettsia spp. in Rhipicephalus turanicus and Hyalomma anatolicum Collected from Sheep in Southern Xinjiang, China. Pathogens 2024; 13: 680.
4. Solomon A, Tanga BM. The First Investigation of Tick Vectors and Tick‐Borne Diseases in Extensively Managed Cattle in Alle District, Southwestern Ethiopia. Vet Med Int 2020; 2020: 8862289.
5. Sisson D, Beechler B, Jabbar A, Jolles A, Hufschmid J. Epidemiology of anaplasma marginale and anaplasma centrale infections in african buffalo (syncerus caffer) from kruger national park, South Africa. Int J Parasitol Parasites Wildl 2023; 21: 47-54.
6. Abdullah DA, Ali FF, Jasim AY, Ola-Fadunsin SD, Gimba FI, Ali MS. Clinical signs, prevalence, and hematobiochemical profiles associated with Anaplasma infections in sheep of North Iraq. Vet World 2020; 13: 1524-1527.
7. Liu Z, Ma M, Wang Z, Wang J, Peng Y, Li Y, et al. Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Appl Environ Microbiol 2012; 78: 464-470.
8. Jiménez C, Benito A, Arnal JL, Ortín A, Gómez M, López A, et al. Anaplasma ovis in sheep: Experimental infection, vertical transmission and colostral immunity. Small Rumin Res 2019; 178: 7-14.
9. Besser TE, Cassirer EF, Lisk A, Nelson D, Manlove KR, Cross PC, et al. Natural history of a bighorn sheep pneumonia epizootic: Source of infection, course of disease, and pathogen clearance. Ecol Evol 2021; 11: 14366-14382.
10. Enferadi A, Sarani S, Mohammadipour S, Hasani SJ, Ajdari A, Asl MN, et al. Molecular detection of Coxiella burnetii in ticks collected from Iran. Infect Genet Evol 2024; 118: 105562.
11. Paulo O, Pappas GJ. Analyses of the genomic variation to study cork oak evolution and adaptation: from past to future climatic changes [Doctoral dissertation]. 2018.
12. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, et al. The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 2008; 31: 241-250.
13. Rahravani M, Moravedji M, Mostafavi E, Mozoun MM, Zeeyaie AH, Mohammadi M, et al. Clinical, hematological and molecular evaluation of piroplasma and Anaplasma infections in small ruminants and tick vectors from Kurdistan province, western Iran. Res Vet Sci 2023; 159: 44-56.
14. Khan A, Muhammed AA, Nasreen N, Iqbal F, Cossio-Bayugar R, ali Sha SS, et al. Tickborne haemoparasitic diseases in small ruminants in Pakistan: Current knowledge and future perspectives. Saudi J Biol Sci 2022; 29: 2014-2025.
15. Khezri M. Seroprevalence of Anaplasma infection in sheep and cattle in Kurdistan province of Iran with an overview of one decades of its epidemiological status in Iran. JSRR 2015; 6: 26-36.
16. Mahmoudvand P, Varshosaz M, Nayebzadeh H, Rocky A, Pourmahdi Borujeni M. Study the frequency of blood parasites of sheep in Dezful suburb, southwest Iran. Iran Vet J 2019; 15: 68-78.
17. Jalali SM, Khaki Z, Kazemi B, Bandehpour M, Rahbari S, Razi Jalali M, et al. Molecular detection and identification of Anaplasma species in sheep from Ahvaz, Iran. Iran J Vet Res 2013; 14: 50-56.
18. Chadi H, Moraga-Fernández A, Sánchez-Sánchez M, Chenchouni H, de Mera IGF, Garigliany MM, et al. Molecular detection and associated risk factors of Anaplasma marginale, A. ovis and A. platys in sheep from Algeria with evidence of the absence of A. phagocytophilum. Acta Trop 2024; 249: 107040.
19. Khoobdel M, Jafari AS, Telmadarraiy Z, Sedaghat MM, Bakhshi H. Tick-borne pathogens in Iran: A meta-analysis. Asian Pac J Trop Med 2021; 14: 486-504.
20. Rivaz S, Nasiri V, Nasrabadi NT, Paykari H. Ticks analysis for molecular detection and phylogenetic evaluation of stray dogs infecting protozoa from Alborz, Iran. Microb Pathog 2024; 192: 106721.
21. Jafarbekloo A, Bakhshi H, Faghihi F, Telmadarraiy Z, Khazeni A, Oshaghi MA, et al. Molecular detection of Anaplasma and Ehrlichia infection in ticks in borderline of Iran-Afghanistan. J Biomed Sci Eng 2014; 7: 919.
22. Mostafavi SM, Khalili M, Akhtardanesh B, Nourollahifard SR, Esmaeili S. Rickettsia spp. in Rhipicephalus sanguineus sensu lato ticks collected from stray dogs in Kerman city, Iran. Ticks Tick Borne Dis 2022; 13: 101985.
23. Zakkyeh T, Ali OM, Nasibeh HV, Reza YEM, Farhang B, Fatemeh M. First molecular detection of Theileria ovis in Rhipicephalus sanguineus tick in Iran. Asian Pac J Trop Med 2012; 5: 29-32.
24. Hosseini-Chegeni A, Tavakoli M, Gh G, Telmadarraiy Z, Sharifdini M, Faghihi F, et al. Molecular detection of Anaplasma marginale and Anaplasma ovis (Rickettsiales: Anaplasmataceae) in ixodid tick species in Iran. Arch Razi Inst 2020; 75: 39-46.
25. Khademi P, Tukmechi A, Ownagh A, Enferadi A, Hadian M. Molecular detection of Coxiella burnetii in blood samples of turtles (Testudo graeca) and their associated ticks. Eur J Wildl Res 2023; 69: 116.
26. Tavassoli E, Rahimi-Asiabi N, Tavassoli M. Hyalomma aegyptium on spur-thighed tortoise (Testudo graeca) in Urmia Region West Azerbaijan, Iran. Iran J Parasitol 2007; 2: 40-47.
27. Enkhtaivan B, Narantsatsral S, Davaasuren B, Otgonsuren D, Amgalanbaatar T, Uuganbayar E, et al. Molecular detection of Anaplasma ovis in small ruminants and ixodid ticks from Mongolia. Parasitol Int 2019; 69: 47-53.
28. Shanan SMH, Abbas SF, Mohammad MK. Ixodid ticks diversity and seasonal dynamic on cattle in north, middle and south of Iraq. Syst Appl Acarol 2017; 22: 1651-1658.
29. Koc S, Aydın L, Cetin H. Tick species (Acari: Ixodida) in Antalya City, Turkey: species diversity and seasonal activity. Parasitol Res 2015; 114: 2581-2586.
30. Hosseini-Vasoukolaei N, Oshaghi MA, Shayan P, Vatandoost H, Babamahmoudi F, Yaghoobi-Ershadi MR, et al. Anaplasma infection in ticks, livestock and human in Ghaemshahr, Mazandaran Province, Iran. J Arthropod Borne Dis 2014; 8: 204-211.
31. Ullah N, Durrani AZ, Avais M, Ahmad N, Ullah S, Ullah S, et al. A first report on prevalence of caprine theileriosis and its association with host biomarkers in Southern Khyber Pakhtunkhwa, Pakistan. Small Rumin Res 2018; 159: 56-61.
32. Belkahia H, Said M Ben, El Hamdi S, Yahiaoui M, Gharbi M, Daaloul-Jedidi M, et al. First molecular identification and genetic characterization of Anaplasma ovis in sheep from Tunisia. Small Rumin Res 2014; 121: 404-410.
33. Yousefi A, Rahbari S, Shayan P, Sadeghi-dehkordi Z, Bahonar A. Molecular detection of Anaplasma marginale and Anaplasma ovis in sheep and goat in west highland pasture of Iran. Asian Pac J Trop Biomed 2017; 7: 455-459.
34. Okely M, Chen Z, Anan R, Gad-Allah S. Updated checklist of the hard ticks (Acari: Ixodidae) of Egypt, with notes of livestock host and tick-borne pathogens. Syst Appl Acarol 2022; 27: 811-838.
35. Atif FA, Ullah S, Cossío-Bayúgar R, Kashif M, Khan AU, Wu WF. Molecular Epidemiology, Seasonality and Phylogenetic Investigations of Anaplasma ovis in Small Ruminants from Diverse Agro-Climatic Regions of Punjab, Pakistan. Microorganisms 2023; 11: 2430.
36. Irshad N, Qayyum M, Hussain M, Khan MQ. Prevalence of tick infestation and theileriosis in sheep and goats. Pak Vet J 2010; 30: 178-180.
37. De Sousa WB, Diniz MF, De Carvalho MN, Lopes AJ, Yamada FH. Parasite biodiversity of Leporinus piau Fowler, 1941 (Characiformes, Anostomidae) in a lentic ecosystem from the Salgado River basin, Caatinga Domain, Brazil. Ann Parasitol 2023; 69: 79-86.
38. Perret JL, Guigoz E, Rais O, Gern L. Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitol Res 2000; 86: 554-557.
39. Dobson ADM, Taylor JL, Randolph SE. Tick (Ixodes ricinus) abundance and seasonality at recreational sites in the UK: hazards in relation to fine-scale habitat types revealed by complementary sampling methods. Ticks Tick Borne Dis 2011; 2: 67-74.
2. de la Fuente J, Estrada-Peña A, Rafael M, Almazán C, Bermúdez S, Abdelbaset AE, et al. Perception of ticks and tick-borne diseases worldwide. Pathogens 2023; 12: 1258.
3. Li Y, Li J, Xieripu G, Rizk MA, Macalanda AMC, Gan L, et al. Molecular Detection of Theileria ovis, Anaplasma ovis, and Rickettsia spp. in Rhipicephalus turanicus and Hyalomma anatolicum Collected from Sheep in Southern Xinjiang, China. Pathogens 2024; 13: 680.
4. Solomon A, Tanga BM. The First Investigation of Tick Vectors and Tick‐Borne Diseases in Extensively Managed Cattle in Alle District, Southwestern Ethiopia. Vet Med Int 2020; 2020: 8862289.
5. Sisson D, Beechler B, Jabbar A, Jolles A, Hufschmid J. Epidemiology of anaplasma marginale and anaplasma centrale infections in african buffalo (syncerus caffer) from kruger national park, South Africa. Int J Parasitol Parasites Wildl 2023; 21: 47-54.
6. Abdullah DA, Ali FF, Jasim AY, Ola-Fadunsin SD, Gimba FI, Ali MS. Clinical signs, prevalence, and hematobiochemical profiles associated with Anaplasma infections in sheep of North Iraq. Vet World 2020; 13: 1524-1527.
7. Liu Z, Ma M, Wang Z, Wang J, Peng Y, Li Y, et al. Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Appl Environ Microbiol 2012; 78: 464-470.
8. Jiménez C, Benito A, Arnal JL, Ortín A, Gómez M, López A, et al. Anaplasma ovis in sheep: Experimental infection, vertical transmission and colostral immunity. Small Rumin Res 2019; 178: 7-14.
9. Besser TE, Cassirer EF, Lisk A, Nelson D, Manlove KR, Cross PC, et al. Natural history of a bighorn sheep pneumonia epizootic: Source of infection, course of disease, and pathogen clearance. Ecol Evol 2021; 11: 14366-14382.
10. Enferadi A, Sarani S, Mohammadipour S, Hasani SJ, Ajdari A, Asl MN, et al. Molecular detection of Coxiella burnetii in ticks collected from Iran. Infect Genet Evol 2024; 118: 105562.
11. Paulo O, Pappas GJ. Analyses of the genomic variation to study cork oak evolution and adaptation: from past to future climatic changes [Doctoral dissertation]. 2018.
12. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, et al. The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 2008; 31: 241-250.
13. Rahravani M, Moravedji M, Mostafavi E, Mozoun MM, Zeeyaie AH, Mohammadi M, et al. Clinical, hematological and molecular evaluation of piroplasma and Anaplasma infections in small ruminants and tick vectors from Kurdistan province, western Iran. Res Vet Sci 2023; 159: 44-56.
14. Khan A, Muhammed AA, Nasreen N, Iqbal F, Cossio-Bayugar R, ali Sha SS, et al. Tickborne haemoparasitic diseases in small ruminants in Pakistan: Current knowledge and future perspectives. Saudi J Biol Sci 2022; 29: 2014-2025.
15. Khezri M. Seroprevalence of Anaplasma infection in sheep and cattle in Kurdistan province of Iran with an overview of one decades of its epidemiological status in Iran. JSRR 2015; 6: 26-36.
16. Mahmoudvand P, Varshosaz M, Nayebzadeh H, Rocky A, Pourmahdi Borujeni M. Study the frequency of blood parasites of sheep in Dezful suburb, southwest Iran. Iran Vet J 2019; 15: 68-78.
17. Jalali SM, Khaki Z, Kazemi B, Bandehpour M, Rahbari S, Razi Jalali M, et al. Molecular detection and identification of Anaplasma species in sheep from Ahvaz, Iran. Iran J Vet Res 2013; 14: 50-56.
18. Chadi H, Moraga-Fernández A, Sánchez-Sánchez M, Chenchouni H, de Mera IGF, Garigliany MM, et al. Molecular detection and associated risk factors of Anaplasma marginale, A. ovis and A. platys in sheep from Algeria with evidence of the absence of A. phagocytophilum. Acta Trop 2024; 249: 107040.
19. Khoobdel M, Jafari AS, Telmadarraiy Z, Sedaghat MM, Bakhshi H. Tick-borne pathogens in Iran: A meta-analysis. Asian Pac J Trop Med 2021; 14: 486-504.
20. Rivaz S, Nasiri V, Nasrabadi NT, Paykari H. Ticks analysis for molecular detection and phylogenetic evaluation of stray dogs infecting protozoa from Alborz, Iran. Microb Pathog 2024; 192: 106721.
21. Jafarbekloo A, Bakhshi H, Faghihi F, Telmadarraiy Z, Khazeni A, Oshaghi MA, et al. Molecular detection of Anaplasma and Ehrlichia infection in ticks in borderline of Iran-Afghanistan. J Biomed Sci Eng 2014; 7: 919.
22. Mostafavi SM, Khalili M, Akhtardanesh B, Nourollahifard SR, Esmaeili S. Rickettsia spp. in Rhipicephalus sanguineus sensu lato ticks collected from stray dogs in Kerman city, Iran. Ticks Tick Borne Dis 2022; 13: 101985.
23. Zakkyeh T, Ali OM, Nasibeh HV, Reza YEM, Farhang B, Fatemeh M. First molecular detection of Theileria ovis in Rhipicephalus sanguineus tick in Iran. Asian Pac J Trop Med 2012; 5: 29-32.
24. Hosseini-Chegeni A, Tavakoli M, Gh G, Telmadarraiy Z, Sharifdini M, Faghihi F, et al. Molecular detection of Anaplasma marginale and Anaplasma ovis (Rickettsiales: Anaplasmataceae) in ixodid tick species in Iran. Arch Razi Inst 2020; 75: 39-46.
25. Khademi P, Tukmechi A, Ownagh A, Enferadi A, Hadian M. Molecular detection of Coxiella burnetii in blood samples of turtles (Testudo graeca) and their associated ticks. Eur J Wildl Res 2023; 69: 116.
26. Tavassoli E, Rahimi-Asiabi N, Tavassoli M. Hyalomma aegyptium on spur-thighed tortoise (Testudo graeca) in Urmia Region West Azerbaijan, Iran. Iran J Parasitol 2007; 2: 40-47.
27. Enkhtaivan B, Narantsatsral S, Davaasuren B, Otgonsuren D, Amgalanbaatar T, Uuganbayar E, et al. Molecular detection of Anaplasma ovis in small ruminants and ixodid ticks from Mongolia. Parasitol Int 2019; 69: 47-53.
28. Shanan SMH, Abbas SF, Mohammad MK. Ixodid ticks diversity and seasonal dynamic on cattle in north, middle and south of Iraq. Syst Appl Acarol 2017; 22: 1651-1658.
29. Koc S, Aydın L, Cetin H. Tick species (Acari: Ixodida) in Antalya City, Turkey: species diversity and seasonal activity. Parasitol Res 2015; 114: 2581-2586.
30. Hosseini-Vasoukolaei N, Oshaghi MA, Shayan P, Vatandoost H, Babamahmoudi F, Yaghoobi-Ershadi MR, et al. Anaplasma infection in ticks, livestock and human in Ghaemshahr, Mazandaran Province, Iran. J Arthropod Borne Dis 2014; 8: 204-211.
31. Ullah N, Durrani AZ, Avais M, Ahmad N, Ullah S, Ullah S, et al. A first report on prevalence of caprine theileriosis and its association with host biomarkers in Southern Khyber Pakhtunkhwa, Pakistan. Small Rumin Res 2018; 159: 56-61.
32. Belkahia H, Said M Ben, El Hamdi S, Yahiaoui M, Gharbi M, Daaloul-Jedidi M, et al. First molecular identification and genetic characterization of Anaplasma ovis in sheep from Tunisia. Small Rumin Res 2014; 121: 404-410.
33. Yousefi A, Rahbari S, Shayan P, Sadeghi-dehkordi Z, Bahonar A. Molecular detection of Anaplasma marginale and Anaplasma ovis in sheep and goat in west highland pasture of Iran. Asian Pac J Trop Biomed 2017; 7: 455-459.
34. Okely M, Chen Z, Anan R, Gad-Allah S. Updated checklist of the hard ticks (Acari: Ixodidae) of Egypt, with notes of livestock host and tick-borne pathogens. Syst Appl Acarol 2022; 27: 811-838.
35. Atif FA, Ullah S, Cossío-Bayúgar R, Kashif M, Khan AU, Wu WF. Molecular Epidemiology, Seasonality and Phylogenetic Investigations of Anaplasma ovis in Small Ruminants from Diverse Agro-Climatic Regions of Punjab, Pakistan. Microorganisms 2023; 11: 2430.
36. Irshad N, Qayyum M, Hussain M, Khan MQ. Prevalence of tick infestation and theileriosis in sheep and goats. Pak Vet J 2010; 30: 178-180.
37. De Sousa WB, Diniz MF, De Carvalho MN, Lopes AJ, Yamada FH. Parasite biodiversity of Leporinus piau Fowler, 1941 (Characiformes, Anostomidae) in a lentic ecosystem from the Salgado River basin, Caatinga Domain, Brazil. Ann Parasitol 2023; 69: 79-86.
38. Perret JL, Guigoz E, Rais O, Gern L. Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitol Res 2000; 86: 554-557.
39. Dobson ADM, Taylor JL, Randolph SE. Tick (Ixodes ricinus) abundance and seasonality at recreational sites in the UK: hazards in relation to fine-scale habitat types revealed by complementary sampling methods. Ticks Tick Borne Dis 2011; 2: 67-74.
| Files | ||
| Issue | Vol 18 No 3 (2026) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v18i3.21666 | |
| Keywords | ||
| Anaplasma Ticks Sheep Goats Blood Iran | ||
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How to Cite
1.
Enferadi A, Tukmechi A, Nofouzi K, Tavakolian Z. Molecular detection of Anaplasma spp. in blood and ticks collected from sheep and goat in West Azerbaijan province, Iran. Iran J Microbiol. 2026;18(3):393-402.
