First detection of Ehrlichia chaffeensis, Ehrlichia canis, and Anaplasma ovis in Rhipicephalus bursa ticks collected from sheep, Turkey
Author:
Ayan A.1, Aslan Çelik B.2, Çelik Ö.Y.3, Orunç Kılınç Ö.4, Akyıldız G.5, Yılmaz A.B.6, Sayın İpek D.N.7, Oktay Ayan Ö.8, Babaoğlu A.R.9
Affiliation:
1. Department of Genetics, Faculty of Veterinary Medicine, Van Yuzuncu Yil University, Van, Turkey 2. Department of Parasitology, Faculty of Veterinary Medicine, Siirt University, Siirt, Turkey 3. Department of Internal Medicine, Faculty of Veterinary Medicine, Siirt University, Siirt, Turkey 4. Özalp Vocational School, Van Yüzüncü Yıl University, Van, Turkey 5. Department of Basic Health Sciences, Faculty of Health Sciences, Marmara University, İstanbul, Turkey 6. Faculty of Health, Van Yuzuncu Yil University, Van, Turkey 7. Department of Parasitology, Faculty of Veterinary Medicine, Dicle University, Diyarbakır, Turkey 8. Department of Parasitology, Faculty of Medicine, Van Yuzuncu Yil University, Van, Turkey 9. Department of Virology, Faculty of Veterinary Medicine, Van Yuzuncu Yil University, Van, Turkey
Abstract
Anaplasmosis and ehrlichiosis are important tick-borne rickettsial diseases of medical and veterinary importance that cause economic losses in livestock. In this study, the prevalence of Anaplasma ovis, Ehrlichia canis and Ehrlichia chaffeensis was investigated in ticks collected from sheep in various farms in Van province, which is located in the Eastern Anatolian Region of Turkey. The ticks used in this study were collected by random sampling in 26 family farm business in 13 districts of Van province. A total of 688 ticks were collected from 88 sheep and 88 tick pools were created. All ticks identified morphologically as Rhipicephalus bursa. Phylogenetic analysis of Chaperonin and 16S rRNA gene sequences confirmed A. ovis, E. canis and E. chaffeensis in this study. Of the 88 tick pools tested, 28.41% (25/88) were positive for at least one pathogen. Anaplasma DNA was detected in five of the 88 pools (5.68%), E. canis DNA was detected in 19 of the 88 pools (21.59%), and E. chaffeensis DNA was detected in one of the 88 pools (1.14%) of R. bursa ticks. To our knowledge, this is the first report describing the presence of A. ovis, E. canis, and E. chaffeensis in R. bursa ticks collected from sheep in Turkey. Further studies are needed to investigate other co-infections in sheep in Turkey.
Publisher
Polish Academy of Sciences Chancellery
Reference1 articles.
1. 1. Aktas M, Altay K, Dumanli N, Kalkan A (2009) Molecular detection and identification of Ehrlichia and Anaplasma species in ixodid ticks. Parasitol Res 104: 1243-1248. 2. Alessandra T, Santo C (2012) Tick-borne diseases in sheep and goats: Clinical and diagnostic aspects. Small Rumin Res 106: S6-S11. 3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410. 4. Anderson BE, Sims KG, Olson JG, Childs JE, Piesman JF, Happ CM, Maupin GO, Johnson BJ (1993) Amblyomma americanum: a potential vector of human ehrlichiosis. Am J Trop Med Hyg 49: 239-244. 5. Aubry P, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis. 58: 1-30. 6. Belkahia H, Ben Said M, El Hamdi S, Yahiaoui M, Gharbi M, Daaloul-Jedidi M, Mhadhbi M, Jedidi M, Darghouth MA, Klabi I, Zribi L, Messadi L (2014) First molecular identification and genetic characterization of Anaplasma ovis in sheep from Tunisia. Small Rumin Res 121: 404-410. 7. Cao WC, Gao YM, Zhang PH, Zhang XT, Dai QH, Dumler JS, Fang LQ, Yang H (2000) Identification of Ehrlichia chaffeensis by nested PCR in ticks from Southern China. J Clin Microbiol 38: 2778-2780. 8. Cicculli V, Masse S, Capai L, De Lamballerie X, Charrel R, Falchi A (2019) First detection of Ehrlichia minasensis in Hyalomma mar-ginatum ticks collected from cattle in Corsica, France. Vet Med Sci 5: 243-248. 9. Cohen SB, Yabsley MJ, Freye JD, Dunlap BG, Rowland ME, Huang J, Dunn JR, Jones TF, Moncayo AC (2010) Prevalence of Ehr-lichia chaffeensis and Ehrlichia ewingii in ticks from Tennessee. Vector Borne Zoonotic Dis 10: 435-440. 10. Dahmani M, Davoust B, Rousseau F, Raoult D, Fenollar F, Mediannikov O (2017) Natural Anaplasmataceae infection in Rhipicephalus bursa ticks collected from sheep in the French Basque Country. Ticks Tick Borne Dis 8: 18-24. 11. Dugan VG, Little SE, Stallknecht DE, Beall AD (2000) Natural infection of domestic goats with Ehrlichia chaffeensis. J Clin Microbiol 38: 448-449. 12. Enkhtaivan B, Narantsatsral S, Davaasuren B, Otgonsuren D, Amgalanbaatar T, Uuganbayar E, Zoljargal M, Myagmarsuren P, Suganuma K, Molefe NI, Sivakumar T, Inoue N, Battur B, Battsetseg B, Yokoyama N (2019) Molecular detection of Anaplasma ovis in small ruminants and ixodid ticks from Mongolia. Parasitol Int 69: 47-53. 13. Estrada-Peña A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean region. A guide to identi-fication of species. University of Zaragoza, Spain 123-126. 14. Haigh JC, Gerwing V, Erdenebaatar J, Hill JE (2008) A novel clinical syndrome and detection of Anaplasma ovis in Mongolian reindeer (Rangifer tarandus). J Wildl Dis 44: 569-577. 15. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Ac-ids Symposium Series 41: 95-98. 16. Jalali SM, Khaki Z, Kazemi B, Bandehpour M, Rahbari S, Razi Jalali MR, Yasini SP (2013) Molecular detection and identification of Anaplasma species in sheep from Ahvaz, Iran. Iran J Vet Res 14: 50-56. 17. Johnson EM, Ewing SA, Barker RW, Fox JC, Crow DW, Kocan KM (1998) Experimental transmission of Ehrlichia canis (Rickettsiales: Ehrlichieae) by Dermacentor variabilis (Acari: Ixodidae). Vet Parasitol 74: 277-288. 18. Kocan KM, Fuente JL, Blouin EF (2008) Advances toward understanding the molecular biology of the Anaplasma-tick interface. Front Biosci 13: 7032-7045. 19. Kramer VL, Randolph MP, Hui LT, Irwin WE, Gutierrez AG, Vugia DJ (1999) Detection of the agents of human ehrlichioses in ixodid ticks from California. Am J Trop Med Hyg 60: 62-65. 20. Lee SO, Na DK, Kim CM, Li YH, Cho YH, Park JH, Lee JH, Eo SK, Klein TA, Chae JS (2005) Identification and prevalence of Ehr-lichia chaffeensis infection in Haemaphysalis longicornis ticks from Korea by PCR, sequencing and phylogenetic analysis based on 16S rRNA gene. J Vet Sci 6: 151-155. 21. Li Y, Galon EM, Guo Q, Rizk MA, Moumouni PF, Liu M, Li J, Ji S, Chahan B, Xuan X (2020) Molecular detection and identification of Babesia spp., Theileria spp., and Anaplasma spp. in sheep from border regions, Northwestern China. Front Vet Sci 7: 630. 22. Liu Z, Ma M, Wang Z, Wang J, Peng Y, Li Y, Guan G, Luo J, Yin H (2011) Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Appl Environ Microbiol 78: 464-470. 23. Ma M, Liu Z, Sun M, Yang J, Guan G, Li Y, Luo J, Yin H (2011) Development and evaluation of a loop-mediated isothermal amplifica-tion method for rapid detection of Anaplasma ovis. J Clin Microbiol 49: 2143-2146. 24. Macieira DB, Messick JB, Cerqueira AM, Freire IM, Linhares GF, Almeida NK, Almosny NR (2005) Prevalence of Ehrlichia canis in-fection in thrombocytopenic dogs from Rio de Janeiro, Brazil. Vet Clin Pathol 34: 44-48. 25. Makino H, Sousa VR, Fujimori M, Rodrigues JY, Dias AF, Dutra V, Nakazato L, de Almeida AB (2015) Ehrlichia canis detection in dogs from Várzea Grande: a comparative analysis of blood and bone marrow samples. Cienc Rural 46: 310-314. 26. Masala G, Chisu V, Foxi C, Socolovschi C, Raoult D, Parola P (2012) First detection of Ehrlichia canis in Rhipicephalus bursa ticks in Sardinia, Italy. Ticks Tick Borne Dis 3: 396-397. 27. Minh BQ, Nguyen MA, Von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30: 1188-1195. 28. Murphy GL, Ewing SA, Whitworth LC, Fox JC, Kocan AA (1998) A molecular and serologic survey of Ehrlichia canis, E. chaffeensis, and E. ewingii in dogs and ticks from Oklahoma. Vet Parasitol 79: 325-339. 29. Noaman V (2012) Identification of hard ticks collected from sheep naturally infected with Anaplasma ovis in Isfahan province, central Iran. Comp Clin Pathol 21: 367-369. 30. Ojeda-Chi MM, Rodriguez-Vivas RI, Esteve-Gasent MD, Perez de León AA, Modarelli JJ, Villegas-Perez SL (2019) Ehrlichia canis in dogs of Mexico: Prevalence, incidence, co-infection and factors associated. Comp Immunol Microbiol Infect Dis 67: 101351. 31. Piratae S, Pimpjong K, Vaisusuk K, Chatan W (2015) Molecular detection of Ehrlichia canis, Hepatozoon canis and Babesia canis vogeli in stray dogs in Mahasarakham province, Thailand. Ann Parasitol 61: 183-187. 32. Renneker S, Abdo J, Salih DE, Karagenç T, Bilgiç H, Torina A, Oliva AG, Campos J, Kullmann B, Ahmed J, Seitzer U (2013) Can Anaplasma ovis in small ruminants be neglected any longer? Transbound Emerg Dis 60 (Suppl 2): 105-112. 33. Roland WE, Everett ED, Cyr TL, Hasan SZ, Dommaraju CB, McDonald GA (1998) Ehrlichia chaffeensis in Missouri ticks. Am J Trop Med Hyg 59: 641-643. 34. Santino I, Iori A, Sessa R, Sulli C, Favia G, Del Piano M (1998) Borrelia burgdorferi s.l. and Ehrlichia chaffeensis in the National Park of Abruzzo. FEMS Microbiol Lett 164: 1-6. 35. Selim A, Abdelhady A, Alahadeb J (2020) Prevalence and first molecular characterization of Ehrlichia canis in Egyptian dogs. Pak Vet J 41: 117-121. 36. Solano‐Gallego L, Trotta M, Razia L, Furlanello T, Caldin M (2006) Molecular survey of Ehrlichia canis and Anaplasma phagocytophi-lum from blood of dogs in Italy. Ann N Y Acad Sci 1078: 515-518. 37. Torina A, Alongi A, Naranjo V, Estrada-Pena A, Vicente J, Scimeca S, Marino AM, Salina F, Caracappa S, de la Fuente J (2008) Prev-alence and genotypes of Anaplasma species and habitat suitability for ticks in a Mediterranean ecosystem. Appl Environ Microbiol 74: 7578-7584. 38. Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44: W232-W235. 39. TUİK (2023) Number of animals in Turkey. Retrieved from Turkish Statistical Institute https://biruni.tuik.gov.tr/ bolgeselistatistik/sorguSayfa.do?target=tablo. Access Date: 10.07.2023. 40. Tumwebaze MA, Lee SH, Moumouni PF, Mohammed-Geba K, Sheir SK, Galal-Khallaf A, Latif HM, Morsi DS, Bishr NM, Galon EM, Byamukama B, Liu M, Li J, Li Y, Ji S, Ringo AE, Rizk MA, Suzuki H, Ibrahim HM, Xuan X (2020) First detection of Anaplasma ovis in sheep and Anaplasma platys-like variants from cattle in Menoufia governorate, Egypt. Parasitol Int 78: 102150. 41. Walker JB, Keirans JE, Horak IG (2000) The genus Rhipicephalus (Acari, Ixodidae): a guide to the brown ticks of the world: Cam-bridge: Cambridge University Press, England. 42. Wang Y, Zhang Q, Han S, Li Y, Wang B, Yuan G, Zhang P, Yang Z, Zhang H, Sun Y, Chen J, Han X, He H (2021) Ehrlichia chaffeensis and four Anaplasma species with veterinary and public health significance identified in Tibetan sheep (Ovis aries) and yaks (Bos grunniens) in Qinghai, China. Front Vet Sci 8: 727166. 43. Yılmaz AB, Deger MS (2011) Determination and Seasonal Distribution of Tick Species on Cattle and Sheep in the Van and Erciş Re-gion. YYU Vet Fak Derg 22: 133-137. 44. Yousefi A, Rahbari S, Shayan P, Sadeghi-dehkordi Z, Bahonar A (2017) Molecular detection of Anaplasma marginale and Anaplasma ovis in sheep and goat in west highland pasture of Iran. Asian Pac J Trop Biomed 7: 455-459. 45. Zhang H, Chang Z, Mehmood K, Wang Y, Rehman MU, Nabi F, Sabir AJ, Liu X, Wu X, Tian X, Zhou D (2017) First report of Ehr-lichia infection in goats, China. Microb Pathog 110: 275-278. 46. Zhang L, Liu H, Xu B, Zhang Z, Jin Y, Li W, Lu Q, Li L, Chang L, Zhang X, Fan D, Cao M, Bao M, Zang Y, Guan Z, Cheng X, Tian L, Wang S, Yu H, Yu Q, Wang Y, Zhang Y, Tang X, Yin J, Lao S, Wu B, Li J, Li W, Xu Q, Shi Y, Huang F (2014) Rural residents in China are at increased risk of exposure to tick-borne pathogens Anaplasma phagocytophilum and Ehrlichia chaffeensis. Biomed Res Int 2014:313867.
|
|