A comprehensive molecular survey of vector-borne blood parasites in cattle in Kyrgyzstan with a note of the first molecular detection of Anaplasma bovis and Candidatus Anaplasma Camelii.

Publisher: Springer Country of Publication: United States NLM ID: 1277355 Publication Model: Electronic Cited Medium: Internet ISSN: 1573-7438 (Electronic) Linking ISSN: 00494747 NLM ISO Abbreviation: Trop Anim Health Prod Subsets: MEDLINE

Publication: 2005- : Heidelberg : Springer
Original Publication: Edinburgh, Livingstone.

Anaplasma*/isolation & purification ; Anaplasma*/genetics ; Cattle Diseases*/epidemiology ; Cattle Diseases*/microbiology ; Cattle Diseases*/parasitology ; Anaplasmosis*/epidemiology ; Anaplasmosis*/microbiology; Animals ; Cattle ; Kyrgyzstan/epidemiology ; Prevalence ; Phylogeny ; Polymerase Chain Reaction/veterinary ; Theileria/isolation & purification ; Theileria/genetics ; Theileriasis/epidemiology ; Theileriasis/parasitology ; Theileriasis/blood ; Polymorphism, Restriction Fragment Length

Vector-borne pathogens continue to increase their impact on the livestock industry worldwide. To protect animals against these pathogens, it is very important to identify the species that cause the disease and understand their prevalence. This study aimed to investigate the presence and prevalence of vector-borne pathogens in apparently healthy cattle in different parts of Kyrgyzstan using molecular diagnostic techniques. For this purpose, 531 blood samples were collected from the Osh, Jalal-Abad, and Batken oblasts of Kyrgyzstan. The blood samples were investigated for vector-borne pathogens using PCR, RLB, and RFLP. Moreover, DNA sequence analyses were used to confirm the results of molecular techniques and phylogenetic analyses of these pathogens. 359 (67.61%) out of 531 samples were found to be infected with at least one pathogen, whereas 172 (32.39%) were detected to be negative. Thirteen vector-borne pathogens were detected in cattle blood samples, and the prevalence of these pathogens was as follows: Theileria orientalis (47.83%), T. annulata (25.61%), Babesia major (0.19%), B. occultans (0.38%), Anaplasma phagocytophilum-like 1 (3.20%), A. capra (3.01%), A. centrale (2.82%), A. bovis (1.13%), (A) ovis (0.19%), Candidatus Anaplasma camelii (0.94%), Trypanosoma theileri (19.21%), Mycoplasma wenyonii (6.03%), and Ca. Mycoplasma haemobos (2.64%). Among the positive samples, one pathogen was identified in 189 cattle (35.59%), and co-infections (two or more pathogens) were determined in 170 (32.01%) animals. Theileria parva, T. mutans, (B) bigemina, B. bovis, B. divergens, and A. marginale could not be detected in the study. Anaplasma bovis and Ca. Anaplasma camelii were detected for the first time in the country. This molecular survey provides important epidemiological and genetic data for the vector-borne pathogens in cattle. The results of the study showed that vector-borne pathogens have a significant spread and distribution in cattle in Kyrgyzstan.
(© 2024. The Author(s), under exclusive licence to Springer Nature B.V.)

Akramov KT, Omuraliev N (2009) Institutional change, rural services, and agricultural performance in Kyrgyzstan. Discussion Paper00904, International Food Policy Research Institute, Washington D.C.
Aktas M, Çolak S (2021) Molecular detection and phylogeny of Anaplasma spp. in cattle reveals the presence of novel strains closely related to A. phagocytophilum in Turkey. Ticks Tick-Borne Dis 12:101604. https://doi.org/10.1016/j.ttbdis.2020.101604. (PMID: 10.1016/j.ttbdis.2020.10160433160190)
Aktas M, Altay K, Dumanli N (2006) A molecular survey of bovine Theileria parasites among apparently healthy cattle and with a note on the distribution of ticks in eastern Turkey. Vet Parasitol 138:179–185. https://doi.org/10.1016/j.vetpar.2006.01.052. (PMID: 10.1016/j.vetpar.2006.01.05216510248)
Aktas M, Altay K, Dumanli N (2011) Molecular detection and identification of Anaplasma and Ehrlichia species in cattle from Turkey. Ticks Tick-Borne Dis 2:62–65. https://doi.org/10.1016/j.ttbdis.2010.11.002. (PMID: 10.1016/j.ttbdis.2010.11.00221771539)
Aktaş M, Kısadere İ, Özübek S, Cihan H, Salıkov R, Cirak VY (2019) First molecular survey of piroplasm species in cattle from Kyrgyzstan. Parasitol Res 118:2431–2435. https://doi.org/10.1007/s00436-019-06370-2. (PMID: 10.1007/s00436-019-06370-231243541)
Altay K, Aktaş M (2004) Sığır Theileriosisi Fırat Üniversitesi Sağlık Bilimleri Dergisi 18:79–86 [In Turkish].
Altay K, Dumanli N, Holman PJ, Aktas M (2005) Detection of Theileria ovis in naturally infected sheep by nested PCR. Vet Parasitol 127:99–104. https://doi.org/10.1016/j.vetpar.2004.09.012. (PMID: 10.1016/j.vetpar.2004.09.01215631901)
Altay K, Dumanli N, Aktas M (2007) Molecular identification, genetic diversity and distribution of Theileria and Babesia species infecting small ruminants. Vet Parasitol 147:161–165. https://doi.org/10.1016/j.vetpar.2007.04.001. (PMID: 10.1016/j.vetpar.2007.04.00117490817)
Altay K, Aydin MF, Dumanli N, Aktas M (2008) Molecular detection of Theileria and Babesia infections in cattle. Vet Parasitol 158:295–301. https://doi.org/10.1016/j.vetpar.2008.09.025. (PMID: 10.1016/j.vetpar.2008.09.02519008048)
Altay K, Atas AD, Ograk YZ, Ozkan E (2020) Survey of Theileria, Babesia and Anaplasma infections of cattle and ticks from Sivas region of Turkey. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17:32–38. https://doi.org/10.32707/ercivet.690618. (PMID: 10.32707/ercivet.690618)
Altay K, Erol U, Sahin OF, Aytmirzakizi A (2022) First molecular detection of Anaplasma species in cattle from Kyrgyzstan; molecular identification of human pathogenic novel genotype Anaplasma capra and Anaplasma phagocytophilum related strain. Ticks Tick-Borne Dis 13:1018601. https://doi.org/10.1016/j.ttbdis.2021.101861.
Altay K, Erol U, Sahin OF (2022) The first molecular detection of Anaplasma Capra in domestic ruminants in the central part of Turkey, with genetic diversity and genotyping of Anaplasma Capra. Trop Anim Health Prod 54:129. https://doi.org/10.1007/s11250-022-03125-7. (PMID: 10.1007/s11250-022-03125-735257219)
Altay K, Erol U, Sahin OF, Aytmirzakizi A, Temizel EM, Aydin MF, Dumanlı N, Aktas M (2022c) The detection and phylogenetic analysis of Anaplasma phagocytophilum-like 1, A. ovis and A. capra in sheep: A. capra divides into two genogroups. Vet Res Commun 46:1271–1279. https://doi.org/10.1007/s11259-022-09998-1. (PMID: 10.1007/s11259-022-09998-136167934)
Altay K, Sahin OF, Erol U, Aytmirzakizi A (2023) First molecular detection and phylogenetic analysis of Mycoplasma wenyonii and Candidatus Mycoplasma haemobos in cattle in different parts of Kyrgyzstan. Biologia 78:633–640. https://doi.org/10.1007/s11756-022-01292-4. (PMID: 10.1007/s11756-022-01292-4)
Altay K, Erol U, Sahin OF (2024) Anaplasma Capra: a new emerging tick-borne zoonotic pathogen. Vet Res Commun 1–12. https://doi.org/10.1007/s11259-024-10337-9.
Amato B, Mira F, Di Marco Lo Presti V, Guercio A, Russotto L, Gucciardi F, Vitale M, Lena A, Loria GR, Puleio R, Cannella V (2019) A case of bovine trypanosomiasis caused by Trypanosoma Theileri in Sicily, Italy. Parasitol Res 118:2723–2727. https://doi.org/10.1007/s00436-019-06390-y. (PMID: 10.1007/s00436-019-06390-y31302757)
Aubry P, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis 58:1–30. https://doi.org/10.1111/j.1865-1682.2010.01173.x. (PMID: 10.1111/j.1865-1682.2010.01173.x21040509)
Bastos AD, Mohammed OB, Bennett NC, Petevinos C, Alagaili AN (2015) Molecular detection of novel Anaplasmataceae closely related to Anaplasma platys and Ehrlichia canis in the dromedary camel (Camelus dromedarius). Vet Microbiol 179:310–314. https://doi.org/10.1016/j.vetmic.2015.06.001. (PMID: 10.1016/j.vetmic.2015.06.00126096752)
Ben Said M, Belkahia H, El Mabrouk N, Saidani M, Hassen MB, Alberti A, Zobba R, Bouattour S, Bouattour A, Messadi L (2017) Molecular typing and diagnosis of Anaplasma spp. closely related to Anaplasma phagocytophilum in ruminants from Tunisia. Ticks Tick-Borne Dis 8:412–422. https://doi.org/10.1016/j.ttbdis.2017.01.005. (PMID: 10.1016/j.ttbdis.2017.01.00528109769)
Bogema DR, Deutscher AT, Fell S, Collins D, Eamens GJ, Jenkins C (2015) Development and validation of a quantitative PCR assay using multiplexed hydrolysis probes for detection and quantification of Theileria Orientalis isolates and differentiation of clinically relevant subtypes. J Clin Microbiol 53:941–950. https://doi.org/10.1128/JCM.03387-14. (PMID: 10.1128/JCM.03387-14255886534390635)
Broka S, Giertz Å, Christensen G, Hanif C, Rasmussen D, Rubaiza R (2016) Kyrgyz Republic Agricultural Sector Risk Assessment. Number 103078-KG. World Bank Group Report, Washington D.C. (PMID: 10.1596/23763)
Brotánková A, Fialová M, Čepička I, Brzoňová J, Svobodová M (2022) Trypanosomes of the Trypanosoma Theileri group: phylogeny and new potential vectors. Microorganisms 10:294. https://doi.org/10.3390/microorganisms10020294. (PMID: 10.3390/microorganisms10020294352087498880487)
Chatanga E, Maganga E, Mohamed WMA, Ogata S, Pandey GS, Abdelbaset AE, Hayashida K, Sugimoto C, Katakura K, Nonaka N, Nakao R (2022) High infection rate of tick-borne protozoan and rickettsial pathogens of cattle in Malawi and the development of a multiplex PCR for Babesia and Theileria species identification. Acta Trop 231:106413. https://doi.org/10.1016/j.actatropica.2022.106413. (PMID: 10.1016/j.actatropica.2022.10641335307457)
Chen SM, Dumler JS, Bakken JS, Walker DH (1994) Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 32:589–595. https://doi.org/10.1128/jcm.32.3.589-595.1994. (PMID: 10.1128/jcm.32.3.589-595.19948195363263091)
Chochlakis D, Ioannou I, Tselentis Y, Psaroulaki A (2010) Human anaplasmosis and Anaplasma ovis variant. Emerg Infect Dis 16:1031. https://doi.org/10.3201/eid1606.090175. (PMID: 10.3201/eid1606.090175205077683086243)
Cufos N, Jabbar A, de Carvalho LM, Gasser RB (2012) Mutation scanning-based analysis of Theileria orientalis populations in cattle following an outbreak. Electrophoresis 33:2036–2040. https://doi.org/10.1002/elps.201200082. (PMID: 10.1002/elps.20120008222806470)
Dantas-Torres F, Chomel BB, Otranto D (2012) Ticks and tick-borne diseases: a one health perspective. Trends Parasitol 28:437–446. https://doi.org/10.1016/j.pt.2012.07.003. (PMID: 10.1016/j.pt.2012.07.00322902521)
De la Cadena E, Camacho M, Vaca F, Enríquez S, Eleizalde MC, Arrivillaga-Henríquez J, Mendoza M, Navarro JC, Ramírez-Iglesias JR (2023) Molecular identification of Trypanosoma Theileri in cattle from the Ecuadorian Amazon. Vet Parasitol: Reg Stud Rep 37:100824. https://doi.org/10.1016/j.vprsr.2022.100824. (PMID: 10.1016/j.vprsr.2022.100824)
de Mello VVC, de Souza Ramos IA, Herrera HM, Mendes NS, Calchi AC, Campos JBV, Macedo GC, Alves JVA, Machado RZ, Andre MR (2019) Occurrence and genetic diversity of hemoplasmas in beef cattle from the Brazilian pantanal, an endemic area for bovine trypanosomiasis in South America. Comp Immunol Microbiol Infect Dis 66:101337. https://doi.org/10.1016/j.cimid.2019.101337. (PMID: 10.1016/j.cimid.2019.10133731437678)
Debbarma A, Pandit S, Jas R, Baidya S, Chandra Mandal S, Sarathi Jana P, Das M (2020) Prevalence of tick-borne haemoparasitic diseases in cattle of West Bengal, India. Biol Rhythm Res 51:310–317. https://doi.org/10.1080/09291016.2018.1528693. (PMID: 10.1080/09291016.2018.1528693)
Díaz-Sánchez AA, Corona-González B, Meli ML, Álvarez DO, Cañizares EV, Rodríguez OF, Rivero EL, Hofmann-Lehmann R (2019) First molecular evidence of bovine hemoplasma species (Mycoplasma spp.) in water buffalo and dairy cattle herds in Cuba. Parasit Vectors 12:1–9. https://doi.org/10.1186/s13071-019-3325-y. (PMID: 10.1186/s13071-019-3325-y)
Erol U, Şahin ÖF, Altay K (2022) Molecular Survey of Anaplasma phagocytophilum and related strains in sheep and goats from Sivas; with a high prevalence of Anaplasma phagocytophilum-like 1. Turkiye Parazitoloji Dergisi 46:293–300. https://doi.org/10.4274/tpd.galenos.2022.47965. (PMID: 10.4274/tpd.galenos.2022.47965)
Erol U, Sahin OF, Altay K (2023) Molecular prevalence of bovine hemoplasmosis in Turkey with first detection of Mycoplasma wenyonii and Candidatus Mycoplasma haemobos in cattle and water buffalo. Vet Res Commun 1–9. https://doi.org/10.1007/s11259-022-09943-2.
Fathi A, Nabavi R, Noaman V, Sarani A, Saadati D, Ben Said M, Ghafar A, Jabbar A, Sazmand A (2024) Molecular identification, risk factor assessment, and phylogenetic analysis of tick-borne pathogens in symptomatic and asymptomatic cattle from South-Eastern Iran. Exp Appl Acarol 1–28. https://doi.org/10.1007/s10493-023-00886-0.
Frenken K (2013) Irrigation in Central Asia in figures: AQUASTAT Survey-2012. FAO Water Rep. https://doi.org/10.13140/RG.2.1.2770.8247.
Galon EM, Zafar I, Ji S, Li H, Ma Z, Xuan X (2022) Molecular reports of ruminant Babesia in Southeast Asia. Pathogens 11:915. https://doi.org/10.3390/pathogens11080915. (PMID: 10.3390/pathogens11080915360150359415187)
Ganguly A, Maharana BR, Ganguly I (2020) Pentaplex PCR assay for rapid differential detection of Babesia Bigemina, Theileria annulata, Anaplasma marginale and Trypanosoma Evansi in cattle. Biologicals 63:81–88. https://doi.org/10.1016/j.biologicals.2019.10.011. (PMID: 10.1016/j.biologicals.2019.10.01131708375)
Garcia HA, Rodrigues AC, Martinkovic F, Minervino AHH, Campaner M, Nunes VL, Paiva F, Hamilton PB, Teixeira MMG (2011) Multilocus phylogeographical analysis of Trypanosoma (Megatrypanum) genotypes from sympatric cattle and water buffalo populations supports evolutionary host constraint and close phylogenetic relationships with genotypes found in other ruminants. Int J Parasitol 41:1385–1396. https://doi.org/10.1016/j.ijpara.2011.09.001. (PMID: 10.1016/j.ijpara.2011.09.00122051399)
Genova SG, Streeter RN, Velguth KE, Snider TA, Kocan KM, Simpson KM (2011) Severe anemia associated with Mycoplasma wenyonii infection in a mature cow. Can Veterinary J 52:1018.
Georges K, Loria GR, Riili S, Greco A, Caracappa S, Jongejan F, Sparagano O (2001) Detection of haemoparasites in cattle by reverse line blot hybridisation with a note on the distribution of ticks in Sicily. Vet Parasitol 99:273–286. https://doi.org/10.1016/s0304-4017(01)00488-5. (PMID: 10.1016/s0304-4017(01)00488-511511414)
Getange D, Bargul JL, Kanduma E, Collins M, Bodha B, Denge D, Chiuya T, Githaka N, Younan M, Fèvre EM, Bell-Sakyi L, Villinger J (2021) Ticks and tick-borne pathogens associated with dromedary camels (Camelus dromedarius) in northern Kenya. Microorganisms 9:1414. https://doi.org/10.3390/microorganisms9071414. (PMID: 10.3390/microorganisms9071414342090608306667)
Gubbels JM, de Vos AP, van der Weide M, Viseras, Jv, Schouls LM, de Vries E, Jongejan F (1999) Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. J Clin Microbiol 37:1782–1789. https://doi.org/10.1128/JCM.37.6.1782-1789.1999. (PMID: 10.1128/JCM.37.6.1782-1789.19991032532484950)
Gunasekara E, Sivakumar T, Kothalawala H, Abeysekera TS, Weerasingha AS, Vimalakumar SC, Kanagaratnam R, Yapa PR, Zhyldyz A, Igarashi I, Silva SSP, Yokoyama N (2019) Epidemiological survey of hemoprotozoan parasites in cattle from low-country wet zone in Sri Lanka. Parasitol Int 71:5–10. https://doi.org/10.1016/j.parint.2019.03.004. (PMID: 10.1016/j.parint.2019.03.00430858106)
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. https://doi.org/10.7589/0090-3558-44.3.569. (PMID: 10.7589/0090-3558-44.3.56918689641)
Hasegawa M, Kishino H, Yano TA (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. https://doi.org/10.1007/BF02101694. (PMID: 10.1007/BF021016943934395)
Hosseini-Vasoukolaei N, Oshaghi MA, Shayan P, Vatandoost H, Babamahmoudi F, Yaghoobi-Ershadi MR, Telmadarraiy Z, Mohtarami F (2014) Anaplasma infection in ticks, livestock and human in Ghaemshahr, Mazandaran Province, Iran. J Arthropod-Borne Dis 8:204. (PMID: 261141344478432)
Jensen WA, Lappin MR, Kamkar S, Reagan WJ (2001) Use of a polymerase chain reaction assay to detect and differentiate two strains of Haemobartonella felis in naturally infected cats. Am J Vet Res 62:604–608. https://doi.org/10.2460/ajvr.2001.62.604. (PMID: 10.2460/ajvr.2001.62.60411327472)
Kamau J, de Vos AJ, Playford M, Salim B, Kinyanjui P, Sugimoto C (2011) Emergence of new types of Theileria orientalis in Australian cattle and possible cause of theileriosis outbreaks. Parasit Vectors 4:1–10. https://doi.org/10.1186/1756-3305-4-22. (PMID: 10.1186/1756-3305-4-22)
Karpathy SE, Kingry L, Pritt BS, Berry JC, Chilton NB, Dergousoff SJ, Cortinas R, Sheldon SW, Oatman S, Anacker M, Petersen J, Paddock CD (2023) Anaplasma bovis–like infections in humans, United States, 2015–2017. Emerg Infect Dis 29(1904). https://doi.org/10.3201/eid2909.230559.
Kawahara M, Rikihisa Y, Lin Q, Isogai E, Tahara K, Itagaki A, Hiramitsu Y, Tajima T (2006) Novel genetic variants of Anaplasma phagocytophilum, Anaplasma bovis, Anaplasma centrale, and a novel Ehrlichia sp. in wild deer and ticks on two major islands in Japan. Appl Environ Microbiol 72:1102–1109. https://doi.org/10.1128/AEM.72.2.1102-1109.2006. (PMID: 10.1128/AEM.72.2.1102-1109.2006164616551392898)
Kim Y, Kim H, Choi JH, Cho HC, Ji MJ, Park YJ, Park J, Choi KS (2024) Preliminary report of Mycoplasma Wenoynii and Candidatus Mycoplasma haemobos infection in Korean native cattle. BMC Vet Res 20:1–7. https://doi.org/10.1186/s12917-024-03976-2. (PMID: 10.1186/s12917-024-03976-2)
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581. (PMID: 10.1007/BF017315817463489)
Kocan KM, de la Fuente J, Blouin EF, Coetzee JF, Ewing SA (2010) The natural history of Anaplasma marginale. Vet Parasitol 167:95–107. https://doi.org/10.1016/j.vetpar.2009.09.012. (PMID: 10.1016/j.vetpar.2009.09.01219811876)
Kolo A (2023) Anaplasma species in Africa—a century of discovery: a review on molecular epidemiology, genetic diversity, and control. Pathogens 12:702. https://doi.org/10.3390/pathogens12050702. (PMID: 10.3390/pathogens120507023724237210222256)
Kuibagarov M, Makhamed R, Zhylkibayev A, Berdikulov M, Abdrakhmanov S, Kozhabayev M, Akhmetollayev I, Mukanov K, Ryskeldina A, Ramankulov Y, Shustov A, Bauer C, Shevtsov A (2023) Theileria and Babesia infection in cfirst–First molecular survey in Kazakhstan. Ticks Tick-Borne Dis 14:102078. https://doi.org/10.1016/j.ttbdis.2022.102078. (PMID: 10.1016/j.ttbdis.2022.10207836395616)
Lbacha HA, Zouagui Z, Alali S, Rhalem A, Petit E, Ducrotoy MJ, Boulouis HJ, Maillard R (2017) Candidatus Anaplasma camelii in one-humped camels (Camelus dromedarius) in Morocco: a novel and emerging anaplasma species? Infect Dis Poverty 6:67–74. https://doi.org/10.1186/s40249-016-0216-8. (PMID: 10.1186/s40249-016-0216-8)
Lew-Tabor AE, Valle MR (2016) A review of reverse vaccinology approaches for the development of vaccines against ticks and tick borne diseases. Ticks Tick-Borne Dis 7:573–585. https://doi.org/10.1016/j.ttbdis.2015.12.012. (PMID: 10.1016/j.ttbdis.2015.12.01226723274)
Li H, Zheng YC, Ma L, Jia N, Jiang BG, Jiang RR, Huo QB, Wang YW, Liu HB, Chu YL, Song YD, Yao NN, Sun T, Zeng FY, Dumler JS, Jiang JF, Cao WC (2015) Human infection with a novel tick-borne Anaplasma species in China: a surveillance study. Lancet Infect Dis 15:663–670. https://doi.org/10.1016/S1473-3099(15)70051-4. (PMID: 10.1016/S1473-3099(15)70051-425833289)
Li Y, Li J, Chahan B, Guo Q, Zhang Y, Moumouni PFA, Lee SH, Liu M, Galon EM, Guo H, Gao Y, Song R, Li M, Tunwebaze MA, Benedicto B, Xuan X (2020) Molecular investigation of tick-borne infections in cattle from Xinjiang Uygur Autonomous Region, China. Parasitol Int 74:101925. https://doi.org/10.1016/j.parint.2019.05.003. (PMID: 10.1016/j.parint.2019.05.00331077806)
Liu Z, Ma M, Wang Z, Wang J, Peng Y, Li Y, Guan G, Luo J, Yin H (2012) Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Appl Environ Microbiol 78:464–470. https://doi.org/10.1128/AEM.06848-11. (PMID: 10.1128/AEM.06848-11220578673255723)
Liu J, Guan G, Yin H (2022) Theileria annulata. Trends Parasitol 38:265–266. https://doi.org/10.1016/j.pt.2021.11.001.
Liu J, Li Z, Liu A, Wang J, Guan G, Yin H, Luo J (2022) Identification and isolation of pathogenic Theileria orientalis Ikeda genotype from confined dairy cattle, in Hebei, China. Parasitol Res 121:395–402. https://doi.org/10.1007/s00436-021-07401-7.
Lu M, Chen Q, Qin X, Lyu Y, Teng Z, Li K, Yu L, Jin X, Chang H, Wang W, Hong D, Sun Y, Kan B, Gong L, Qin T, China (2022) Anaplasma bovis infection in fever and thrombocytopenia patients—Anhui Province, China, 2021. China CDC Wkly 4:249. https://doi.org/10.46234/ccdcw2022.053. (PMID: 10.46234/ccdcw2022.053354330839005486)
McFadden AMJ, Ha HJ, Donald JJ, Bueno IM, Van Andel M, Thompson JC, Tisdall DJ, Pulford DJ (2016) Investigation of bovine haemoplasmas and their association with anaemia in New Zealand cattle. N Z Vet J 64:65–68. https://doi.org/10.1080/00480169.2015.1090356. (PMID: 10.1080/00480169.2015.109035626411673)
Meli ML, Willi B, Dreher UM, Cattori V, Knubben-Schweizer G, Nuss K, Braun U, Lutz H, Hofmann-Lehmann R (2010) Identification, molecular characterization, and occurrence of two bovine hemoplasma species in Swiss cattle and development of real-time TaqMan quantitative PCR assays for diagnosis of bovine hemoplasma infections. J Clin Microbiol 48:3563–3568. https://doi.org/10.1128/JCM.02224-09. (PMID: 10.1128/JCM.02224-09206860932953077)
Narladkar BW (2018) Projected economic losses due to vector and vector-borne parasitic diseases in livestock of India and its significance in implementing the concept of integrated practices for vector management. Vet World 11:151. https://doi.org/10.14202/vetworld.2018.151-160. (PMID: 10.14202/vetworld.2018.151-160296573965891867)
Niethammer FM, Ade J, Hoelzle LE, Schade B (2018) Hemotrophic mycoplasma in Simmental cattle in Bavaria: prevalence, blood parameters, and transplacental transmission of ‘Candidatus Mycoplasma haemobos’ and Mycoplasma wenyonii. Acta Vet Scand 60:1–8. https://doi.org/10.1186/s13028-018-0428-y. (PMID: 10.1186/s13028-018-0428-y)
Oakes VJ, Yabsley MJ, Schwartz D, LeRoith T, Bissett C, Broaddus C, Schlater JL, Todd SM, Boes KM, Brookhart M, Lahmers KK (2019) TheiOrientalisntalis Ikeda genotype in cattle. Va USA Emerg Infect Dis 25:1653. https://doi.org/10.3201/eid2509.190088. (PMID: 10.3201/eid2509.190088)
Ota N, Mizuno D, Kuboki N, Igarashi I, Nakamura Y, Yamashina H, Hanzaike T, Sadao KF, Hata H, Kondo S, Matsui S, Koga M, Matsumoto K, Inokuma H, Yokoyama N (2009) Epidemiological survey of Theileria orientalis infection in grazing cattle in the eastern part of Hokkaido, Japan. J Vet Med Sci 71:937–944. https://doi.org/10.1292/jvms.71.937. (PMID: 10.1292/jvms.71.93719652482)
Ozubek S, Ulucesme MC, Cirak VY, Aktas M (2022) Detection of Theileria orientalis genotypes from cattle in Kyrgyzstan. Pathogens 11:1185. https://doi.org/10.3390/pathogens11101185. (PMID: 10.3390/pathogens11101185362972429606894)
Pacheco TDA, Marcili A, Costa APD, Witter R, Melo ALT, Boas RV, Chitarra CS, Durta V, Nakazato L, Pacheco RDC (2018) Genetic diversity and molecular survey of Trypanosoma (Megatrypanum) theileri in cattle in Brazil’s western Amazon region. Rev Bras Parasitol Vet 27:579–583. https://doi.org/10.1590/S1984-296120180049. (PMID: 10.1590/S1984-29612018004930133593)
Pfäffle M, Littwin N, Muders SV, Petney TN (2013) The ecology of tick-borne diseases. Int J Parasitol 43:1059–1077. https://doi.org/10.1016/j.ijpara.2013.06.009. (PMID: 10.1016/j.ijpara.2013.06.00923911308)
Rar V, Golovljova I (2011) Anaplasma, Ehrlichia, and Candidatus Neoehrlichia bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect Genet Evol 11:1842–1861. https://doi.org/10.1016/j.meegid.2011.09.019. (PMID: 10.1016/j.meegid.2011.09.01921983560)
Rar V, Tkachev S, Tikunova N (2021) Genetic diversity of Anaplasma bacteria: twenty years later. Infect Genet Evol 91:104833. https://doi.org/10.1016/j.meegid.2021.104833. (PMID: 10.1016/j.meegid.2021.10483333794351)
Renneker S, Abdo J, Salih DEA, 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 60:105–112. https://doi.org/10.1111/tbed.12149. (PMID: 10.1111/tbed.1214924589109)
Rodrigues AC, Garcia HA, Ortiz PA, Cortez AP, Martinkovic F, Paiva F, Batista JS, Minervino AH, Campaner M, Pral EM, Alfieri SC, Teixeira MM (2010) Cysteine proteases of Trypanosoma (Megatrypanum) theileri: cathepsin L-like gene sequences as targets for phylogenetic analysis, genotyping diagnosis. Parasitol Int 59:318–325. https://doi.org/10.1016/j.parint.2010.03.002. (PMID: 10.1016/j.parint.2010.03.00220230907)
Sahin OF, Erol U, Altay K (2022) Buffaloes as new hosts for Anaplasma Capra: Molecular prevalence and phylogeny based on gtlA, groEL, and 16S rRNA genes. Res Vet Sci 152:458–464. https://doi.org/10.1016/j.rvsc.2022.09.008. (PMID: 10.1016/j.rvsc.2022.09.00836148715)
Sahin OF, Erol U, Duzlu O, Altay K (2023) Molecular survey of Anaplasma phagocytophilum and related variants in water buffaloes: the first detection of Anaplasma phagocytophilum-like 1. Comp Immunol Microbiol Infect Dis 98:102004. https://doi.org/10.1016/j.cimid.2023.102004. (PMID: 10.1016/j.cimid.2023.10200437356166)
Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ahmed JS (2004) Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting. Parasitol Res 92:189–196. https://doi.org/10.1007/s00436-003-0980-9. (PMID: 10.1007/s00436-003-0980-914652747)
Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison DA (2012) Babesia: a world emerging. Infect Genet Evol 12:1788–1809. https://doi.org/10.1016/j.meegid.2012.07.004. (PMID: 10.1016/j.meegid.2012.07.00422871652)
Schouls LM, Van De Pol I, Rijpkema SG, Schot CS (1999) Detection and identification of Ehrlichia, Borrelia burgdorferi Sensu Lato, and Bartonella species in Dutch Ixodes ricinus ticks. J Clin Microbiol 37:2215–2222. https://doi.org/10.1128/JCM.37.7.2215-2222.1999. (PMID: 10.1128/JCM.37.7.2215-2222.19991036458885121)
Seo MG, Ouh IO, Lee H, Geraldino PJL, Rhee MH, Kwon OD, Kwak D (2018) Differential identification of Anaplasma in cattle and potential of cattle to serve as reservoirs of Anaplasma Capra, an emerging tick-borne zoonotic pathogen. Vet Microbiol 226:15–22. https://doi.org/10.1016/j.vetmic.2018.10.008. (PMID: 10.1016/j.vetmic.2018.10.00830389039)
Sharifiyazdi H, Jafari S, Ghane M, Nazifi S, Sanati A (2017) Molecular investigation of Anaplasma and Ehrlichia natural infections in the dromedary camel (Camelus dromedarius) in Iran. Comp Clin Pathol 26:99–103. https://doi.org/10.1007/s00580-016-2350-x. (PMID: 10.1007/s00580-016-2350-x)
Shaw WR, Catteruccia F (2019) Vector biology meets disease control: using basic research to fight vector-borne diseases. Nat Microbiol 4:20–34. https://doi.org/10.1038/s41564-018-0214-7. (PMID: 10.1038/s41564-018-0214-730150735)
Shi H, Duan L, Liu F, Hu Y, Shi Z, Chen X, Yang H, Yan B, Yao L (2019) Rhipicephalus (Boophilus) microplus ticks as reservoir and vector of ‘Candidatus Mycoplasma haemobos.’ China Vet Parasitol 274:108929. https://doi.org/10.1016/j.vetpar.2019.108929. (PMID: 10.1016/j.vetpar.2019.10892931568995)
Suarez CE, Noh S (2011) Emerging perspectives in the research of bovine babesiosis and anaplasmosis. Vet Parasitol 180:109–125. https://doi.org/10.1016/j.vetpar.2011.05.032. (PMID: 10.1016/j.vetpar.2011.05.03221684084)
Suganuma K, Kayano M, Kida K, Gröhn YT, Miura R, Ohari Y, Mizushima D, Inoue N (2022) Genetic and seasonal variations of Trypanosoma Theileri and the association of Trypanosoma Theileri infection with dairy cattle productivity in Northern Japan. Parasitol Int 86:102476. https://doi.org/10.1016/j.parint.2021.102476. (PMID: 10.1016/j.parint.2021.10247634610467)
Tagawa M, Yamakawa K, Aoki T, Matsumoto K, Ishii M, Inokuma H (2013) Effect of chronic hemoplasma infection on cattle productivity. J Vet Med Sci 75:1271–1275. https://doi.org/10.1292/jvms.13-0119. (PMID: 10.1292/jvms.13-0119236762783942926)
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752. (PMID: 10.1093/oxfordjournals.molbev.a0407521630306)
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023. (PMID: 10.1093/oxfordjournals.molbev.a0400238336541)
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120. (PMID: 10.1093/molbev/msab120338924918233496)
Villa A, Gutierrez C, Gracia E, Moreno B, Chacón G, Sanz PV, Büscher P, Touratier L (2008) Presence of Trypanosoma Theileri in Spanish cattle. Ann N Y Acad Sci 1149:352–354. https://doi.org/10.1196/annals.1428.016. (PMID: 10.1196/annals.1428.01619120247)
Watts JG, Playford MC, Hickey KL (2016) Theileria orientalis: a review. N Z Vet J 64:3–9. https://doi.org/10.1080/00480169.2015.1064792. (PMID: 10.1080/00480169.2015.106479226143684)
Weerasooriya G, Sivakumar T, Lan DTB, Long PT, Takemae H, Igarashi I, Inoue N, Yokoyama N (2016) Epidemiology of bovine hemoprotozoa parasites in cattle and water buffalo in Vietnam. J Vet Med Sci 78:1361–1367. https://doi.org/10.1292/jvms.16-0099. (PMID: 10.1292/jvms.16-0099271498945053943)
Yang J, Liu Z, Niu Q, Liu J, Han R, Liu G, Shi Y, Yin H (2016) Molecular survey and characterization of a novel Anaplasma species closely related to Anaplasma Capra in ticks, northwestern China. Parasit Vectors 9:1–5. https://doi.org/10.1186/s13071-016-1886-6. (PMID: 10.1186/s13071-016-1886-6267285234700674)
Ybañez AP, Sivakumar T, Ybañez RHD, Vincoy MRB, Tingson JA, Perez ZO, Gabotero SH, Buchorno LP, Inoue N, Matsumoto K, Inokuma H, Yokoyama N (2013) Molecular survey of bovine vector-borne pathogens in Cebu. Philipp Vet Parasitol 196:13–20. https://doi.org/10.1016/j.vetpar.2013.02.013. (PMID: 10.1016/j.vetpar.2013.02.013)
Ybañez AP, Ybañez RHD, Armonia RKM, Chico JKE, Ferraren KJV, Tapdasan EP, Salces CB, Maurillo BCA, Galon EMS, Macalanda AMC, Moumouni PFA, Xuan X (2019) First molecular detection of Mycoplasma wenyonii and the ectoparasite biodiversity in dairy water buffalo and cattle in Bohol. Philipp Parasitol Int 70:77–81. https://doi.org/10.1016/j.parint.2019.02.004. (PMID: 10.1016/j.parint.2019.02.004)
Zhyldyz A, Aitakin K, Atabek B, Elmurat J, Rysbek N, Jailobek O, Ahedır B, Otgonsuren D, Mumbi NNM, Guswanto A, Sivakumar T, Yokoyama N (2023) An epidemiological survey of vector-borne pathogens infecting cattle in Kyrgyzstan. Parasitol Int 97:102791. https://doi.org/10.1016/j.parint.2023.102791. (PMID: 10.1016/j.parint.2023.10279137544641)
Zobba R, Anfossi AG, Pinna Parpaglia ML, Dore GM, Chessa B, Spezzigu A, Rocca S, Visco S, Pittau M, Alberti A (2014) Molecular investigation and phylogeny of Anaplasma spp. in Mediterranean ruminants reveal the presence of neutrophil-tropic strains closely related to A. platys. Appl Environ Microbiol 80:271–280. https://doi.org/10.1128/AEM.03129-13. (PMID: 10.1128/AEM.03129-13241625693911010)

Keywords: Cattle; Kyrgyzstan; PCR; Phylogeny; RFLP; RLB; Vector-borne pathogens

Date Created: 20240921 Date Completed: 20240921 Latest Revision: 20241210

20250114

10.1007/s11250-024-04112-w

39305339