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Leading report of molecular prevalence of tick borne Anaplasma marginale and Theileria ovis in yaks (Bos grunniens) from Pakistan

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Abstract

Domestic yak (Bos grunniens) is an economically important feature of the mountainous region of Gilgit-Baltistan in Pakistan where agriculture is restricted and yaks play multiple roles which includes being a source of milk, meat, hides, fuel and power. However little is known about the parasitic infections in Pakistani yaks. Aim of this research was to report the prevalence and genetic diversity of protozoa parasite (Theileria ovis, 18 S rDNA gene was targeted) and an obligate bacterium (Anaplasma marginale, msp-1 gene was amplified) in the blood that was sampled from 202 yaks collected from four districts in Gilgit-Baltistan during January 2023 till January 2024. Results revealed that 6/202 (3%) yaks were of Theileria ovis while 8/202 (4%) were Anaplasma marginale infected. Positive PCR products of both parasites were confirmed by DNA sequencing and their similarity with previously available pathogen sequences was determined by BLAST analysis. Phylogenetic tree indicated that isolates of both parasites displayed genetic. Anaplasma marginale infection varied with the sampling districts and Shigar district had the highest rate of bacterial infection. Cows were significantly more prone to Theileria ovis infection than bulls. Calf and hybrid yaks were more prone to Anaplasma marginale infection. In conclusion, this is the first report that yaks residing the Gilgit-Baltistan region in Pakistan are infected with Theileria ovis and Anaplasma marginale. Similar larger scales studies are recommended in various regions of Gilgit-Baltistan to document the infection rates of these parasites to formulate strategies that will lead to the effective control of these pathogens.

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References

  • Abid K, Bukhari S, Asif M et al (2021) Molecular detection and prevalence of Theileria ovis and Anaplasma marginale in sheep blood samples collected from Layyah district in Punjab, Pakistan. Trop Anim Health Prod 53:439. https://doi.org/10.1007/s11250-021-02870-5

    Article  PubMed  Google Scholar 

  • Altay K, Aktas M, Dumanli N (2007) Theileria infections in small ruminants in the east and south east Anatolia. Türk Parazitol Dergi 31:268–271

    Google Scholar 

  • Arif M, Saeed S, Bashir A, Farooq M, Nasreen N, Adil K, Asif M, Khalil MA, Ijaz M, Muqadas H, Mehmood N, Iqbal F, Chen C (2023) Molecular prevalence and phylogeny of Anaplasma marginale, Anaplasma ovis and Theileria ovis in goats and sheep enrolled from a hill station in Punjab, Pakistan. PLoS ONE 18(11):e0291302. https://doi.org/10.1371/journal.pone.0291302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asif M, Parveen A, Ashraf S, Hussain M, Aktas M, Ozubek S, Shaikh RS, Iqbal F (2020) First Report regarding the simultaneous molecular detection of Anaplasma marginale and theileria annulata in equine blood samples collected from Southern Punjab in Pakistan. Acta Parasitol 65(1):259–263. https://doi.org/10.2478

    Article  CAS  PubMed  Google Scholar 

  • Atif FA, Abbas RZ, Mehnaz S, Qamar MF, Hussain K, Nazir MU, Zaman MA, Khan AU, Said MB (2022) First report on molecular surveillance based on duplex detection of Anaplasma marginale and theileria annulata in dairy cattle from Punjab. Pakistan Trop Anim Health Prod 54(2):155. https://doi.org/10.1007/s11250-022-03158-y

    Article  PubMed  Google Scholar 

  • Bawm S, Sagara R, Kakisaka K, Thu MY, Hmoon MM, Htun LL, Win MM, Nonaka N, Nakao R, Suzuki H, Katakura K (2021) Identification, genetic variation, and structural analysis of 18S rRNA of Theileria Orientalis and Theileria velifera-like isolates from Myanmar. Parasitol Int 82:102299. https://doi.org/10.1016/j.parint.2021.102299

    Article  CAS  PubMed  Google Scholar 

  • Bilgic HB, Karagenc T, Simuunza M, Shiels B, Tait A, Eren H, Weir W (2013) Development of multiplex PCR assay for simultaneous detection of Theileria Annulata, Babesia Bovis and Anaplasma marginale in cattle. Exp Parasitol 13:222–229

    Article  Google Scholar 

  • Bowie MV, de la Fuente J, Kocan KM, Blouin EF, Barbet AF (2002) Conservation of major surface protein 1 genes of Anaplasma marginale during cyclic transmission between ticks and cattle. Gene 282(1–2):95–102. https://doi.org/10.1016/s0378-1119(01)00845-9

    Article  CAS  PubMed  Google Scholar 

  • Ceylan C, Ekici ÖD (2022) Molecular investigation of ovine and caprine anaplasmosis in south-eastern Anatolia region of Turkey. Pak Vet J. https://doi.org/10.29261/pakvetj/2022.070

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Hameed A, Schlecht E, Tariq M, Buerkert A, Scheper C, König S, Roessler R (2022) Phenotypic and genetic diversity of domestic yak (Bos grunniens) in high-altitude rangelands of Gilgit-Baltistan, Pakistan. J Anim Breed Genet 139:723–737. https://doi.org/10.1111/jbg.12730

    Article  CAS  PubMed  Google Scholar 

  • He Y, Chen W, Ma P, Wei Y, Li R, Chen Z, Tian S, Qi T, Yang J, Sun Y, Li J, Kang M, Li Y (2021) Molecular detection of Anaplasma spp., Babesia spp. and Theileria spp. in yaks (Bos grunniens) and tibetan sheep (Ovis aries) on the Qinghai-Tibetan Plateau, China. Parasites Vectors 14(613). https://doi.org/10.1186/s13071-021-05109-2

  • Hussain T, Wajid A, Soail M, Ali A, Abbas K, Marikar FMMT, Musthafa M, Babar ME (2021) Molecular phylogeny and genetic diversity of domestic yaks (Bos grunniens) in Pakistan based on mitochondrial and microsatellite markers. Veterinarska Stanica 52(6). https://doi.org/10.46419/vs.52.6.5

  • Irfan M, Chang SC, Iqbal RK, Tanveer M, Asif M, Adil K, Nasreen N, Atif FA, Shaikh RS, Aktas M, Ben Said M, Iqbal F, Chen C (2023) Seasonality, epidemiology and phylogeny of Theileria ovis with a note on hematological and biochemical changes in asymptomatic infected goats from Pakistan. PLoS ONE 18(8):e0290620. https://doi.org/10.1371/journal.pone.0290620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Chapter  Google Scholar 

  • Khan B, Abbas S, Khan MZ, Khan G, Anjum M, Baig S, Jamal S (2016) Indigenous practices of yak breeding in Gilgit-Baltistan: Current status and future prospects for transboundary yak husbandry in the Karakoram-Pamir mountain area. In W. Ning, Y. Shailiang, S. Joshi, & N. Bisht (Eds.), Yak on the move: Transboundary challenges and opportunities for yak raising in a changing Hindu Kush Himalayan region. International Centre for Integrated Mountain Development (ICIMOD). 38: 167–180

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lan Y, Li K, Mehmood K, Qudratullah (2021) Molecular investigation of important protozoal infections in yaks. Pak Vet J 41(4):557–561. https://doi.org/10.29261/pakvetj/2020.048

    Article  CAS  Google Scholar 

  • Li Y, Guan G, Ma M, Liu J, Ren Q, Luo J, Yin H (2011) Theileria ovis discovered in China. Exp Parasitol 127(1):304–307. https://doi.org/10.1016/j.exppara.2010.07.002

    Article  CAS  PubMed  Google Scholar 

  • Li J, Jian Y, Jia L, Galon EM, Benedicto B, Wang G, Cai Q, Liu M, Li Y, Ji S, Tumwebaze MA, Ma L, Xuan X (2020) Molecular characterization of tick-borne bacteria and protozoans in yaks (Bos grunniens), tibetan sheep (Ovis aries) and bactrian camels (Camelus bactrianus) in the Qinghai-Tibetan Plateau Area, China. Ticks and Tick-borne diseases. 11(5):101466. https://doi.org/10.1016/j.ttbdis.2020.101466

  • Ma Y, Jian Y, Wang G, Li J, Zafar I, Li X, Wang G, Hu Y, Li H, Liu M, Yokoyama N, Ma L, Xuan X (2023) Epidemiological investigation of Tick-Borne bacterial pathogens in domestic animals from the Qinghai-Tibetan Plateau Area, China. https://doi.org/10.20944/preprints202312.1294.v1. Preprints

  • Molad T, Mazuz ML, Fleiderovitz L, Fish L, Savitsky I, Krigel Y, Leibovitz B, Molloy J, Jongejan F, Shkap V (2006) Molecular and serological detection of A. centrale- and A. marginale-infected cattle grazing within an endemic area. Vet Microbiol 113(1–2):55–62. https://doi.org/10.1016/j.vetmic.2005.10.026

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay B, Khan A (2015) A reevaluation of the snowmelt and glacial melt in river flows within upper Indus Basin and its significance in a changing climate. J Hydrol 527:119–132

    Article  Google Scholar 

  • Naveed S, Hussain T, Wajid A, Ali T, Ashdar A, Hussain SM, Ain QU, Bano B, Babar ME (2023) Single nucleotide polymorphism in prolactin (PRL) gene of yak (Bos grunniens) population of Gilgit-Baltistan, Pakistan. Intl J Agric Biol 29:324–329

    CAS  Google Scholar 

  • Niaz S, Ur Rahman Z, Ali I, Cossío-Bayúgar R, Amaro-Estrada I, Alanazi AD, Khattak I, Zeb J, Nasreen N, Khan A (2021) Molecular prevalence, characterization and associated risk factors of Anaplasma spp. and Theileria spp. in small ruminants in Northern Pakistan. Parasite 28, 3

  • Ochirkhuu N, Konnai S, Odbileg R, Murata S, Ohashi K (2017) Molecular Epidemiological Survey and genetic characterization of Anaplasma Species in Mongolian Livestock.Vector-Borne and Zoonotic diseases. https://doi.org/10.1089/vbz.2017.2111

  • Pierlé SA, Rosshandler II, Kerudin AA, Sambono J, Lew-Tabor A, Rolls P, Rangel-Escareño C, Brayton KA (2014) Genetic diversity of Tick-Borne Rickettsial pathogens; insights gained from distant strains. Pathogens (Basel Switzerland) 3(1):57–72. https://doi.org/10.3390/pathogens3010057

    Article  CAS  PubMed  Google Scholar 

  • Qazalbash MA, Masud T, Ahmad A, Hayat R, Ibrahim MS, Mujtaba A, Mumtaz A, Asad MJ (2021) Diversity of lactic acid bacteria associated with raw yak (Bos grunniens) milk produced in Pakistan. J Anim Feed Sci 30(1):42–51. https://doi.org/10.22358/jafs/133201/2021

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Viseshakul N, Kamper S, Bowie MV, Barbet AF (2000) Sequence and expression analysis of a surface antigen gene family of the rickettsia Anaplasma marginale. Gene 253(1):45–53. https://doi.org/10.1016/s0378-1119(00)00241-9

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wang B, Zhang Q, Yang Z, Han S, Yuan G, Wang G, He H (2021) The common occurrence of Theileria ovis in Tibetan Sheep and the First Report of Theileria sinensis in yaks from Southern Qinghai. China Acta Parasit 66:1177–1185. https://doi.org/10.1007/s11686-021-00381-9

    Article  Google Scholar 

  • Yang J, Liu Z, Niu Q, Junlong L, Guiquan G, Jingying X, Jianxun L, Shuqing W, Shufang W, Hong Y (2016) First molecular survey and identification of Anaplasma spp. in white yaks (Bos grunniens) in China. Parasitology. 2016;143(6):686–691. https://doi.org/10.1017/S003118201600041X

  • Ye W, Qingxun Z, Shuyi H, Ying L, Bo W, Guohui Y, Peiyang Z, Ziwen Y, Heng Z, Yali S, Jiyong C, Xueqing H, Hongxuan 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 Veterinary Sci 8. https://doi.org/10.3389/fvets.2021.727166

  • Zafar SNUA, Khan A, Niaz S, Aktas M, Ozubek S, Farooq M, Adil MM, Zając Z, Iqbal F, Alhimaidi AR, Swelum AA (2022) Prevalence of Anaplasma marginale in cattle blood samples collected from two important livestock regions in Punjab (Pakistan) with a note on epidemiology and phylogeny of parasite. Saudi J Biol Sci 29(3):1515–1520. https://doi.org/10.1016/j.sjbs.2021.11.020

    Article  CAS  PubMed  Google Scholar 

  • Zakkyeh T, Oshaghi MA, Hosseini- Vasoukolaei N, Yaghoobi EMR, Babamahmoudi F, Mohtarami F (2012) First molecular detection of Theileria ovis in Rhipicephalus sanguineus tick in Iran. Asia Pac J Trop Med 5:29–32

    Article  CAS  Google Scholar 

  • Zhang J, Ma H, Ai J, Qi T, Kang M, Li J, Sun Y (2022) Serological analysis of IgG and IgM antibodies against Anaplasma spp. in various animal species of the Qinghai-Tibetan Plateau. Animals 12(19):2723. https://doi.org/10.3390/ani12192723

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou Z, Li K, Sun Y, Shi J, Li H, Chen Y et al (2019) Molecular epidemiology and risk factors of Anaplasma spp., Babesia spp. and Theileria spp. infection in cattle in Chongqing, China. PLoS ONE 14(7):e0215585. https://doi.org/10.1371/journal.pone.0215585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by the Livestock, Dairy Development and Poultry Production Department of Gilgit-Baltistan, Virtual University of Pakistan, Islamabad and the YCF through the grant P2023/1 for the collection and processing of yak samples from different districts of the Gilgit-Baltistan, Pakistan.

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FI and TH had designed and supervised this study. MMS, TA ZUR and TH collected the yak samples and epidemiological data. Mu N, MN and MA performed the wet lab experiments. TH, Ad K and Af K performed the phylogenetic analysis. AK and MB performed the statistical analysis. All authors contributed to the writing of manuscript and approved the final version for submission.

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Correspondence to Adil Khan or Furhan Iqbal.

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Communicated by Yusuf Akhter.

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Nawaz, M., Ullah, R., Rehman, Z.U. et al. Leading report of molecular prevalence of tick borne Anaplasma marginale and Theileria ovis in yaks (Bos grunniens) from Pakistan. Arch Microbiol 206, 149 (2024). https://doi.org/10.1007/s00203-024-03916-6

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  • DOI: https://doi.org/10.1007/s00203-024-03916-6

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