Molecular analysis of Anaplasma ovis, Theileria ovis and Brucella abortus in adult Ornithodoros lahorensis soft ticks (Acari: Ixodida: Argasidae) isolated from the Xinjiang Uygur Autonomous Region, China

Liu, Dandan; Wang, Jinming; Liu, Yutong; Wang, Shuiyi; Zhu, Huiru; Jiang, Bingbing; Li, Yongchang; Zhang, Yang; Chahan, Bayin; Zhang, Wei

doi:10.2478/jvetres-2024-0049

Abstract

Introduction

Ticks are obligate blood-feeding arthropods that cause significant economic losses in domestic animal husbandry and threaten public health. However, information about soft ticks (Acari: Argasidae) and tick-borne pathogens in the Xinjiang Uygur Autonomous Region (XUAR) of China is scarce.

Material and Methods

In this study, PCR assays and gene sequencing were used to detect and analyse the epidemiological features of Anaplasma ovis, Theileria ovis and Brucella abortus parasitic infections in 366 Ornithodoros lahorensis soft ticks collected from five sampling sites in the XUAR from October 2019 to March 2022. The ticks were identified by morphological and molecular methods as O. lahorensis. The PCR was conducted using primers complementary to the major surface protein 4 (Msp4) gene of A. ovis, the 18S ribosomal RNA (18S rRNA) of T. ovis and the outer membrane protein 22 (Omp22) gene of B. abortus.

Results

The overall infection rate was 91/366 (24.9%) for A. ovis, 127/366 (34.7%) for T. ovis and 94/366 (25.6%) for B. abortus. Sequencing analysis indicated that A. ovis Msp4, T. ovis 18S rRNA and B. abortus Omp22 genes from XUAR isolates showed 99.58–100% identity with documented isolates from other countries.

Conclusion

This study provides fundamental evidence for the occurrence of A. ovis, T. ovis and B. abortus in O. lahorensis. Therefore, the potential threat of soft ticks to livestock and humans should not be ignored. This study expands the understanding of the existence of tick-borne pathogens in O. lahorensis and is expected to improve the strategies for prevention and control of ticks and tick-borne diseases in China.

References

Aktas M., Altay K., Dumanli N.: PCR-based detection of Theileria ovis in Rhipicephalus bursa adult ticks. Vet Parasitol 2006, 140, 259–263, doi: 10.1016/j.vetpar.2006.04.005.
Open DOI Search in Google Scholar Back to article
Al-Hosary A.A., ElSify A., Salama A.A., Nayel M., Elkhtam A., Elmajdoub L.O., Rizk M.A., Hawash M.M., Al-Wabel M.A., Almuzaini A.M., Ahmed L.S.E.D., Paramasivam A., Mickymaray S., Omar M.A.: Phylogenetic study of Theileria ovis and Theileria lestoquardi in sheep from Egypt: Molecular evidence and genetic characterization. Vet World 2021, 14, 634–639, doi: 10.14202/VETWORLD.2021.634-639.
Open DOI Search in Google Scholar Back to article
Bakkes D.K., de Klerk D., Latif A.A., Mans B.J.: Integrative taxonomy of Afrotropical Ornithodoros (Ornithodoros) (Acari: Ixodida: Argasidae). Ticks Tick Borne Dis 2018, 9, 1006–1037, doi: 10.1016/j.ttbdis.2018.03.024.
Open DOI Search in Google Scholar Back to article
Balashov Yu.S.: Blood sucking ticks (Ixodoidea)—vectors of diseases of man and animals. Misc Publ Entomol Soc Am 1972, 8.
Search in Google Scholar Back to article
Ben Said M., Belkahia H., Messadi L.: Anaplasma spp. in North Africa: A review on molecular epidemiology, associated risk factors and genetic characteristics. Ticks Tick Borne Dis 2018, 9, 543–555, doi: 10.1016/j.ttbdis.2018.01.003.
Open DOI Search in Google Scholar Back to article
Chochlakis D., Ioannou I., Tselentis Y., Psaroulaki A.: Human anaplasmosis and Anaplasma ovis variant. Emerg Infect Dis 2010, 16, 1031–1032, doi: 10.3201/eid1606.090175.
Open DOI Search in Google Scholar Back to article
Corbel M.J.: Brucellosis in humans and animals, edited by M.J. Corbel, S.S. Elberg, O. Cosivi, WHO Press, Geneva, Switzerland, 2006.
Search in Google Scholar Back to article
Dorneles E.M.S., Sriranganathan N., Lage A.P.: Recent advances in Brucella abortus vaccines. Vet Res 2015, 46, 76, doi: 10.1186/s13567-015-0199-7.
Open DOI Search in Google Scholar Back to article
Estrada-Peña A., Jongejan F.: Ticks feeding on humans: A review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 1999, 23, 685–715, doi: 10.1023/A:1006241108739.
Open DOI Search in Google Scholar Back to article
Garin-Bastuji B., Oudar J., Richard Y., Gastellu J.: Isolation of Brucella melitensis biovar 3 from a chamois (Rupicapra rupicapra) in the southern French Alps. J Wildl Dis 1990, 26, 116–118, doi: 10.7589/0090-3558-26.1.116.
Open DOI Search in Google Scholar Back to article
Gradwell D.V., Schutte A.P., van Niekerk C.A., Roux D.J.: The isolation of Brucella abortus biotype I from African buffalo in the Kruger National Park. J S Afr Vet Assoc 1977, 48, 41–43, https://hdl.handle.net/10520/AJA00382809_4663.
Search in Google Scholar Back to article
Gray J.S., Dautel H., Estrada-Peña A., Kahl O., Lindgren E.: Effects of Climate Change on Ticks and Tick-Borne Diseases in Europe. Interdiscip Perspect Infect Dis 2009, 2009, 593232, doi: 10.1155/2009/593232.
Open DOI Search in Google Scholar Back to article
Han R., Yang J., Liu Z., Gao S., Niu Q., Hassan M.A., Luo J., Yin H.: Characterization of Anaplasma ovis strains using the major surface protein 1a repeat sequences. Parasit Vectors 2017, 10, 447, doi: 10.1186/s13071-017-2363-6.
Open DOI Search in Google Scholar Back to article
Hoogstraal H.: Argasid and Nuttalliellid Ticks as Parasites and Vectors. Adv Parasitol 1985, 24, 135–238, doi: 10.1016/S0065-308X(08)60563-1.
Open DOI Search in Google Scholar Back to article
Hoogstraal H., Wassef H.Y., Diab F.M., Al-Asgah N.A., Al-Khalifa M.S.: Acarina of Saudi Arabia: Ornithodoros (Alveonasus) laborensis (Fam. Argasidae) in Saudi Arabia: biological, veterinary, and medical implications. Fauna Saudi Arab 1984, 6, 166–169.
Search in Google Scholar Back to article
Horak I.G., Camicas J.-L., Keirans J.E.: The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): A world list of valid tick names. Exp Appl Acarol 2002, 28, 27–54, doi: 10.1023/A:1025381712339.
Open DOI Search in Google Scholar Back to article
Jongejan F., Uilenberg G.: The global importance of ticks. Parasitology 2004, 129, S3–S14, doi: 10.1017/S0031182004005967.
Open DOI Search in Google Scholar Back to article
Khosravi A.D., Abassi E., Alavi S.M.: Isolation of Brucella melitensis and Brucella abortus from brucellosis patients by conventional culture method and polymerase chain reaction technique. Pak J Med Sci 2006, 22, 369–400.
Search in Google Scholar Back to article
Kleinerman G., Baneth G.: Part I, Family Argasidae Koch, 1844; Ornithodoros (Alectorobius) lahorensis Neumann, 1908 (Figs. 19 and 20). In: Ticks of Europe and North Africa, edited by A. Estrada-Peña, A.D. Mihalca, T.N. Petney, Springer Nature, Cham, Switzerland, 2018, pp. 63-66, doi: 10.1007/978-3-319-63760-0_15.
Open DOI Search in Google Scholar Back to article
Kumar S., Stecher G., Li M., Knyaz C., Tamura K.: MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol 2018, 35, 1547–1549, doi: 10.1093/molbev/msy096.
Open DOI Search in Google Scholar Back to article
Li S., Zhang L., Zhou P., Li Z., Song H., Song Y., Li C., Xiangzheng W., Wu J.: Detection of Babesia spp., Theileria spp., and Anaplasma ovis in Ornithodoros lahorensis from southern Xinjiang, China. J Vet Res 2023, 67, 79–85, doi: 10.2478/jvetres-2023-0016.
Open DOI Search in Google Scholar Back to article
Li Y., Guan G., Ma M., Liu J., Ren Q., Luo J., Yin H.: Theileria ovis discovered in China. Exp Parasitol 2011, 127, 304–307, doi: 10.1016/j.exppara.2010.07.002.
Open DOI Search in Google Scholar Back to article
Li Y., Li J., Chahan B., Guo Q., Zhang Y., Moumouni P.F.A., Lee S.H., Liu M., Galon E.M., Guo H., Gao Y., Song R., Li M., Tumwebaze M.A., Benedicto B., Xuan X.: Molecular investigation of tick-borne infections in cattle from Xinjiang Uygur Autonomous Region, China. Parasitol Int 2020, 74, 101925, doi: 10.1016/j.parint.2019.05.003.
Open DOI Search in Google Scholar Back to article
Li Y., Wen X., Li M., Moumouni P.F.A., Galon E.M., Guo Q., Rizk M.A., Liu M., Li J., Ji S., Tumwebaze M.A., Byamukama B., Chahan B., Xuan X.: Molecular detection of tick-borne pathogens harbored by ticks collected from livestock in the Xinjiang Uygur Autonomous Region, China. Ticks Tick Borne Dis 2020, 11, 101478, doi: 10.1016/j.ttbdis.2020.101478.
Open DOI Search in Google Scholar Back to article
Mans B.J., de Klerk D., Pienaar R., Latif A.A.: Nuttalliella namaqua: A living fossil and closest relative to the ancestral tick lineage: Implications for the evolution of blood-feeding in ticks. PLoS One 2011, 6, e23675, doi: 10.1371/journal.pone.0023675.
Open DOI Search in Google Scholar Back to article
Moradi-Asl E., Jafari S.: The habitat suitability model for the potential distribution of Ornithodoros tholozani (Laboulbène et Mégnin, 1882) and Ornithodoros lahorensis (Neumann, 1908) (Acari: Argasidae): the main vectors of tick-borne relapsing fever in Iran. Ann Parasitol 2020, 66, 357–363, doi: 10.17420/ap6603.274.
Open DOI Search in Google Scholar Back to article
Ochirkhuu N., Konnai S., Mingala C.N., Okagawa T., Villanueva M., Pilapil F.M.I., Murata S., Ohashi K.: Molecular epidemiological survey and genetic analysis of vector-borne infections of cattle in Luzon Island, the Philippines. Vet Parasitol 2015, 212, 161–167, doi: 10.1016/j.vetpar.2015.05.019.
Open DOI Search in Google Scholar Back to article
Parola P., Raoult D.: Ticks and tickborne bacterial diseases in humans: An emerging infectious threat. Clin Infect Dis 2001, 32, 897–928, doi: 10.1086/319347.
Open DOI Search in Google Scholar Back to article
Philip C.B., Burgdorfer W.: Arthropod vectors as reservoirs of microbial disease agents. Annu Rev Entomol 1961, 6, 391–412, doi: 10.1146/annurev.en.06.010161.002135.
Open DOI Search in Google Scholar Back to article
Reháçek J.: Ecological relationships between ticks and rickettsiae. Eur J Epidemiol 1989, 5, 407–413, doi: 10.1007/BF00140130.
Open DOI Search in Google Scholar Back to article
Rodríguez Y., Rojas M., Gershwin M.E., Anaya J.M.: Tick-borne diseases and autoimmunity: A comprehensive review. J Autoimmun 2018, 88, 21–42, doi: 10.1016/j.jaut.2017.11.007.
Open DOI Search in Google Scholar Back to article
Sidorov V.E., Gubina E.A.: On the preservation of vaccinal strains of Br. abortus 19-BA in the tick Ornithodoros lahorensis Neumann. Zh Mikrobiol Epidemiol Immunobiol 1962, 33, 130–133.
Search in Google Scholar Back to article
Takada N., Masuzawa T., Ishiguro F., Fujita H., Kudeken M., Mitani H., Fukunaga M., Tsuchiya K., Yano Y., Ma X.H.: Lyme Disease Borrelia spp. in Ticks and Rodents from Northwestern China. Appl Environ Microbiol 2001, 67, 5161, doi: 10.1128/aem.67.11.5161-5165.2001.
Open DOI Search in Google Scholar Back to article
Tavassoli M., Malekifard F., Soleimanzadeh A., Pourseyed S.H., Bernousi I., Mardani K.: Susceptibility of different life stages of Ornithodoros lahorensis to entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Parasitol Res 2012, 111, 1779–1783, doi: 10.1007/s00436-012-3023-6.
Open DOI Search in Google Scholar Back to article
Telmadarraiy Z., Ghiasi S.M., Moradi M., Vatandoost H., Eshraghian M.R., Faghihi F., Zarei Z., Haeri A., Chinikar S.: A survey of Crimean-Congo haemorrhagic fever in livestock and ticks in Ardabil Province, Iran during 2004-2005. Scand J Infect Dis 2010, 42, 137–141, doi: 10.3109/00365540903362501.
Open DOI Search in Google Scholar Back to article
Tovar R.M.: Infection and transmission of Brucella by ectoparasites. Am J Vet Res 1947, 8, 138.
Search in Google Scholar Back to article
Vial L.: Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite 2009, 16, 191–202, doi: 10.1051/parasite/2009163191.
Open DOI Search in Google Scholar Back to article
Wang Q., Zhao S., Wureli H., Xie S., Chen C., Wei Q., Cui B., Tu C., Wang Y.: Brucella melitensis and B. abortus in eggs, larvae and engorged females of Dermacentor marginatus. Ticks Tick Borne Dis 2018, 9, 1045–1048, doi: 10.1016/j.ttbdis.2018.03.021.
Open DOI Search in Google Scholar Back to article
Wu X.B., Na R.H., Wei S.S., Zhu J.S., Pen H.J.: Distribution of tick-borne diseases in China. Parasit Vectors 2013, 6, 1–8, doi: 10.1186/1756-3305-6-119.
Open DOI Search in Google Scholar Back to article
Zhao G.-P., Wang Y.-X., Fan Z.-W., Ji Y., Liu M.-J., Zhang W.-H., Li X.-L., Zhou S.-X., Li H., Liang S., Liu W., Yang Y., Fang L.-Q.: Mapping ticks and tick-borne pathogens in China. Nat Commun 2021, 12, 1075, doi: 10.1038/s41467-021-21375-1.
Open DOI Search in Google Scholar Back to article
Zhao L., Lin X.-M., Li F., Li K.-R., He B., Zhang L.-Y., Pan J.-J., Wang Q.-R., Gao J.-M., Johnson N., Yuan X.-F., Lv J.-Z., Wu S.-Q., Liu Y.-H.: A survey of argasid ticks and tick-associated pathogens in the Peripheral Oases around Tarim Basin and the first record of Argas japonicus in Xinjiang, China. PLoS One 2018, 13, e0208615, doi: 10.1371/journal.pone.0208615.
Open DOI Search in Google Scholar Back to article
Zhao L., Lv J., Li F., Li K., He B., Zhang L., Han X., Wang H., Johnson N., Lin X., Wu S., Liu Y.: Identification and molecular analysis of ixodid ticks (Acari: Ixodidae) infesting domestic animals and tick-borne pathogens at the tarim basin of Southern Xinjiang, China. Korean J Parasitol 2020, 58, 37–46, doi: 10.3347/kjp.2020.58.1.37.
Open DOI Search in Google Scholar Back to article
Zhao L., Wang J., Ding Y., Li K., He B., Li F., Zhang L., Li X., Liu Y.: Theileria ovis (Piroplasmida: Theileriidae) Detected in Melophagus ovinus (Diptera: Hippoboscoidea) and Ornithodoros lahorensis (Ixodida: Argasidae) Removed from Sheep in Xinjiang, China. J Med Entomol 2020, 57, 631–635, doi: 10.1093/jme/tjz193.
Open DOI Search in Google Scholar Back to article