Abstract
Introduction
Tick-borne diseases (TBDs) pose a major hindrance to livestock production in countries with limited resources. Effective prevention and management of TBDs require a thorough understanding of disease vectors and pathogens. However, there is limited information on studies of bovine tick-borne pathogens (TBPs) using molecular methods in Malawi. This study aimed to detect TBPs of cattle populations in southern Malawi, which has the largest cattle population in the country.
Methodology
A total of 220 blood samples from apparently healthy cattle were collected in six districts, and were screened for selected TBPs using polymerase chain reaction (PCR).
Results
The overall detection rate of TBPs was 72.3%. Among the detected pathogens, Babesia bigemina had the highest detection rate (34.5%), followed by Anaplasma marginale (23.2%), Anaplasma phagocytophilum (22.3%), Theileria taurotragi (22.3%), Theileria parva (15.5%), Anaplasma bovis (9.6%), Babesia bovis (7.3%), Theileria mutans (4.1%), and Babesia naoakii (2.7%). Among the positive samples, 64.2% were found to be co-infected with two or more TBPs, with the highest number of seven pathogens detected in a single sample. The study documents the existence of A. phagocytophilum, B. bovis, and B. naoakii in Malawian cattle for the first time.
Conclusion
The findings herein demonstrate a significant burden of TBPs on cattle in Malawi, which gives a challenge in combating TBDs. The high TBP burden, along with the high co-infection frequencies in Malawian cattle necessitates the urgency to implement effective control strategies to enhance cattle production in the country.
Similar content being viewed by others
Data availability
The data will be available on request from the corresponding authors.
References
Adjou Moumouni PF, Aboge GO, Terkawi MA, Masatani T, Cao S, Kamyingkird K, Jirapattharasate C, Zhou M, Wang G, Liu M, Iguchi A, Vudriko P, Ybanez AP, Inokuma H, Shirafuji-Umemiya R, Suzuki H, Xuan X (2015) Molecular detection and characterization of Babesia bovis, Babesia bigemina, Theileria species and Anaplasma marginale isolated from cattle in Kenya. Parasit Vectors 8:496. https://doi.org/10.1186/s13071-015-1106-9
Berggren SA (1978) Cattle ticks in Malawi. Vet Parasitol 4:289–297. https://doi.org/10.1016/0304-4017(78)90055-9
Bock R, Jackson L, de Vos A, Jorgensen W (2004) Babesiosis of cattle. Parasitology 129:247–269. https://doi.org/10.1017/S0031182004005190
Byaruhanga C, Collins NE, Knobel D, Chaisi ME, Vorster I, Steyn HC, Oosthuizen MC (2016) Molecular investigation of tick-borne haemoparasite infections among transhumant zebu cattle in Karamoja Region, Uganda. Vet Parasitol Reg Stud Rep 3–4:27–35. https://doi.org/10.1016/j.vprsr.2016.06.004
Cao WC, Zhao QM, Zhang PH, Dumler JS, Zhang XT, Fang LQ, Yang H (2000) Granulocytic Ehrlichiae in Ixodes persulcatus ticks from an area in China where Lyme disease is endemic. J Clin Microbiol 38:4208–4210. https://doi.org/10.1128/jcm.38.11.4208-4210.2000
Chaisi ME, Collins NE, Potgieter FT, Oosthuizen MC (2013) Sequence variation identified in the 18S rRNA gene of Theileria mutans and Theileria velifera from the African buffalo (syncerus caffer). Vet Parasitol 191:132–137. https://doi.org/10.1016/j.vetpar.2012.08.005
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
Chikufenji B, Chatanga E, Galon EM, Mohanta UK, Mdzukulu G, Nkhata M, Ma Y, Shirafuji-Umemiya R, Xuan X (2024) First report of dog ticks and tick-borne pathogens they are carrying in Malawi. J Vet Med Sci 86:150–159. https://doi.org/10.1292/jvms.23-0397
DAHLD, 2006. Policy document on livestock in Malawi. Ministry of Agriculture, Irrigation and Water Development (MoAIWD); Department of Animal Health and Livestock Development (DAHLD): Lilongwe, Malawi
De Vos AJ, Bessenger R, Banting LF (1981) Research communication Theileria taurotragi: A probable agent of bovine cerebral theileriosis Onderstepoort. J Vet Res 48:177–178
Dugat T, Lagrée AC, Maillard R, Boulouis HJ, Haddad N (2015) Opening the black box of Anaplasma phagocytophilum diversity: Current situation and future perspectives. Front Cell Infect Microbiol 5:00061. https://doi.org/10.3389/fcimb.2015.00061
Inokuma H, Oyamada M, Kelly PJ, Jacobson LA, Fournier PE, Itamoto K, Okuda M, Brouqui P (2005) Molecular detection of a new Anaplasma species closely related to Anaplasma phagocytophilum in canine blood from South Africa. J Clin Microbiol 43:2934–2937. https://doi.org/10.1128/jcm.43.6.2934-2937.2005
Jurković D, Mihaljević Ž, Duvnjak S, Silaghi C, Beck R (2020) First reports of indigenous lethal infection with Anaplasma marginale, Anaplasma bovis and Theileria orientalis in Croatian cattle. Ticks Tick-Borne Dis 11:101469. https://doi.org/10.1016/j.ttbdis.2020.101469
Mangold AJ, Bargues MD, Mas-Coma S (1998) Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res 84:478–484. https://doi.org/10.1007/s004360050433
Martins TM, Pedro OC, Caldeira RA, do Rosário VE, Neves L, Domingos A, (2008) Detection of bovine babesiosis in Mozambique by a novel semi-nested hot-start PCR method. Vet Parasitol 153:225–230. https://doi.org/10.1016/j.vetpar.2008.01.037
Minjauw B, McLeod A (2003) Tick-Borne Diseases and Poverty. The Impact of Ticks and Tick-Borne Diseases on the Livelihood of Small-Scale and Marginal Livestock Owners in India and Eastern and Southern Africa. UK: Research Report, DFID Animal Health Programme, Centre for Tropical Veterinary Medicine, University of Edinburgh 116
MoAIWD, (2022) Agricultural production estimates survey. Ministry of Agriculture Irrigation and Water Development, Lilongwe, Malawi
Mohanta UK, Chikufenji B, Galon EM, Ji S, Ma Z, El-Sayed SAES, Amer MM, Do TT, Xuan X (2023) Molecular characterization and phylogeny of Anaplasma marginale, A. Phagocytophilum and A. Bovis in livestock of Bangladesh. Parasitol Int 97:102790. https://doi.org/10.1016/j.parint.2023.102790
Mohanta UK, Chikufenji B, Galon EM, Ji S, Ma Z, El-Sayed SAES, Ringo AE, Do TT, Xuan X (2023) Molecular Detection and Phylogenetic Analyses of Babesia spp. and Theileria spp. in Livestock in Bangladesh. Microorganisms 11:1563. https://doi.org/10.3390/microorganisms11061563
Mtshali K, Khumalo ZTH, Nakao R, Grab DJ, Sugimoto C, Thekisoe OMM (2016) Molecular detection of zoonotic tick-borne pathogens from ticks collected from ruminants in four South African provinces. J Vet Med Sci 77:1573–1579. https://doi.org/10.1292/jvms.15-0170
Ocaido M, Muwazi RT, Opuda JA (2009) Economic impact of ticks and tick-borne diseases on cattle production systems around Lake Mburo National Park in South Western Uganda. Trop Anim Health Prod 41:731–739. https://doi.org/10.1007/S11250-008-9245-Z
Odongo DO, Sunter JD, Kiara HK, Skilton RA, Bishop RP (2010) A nested PCR assay exhibits enhanced sensitivity for detection of Theileria parva infections in bovine blood samples from carrier animals. Parasitol Res 106:357–365. https://doi.org/10.1007/s00436-009-1670-z
Olds CL, Mason KL, Scoles GA (2018) Rhipicephalus appendiculatus ticks transmit Theileria parva from persistently infected cattle in the absence of detectable parasitemia: Implications for East Coast fever epidemiology. Parasit Vectors 11:126. https://doi.org/10.1186/s13071-018-2727-6
Ota N, Mizuno D, Kuboki N, Igarashi I, Nakamura Y, Yamashina H, Hanzaike T, Fujii K, Onoe S, 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
Otgonsuren D, Sivakumar T, Amgalanbaatar T, Narantsatsral S, Tuvshintulga B, Zoljargal M, Munkhgerel D, Davkharbayar B, Baatarjargal P, Myagmarsuren P, Battsetseg B, Battur B, Yokoyama N (2020) Molecular epidemiological survey of Babesia bovis, Babesia bigemina, and Babesia sp. Mymensingh infections in Mongolian cattle. Parasitol Int 77:102107. https://doi.org/10.1016/j.parint.2020.102107
Parola P, Raoult D (2001) Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Ticks Tick-Borne Dis 32:897–928. https://doi.org/10.1086/319347
Ringo AE, Adjou Moumouni PF, Lee SH, Liu M, Khamis YH, Gao Y, Guo H, Zheng W, Efstratiou A, Galon EM, Li J, Tiwananthagorn S, Inoue N, Suzuki H, Thekisoe O, Xuan X (2018) Molecular detection and characterization of tick-borne protozoan and rickettsial pathogens isolated from cattle on Pemba Island, Tanzania. Ticks Tick-Borne Dis 9:1437–1445. https://doi.org/10.1016/j.ttbdis.2018.06.014
Ringo AE, Nonga HE, Galon EM, Ji S, Rizk MA, El-Sayed SAES, Mohanta UK, Ma Z, Chikufenji B, Do TT, Xuan X (2022) Molecular Investigation of Tick-Borne Haemoparasites Isolated from Indigenous Zebu Cattle in the Tanga Region Tanzania. Animals 12:3171. https://doi.org/10.3390/ani12223171
Simuunza M, Weir W, Courcier E, Tait A, Shiels B (2011) Epidemiological analysis of tick-borne diseases in Zambia. Vet Parasitol 175:331–342. https://doi.org/10.1016/j.vetpar.2010.09.027
Sivakumar T, Tuvshintulga B, Kothalawala H, Silva SSP, Lan DTB, Long PT, Ybañez AP, Ybañez RHD, Benitez DF, Tayebwa DS, de Macedo ACC, Schnittger L, Yokoyama N (2020) Host range and geographical distribution of Babesia sp. Mymensingh. Trans Emerg Dis 67:2233–2239. https://doi.org/10.1111/tbed.13546
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
Tembo S, Collins NE, Sibeko-Matjila KP, Troskie M, Vorster I, Byaruhanga C, Oosthuizen MC (2018) Occurrence of tick-borne haemoparasites in cattle in the Mungwi district, Northern Province, Zambia. Ticks Tick Borne Dis 9:707–717. https://doi.org/10.1016/j.ttbdis.2018.02.004
Terkawi MA, Huyen NX, Shinuo C, Inpankaew T, Maklon K, Aboulaila M, Ueno A, Goo YK, Yokoyama N, Jittapalapong S, Xuan X, Igarashi I (2011) Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Vet Parasitol 178:201–207. https://doi.org/10.1016/j.vetpar.2011.01.041
Teshale S, Geysen D, Ameni G, Dorny P, Berkvens D (2018) Survey of Anaplasma phagocytophilum and Anaplasma sp. “Omatjenne” infection in cattle in Africa with special reference to Ethiopia. Parasit Vectors 11:162. https://doi.org/10.1186/s13071-018-2633-y
Uilenberg G (1992) Veterinary Significance of Ticks and Tick-Borne Diseases. Tick Vect Biol. https://doi.org/10.1007/978-3-642-76643-5_2
Walker AR, Bouattour A, Camicas JL, Estrada-Pena A, Horak I, Latif A, Pegram RG, Preston PM (2003) Ticks of domestic animals in Africa: a guide to identification of species Bioscience Reports, Edinburgh, UK
Woldehiwet Z (2009) The natural history of Anaplasma phagocytophilum. Vet Parasitol 167:108–122. https://doi.org/10.1016/j.vetpar.2009.09.013
Woodford JD, Jones TW, Rae PF, Boid R, Bell-Sakyi L (1990) Seroepidemiological studies of bovine babesiaosis on Pemba Island, Tanzania. Vet Parasitol 37:175–184. https://doi.org/10.1016/0304-4017(90)90001-R
Ybañez AP, Ybañez RH, Claveria FG, Cruz-Flores MJ, Xuan X, Yokoyama N, Inokuma H (2014) High genetic diversity of Anaplasma marginale detected from Philippine cattle. J Vet Med Sci 76:1009–1014
Acknowledgements
We thank Madalitso Jessie Nkhata, Vincent Kachisi, Joe Magombo, and the animal owners for the various roles played in this study.
Funding
This study was funded by the grant-in-Aid for Scientific Research (18KK0188), JSPS Core-to-Core program, and Strategic International Collaborative Research Project (JPJ008837) sponsored by the Ministry of Agriculture, Forestry, and Fisheries of Japan.
Author information
Authors and Affiliations
Contributions
Conceptualization, formal analysis, data curation, investigation, visualisation, methodology, writing original draft: Boniface Chikufenji. Writing-review and editing the original draft: Elisha Chatanga and Kyoko Hayashida. Methodology and Writing-review and editing: Uday Kumar Mohanta. Methodology and logistics: Nathan Kamanga, Eloiza May Galon, Aaron Ringo and Zhuowei Ma. Conceptualization, funding acquisition, resources, supervision, writing -review and editing: Xuenan Xuan.
Corresponding authors
Ethics declarations
Ethical approval and consent to participate
Authorization (permission ID number: DAHLD 002/2022) for sampling from cattle in the study locations was obtained from the Ministry of Agriculture Irrigation and Water Development (MoAIWD) through the Department of Animal Health and Livestock Development (DAHLD). Before sample collection, cattle owners were briefed on the significance of the activity and freely accepted to take part. Blood was collected by licensed veterinarians by following the ethical guidelines of Obihiro University of Agriculture and Veterinary Medicine, Hokkaido, Japan (animal experiment approval ID numbers: 22–23).
Consent for publication
All authors have read and approved the final version of this paper and have agreed for its publication.
Competing interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chikufenji, B., Mohanta, U.K., Hayashida, K. et al. Molecular detection and phylogenetic analysis of tick-borne pathogens in cattle from southern Malawi. Vet Res Commun (2024). https://doi.org/10.1007/s11259-024-10395-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11259-024-10395-z