Abstract
In this study, we investigated and confirmed natural lumpy skin disease virus (LSDV) infection in Himalayan yaks (Bos grunniens) in Himachal Pradesh, India, based on clinical manifestations and results of genome detection, antibody detection, virus isolation, and nucleotide sequencing. Subsequent phylogenetic analysis based on complete GPCR, RPO30, and EEV gene sequences revealed that the LSDV isolates from these yaks and local cattle belonged to LSDV subcluster 1.2.1 rather than the dominant subcluster 1.2.2, which is currently circulating in India, suggesting a separate recent introduction. This is the first report of natural LSDV infection in yaks in India, expanding the known host range of LSDV. Further investigations are needed to assess the impact of LSDV infection in yaks.
Data availability
All of the required data are available in the figures and main text of the article or in the supplementary materials. The sequence data generated in this study were submitted to the GenBank database and are available under the accession numbers OR026634-OR026642. The datasets generated and/or analysed in the present study are available from the corresponding author on reasonable request.
References
World Organization for Animal Health (2022) Frequently asked questions (FAQ) on lumpy skin disease. Available online: https://www.woah.org/en/document/faq-on-lumpy-skin-disease-lsd/ (accessed on 02 December 2022)
Tulman ER, Afonso CL, Lu Z, Zsak L, Kutish GF, Rock DL (2001) Genome of lumpy skin disease virus. J Virol 75:7122–7130
Tuppurainen ESM, Venter EH, Shisler JL, Gari G, Mekonnen GA, Jule N et al (2017) Review: Capripoxvirus Diseases: Current Status and Opportunities for Control. Transbound Emerg Dis 64:729–745
Babiuk S, Bowden TR, Parkyn G, Dalman B, Manning L, Neufeld J et al (2008) Quantification of lumpy skin disease virus following experimental infection in cattle. Transbound Emerg Dis 55:299–307
Shumilova I, Nesterov A, Byadovskaya O, Prutnikov P, Wallace DB, Mokeeva M et al (2022) A Recombinant Vaccine-like Strain of Lumpy Skin Disease Virus Causes Low-Level Infection of Cattle through Virus-Inoculated Feed. Pathogens 11:920
Azeem S, Sharma B, Shabir S, Akbar H, Venter EH (2022) Lumpy skin disease is expanding its geographic range: A challenge for Asian livestock management and food security. Vet J 279:105785
Lu G, Xie J, Luo J, Shao R, Jia K, Li S (2021) Lumpy skin disease outbreaks in China, since 3 August 2019. Transbound Emerg Dis 68:216–219
Biswas D, Saha S, Sayeed S (2020) Outbreak of lumpy skin disease of cattle in south-west part of Bangladesh and its clinical management. Vet Sci Res Rev 6:100–108
Sudhakar SB, Mishra N, Kalaiyarasu S, Jhade SK, Hemadri D, Sood R et al (2020) Lumpy skin disease (LSD) outbreaks in cattle in Odisha state, India in August 2019: Epidemiological features and molecular studies. Transbound Emerg Dis 67:2408–2422
Sudhakar SB, Mishra N, Kalaiyarasu S, Jhade SK, Singh VP (2022) Genetic and phylogenetic analysis of lumpy skin disease viruses (LSDV) isolated from the first and subsequent field outbreaks in India during 2019 reveals close proximity with unique signatures of historical Kenyan NI-2490/Kenya/KSGP-like field strains. Transbound Emerg Dis 69:e451–e462
DAHD (2023) Report of Lumpy Skin Disease in India. Department of Animal Husbandary, Dairying and Fisheries. Government of India
World Organization for Animal Health (2022) Lumpy skin disease. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Available online (accessed on 02 December 2022).
Porco A, Chea S, Sours S, Nou V, Groenenberg M, Agger C et al (2023) Case report: Lumpy skin disease in an endangered wild banteng (Bos javanicus) and initiation of a vaccination campaign in domestic livestock in Cambodia. Front Vet Sci 10:1228505. https://doi.org/10.3389/fvets.2023.1228505
Mishra N, Vilcek S, Rajukumar K, Dubey R, Tiwari A, Galav V, Pradhan HK (2008) Identification of bovine viral diarrhea virus type 1 in Yaks (Bos poephagus grunniens) in the Himalayan region. Res Vet Sci 84:507–510
Rout M, Doley J, Maiti S, Bera AK, Chatterjee N, Bhattacharya D, Mohapatra JK (2016) Evidence of foot-and-mouth disease virus infection in yaks reared in a farm of Arunachal Pradesh. Ind J Vet Path 40:284–286
Bowden TR, Babiuk SL, Parkyn GR, Copps JS, Boyle DB (2008) Capripoxvirus tissue tropism and shedding: a quantitative study in experimentally infected sheep and goats. Virology 371:380–393
Pestova YE, Artyukhova EE, Kostrova EE, Shumoliva IN, Kononov AV, Sprygin AV (2018) Real time PCR for the detection of field isolates of lumpy skin disease virus in clinical samples from cattle. Agri Biol 53:422–429
Zhou T, Jia H, Chen G, He X, Fang Y, Wang X et al (2012) Phylogenetic analysis of Chinese sheeppox and goatpox virus isolates. Virol J 9:25
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Hedger RS, Hamblin C (1983) Neutralising antibodies to lumpy skin disease virus in African wildlife. Comp Immunol Microbiol Infect Dis 6:209–213
Greth A, Gourreau JM, Vassart M, Nguyen-Ba-Vy, Wyers M, Lefevre PC (1992) Capripoxvirus disease in an Arabian oryx (Oryx leucoryx) from Saudi Arabia. J Wildl Dis 28:295–300
Le Goff C, Lamien CE, Fakhfakh E, Chadeyras A, Aba-Adulugba E, Libeau G, Tuppurainen E et al (2009) Capripoxvirus G-protein-coupled chemokine receptor: A host-range gene suitable for virus animal origin discrimination. J GenVirol 90:1967–1977
Fagbo S, Coetzer JAW, Venter EH (2014) Seroprevalence of Rift Valley fever and lumpy skin disease in African buffalo (Syncerus caffer) in the Kruger National Park and Hluhluwe-iMfolozi Park, South Africa. J S Afr Vet Assoc 85:e1–e7
Dao TD, Tran LH, Nguyen HD, Hoang TT, Nguyen GH, Tran KVD et al (2022) Characterization of Lumpy skin disease virus isolated from a giraffe in Vietnam. Transbound Emerg Dis 69:e3268–e3272
Sudhakar SB, Mishra N, Kalaiyarasu S, Ahirwar K, Chatterji S, Parihar O, Singh VP, Sanyal A (2023) Lumpy skin disease virus infection in free-ranging Indian gazelles (Gazella bennettii), Rajasthan, India. Emerg Infect Dis 29(7):1407–1410. https://doi.org/10.3201/eid2907.230043
Kumar R, Godara B, Chander Y, Kachhawa JP, Dedar RK, Verma A et al (2023) Evidence of lumpy skin disease virus infection in camels. Acta Trop 242:106922
Li Y, Zeng Z, Li K, Rehman MU, Nawaz S, Kulyar MF et al (2023) Detection of Culex tritaeniorhynchus Giles and Novel Recombinant Strain of Lumpy Skin Disease Virus Causes High Mortality in Yaks. Viruses 15:880. https://doi.org/10.3390/v15040880
Biswas S, Noyce RS, Babiuk LA, Lung O, Bulach DM, Bowden TR et al (2020) Extended sequencing of vaccine and wild-type Capripoxvirus isolates provides insights into genes modulating virulence and host range. Transbound Emerg Dis 67:80–97
Van Schalwyk A, Byadovskaya O, Shumilova I, Wallace DB, Sprygin A (2021) Estimating evolutionary changes between highly passaged and original parental lumpy skin disease virus strains. Transbound Emerg Dis 69:e486–e496
Breman FC, Haegeman A, Kreši´c N, Philips W, De Regge N (2023) Lumpy Skin Disease Virus Genome Sequence Analysis: Putative Spatio-Temporal Epidemiology, Single Gene versus Whole Genome Phylogeny and Genomic Evolution. Viruses 15:1471. https://doi.org/10.3390/v15071471
Manic M, Stojiljkovic M, Petrovic M, Nisavic J, Bacic D, Petrovic T (2016) Epizootic features and control measures for lumpy skin disease in south-east Serbia in 2016. Transbound Emerg Dis 66:2087–2099
Molini U, Boshoff E, Niel AP, Phillips J, Khaiseb S, Settypalli TB et al (2021) Detection of Lumpy Skin Disease Virus in an Asymptomatic Eland (Taurotragus oryx) in Namibia. J Wildl Dis 57:708–711
Acknowledgements
We thank the Department of Animal Husbandry & Dairying, Ministry of Fisheries, Animal Husbandry and Dairying, New Delhi, for funding support, and the Director, ICAR-NIHSAD, Bhopal, for infrastructure facilities and administrative support.
Funding
This study was supported by a grant from the Department of Animal Husbandry & Dairying, Ministry of Fisheries, Animal Husbandry and Dairying, New Delhi, India (grant no. CDDL1005235).
Author information
Authors and Affiliations
Contributions
Conceptualization: All authors contributed to the conception and design of the study. Data curation: S.B.S., S.K., R.K.S., K.A., V.S.V., and N.M. Methodology: S.B.S., S.K., R.K.S., K.A., V.S.V., and N.M. Data analysis and interpretation of results: S.B.S., S.K., and N.M. Supervision, N.M. and A.S. Writing – original draft, N.M. Review and Editing of the Manuscript: N.M. and A.S. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Ethical approval
This study was based on samples (nasal swabs and serum) collected from domestic yaks by qualified veterinarians as per standard practices, without the use of anaesthesia, and submitted to the ICAR-National Institute of High Security Animal Diseases, Bhopal, India, for laboratory diagnosis of LSD, and hence did not require any animal ethical approval.
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by William G Dundon
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material
Rights and permissions
About this article
Cite this article
Sudhakar, S.B., Mishra, N., Kalaiyarasu, S. et al. Emergence of lumpy skin disease virus (LSDV) infection in domestic Himalayan yaks (Bos grunniens) in Himachal Pradesh, India. Arch Virol 169, 51 (2024). https://doi.org/10.1007/s00705-024-05994-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00705-024-05994-9