First Detection and Genetic Characterization of New Equine Parvovirus Species Circulating among Horses in Korea
Abstract
:1. Introduction
2. Material and Methods
2.1. Sample Collection
2.2. Virus Detection and Complete Coding Sequence Assembly
2.3. Phylogenetic Tree and Similarity Assessment
2.4. Statistical Analysis
3. Results
3.1. Prevalence of EqPV-CSF and EqCoPV
3.2. Analysis of Risk Factors for Virus Infection
3.3. Phylogenetic Analysis and Sequence Similarity
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Altan, E.; Li, Y.; Sabino-Santos, G., Jr.; Sawaswong, V.; Barnum, S.; Pusterla, N.; Deng, X.; Delwart, E. Viruses in horses with neurologic and respiratory diseases. Viruses 2019, 11, 942. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Giannitti, F.; Low, J.; Keyes, C.; Ullmann, L.S.; Deng, X.; Aleman, M.; Pesavento, P.A.; Pusterla, N.; Delwart, E. Exploring the virome of diseased horses. J. Gen. Virol. 2015, 96, 2721–2733. [Google Scholar] [CrossRef] [Green Version]
- Wong, F.; Spearman, J.; Smolenski, M.; Loewen, P. Equine parvovirus: Initial isolation and partial characterization. Can. J. Comp. Med. 1985, 49, 50–54. [Google Scholar] [PubMed]
- Divers, T.J.; Tennant, B.C.; Kumar, A.; McDonough, S.; Cullen, J.; Bhuva, N.; Jain, K.; Chauhan, L.S.; Scheel, T.K.H.; Lipkin, W.I. New parvovirus associated with serum hepatitis in horses after inoculation of common biological product. Emerg. Infect. Dis. 2018, 24, 303–310. [Google Scholar] [CrossRef] [PubMed]
- Ramsauer, A.S.; Badenhorst, M.; Cavalleri, J.M. Equine Parvovirus Hepatitis. Equine Vet. J. 2021, 53, 886–894. [Google Scholar] [CrossRef]
- Tomlinson, J.E.; Jager, M.; Struzyna, A.; Laverack, M.; Fortier, L.A.; Dubovi, E.; Foil, L.D.; Burbelo, P.D.; Divers, T.J.; Van de Walle, G.R. Tropism, pathology, and transmission of equine parvovirus-hepatitis. Emerg. Microbes Infect. 2020, 9, 651–663. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tomlinson, J.E.; Van de Walle, G.R.; Divers, T.J. What do we know about hepatitis viruses in horses? Vet. Clin. Equine Pract. 2019, 35, 351–362. [Google Scholar] [CrossRef]
- Yoon, J.; Park, T.; Kim, A.; Park, J.; Park, B.-J.; Ahn, H.-S.; Go, H.-J.; Kim, D.-H.; Jung, S.; Seo, Y.; et al. First Clinical Case of Equine Parvovirus-Hepatitis-Related Theiler’s Disease in Asia. Viruses 2021, 13, 1917. [Google Scholar] [CrossRef]
- Reinecke, B.; Klöhn, M.; Brüggemann, Y.; Kinast, V.; Todt, D.; Stang, A.; Badenhorst, M.; Koeppel, K.; Guthrie, A.; Groner, U. Clinical Course of Infection and Cross-Species Detection of Equine Parvovirus-Hepatitis. Viruses 2021, 13, 1454. [Google Scholar] [CrossRef]
- Badenhorst, M.; de Heus, P.; Auer, A.; Tegtmeyer, B.; Stang, A.; Dimmel, K.; Tichy, A.; Kubacki, J.; Bachofen, C.; Steinmann, E. Active equine parvovirus-hepatitis infection is most frequently detected in Austrian horses of advanced age. Equine Vet. J. 2021, in press. [Google Scholar] [CrossRef]
- Vengust, M.; Jager, M.C.; Zalig, V.; Cociancich, V.; Laverack, M.; Renshaw, R.W.; Dubovi, E.; Tomlinson, J.E.; Van de Walle, G.R.; Divers, T.J. First report of equine parvovirus-hepatitis-associated Theiler’s disease in Europe. Equine Vet. J. 2020, 52, 841–847. [Google Scholar] [CrossRef] [PubMed]
- Tomlinson, J.E.; Wolfisberg, R.; Fahnøe, U.; Sharma, H.; Renshaw, R.; Nielsen, L.; Nishiuchi, E.; Holm, C.; Dubovi, E.; Rosenberg, B.R. Equine pegiviruses cause persistent infection of bone marrow and are not associated with hepatitis. PLoS Pathog. 2020, 16, e1008677. [Google Scholar] [CrossRef] [PubMed]
- Kopper, J.; Schott, H.; Divers, T.; Mullaney, T.; Huang, L.; Noland, E.; Smedley, R. Theiler’s disease associated with administration of tetanus antitoxin contaminated with nonprimate (equine) hepacivirus and equine parvovirus-hepatitis virus. Equine Vet. Educ. 2020, 32, e5–e9. [Google Scholar] [CrossRef]
- Tomlinson, J.E.; Tennant, B.C.; Struzyna, A.; Mrad, D.; Browne, N.; Whelchel, D.; Johnson, P.J.; Jamieson, C.; Löhr, C.V.; Bildfell, R. Viral testing of 10 cases of Theiler’s disease and 37 in-contact horses in the absence of equine biologic product administration: A prospective study (2014–2018). J. Vet. Intern. Med. 2019, 33, 258–265. [Google Scholar] [CrossRef] [PubMed]
- Tomlinson, J.E.; Kapoor, A.; Kumar, A.; Tennant, B.C.; Laverack, M.A.; Beard, L.; Delph, K.; Davis, E.; Schott II, H.; Lascola, K. Viral testing of 18 consecutive cases of equine serum hepatitis: A prospective study (2014–2018). J. Vet. Intern. Med. 2019, 33, 251–257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, J.; Tong, P.; Zhang, A.; Song, X.; Zhang, L.; Shaya, N.; Kuang, L. An emerging equine parvovirus circulates in thoroughbred horses in north Xinjiang, China, 2018. Transbound Emerg. Dis. 2020, 67, 1052–1056. [Google Scholar] [CrossRef]
- Stewart, H.L.; Pitta, D.; Indugu, N.; Vecchiarelli, B.; Engiles, J.B.; Southwood, L.L. Characterization of the fecal microbiota of healthy horses. Am. J. Vet Res. 2018, 79, 811–819. [Google Scholar] [CrossRef]
- Sterky, F.; Lundeberg, J. Sequence analysis of genes and genomes. J. Biotechnol. 2000, 76, 1–31. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Altan, E.; Hui, A.; Li, Y.; Pesavento, P.; Asín, J.; Crossley, B.; Deng, X.; Uzal, F.A.; Delwart, E. New Parvoviruses and Picornavirus in Tissues and Feces of Foals with Interstitial Pneumonia. Viruses 2021, 13, 1612. [Google Scholar] [CrossRef]
- Lecollinet, S.; Pronost, S.; Coulpier, M.; Beck, C.; Gonzalez, G.; Leblond, A.; Tritz, P. Viral equine encephalitis, a growing threat to the horse population in Europe? Viruses 2020, 12, 23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, G.; Wu, L.; Ou, J.; Li, S. Equine Parvovirus-Hepatitis in China: Characterization of Its Genetic Diversity and Evidence for Natural Recombination Events Between the Chinese and American Strains. Front. Vet. Sci. 2020, 7, 121. [Google Scholar] [CrossRef]
- Meister, T.L.; Tegtmeyer, B.; Brüggemann, Y.; Sieme, H.; Feige, K.; Todt, D.; Stang, A.; Cavalleri, J.; Steinmann, E. Characterization of equine parvovirus in thoroughbred breeding horses from Germany. Viruses 2019, 11, 965. [Google Scholar] [CrossRef] [Green Version]
- Lu, G.; Sun, L.; Ou, J.; Xu, H.; Wu, L.; Li, S. Identification and genetic characterization of a novel parvovirus associated with serum hepatitis in horses in China. Emerg. Microbes Infect. 2018, 7, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Paillot, R. Special Issue “Equine Viruses”: Old “Friends” and New Foes? Viruses 2020, 12, 153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Motlou, T.P.; Williams, J.; Venter, M. Epidemiology of Shuni Virus in Horses in South Africa. Viruses 2021, 13, 937. [Google Scholar] [CrossRef]
- Carpenter, S.; Mellor, P.S.; Fall, A.G.; Garros, C.; Venter, G.J. African horse sickness virus: History, transmission, and current status. Annu. Rev. Entomol. 2017, 62, 343–358. [Google Scholar] [CrossRef] [PubMed]
- Yadav, M.P.; Singh, R.K.; Malik, Y.S. Emerging and transboundary animal viral diseases: Perspectives and preparedness. In Emerging and Transboundary Animal Viruses. Livestock Disease and Management; Springer: Singapore, 2020; Volume 1. [Google Scholar]
- Cotmore, S.F.; Agbandje-McKenna, M.; Canuti, M.; Chiorini, J.A.; Eis-Hubinger, A.-M.; Hughes, J.; Mietzsch, M.; Modha, S.; Ogliastro, M.; Pénzes, J.J. ICTV virus taxonomy profile: Parvoviridae. J. Gen. Virol. 2019, 100, 367–368. [Google Scholar] [CrossRef]
- Pénzes, J.J.; Söderlund-Venermo, M.; Canuti, M.; Eis-Hübinger, A.M.; Hughes, J.; Cotmore, S.F.; Harrach, B. Reorganizing the family Parvoviridae: A revised taxonomy independent of the canonical approach based on host association. Arch. Virol. 2020, 165, 2133–2146. [Google Scholar] [CrossRef]
Purpose | Breed | Average Age b (Range) | Country of Foaling | Prevalence | |||||
---|---|---|---|---|---|---|---|---|---|
TB | Jeju Horse | Others | Korea | U.S. | Others | ||||
EqPV-CSF a | Racing | 2/32 (6.3%) | 0/52 (0%) | 0/8 (0%) | 3.4 (0–11) | 2/91 (2.2%) | 0/1 (0%) | – | 2/92 (2.2%) |
Breeding | 2/23 (8.7%) | – | 13.2 (7–22) | 0/6 (0%) | 2/17 (11.8%) | – | 2/23 (8.7%) | ||
Riding | 0/6 (0%) | 0/1 (0%) | 1/11 (9.1%) | 8.8 (2–18) | 0/11 (0%) | 0/1 (0%) | 1/6 (16.7%) | 1/18 (5.6%) | |
Total | 4/61 (6.6%) | 0/53 (0%) | 1/19 (5.3%) | 5.8 (0–22) | 2/108 (1.9%) | 2/19 (10.5%) | 1/6 (16.7%) | 5/133 (3.8%) | |
EqCoPV a | Racing | 3/32 (9.4%) | 6/52 (11.5%) | 1/8 (12.5%) | 3.4 (0–11) | 10/91 (11.0%) | 0/1 (0%) | – | 10/92 (10.9%) |
Breeding | 2/23 (8.7%) | – | – | 13.2 (7–22) | 0/6 (0%) | 2/17 (11.8%) | – | 2/23 (8.7%) | |
Riding | 0/6 (0%) | 0/1 (0%) | 1/11 (9.1%) | 8.8 (2–18) | 0/11 (0%) | 0/1 (0%) | 1/6 (16.7%) | 1/18 (5.6%) | |
Total | 5/61 (8.2%) | 6/53 (11.3%) | 2/19 (10.5%) | 5.8 (0–22) | 10/108 (9.3%) | 2/19 (10.5%) | 1/6 (16.7%) | 13/133 (9.8%) |
ID | Country of Foaling | Age a | Breed | Purpose | Chief Complaint | EqPV-CSF | EqCoPV |
---|---|---|---|---|---|---|---|
1 | USA | 17 | Thoroughbred | Breeding | Laminitis | + | |
5 | USA | 12 | Thoroughbred | Breeding | Healthy | + | |
11 | USA | 19 | Thoroughbred | Breeding | Healthy | + | |
23 | Korea | 8 | Jeju-horse | Racing | Healthy | + | |
31 | Korea | 5 | Jeju-horse | Racing | Healthy | + | |
38 | Australia | 18 | Warm blood | Riding | Colic | + | + |
52 | Korea | 2 | Thoroughbred | Racing | Colic | + | |
58 | Korea | 6 | Jeju-horse | Racing | Healthy | + | |
62 | Korea | 7 | Jeju-horse | Racing | Healthy | + | |
75 | Korea | 0 | Thoroughbred | Racing | Colic | + | |
84 | Korea | 9 | Jeju-horse | Racing | Healthy | + | |
88 | Korea | 3 | Mixed | Racing | Healthy | + | |
97 | Korea | 9 | Jeju-horse | Racing | Cachexia | + | |
102 | Korea | 0 | Thoroughbred | Racing | Colic | + | |
109 | Korea | 0 | Thoroughbred | Racing | Colic | + | |
111 | USA | 10 | Thoroughbred | Breeding | Colic | + | |
133 | Korea | 2 | Thoroughbred | Racing | Colic | + |
Factors | p-Value | Odds Ratio | 95% Confidence Interval | ||
---|---|---|---|---|---|
Lower | Upper | ||||
EqPV-CSF | Age | 0.016 * | 1.20922 | 1.03606 | 1.4113 |
Country of foaling-Korea | 0.016 * | 0.138 | 0.0218 | 0.877 | |
Clinical disease—Colic | 0.008 * | 8.61 | 1.35 | 55.0 | |
Purpose-Racing | 0.150 | 0.281 | 0.0452 | 1.75 | |
Purpose-Breeding | 0.171 | 3.4 | 0.534 | 21.6 | |
Breed-Thoroughbred | 0.118 | 4.98 | 0.542 | 45.8 | |
EqCoPV | Age | 0.502 | 1.0383 | 0.9303 | 1.159 |
Country of foaling-Korea | 0.678 | 0.748 | 0.19 | 2.95 | |
Clinical disease-Colic | 0.025 * | 3.79 | 1.11 | 12.9 | |
Purpose-Racing | 0.524 | 1.54 | 0.402 | 5.94 | |
Purpose-Breeding | 0.848 | 0.857 | 0.177 | 4.16 | |
Breed-Thoroughbred | 0.573 | 0.714 | 0.221 | 2.31 |
EqPV-CSF (Korea) | EqPV-CSF (USA) | EqCo-PV (Korea) | EqCo-PV-11 (USA) | EqCo-PV-8 (USA) | Sesa-Virus | BPV2 | PPV4 | RDCV | PPV6 | Bosa-Virus | EqPV-H | |
---|---|---|---|---|---|---|---|---|---|---|---|---|
EqPV-CSF (Korea) | 97.9 | 56.5 | 57.1 | 58.0 | 48.0 | 50.1 | 46.5 | 46.4 | 44.9 | 48.1 | 46.8 | |
EqPV-CSF (USA) | 99.3 | 57.3 | 57.8 | 58.2 | 48.1 | 50.1 | 45.9 | 46.4 | 44.7 | 48.2 | 46.4 | |
EqCoPV (Korea) | 40.4 | 40.5 | 92.1 | 92.4 | 47.3 | 47.1 | 46.5 | 45.0 | 44.7 | 48.3 | 43.1 | |
EqCoPV-11 (USA) | 40.3 | 40.4 | 95.0 | 95.7 | 47.6 | 47.0 | 46.5 | 44.6 | 44.4 | 48.3 | 42.7 | |
EqCoPV-8 (USA) | 40.9 | 41.0 | 95.2 | 96.1 | 48.0 | 47.6 | 47.1 | 45.0 | 43.9 | 48.9 | 43.6 | |
Sesavirus | 28.1 | 28.3 | 25.1 | 25.3 | 25.6 | 45.3 | 45.1 | 42.5 | 44.6 | 45.0 | 44.5 | |
BPV2 | 29.3 | 29.2 | 27.8 | 27.5 | 27.5 | 27.5 | 49.0 | 53.0 | 45.2 | 49.7 | 46.5 | |
PPV4 | 30.4 | 30.5 | 32.1 | 31.1 | 31.3 | 28.5 | 35.6 | 48.4 | 57.7 | 47.5 | 46.9 | |
RDCV | 28.8 | 28.9 | 26.1 | 25.8 | 25.8 | 25.3 | 48.8 | 33.5 | 48.4 | 47.7 | 44.7 | |
PPV6 | 29.2 | 29.4 | 29.9 | 29.7 | 29.5 | 28.1 | 33.5 | 57.5 | 33.2 | 47.4 | 46.5 | |
Bosavirus | 25.0 | 25.2 | 28.6 | 28.9 | 29.1 | 25.4 | 31.0 | 34.6 | 32.6 | 35.4 | 46.7 | |
EqPV-H | 28.5 | 28.3 | 26.7 | 26.6 | 26.6 | 28.4 | 35.2 | 34.6 | 30.1 | 34.6 | 32.4 |
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Yoon, J.; Park, T.; Kim, A.; Song, H.; Park, B.-J.; Ahn, H.-S.; Go, H.-J.; Kim, D.-H.; Lee, J.-B.; Park, S.-Y.; et al. First Detection and Genetic Characterization of New Equine Parvovirus Species Circulating among Horses in Korea. Vet. Sci. 2021, 8, 268. https://doi.org/10.3390/vetsci8110268
Yoon J, Park T, Kim A, Song H, Park B-J, Ahn H-S, Go H-J, Kim D-H, Lee J-B, Park S-Y, et al. First Detection and Genetic Characterization of New Equine Parvovirus Species Circulating among Horses in Korea. Veterinary Sciences. 2021; 8(11):268. https://doi.org/10.3390/vetsci8110268
Chicago/Turabian StyleYoon, Jungho, Taemook Park, Ahram Kim, Heeeun Song, Byung-Joo Park, Hee-Seop Ahn, Hyeon-Jeong Go, Dong-Hwi Kim, Joong-Bok Lee, Seung-Yong Park, and et al. 2021. "First Detection and Genetic Characterization of New Equine Parvovirus Species Circulating among Horses in Korea" Veterinary Sciences 8, no. 11: 268. https://doi.org/10.3390/vetsci8110268