Assessing the potential of plains zebra to maintain African horse sickness in the Western Cape Province, South Africa


Autoři: Thibaud Porphyre aff001;  John D. Grewar aff002
Působiště autorů: The Roslin Institute, University of Edinburgh, Edinburgh, Scotland, United Kingdom aff001;  South African Equine Health & Protocols NPC, Paardevlei, Cape Town, South Africa aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222366

Souhrn

African horse sickness (AHS) is a disease of equids that results in a non-tariff barrier to the trade of live equids from affected countries. AHS is endemic in South Africa except for a controlled area in the Western Cape Province (WCP) where sporadic outbreaks have occurred in the past 2 decades. There is potential that the presence of zebra populations, thought to be the natural reservoir hosts for AHS, in the WCP could maintain AHS virus circulation in the area and act as a year-round source of infection for horses. However, it remains unclear whether the epidemiology or the ecological conditions present in the WCP would enable persistent circulation of AHS in the local zebra populations. Here we developed a hybrid deterministic-stochastic vector-host compartmental model of AHS transmission in plains zebra (Equus quagga), where host populations are age- and sex-structured and for which population and AHS transmission dynamics are modulated by rainfall and temperature conditions. Using this model, we showed that populations of plains zebra present in the WCP are not sufficiently large for AHS introduction events to become endemic and that coastal populations of zebra need to be >2500 individuals for AHS to persist >2 years, even if zebras are infectious for more than 50 days. AHS cannot become endemic in the coastal population of the WCP unless the zebra population involves at least 50,000 individuals. Finally, inland populations of plains zebra in the WCP may represent a risk for AHS to persist but would require populations of at least 500 zebras or show unrealistic duration of infectiousness for AHS introduction events to become endemic. Our results provide evidence that the risk of AHS persistence from a single introduction event in a given plains zebra population in the WCP is extremely low and it is unlikely to represent a long-term source of infection for local horses.

Klíčová slova:

Death rates – Epidemiology – Horses – Population density – Population size – South Africa – Vector-borne diseases – Zebras


Zdroje

1. Zientara S, Weyer CT, Lecollinet S. African horse sickness. Rev. Sci. Tech. Off. Int. Epiz. 2015; 34(2): 315–327. doi: 10.20506/rst.34.2.2359

2. Sergeant ES, Grewar JD, Weyer CT, Guthrie AJ. Quantitative risk assessment for African horse sickness in live horses exported from South Africa. PLoS ONE 2016; 11(3): e0151757. doi: 10.1371/journal.pone.0151757 26986002

3. Grewar JD. The economic impact of bluetongue and other orbiviruses in sub-Saharan Africa, with special reference to Southern Africa. Vet Ital. 2016; 52(3–4): 375–381. doi: 10.12834/VetIt.503.2427.3 27723050

4. Bosman P, Brückner GK, Faul A. African horse sickness surveillance systems and regionalisation/zoning: the case of South Africa. Rev. Sci. Tech. Off. Int. Epiz. 1995; 14(3): 645–653. doi: 10.20506/rst.14.3.866

5. Barnard BJ. Circulation of African horse sickness virus in zebra (Equus burchelli) in the Kruger National Park, South Africa, as measured by the prevalence of type specific antibodies. Onderstepoort J Vet Res 1993; 60: 111–117. 8332321

6. Barnard BJ. Epidemiology of African horse sickness and the role of the zebra in South Africa. Arch Virol Suppl. 1998; 14: 13–19. 9785491

7. Weyer CT, Grewar JD, Burger P, Russouw E, Lourens CW, Joone C et al. African horse sickness caused by genome reassortment and reversion to virulence of live, attenuated vaccine viruses, South Africa, 2004–2014. Emerg Infect Dis. 2016; 22(12): 2087–2096. doi: 10.3201/eid2212.160718 27442883

8. MacLachlan NJ, Guthrie AJ. Re-emergence of bluetongue, African horse sickness, and other Orbivirus diseases. Vet Res. 2010; 41(6): 35. doi: 10.1051/vetres/2010007 20167199

9. Mellor PS, Leake CJ. Climatic and geographic influences on arboviral infections and vectors. Rev. Sci. Tech. Off. Int. Epiz. 2000; 19(1): 41–54. doi: 10.20506/rst.19.1.1211

10. Tarlinton R, Daly J, Dunham S, Kydd J. The challenge of Schmallenberg virus emergence in Europe. Vet. J. 2012; 194(1): 10–18. doi: 10.1016/j.tvjl.2012.08.017 23026716

11. Coetzer J, Guthrie AJ. African horse sickness. In: Coetzer JAW, Tustin RC, editors. Infectious diseases of livestock (2nd Edition). Cape Town: Oxford University Press Southern Africa; 2004, pp. 1231–1246.

12. Backer JA, Nodelijk G. Transmission and control of African horse sickness in The Netherlands: A model analysis. PLoS One 2011, 6: e23066. doi: 10.1371/journal.pone.0023066 21850252

13. Bessell PR, Searle KR, Auty HK, Handel IG, Purse BV, et al. Epidemic potential of an emerging vector borne disease in a marginal environment: Schmallenberg in Scotland. Sci. Rep. 2013, 3: 1178.

14. Græsbøll K, Bødker R, Enøe C, Christiansen LE. Simulating spread of bluetongue virus by flying vectors between hosts on pasture. Sci. Rep. 2012, 2: 863. doi: 10.1038/srep00863 23162689

15. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018.

16. Georgiadis N, Hack M, Turpin K. The influence of rainfall on zebra population dynamics: implications for management. J Appl Ecol. 2003; 40: 125–136. doi: 10.1046/j.1365-2664.2003.00796.x

17. Smuts GL. Population characteristics of Burchell’s Zebra (Equus burchelli antiquorum, H. Smith, 1841) in the Kruger National Park. Afr J Wildl Res 1976; 6: 99–112.

18. Barnard BJ, Bengis R, Keet D, Dekker EH. Epidemiology of African horse sickness: duration of viraemia in zebra (Equus burchelli). Onderstepoort J Vet Res 1994; 61: 391–393. 7501371

19. Venter GJ, Nevill EM, Van Der Linde TC. Seasonal abundance and parity of stock-associated Culicoides species (Diptera: Ceratopogonidae) in different climatic regions in southern Africa in relation to their viral vector potential. Onderstepoort J Vet Res 1997; 64: 259–271. 9551477

20. Scanlen M, Paweska JT, Verschoor JA, van Dijk AA. The protective efficacy of a recombinant VP2-based African horse sickness subunit vaccine candidate is determined by adjuvant. Vaccine 2002; 20: 1079–1088. doi: 10.1016/s0264-410x(01)00445-5 11803068

21. Roy P, Bishop DHL, Howard S, Aitchison H, Erasmus B. Recombinant baculovirus-synthesized African horse sickness virus (AHSV) outer-capsid protein VP2 provides protection against virulent AHSV challenge. J Gen Virol 1996; 77: 2053–2057. doi: 10.1099/0022-1317-77-9-2053 8811002

22. House JA, Lombard M, Dubourget P, House C, Mebus CA. Further studies on the efficacy of an inactivated African horse sickness serotype 4 vaccine. Vaccine 1994; 12: 142–144. doi: 10.1016/0264-410x(94)90052-3 8147096

23. Meiswinkel R, Venter GJ, Nevill EM. Vectors: Culicoides spp. In: Coetzer JAW, Tustin RC, editors. Infectious diseases of livestock (2nd Edition). Cape Town: Oxford University Press Southern Africa; 2004, pp. 93–136.

24. Wickham H. rvest: Easily Harvest (Scrape) Web Pages. R package version 0.3.4; 2019. https://CRAN.R-project.org/package=rvest

25. Venter GJ, Boikanyo SNB, de Beer CJ. The influence of temperature and humidity on the flight activity of Culicoides imicola both under laboratory and field conditions. Parasites & Vectors 2019; 12: 4. doi: 10.1186/s13071-018-3272-z

26. King SRB, Moehlman PD. Equus quagga. The IUCN Red List of Threatened Species 2016; e.T41013A45172424. http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T41013A45172424.en

27. Grewar J. AHS vaccination policy in the controlled area. Western Cape Department of Agriculture: Epidemiology Report 2015; 7(3): 1–2. Available from: http://www.elsenburg.com/vetepi/epireport_pdf/March2015.pdf

28. Guichard S, Guis H, Tran A, Garros C, Balenghien T, et al. Worldwide niche and future potential distribution of Culicoides imicola, a major vector of bluetongue and African horse sickness viruses. PLoS ONE 2014; 9(11): e112491. doi: 10.1371/journal.pone.0112491 25391148

29. Meiswinkel R. The 1996 outbreak of African horse sickness in South Africa—The entomological perspective. Arch. Virol. 1998; 14: 63–77.

30. Venter EH, Steyn J, Coetzee P, van Vuuren M, Crafford J, et al. The prevalence of Culicoides spp. in 3 geographic areas of South Africa. Vet Ital. 2016; 52(3–4): 281–289. 27723037

31. Liebenberg D, Piketh S, Labuschagne K, Venter G, Greyling T, et al. Culicoides species composition and environmental factors influencing African horse sickness distribution at three sites in Namibia. Acta Trop. 2016; 163: 70–79. doi: 10.1016/j.actatropica.2016.07.024 27491343

32. Siebert S, Doll P, Hoogeveen J, Faures J-M, Frenken K, et al. Development and validation of the global map of irrigation areas. Hydrol Earth Syst Sci 2005; 9: 535–547. doi: 10.5194/hess-9-535-2005

33. Baylis M, Meiswinkel R, Venter GJ. A preliminary attempt to use climate data and satellite imagery to model the abundance and distribution of Culicoides imicola (Diptera: Ceratopogonidae) in southern Africa. J S Afr Vet Assoc 1999; 70(2): 80–89. doi: 10.4102/jsava.v70i2.759 10855827

34. Diarra M, Fall M, Gueye Fall A, Diop A, Lancelot R, Seck MT et al. Spatial distribution modelling of Culicoides (Diptera: Ceratopogonidae) biting midges, potential vectors of African horse sickness and bluetongue viruses in Senegal. Parasites & Vectors 2018; 11: 341. doi: 10.1186/s13071-018-2920-7

35. Hrabar H, Kerley GIH. Conservation goals for the Cape mountain zebra Equus zebra zebra—security in numbers? Oryx 2013; 47(3): 403–409. doi: 10.1017/S0030605311002018

36. Georgiadis NJ, Ojwang’ G, Olwero N, Aike G. Reassessing aerial sample surveys for wildlife monitoring, conservation, and management. Smithson. Contrib. Zool. 2011; 632: 31–42. doi: 10.5479/si.00810282.632.31

37. Lord CC, Woolhouse ME, Barnard BJ. Transmission and distribution of virus serotypes: African horse sickness in zebra. Epidemiol Infect 1997; 118: 43–50. doi: 10.1017/s0950268896006929 9042034

38. Bessell PR, Auty HK, Searle KR, Handel IG, Purse BV, et al. Impact of temperature, feeding preference and vaccination on Schmallenberg virus transmission in Scotland. Sci. Rep. 2014; 4: 5746. doi: 10.1038/srep05746 25034464

39. Gubbins S, Carpenter S, Baylis M, Wood JLN, Mellor PS. Assessing the risk of bluetongue to UK livestock: Uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number. J R Soc Interface 2008; 5(20): 363–371. doi: 10.1098/rsif.2007.1110 17638649

40. Lord CC, Woolhouse MEJ, Heesterbeek JAP, Mellor PS. Vector-borne diseases and the basic reproduction number: A case study of African horse sickness. Med. Vet. Entomol. 1996; 10: 19–28. doi: 10.1111/j.1365-2915.1996.tb00077.x 8834738

41. Lo Iacono G, Robin CA, Newton JR, Gubbins S, Wood JLN. Where are the horses? With the sheep or cows? Uncertain host location, vector-feeding preferences and the risk of African horse sickness transmission in Great Britain. J R Soc Interface 2013; 10: 20130194. doi: 10.1098/rsif.2013.0194 23594817

42. Meiswinkel R, Paweska JT. Evidence for a new field Culicoides vector of African horse sickness in South Africa. Prev Vet Med. 2003; 60(3): 243–53. doi: 10.1016/S0167-5877(02)00231-3 12900162

43. . Virus recovery rates for wildtype and live-attenuated vaccine strains of African horse sickness virus serotype 7 in orally infected South African Culicoides species. Med Vet Entomol 2007; 21: 377–383. doi: 10.1111/j.1365-2915.2007.00706.x 18092976

44. Venter GJ. Culicoides (Diptera: Ceratopogonidae) as vectors of African horse sickness virus in South Africa. In: Abstracts of the XXV International Congress of Entomology, 25–30 September 2016, Orlando, USA.

45. Mellor PS, Boorman J, Baylis M. Culicoides biting midges: their role as arbovirus vectors. Annu. Rev. Entomol. 2000; 45: 307–340. doi: 10.1146/annurev.ento.45.1.307 10761580

46. Riddin MA, Venter GJ, Labuschagne K, Villet MH. Culicoides species as potential vectors of African horse sickness virus in the southern regions of South Africa. Med Vet Entomol 2019. doi: 10.1111/mve.12391

47. Meiswinkel R, Labuschagne K, Baylis M, Mellor PS. Multiple vectors and their differing ecologies: observations on two bluetongue and African horse sickness vector Culicoides species in South Africa. Vet Ital. 2004; 40: 296–302. 20419682

48. Venter GJ, Koekemoer JJO, Paweska JT. Investigations on outbreaks of African horse sickness in the surveillance zone in South Africa. Rev. sci. tech. Off. int. Epiz. 2006; 25: 1097–1109. doi: 10.20506/rst.25.3.1719

49. Turner J, Bowers RG, Baylis M. Two-host, two-vector basic reproduction ratio (R0) for blue-tongue. PLoS ONE 8(1): e53128. doi: 10.1371/journal.pone.0053128 23308149


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