Neutralizing antibodies against Rift Valley fever virus in wild antelope in far northern KwaZulu-Natal, South Africa, indicate recent virus circulation.
Animals
Animals, Wild
/ immunology
Antelopes
/ blood
Antibodies, Neutralizing
/ blood
Antibodies, Viral
/ blood
Disease Outbreaks
/ veterinary
Female
Humans
Male
Rift Valley Fever
/ blood
Rift Valley fever virus
/ immunology
Seroepidemiologic Studies
South Africa
/ epidemiology
Zoonoses
/ epidemiology
antelope
rift valley fever virus
seroprevalence
wildlife
zoonosis
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
May 2020
May 2020
Historique:
received:
14
06
2019
revised:
03
11
2019
accepted:
09
01
2020
pubmed:
17
1
2020
medline:
21
10
2020
entrez:
17
1
2020
Statut:
ppublish
Résumé
Rift Valley fever (RVF) is a zoonotic viral disease of domestic ruminants in Africa and the Arabian Peninsula caused by a mosquito-borne Phlebovirus. Outbreaks in livestock and humans occur after heavy rains favour breeding of vectors, and the virus is thought to survive dry seasons in the eggs of floodwater-breeding aedine mosquitoes. We recently found high seroconversion rates to RVF virus (RVFV) in cattle and goats, in the absence of outbreaks, in far northern KwaZulu-Natal (KZN), South Africa. Here, we report the prevalence of, and factors associated with, neutralizing antibodies to RVFV in 326 sera collected opportunistically from nyala (Tragelaphus angasii) and impala (Aepyceros melampus) culled during 2016-2018 in two nature reserves in the same area. The overall seroprevalence of RVFV, determined using the serum neutralization test, was 35.0% (114/326; 95%CI: 29.8%-40.4%) and tended to be higher in Ndumo Game Reserve (11/20; 55.0%; 95%CI: 31.5%-76.9%) than in Tembe Elephant Park (103/306; 33.6%; 95%CI: 28.4%-39.3%) (p = .087). The presence of antibodies in juveniles (6/21; 28.6%; 95%CI: 11.3%-52.2%) and sub-adults (13/65; 20.0%; 95%CI: 11.1%-37.8%) confirmed that infections had occurred at least until 2016, well after the 2008-2011 RVF outbreaks in South Africa. Odds of seropositivity was higher in adults than in sub-adults (OR = 3.98; 95%CI: 1.83-8.67; p = .001), in males than in females (OR = 2.66; 95%CI: 1.51-4.68; p = .001) and in animals collected ≤2 km from a swamp or floodplain compared with those collected further away (OR = 3.30; 95%CI: 1.70-6.38; p < .001). Under similar ecological conditions, domestic and wild ruminants may play a similar role in maintenance of RVFV circulation and either or both may serve as the mammalian host in a vector-host reservoir system. The study confirms the recent circulation of RVFV in the tropical coastal plain of northern KZN, providing the basis for investigation of factors affecting virus circulation and the role of wildlife in RVF epidemiology.
Substances chimiques
Antibodies, Neutralizing
0
Antibodies, Viral
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1356-1363Subventions
Organisme : CDC HHS
ID : 5NU2GGH001874-02-00
Pays : United States
Organisme : CDC HHS
ID : 5NU2GGH001874-02-00
Pays : United States
Informations de copyright
© 2020 Blackwell Verlag GmbH.
Références
Adams, M. J., Lefkowitz, E. J., King, A. M., Harrach, B., Harrison, R. L., Knowles, N. J., … Mushegian, A. R. (2017). Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Archives of Virology, 162, 2505-2538. https://doi.org/10.1007/s00705-017-3358-5
Alexander, R. (1951). Rift Valley fever in the Union. Journal of the South African Veterinary Association, 22, 105-112.
Anyamba, A., Linthicum, K. J., & Tucker, C. J. (2001). Climate-disease connections: Rift Valley fever in Kenya. Cadernos De Saude Publica, 17, S133-S140. https://doi.org/10.1590/S0102-311X2001000700022
Barnard, M. (1977). An inactivated Rift Valley fever vaccine. Journal of the South African Veterinary Association, 48, 45-48.
Beechler, B. R., Bengis, R., Swanepoel, R., Paweska, J. T., Kemp, A., van Vuren, P. J., … Jolles, A. E. (2015). Rift Valley fever in Kruger National Park: Do buffalo play a role in the inter-epidemic circulation of virus? Transboundary and Emerging Diseases, 62, 24-32. https://doi.org/10.1111/tbed.12197
Bird, B. H., Githinji, J. W., Macharia, J. M., Kasiiti, J. L., Muriithi, R. M., Gacheru, S. G., … Oliver, J. B. (2008). Multiple virus lineages sharing recent common ancestry were associated with a large Rift Valley fever outbreak among livestock in Kenya during 2006-2007. Journal of Virology, 82, 11152-11166. https://doi.org/10.1128/JVI.01519-08
Britch, S. C., Binepal, Y. S., Ruder, M. G., Kariithi, H. M., Linthicum, K. J., Anyamba, A., … Oriko, A. A. (2013). Rift Valley fever risk map model and seroprevalence in selected wild ungulates and camels from Kenya. PLoS ONE, 8, e66626. https://doi.org/10.1371/journal.pone.0066626
Calverley, P. M., & Downs, C. T. (2014). Population Status of Nile Crocodiles in Ndumo Game Reserve, Kwazulu-Natal, South Africa (1971-2012). Herpetologica, 70, 417-425. https://doi.org/10.1655/HERPETOLOGICA-D-13-00090
Clements, A. N. (1999). The biology of mosquitoes. Volume 2: Sensory reception and behaviour. Wallingford: CABI Publishing.
DAFF (2011). Department of Agriculture, Forestry and Fisheries Disease Database. Retrieved from www.nda.agric.za/vetweb/epidemiology/Disease%20Database/OIEData/OIE_query_Criteria.asp.
Daubney, R., Hudson, J., & Garnham, P. (1931). Enzootic hepatitis or Rift Valley fever. An undescribed virus disease of sheep cattle and man from East Africa. The Journal of Pathology and Bacteriology, 34, 545-579.
Davies, C., Ayres, J., Dye, C., & Deane, L. (1991). Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology, 5, 655-662. https://doi.org/10.2307/2389485
Dondona, A. C., Aschenborn, O., Pinoni, C., Di Gialleonardo, L., Maseke, A., Bortone, G., … Monaco, F. (2016). Rift valley fever virus among wild ruminants, Etosha National Park, Namibia, 2011. Emerging Infectious Diseases, 22, 128. https://doi.org/10.3201/eid2201.150725
EKZN Wildlife (2015). Ezemvelo Protected Area boundary (ekznw_pabnd_2015_wdd.zip). Biodiversity Conservation Planning Division, Ezemvelo KZN Wildlife. Retrieved from www.sasdi.net/metaview.aspx?uuxml:id=78e859b1c3161984b3e02739c58b3241.
Evans, A., Gakuya, F., Paweska, J., Rostal, M., Akoolo, L., Van Vuren, P. J., … Feikin, D. (2008). Prevalence of antibodies against Rift Valley fever virus in Kenyan wildlife. Epidemiology and Infection, 136, 1261-1269. https://doi.org/10.1017/S0950268807009806
Fafetine, J., Neves, L., Thompson, P. N., Paweska, J. T., Rutten, V. P., & Coetzer, J. A. (2013). Serological evidence of Rift Valley fever virus circulation in sheep and goats in Zambezia Province, Mozambique. PLOS Neglected Tropical Diseases, 7, e2065.
Fagbo, S., Coetzer, J. A., & Venter, E. H. (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. Journal of the South African Veterinary Association, 85, 01-07.
Gear, J., De Meillon, B., Measroch, V., & Davis, D. (1951). Rift Valley fever in South Africa: 2: The occurrence of human cases in the Orange Free State, the North-Western Cape Province, the Western And Southern Transvaal: B: Field and laboratory investigations. African Journal of Health Professions Education, 25, 908-912.
Haydon, D. T., Cleaveland, S., Taylor, L. H., & Laurenson, M. K. (2002). Identifying reservoirs of infection: A conceptual and practical challenge. Emerging Infectious Diseases, 8(12), 1468-1473.
Jeanmaire, E. M., Rabenarivahiny, R., Biarmann, M., Rabibisoa, L., Ravaomanana, F., Randriamparany, T., … de La Rocque, S. (2011). Prevalence of Rift Valley fever infection in ruminants in Madagascar after the 2008 outbreak. Vector-Borne and Zoonotic Diseases, 11, 395-402. https://doi.org/10.1089/vbz.2009.0249
Jori, F., Alexander, K. A., Mokopasetso, M., Munstermann, S., Moagabo, K., & Paweska, J. T. (2015). Serological evidence of Rift Valley fever virus circulation in domestic cattle and African buffalo in Northern Botswana (2010-2011). Frontiers in Veterinary Science, 2, 63. https://doi.org/10.3389/fvets.2015.00063
Jupp, P., Kemp, A., Grobbelaar, A., Leman, P., Burt, F., Alahmed, A., … Swanepoel, R. (2002). The 2000 epidemic of Rift Valley fever in Saudi Arabia: Mosquito vector studies. Medical and Veterinary Entomology, 16, 245-252. https://doi.org/10.1046/j.1365-2915.2002.00371.x
Karber, G. (1931). 50% end point calculation. Archiv Fur Experimentelle Pathologie Und Pharmakologie, 162, 480-483.
LaBeaud, A. D., Cross, P. C., Getz, W. M., Glinka, A., & King, C. H. (2011). Rift Valley fever virus infection in African buffalo (Syncerus caffer) herds in rural South Africa: Evidence of interepidemic transmission. The American Journal of Tropical Medicine and Hygiene, 84(4), 641-646. https://doi.org/10.4269/ajtmh.2011.10-0187
Lernout, T., Cardinale, E., Jego, M., Desprès, P., Collet, L., Zumbo, B., … Filleul, L. (2013). Rift valley fever in humans and animals in Mayotte, an endemic situation? PLoS ONE, 8, e74192. https://doi.org/10.1371/journal.pone.0074192
Linthicum, K., Davies, F., Bailey, C., & Kairo, A. (1983). Mosquito species succession in a dambo in an East African forest [Kenya]. Mosquito News, 43, 464-470.
Linthicum, K., Davies, F., Kairo, A., & Bailey, C. (1985). Rift Valley fever virus (family Bunyaviridae, genus Phlebovirus). Isolations from Diptera collected during an inter-epizootic period in Kenya. Epidemiology and Infection, 95, 197-209.
Manore, C., & Beechler, B. (2015). Inter-epidemic and between-season persistence of Rift Valley fever: Vertical transmission or cryptic cycling? Transboundary and Emerging Diseases, 62, 13-23. https://doi.org/10.1111/tbed.12082
Matthews, W., Van Wyk, A., Van Rooyen, N., & Botha, G. (2001). Vegetation of the Tembe Elephant Park, Maputaland, South Africa. South African Journal of Botany, 67, 573-594. https://doi.org/10.1016/S0254-6299(15)31188-1
Metras, R., Porphyre, T., Pfeiffer, D. U., Kemp, A., Thompson, P. N., Collins, L. M., & White, R. G. (2012). Exploratory space-time analyses of Rift Valley fever in South Africa in 2008-2011. PLOS Neglected Tropical Diseases, 6, e1808. https://doi.org/10.1371/journal.pntd.0001808
Moiane, B., Mapaco, L., Thompson, P., Berg, M., Albihn, A., & Fafetine, J. (2017). High seroprevalence of Rift Valley fever phlebovirus in domestic ruminants and African Buffaloes in Mozambique shows need for intensified surveillance. Infection Ecology and Epidemiology, 7, 1416248. https://doi.org/10.1080/20008686.2017.1416248
Moll, E., & White, F. (1978). The Indian Ocean coastal belt. In M. J. A. Werger (Ed.), Biogeography and Ecology of Southern Africa (pp. 561-598). Dordrecht: Springer.
Muench, H. (1959). Catalytic Models in Epidemiology, Vol. 2. Cambridge, MA: Harvard University Press.
NFEPA. (2016). Wetland Freshwater Ecosystem Priority Areas (NFEPA_Wetlands.shp). South African National Biodiversity Institute. Retrieved from www.sasdi.net/metaview.aspx?uuxml:id=330feba934dbd53fc832cee55768e188.
OIE (2012). World Organisation for Animal Health. Rift Valley fever. In S. Edwards (Ed.), Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (7th ed., pp. 283-293). Paris: OIE.
Olive, M.-M., Goodman, S. M., & Reynes, J.-M. (2012). The role of wild mammals in the maintenance of Rift Valley fever virus. Journal of Wildlife Diseases, 48, 241-266. https://doi.org/10.7589/0090-3558-48.2.241
Paweska, J. T. (2015). Rift Valley fever. Revue Scientifique et Technique (International Office of Epizootics), 34(2), 375-389. https://doi.org/10.20506/rst.34.2.2364
Pepin, M., Bouloy, M., Bird, B. H., Kemp, A., & Paweska, J. (2010). Rift Valley fever virus (Bunyaviridae: Phlebovirus): An update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Veterinary Research, 41, 61.
Pienaar, N. J., & Thompson, P. N. (2013). Temporal and spatial history of Rift Valley fever in South Africa: 1950 to 2011. Onderstepoort Journal of Veterinary Research, 80, 1-13. https://doi.org/10.4102/ojvr.v80i1.384
Pooley, A. C. (1982). The ecology of the Nile crocodile Crocodylus niloticus in Zululand, South Africa. MSc thesis. University of Natal.
ProMED-mail. (1999). Rift Valley fever-South Africa. ProMED-mail 08 Feb 1999: 19990208.0177. Retrieved from http://www.promedmail.org.
Swanepoel, R., & Coetzer, J. (2004). Rift Valley fever. In J. A. W. Coetzer, & R. C. Tustin (Eds.), Infectious Diseases of Livestock, vol. 2 (pp. 1037-1070). Cape Town: Oxford University Press.
Van den Bergh, C., Venter, E. H., Swanepoel, R., & Thompson, P. N. (2019). High seroconversion rate to Rift Valley fever virus in cattle and goats in far northern KwaZulu-Natal, South Africa, in the absence of reported outbreaks. PLOS Neglected Tropical Diseases, 13, e0007296. https://doi.org/10.1371/journal.pntd.0007296
Verdonschot, P. F., & Besse-Lototskaya, A. A. (2014). Flight distance of mosquitoes (Culicidae): A metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica-Ecology and Management of Inland Waters, 45, 69-79. https://doi.org/10.1016/j.limno.2013.11.002
Vincent, J. (1979). The population dynamics of impala in the Mkuze Game Reserve, Zululand. PhD thesis, University of Natal.
Walsh, M. G., De Smalen, A. W., & Mor, S. M. (2017). Wetlands, wild Bovidae species richness and sheep density delineate risk of Rift Valley fever outbreaks in the African continent and Arabian Peninsula. PLOS Neglected Tropical Diseases, 11, e0005756. https://doi.org/10.1371/journal.pntd.0005756
Wilson, M. L. (1994). Rift valley fever virus ecology and the epidemiology of disease emergence. Annals of the New York Academy of Sciences, 740, 169-180. https://doi.org/10.1111/j.1749-6632.1994.tb19867.x