Rift Valley fever virus circulation in livestock and wildlife, and population dynamics of potential vectors, in northern KwaZulu-Natal, South Africa

Abstract

Rift Valley fever virus (RVFV) is a mosquito-borne virus and a member of the family Phenuiviridae and genus Phlebovirus. The single stranded RNA genome consists of three segments, Large (L), Medium (M) and Small (S). Rift Valley fever (RVF) is a mosquito-borne zoonotic disease that may cause large epidemics in ruminants and humans. Infection in humans causes influenza-like symptoms but the disease can also be more severe and fatal. Outbreaks in livestock are classified by abortion storms and young and newborn animals are severely affected with a high mortality rate. Rift Valley fever causes severe health and economic consequences in the areas where it occurs. Since the first recorded incidence of RVF in Kenya in 1930, South Africa has had three major countrywide outbreaks: in 1950-1951, 1973-1975 and 2008-2011. The disease is characterized in southern Africa by large epidemics at long, irregular intervals. The epidemics are usually associated with conditions favourable for proliferation of mosquito populations, such as high rainfall and flooding. Rift Valley fever has previously been isolated from 12 different mosquito species in South Africa including 5 Aedes spp., 3 Culex spp., 3 Anopheles spp. and 1 Eretmapodites sp. The presence of the virus and patterns of occurrence of the disease in the eastern parts of South Africa are poorly understood. Multiple studies were conducted; the aim of the first study was to detect the presence of RVFV in far northern KwaZulu-Natal Province, South Africa and to estimate the incidence rate of seroconversion. Cross-sectional studies were performed in communally farmed cattle (n=423) and goats (n=104), followed by longitudinal follow-up of seronegative livestock (n=253) 14 times over 24 months, representing 160.3 animal-years at risk. Exposure to RVFV was assessed using an IgG sandwich ELISA and a serum neutralization test (SNT) and seroconversion was assessed using SNT. Initial overall seroprevalence was 34.0% (95%CI: 29.5-38.8%) in cattle and 31.7% (95%CI: 22.9-41.6%) in goats, varying by locality from 18-54%. Overall seroconversion rate in cattle was 0.59 per animal-year (95% CI: 0.46-0.75) and in goats 0.41 per animal-year (95% CI: 0.25-0.64), varying significantly over short distances. The high seroprevalence in all age groups and evidence of year-round viral circulation provide evidence for a hyperendemic situation in the study area. The second study investigated the seroprevalence and associated risk factors of RVFV in antelope in the Tembe Elephant Park (TEP) and the Ndumo Game Reserve (NGR), using 326 sera from nyala (Tragelaphus angasii) and impala (Aepyceros melampus) routinely culled over a two-year period. The overall seroprevalence of RVFV was 35.0% (114/326; 95% CI 29.8-40.4%); 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 subsequent to the 2008-2011 RVF outbreaks in South Africa. Seroprevalence was highest in adults and inversely associated with distance from a swamp or floodplain. The third study aimed to investigate the diversity, abundance, and seasonal dynamics of mosquitoes in the study area, and to screen mosquitoes for RVFV. Monthly collections of adult mosquitoes were carried out from January 2017 to June 2018 at three sites using CO2-baited tent traps. Mosquitoes were identified, pooled and screened for RVFV by quantitative reverse transcriptase (RT)-polymerase chain reaction (PCR) directed toward amplification of a 217-bp fragment of the L segment. A total of 34,848 mosquitoes of 7 genera and 48 species, were captured; Culex (Cux.) tritaeniorhynchus (31%), Cx. (Cux.) antennatus (29%), Aedes (Adm.) durbanensis (12%) and Cx. (Cux.) neavei (10%) were the most abundant species collected. Genera differences were noted between the collection sites. Cumulative rainfall and average minimum temperatures 30 days prior to collection were positively associated with the number of mosquitoes collected while maximum temperatures were only associated with the number of Culex mosquitoes caught. A single pool of Ae. durbanensis was found to be positive for RVFV genomic RNA. The same pool was also positive for Chikungunya virus (Family Togaviridae, genus Alphavirus) (CHIKV) and Sindbis virus (Family Togaviridae, genus Alphavirus) (SINV). The RVFV isolate was closely related to one obtained from Ae. (Neo.) circumluteolus at Simbu pan in 1955, ±20 km from the collection sites for this study. Further investigation should be done on the human health implications of the presence of these three zoonotic arboviruses. It is possible that these viruses are causing disease among the communities in the area and that the diseases are under-reported. The results of this study show that RVFV is circulating in the area in domestic ruminants and wildlife, in the absence of apparent clinical disease, at a rate that varies by location, season and year. It appears that, under similar ecological conditions, domestic and wild ruminants may play a similar role in maintenance of viral circulation, and either or both may serve as the mammalian host in a vector-host maintenance system. The study also demonstrates the presence of a wide variety of mosquito species, several of which are known to be competent RVFV vectors.