An Unexpected Recurrent Transmission of Rift Valley Fever Virus in Cattle in a Temperate and Mountainous Area of Madagascar

Abstract

Rift Valley fever is an acute, zoonotic viral disease of domestic ruminants, caused by a phlebovirus (Bunyaviridae family). A large outbreak occurred in Madagascar in 2008–2009. The goal of the present study was to evaluate the point prevalence of antibodies against Rift Valley Fever Virus (RVFV) in cattle in the Anjozorobe district, located in the wet and temperate highland region of Madagascar and yet heavily affected by the disease, and analyse environmental and trade factors potentially linked to RVFV transmission. A serological study was performed in 2009 in 894 bovines. For each bovine, the following variables were recorded: age, location of the night pen, minimum distance from the pen to the nearest water point and the forest, nearest water point type, and herd replacement practices. The serological data were analyzed using a generalized linear mixed model. The overall anti-RVFV IgG seroprevalence rate was 28% [CI95% 25–31]. Age was statistically linked to prevalence (p = 10 ⁻⁴), being consistent with a recurrent RVFV circulation. Distance from the night pen to the nearest water point was a protective factor (p = 5.10 ⁻³), which would be compatible with a substantial part of the virus transmission being carried out by nocturnal mosquito vectors. However, water point type did not influence the risk of infection: several mosquito species are probably involved. Cattle belonging to owners who purchase animals to renew the herd were significantly more likely to have seroconverted than others (p = 0.04): cattle trade may contribute to the introduction of the virus in this area. The minimum distance of the night pen to the forest was not linked to the prevalence. This is the first evidence of a recurrent transmission of RVFV in such an ecosystem that associates a wet, temperate climate, high altitude, paddy fields, and vicinity to a dense rain forest. Persistence mechanisms need to be further investigated.

Author Summary

Rift Valley fever (RVF) is a viral disease of domestic ruminants, which may affect humans. The RVF virus (RVFV) may be transmitted either by mosquitoes or through direct contact with vireamic body fluids or products. Until now, this disease had been described in arid, hot and irrigated or tropical areas. Performed in the year following the 2008–2009 RVFV outbreak in Madagascar, this study demonstrates for the first time a regular and intense transmission of this disease in a temperate and mountainous region.The area chosen as a pilot project shows that cattle are regularly and heavily affected in the highlands of Madagascar. Statistical analyses suggest that (i) a substantial part of the transmission is due to mosquito vectors; (ii) many mosquito species such as Culex and Anopheles, are probably involved in the transmission; (iii) cattle trade, by a regular introduction of the virus via herds coming from infected areas of the island, may explain the recurrence of the disease in this region. Further investigations are needed to understand the mechanisms of transmission of the disease, and design and implement appropriate surveillance and control measures in this area.