Elsevier

Acta Tropica

Volume 126, Issue 1, April 2013, Pages 19-27
Acta Tropica

Description and analysis of the cattle trade network in the Madagascar highlands: Potential role in the diffusion of Rift Valley fever virus

https://doi.org/10.1016/j.actatropica.2012.12.013Get rights and content

Abstract

In 2008–2009 a Rift Valley Fever (RVF) outbreak occurred in the Anjozorobe area, a temperate and mountainous area of the Madagascar highlands. The results of a serosurvey conducted in 2009 suggested recurrent circulation of RVF virus (RVFV) in this area and potential involvement of the cattle trade in RVFV circulation. The objective of this study was to describe the cattle trade network of the area and analyse the link between network structure and RVFV circulation. Five hundred and sixteen animals that tested negative in 2009 were sampled again in 2010. The 2009–2010 cattle-level seroconversion rate was estimated at 7% (95% CI: 5–10%). Trade data from 386 breeders of 48 villages were collected and analysed using social network analysis methodology, nodes being villages and ties being any movements of cattle connecting villages. The specific practice of cattle barter, known as kapsile, that involves frequent contacts between cattle of two breeders, was observed in addition to usual trade. Trade data were analysed using a logistic model, the occurrence of seroconversion at the village level being the outcome variable and the network centrality measures being the predictors. A negative association was observed between the occurrence of seroconversion in the village and introduction of cattle by trade (p = 0.03), as well as the distance to the nearest water point (p = 0.002). Conversely, the practice of kapsile, was a seroconversion risk factor (p = 0.007). The kapsile practice may be the support for inter-village RVFV circulation whereas the trade network is probably rather implicated in the introduction of RVFV to the area from other parts of Madagascar. The negative association of the distance to the nearest water point suggests that after RVFV introduction, a substantial part of transmission may be due to vectors.

Highlights

► The 2009–2010 cattle-level seroconversion rate was estimated at 7%. ► A specific practice of cattle barter, known as kapsile, was observed in addition to usual trade. ► The kapsile practice may be the support for inter-village RVFV circulation. ► The trade network is probably implicated in the introduction of RVFV to the area from other parts of Madagascar. ► Analyse suggests that after RVFV introduction, vector-based transmission may support a substantial part of the circulation.

Introduction

Rift Valley Fever (RVF) is a mosquito-borne zoonosis affecting ruminants and humans (Daubney et al., 1931). It is caused by a virus of Bunyaviridae family, Phlebovirus genus (Xu et al., 2007). The virus is transmitted from ruminants to other ruminants by mosquito bites, and although never demonstrated, by direct contact with body fluids of viremic animals. The disease in animals results in high mortality rates, especially in new-born ruminants, and abortions in pregnant females. Humans may be infected either directly after exposure to blood, tissues or body fluid from viremic animals or by mosquito-borne transmission. Infection in humans is generally associated with moderate influenza-like illness, but severe complications – encephalitis, retinitis or a hemorrhagic form – may occur in a small proportion of patients (1% for each syndrome). The hemorrhagic form leads to high mortality (rate of approximately 50%) (Gerdes, 2004, Pépin et al., 2010).

RVF disease is known to be endemic in Africa since 1912 (Peters and Linthicum, 1994). The disease spread for the first time to the Arabian Peninsula in 2000 (Ahmad, 2000). In 2006–2007, a large outbreak occurred in the Horn of Africa, first in Kenya (CDC, 2007), Tanzania and Somalia (WHO, 2007), then in Sudan (Adam et al., 2010). In May 2007, RVF was detected on the French island of Mayotte. The virus was probably introduced by the trade of live ruminants imported from eastern Africa during the 2006–2007 epidemics (Paweska et al., 2010).

In Madagascar, RVFV was first isolated in 1979 from a pool of mosquitoes trapped in the highlands, in the absence of any human or animal cases (Clerc et al., 1982, Fontenille et al., 1988, Morvan et al., 1991). During the rainy season of 1990–1991, outbreaks occurred on the highlands, in the human and animal population (Morvan et al., 1992). In 2008 a large outbreak occurred affecting most of the island's regions (Andriamandimby et al., 2010), and leading to 59 confirmed human cases. Nineteen of these cases were fatal. A study conducted on RVFV isolated during the 1979, 1990–1991 and 2008 outbreaks showed that the strains involved were genetically different (Carroll et al., 2011) and probably introduced prior to each outbreak by cattle exchanges with the African mainland (eastern/central Africa). The Anjozorobe district located in the highlands was heavily affected during the 2008 outbreak (J.M. Reynes, personal communication) (Andriamandimby et al., 2010). This region, located at an average altitude of 1000 m, is characterized by a high annual rainfall level (Goodman et al., 2007) and a temperate climate with an average annual temperature of about 18 °C (with a minimum of 9 °C in August and a maximum of 27 °C in November). Due to a rather cold temperature in winter, this area is not favourable to permanent RVFV circulation. Nevertheless, a serological study conducted on 894 cattle in 2009 showed an IgG seroprevalence rate of 28% [IC95% 25–31] and the existence of recurrent transmission of the virus. This study also suggested that (i) a substantial part of the virus transmission was probably carried out by several species of mosquito vectors, (ii) the recurrence of circulation could not be explained by the presence of wild rodents as reservoirs, but that (iii) cattle trade may contribute to the introduction and the persistence of the virus in this area (Chevalier et al., 2011).

The role of the trading network or of one of its components (e.g. market) and of movements of livestock has already been established in the spread of animal diseases (Gilbert et al., 2005, Kiss et al., 2006) and especially for RVFV (Favier et al., 2006, Swanepoel et al., 2004): from Sudan to Egypt in the 1970s (Abd El-Rahim et al., 1999), from Kenya to the Arabian Peninsula in 2000 (Shoemaker et al., 2002) and from eastern Africa to the Comoro Islands in 2008 (Sissoko et al., 2009).

The aim of this study was to describe the cattle trading network of the Anjozorobe area, analyse its structure and assess the potential role of its components in RVFV circulation.

Section snippets

Study area

The study area was the Ambongamarina commune located in the Anjozorobe district, north of the capital Antananarivo (Chevalier et al., 2011). This district includes 18 communes (which are small administrative subdivisions) including our study area. Surrounded by the rainforest, the main route joining the commune with the surrounding areas is a track that links the town of Anjozorobe (in the west) to the Alaotra Lake (in the north-east) through the rainforest (Fig. 1). The study area, containing

Results

The survey concerned 48 villages of the Ambongamarina commune. Three hundred eighty six breeders were interrogated. Only one little “market”, the market of Ambatolampy, was found inside the area (Fig. 1). The survey showed that 40% of kapsile users had exchanged cattle more than once a year (vs 22% of buyers) and 60% of kapsile users did so because the animal was too old to work efficiently (vs 78% of buyers). Seventy seven barters were reported by breeders (3 for slaughter, 27 for work,

Discussion

Serosurveys performed in 2009 and 2010 showed that, 2 years after the 2008 outbreak, RVFV was still circulating in the Anjozorobe area. Even if a global seroconversion rate of 7% was observed, no clinical cases had been reported. Intra-village seroconversion rates ranged from 0 to 20%. These values are close to the average incidence rate observed in small ruminants around ponds in Senegal during the 2003 rainy season (5.4% ranging from 0% to 20%; Chevalier et al., 2005). Similarly, and despite

Acknowledgements

We acknowledge the personnel of the Veterinary Services, breeders and the Pasteur Institute of Madagascar for their involvement and laboratory support. This study was granted by the Regional Centre of Monitoring of the Indian Ocean (CRVOI) through the project entitled “Rift Valley fever in the Indian Ocean Islands” (RIFT-OI), CIRAD and ANSES.

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