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Drivers of Rift Valley Fever Epidemics in Madagascar

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Drivers of Rift Valley Fever Epidemics in Madagascar Drivers of Rift Valley fever epidemics in Madagascar Renaud Lancelota,b,1, Marina Beral´ b,c,d, Vincent Michel Rakotoharinomee, Soa-Fy Andriamandimbyf, Jean-Michel Heraud´ f, Caroline Costea,b, Andrea Apollonia,b,Cecile´ Squarzoni-Diawg, Stephane´ de La Rocquea,b,h,i, Pierre B. H. Formentyj,Jer´ emy´ Bouyera,b, G. R. William Wintk, and Eric Cardinaleb,c,d aFrench Agricultural Research and International Cooperation Organization for Development (Cirad), Department of Biological Systems (Bios), UMR Animals, Health, Territories, Risks, and Ecosystems (Astre), Campus International de Baillarguet, 34398 Montpellier, France; bFrench National Agricultural Research Center for International Development, Animal Health Department, UMR Astre, Campus International de Baillarguet, 34398 Montpellier, France; cCirad, Bios Department, UMR Astre, 97490 Sainte Clotilde, La Reunion,´ France; dCentre de Recherche et de Veille sur les Maladies Emergentes´ de l’Ocean´ Indien, 97490 Sainte Clotilde, La Reunion,´ France; eMinistere` de l’Agriculture, de l’Elevage et de la Peche,ˆ Direction des Services Vet´ erinaires,´ Ambatofotsikely, BP 530 Antananarivo 101, Madagascar; fUnite´ de Virologie, Institut Pasteur de Madagascar, BP 1274 Antananarivo 101, Madagascar; gAnimal Production and Health Division, Food and Agriculture Organization of the United Nations, 00153 Rome, Italy; hWorld Organization for Animal Health, 75017 Paris, France; iInternational Health Regulations Monitoring Procedure and Information Team, Global Capacity and Response Department, World Health Organization (WHO), 1211 Geneva 27, Switzerland; jEmerging and Epidemic Zoonotic Diseases, Pandemic and Epidemic Disease Department, WHO, Geneva 27, Switzerland; and kDepartment of Zoology, Environmental Research Group Oxford, Oxford OX1 3PS, United Kingdom Edited by Burton H. Singer, University of Florida, Gainesville, FL, and approved December 8, 2016 (received for review May 18, 2016) Rift Valley fever (RVF) is a vector-borne viral disease widespread the slaughtering of viremic animals (11): Blood aerosol produced in Africa. The primary cycle involves mosquitoes and wild and on this occasion is highly infectious (12). The virus is not trans- domestic ruminant hosts. Humans are usually contaminated after mitted from person to person. contact with infected ruminants. As many environmental, agricul- In Madagascar, the first known RVF epidemic occurred in tural, epidemiological, and anthropogenic factors are implicated 1990–1991 on the East Coast and in the central highlands (7). in RVF spread, the multidisciplinary One Health approach was A second epidemic occurred in 2008–2009 with official reports needed to identify the drivers of RVF epidemics in Madagascar. suggesting at least 700 suspected cases and 26 RVFV laboratory- We examined the environmental patterns associated with these confirmed fatalities. However, due to underreporting, an excess epidemics, comparing human and ruminant serological data with of 10,000 human cases was estimated (13–15). environmental and cattle-trade data. In contrast to East Africa, Madagascar is one of the poorest countries in the World, with SCIENCES environmental drivers did not trigger the epidemics: They only 90% of the population living with less than USD 1.5 inhab.−1·d−1 APPLIED BIOLOGICAL modulated local Rift Valley fever virus (RVFV) transmission in (16). Because public health resources are limited in such a set- ruminants. Instead, RVFV was introduced through ruminant trade ting, it is crucial to identify the most exposed populations, based and subsequent movement of cattle between trade hubs caused on scientific evidence. To this end, we aimed at understanding its long-distance spread within the country. Contact with cat- the circumstances in which RVF epidemics occurred. We first tle brought in from infected districts was associated with higher assessed the risk of RVFV introduction to ruminants via live- infection risk in slaughterhouse workers. The finding that anthro- stock trade. Then, we described the environmental conditions pogenic rather than environmental factors are the main drivers of associated with the start of the 1990 and 2008 epidemics and with RVF infection in humans can be used to design better prevention local RVFV transmission. We then aimed to build risk indexes and early detection in the case of RVF resurgence in the region. of RVFV human infection related to the local environment (local risk) and cattle trade (remote risk), assess their relative vector-borne infection j zoonosis j El Nino˜ j cattle trade j One Health Significance ift Valley fever (RVF) is a vector-borne infection caused by Rift Valley fever (RVF) is an emerging, mosquito-borne viral the RVF virus (RVFV). Mosquito species from the Aedes, R infection of ruminants, transmissible to people, and linked Culex, and Mansonia genera are the main RVFV vectors (1). The to rainfall. By investigating a wider range of possible drivers virus persists in the environment either by vertical transmission this study confirms the assumption that RVF occurrence can occurring in some Aedes species or by an enzootic cycle involv- also be dependent on nonenvironmental drivers. In Mada- ing ruminants and mosquitoes. When environmental conditions gascar, human and ruminant infections were geographically are favorable to mosquito proliferation, this cycle is amplified by distinct, with introduction and long-distance disease spread Culex populations, leading to RVF epidemics (2). In the Horn linked to livestock trading. Human infections were highest in of Africa, these circumstances are met during the warm phases those involved with slaughtering and handling fresh meat. of El Nino˜ southern oscillation (ENSO) and the Indian Ocean The identification of possible introduction routes, major cat- dipole zonal mode: Warm sea-surface temperatures in the equa- tle trade hubs, and areas of high risk to ruminants has shown torial eastern-central Pacific Ocean and the western equatorial how multidisciplinary analyses are needed to properly under- Indian Ocean result in heavy autumn rainfall and subsequent stand disease dynamics and spread, thereby improving early greening of the vegetation (3–5). The latter can be monitored detection and prevention of RVF in humans. by the remotely sensed normalized difference vegetation index (NDVI). Besides these environmental conditions triggering epi- Author contributions: R.L., V.M.R., S.-F.A., J.M.-H., C.S.-D., S.d.l.R., P.B.H.F., G.R.W.W., demics, long-distance RVFV dissemination is often related to and E.C. designed research; R.L., M.B., V.M.R., S.-F.A., J.M.-H., C.C., A.A., C.S.-D., S.d.l.R., ruminant trade (6), as reported in Madagascar and Saudi Ara- P.B.H.F., and E.C. performed research; R.L., M.B., C.C., A.A., and G.R.W.W. analyzed data; bia (7–9). and R.L., M.B., V.M.R., S.-F.A., J.M.-H., C.C., A.A., C.S.-D., S.d.l.R., P.B.H.F., J.B., G.R.W.W., In domestic ruminants, the RVFV causes mass abortions and and E.C. wrote the paper. high neonatal mortality (10). Humans may get infected after the The authors declare no conflict of interest. bites of infected mosquitoes or the consumption of raw milk. This article is a PNAS Direct Submission. However, most clinical cases occur after contact with blood, Freely available online through the PNAS open access option. aborted fetuses, and placenta of viremic animals. Farmers, vet- 1To whom correspondence should be addressed. Email: [email protected]. erinarians, slaughterhouse workers, and butchers are thus the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. most exposed to the risk of RVF, as well as any people attending 1073/pnas.1607948114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1607948114 PNAS Early Edition j 1 of 6 importance, identify and map high-risk areas, and assess the con- A sequences for human health. 2 0 Results SOI Risk of Virus Introduction by Livestock Trade. Queries in the United −2 SOI (std dev.) Nations (UN) ComTrade database did not reveal direct impor- Mar 1990 Jan 2008 tations of live ruminants from mainland Africa to Madagascar. B However, they highlighted several official importations from the 2 Union of Comoros in 2005–2007 (Table 1). Although the num- 0 bers are small, they confirmed the risk of RVFV introduction in −2 Moist forest Mar 1990 Jan 2008 Madagascar from an infected country, via livestock trade. 2 In addition to this official trade, illegal cattle movements 0 between the Comoros Archipelago and Madagascar were proba- Dry forest Mar 1990 Jan 2008 bly much more frequent. Informal surveys conducted in 2009 and −2 Rainfall (std dev.) 2010 in the main Comoros harbors and in the northwest of Mada- 2 gascar (Mahajanga and Antsiranana) revealed the frequent pres- 0 ence of cattle and small ruminants on board freighters and −2 Xeric shrub. Mar 1990 Jan 2008 botry (dhows) traveling from the Comoros Islands to Madagas- C Mar 1990 Jan 2008 car and from port to port. This coastal navigation is widespread 0 in Madagascar, given the weakness of the terrestrial-road net- work (Fig. S1). Therefore, RVFV could have been introduced −2 Moist forest to Madagascar through ruminant trade from Comoros Islands— Mar 1990 Jan 2008 which were previously infected (17, 18)—and further dissemi- 0 nated through coastal navigation between Malagasy sea ports. −2 Dry forest NDVI (std dev.) Environmental Conditions and RVFV Epidemics. Mar 1990 Jan 2008 Triggering RVF epidemics. Conditions at the start of the two RVF 0 epidemics in humans (March 1990 and January 2008) are shown on Fig. 1. For the three indicators [southern oscillation index −2 Xeric shrub. (SOI), rainfall, and NDVI] and three biomes (Fig. S2A), the two 1985 1990 1995 2000 2005 2010 epidemics did not occur in typical RVF conditions according to Fig. 1. Environmental conditions (monthly average) in the main Mala- the eastern African standards (14). In March 1990, a marked gasy biomes with respect to the 1990–1991 and 2008–2009 RVF epidemics.
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