Downloaded by guest on September 27, 2021 otepsdt h iko V,a ela n epeattending people any as well the as RVF, thus of are risk the blood, butchers to vet- exposed and with Farmers, most animals. workers, contact viremic milk. slaughterhouse after of raw erinarians, placenta occur of and cases fetuses, consumption aborted clinical the or most mosquitoes the However, after infected infected get of may bites Humans (10). mortality neonatal high Ara- Saudi and to in reported (7–9). related bia as often (6), is trade dissemination ruminant RVFV epi- long-distance triggering index monitored conditions demics, vegetation environmental be difference these can normalized Besides latter subsequent (NDVI). sensed The and remotely (3–5). the rainfall vegetation by autumn the heavy of equatorial in greening western result the Ocean and Indian Ocean equa- Pacific the in eastern-central temperatures torial sea-surface Warm phases mode: warm zonal the dipole during Ni met El are of circumstances these Africa, of by amplified is cycle this Culex proliferation, mosquito conditions to environmental favorable When are mosquitoes. and ruminants transmission ing vertical by some either in environment occurring the in persists virus and Culex, R infection vector-borne region. the in resurgence RVF prevention of better case design the to in used detection early be and can of humans drivers in main infection the RVF are factors anthro- environmental that higher than cat- finding rather with The pogenic with associated workers. slaughterhouse was Contact in districts risk country. infected infection from the in brought within caused tle hubs spread trade long-distance in between cattle its transmission of (RVFV) movement trade subsequent ruminant virus through and introduced only fever was RVFV They Valley Instead, epidemics: ruminants. Rift Africa, the East local trigger to not modulated contrast did In drivers data. environmental cattle-trade with data and serological these environmental ruminant Madagascar. with and in human associated epidemics comparing was patterns epidemics, RVF environmental approach of the Health drivers examined We One the identify multidisciplinary to the needed implicated spread, are RVF factors in anthropogenic and agricul- and epidemiological, environmental, many tural, wild As ruminants. and after infected contaminated mosquitoes with usually contact are involves Humans cycle hosts. widespread 2016) ruminant primary disease 18, domestic May viral The review vector-borne for Africa. a (received 2016 is in 8, (RVF) December fever approved and Valley FL, Rift Gainesville, Florida, of University Singer, H. Burton by Edited and Switzerland; Switzerland; 27, 27, Geneva Geneva WHO, 1211 (WHO), Organization Health World France; Paris, 75017 Health, g Formenty H. B. Pierre www.pnas.org/cgi/doi/10.1073/pnas.1607948114 Madagascar; 101, France; Montpellier, 530 34398 R BP Baillarguet, Ambatofotsikely, La de Clotilde, International Sainte Campus 97490 Astre, France; Indien, UMR Montpellier, Department, 34398 Health Baillarguet, Animal de Development, International International c Campus for (Astre), Center Ecosystems Research and Risks, Territories, Health, Animals, a Madagascar H in Jean-Michel epidemics Lancelot fever Renaud Valley Rift of Drivers ia,Bo eatet M sr,940Sit ltle aR La Clotilde, Sainte 97490 Astre, UMR Department, Bios Cirad, rnhArclua eerhadItrainlCoeainOgnzto o eeomn Crd,Dprmn fBooia ytm Bo) UMR (Bios), Systems Biological of Department (Cirad), Development for Organization Cooperation International and Research Agricultural French nmlPouto n elhDvso,Fo n giutr raiaino h ntdNtos 05 oe Italy; Rome, 00153 Nations, United the of Organization Agriculture and Food Division, Health and Production Animal ndmsi uiat,teRF assms brin and abortions mass causes RVFV the ruminants, domestic In h V iu RF) oqioseisfo the from species by Mosquito caused (RVFV). infection virus vector-borne RVF a is the (RVF) fever Valley ift ouain,laigt V pdmc 2.I h Horn the In (2). epidemics RVF to leading populations, osuhr silto ES)adteIda Ocean Indian the and (ENSO) oscillation southern no ˜ Mansonia eraud ´ a,b,1 Aedes | zoonosis eeaaetemi VVvcos() The (1). vectors RVFV main the are genera f aiaB Marina , aoieCoste Caroline , i j nentoa elhRgltosMntrn rcdr n nomto em lblCpct n epneDepartment, Response and Capacity Global Team, Information and Procedure Monitoring Regulations Health International J , pce rb nezoi yl involv- cycle enzootic an by or species er ´ | uin France; eunion, m Bouyer emy ´ ´ lNi El k eateto olg,EvrnetlRsac ru xod xodO13S ntdKingdom United 3PS, OX1 Oxford Oxford, Group Research Environmental Zoology, of Department eral ´ no ˜ | b,c,d atetrade cattle a,b icn ihlRakotoharinome Michel Vincent , nraApolloni Andrea , a,b e Minist .R ila Wint William R. G. , r elArclue elEeaee el P la de et l’Elevage de l’Agriculture, de ere f | ` Unit n Health One eVrlge ntttPserd aaacr P17 naaaio11 Madagascar; 101, Antananarivo 1274 BP Madagascar, de Pasteur Institut Virologie, de e ´ uin France; eunion, ´ j mrigadEiei ontcDsae,Pnei n pdmcDsaeDepartment, Disease Epidemic and Pandemic Diseases, Zoonotic Epidemic and Emerging Aedes, a,b C , k cl Squarzoni-Diaw ecile n rcCardinale Eric and , ´ 1073/pnas.1607948114/-/DCSupplemental at online information supporting contains article This option. access open 1 PNAS the through online available Freely Submission. Direct PNAS a is article This interest. of conflict no declare G.R.W.W., authors J.B., P.B.H.F., The S.d.l.R., C.S.-D., paper. A.A., the wrote C.C., data; E.C. J.M.-H., analyzed and G.R.W.W. S.-F.A., S.d.l.R., V.M.R., and C.S.-D., A.A., M.B., A.A., C.C., R.L., M.B., C.C., and R.L., J.M.-H., S.-F.A., research; V.M.R., performed M.B., E.C. and P.B.H.F., R.L., research; designed E.C. and lclrs)adctl rd rmt ik,ass hi relative their environment assess local risk), the (remote trade to cattle related and indexes infection risk risk) build (local human to aimed RVFV then with of and We epidemics transmission. conditions 2008 and RVFV environmental live- 1990 local the the via of start described ruminants the with we to associated first introduction Then, We RVFV trade. occurred. of stock understanding epidemics risk at RVF the aimed which assessed we in end, based circumstances this populations, the set- To exposed a most evidence. the such scientific identify in on to limited crucial are is it resources ting, health inhab. 1.5 public USD Because than less (16). with living population the of 90% (13–15). estimated was excess cases an human underreporting, 10,000 to of laboratory- due RVFV reports However, 26 (7). fatalities. official and cases confirmed highlands with suspected central 700 2008–2009 least the in at suggesting in occurred and epidemic Coast second A East the on trans- 1990–1991 not is virus The person. to (12). person infectious from highly mitted is occasion produced aerosol this Blood on (11): animals viremic of slaughtering the d uhrcnrbtos ...... FA,JM-. ..D,SdlR,PBHF,G.R.W.W., P.B.H.F., S.d.l.R., C.S.-D., J.M.-H., S.-F.A., V.M.R., R.L., contributions: Author owo orsodnesol eadesd mi:[email protected]. Email: addressed. be should correspondence whom To eted ehrh td elesrlsMaladies les sur Veille de et Recherche de Centre eeto n rvnino V nhumans. in early RVF improving of prevention thereby and spread, detection and under- dynamics shown properly disease has to ruminants stand needed to are risk analyses high multidisciplinary of cat- how areas major and meat. routes, hubs, trade fresh introduction tle possible handling of and identification slaughtering The in highest with were involved infections spread Human those trading. disease livestock long-distance to and linked geographically Mada- introduction were In with infections distinct, drivers. ruminant nonenvironmental and can occurrence human on gascar, RVF dependent that be drivers assumption possible also the of linked confirms range and wider study a this people, investigating viral to By mosquito-borne rainfall. transmissible to emerging, ruminants, an of is infection (RVF) fever Valley Rift Significance aaacri n ftepoetcutisi h ol,with World, the in countries poorest the of one is Madagascar in occurred epidemic RVF known first the Madagascar, In e o-yAndriamandimby Soa-Fy , ce ieto e evcsV Services des Direction eche, ˆ b,c,d g St , paed aRocque La de ephane ´ . h ol raiainfrAnimal for Organization World b rnhNtoa Agricultural National French www.pnas.org/lookup/suppl/doi:10. f , NSEryEdition Early PNAS et ´ mretsd l’Oc de Emergentes ´ erinaires, ´ a,b,h,i , −1 | ean f6 of 1 ´ ·d −1

APPLIED BIOLOGICAL SCIENCES 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. negative anomaly was observed for SOI, one of the main indi- (A) Standardized southern oscillation index (19). (B) Standardized rain- cators of ENSO (Fig. 1A). Rainfall was lower than normal in fall anomalies. Source: National Oceanic and Atmospheric Administration all three biomes (Fig. 1B). March 1990 was also at the end of (NOAA)’s precipitation reconstruction over Land (PREC/L) provided by the a period of positive NDVI anomalies and before a short period NOAA/Office of Oceanic and Atmospheric Research/Earth Sciences Research of negative anomalies for the dry forest and xeric shrubland. The Laboratory - Physical Sciences Divisions, Boulder, CO. (C) Standardized NDVI pattern was not clear for the moist forest where the epi- NDVI anomalies. Source: Global Inventory Modeling and Mapping Studies demics started (Fig. 1C). Conditions during the 2008 epidemic (GIMMS), Advanced Very High Resolution Radiometer (AVHRR) NDVI version 3 (20). On each plot, favorable conditions for RVF are shown in red. were almost the reverse as it occurred during a cold (positive) anomaly of SOI, when rainfall was close to normal in the moist forest and somewhat higher than normal in the two other biomes. These general impressions were corroborated by the results nant sera collected at the end of the 2008 epidemic to assess of partial triadic analysis and hierarchical clustering (Fig. S3): the role of environmental conditions in RVF spread in livestock. The environmental conditions of RVF epidemics fell into quite The subset of plausible models according to the available data different clusters in 1990–1991 and in 2008–2009: With a three- is shown in Table S1. The importance of environmental predic- class partition, the 1990 epidemics occurred in a category of rainy tors with respect to the selected subset of plausible models is dis- seasons with close-to-normal mean values for SOI (0.01), rainfall played in Table S2. Multimodel averaged coefficients are shown (0.16), and NDVI (−0.11). In 2008, the epidemic fell into a cat- in Table S3. Higher rainfall, municipalities within 50 km from egory with a high mean SOI (1.38) and close-to-normal mean a sea port, and lower altitude were associated with higher sero- values for NDVI (0.07) and rainfall (−0.16). prevalence rate in ruminants. See SI Results and Figs. S4 and S5 RVFV spread at the end of 2008 epidemic. We modeled the sero- for details on exploratory data analysis. prevalence rate of immunoglobulins of type G (IgG) in rumi- The receiver operating characteristic (ROC) curve for the averaged model had an area under the curve of 74%. The map of predicted sero-prevalence rate showed high-risk areas on the northwestern and northeastern coasts (lowlands). Southern Table 1. Importation of live ruminants in Madagascar from the regions and highlands were less affected with the exception of Union of Comoros between 2005 and 2007 (source: UN ComTrade) sea-port municipalities (Fig. 2). See SI Results for details. Year Species Quantity, head The Cattle Trade Network and RVFV Dissemination. Cattle trade 2005 Cattle 30* data were collected monthly from 2007 to 2011, with large varia- Goats 9* tions in numbers across the years. The overall network activity 2006 Goats 14* is presented in Fig. S6A: Each segment corresponds to a link 2007 Cattle 7 between two nodes; a segment is drawn if at least one move- Goats 88 ment has been recorded along that link on a given month; its Sheep 47 color is related to its recorded frequency during the 5-y survey. *Estimated number from the reported financial value. No imports of live To assess the influence of the cattle trade network on the risk of ruminants were reported from the Union of Comoros in 2003 and 2004. RVFV in humans, we quantified the trade flows using the most

2 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1607948114 Lancelot et al. Downloaded by guest on September 27, 2021 Downloaded by guest on September 27, 2021 acrwr h ao ore ftetae ate(i.3A) (Fig. cattle traded al. et Lancelot the of sources major the were gascar infec- an of RVFV. diffusion the like the disrupt agent would limit tious removal thus Their and network: connectedness were the network hubs in These points (22). cut neighborhood infection also their of in risk locations the con- other strongly increasing for were thus GSC themselves, these between to nected belonging in Nodes one. were same Ihosy the and different (GSC)—Ambalavao three components to strong belonged giant hubs network four highest The the had and betweenness. also Ambalavao, and hubs distribu- Tsiroanomandy, connected power-law highly (Ihosy, were a nodes Mampikony) few matched a node) Only given tion. a for links outgoing otedfuino VV h vrg pdmctrsodwas threshold q epidemic average The prone RVFV: q was of network diffusion trade whole the The of to network. variations backbone the the by in influenced volume strongly was it Conversely, variations, large these occasional Despite of October. q and number May The in size S6B). peaked January (Fig. plateau links season) its in dry reaching smallest (early until April risk the increased in the then was higher and network the season) backbone is, (rainy value The its spread. lower spread of to The virus network: the for the probability through critical the of estimate an threshold vides epidemic eval- corresponding we and the snapshots uated network monthly separate considered we in present already were year. 2010 volume previous in small the the active of a links Most only and links. occasional nodes number, these backbone large on traded their was Despite animals of mo. (3%) for 2 active or links constituting occasional mo those links) 1 and links: the network of the of of slaughter- sets (56% backbone two year the and the distinguish throughout markets, could active We farms, those (346). (257 links and nodes the houses) had of network number This 2010. largest in collected dataset, comprehensive variation. of pre- coefficient (A) (B) model: and regression rate logistic dicted beta-binomial averaged the by predicted 2. Fig. ˆ ˆ ¯ 25 20 15 A ° ° ° a lgtyafce ytepeec fteeocsoa links. occasional these of presence the by affected slightly was ' ' h atrlaeso otws n otws fMada- of northwest and southwest of areas pastoral The incoming/ of (number degrees in/out of distribution The oass h oeo h cainllnso VVspread, RVFV on links occasional the of role the assess To S S S h eido aiu ikfo ac oMy with ( May, risk to minimum March the from and risk 1.5%, maximum of period the 2.1%, eopeaec aeo niRF g nrmnns(Madagascar) ruminants in IgG anti-RVFV of rate Sero-prevalence Toliara 300km 0 Morondava 44 ° E Sero . . . 0.8 0.6 0.4 0.2 Mahajanga 46 prevalence rate Taolagnaro ° E48 Manakara ° Antsiranana E50 Antalaha ° E q ˆ ' B nJanuary. in 3.9%) Coefficient ofvariation q . . . 0.4 0.3 0.2 0.1 2) hc pro- which (21), bos 27). (26, national 2015 strengthened in and surveillance regional epidemic) (shortly and RVF 1994 1990–1991 in the measures to after surveillance related specific despite Madagascar, occurrence detected rainfall Ni in the torrential El 2015 strong with recently, the February–March More 1994 (24). in in first cyclone occurred e.g., the Geralda heavy 1990, after the Prolonged of occurred of Africa. anomalies epidemics South NDVI known positive and disease and the East of rainfall and behavior contrasting Madagascar the in out pointed already has Epidemics. RVF and Conditions Environmental exported Islands. ruminants Comoros for the to reinforced Africa continental be from should quar- Also, circulation. measures RVFV new antine of event share the to in Malagasy important detection be early and would services Comoros, veterinary and health African, strengthen- public between practice, In communication Madagascar. ing in avoid to epidemics essential Madagas- RVF therefore in further is RVFV introductions pro- such of Islands Preventing introduction car. Comoros the the for from opportunities existence vided importation The livestock (23). Comoros Africa illegal East the of with into trade introduced cattle through probably (15) Islands Africa was mainland RVFV in that circulating suggest previously closely 2008. viruses were in to RVFV least related Malagasy at that humans, to showing spread studies trade-related its Phylogenetic to subsequent led and cattle of intro- livestock movements RVFV Introduction. Madagascar for driver to RVFV main duction of the were Risk Comoros from the ruminants and Trade Cattle Discussion Antsirabe of regions the See in Alaotra. Lake found and was risk) trade-related is cattle pattern This highlands. in central emphasized of in spatial areas highlighted encountered clear populated were both a densely rates the with S8) sero-prevalence rate, highest (Fig. infection The the variations pattern. in random variations spatial of large plot the and trade cattle of livestock. intensity infected getting with the humans areas with of from increased risk RVFV The with 2.7]). OR infected [1.1; was latter (CI): S4 the coef- interval for (Table (OR) confidence the index ratio to odds trade-related The contrast cattle S7). Fig. in remote, significant, the not for trans- ficient was RVFV humans of index to environment-related mission Humans. local, in the Infection for RVFV of ficient Risk the and Trade Cattle showed spread. opportunities hubs RVFV numerous four long-distance offered for these flows of outgoing small, examination many close that Ambalavao a cen- consumption addition, to a In sent being ter. then also mar- and Tsiroanomandy the Ihosy slaughtering, in for and collected were Tsiroanomandy Cattle of 3C: kets Fig. on infor- provided Further is balance. mation positive local large, (Ambalavao a low hubs had with two Tsiroanomandy) hand, balance network, and other the negative the On in a 3B). human sources (Fig. had were consumption low They markets and flows: of cattle density majority in cattle great high The by density. characterized were and h otws fteiln,cvrdb h r oet Moreover, forest. dry the by covered flooding). island, the in no of cattle rainfall, northwest in observed the heavy subopti- were municipalities rates (no in sero-prevalence neighboring vectors high introduced Conversely, the was the for virus in conditions the mal because low probably sero-prevalence was 2), the (Fig. ruminants RVF, by in hit rate was Although A). S2 municipality Mada- (Fig. southwest sea-port shrublands xeric of this by region covered Toliara are that the gascar in ecosystems to similar V pdmc sal tr nteai niomnsof environments arid the in start usually epidemics RVF 4) (Fig. humans in rate sero-prevalence predicted of map The Es fia and/or Africa) (East togadtoa ik(ihrsetto respect (with risk additional strong A S8B: Fig. ocniin 2) oRFotra ol be could outbreak RVF No (25). conditions no ˜ IResults SI pans suhr fia 1,wihare which (1), Africa) (southern o details. for NSEryEdition Early PNAS nab ta.(14) al. et Anyamba mot flive of Imports C . (95% 1.7 = h coef- The | dam- f6 of 3 and

APPLIED BIOLOGICAL SCIENCES ABC

Fig. 3. Cattle flows in the Malagasy cattle trade network, 2010. (A) Municipality of origin (number of flows). (B) Balance in cattle flows at the municipality level (number of heads). (C) Directed flows (number of heads).

in East Africa, Aedes mosquitoes are the primary RVFV vec- Madagascar (8). The connectedness of the cattle trade net- tors (1): Their biology and ecology are well adapted to arid envi- work and its low percolation threshold make the risk of seeding ronments. Regarding Madagascar, 23 mosquito species might be epidemics high. considered as potential RVFV vectors, including no floodwater Lake Alaotra and Antsirabe (Fig. S2A) are two major crop Aedes mosquito species (28–30). A single species, Culex antenna- and livestock farming regions. The former is the largest rice- tus, meets all criteria for formal classification as an RVFV vec- production basin in Madagascar, with many paddies and swamps tor (31). This mosquito is widespread in Madagascar (except in the North), including in rice paddies that cover large areas of the island. The introduction of infected animals in conjunction with Culex hatching, during a standard rainy season profile, might AB have amplified the outbreak locally, in many places. Two major differences are thus highlighted between Madagas- car and East Africa: (i) the lack of connection between the start of 1990–1991 and 2008–2009 RVF epidemics and El Nino˜ events and, more generally, with anomalous heavy rainfall and (ii) no obvious role of Aedes mosquitoes in the primary RVFV trans- mission cycle, as well as the wide distribution of Culex (and other mosquito species). Apparently, the climatic conditions observed during the two epidemics are common in Madagascar: The drivers triggering RVFV epidemics must therefore be sought elsewhere. Neverthe- less, these climatic conditions remain important for the amplifi- cation of the primary epidemiological cycle between mosquitoes and ruminants (Table S2). Cattle Trade as a Driver of RVF Epidemics. The Malagasy popu- lation is growing fast, from 16 million to 24 million between 2000 and 2015 (16), and is concentrating in Antananarivo and other large cities (Fig. S2B). Cattle are omnipresent in Malagasy agriculture, economy, and culture. This leads to an ever-growing Fig. 4. Sero-prevalence rate in humans predicted by a mixed-effect bino- mial logistic regression model: (A) predicted rate and (B) coefficient of vari- demand for cattle meat and draught power for crops. Conse- ation. In A, numbers were placed at the centroid of districts with the highest quently, the increasing cattle trade provides more opportuni- predicted rates (10th decile): 1, Ambohidratrimo; 2, Antananarivo Renivohi- ties for RVF epidemics to spread (7, 8). Our description of tra; 3, Antananarivo-Sud; 4, Antsirabe Rural; 5, Antsirabe Urban; 6, Betafo; the national cattle trade network strongly supports this assump- 7, Faratsiho; 8, ; 9, ; 10, Anosibe; and 11, tion and further extends a previous analysis in the North of Moramanga.

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Rollin D, Fontenille JF, Saluzzo J, Morvan 7. P V, outbreak. Chevalier fever Valley 6. Rift a of the Prediction in (2009) al. mode et dipole A, A Anyamba (1999) T 5. Yamagata PN, Vinayachandran fever BN, Valley Goswami Rift NH, forecast Saji to indicators 4. satellite and Climate (1999) al. et K, Linthicum 3. warn- early and ecology Disease fever: Valley Rift (2010) P Formenty mosquito- S, emerging LaRocque An de fever: Valley Rift 2. (2016) A Anyamba SC, Britch KJ, Linthicum 1. oass h ik fRF pedwti aaacr eue two used we Madagascar, within spread RVFV of risks the assess To we epidemics, RVF past the of conditions environmental the describe To is anthropologists and sociologists with collaboration More and butcheries, markets, of network the using Additionally, nlsso h atetaentoki h aaacrhglns oeta oein role Potential highlands: virus. Madagascar fever the Valley in Rift of network diffusion trade the cattle the of analysis Madagascar. of coast east the Surveill Euro USA Ocean. Indian tropical Nations, United the Kenya. in of epidemics Organization Agriculture and (Food 327–333. pp G Rome), Viljoen M, Garcia ing. disease. borne 106(3):955–959. utial aaeeto nmlPouto n Health and Production Animal of Management Sustainable ceprsarnsfrtaees,frestyt eltheir sell to try farmers travelers), for restaurants (cheap 15(10):19506. pnM Pl M, epin ´ nuRvEntomol Rev Annu niomna aaslce mn h atr finter- of factors the among selected data environmental ) Science Nature eL acltR(00 itVle ee– hetfrEurope? for threat fever–A Valley Rift (2010) R Lancelot L, ee ´ 285(5426):397–400. e Virol Res 401(6751):360–363. 61:395–415. caTrop Acta 142(6):475–482. 126(1):19–27. analdt,o cru- of data, rainfall ) h O samain a as SOI the ) rcNt cdSci Acad Natl Proc d dnoN, Odongo eds , ) 5 arl A ta.(01 eei vdnefrRf alyfvrout- fever Valley Rift for evidence Genetic (2011) al. et SA, Carroll 15. East in activity fever causes Valley Rift the of virus assessment Prediction, (2010) al. fever Madagascar, et A, seasons, Anyamba rainy Valley during 14. fever Valley Rift Rift (2010) to al. et SF, Andriamandimby exposure 13. Aerosol (2013) al. et Kenya, in infection C, fever Valley Rift Reed severe for 12. factors Risk (2010) al. et AS, fever. Anyangu Valley Rift 11. (2004) G Gerdes 10. mrigVrlVco-on iess(MRE n sctlgdb the by ( cataloged United VMERGE019 is the as FP7-613996 and Committee Grant of (VMERGE) Union Steering Diseases Fund European VMERGE United by Vector-Borne Response funded Viral the partially Emergency Emerging of also was Central Organization It Agriculture the Nations. and through Food Nations the and Organization ACKNOWLEDGMENTS. analyses. the in links used as datasets well ran- as the methods, download nested statistical to and the sources data as rate on See region information sero-prevalence intercept. detailed and the of with district variations associated administrative effects local dom the the with study humans, to regres- in used logistic binomial was mixed-effect model a Finally, sion model. human BBLR with a with correlated assessed positively be should infec- trade RVFV cattle of density. slaughter- risk to of the densities related Consequently, higher markets. tion with meat proportionally (43), and areas is butchers, This rural consumption density. houses, in than meat human urban local because in and included higher was origin, was the It variable predicted at trade. head), (ii latter cattle cattle of (number index. in to flow this rate incoming the related cattle sero-prevalence in risk of in product involved transmission considered the RVFV not as not defined of are wild index was Humans known an density 42). of created their (41, absence Madagascar Therefore, the cap- in cycle. in to RVFV ruminants, built for domestic was involv- sero- hosts cycle index and epidemiological predicted RVFV This mosquitoes primary local density. the ing with of cattle associated risk and product the cattle the ture indexes in by two rate (i defined defined humans: prevalence recent risk, in We a infection transmission (13). RVFV indicating RVFV published of IgM, risk were anti-RVFV the results of for the presence consent. the and informed written for infection, Com- gave tested Ethical they National were if Malagasy Sera included the by were 2008 approved Participants in was mittee. performed study workers The slaughterhouse 2009. of and survey nationwide a during of the movement animals. and traded places, trade of destination number a and the to origin was the volume corresponded indicated nodes direction two The net- animals. between trade cattle link directed a A of work. nodes the were slaughterhouses and markets, of (ii prediction and network and the averaging level. model municipality the for A at kept cattle predictors. in was best rate models the sero-prevalence select plausible We IgG. to of anti-RVFV epidemics approach of set inference 2008 presence multimodel the the munici- for a after tested the adopted collected were at Sera were cattle (39). data published for and serological rate The sero-prevalence level. RVFV pality the predict to study. models this of purpose the for slaughterhouses, 2011 and to markets 2007 livestock from implemented in surveys nationwide repeated (ii pro- ing and the and in methodology; databases list favoring standard international using the conditions from cessed (see obtained in were (37) which changes rest- etc. Methods), stage, of seasonal and immature availability the their the or of to sites development related breeding i.e., or infections, ing mosquito-borne for est o eesrl eetteveso h uoenCommission. European do the and of authors the views of the responsibility reflect sole necessarily the not are publication this of contents .SomkrT ta.(02 eei nlsso iue soitdwt emergence with associated viruses of analysis Genetic (2002) al. et T, Shoemaker 9. h feto hs w nee nhmnsr-rvlnert was rate sero-prevalence human on indexes two these of effect The collected sera using humans, in infection RVFV of risk the assessed We (i used were data trade Cattle (BBLR) regression logistic beta-binomial in used were data Environmental rasi aaacrrsligfo iu nrdcin rmteEast the from introductions maintenance. virus enzootic than from rather resulting 6167. mainland Madagascar African in breaks strategies. control vector Hyg possible and 2006-2008 Africa has Southern and which model, 2009. murine and 2008 the in development. neuropathology therapeutic e2156. for severe implications more important and earlier 2007. 2000-01. Yemen, and Arabia Saudi in fever 1415–1420. Valley Rift of 32Suppl):43–51. 83(2 mJTo e Hyg Med Trop J Am mr netDis Infect Emerg oass h iko ua neto ihRF.Farms, RVFV. with infection human of risk the assess to ) hssuywsprilyfne yteWrdHealth World the by funded partially was study This 32Suppl):14–21. 83(2 16(6):963–970. e c Tech Sci Rev oass h iko VVsra through spread RVFV of risk the assess to ) 23(2):613–623. atetaedt olce dur- collected data trade cattle ) ecetda ne flocal of index an created We ) IMtrasadMethods and Materials SI .The http:/www.vmerge.eu). NSEryEdition Early PNAS LSNg rpDis Trop Negl PLoS mr netDis Infect Emerg Virol J mJTo Med Trop J Am IMaterials SI 85(13):6162– | f6 of 5 We ) 8(12): 7(4): for

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