Rift Valley Fever During Rainy Seasons, Madagascar, 2008 and 2009 Soa Fy Andriamandimby, Armand Eugène Randrianarivo-Solofoniaina, Elisabeth M
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Rift Valley Fever during Rainy Seasons, Madagascar, 2008 and 2009 Soa Fy Andriamandimby, Armand Eugène Randrianarivo-Solofoniaina, Elisabeth M. Jeanmaire, Lisette Ravololomanana, Lanto Tiana Razafi manantsoa, Tsanta Rakotojoelinandrasana, Josette Razainirina, Jonathan Hoffmann, Jean-Pierre Ravalohery, Jean-Théophile Rafi sandratantsoa, Pierre E. Rollin, and Jean-Marc Reynes1 During 2 successive rainy seasons, January 2008 of abortion and death in young and adult animals. Eco- through May 2008 and November 2008 through March nomic consequences of this disease can be devastating. In 2009, Rift Valley fever virus (RVFV) caused outbreaks in humans, symptoms are usually mild, but in severe cases Madagascar. Human and animal infections were confi rmed hemorrhage, meningoencephalitis, retinopathy, and death on the northern and southern coasts and in the central can occur. RVFV has been detected across Africa, from highlands. Analysis of partial sequences from RVFV strains Senegal to Madagascar and from Egypt to South Africa. In showed that all were similar to the strains circulating in Ke- nya during 2006–2007. A national cross-sectional serologic 2000, RVFV reached the Arabian Peninsula (1). survey among slaughterhouse workers at high risk showed Animals are typically infected before humans. RVFV that RVFV circulation during the 2008 outbreaks included is transmitted between ruminants primarily by bites of all of the Malagasy regions and that the virus has circulated mosquitoes of numerous genera and species. Humans can in at least 92 of Madagascar’s 111 districts. To better pre- also be infected by these vectors as well as by contact or in- dict and respond to RVF outbreaks in Madagascar, further halation of aerosols generated when handling sick or dead epidemiologic studies are needed, such as RVFV complete infected animals or their fresh tissues. Treatment of human genome analysis, ruminant movement mapping, and sur- patients is based on signs and symptoms; a commercial veillance implementation. vaccine is available for animals only. RVFV outbreaks are periodic and occur every 10–15 years. Between epidem- ift Valley fever virus (RVFV) belongs to the family ics, the virus is believed to be maintained through vertical RBunyaviridae, genus Phlebovirus, and was fi rst iso- transmission by mosquitoes of the genus Aedes. Outbreaks lated in 1930 during an investigation of a large epizootic in are closely linked to climate variations, especially wide- Kenya. Virions are enveloped and contain 3 single-stranded spread increased rainfall, that favor the hatching of mosqui- RNA genome segments designated large (L), medium (M), to eggs and the subsequent emergence of a large number of and small (S) coding for the viral proteins. adult mosquitoes (2). Moderate or large outbreaks that have Rift Valley fever (RVF) is an arthropod-borne zoono- been documented in the Horn of Africa (1989, 1997–1998, sis; it affects ruminants and is characterized by high rates 2006–2007) were associated with widespread rainfall. For the purpose of predicting RVF outbreaks in this area, a Author affi liations: Institut Pasteur, Antananarivo, Madagascar (S.F. model based on several satellite-derived observations has Andriamandimby, T. Rakotojoelinandrasana, J. Razainirina, J. Hoff- been proposed (3). mann, J.-P. Ravalohery, J.-T. Rafi sandratantsoa, J.-M. Reynes); RVFV has also been detected in Madagascar. The Ministère de la Santé et du Planning Familial, Antananarivo (A.E. fi rst isolate was obtained from mosquitoes caught during Randrianarivo-Solofoniaina, L. Ravololomanana); Food and Agri- the March 1979 rainy season in a forest area in the Mora- culture Organization, Antananarivo (E.M. Jeanmaire); Ministère de manga district (no. 514; online Appendix Figure, www. l’Agriculture, d’Elevage et de la Pêche, Antananarivo, (L.T. Razafi - cdc.gov/EID/content/16/6/963-appF.htm), 120 km east of manantsoa); and Centers for Disease Control and Prevention, Antananarivo (4). Then in March 1990, an RVF epizootic Atlanta, Georgia, USA (P.E. Rollin) 1Current affi liation: Centre Pasteur du Cameroon, Yaounde, DOI: 10.3201/eid1606.091266 Cameroon. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 6, June 2010 963 RESEARCH occurred in Fenoarivo Atsinana (district 509) on the east completed by using inactivated RVFV-infected Vero E6 coast, where an abnormally high incidence of abortions and cell antigens and uninfected Vero E6 cell antigens; 4 dilu- disease in humans was reported (5,6). A year later, from tions of each serum (1:100, 1:400, 1:1,600, 1:6,400) were February through April 1991, RVFV was responsible for used. Titers and the cumulative sum of optical densities of abortions and deaths of cattle in the central highlands. Hu- each dilution (SUMOD) minus the background absorbance man cases were also confi rmed (7,8). After the outbreaks of of uninfected control Vero E6 cells (adjusted SUMOD) RVF in 2006 and 2007 in the Horn of Africa (9), 17 years were recorded. Results of the assays for serum samples later, the virus was again detected in Madagascar during a were considered positive only if the adjusted SUMOD and major outbreak. We report some features of this outbreak titer were above preestablished conservative cutoff values, and the results of preliminary molecular characterization which were set for IgM ELISA (>0.75 and >400, respec- of the circulating virus. We also performed a nationwide tively) and IgG ELISA (>0.95 and >400, respectively). A serosurvey to determine the range of past and recent RVFV probable RVFV infection was one in which no RVFV was circulation. detected but antibodies were detected. Infection was con- sidered recent when IgM against RVFV was detected and Materials and Methods past when only IgG against RVFV (no IgM against RVFV) was detected. Human Surveillance Systems In 1996, in accordance with World Health Organiza- Virologic Assays tion resolution AFR/RC43/R7, the Integrated Diseases Virus isolation was performed on mosquito cell lines Surveillance and Response system was implemented by the (AP61 and Vero E6) by using acute-phase serum samples Direction des Urgences et de la Lutte contre les Maladies (diluted 1:10), and virus identifi cation was performed by (DULM) from the Malagasy Ministry of Health. Hemor- an indirect immunofl uorescence assay that used pools of rhagic fevers are among the reportable diseases. Each week, mouse immune ascetic fl uids (11). These fl uids reacted basic health centers and hospitals (district and regional) against several arboviruses previously isolated from Mada- must notify DULM about cases or absence of cases. gascar, including RVFV. In addition, in 2007 the DULM set up, in collabora- tion with the Institut Pasteur de Madagascar (IPM), a sen- Molecular Assays tinel surveillance system including 19 clinical sites (basic Liver or spleen specimens (50–100 mg) from dead health centers). Each site reports daily to the central level animals with suspected RVF were homogenized at a dilu- (DULM and IPM) the number of patients, persons with fe- tion of 1:10 in culture medium containing 30% fetal bo- ver, confi rmed malaria cases, suspected arboviral disease vine serum. The supernatant was collected after centrifu- cases, and suspected infl uenza cases. Suspected arboviral gation. Viral RNA was extracted from the serum samples disease cases were defi ned as cases in patients with axillary of patients and animals suspected of having infection by temperature >37.5°C and >2 of the following signs: head- using the QIAamp Viral RNA Mini Kit (QIAGEN GmbH, ache, myalgia, arthralgia, retro-orbital pain, and cutaneous Hilden, Germany) and from organ supernatants by using rash or hemorrhagic signs. Of the 19 centers, 4 are also TRIzol LS reagent (Invitrogen, Carlsbad, CA, USA) ac- biological surveillance sites. Serum samples from patients cording to the manufacturers’ instructions. with suspected arboviral disease are sent weekly in liquid The molecular detection of the virus was performed nitrogen to the IPM. by using a nested reverse transcription–PCR (RT-PCR) de- During the outbreak, a suspected case of RVF was de- scribed by Sall et al. (12) or a real-time RT-PCR described fi ned as illness in a person with a hemorrhagic syndrome by Weidmann et al. (13). The minimum level of detec- and history of fever or as encephalitis and a dengue-like tion was 25 transcript RNA copies per assay. A confi rmed syndrome after exposure to sick or dead ruminants or ex- RVFV infection was an infection in which RVFV was iso- posure to ruminants in a village where sick or dead animals lated or RVFV RNA was detected. had been reported since detection of the fi rst cases. Molecular Characterization Laboratory Diagnosis Parts of the S, M, and L segments of RVFV were am- plifi ed and sequenced. S-amplifi ed product (portion of non- Serologic Assays structural protein) was obtained by using the nested RT- RVFV immunoglobulin (Ig) M and IgG ELISAs were PCR technique published by Sall et al. (12). M-amplifi ed performed as described previously (10). After heat and product (portion of G2) was obtained by using RT-PCR detergent inactivation, serum samples were tested by anti- primers M-F675 (5′-ACCATCATTGCAAAGGCTGA-3′) RVFV–specifi c IgM and IgG ELISAs. The assays were and M-R1645 (5′-GCCATGTGAACCCCTATGTC-3′) 964 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 6, June 2010 Rift Valley Fever, Madagascar and nested PCR primers MRV1a and MRV2g used by Sall et al. (14). L-amplifi ed product (portion of L) was obtained by using RT-PCR primers L-F4209 (5′- GCGCATTGCAGAGAAAGTC) and L-R5113 (5′-CAA CGTGATCACCATCTAGAAA-3′) and nested PCR prim- ers L-F4273 (5′-TGTAAAGTCATGGCCTCAGC-3′) and L-R4878 (5′-CATCCGGGAGAAATTGTCA-3′). M-F675, M-R1645, L-F4209, L-R5113, L-F4273, and L-R4878 were designed to obtain M- and L-nested PCR products >600 bp; Primer3Plus software (15) was used according to 33 pub- lished complete RVFV M or L sequences (16).