LETTERS

4. Vázquez A, Ruiz S, Herrero L, Moreno Absence of they might play a role in the mainte- J, Molero F, Magallanes A, et al. West nance of RVFV. However, genetic evi- Nile and Usutu viruses in mosquitoes Rift Valley Fever in Spain, 2008–2009. Am J Trop Med dence indicates that RVFV outbreaks Hyg. 2011;85:178–81. http://dx.doi. Virus in Wild Small in Madagascar are not associated with org/10.4269/ajtmh.2011.11-0042 , emergence from enzootic cycles but 5. Sotelo E, Llorente F, Rebollo B, Camunas that they are associated with recur- A, Venteo A, Gallardo C, et al. Develop- Madagascar ment and evaluation of a new epitope- rent virus introductions from main- blocking ELISA for universal detection To the Editor: Rift Valley fever land east Africa (7). Although these of antibodies to West Nile virus. J Virol virus (RVFV) is a mosquito-borne mechanisms for RVFV epidemiology Methods. 2011;174:35–41. http://dx.doi. on Madagascar are documented, the org/10.1016/j.jviromet.2011.03.015 zoonotic virus in the family Bunya- 6. Figuerola J, Jimenez-Clavero MA, Rojo G, viridae, genus Phlebovirus, which af- possibility of a wild reser- Gomez-Tejedor C, Soriguer R. Prevalence fects mainly domestic ruminants and voir cannot be excluded. We therefore of West Nile virus neutralizing antibodies humans on continental Africa, Mada- explored the role of wild terrestrial in colonial aquatic birds in southern Spain. small mammals in the maintenance of Avian Pathol. 2007;36:209–12. http:// gascar, and the Arabian Peninsula (1). dx.doi.org/10.1080/03079450701332329 RVFV is transmitted between rumi- RVFV in Madagascar, especially the 7. Scaramozzino N, Crance JM, Jouan A, nants mainly by bites of mosquitoes of nonnative, abundant, and ubiquitous DeBriel DA, Stoll F, Garin D. Com- several genera (1). Infection can lead black rats (Rattus rattus) (8), as has parison of flavivirus universal primer been suggested in rural Egypt (9,10). pairs and development of a rapid, highly to mild symptoms or can cause abor- sensitive heminested reverse transcrip- tion in pregnant and high mor- For this study, 1,610 blood sam- tion–PCR assay for detection of fla- tality rates among newborns. Humans ples were obtained from different spe- viviruses targeted to a conserved re- are mostly infected by aerosol trans- cies of wild terrestrial small mammals gion of the NS5 gene sequences. J Clin in Madagascar (Figure). Permits to Microbiol. 2001;39:1922–7. http://dx.doi. mission when handling infected tissues org/10.1128/JCM.39.5.1922-1927.2001 (aborted fetuses or meat), which results capture and collect animals were ob- 8. Dupuis AP II, Marra PP, Kramer LD. Se- in dengue-like illness. Some cases in tained from national authorities. Ani- rologic evidence of West Nile virus trans- humans can be in a severe form (hem- mals were sampled from October 2008 mission, Jamaica, West Indies. Emerg through March 2010 at a site in the Infect Dis. 2003;9:860–3. http://dx.doi. orrhagic fever and meningoencephali- org/10.3201/eid0907.030249 tis), which can be fatal. Outbreaks in Anjozorobe-Angavo (Anjozorobe Dis- 9. Monaco F, Savini G, Calistri P, Polci A, southern and eastern Africa are associ- trict) forest corridor (18°18′′41.9′ S, Pinoni C, Bruno R, et al. West Nile disease ated with periods of heavy rainfall (1). 48°00′′57.6′ E), where RVFV was first epidemic in Italy: first evidence of over- detected in humans and cattle in Febru- wintering in Western Europe? Res Vet Sci. In eastern Africa, RVFV is believed to 2011;91:321–6. be maintained during interepizootic ary 2008 (4) and within 100 km from 10. Sotelo E, Fernandez-Pinero J, Llorente periods through vertical transmission where the first RVFV was isolated in F, Vazquez A, Moreno A, Aguero M, et in Aedes spp. mosquitoes (1). It has 1979 (3). We collected 378 serum sam- al. Phylogenetic relationships of western ples from 11 native Tenrecidae (Af- Mediterranean West Nile virus strains been suspected that wild mammals, (1996–2010) using full-length genome se- especially rodents, play a role in the rosoricida) , 114 samples from 6 quences: single or multiple introductions? maintenance of RVFV during interepi- native Nesomyidae (Rodentia) rodents, J Gen Virol. 2011;92:2512–22. http:// and 471 samples from introduced R. dx.doi.org/10.1099/vir.0.033829-0 zootic periods (2). However, evidence of a wild mammal reservoir in the epi- Rattus (Muridae, Rodentia) rats (online Technical Appendix, wwwnc.cdc.gov/ Address for correspondence: Miguel Ángel demiologic cycle of RVFV has yet to EID/article/19/6/12-1074-Techapp1. Jiménez-Clavero, Centro de Investigación en be demonstrated (2). pdf). In addition, during 2008, we ob- Sanidad CISA (INIA), Ctra Algete—El In Madagascar, the first RVFV tained serum samples from 647 R. rat- Casar s/n, 28130, Valdeolmos, Spain; email: isolate was obtained from mosquitoes tus or R. norvegicus rats living near [email protected] captured in the Périnet Forest (Anda- sibe, Moramanga District) in 1979, humans in areas where RVFV was outside an epizootic period (3). Two reportedly circulating during 2008 and Books, Other Media epizootic episodes occurred, during 2009: the districts of Ankazobe, An- 1990–91 and 2008–09 (4). After the tsiranana, Betafo, Ihosy, Marovoay, Reviews (250-500) words of most recent episode, domestic rumi- and Moramanga (4,5) (Figure). new books or other media on Serum samples were tested for emerging disease issues are nants were shown to be involved in welcome. Name, publisher, RVFV circulation during interepizo- IgG against RVFV by ELISA, as number of pages, and other otic periods (5,6); together with the described (4), by using peroxidase- pertinent details should be potential vertical transmission in Ae- labeled recombinant protein A/G included. des spp. mosquitoes in Madagascar, (Pierce, Rockford, IL, USA) or

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 6, June 2013 1025 LETTERS

Egypt (9,10). The absence of infec- tion in Rattus spp. rats during a period of intense RVFV circulation does not support its potential role during the outbreak and, a fortiori, in the main- tenance of RVFV during interepizo- otic periods. Among wild terrestrial mammals in Madagascar, animals of the orders Carnivora and Primata are not considered as candidates for the maintenance of RVFV; however, bats ( Chiroptera) and introduced bushpigs (order Artiodactyla , family Suidae, genus Potamochoerus) could be candidates, and their role in RVFV maintenance should be investigated (2). At present, no evidence is avail- able for the maintenance of RVFV in wild terrestrial small mammals (na- tive and introduced) in Madagascar.

Acknowledgments We thank Lalaina Nomenjanahary and Gabriel Ravelojaona for their partici- pation in the field work. We are grateful to Lila Rahalison for sharing some of the rodent serum. This study was supported by a grant from the Groupement d’Intérêt Scientifique, Centre de Recherche et de Veille sur les Maladies Emergentes dans l’Océan (project Figure. Collection sites of wild terrestrial small mammals on Madagascar and the number of mammals tested for Rift Valley fever virus (RVFV). At certain localities, the genus and RIFT-OI no. PRAO/AIRD/CRVOI/08/07). species of sampled rats were Rattus rattus or R. norvegicus. Marie-Marie Olive, anti-mouse or rat IgG (H+L) accord- Carlsbad, CA, USA) according to the Nadia Razafindralambo, ing to the ability to recognize the im- manufacturers’ instructions. Detec- Tony Andrianaivo Barivelo, munoglobulin of species endemic to tion of RVFV RNA was attempted by Jean-Théophile Madagascar (data not shown). The using real-time reverse transcription Rafisandratantsoa, results were negative for all samples PCR (4). The results were negative for Voahangy Soarimalala, tested. Liver and spleen samples from the 220 monospecific pools tested. Steven M. Goodman, 947 animals caught in the Anjozo- Serologic and virologic results Pierre E. Rollin, robe-Angavo forest corridor were also from rodent and samples col- Jean-Michel Heraud, tested. Approximately 50–100 mg of lected during and after the epizootic and Jean-Marc Reynes liver and spleen from each individual 2008–2009 periods were negative for Author affiliations: Institut Pasteur, Antanan- was mixed and homogenized at a di- RVFV; 72.8% had been collected in arivo, Madagascar (M.-M. Olive, N. Razaf- lution of 1:10 in culture medium con- municipalities where RVFV cases indralambo, J.-T. Rafisandratantsoa, J.-M. taining 40% fetal bovine serum. After were reported. This finding does not Heraud); Association Vahatra, Antananari- centrifugation, supernatants were col- indicate a role of native Rodentia and vo (T. Andrianaivo Barivelo, V. Soarimalala, lected and pooled by species (maxi- Afrosoricida mammals in the epide- S.M. Goodman); Université d’Antananarivo, mum 5 individuals/pool). RNA was miology of RVFV in Madagascar, nor Antananarivo (T. Andrianaivo Barivelo); extracted from pooled supernatants by does it indicate evidence of infection Field Museum of Natural History, Chicago, using TRIzol LS reagent (Invitrogen, of Rattus spp. rats, as suggested in Illinois, USA (S.M. Goodman); Centers for

1026 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 6, June 2013 LETTERS

Disease Control and Prevention, Atlanta, antibodies in R. rattus blood samples by calf was identified during pre-export Georgia, USA (P.E. Rollin); and Institut Pas- both enzyme linked immuno sorbent as- testing. And in Yorkshire, England, 2 say (ELISA) and immuno-diffusion tech- teur, Lyon, France (J.-M. Reynes) nique (ID). J Egypt Public Health Assoc. more BLV-seropositive calves, also 2001;76:431–41. artificial insemination bull candidates, DOI: http://dx.doi.org/10.3201/eid1906.121074 were identified. All calves were home Address for correspondence: Marie-Marie bred, and there was no evidence (as References Olive, Unité de Virologie, Institut Pasteur de documented by serologic testing) or 1. Swanepoel R, Coetzer JAW. Rift Valley Madagascar, Antananarivo 101, Madagascar; history of EBL within the herd. The fever. In: Coetzer JAW, Thomson GR, email: [email protected] farms were considered to have low risk Tustin RC, editors. Infectious diseases of for disease incursion because the intro- livestock. Oxford (UK): Oxford Univer- duction of new animals was limited. sity Press; 2004. p. 1037–70. 2. Olive MM, Goodman SM, Reynes JM. Further inquiry revealed that The role of the wild mammals in the main- the calves had each been exclusively tenance of Rift Valley fever virus. J Wildl fed a colostrum replacer from North Dis. 2012;48:241–66. America, where BLV is endemic. 3. Fontenille D. Arbovirus transmission cycles in Madagascar [in French]. Arch Antibodies to BLV might have been Inst Pasteur Madagascar. 1989;55:1–317. Colostrum Replacer present in the colostrum replacer and 4. Andriamandimby SF, Randrianari- thus passively acquired by the calves, vo-Solofoniaina AE, Jeanmaire EM, and Bovine resulting in seropositivity. Ravololomanana L, Razafimanantsoa LT, Rakotojoelinandrasana T, et al. Rift Val- Leukemia Virus The hypothesis was tested by ley fever during rainy seasons, Mada- Seropositivity monthly blood sampling and ELISA gascar, 2008 and 2009. Emerg Infect analysis for antibodies against BLV Dis. 2010;16:963–70. http://dx.doi. in Calves (Institute Pourquier, Montpellier, org/10.3201/eid1606.091266 5. Jeanmaire EM, Rabenarivahiny R, To the Editor: Bovine leukemia France). Although the batch of colos- Biarmann M, Rabibisoa L, Ravaomanana virus (BLV), a deltaretrovirus in the trum replacer that had been fed to the F, Randriamparany T, et al. Prevalence of family Retroviridae, is the causative calves from Dumfriesshire was not Rift Valley fever infection in ruminants in available for investigation, another Madagascar after the 2008 outbreak. Vec- agent of enzootic bovine leukosis tor Borne Zoonotic Dis. 2011;11:395–402. (EBL). Although EBL is still endemic colostrum sample was obtained from http://dx.doi.org/10.1089/vbz.2009.0249 to the Americas and eastern Europe, the same manufacturer for analysis. 6. Chevalier V, Rakotondrafara T, Jourdan most countries in western Europe are The reconstituted colostrum replacer M, Heraud JM, Andriamanivo HR, Du- was tested by AGIDT (IDEXX, Bern, rand B, et al. An unexpected recurrent EBL free in accordance with European transmission of Rift Valley fever virus Union legislation; for example, Great Switzerland) at the following dilutions: in cattle in a temperate and mountainous Britain has held EBL-free status since neat (manufacturer’s guidelines), 1:2, area of Madagascar. PLoS Negl Trop Dis. 1999. EBL is notifiable to the World 1:4, and 1:8. In addition, 2 commer- 2011;5:e1423. http://dx.doi.org/10.1371/ cial ELISA tests (Institute Pourquier journal.pntd.0001423 Organisation for Animal Health (1), 7. Carroll SA, Reynes JM, Khristova ML, with disease incursion affecting inter- and IDEXX) were used over a series Andriamandimby SF, Rollin PE, Nichol national trade. Infection with BLV is of dilutions to 1:125. All serologic tests ST. Genetic evidence for Rift Valley fever life-long and persistent; the presence of were conducted according to manufac- outbreaks in Madagascar resulting from turer’s recommendations. To examine virus introductions from the East African antibodies or integrated proviral DNA mainland rather than enzootic mainte- are indicators of virus exposure. Two the samples for proviral DNA, we con- nance. J Virol. 2011;85:6162–7. http:// tests prescribed for international trade ducted PCRs to amplify a 385-bp frag- dx.doi.org/10.1128/JVI.00335-11. are the agar gel immunodiffusion test ment of the envelope gene (3). 8. Soarimalala V, Goodman SM. Les petits At the various dilutions of colos- mammifères de Madagascar. Antanana- (AGIDT) and ELISA (1); these tests rivo (Madagascar): Association Vahatra; are used widely for diagnosis (2). trum replacer, all serologic tests gave 2011. We report 5 cases that occurred in clearly positive reactions. Proviral PCR 9. Youssef BZ, Donia HA. The potential role the United Kingdom during 2009, in of the colostrum replacer also returned of Rattus rattus in enzootic cycle of Rift positive results, which were confirmed Valley fever in Egypt. 2–Application of which calves became seropositive for reverse transcriptase polymerase chain re- BLV after consuming colostrum replac- by sequencing. The resultant enve- action (RT-PCR) in blood samples of Rat- er. In Dumfriesshire, Scotland, routine lope sequence (GenBank accession tus rattus. J Egypt Public Health Assoc. serologic screening for BLV detected no. HF545344) was aligned with 23 2002;77:133–41. other sequences obtained from Gen- 10. Youssef BZ, Donia HA. The potential role seropositivity in 2 calves, which were of Rattus rattus in enzootic cycle of Rift artificial insemination bull candidates. Bank, which encompassed all known Valley fever in Egypt. 1–Detection of RVF In Newport, Wales, a BLV-seropositive BLV genotypes. Phylogenetic analysis

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 6, June 2013 1027 Article DOI: http://dx.doi.org/10.3201/eid1906.121074 Absence of Rift Valley Fever Virus in Wild Mammals, Madagascar

Technical Appendix

Technical Appendix Table. of small terrestrial animals sampled in Anjozorobe, Madagascar, October 2008 and 2009, March 2009 and 2010 Order Family Species No.

Hemicentetes semispinosus 25

Microgale dobsoni 219

M. fotsifotsy 3

M. gymnorhyncha 3

M. longicaudata/majori 8

Afrosoricida Tenrecidae M. parvula 2

M. thomasi 15

M. soricoides 61

Oryzorictes hova 38

Tenrec ecaudatus 2

Setifer setosus 2

Eliurus majori 15

E. minor 17

E. tanala 15 Nesomyidae E. grandidieri 3 Rodentia Gymnuromys roberti 11

Nesomys rufus 53

Muridae Rattus rattus 471

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