LETTERS pathogens intrusion. Blackleg (1970, Author affi liations: Centre for Scientifi c 8. Andriamandimby SF, Randrianarivo- 1995) and the contagious ecthyma Research and Intelligence on Emerging Solofoniaina AE, Jeanmaire EM, Ra- vololomanana L, Razafi manantsoa LT, Infectious Diseases in the Indian Ocean, (1999) were probably introduced Rakotojoelinandrasana T, et al. Rift Val- into the country by live ruminants Sainte-Clotilde, La Réunion Island, France ley fever during rainy seasons, Madagas- imported from Madagascar (9). Since (M. Roger, E. Cardinale); French Agricultural car, 2008 and 2009. Emerg Infect Dis. 2002, importation of live Research Center for International 2010;16:963–70. 9. Timmermans E, Ruppol P, Saido A, On- Development (CIRAD), Montpellier, France from Tanzania has been common, clin M. Infl uence du marché international increasing the risk of introducing (M. Roger, S. Girard, C. Cetre-Sossah, E. et des stratégies d’approvisionnement en continental pathogens or vectors Cardinale); CIRAD, Mamoudzou, Mayotte viande sur les risques d’importation de as illustrated with outbreaks of (S. Girard); Vice-President, Ministry of maladies. Le cas de l’ecthyma en Répub- lique Fédérale Islamique des Comores. Agriculture, Fisheries, Environment, East Coast fever in 2003 and 2004 2000 [cited 2010 Dec 1]. http://www.vsf- in Grande Comore (10). RVFV Industry, Energy and Handicraft, Moroni, belgium.org/docs/ecthyma_contagieux. circulation presented in this study Republic of Comoros (A. Faharoudine, M. pdf is another example of the exposure Halifa); and Institut Pasteur, Paris, France 10. De Deken R, Martin V, Saido A, Mad- der M, Brandt J, Geysen D. An outbreak (M. Bouloy) of the Republic of Comoros to of East Coast fever on the Comoros: a emerging pathogens and potentially DOI: 10.3201/eid1707.102031 consequence of the import of immun- bears major consequences for the ised cattle from Tanzania? Vet Parasitol. local economy and for public health. 2007;143:245–53. doi:10.1016/j.vetpar. References 2006.08.018 The improvement of the Comorian veterinary services and the setting up 1. Turell MJ, Linthicum KJ, Patrican LA, Address for correspondence: Matthieu Roger, Davies FG, Kairo A, Bailey CL. Vec- of surveillance programs are essential CRVOI–CIRAD UMR 15, CYROI Technopole to limit the risk of introducing tor competence of selected African mosquito (Diptera: Culicidae) species 2 Rue Maxime Rivière Sainte Clotilde 97490, devastating diseases in the area. for Rift Valley fever virus. J Med Ento- La Réunion, France; email: matthieu.roger@ mol. 2008;45:102–8. doi:10.1603/0022- cirad.fr Acknowledgments 2585(2008)45[102:VCOSAM]2.0.CO;2 2. Swanepoel R, Coetzer JAW. Rift Valley We thank the vice president in fever. In: Coetzer JAW, Thomson GR, charge of the Ministry of Agriculture, Tustin RC, editors. Infectious diseases of Fisheries, Environment, Industry, Energy, livestock. Oxford (UK): Oxford Univer- and Handicraft for providing logistical sity Press; 2004. p. 1037–70. 3. Paweska JT, Mortimer E, Leman PA, assistance and laboratory facilities and all Swanepoel R. An inhibition enzyme- herders and their representatives from the linked immunosorbent assay for the de- Comorian Farmers National Federation for tection of antibody to Rift Valley fever Yersinia pestis in their collaboration. We are also grateful to virus in humans, domestic and wild rumi- nants. J Virol Methods. 2005;127:10–8. Small , the Departmental Veterinary Laboratory doi:10.1016/j.jviromet.2005.02.008 Mongolia at Mamoudzou, Mayotte, particularly 4. World Organisation for Health. Stéphanie Maeder and Abdou Achirafi for Rift Valley fever. In: OIE manual of di- To the Editor: Plague is known performing ELISA. agnostic tests and vaccines for terrestrial animals, vol. 1. 5th ed. Paris: Offi ce Inter- to be endemic in several areas of This work was supported with Fonds national des Epizooties; 2004. p. 185–94 Mongolia, but transmission to humans 5. Digoutte JP, Calvo-Wilson MA, Mondo Européens de Développement Régional seems to play only a minor role M, Traoré-Laminzana M, Adam F. Con- because the number of recognized funds from the European Union within tinuous cell lines and immune ascitic fl u- the Project “Programme de Coopération ids pools in arbovirus detection. Res Virol. cases is relatively low (Figure) (1). Scientifi que sur les Maladies Animales 1992;143:417–22. doi:10.1016/S0923- The fi rst human cases in Mongolia 2516(06)80135-4 Emergentes dans l’Océan Indien.” were reported to the World Health 6. Outbreaks of Rift Valley fever in Kenya, Organization in 1980, and <20 human Somalia and United Republic of Tanzania, cases have occurred each year since Matthieu Roger, December 2006–April 2007. Wkly Epide- miol Rec. 2007;82:169–78. then (2). However, human plague Sébastien Girard, 7. Sissoko D, Giry C, Gabrie P, Tarantola was fi rst reported in 1897 (3), such Abdourahime Faharoudine, A, Pettinelli F, Collet L, et al. Rift Val- infections have been documented ley fever, Mayotte, 2007–2008. Emerg Mohamed Halifa, since the 1940s, and Yersinia pestis Michèle Bouloy, Infect Dis. 2009;15:568–70. doi:10.3201/ eid1504.081045 can be found in many provinces of Catherine Cetre-Sossah, Mongolia (Figure; T. Damindorj, pers. and Eric Cardinale comm.) (3,4). The most common source of

1320 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 7, July 2011 LETTERS human plague in Mongolia is contact of laboratory rodents tested negative. of the Yunnan–Guangdong–Fujian with and consumption of the marmot Identifi cation of several host species provinces in the People’s Republic of (Marmota sibirica) (1). Moreover, was supported by partial sequencing China (8). the great gerbil (Rhombomys opimus) of the cytochrome b gene (7). The Detection of Y. pestis–specifi c and the Mongolian gerbil (Meriones animals tested positive for plague DNA in wild rodents has been unguiculatus) are suspected of were gerbils (Meriones sp., 1; M. described. For instance, a wild being enzootic reservoirs. Although unguiculatus, 2; Rhombomys opimus, community in the eastern Sierra small rodents are also assumed to be 2) and ( sibirica, 1; Nevada mountains in the United reservoirs of Y. pestis, the interaction Cardiocranius paradoxus, 1). States was screened for plague by pla- of individual or fl eas of The identity of the 230-bp pla specifi c real-time PCR; of 89 rodents, particular species in the infectious PCR fragment was confi rmed by DNA 1 chipmunk (1.1%) had positive cycle and the dynamics of an epizootic sequencing, showing 100% similarity results (9). are not yet clear (5). In a retrospective to the pla gene sequences deposited The permanent presence of Y. study, we screened tissue samples in the European Molecular Biology pestis in rodent communities in North from small rodents for Y. pestis DNA Laboratory nucleotide database. America has led to smaller and more to investigate the prevalence of Y. Molecular subtyping of the 7 pla- distant-living colonies of prairie dogs pestis in a potential enzootic reservoir. positive DNA samples was attempted (10). Strikingly, in the present study, During the course of zoologic by clustered regularly interspaced >5% of the screened rodents were investigations in Mongolia during short palindromic repeats analysis, found to carry Y. pestis DNA. This 2002, 2005, and 2006, 133 rodents targeting the 3 loci YPa, YPb, and YPc, high number was unexpected for the (gerbils, jerboas, and squirrels) were respectively. Also included was DNA investigated areas, which have had a trapped by standard methods (5), originating from the above-mentioned low level of plague activity (Figure). dissected, and cataloged (Figure). negative control tissues. However, To our knowledge, Y. pestis has also Documentation included species, only 1 sample from the spleen of a not yet been reported in Manlai Sum sex, date and location of trapping, M. unguiculatus gerbil found the YPb (district) in the Umnugovi Aimag animal size (weight, length) and organ locus, which then was sequenced, and (subdivision) (Figure) (2–4) nor has dimensions, as well as all pathologic resulted in the spacer signature b1-b2- the presence of Y. pestis DNA in a fi ndings. Although the trapped animals b3-b4-b5′. This signature is known Cardiocranius paradoxus . showed a high degree of parasitic from a Y. pestis biovar, Orientalis, Our fi ndings emphasize that infestation, signs of a severe infectious that has been isolated from Rattus rodents play a role as zoonotic disease were not observed. After the fl avipectus rats in the plague focus reservoirs of Y. pestis in Mongolia and dissection of animals, samples were conserved in 70% ethanol. Subsequently, total DNA was extracted from alcohol-conserved spleen and liver tissue of 133 animals by using QIAamp DNA Mini Kit (QIAGEN, Hamburg, Germany), according to the manufacturer’s instructions. Screening was performed by using a real-time PCR targeting the pla gene of Y. pestis pPCP1, including a PCR inhibition control, as described (6). As positive control, the Y. pestis vaccine strain EV76 was used. As negative controls, we included tissues Figure. Yersina pestis in rodents in Mongolia. Shaded areas show the known distribution of of 53 laboratory rodents, which were enzootic plague in Mongolia during 1948–1999 (V. Batsaikhan, J. Myagmar, G. Bolormaa, processed analogs, beginning with National Center for Infectious Diseases with Natural Foci, Ulanbaatar, Mongolia; pers. DNA extraction. comm.). The following 133 rodents were investigated: gerbils (Meriones unguiculatus, In the real-time PCR targeting the 61; M. meridianus, 25; Rhombomys opimus, 17); jerboas (Allactaga sibirica, 6; Stylodipus pla gene, 7 (5.3%) of 133 spleen tissue telum, 1; Dipus sagitta, 4; Cardiocranius paradoxus, 1), and squirrels (Spermophilus alaschanicus, 1; Citellus dauricus, 1). Plague-positive trapping loci were the following: samples were positive for Y. pestis. In 1, Tuv Aimag, Bayanunjuul Sum; 2–4, Umnugovi Aimag (2, Nomgon Sum; 3, Bayandalai contrast, all liver samples and samples Sum; 4, Manlai Sum). Y. pestis DNA was found in 7 rodents (gerbils and jerboas).

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 7, July 2011 1321 LETTERS that the actual prevalence of plague 4. Anisimov AP, Lindler LE, Pier GB. In- Typhoon-related seems to be underestimated. The traspecifi c diversity of Yersinia pestis. Clin Microbiol Rev. 2004;17:434–64. Leptospirosis and low population density in Mongolia doi:10.1128/CMR.17.2.434-464.2004 explains the low amount of illness 5. Brinkerhoff RJ, Collinge SK, Ray C, Melioidosis, in humans. Further investigations Gage KL. Rodent and fl ea abundance fail Taiwan, 2009 should include the screening of to predict a plague epizootic in black- tailed prairie dogs. Vector Borne Zoo- rodent populations near the plague- notic Dis. 2010;10:47–52. doi:10.1089/ To the Editor: Global climatic positive loci. In addition, fl eas and vbz.2009.0044 changes have resulted in more other parasites (and also predators of 6. Tomaso H, Reisinger EC, Al Dahouk S, natural disasters worldwide. These small mammals) should be studied. Frangoulidis D, Rakin A, Landt O, et al. natural disasters can then cause Rapid detection of Yersinia pestis with Mongolia is a key area of plague multiplex real-time PCR assays using fl u- outbreaks of emerging infectious genesis and therefore is an ideal orescent hybridisation probes. FEMS Im- diseases, including leptospirosis location for more detailed study of munol Med Microbiol. 2003;38:117–26. and melioidosis (1–7). In 2009, the the role of rodents as epizootic and doi:10.1016/S0928-8244(03)00184-6 moderate-strength Typhoon Morakot, 7. Essbauer S, Schmidt J, Conraths FJ, Fried- enzootic reservoirs of Y. pestis. rich R, Koch J, Hautmann W, et al. A new with a maximum cumulative rainfall Puumala hantavirus subtype in rodents as- amount up to 3,059.5 mm, damaged Acknowledgments sociated with an outbreak of nephropathia Taiwan. After this natural disaster, epidemica in south-east Germany in 2004. We thank Gabriele Echle, Philipp unusual epidemics of leptospirosis Epidemiol Infect. 2006;134:1333–44. Vette, and Astrid Thomas for excellent doi:10.1017/S0950268806006170 and melioidosis occurred. The main technical assistance and Gilles Vergnaud 8. Cui Y, Li Y, Gorgé O, Platonov ME, Yan Y, objective of this study was to clarify for providing access to the CRISPR Guo Z, et al. Insight into microevolution whether these epidemics have resulted of Yersinia pestis by clustered regularly database (http://crispr.u-psud.fr/crispr). from this natural disaster. interspaced short palindromic repeats. PLoS ONE. 2008;3:e2652. doi:10.1371/ Information about past typhoons that affected Taiwan was collected Julia M. Riehm, journal.pone.0002652 9. Adjemian JZ, Adjemian MK, Foley P, from the website of the Taiwan Damdindorj Tserennorov, Chomel BB, Kasten RW, Foley JE. Evi- Meteorological Bureau (http:// Daniel Kiefer, Ingo W. Stuermer, dence of multiple zoonotic agents in a photino.cwb.gov.tw/tyweb/mainpage. Herbert Tomaso, Lothar Zöller, wild rodent community in the eastern htm; www.cwb.gov.tw) during Dashdavaa Otgonbaatar, Sierra Nevada. J Wildl Dis. 2008;44:737– 42. January–August, 2009. The infl uential and Holger C. Scholz 10. Cully JF, Johnson TL, Collinge SK, Ray period of Morakot was in the 32nd Author affi liations: Bundeswehr Institute C. Disease limits populations: plague and week (August 5–August 10) in 2009. of Microbiology, Munich, Germany (J.M. black-tailed prairie dogs. Vector Borne Zoonotic Dis. 2010;10:7–15. doi:10.1089/ To evaluate the effects of this specifi c Riehm, D. Kiefer, L. Zöller, H.C. Scholz); vbz.2009.0045 natural disaster, we divided the period National Center for Infectious Diseases into 2 intervals for analysis. The early with Natural Foci, Ulanbaatar, Mongolia Address for correspondence: Julia M. Riehm, period (before the typhoon) was from (D. Tserennorov, D. Otgonbaatar); Institute Bundeswehr Institute of Microbiology, the 28th through the 32nd weeks, and for Zoology and Anthropology, Goettingen, Neuherbergstr. 11, 80939 Munich, Germany; the latter period (after the typhoon) Germany (I.W. Stuermer); and Friedrich- email: [email protected] was from the 33th through the 37th Loeffl er-Institut, Jena, Germany (H. weeks in 2009. Information regarding Tomaso) 16 typhoons from 2000 through 2009 DOI: 10.3201/eid1707.100740 was further collected to evaluate effects of typhoon level, rainfall References level, and maximum cumulative rainfall amounts on case numbers of 1. Ebright JR, Altantsetseg T, Oyungerei R. Emerging infectious diseases in Mongo- leptospirosis and melioidosis after a lia. Emerg Infect Dis. 2003;9:1509–15. typhoon. 2. World Health Organization. Plague man- The historical records of numbers ual: epidemiology, distribution, surveil- of leptospirosis and melioidosis cases lance and control. Geneva: The Organiza- tion; 1999. for analysis were obtained from the 3. Galdan B, Baatar U, Molotov B, Dash- database collected weekly by the davaa O. Plague in Mongolia. Vector Centers for Disease Control, Taiwan. Borne Zoonotic Dis. 2010;10:69–75. The information was referred to the doi:10.1089/vbz.2009.0047 website of the Taiwan Center for

1322 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 7, July 2011