Abstract
In Madagascar, the black rat, Rattus rattus, is the main reservoir of plague (Yersinia pestis infection), a disease still responsible for hundreds of cases each year in this country. This study used experimental plague challenge to assess susceptibility in wild-caught rats to better understand how R. rattus can act as a plague reservoir. An important difference in plague resistance between rat populations from the plague focus (central highlands) and those from the plague-free zone (low altitude area) was confirmed to be a widespread phenomenon. In rats from the plague focus, we observed that sex influenced plague susceptibility, with males slightly more resistant than females. Other individual factors investigated (weight and habitat of sampling) did not affect plague resistance. When infected at high bacterial dose (more than 105 bacteria injected), rats from the plague focus died mainly within 3–5 days and produced specific antibodies, whereas after low-dose infection (< 5,000 bacteria), delayed mortality was observed and surviving seronegative rats were not uncommon. These results concerning plague resistance level and the course of infection in the black rat would contribute to a better understanding of plague circulation in Madagascar.
References
Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology and Evolution 18:589-596.
Biggins DE, Kosoy MY (2001) Influences of introduced plague on North American mammals: implications from ecology of plague in Asia. Journal of Mammalogy 82:906-916.
Boisier P, Rahalison L, Rasolomaharo M, Ratsitorahina M, Mahafaly M, Razafimahefa M, et al. (2002) Epidemiologic features of four successive annual outbreaks of bubonic plague in Mahajanga, Madagascar. Emerging Infectious Diseases 8:311-316.
Brygoo ER (1966) Epidémiologie de la peste à Madagascar. Archives de l’Institut Pasteur de Madagascar 35:9-147.
Chanteau S, Rahalison L, Ralafiarisoa L, Foulon J, Ratsitorahina M, Ratsifasoamanana L, et al. (2003) Development and testing of a rapid diagnostic test for bubonic and pneumonic plague. Lancet 361:211-216.
Clopper CJ, Pearson ES (1934) The use of confidence or fiducial limits illustrated by the case of binomial. Biometrika 26:404-413.
Davis S, Makundi RH, Machang’u RS, Leirs H (2006) Demographic and spatio-temporal variation in human plague at a persistent focus in Tanzania. Acta Tropica 100:133-141.
Dennis DT, Gage KL, Gratz N, Poland J, Tikhomirov E (1999) Plague manual: epidemiology, distribution, surveillance and control. Geneva: WHO, p 171.
Dromigny J-A (1997) Contribution à la connaissance du cycle épidémiologique de la peste à Madagascar: étude sérologique des rats et des musaraignes. Unpublished Master Report. Université Pierre et Marie Curie, Paris VI, Paris.
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17:431-449.
Duplantier J-M, Duchemin J-B, Chanteau S, Carniel E (2005) From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Veterinary Research 36:437-453.
Duplantier JM, Duchemin JB (2003) Human diseases and introduced small mammals. In: The Natural History of Madagascar, Goodman SM, Benstead JP (editors), Chicago: University of Chicago Press, pp 158-161.
Eisen RJ, Gage KL (2009) Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods. Veterinary Research 40:1–14.
Gage KL, Kosoy MY (2005) Natural history of plague: perspectives from more than a century of research. Annual Review of Entomology 50:505-528.
Gilabert A, Loiseau A, Duplantier JM, Rahelinirina S, Rahalison L, Chanteau S, et al. (2007) Genetic structure of black rat populations in a rural plague focus in Madagascar. Canadian Journal of Zoology 85:965-972.
Gratz NG (1997) The burden of rodent-borne diseases in Africa South of the Sahara. Belgian Journal of Zoology 127:71-84.
Haldane JBS (1956) The estimation and significance of the logarithm of a ratio of frequencies. Annals of Human Genetics 20:309-311.
Isaacson M, Taylor P, Arntzen L (1983) Ecology of plague in Africa: response of indigenous wild rodents to experimental plague infection. Bulletin of the World Health Organization 61:339-344.
Keeling MJ, Gilligan CA (2000) Metapopulation dynamics of bubonic plague. Nature 407:903-906.
Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826-830.
Lorange EA, Race BL, Sebbane F, Hinnebusch J (2005) Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. The Journal of Infectious Diseases 191:1907-1912.
Meerburg BG, Singleton G, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35:221–270.
Migliani R, Chanteau S, Rahalison L, Ratsitorahina M, Boutin JP, Ratsifasoamanana L, et al. (2006) Epidemiological trends for human plague in Madagascar during the second half of the 20th century: a survey of 20 900 notified cases. Tropical Medicine and International Health 11:1228-1237.
Mills JN, Yates TL, Childs JE, Parmenter RR, Ksiazek TG, Rollin PE, et al. (1995) Guidelines for working with rodents potentially infected with hantavirus. Journal of Mammalogy 76:716-722.
Perry RD, Fetherston JD (1997) Yersinia pestis: etiologic agent of plague. Clinical Microbiology Reviews 10:35-66.
Prentice MB, Rahalison L (2007) Plague. Lancet 369:1196-1207.
Quan SF, Kartman L (1962) Ecological studies of wild rodent plague in the San Francisco Bay area of California. VIII. Susceptibility of wild rodents to experimental plague infection. Zoonoses Research 1:121-144.
Quan SF, Wheeler CM, Goldenberg MI, Kartman L (1965) The susceptibility of Rattus species from two areas of Hawaii to infection with Pasteurella pestis. American Journal of Tropical Medicine and Hygiene 14:638-642.
Rahalison L, Ranjalahy M, Duplantier J-M, Duchemin J-B, Ravelosaona J, Ratsifasoamanana L, et al. (2003) Susceptibility to plague of the rodents in Antananarivo, Madagascar. In: The Genus Yersinia, New York: Kluwer Academic/Plenum Publishers.
Rahelinirina S (2009) Le risque pesteux dans les foyers ruraux du Moyen-Ouest malgache: déplacements et structuration des populations de rats noirs de l’échelle de l’habitat à celle du paysage. Thesis. Antananarivo, Antananarivo.
Rasoamanana B, Leroy F, Boisier P, Rasolomaharo M, Buchy P, Carniel E, et al. (1997) Field evaluation of an immunoglobulin G anti-F1 enzyme-linked immunosorbent assay for serodiagnosis of human plague in Madagascar. Clinical and Diagnostic Laboratory Immunology 4:587-591.
Sebbane F, Gardner D, Long D, Gowen BB, Hinnebusch J (2005) Kinetics of disease progression and host response in a rat model of bubonic plague. American Journal of Pathology 166:1427-1439.
Shepherd AJ, Leman PA, Hummitzsch DE (1986) Experimental plague infection in South African wild rodents. Journal of Hygiene (Cambridge) 96:171-183.
Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, et al. (2008) Plague: past, present, and future. Plos Medicine 5:9-13.
Thomas RE, Barnes AM, Quan TJ, Beard ML, Carter LG, Hopia CE (1988) Susceptibility to Yersinia pestis in the northern grasshopper mouse (Onychomys leucogaster). Journal of Wildlife Diseases 24:327-333.
Tollenaere C, Brouat C, Duplantier JM, Rahalison L, Rahelinirina S, Pascal M, et al. (2010) Phylogeography of the introduced species Rattus rattus in the western Indian Ocean, with special emphasis on the colonization history of Madagascar. Journal of Biogeography 37:398-410.
Twigg GI (1978) The role of rodents in plague dissemination: a worldwide review. Mammal Review 8:77-110.
Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics 32:569-577.
World Health Organization (2003) Human plague in 2000–2001. Weekly Epidemiological Record 78:130-135.
Acknowledgments
We are grateful to all staff of the Plague laboratory of the Institut Pasteur de Madagascar for assistance during the fieldwork, experimentation, and serological analysis. We thank Florent Sebbane for helpful comments on earlier versions of the manuscript, as well as Nathalie Charbonnel for constructive discussions. Funding was provided by the IRD (Institut de Recherche pour le Développement), the IPM (Institut Pasteur de Madagascar) and an ANR-SEST (Agence Nationale pour la Recherche, Santé - Environnement et Santé - Travail) program on plague diffusion.
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Tollenaere, C., Rahalison, L., Ranjalahy, M. et al. Susceptibility to Yersinia pestis Experimental Infection in Wild Rattus rattus, Reservoir of Plague in Madagascar. EcoHealth 7, 242–247 (2010). https://doi.org/10.1007/s10393-010-0312-3
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DOI: https://doi.org/10.1007/s10393-010-0312-3