Volume 82, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



A natural focus of plague exists in the Western Usambara Mountains of Tanzania. Despite intense research, questions remain as to why and how plague emerges repeatedly in the same suite of villages. We used human plague incidence data for 1986–2003 in an ecological-niche modeling framework to explore the geographic distribution and ecology of human plague. Our analyses indicate that plague occurrence is related directly to landscape-scale environmental features, yielding a predictive understanding of one set of environmental factors affecting plague transmission in East Africa. Although many environmental variables contribute significantly to these models, the most important are elevation and Enhanced Vegetation Index derivatives. Projections of these models across broader regions predict only 15.5% (under a majority-rule threshold) or 31,997 km of East Africa as suitable for plague transmission, but they successfully anticipate most known foci in the region, making possible the development of a risk map of plague.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Gage KL, Kosoy MY, , 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505528.[Crossref] [Google Scholar]
  2. Dennis DT, Gage KL, Gratz NG, Poland JD, Tikhomirov E, , 1999. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization. [Google Scholar]
  3. Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, Gage KL, Leirs H, Rahalison L, , 2008. Plague: past, present, and future. PLoS Med 5: e3.[Crossref] [Google Scholar]
  4. Neerinckx S, Bertherat E, Leirs H, , 2010. Historical plague occurrences in Africa–an overview from 1877 to 2008. Trans R Soc Trop Med Hyg 104: 97103.[Crossref] [Google Scholar]
  5. WHO, 2008. Epidemic and pandemic alert and response. Proceedings of the Interregional Meeting on Prevention and Control of Plague, April 7–11, 2006; Antananarivo, Madagascar. [Google Scholar]
  6. Laudisoit A, Leirs H, Makundi RH, Van Dongen S, Davis S, Neerinckx S, Deckers J, Libois R, , 2007. Plague and the human flea, Tanzania. Emerg Infect Dis 13: 687693.[Crossref] [Google Scholar]
  7. Misonne X, , 1920. Les rongeurs des foyers de peste congolais. Ann Soc Belg Med Trop 39: 437493. [Google Scholar]
  8. Kilonzo BS, Mvena ZS, Machangu RS, Mbise TJ, , 1997. Preliminary observations on factors responsible for long persistence and continued outbreaks of plague in Lushoto district, Tanzania. Acta Trop 68: 215227.[Crossref] [Google Scholar]
  9. Nakazawa Y, Williams R, Peterson AT, Mead P, Staples JE, Gage K, , 2007. Climate change effects on plague and tularemia in the United States. Vector Borne Zoonotic Dis 7: 529540.[Crossref] [Google Scholar]
  10. Ben Ari T, Gershunov A, Gage KL, Snall T, Ettestad P, Kausrud KL, Stenseth NC, , 2008. Human plague in the USA: the importance of regional and local climate. Biol Lett 4: 737740.[Crossref] [Google Scholar]
  11. Eisen RJ, Reynolds PJ, Ettestad P, Brown T, Enscore RE, Biggerstaff BJ, Cheek J, Bueno R, Targhetta J, Montenieri JA, Gage KL, , 2007. Residence-linked human plague in New Mexico: a habitat-suitability model. Am J Trop Med Hyg 77: 121125. [Google Scholar]
  12. Neerinckx SB, Peterson AT, Gulinck H, Deckers J, Leirs H, , 2008. Geographic distribution and ecological niche of plague in sub-Saharan Africa. Int J Health Geogr 7: 54.[Crossref] [Google Scholar]
  13. Winters AM, Staples JE, Ogen-Odoi A, Mead PS, Griffith K, Owor N, Babi N, Enscore RE, Eisen L, Gage KL, Eisen RJ, , 2009. Spatial risk models for human plague in the West Nile region of Uganda. Am J Trop Med Hyg 80: 10141022. [Google Scholar]
  14. Kilonzo BS, Mhina JI, , 1982. The first outbreak of human plague in Lushoto district, north-east Tanzania. Trans R Soc Trop Med Hyg 76: 172177.[Crossref] [Google Scholar]
  15. 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 Trop 100: 133141.[Crossref] [Google Scholar]
  16. Laudisoit A, Neerinckx S, Makundi RH, Leirs H, Krasnov B, , 2009. Are local plague endemicity and ecological characteristics of vectors and reservoirs related? A case study in north-east Tanzania. Curr Zool 55: 199211. [Google Scholar]
  17. Makundi RH, Kilonzo BS, Massawe AW, , 2003. Interaction between rodent species in agro-forestry habitats in the western Usambara Mountains, north-eastern Tanzania, and its potential for plague transmission to humans. Singleton GR, ed. Rats, Mice and People: Rodent Biology and Management. Canberra: Australian Centre for International Agricultural Research, 2024. [Google Scholar]
  18. Lyamuya EF, Nyanda P, Mohammedali H, Mhalu FS, , 1992. Laboratory studies on Yersinia pestis during the 1991 outbreak of plague in Lushoto, Tanzania. J Trop Med Hyg 95: 335338. [Google Scholar]
  19. Kilonzo BS, , 2000. Demonstration of Yersinia Pestis DNA and Antibodies in Humans and Animals in Lushoto District: Need to Improve Diagnostic Services. Moshi, Tanzania Tanzania Public Health Association Publications. Proceedings of the 19th Annual Scientific Conference of the Tanzania Public Health Association, November 20–24, 2000, pp. 172 176. [Google Scholar]
  20. SMRT, 2008 90 m digital elevation data. Available at: http://srtm.csi.cgiar.org/. [Google Scholar]
  21. Soberón J, Peterson AT, , 2005. Interpretation of models of fundamental ecological niches and species' distributional areas. Biodivers Inf 2: 110. [Google Scholar]
  22. Peterson AT, , 2008. Biogeography of diseases: a framework for analysis. Naturwissenschaften 95: 483491.[Crossref] [Google Scholar]
  23. Stockwell D, Peters D, , 1999. The GARP modeling system: problems and solutions to automated spatial prediction. Int J Geogr Inf Sci 13: 143158.[Crossref] [Google Scholar]
  24. Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE, , 2006. Novel methods improve prediction of species' distributions from occurrence data. Ecography 29: 129151.[Crossref] [Google Scholar]
  25. Peterson AT, Papes M, Eaton M, , 2007. Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30: 550560.[Crossref] [Google Scholar]
  26. Peterson AT, Papes M, Soberon J, , 2008. Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecol Modell 213: 6372.[Crossref] [Google Scholar]
  27. Peterson AT, Bauer JT, Mills JN, , 2004. Ecologic and geographic distribution of filovirus disease. Emerg Infect Dis 10: 4047.[Crossref] [Google Scholar]
  28. Peterson AT, Sánchez-Cordero V, Beard CB, Ramsey JM, , 2002. Ecologic niche modeling and potential reservoirs for Chagas disease, Mexico. Emerg Infect Dis 8: 662667.[Crossref] [Google Scholar]
  29. Peterson AT, Shaw J, , 2003. Lutzomyia vectors for cutaneous leishmaniasis in Southern Brazil: ecological niche models, predicted geographic distributions, and climate change effects. Int J Parasitol 33: 919931.[Crossref] [Google Scholar]
  30. Anderson RP, Lew D, Peterson AT, , 2003. Evaluating predictive models of species' distributions: criteria for selecting optimal models. Ecol Modell 162: 211232.[Crossref] [Google Scholar]
  31. Pearson RG, Raxworthy CJ, Nakamura M, Peterson AT, , 2007. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34: 102117.[Crossref] [Google Scholar]
  32. Peterson AT, Cohoon KP, , 1999. Sensitivity of distributional prediction algorithms to geographic data completeness. Ecol Modell 117: 159164.[Crossref] [Google Scholar]
  33. Phillips SJ, Anderson RP, Schapire RE, , 2006. Maximum entropy modeling of species geographic distributions. Ecol Modell 190: 231259.[Crossref] [Google Scholar]
  34. Roberts JI, , 1935. The endemicity of plague in East Africa. East Afr Med J 12: 200219. [Google Scholar]
  35. Davis DH, , 1953. Plague in Africa from 1935 to 1949; a survey of wild rodents in African territories. Bull World Health Organ 9: 665700. [Google Scholar]
  36. Orochi Orach S, , 2002. Plague Outbreaks: the Gender and Age Perspective in Okoro County, Nebbi District, Uganda. Nebbe, Uganda: Agency for Accelerated Regional Development. [Google Scholar]
  37. Migliani R, Chanteau S, Rahalison L, Ratsitorahina M, Boutin JP, Ratsifasoamanana L, Roux J, , 2006. Epidemiological trends for human plague in Madagascar during the second half of the 20th century: a survey of 20,900 notified cases. Trop Med Int Health 11: 12281237.[Crossref] [Google Scholar]
  38. Eisen RJ, Enscore RE, Biggerstaff BJ, Reynolds PJ, Ettestad P, Brown T, Pape J, Tanda D, Levy CE, Engelthaler DM, Cheek J, Bueno R, Targhetta J, Montenieri JA, Gage KL, , 2007. Human plague in the southwestern United States, 1957–2004: spatial models of elevated risk of human exposure to Yersinia pestis . J Med Entomol 44: 530537.[Crossref] [Google Scholar]
  39. Gage KL, Burkot TR, Eisen RJ, Hayes EB, , 2008. Climate and vectorborne diseases. Am J Prev Med 35: 436450.[Crossref] [Google Scholar]
  40. Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV, , 2001. Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38: 629637.[Crossref] [Google Scholar]
  41. Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RF, Reynolds PJ, Engelthaler DM, Levy CE, Parmenter RR, Montenieri JA, Cheek JE, Grinnell RK, Ettestad PJ, Gage KL, , 2002. Modeling relationships between climate and the frequency of human plague cases in the southwestern United States, 1960–1997. Am J Trop Med Hyg 66: 186196. [Google Scholar]
  42. Kausrud KL, Viljugrein H, Frigessi A, Begon M, Davis S, Leirs H, Dubyanskiy V, Stenseth NC, , 2007. Climatically driven synchrony of gerbil populations allows large-scale plague outbreaks. Proc R Soc Lond B Biol Sci 274: 19631969.[Crossref] [Google Scholar]
  43. Parmenter RR, Yadav EP, Parmenter CA, Ettestad P, Gage KL, , 1999. Incidence of plague associated with increased winter-spring precipitation in New Mexico. Am J Trop Med Hyg 61: 814821. [Google Scholar]
  44. Stenseth NC, Samia NI, Viljugrein H, Kausrud KL, Begon M, Davis S, Leirs H, Dubyanskiy VM, Esper J, Ageyev VS, Klassovskiy NL, Pole SB, Chan KS, , 2006. Plague dynamics are driven by climate variation. Proc Natl Acad Sci USA 103: 1311013115.[Crossref] [Google Scholar]
  45. Peterson AT, , 2008. Improving methods for reporting spatial epidemiologic data. Emerg Infect Dis 14: 13351336.[Crossref] [Google Scholar]
  46. Eisen L, Eisen RJ, , 2007. Need for improved methods to collect and present spatial epidemiologic data for vectorborne diseases. Emerg Infect Dis 13: 18161820.[Crossref] [Google Scholar]

Data & Media loading...

  • Received : 27 Jul 2009
  • Accepted : 11 Dec 2009
  • Published online : 05 Mar 2010

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error