Volume 86, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



East Africa has been identified as a region where vector-borne and zoonotic diseases are most likely to emerge or re-emerge and where morbidity and mortality from these diseases is significant. Understanding when and where humans are most likely to be exposed to vector-borne and zoonotic disease agents in this region can aid in targeting limited prevention and control resources. Often, spatial and temporal distributions of vectors and vector-borne disease agents are predictable based on climatic variables. However, because of coarse meteorological observation networks, appropriately scaled and accurate climate data are often lacking for Africa. Here, we use a recently developed 10-year gridded meteorological dataset from the Advanced Weather Research and Forecasting Model to identify climatic variables predictive of the spatial distribution of human plague cases in the West Nile region of Uganda. Our logistic regression model revealed that within high elevation sites (above 1,300 m), plague risk was positively associated with rainfall during the months of February, October, and November and negatively associated with rainfall during the month of June. These findings suggest that areas that receive increased but not continuous rainfall provide ecologically conducive conditions for transmission in this region. This study serves as a foundation for similar modeling efforts of other vector-borne and zoonotic disease in regions with sparse observational meteorologic networks.


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  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. Eisen RJ, Gage KL, , 2009. Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods. Vet Res 40: 1.[Crossref] [Google Scholar]
  3. Dennis DT, Chow CC, , 2004. Plague. Pediatr Infect Dis J 23: 6971.[Crossref] [Google Scholar]
  4. Crook LD, Tempest B, , 1992. Plague. A clinical review of 27 cases. Arch Intern Med 152: 12531256.[Crossref] [Google Scholar]
  5. Poland JD, Dennis DT, , 1999. Diagnosis and clinical manifestations. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization, 4354. [Google Scholar]
  6. Neerinckx S, Bertherat E, Leirs H, , 2010. Human plague occurrences in Africa: an overview from 1877 to 2008. Trans R Soc Trop Med Hyg 104: 97103.[Crossref] [Google Scholar]
  7. 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]
  8. WHO, 2005. Outbreak news index 2005. Wkly Epidemiol Rec 80: 433440. [Google Scholar]
  9. WHO, 2009. Human plague: review of regional morbidity and mortality, 2004–2009. Wkly Epidemiol Rec 85: 4045. [Google Scholar]
  10. Kilonzo BS, , 1999. Plague epidemiology and control in eastern and southern Africa during the period 1978 to 1997. Cent Afr J Med 45: 7076. [Google Scholar]
  11. Eisen RJ, Griffith KS, Borchert JN, MacMillan K, Apangu T, Owor N, Acayo S, Acidri R, Zielinski-Gutierrez E, Winters AM, Enscore RE, Schriefer ME, Beard CB, Gage KL, Mead PS, , 2010. Assessing human risk of exposure to plague bacteria in northwestern Uganda based on remotely sensed predictors. Am J Trop Med Hyg 82: 904911.[Crossref] [Google Scholar]
  12. 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]
  13. MacMillan K, Enscore RE, Ogen-Odoi A, Borchert JN, Babi N, Amatre G, Atiku LA, Mead PS, Gage KL, Eisen RJ, , 2011. Landscape and residential variables associated with plague-endemic villages in the West Nile region of Uganda. Am J Trop Med Hyg 84: 435442.[Crossref] [Google Scholar]
  14. Eisen RJ, Borchert JN, Holmes JL, Amatre G, Van Wyk K, Enscore RE, Babi N, Atiku LA, Wilder AP, Vetter SM, Bearden SW, Montenieri JA, Gage KL, , 2008. Early-phase transmission of Yersinia pestis by cat fleas (Ctenocephalides felis) and their potential role as vectors in a plague-endemic region of Uganda. Am J Trop Med Hyg 78: 949956. [Google Scholar]
  15. 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]
  16. Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RE, 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]
  17. Davis S, Calvet E, Leirs H, , 2005. Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector Borne Zoonotic Dis 5: 305314.[Crossref] [Google Scholar]
  18. 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 Biol Sci 274: 19631969.[Crossref] [Google Scholar]
  19. Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JF, Gage KL, Kosoy M, Loye JE, Martin A, , 2005. Testing the generality of the tropic-cascade model for plague. EcoHealth 2: 102112.[Crossref] [Google Scholar]
  20. Mann JM, Martone WJ, Boyce JM, Kaufmann AF, Barnes AM, Weber NS, , 1979. Endemic human plague in New Mexico: risk factors associated with infection. J Infect Dis 140: 397401.[Crossref] [Google Scholar]
  21. Akiev AK, , 1982. Epidemiology and incidence of plague in the world, 1958–79. Bull World Health Organ 60: 165169. [Google Scholar]
  22. Gratz N, , 1999. Control of plague transmission. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization, 97134. [Google Scholar]
  23. Cavanaugh DC, Marshall JD, Jr, 1972. The influence of climate on the seasonal prevalence of plague in the Republic of Vietnam. J Wildl Dis 8: 8594.[Crossref] [Google Scholar]
  24. Gage KL, Burkot TR, Eisen RJ, Hayes EB, , 2008. Climate and vector-borne diseases. Am J Prev Med 35: 436450.[Crossref] [Google Scholar]
  25. Davis S, Begon M, De Bruyn L, Ageyev VS, Klassovskiy NL, Pole SB, Viljugrein H, Stenseth NC, Leirs H, , 2004. Predictive thresholds for plague in Kazakhstan. Science 304: 736738.[Crossref] [Google Scholar]
  26. Davis S, Trapman P, Leirs H, Begon M, Heesterbeek JA, , 2008. The abundance threshold for plague as a critical percolation phenomenon. Nature 454: 634637.[Crossref] [Google Scholar]
  27. Hirst LF, , 1953. The Conquest of Plague. Oxford, UK: Clarendon Press, 478. [Google Scholar]
  28. Krasnov BR, Khokhlova IS, , 2001. The effect of behavioral interactions on the transfer of fleas (Siphonaptera) between two rodent species. J Vector Ecol 26: 181190. [Google Scholar]
  29. Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R, , 2006. Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia 149: 474481.[Crossref] [Google Scholar]
  30. Brown HE, Ettestad P, Reynolds PJ, Brown TL, Hatton ES, Holmes JL, Glass GE, Gage KL, Eisen RJ, , 2010. Climatic predictors of the intra- and inter-annual distributions of plague cases in New Mexico based on 29 years of animal-based surveillance data. Am J Trop Med Hyg 82: 95102.[Crossref] [Google Scholar]
  31. Ari TB, Gershunov A, Tristan R, Cazelles B, Gage K, Stenseth NC, , 2010. Interannual variability of human plague occurrence in the Western United States explained by tropical and North Pacific Ocean climate variability. Am J Trop Med Hyg 83: 624632.[Crossref] [Google Scholar]
  32. Ari TB, 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]
  33. Amatre G, Babi N, Enscore RE, Ogen-Odoi A, Atiku LA, Akol A, Gage KL, Eisen RJ, , 2009. Flea diversity and infestation prevalence on rodents in a plague-endemic region of Uganda. Am J Trop Med Hyg 81: 718724.[Crossref] [Google Scholar]
  34. Chu MC, , 2000. Laboratory Training Manual of Plague Diagnostic Tests. Atlanta, GA: Centers for Disease Control and Prevention and Geneva: World Health Organization. [Google Scholar]
  35. Skamarock WC, Klemp JB, , 2008. A time-split nonhydrostatic atmospheric model for weather research and forecasting applications. J Comput Phys 227: 34653485.[Crossref] [Google Scholar]
  36. Chen F, Dudhia J, , 2001. Coupling an advanced land surface-hydrology model with the Penn State-NCAR MM5 modeling system. Part I: Model implementation and sensitivity. Mon Weather Rev 129: 569585.[Crossref] [Google Scholar]
  37. Kanamitsu M, Ebisuzaki W, Woollen J, Yang SK, Hnilo JJ, Fiorino M, Potter GL, , 2002. Ncep-Doe Amip-Ii Reanalysis (R-2). Bull Am Meteorol Soc 83: 16311643.[Crossref] [Google Scholar]
  38. Monaghan AJ, Rife DL, Pinto JO, Davis CA, Hannan JR, , 2010. Global precipitation extremes associated with diurnally varying low-level jets. J Clim 23: 50655084.[Crossref] [Google Scholar]
  39. Rife DL, Pinto JO, Monaghan AJ, Davis CA, Hannan JR, , 2010. Global distribution and characteristics of diurnally varying low-level jets. J Clim 23: 50415064.[Crossref] [Google Scholar]
  40. Reynolds RW, Rayner NA, Smith TM, Stokes DC, Wang WQ, , 2002. An improved in situ and satellite SST analysis for climate. J Clim 15: 16091625.[Crossref] [Google Scholar]
  41. Wan Z, , 2009. MODIS Land Surface Temperature Products Users' Guide. Santa Barbara, CA: University of California, ICESS. [Google Scholar]
  42. Rodell M, Houser PR, Jambor U, Gottschalck J, Mitchell K, Meng CJ, Arsenault K, Cosgrove B, Radakovich J, Bosilovich M, Entin JK, Walker JP, Lohmann D, Toll D, , 2004. The global land data assimilation system. Bull Am Meteorol Soc 85: 381.[Crossref] [Google Scholar]
  43. Wood AW, Leung LR, Sridhar V, Lettenmaier DP, , 2004. Hydrologic implications of dynamical and statistical approaches to downscaling climate model outputs. Clim Change 62: 189216.[Crossref] [Google Scholar]
  44. Monaghan AJ, Eisen RJ, MacMillan K, Gage KL, Moore SM, Hayden MH, , 2011. Modeling regional climate and human plague in the West Nile region of Uganda. J Appl Meteorol Climatol (in review). [Google Scholar]
  45. Akaike H, , 1974. A new look at the statistical model identification. IEEE Trans Automat Contr 19: 716723.[Crossref] [Google Scholar]
  46. Burnham KP, Anderson DR, , 1988. Model Selection and Inference: A Practical Information-Theoretic Approach. New York: Springer. [Google Scholar]
  47. Fielding AH, Bell JF, , 1997. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24: 3849.[Crossref] [Google Scholar]
  48. Eisen RJ, Enscore RE, Biggerstaff BJ, Reynolds PJ, Ettestad P, Brown T, Pape J, Tanda D, Levy CE, Engelthaler DM, Cheek J, Bueno R, Jr 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]
  49. 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]
  50. Hopkins G, , 1949. Report on Rats, Fleas and Plague in Uganda. Nairobi, Kenya: East African Standard, Ltd. [Google Scholar]
  51. Davis DH, , 1949. Current methods of controlling rodents and fleas in the campaign against bubonic plague and murine typhus. J R Sanit Inst 69: 170175. [Google Scholar]
  52. Sharif M, , 1951. Spread of plague in the southern and central divisions of Bombay Province and plague endemic centers in the Indo-Pakistan subcontinent. Bull World Health Organ 4: 75109. [Google Scholar]
  53. Cavanaugh DC, Dangerfield HG, Hunter DH, Joy RJ, Marshall JD, Jr Quy DV, Vivona S, Winter PE, , 1968. Some observations on the current plague outbreak in the Republic of Vietnam. Am J Public Health Nations Health 58: 742752.[Crossref] [Google Scholar]
  54. Marshall JD, Ouy DV, Gibson FL, Dung TC, Cavanaugh DC, , 1967. Ecology of plague in Vietnam: commensal rodents and their fleas. Mil Med 132: 896903. [Google Scholar]
  55. Eisen RJ, Glass GE, Eisen L, Cheek J, Enscore RE, Ettestad P, Gage KL, , 2007. A spatial model of shared risk for plague and hantavirus pulmonary syndrome in the southwestern United States. Am J Trop Med Hyg 77: 9991004. [Google Scholar]
  56. Holt AC, Salkeld DJ, Fritz CL, Tucker JR, Gong P, , 2009. Spatial analysis of plague in California: niche modeling predictions of the current distribution and potential response to climate change. Int J Health Geogr 8: 38.[Crossref] [Google Scholar]
  57. Duplantier JM, Duchemin JB, Chanteau S, Carniel E, , 2005. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res 36: 437453.[Crossref] [Google Scholar]
  58. Nakazawa Y, Williams R, Peterson AT, Mead P, Staples E, Gage KL, , 2007. Climate change effects on plague and tularemia in the United States. Vector Borne Zoonotic Dis 7: 529540.[Crossref] [Google Scholar]
  59. Roberts JI, , 1936. Plague conditions in an urban area of Kenya (Nairobi township). J Hyg (Lond) 36: 467484.[Crossref] [Google Scholar]
  60. Kilonzo BS, Patel NR, Mtoi RS, , 1981. Studies on the seasonal fluctuations of rodents and their fleas in north-eastern Tanzania. Tanzanian Veterinary Bulletin 3: 319. [Google Scholar]
  61. Rahelinirina S, Duplantier JM, Ratovonjato J, Ramilijaona O, Ratsimba M, Rahalison L, , 2010. Study on the movement of Rattus rattus and evaluation of the plague dispersion in Madagascar. Vector Borne Zoonotic Dis 10: 7784.[Crossref] [Google Scholar]
  62. Duplantier JM, Duchemin JB, Chanteau S, Carniel E, , 1999. The rodent problem in Madagascar: agricultural pest and threat to human health. ACIAR, ed. Ecologically Based Rodent Management. Canberra, Australia: ACIAR, 441459. [Google Scholar]
  63. Makundi R, Oguge NO, Mwanjabe PS, , 1999. Rodent pest management in East Africa: an ecological approach. Ecologically Based Rodent Management. Canberra, Australia: Australian Centre for International Agricultural Research. [Google Scholar]
  64. Eisen RJ, Eisen L, Gage KL, , 2009. Studies of vector competency and efficiency of North American fleas for Yersinia pestis: state of the field and future research needs. J Med Entomol 46: 737744.[Crossref] [Google Scholar]
  65. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, , 2008. Global trends in emerging infectious diseases. Nature 451: 990993.[Crossref] [Google Scholar]
  66. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, , 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25: 19651978.[Crossref] [Google Scholar]

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  • Received : 08 Sep 2011
  • Accepted : 22 Oct 2011
  • Published online : 01 Mar 2012

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