• 1.

    Gage KL, Kosoy MY, 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505528.

  • 2.

    Hirst LF, 1953. The Conquest of Plague. London, UK: Oxford University Press.

  • 3.

    Pollitzer R, 1954. Plague. World Health Organization Monograph Series No. 22. Geneva, Switzerland: World Health Organization.

  • 4.

    Mead PS, 2018. Plague in Madagascar—a tragic opportunity for improving public health. N Engl J Med 378: 106108.

  • 5.

    Ramalingaswami V, 2001. Psychosocial effects of the 1994 plague outbreak in Surat, India. Mil Med 166: 2930.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 7.

    Abedi AA 2018. Ecologic features of plague outbreak areas, Democratic Republic of the Congo, 2004–2014. Emerg Infect Dis 24: 210220.

  • 8.

    Lakwo A, Cwinyaai W, Abdallay O, 2008. West Nile Profiling. Nebbi, Uganda: Agency for Accelerated Regional Development.

  • 9.

    MacMillan K 2012. Climate predictors of the spatial distribution of human plague cases in the West Nile region of Uganda. Am J Trop Med Hyg 86: 514523.

    • Search Google Scholar
    • Export Citation
  • 10.

    Monaghan AJ, MacMillan K, Moore SM, Mead PS, Hayden MH, Eisen RJ, 2012. A regional climatography of West Nile, Uganda, to support human plague modeling. J Appl Meteorol Climatol 51: 12011221.

    • Search Google Scholar
    • Export Citation
  • 11.

    Moore SM, Monaghan A, Griffith KS, Apangu T, Mead PS, Eisen RJ, 2012. Improvement of disease prediction and modeling through the use of meteorological ensembles: human plague in Uganda. PLoS One 7: e44431.

    • Search Google Scholar
    • Export Citation
  • 12.

    Hopkins GHE, 1949. Report on Rats, Fleas and Plague in Uganda. Kampala, Uganda: East African Standard, Ltd., 52.

  • 13.

    Orochi-Orach S, 2003. Plague outbreaks: the gender and age perspective in Okoro Counti, Nebbi District, Uganda. Nebbi, Uganda: Agency for Accelerated Regional Development, 51.

  • 14.

    Winters AM 2009. Spatial risk models for human plague in the West Nile region of Uganda. Am J Trop Med Hyg 80: 10141022.

  • 15.

    Chu MC, 2000. Laboratory Manual of Plague Diagnostics. Atlanta, GA and Geneva, Switzerland: Centers for Disease Control and Prevention and World Health Organization.

  • 16.

    Eisen RJ, Atiku LA, Mpanga JT, Enscore RE, Acayo S, Kaggwa J, Yockey BM, Apangu T, Kugeler KJ, Mead PS, 2020. An evaluation of the flea index as a predictor of plague epizootics in the West Nile region of Uganda. J Med Entomol 57: 893900.

    • Search Google Scholar
    • Export Citation
  • 17.

    Forrester JD 2017. Patterns of human plague in Uganda, 2008–2016. Emerg Infect Dis 23: 15171521.

  • 18.

    Eisen RJ 2010. Assessing human risk of exposure to plague bacteria in northwestern Uganda based on remotely sensed predictors. Am J Trop Med Hyg 82: 904911.

    • Search Google Scholar
    • Export Citation
  • 19.

    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.

    • Search Google Scholar
    • Export Citation
  • 20.

    Moore SM, Monaghan A, Borchert JN, Mpanga JT, Atiku LA, Boegler KA, Montenieri J, MacMillan K, Gage KL, Eisen RJ, 2015. Seasonal fluctuations of small mammal and flea communities in a Ugandan plague focus: evidence to implicate Arvicanthis niloticus and Crocidura spp. as key hosts in Yersinia pestis transmission. Parasit Vectors 8: 11.

    • Search Google Scholar
    • Export Citation
  • 21.

    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.

    • Search Google Scholar
    • Export Citation
  • 22.

    Davis DH, 1953. Plague in Africa from 1935 to 1949; a survey of wild rodents in African territories. Bull World Health Organ 9: 665700.

    • Search Google Scholar
    • Export Citation
  • 23.

    Gage KL, Burkot TR, Eisen RJ, Hayes EB, 2008. Climate and vectorborne diseases. Am J Prev Med 35: 436450.

  • 24.

    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 23: 7.

    • Search Google Scholar
    • Export Citation
  • 25.

    Eisen RJ, Borchert JN, Mpanga JT, Atiku LA, MacMillan K, Boegler KA, Montenieri JA, Monaghan A, Gage KL, 2012. Flea diversity as an element for persistence of plague bacteria in an East African plague focus. PLoS One 7: e35598.

    • Search Google Scholar
    • Export Citation
  • 26.

    Eisen RJ 2013. Evidence that rodent control strategies ought to be improved to enhance food security and reduce the risk of rodent-borne illnesses within subsistence farming villages in the plague-endemic West Nile region, Uganda. Int J Pest Manage 59: 259270.

    • Search Google Scholar
    • Export Citation
  • 27.

    Eisen RJ, MacMillan K, Atiku LA, Mpanga JT, Zielinski-Gutierrez E, Graham CB, Boegler KA, Enscore RE, Gage KL, 2014. Identification of risk factors for plague in the West Nile Region of Uganda. Am J Trop Med Hyg 90: 10471058.

    • Search Google Scholar
    • Export Citation
  • 28.

    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.

    • Search Google Scholar
    • Export Citation
  • 29.

    Enscore RE, Babi N, Amatre G, Atiku L, Eisen RJ, Pepin KM, Vera-Tudela R, Sexton C, Gage KL, 2020. The changing triad of plague in Uganda: invasive black rats (Rattus rattus), indigenous small mammals, and their fleas. J Vector Ecol 45: 333355.

    • Search Google Scholar
    • Export Citation
  • 30.

    Boegler KA, Atiku LA, Mpanga JT, Clark RJ, Delorey MJ, Gage KL, Eisen RJ, 2014. Use of insecticide delivery tubes for controlling rodent-associated fleas in a plague endemic region of West Nile, Uganda. J Med Entomol 51: 12541263.

    • Search Google Scholar
    • Export Citation
  • 31.

    Borchert JN, Eisen RJ, Atiku LA, Delorey MJ, Mpanga JT, Babi N, Enscore RE, Gage KL, 2012. Efficacy of indoor residual spraying using lambda-cyhalothrin for controlling nontarget vector fleas (Siphonaptera) on commensal rats in a plague endemic region of northwestern Uganda. J Med Entomol 49: 10271034.

    • Search Google Scholar
    • Export Citation
  • 32.

    Borchert JN 2012. Evaluation and modification of off-host flea collection techniques used in northwest Uganda: laboratory and field studies. J Med Entomol 49: 210214.

    • Search Google Scholar
    • Export Citation
  • 33.

    Borchert JN, Enscore RE, Eisen RJ, Atiku LA, Owor N, Acayo S, Babi N, Montenieri JA, Gage KL, 2010. Evaluation of rodent bait containing imidacloprid for the control of fleas on commensal rodents in a plague-endemic region of northwest Uganda. J Med Entomol 47: 842850.

    • Search Google Scholar
    • Export Citation
  • 34.

    Eisen RJ, Atiku LA, Boegler KA, Mpanga JT, Enscore RE, MacMillan K, Gage KL, 2018. An evaluation of removal trapping to control rodents inside homes in a plague-endemic region of rural northwestern Uganda. Vector Borne Zoonotic Dis 18: 458463.

    • Search Google Scholar
    • Export Citation
  • 35.

    Boegler KA 2018. Rat fall surveillance coupled with vector control and community education as a plague prevention strategy in the West Nile Region, Uganda. Am J Trop Med Hyg 98: 238247.

    • Search Google Scholar
    • Export Citation
  • 36.

    Eisen RJ, Wilder AP, Bearden SW, Montenieri JA, Gage KL, 2007. Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efficient as transmission by blocked fleas. J Med Entomol 44: 678682.

    • Search Google Scholar
    • Export Citation
  • 37.

    Graham CB, Borchert JN, Black WCt, Atiku LA, Mpanga JT, Boegler KA, Moore SM, Gage KL, Eisen RJ, 2013. Blood meal identification in off-host cat fleas (Ctenocephalides felis) from a plague-endemic region of Uganda. Am J Trop Med Hyg 88: 381389.

    • Search Google Scholar
    • Export Citation
  • 38.

    Eisen RJ 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.

    • Search Google Scholar
    • Export Citation
  • 39.

    Eisen RJ, Gage KL, 2009. Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods. Vet Res 40: 1.

  • 40.

    Kugeler KJ 2017. Knowledge and practices related to plague in an endemic area of Uganda. Int J Infect Dis 64: 8084.

  • 41.

    Uganda Ministry of Health, 2019. Zoonotic diseases: In: National Action Plan for Health Security 2019–2023. Kampala, Uganda: Uganda Ministry of Health, 34–36.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Epidemiology, Ecology and Prevention of Plague in the West Nile Region of Uganda: The Value of Long-Term Field Studies

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  • 1 Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
  • 2 Plague Unit, Uganda Virus Research Institute, Entebbe, Uganda

Abstract.

Plague, a fleaborne rodent-associated zoonosis, is a neglected disease with most recent cases reported from east and central Africa and Madagascar. Because of its low incidence and sporadic occurrence, most of our knowledge of plague ecology, prevention, and control derives from investigations conducted in response to human cases. Long-term studies (which are uncommon) are required to generate data to support plague surveillance, prevention, and control recommendations. Here we describe a 15-year, multidisciplinary commitment to plague in the West Nile region of Uganda that led to significant advances in our understanding of where and when persons are at risk for plague infection and how to reduce morbidity and mortality. These findings provide data-driven support for several existing recommendations on plague surveillance and prevention and may be generalizable to other plague foci.

Author Notes

Address correspondence to Rebecca J. Eisen, Centers for Disease Control and Prevention, 3156 Rampart Road, Fort Collins, CO 80521. E-mail: dyn2@cdc.gov

Financial support: Funding for this review was provided by the CDC DVBD. The findings and conclusions of this study are by the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Authors’ addresses: Rebecca J. Eisen, Russell E. Enscore, Paul S. Mead, Brook M. Yockey, Jeff N. Borchert, Charles B. Beard, and Kenneth L. Gage, Division of Vector-Borne Infectious Diseases, CDC, Ft. Collins, CO, E-mails: dyn2@cdc.gov, renscore@cdc.gov, pfm0@cdc.gov, bmy0@cdc.gov, gqx1@cdc.gov, cbb0@cdc.gov, and klg0@cdc.gov. Linda A. Atiku, Joseph T. Mpanga,Sarah Acayo, and Titus Apangu, Plague Unit, Uganda Virus Research Institute, Entebbe, Uganda, E-mails: l_atikupraise@yahoo.com, socakabrown@yahoo.ca, joe1ug@msn.com, and apangu26@gmail.com.

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