ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Gage KL , Kosoy MY , 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505–528.
-
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: 106–108.
-
5.
Ramalingaswami V , 2001. Psychosocial effects of the 1994 plague outbreak in Surat, India. Mil Med 166: 29–30.
-
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: 97–103.
-
7.
Abedi AA et al. 2018. Ecologic features of plague outbreak areas, Democratic Republic of the Congo, 2004–2014. Emerg Infect Dis 24: 210–220.
-
8.
Lakwo A , Cwinyaai W , Abdallay O , 2008. West Nile Profiling. Nebbi, Uganda: Agency for Accelerated Regional Development.
-
9.
MacMillan K et al. 2012. Climate predictors of the spatial distribution of human plague cases in the West Nile region of Uganda. Am J Trop Med Hyg 86: 514–523.
-
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: 1201–1221.
-
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.
-
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 et al. 2009. Spatial risk models for human plague in the West Nile region of Uganda. Am J Trop Med Hyg 80: 1014–1022.
-
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: 893–900.
-
17.
Forrester JD et al. 2017. Patterns of human plague in Uganda, 2008–2016. Emerg Infect Dis 23: 1517–1521.
-
18.
Eisen RJ et al. 2010. Assessing human risk of exposure to plague bacteria in northwestern Uganda based on remotely sensed predictors. Am J Trop Med Hyg 82: 904–911.
-
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: 435–442.
-
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.
-
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: 170–175.
-
22.
Davis DH , 1953. Plague in Africa from 1935 to 1949; a survey of wild rodents in African territories. Bull World Health Organ 9: 665–700.
-
23.
Gage KL , Burkot TR , Eisen RJ , Hayes EB , 2008. Climate and vectorborne diseases. Am J Prev Med 35: 436–450.
-
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.
-
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.
-
26.
Eisen RJ et al. 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: 259–270.
-
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: 1047–1058.
-
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: 718–724.
-
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: 333–355.
-
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: 1254–1263.
-
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: 1027–1034.
-
32.
Borchert JN et al. 2012. Evaluation and modification of off-host flea collection techniques used in northwest Uganda: laboratory and field studies. J Med Entomol 49: 210–214.
-
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: 842–850.
-
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: 458–463.
-
35.
Boegler KA et al. 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: 238–247.
-
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: 678–682.
-
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: 381–389.
-
38.
Eisen RJ et al. 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: 949–956.
-
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 et al. 2017. Knowledge and practices related to plague in an endemic area of Uganda. Int J Infect Dis 64: 80–84.
-
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.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 3771 | 1453 | 124 |
| Full Text Views | 682 | 114 | 1 |
| PDF Downloads | 321 | 27 | 1 |
Epidemiology, Ecology and Prevention of Plague in the West Nile Region of Uganda: The Value of Long-Term Field Studies
Rebecca J. Eisen
Rebecca J. Eisen
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Linda A. Atiku
Linda A. Atiku
Plague Unit, Uganda Virus Research Institute, Entebbe, Uganda
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Russell E. Enscore
Russell E. Enscore
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Joseph T. Mpanga
Joseph T. Mpanga
Plague Unit, Uganda Virus Research Institute, Entebbe, Uganda
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Sarah Acayo
Sarah Acayo
Plague Unit, Uganda Virus Research Institute, Entebbe, Uganda
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Paul S. Mead
Paul S. Mead
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Titus Apangu
Titus Apangu
Plague Unit, Uganda Virus Research Institute, Entebbe, Uganda
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Brook M. Yockey
Brook M. Yockey
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Jeff N. Borchert
Jeff N. Borchert
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Charles B. Beard
Charles B. Beard
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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Kenneth L. Gage
Kenneth L. Gage
Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado;
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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
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.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Gage KL , Kosoy MY , 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505–528.
-
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: 106–108.
-
5.
Ramalingaswami V , 2001. Psychosocial effects of the 1994 plague outbreak in Surat, India. Mil Med 166: 29–30.
-
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: 97–103.
-
7.
Abedi AA et al. 2018. Ecologic features of plague outbreak areas, Democratic Republic of the Congo, 2004–2014. Emerg Infect Dis 24: 210–220.
-
8.
Lakwo A , Cwinyaai W , Abdallay O , 2008. West Nile Profiling. Nebbi, Uganda: Agency for Accelerated Regional Development.
-
9.
MacMillan K et al. 2012. Climate predictors of the spatial distribution of human plague cases in the West Nile region of Uganda. Am J Trop Med Hyg 86: 514–523.
-
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: 1201–1221.
-
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.
-
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 et al. 2009. Spatial risk models for human plague in the West Nile region of Uganda. Am J Trop Med Hyg 80: 1014–1022.
-
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: 893–900.
-
17.
Forrester JD et al. 2017. Patterns of human plague in Uganda, 2008–2016. Emerg Infect Dis 23: 1517–1521.
-
18.
Eisen RJ et al. 2010. Assessing human risk of exposure to plague bacteria in northwestern Uganda based on remotely sensed predictors. Am J Trop Med Hyg 82: 904–911.
-
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: 435–442.
-
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.
-
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: 170–175.
-
22.
Davis DH , 1953. Plague in Africa from 1935 to 1949; a survey of wild rodents in African territories. Bull World Health Organ 9: 665–700.
-
23.
Gage KL , Burkot TR , Eisen RJ , Hayes EB , 2008. Climate and vectorborne diseases. Am J Prev Med 35: 436–450.
-
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.
-
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.
-
26.
Eisen RJ et al. 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: 259–270.
-
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: 1047–1058.
-
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: 718–724.
-
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: 333–355.
-
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: 1254–1263.
-
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: 1027–1034.
-
32.
Borchert JN et al. 2012. Evaluation and modification of off-host flea collection techniques used in northwest Uganda: laboratory and field studies. J Med Entomol 49: 210–214.
-
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: 842–850.
-
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: 458–463.
-
35.
Boegler KA et al. 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: 238–247.
-
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: 678–682.
-
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: 381–389.
-
38.
Eisen RJ et al. 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: 949–956.
-
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 et al. 2017. Knowledge and practices related to plague in an endemic area of Uganda. Int J Infect Dis 64: 80–84.
-
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.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 3771 | 1453 | 124 |
| Full Text Views | 682 | 114 | 1 |
| PDF Downloads | 321 | 27 | 1 |