Spatial Risk Models for Human Plague in the West Nile Region of Uganda

Anna M. Winters Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Anna M. Winters in
Current site
Google Scholar
PubMed
Close
,
J. Erin Staples Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by J. Erin Staples in
Current site
Google Scholar
PubMed
Close
,
Asaph Ogen-Odoi Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Asaph Ogen-Odoi in
Current site
Google Scholar
PubMed
Close
,
Paul S. Mead Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Paul S. Mead in
Current site
Google Scholar
PubMed
Close
,
Kevin Griffith Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Kevin Griffith in
Current site
Google Scholar
PubMed
Close
,
Nicholas Owor Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Nicholas Owor in
Current site
Google Scholar
PubMed
Close
,
Nackson Babi Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Nackson Babi in
Current site
Google Scholar
PubMed
Close
,
Russell E. Enscore Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Russell E. Enscore in
Current site
Google Scholar
PubMed
Close
,
Lars Eisen Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Lars Eisen in
Current site
Google Scholar
PubMed
Close
,
Kenneth L. Gage Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Kenneth L. Gage in
Current site
Google Scholar
PubMed
Close
, and
Rebecca J. Eisen Division of Vector-Borne Infectious Diseases, National Center for Vector-Borne, Zoonotic and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado; Uganda Virus Research Institute, Entebbe, Uganda

Search for other papers by Rebecca J. Eisen in
Current site
Google Scholar
PubMed
Close
Restricted access

The West Nile region of Uganda represents an epidemiologic focus for human plague in east Africa. However, limited capacity for diagnostic laboratory testing means few clinically diagnosed cases are confirmed and the true burden of disease is undetermined. The aims of the study were 1) describe the spatial distribution of clinical plague cases in the region, 2) identify ecologic correlates of incidence, and 3) incorporate these variables into predictive models that define areas of plague risk. The model explained 74% of the incidence variation and revealed that cases were more common above 1,300 m than below. Remotely-sensed variables associated with differences in soil or vegetation were also identified as incidence predictors. The study demonstrated that plague incidence can be modeled at parish-level scale based on environmental variables and identified parishes where cases may be under-reported and enhanced surveillance and preventative measures may be implemented to decrease the burden of plague.

Author Notes

  • 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

    Dennis DT, Gage KL, Plague. Cohen J, Powderly WG, eds. Infectious Diseases. Volume 2. London: Mosby, 2003; 1641–1648.

    • PubMed
    • Export Citation
  • 3

    WHO, 2004. Human plague in 2002 and 2003. Wkly Epidemiol Rec 79 :301–308.

  • 4

    WHO, 2005. Outbreak news index 2005. Wkly Epidemiol Rec 80 :433–440.

  • 5

    Kilonzo BS, 1999. Plague epidemiology and control in eastern and southern Africa during the period 1978 to 1997. Cent Afr J Med 45 :70–76.

  • 6

    WHO, 1983. Weekly epidemiological record. Wkly Epidemiol Rec 58 :265–272.

  • 7

    Aikimbajev A, Meka-Mechenko T, Temiralieva G, Bekenov J, Sagiyev Z, Kaljan K, Mukhambetova AK, 2003. Plague in Kazakhstan at the present time. Przegl Epidemiol 57 :593–598.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Hull HF, Montes JM, Mann JM, 1987. Septicemic plague in New Mexico. J Infect Dis 155 :113–118.

  • 9

    Mann JM, Schmid GP, Stoesz PA, Skinner MD, Kaufmann AF, 1982. Peripatetic plague. JAMA 247 :47–48.

  • 10

    MMWR, 1994. Human plague—United States, 1993–1994. MMWR 43 :242–246.

  • 11

    MMWR, 2002. Imported plague: New York City, 2002. MMWR 52 :725–728.

  • 12

    MMWR, 2006. Human plague—four states, 2006. MMWR 55 :940–943.

  • 13

    Crook LD, Tempest B, 1992. Plague. A clinical review of 27 cases. Arch Intern Med 152 :1253–1256.

  • 14

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

    • PubMed
    • Export Citation
  • 15

    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 :121–125.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    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 :529–540.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Barnes AM, 1980. Plague surveillance and control. WHO Chron 34 :139–143.

  • 19

    Gage KL, 1999. Plague surveillance. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: WHO, 135–165.

    • PubMed
    • Export Citation
  • 20

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

    • PubMed
    • Export Citation
  • 21

    Orochi-Orach, 2002. Plague Outbreaks: The Gender and Age Perspective in Okoro County, Nebbi District, Uganda. Nebbe, Uganda: Agency for Accelerated Regional Development.

    • PubMed
    • Export Citation
  • 22

    Jensen J, 2007. Remote Sensing of the Environment: An Earth Resource Perspective. Second edition. Upper Saddle River: Prentice Hall.

    • PubMed
    • Export Citation
  • 23

    Chander G, Markham B, 2003. Revised Landsat-5 TM radiometric calibration procedures and postcalibration dynamic ranges. IEEE Trans Geosci Rem Sens 41 :2674–2677.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Chen Y, Guo D, Zhou T, 1999. Noise removal of thermal image and the determination of the temperatures. Remote Sensing Information 11 :7–9.

  • 25

    Han-qiu X, Ben-qing C, 2004. Remote sensing of the urban heat island and its changes in Xiamen City of SE China. J Environ Sci (China) 16 :276–281.

  • 26

    Landsat 7 Science Data Users Handbook. Available at: http://landsathandbook.gsfc.nasa.gov/handbook/handbook_toc.html. Accessed December 3, 2008.

    • PubMed
    • Export Citation
  • 27

    USGS - EROS Data Center, 2006. MRLC 2001 Image Processing Procedure.

  • 28

    Getting Started with ENVI—version 4.5. Available at: http://www.ittvis.com/ProductServices/ENVI/ProductDocumentation.aspx. Accessed December 3, 2008.

    • PubMed
    • Export Citation
  • 29

    Jensen J, 1995. Introductory Digital Image Processing: A Remote Sensing Perspective. Second edition. Upper Saddle River: Prentice Hall.

    • PubMed
    • Export Citation
  • 30

    Gelman A, Hill J, 2007. Data Analysis Using Regression and Multilevel/Hierarchical Models. New York: Cambridge University Press.

    • PubMed
    • Export Citation
  • 31

    Burnham K, Anderson D, 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York: Springer.

    • PubMed
    • Export Citation
  • 32

    Sall J, Creighton L, Lehman A, 2005. JMP Start Statistics. Third edition. Belmont: Brooks/Cole, 584.

    • PubMed
    • Export Citation
  • 33

    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 :949–956.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    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 :530–537.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    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 :999–1004.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Velimirovic B, Zikmund V, Herman J, 1968. Plague in the Lake Edwards focus: the Democratic Republic of Congo, 1960–1966. Z Tropenmed Parasitol 20 :373–387.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    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.

  • 38

    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.

  • 39

    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 :85–94.

  • 40

    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 :742–752.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Marshall JD, Ouy DV, Gibson FL, Dung TC, Cavanaugh DC, 1967. Ecology of plague in Vietnam: commensal rodents and their fleas. Mil Med 132 :896–903.

  • 42

    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 :186–196.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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 :814–821.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Gage KL, 2008. Climate and vectorborne diseases. Am J Prev Med 35 :436–450.

  • 45

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

  • 46

    Keeling MJ, Gilligan CA, 2000. Metapopulation dynamics of bubonic plague. Nature 407 :903–906.

  • 47

    Snall T, O’Hara RB, Ray C, Collinge SK, 2008. Climate-driven spatial dynamics of plague among prairie dog colonies. Am Nat 171 :238–248.

  • 48

    Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JF, Gage KL, Kosoy MY, Loye JE, Martin AP, 2005. Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landscape Ecol 20 :941–955.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Davis S, Leirs H, Viljugrein H, Stenseth NC, De Bruyn L, Klassovskiy N, Ageyev V, Begon M, 2007. Empirical assessment of a threshold model for sylvatic plague. J R Soc Interface 4 :649–657.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Barnes AM, Maupin GO, 1982. Observations on the biting of humans by Euhoplopsyllus-Glacialis-Affinis (Siphonaptera, Pulicidae) and a review of is plague-transmission potential. J Med Entomol 19 :748–749.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Poland JD, 1999. Diagnosis and clinic manifestations. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 52

    Chu MC, 2000. Laboratory Manual of Plague Diagnostics. Geneva: Centers for Disease Control and Prevention and World Health Organization, 129.

    • PubMed
    • Export Citation
  • 53

    Akiev AK, 1982. Epidemiology and incidence of plague in the world, 1958–79. Bull World Health Organ 60 :165–169.

  • 54

    Gratz NG, 1999. Control of plague transmission. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: World Health Organization, 97–134.

    • PubMed
    • Export Citation
  • 55

    Poland JD, Barnes AM, 1979. Plague. Steele JH, ed. CRC Handbook Series in Zoonoses. Section A: Bacterial, Rickettsial and Mycotic Diseases. Volume I. Boca Raton: CRC Press Inc., 515–559.

    • PubMed
    • Export Citation
  • 56

    Gage KL, 1999. National health services in prevention and control. Plague Manual: Epidemiology, Distribution, Surveillance and Control. Geneva: WHO, 167–171.

    • PubMed
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 516 484 19
Full Text Views 231 5 1
PDF Downloads 67 6 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save