Ecoepidemiology of Tularemia in the Southcentral United States

Rebecca J. Eisen Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado; Office of the State Epidemiologist, Oklahoma State Department of Health, Oklahoma City, Oklahoma

Search for other papers by Rebecca J. Eisen in
Current site
Google Scholar
PubMed
Close
,
Paul S. Mead Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado; Office of the State Epidemiologist, Oklahoma State Department of Health, Oklahoma City, Oklahoma

Search for other papers by Paul S. Mead in
Current site
Google Scholar
PubMed
Close
,
Andrew M. Meyer Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado; Office of the State Epidemiologist, Oklahoma State Department of Health, Oklahoma City, Oklahoma

Search for other papers by Andrew M. Meyer in
Current site
Google Scholar
PubMed
Close
,
Liza E. Pfaff Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado; Office of the State Epidemiologist, Oklahoma State Department of Health, Oklahoma City, Oklahoma

Search for other papers by Liza E. Pfaff in
Current site
Google Scholar
PubMed
Close
,
Kristy K. Bradley Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado; Office of the State Epidemiologist, Oklahoma State Department of Health, Oklahoma City, Oklahoma

Search for other papers by Kristy K. Bradley in
Current site
Google Scholar
PubMed
Close
, and
Lars Eisen Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado; Office of the State Epidemiologist, Oklahoma State Department of Health, Oklahoma City, Oklahoma

Search for other papers by Lars Eisen in
Current site
Google Scholar
PubMed
Close
Restricted access

We combined county-based data for tularemia incidence from 1990 to 2003 for a nine-state region (Arkansas, Illinois, Indiana, Kansas, Kentucky, Missouri, Nebraska, Oklahoma, and Tennessee) in the southcentral United States with Geographic Information System (GIS)-based environmental data to determine associations between coverage by different habitats (especially dry forest representing suitable tick habitat) and tularemia incidence. High-risk counties (> 1 case per 100,000 person-years) clustered in Arkansas-Missouri and far eastern Oklahoma and Kansas. County tularemia incidence was positively associated with coverage by dry forested habitat suitable for vector ticks for Oklahoma-Kansas-Nebraska and Arkansas-Missouri but not for Illinois-Indiana-Kentucky-Tennessee. A multivariate logistic regression model predicting presence of areas with risk of tularemia based on GIS-derived environmental data was developed for the Arkansas-Missouri tularemia focus. The study shows the potential for research on tularemia ecoepidemiology and highlights the need for further modeling efforts based on acarologic data and more fine-scale point or zip code/census tract epidemiologic data.

Author Notes

Reprint requests: Rebecca J. Eisen, Division of Vector-Borne Infectious Diseases, National Center for Zoonotic, Vector-Borne and Enteric Diseases, Centers for Disease Control and Prevention, 3150 Rampart Road, Fort Collins, CO 80521, E-mail: dyn2@cdc.gov.
  • 1

    Hayes EB, 2005. Tularemia. Goodman JL, Dennis DT, Sonenshine DE, eds. Tick-Borne Diseases of Humans. Washington, DC: ASM Press, 207–217.

    • PubMed
    • Export Citation
  • 2

    Jellison WL, 1974. Tularemia in North America, 1930–1974. Missoula, MT: University of Montana.

    • PubMed
    • Export Citation
  • 3

    Ellis J, Oyston PCF, Green M, Titball RW, 2002. Tularemia. Clin Microbiol Rev 15 :631–646.

  • 4

    Hopla CE, 1974. The ecology of tularemia. Adv Vet Sci Comp Med 18 :25–53.

  • 5

    Choi E, 2002. Tularemia and Q fever. Med Clin North Am 85 :393–416.

  • 6

    Centers for Disease Control, 2005. Summary of notifiable diseases—United States, 2003. MMWR Morb Mortal Wkly Rep 52 :1–85.

  • 7

    Centers for Disease Control, 2002. Tularemia: United States, 1990–2000. MMWR Morb Mortal Wkly Rep 51 :181–184.

  • 8

    Centers for Disease Control, 2006. Summary of notifiable diseases—United States, 2004. MMWR Morb Mortal Wkly Rep 53 :1–84.

  • 9

    Feldman KA, 2003. Tularemia. J Am Vet Med Assoc 222 :725–730.

  • 10

    Eisen L, 2007. A call for renewed research on tick-borne Francisella tularensis in the Arkansas-Missouri primary national focus of tularemia in humans. J Med Entomol 44 :389–397.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Goddard J, McHugh CP, 1990. Impact of a severe tick infestation at Little Rock AFB, Arkansas, on Volant Scorpion military training. Mil Med 155 :277–280.

  • 12

    Hair JA, Howell DE, 1970. Lone Star Ticks. Their Biology and Control in Ozark Recreation Areas. Oklahoma Agric. Exp. Stn. Bull. 8679.

    • PubMed
    • Export Citation
  • 13

    Assal N, Blenden DC, Price ER, 1967. Epidemiologic study of human tularemia reported in Missouri, 1949–65. Public Health Rep 82 :627–632.

  • 14

    Assal NR, Lindeman RD, Carpenter RL, 1968. Epidemiologic study on reported human tularemia in Oklahoma, 1944–65. J Okla State Med Assoc 61 :120–124.

  • 15

    Bost RB, Percefull SC, Leming HE, 1948. Tularemia in the Ozarks region. JAMA 137 :352–354.

  • 16

    Callaway GD, Peterson SS, Good JT, 1954. Tularemia in Southwest Missouri; a report and discussion of seventy-eight cases. Mo Med 51 :906–909.

  • 17

    Corwin WC, Stubbs SP, 1952. Further studies on tularemia in the Ozarks. Review of forty-four cases during a three-year period. JAMA 149 :343–345.

  • 18

    Cox SK, Everett ED, 1981. Tularemia, an analysis of 25 cases. Mo Med 78 :70–74.

  • 19

    Evans ME, Gregory DW, Schaffner W, McGee ZA, 1985. Tularemia: a 30-year experience with 88 cases. Medicine 64 :251–269.

  • 20

    Lopez CE, Kornblatt AN, Sikes RK, Hanes OE, 1982. Tularemia: review of eight cases of tick-borne infection and the epidemiology of the disease in Georgia. South Med J 75 :404–407.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    McChesney TC, Narain J, 1983. A five-year evaluation of tularemia in Arkansas. J Ark Med Soc 80 :257–262.

  • 22

    Pullen RL, Stuart BM, 1945. Tularemia. Analysis of 225 cases. JAMA 129 :495–500.

  • 23

    Taylor JP, Istre GR, McChesney TC, Satalowich FT, Parker RL, McFarland LM, 1991. Epidemiologic characteristics of human tularemia in the southwest-central states, 1981–1987. Am J Epidemiol 133 :1032–1038.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Washburn AM, Tuohy JM, 1949. The changing picture of tularemia transmission in Arkansas. A study of 704 case histories. South Med J 42 :60–62.

  • 25

    Rohrbach BW, Westerman E, Istre GR, 1991. Epidemiology and clinical characteristics of tularemia in Oklahoma, 1979 to 1985. South Med J 84 :1091–1096.

  • 26

    Centers for Disease Control. 1997. Case definitions for infectious conditions under public health surveillance. Centers for Disease Control and Prevention. MMWR Recomm Rep 46 :1–55.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Centers for Disease Control. 2002. Tularemia—United States, 1990–2000. MMWR Morb Mortal Wkly Rep 51 :182–184.

  • 28

    Sonenshine DE, Atwood EL, Lamb JT Jr, 1966. The ecology of ticks transmitting Rocky Mountain spotted fever in a study area in Virginia. Ann Entomol Soc Am 59 :1234–1262.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Sonenshine DE, Levy GF, 1972. Ecology of the American dog tick, Dermacentor variabilis, in a study area in Virginia. 2. Distribution in relation to vegetative types. Ann Entomol Soc Am 65 :1175–1182.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sonenshine DE, 1993. Biology of Ticks. Volume 2. New York: Oxford University Press.

    • PubMed
    • Export Citation
  • 31

    Yabsley MJ, Wimberly MC, Stallknecht DE, Little SE, Davidson WR, 2005. Spatial analysis of the distribution of Ehrlichia chaffeensis, causative agent of human monocytotropic ehrlichiosis, across a multi-state region. Am J Trop Med Hyg 72 :840–850.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

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

    • PubMed
    • Export Citation
  • 33

    Hopla CE, 1962. Ixodes scapularis as a vector of tularemia organisms in the southern United States. Verh. 11 Int. Kongr. Ent. Vienna, August 17–25, 1960.

    • PubMed
    • Export Citation
  • 34

    Staples JE, Kubota KA, Chalcraft LG, Mead PS, Petersen JM, 2006. Epidemiologic and molecular analysis of human tularemia, United States, 1964–2004. Emerg Infect Dis 12 :1113–1118.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Eisen L, Eisen RJ, 2007. Need for improved methods to collect and present spatial epidemiologic data for vectorborne diseases. Emerg Infect Dis 13 :1816–1820.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    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 :530–537.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    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
  • 38

    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
  • 39

    Eisen RJ, Lane RS, Fritz CL, Eisen L, 2006. Spatial patterns of Lyme disease risk in California based on disease incidence data and modeling of vector-tick exposure. Am J Trop Med Hyg 75 :669–676.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Eisen RJ, Eisen L, Lane RS, 2006. Predicting density of Ixodes pacificus nymphs in dense woodlands in Mendocino County, California, based on geographic information systems and remote sensing versus field-derived data. Am J Trop Med Hyg 74 :632–640.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Eisen L, Meyer AM, Eisen RJ, 2007. Climate-based model predicting acarological risk of encountering the human-biting adult life stage of Dermacentor andersoni (Acari: Ixodidae) in a key habitat type in Colorado. J Med Entomol 44 :694–704.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Barbour AG, Maupin GO, Teltow GJ, Carter CJ, Piesman J, 1996. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 173 :403–409.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Chapman AS, Murphy SM, Demma LJ, Holman RC, Curns AT, McQuiston JH, Krebs JW, Swerdlow DL, 2006. Rocky Mountain spotted fever in the United States, 1997–2002. Vector Borne Zoonotic Dis 6 :170–178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Dalton MJ, Clarke MJ, Holman RC, Krebs JW, Fishbein DB, Olson JG, Childs JE, 1995. National surveillance for Rocky Mountain spotted fever, 1981–1992: epidemiologic summary and evaluation of risk factors for fatal outcome. Am J Trop Med Hyg 52 :405–413.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Demma LJ, Holman RC, McQuiston JH, Krebs JW, Swerdlow DL, 2005. Epidemiology of human ehrlichiosis and anaplasmosis in the United States, 2001–2002. Am J Trop Med Hyg 73 :400–409.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    James AM, Liveris D, Wormser GP, Schwartz I, Montecalvo MA, Johnson BJB, 2001. Borrelia lonestari infection after a bite by an Amblyomma americanum tick. J Infect Dis 183 :1810–1814.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    McQuiston JH, Paddock CD, Holman RC, Childs JE, 1999. The human ehrlichioses in the United States. Emerg Infect Dis 5 :635–642.

  • 48

    Paddock CD, Childs JE, 2003. Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin Microbiol Rev 16 :37–64.

  • 49

    Varela AS, Luttrell MP, Howerth EW, Moore VA, Davidson WR, Stallknecht DE, Little SE, 2004. First culture isolation of Borrelia lonestati, putative agent of southern tick-associated rash illness. J Clin Microbiol 42 :1163–1169.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Farlow J, Wagner DM, Dukerich M, Stanley M, Chu M, Kubota K, Petersen J, Keim P, 2005. Francisella tularensis in the United States. Emerg Infect Dis 11 :1835–1841.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Kugeler KJ, Gurfield N, Creek JG, Mahoney KS, Versage JL, Petersen JM, 2005. Discrimination between Francisella tula-rensis and Francisella-like endosymbionts when screening ticks by PCR. Appl Environ Microbiol 71 :7594–7597.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52

    Johansson A, Farlow J, Larsson P, Dukerich M, Chambers E, Byström M, Fox J, Chu M, Forsman M, Sjöstedt A, Keim P, 2004. Worldwide genetic relationships among Francisella tula-rensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol 186 :5808–5818.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53

    Farlow J, Smith KL, Wong J, Abrams M, Lytle M, Keim P, 2001. Francisella tularensis strain typing using multiple-locus, variable-number tandem repeat analysis. J Clin Microbiol 39 :3186–3192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54

    Goethert HK, Shani I, Telford SR III, 2004. Genotypic diversity of Francisella tularensis infecting Dermacentor variabilis ticks on Martha’s Vineyard, Massachusetts. J Clin Microbiol 42 :4968–4973.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55

    Markowitz LE, Hynes NA, de la Cruz P, Campos E, Barbaree JM, Plikaytis BD, Mosier D, Kaufmann AF, 1985. Tick-borne tularemia. An outbreak of lymphadenopathy in children. JAMA 254 :2922–2925.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56

    Schmid GP, Kornblatt AN, Connors CA, Patton C, Carney J, Hobbs J, Kaufmann AF, 1983. Clinically mild tularemia associated with tick-borne Francisella tularensis. J Infect Dis 148 :63–67.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 775 572 8
Full Text Views 289 9 0
PDF Downloads 101 12 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save