Emergence of Tick-Borne Granulocytic Anaplasmosis Associated with Habitat Type and Forest Change in Northern California

Janet E. Foley Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, California; Department of Biological Sciences, California State University, Sacramento, California

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Nathan C. Nieto Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, California; Department of Biological Sciences, California State University, Sacramento, California

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Patrick Foley Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, California; Department of Biological Sciences, California State University, Sacramento, California

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An important ecosystem service of intact forests is protection from some emerging infectious diseases. Tick-transmitted disease granulocytic anaplasmosis increasingly occupies second-growth forest. We hypothesized that areas of second growth would have increases in tick and rodent abundance, facilitating emergence of anaplasmosis. We predicted Anaplasma phagocytophilum presence as a function of biocomplexity and forest structure, including vegetation, ticks, and rodents in four sites in California. Significant risk factors for exposure included host species (woodrats with 13% seroprevalence, odds ratio [OR] = 8.3 and chipmunks with 27% seroprevalence, OR = 20.7), and park location (northern parks, OR 25.5–27.7). Exposure to A. phagocytophilum was more likely among chipmunks in redwood sites at one park, but with woodrats and oaks at another. Overall, transects on which small mammals showed greatest A. phagocytophilum exposure had high biodiversity in ticks, rodents, and vegetation, as well as intermediate-sized trees with a high mean and variance in diameter at breast height, findings which suggest that a dilution effect, where increased biodiversity reduces disease risk, does not necessarily apply in this system. Thus, enzootic and potentially emerging anaplasmosis were linked to high biodiversity and mature second-growth forest.

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  • 1

    Randolph S, 2001. The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lond B Biol Sci 356 :1045–1056.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Foley JE, Foley P, Brown RN, Lane RS, Dumler JS, Madigan JE, 2004. Ecology of granulocytic ehrlichiosis and Lyme disease in the western United States. J Vector Ecol 29 :41–50.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Vector Borne Disease Section, 2008. Vector-Borne Diseases in California. 2006 Annual Report. Sacramento, CA: Infectious Diseases Branch, California Department of Health Services.

    • PubMed
    • Export Citation
  • 4

    Foley JE, Foley P, Madigan JE, 2001. Spatial distribution of seropositivity to the causative agent of granulocytic ehrlichiosis in dogs in California. Am J Vet Res 62 :1599–1605.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Madigan J, Hietala A, Chambers S, 1990. Seroepidemiologic survey of antibodies to Ehrlichia equi in horses in northern California. J Am Vet Med Assoc 196 :1962–1964.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Brown RN, Lane R, Dennis DT, 2005. Geographic distributions of tick-borne diseases and their vectors. Goodman JL, Dennis DT, Sonenshine DE, eds. Tick-Borne Diseases of Humans. Washington, DC: American Society for Microbiology Press, 363–391.

    • PubMed
    • Export Citation
  • 7

    Nieto N, Foley J, 2009. The redwood chipmunk, Tamias ochrogenys, is reservoir competent for Anaplasma phagocytophilum, the agent of granulocytic anaplasmosis. Vector Borne Zoonotic Dis (in press).

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Nieto NC, Foley JE, 2008. Evaluation of squirrels (Rodentia: Sciuridae) as ecologically significant hosts for Anaplasma phagocytophilum in California. J Med Entomol 45 :763–769.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Cao W, Lin Z, He J, Foley J, Jiang B, Yang H, Richardus J, Habbema D, 2006. Natural infection of Anaplasma phagocytophilum in ticks and rodents from a forest area of Jilin Province, China. Am J Trop Med Hyg 75 :664–668.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Bown K, Begon M, Bennett M, Woldehiwet Z, Ogden N, 2003. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerg Infect Dis 9 :63–70.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Foley JE, Kramer VL, Weber D, 2002. Experimental ehrlichiosis in dusky footed woodrats (Neotoma fuscipes). J Wildl Dis 38 :194–198.

  • 12

    Blanco JR, Oteo JA, 2002. Human granulocytic ehrlichiosis in Europe. Clin Microbiol Infect 8 :763–672.

  • 13

    Nicholson WL, Castro MB, Kramer VL, Sumner JW, Childs JE, 1999. Dusky-footed wood rats (Neotoma fuscipes) as reservoirs of granulocytic Ehrlichiae (Rickettsiales: Ehrlichieae) in northern California. J Clin Microbiol 37 :3323–3327.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Telford SR, Dawson JE, Katavolos P, Warner CK, Kolbert CP, Persing DH, 1996. Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. Proc Natl Acad Sci USA 93 :6209–6214.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Furman DP, Loomis EC, 1984. The Ticks of California (Acari: Ixodida). Berkeley, CA: University of California Press.

    • PubMed
    • Export Citation
  • 16

    Webb JP, Bennett S, Challet G, 1990. The larval ticks of the genus Ixodes latreille (Acari: Ixodidae) of California. Bull Soc Vector Biol 15 :73–124.

  • 17

    Dumler SJ, Asanovich KM, Bakken JS, Richter P, Kimsey R, Madigan JE, 1995. Serologic cross-reactions among Ehrlichia equi, Ehrlichia phagocytophila, and human granulocytic ehrlichia. J Clin Microbiol 33 :1098–1103.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Drazenovich NL, Brown RN, Foley JE, 2006. Use of real-time quantitative PCR targeting the msp2 protein gene to identify cryptic Anaplasma phagocytophilum infections in wildlife and domestic animals. Vector Borne Zoonotic Dis 6 :83–90.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Begon M, Harper J, Townsend C, 1996. Ecology. Oxford: Blackwell.

  • 20

    Morse SS, 1995. Factors in the emergence of infectious diseases. Emerg Infect Dis 1 :7–15.

  • 21

    Courtenay O, Quinnell J, Garcez L, Dye C, 2002. Low infectiousness of a wildlife host to Leishmania infantum: the crab-eating fox is not important for transmission. Parasitology 125 :407–414.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Centers for Disease Control and Prevention, 2007. Lyme disease—United States 2003–2005. MMWR Morb Mortal Wkly Rep 56 :573–576.

  • 23

    Barbour AG, Fish D, 1993. The biological and social phenomenon of Lyme disease. Science 260 :1610–1616.

  • 24

    Linsdale JM, Tevis LP, 1951. The Dusky-Footed Wood Rat; A Record of Observations Made on the Hastings Natural History Reservation. Berkeley, CA: University of California Press.

    • PubMed
    • Export Citation
  • 25

    Sakai H, Noon B, 1993. Dusky-footed woodrat abundance in different-aged forests in northwestern California. J Wildl Manage 57 :373–382.

  • 26

    Foley J, Nieto N, Adjemian J, Dabritz H, Brown R, 2008. Anaplasma phagocytophilum infection in small mammal hosts of Ixodes spp. ticks, western United States. Emerg Infect Dis 14 :1147–1150.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Best T, Granai N, 1994. Tamias merriami. Mamm Species 476 :1–9.

  • 28

    Gannon W, Forbes R, Kain D, 1993. Tamias ochrogenys. Mamm Species 445 :1–4.

  • 29

    Walls J, Greig B, Neitzel D, Dumler J, 1997. Natural infection of small mammal species in Minnesota with the agent of human granulocytic ehrlichiosis. J Clin Microbiol 35 :853–855.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Foley J, Clueit S, Brown RN, 2008. Differential exposure to Anaplasma phagocytophilum in rodent species in northern California. Vector Borne Zoonotic Dis 8 :49–55.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F, 2006. Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biol 4 :e145.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Zeidner NS, Burkot TR, Massung R, Nicholson WL, Dolan MC, Rutherford JS, Biggerstaff BJ, Maupin GO, 2000. Transmission of the agent of human granulocytic ehrlichiosis by Ixodes spinipalpis ticks: evidence of an enzootic cycle of dual infection with Borrelia burgdorferi in northern Colorado. J Infect Dis 182 :616–619.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Eisen R, Eisen L, Castro MB, Lane RS, 2003. Environmentally related variability in risk of exposure to Lyme disease spirochetes in northern California: effect of climatic conditions and habitat type. Environ Entomol 32 :1010–1018.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    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
  • 35

    Nieto N, Foley J, Bettaso J, Lane R, 2009. Reptile infection with Anaplasma phagocytophilum, the causative agent of granulocytic anaplasmosis. J Parasitol Mar 12 :1 [Epub ahead of print].

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Lane RS, Mun J, Eisen RJ, Eisen L, 2005. Western gray squirrel (Rodentia: Sciuridae): a primary reservoir host of Borrelia burgdorferi in Californian oak woodlands? J Med Entomol 42 :388–396.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Kaufmann M, Binkley D, Fule P, Johnson M, Stephens S, Swetman T, 2007. Defining old-growth for fire-adapted forests of the western United States. Ecology and Society 12 :15.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Ostfeld RS, Keesing F, 2000. Biodiversity and disease risk: the case of Lyme disease. Conserv Biol 14 :722–728.

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