Use of tick surveys and serosurveys to evaluate pet dogs as a sentinel species for emerging Lyme disease

Sarah A. Hamer Department of Fisheries and Wildlife, College of Agricultural and Natural Resources, Michigan State University, East Lansing, MI 48824

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Jean I. Tsao Department of Fisheries and Wildlife, College of Agricultural and Natural Resources, Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824

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Edward D. Walker Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824

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Linda S. Mansfield Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824

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Erik S. Foster Michigan Department of Community Health, 201 Townsend St, Lansing, MI 48913

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Graham J. Hickling Department of Fisheries and Wildlife, College of Agricultural and Natural Resources, Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824

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Abstract

Objective—To evaluate dogs as a sentinel species for emergence of Lyme disease in a region undergoing invasion by Ixodes scapularis.

Sample Population—353 serum samples and 78 ticks obtained from dogs brought to 18 veterinary clinics located in the lower peninsula of Michigan from July 15, 2005, through August 15, 2005.

Procedures—Serum samples were evaluated for specific antibodies against Borrelia burgdorferi by use of 3 serologic assays. Ticks from dogs were subjected to PCR assays for detection of pathogens.

Results—Of 353 serum samples from dogs in 18 counties in 2005, only 2 (0.6%) contained western blot analysis–confirmed antibodies against B burgdorferi. Ten of 13 dogs with I scapularis were from clinics within or immediately adjacent to the known tick invasion zone. Six of 18 I scapularis and 12 of 60 noncompetent vector ticks were infected with B burgdorferi. No ticks were infected with Anaplasma phagocytophilum, and 3 were infected with Babesia spp.

Conclusions and Clinical Relevance—Serosurvey in dogs was found to be ineffective in tracking early invasion dynamics of I scapularis in this area. Tick chemoprophylaxis likely reduces serosurvey sensitivity in dogs. Ticks infected with B burgdorferi were more common and widely dispersed than seropositive dogs. In areas of low tick density, use of dogs as a source of ticks is preferable to serosurvey for surveillance of emerging Lyme disease. Impact for Human Medicine—By retaining ticks from dogs for identification and pathogen testing, veterinarians can play an important role in early detection in areas with increasing risk of Lyme disease.

Abstract

Objective—To evaluate dogs as a sentinel species for emergence of Lyme disease in a region undergoing invasion by Ixodes scapularis.

Sample Population—353 serum samples and 78 ticks obtained from dogs brought to 18 veterinary clinics located in the lower peninsula of Michigan from July 15, 2005, through August 15, 2005.

Procedures—Serum samples were evaluated for specific antibodies against Borrelia burgdorferi by use of 3 serologic assays. Ticks from dogs were subjected to PCR assays for detection of pathogens.

Results—Of 353 serum samples from dogs in 18 counties in 2005, only 2 (0.6%) contained western blot analysis–confirmed antibodies against B burgdorferi. Ten of 13 dogs with I scapularis were from clinics within or immediately adjacent to the known tick invasion zone. Six of 18 I scapularis and 12 of 60 noncompetent vector ticks were infected with B burgdorferi. No ticks were infected with Anaplasma phagocytophilum, and 3 were infected with Babesia spp.

Conclusions and Clinical Relevance—Serosurvey in dogs was found to be ineffective in tracking early invasion dynamics of I scapularis in this area. Tick chemoprophylaxis likely reduces serosurvey sensitivity in dogs. Ticks infected with B burgdorferi were more common and widely dispersed than seropositive dogs. In areas of low tick density, use of dogs as a source of ticks is preferable to serosurvey for surveillance of emerging Lyme disease. Impact for Human Medicine—By retaining ticks from dogs for identification and pathogen testing, veterinarians can play an important role in early detection in areas with increasing risk of Lyme disease.

  • 1.

    Steere AC, Coburn J, Glickstein L. The emergence of Lyme disease. J Clin Invest 2004;113:10931101.

  • 2.

    Appel MJG, Allan S, Jacobson RH, et al. Experimental Lyme disease in dogs produces arthritis and persistent infection. J Infect Dis 1993;167:651664.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Hamer SA, Roy PL, Hickling GJ, et al. Zoonotic pathogens in Ixodes scapularis, Michigan. Emerg Infect Dis 2007;13:11311133.

  • 4.

    Pinger RR, Timmons L, Karris K. Spread of Ixodes scapularis (Acari: Ixodidae) in Indiana: collections of adults in 1991–1994 and description of a Borrelia burgdorferi-infected population. J Med Entomol 1996;33:852855.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Falco RC, Smith HA, Fish D, et al. The distribution of canine exposure to Borrelia burgdorferi in a Lyme disease endemic area. Am J Public Health 1993;83:13051310.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Merino FJ, Serrano JL, Saz JV, et al. Epidemiological characteristics of dogs with Lyme borreliosis in the province of Soria (Spain). Eur J Epidemiol 2000;16:97100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Guerra MA, Walker ED, Kitron U. Canine surveillance system for Lyme borreliosis in Wisconsin and northern Illinois: geographic distribution and risk factor analysis. Am J Trop Med Hyg 2001;65:546552.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Bhide M, Travnicek M, Curlik J, et al. The importance of dogs in eco-epidemiology of Lyme borreliosis: a review. Vet Med (Praha) 2004;49:135142.

    • Search Google Scholar
    • Export Citation
  • 9.

    Eng TR, Wilson ML, Spielman A, et al. Greater risk of Borrelia burgdorferi infection in dogs than in people. J Infect Dis 1988;158:14101411.

  • 10.

    Jones TF, Garman RL, LaFleur B, et al. Risk factors for tick exposure and suboptimal adherence to preventive recommendations. Am J Prev Med 2002;23:4750.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Rand PW, Smith RP, Lacombe EH. Canine seroprevalence and the distribution of Ixodes dammini in an area of emerging Lyme disease. Am J Public Health 1991;81:13311334.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Rand PW, Lacombe EH, Smith RP, et al. Low seroprevalence of human Lyme disease near a focus of high entomologic risk. Am J Trop Med Hyg 1996;55:160164.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Duncan AW, Correa MT, Levine JF, et al. The dog as a sentinel for human infection: prevalence of Borrelia burgdorferi C6 antibodies in dogs from southeastern and mid-Atlantic states. Vector Borne Zoonotic Dis 2004;4:221229.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Gauthier DT, Mansfield LS. Western immunoblot analysis for distinguishing vaccination and infection status with Borrelia burgdorferi (Lyme disease) in dogs. J Vet Diagn Invest 1999;11:259265.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Lindenmayer J, Weber M, Bryant J, et al. Comparison of indirect immunofluorescent antibody assay, enzyme-linked immunosorbent assay, and western immunoblot for the diagnosis of Lyme disease in dogs. J Clin Microbiol 1990;28:9296.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Levy SA, O'Connor TP, Hanscom JL, et al. Evaluation of a canine C6 ELISA Lyme disease test for the determination of the infection status of cats naturally exposed to Borrelia burgdorferi. Vet Ther 2003;4:172177.

    • Search Google Scholar
    • Export Citation
  • 17.

    Walker ED, Stobierski MG, Poplar ML, et al. Geographic distribution of ticks (Acari: Ixodidae) in Michigan, with emphasis on Ixodes scapularis and Borrelia burgdorferi. J Med Entomol 1998;35:872882.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Durden LA, Keirans JE. Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification key, distribution, hosts, and medical/veterinary importance. Lanham, Md: Entomological Society of America, 1996.

    • Search Google Scholar
    • Export Citation
  • 19.

    Sonenshine DE. Ticks of Virginia. Blacksburg, Va: Virginia Polytechnic Institute and State University, College of Agriculture and Life Sciences, 1979.

    • Search Google Scholar
    • Export Citation
  • 20.

    Bunikis J, Garpmo U, Tsao J, et al. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 2004;150:17411755.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Zeidner NS, Burkot TR, Massung R, et al. 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 2000;182:616619.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Steiner FE, Pinger RR, Vann CN, et al. Detection of Anaplasma phagocytophilum and Babesia odocoilei DNA in Ixodes scapularis (Acari: Ixodidae) collected in Indiana. J Med Entomol 2006;43:437442.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Armstrong PM, Katavolos P, Caporale DA, et al. Diversity of Babesia infecting deer ticks (Ixodes dammini). Am J Trop Med Hyg 1998;58:739742.

  • 24.

    R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2006.

    • Search Google Scholar
    • Export Citation
  • 25.

    Burgess EC. Natural exposure of Wisconsin dogs to the Lyme disease spirochete (Borrelia burgdorferi). Lab Anim Sci 1986;36:288290.

  • 26.

    Magnarelli LA, Anderson JF, Schreier AB, et al. Clinical and serologic studies of canine borreliosis. J Am Vet Med Assoc 1987;191:10891094.

    • Search Google Scholar
    • Export Citation
  • 27.

    Wright JC, Chambers M, Mullen GR, et al. Seroprevalence of Borrelia burgdorferi in dogs in Alabama, USA. Prev Vet Med 1997;31:127131.

  • 28.

    Cohen ND, Carter CN, Thomas MA Jr, et al. Clinical and epizootiologic characteristics of dogs seropositive for Borrelia burgdorferi in Texas: 110 cases (1988). J Am Vet Med Assoc 1990;197:893898.

    • Search Google Scholar
    • Export Citation
  • 29.

    Stone EG, Lacombe EH, Rand PW. Antibody testing and Lyme disease risk. Emerg Infect Dis 2005;11:722724.

  • 30.

    Hinrichsen VL, Whitworth UG, Breitschwerdt EB, et al. Assessing the association between the geographic distribution of deer ticks and seropositivity rates to various tick-transmitted disease organisms in dogs. J Am Vet Med Assoc 2001;218:10921097.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Walker ED, Smith TW, Dewitt J, et al. Prevalence of Borrelia burgdorferi in host-seeking ticks (Acari, Ixodidae) from a Lyme disease endemic area in Northern Michigan. J Med Entomol 1994;31:524528.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Piesman J, Sinsky RJ. Ability of Ixodes scapularis, Dermacentor variabilis, and Amblyomma americanum (Acari, Ixodidae) to acquire, maintain, and transmit Lyme disease spirochetes (Borrelia burgdorferi). J Med Entomol 1988;25:336339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Randolph SE, Gern L, Nuttall PA. Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol Today 1996;12:472479.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Piesman J, Happ CM. The efficacy of co-feeding as a means of maintaining Borrelia burgdorferi: a North American model system. J Vector Ecol 2001;26:216220.

    • Search Google Scholar
    • Export Citation

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