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Invasion of the Lyme Disease Vector Ixodes scapularis: Implications for Borrelia burgdorferi Endemicity

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Abstract

Lyme disease risk is increasing in the United States due in part to the spread of blacklegged ticks Ixodes scapularis, the principal vector of the spirochetal pathogen Borrelia burgdorferi. A 5-year study was undertaken to investigate hypothesized coinvasion of I. scapularis and B. burgdorferi in Lower Michigan. We tracked the spatial and temporal dynamics of the tick and spirochete using mammal, bird, and vegetation drag sampling at eight field sites along coastal and inland transects originating in a zone of recent I. scapularis establishment. We document northward invasion of these ticks along Michigan’s west coast during the study period; this pattern was most evident in ticks removed from rodents. B. burgdorferi infection prevalences in I. scapularis sampled from vegetation in the invasion zone were 9.3% and 36.6% in nymphs and adults, respectively, with the majority of infection (95.1%) found at the most endemic site. There was no evidence of I. scapularis invasion along the inland transect; however, low-prevalence B. burgdorferi infection was detected in other tick species and in wildlife at inland sites, and at northern coastal sites in years before the arrival of I. scapularis. These infections suggest that cryptic B. burgdorferi transmission by other vector-competent tick species is occurring in the absence of I. scapularis. Other Borrelia spirochetes, including those that group with B. miyamotoi and B. andersonii, were present at a low prevalence within invading ticks and local wildlife. Reports of Lyme disease have increased significantly in the invasion zone in recent years. This rapid blacklegged tick invasion—measurable within 5 years—in combination with cryptic pathogen maintenance suggests a complex ecology of Lyme disease emergence in which wildlife sentinels can provide an early warning of disease emergence.

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References

  • Alerstam T (1978) Re-oriented bird migration in coastal areas: dispersal to suitable resting grounds. Oikos 30:405-408

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215:403-410

    CAS  Google Scholar 

  • Anderson JF, Magnarelli LA, Lefebvre RB, Andreadis TG, McAninch JB, Perng GC, Johnson RC (1989) Antigenically variable Borrelia burgdorferi isolated from cottontail rabbits and Ixodes dentatus in rural and urban areas. Journal of Clinical Microbiology 27:13-20

    CAS  Google Scholar 

  • Bacon RM, Kugeler KJ, Griffith KS, Mead PS (2008) Surveillance for Lyme disease - United States, 1992-2006. Morbidity and Mortality Weekly Report 56:1-9

    Google Scholar 

  • Barbour AG, Bunikis J, Travinsky B, Hoen AG, Diuk-Wasser MA, Fish D, Tsao JI (2009) Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. American Journal of Tropical Medicine and Hygiene 81:1120-1131

    Article  Google Scholar 

  • Bouseman JK, Kitron U, Kirkpatrick CE, Siegel J, Todd KS (1990) Status of Ixodes dammini (Acari, Ixodidae) in Illinois. Journal of Medical Entomology 27:556-560

    CAS  Google Scholar 

  • Brown RN, Lane RS (1992) Lyme disease in California: a novel enzootic transmission cycle of Borrelia burgdorferI. Science 256:1439-1442

    Article  CAS  Google Scholar 

  • Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG (2004) Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150:1741-1755

    Article  CAS  Google Scholar 

  • Cortinas MR, Kitron U (2006) County-level surveillance of white-tailed deer infestation by Ixodes scapularis and Dermacentor albipictus (Acari: Ixodidae) along the Illinois River. Journal of Medical Entomology 43:810-819

    Article  Google Scholar 

  • Daniels TJ, Falco RC, Curran KL, Fish D (1996) Timing of Ixodes scapularis (Acari: Ixodidae) oviposition and larval activity in southern New York. Journal of Medical Entomology 33:140-147

    CAS  Google Scholar 

  • Dennis DT, Nekomoto TS, Victor JC, Paul WS, Piesman J (1998) Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari : Ixodidae) in the United States. Journal of Medical Entomology 35:629-638

    CAS  Google Scholar 

  • Diehl RH, Larkin RP, Black JE (2003) Radar observations of bird migration over the Great Lakes. Auk 120:278-290

    Article  Google Scholar 

  • Diuk-Wasser MA, Gatewood AG, Cortinas MR, Yaremych-Hamer S, Tsao J, Kitron U, et al. (2006). Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari : Iodidae) in the United States. Journal of Medical Entomology 43:166-176

    Article  CAS  Google Scholar 

  • Drew ML, Loken KI, Bey RF, Swiggum RD (1988) Ixodes dammini - occurrence and prevalence of infection with Borrelia species in Minnesota. Journal of Wildlife Diseases 24:708-710

    CAS  Google Scholar 

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

  • Falco RC, Daniels TJ, Fish D (1995) Increase in abundance of immature Ixodes scapularis (Acari: Ixodidae) in an emergent Lyme disease endemic area. Journal of Medical Entomology 32:522-526

    CAS  Google Scholar 

  • Falco RC, Fish D (1992) A comparison of methods for sampling the deer tick, Ixodes dammini, in a Lyme disease endemic area. Experimental & Applied Acarology 14:165-173

    Article  CAS  Google Scholar 

  • Fish D (1993) Population ecology of Ixodes damminI. In: Ecology and Environmental Management of Lyme Disease, Ginsberg HS (editor), New Brunswick, NJ: Rutgers University Press

    Google Scholar 

  • Fish D, Daniels TJ (1990) The role of medium-sized mammals as reservoirs of Borrelia burgdorferi in Southern New York. Journal of Wildlife Diseases 26:339-345

    CAS  Google Scholar 

  • Foster ES (2004) Ixodes scapularis (Acari: Ixodidae) and Borrelia burgdorferi in southwest Michigan: population ecology and verification of a geographic risk model. Masters Thesis, Michigan State University, East Lansing

  • Gatewood AG, Liebman KA, Vourc’h G, Bunikis J, Hamer SA, Cortinas R, et al. (2009) Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Applied and Environmental Microbiology 75:2476-2483

    Article  CAS  Google Scholar 

  • Githeko AK, Lindsay SW, Confalonieri UE, Patz JA (2000) Climate change and vector-borne diseases: a regional analysis. Bulletin of the World Health Organization 78:1136-1147

    CAS  Google Scholar 

  • Godsey MS, Amundson TE, Burgess EC, Schell W, Davis JP, Kaslow R, et al. (1987) Lyme disease ecology in Wisconsin: distribution and host preferences of Ixodes dammini, and prevalence of antibody to Borrelia burgdorferi in small mammals. American Journal of Tropical Medicine and Hygiene 37:180-187

    Google Scholar 

  • Guerra M, Walker E, Jones C, Paskewitz S, Cortinas MR, Stancil A, Beck L, Bobo M, Kitron U (2002) Predicting the risk of Lyme disease: habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8:289-297

    Article  Google Scholar 

  • Hamer SA, Roy PL, Hickling GJ, Walker ED, Foster ES, Barber CC, Tsao JI (2007) Zoonotic pathogens in Ixodes scapularis, Michigan. Emerging Infectious Diseases 13:1131-1133

    Google Scholar 

  • Hamer SA, Tsao JI, Walker ED, Mansfield LS, Foster ES, Hickling GJ (2009) Use of tick surveys and serosurveys to evaluate pet dogs as a sentinel species for emerging Lyme disease. American Journal of Veterinary Research 70:49-56

    Article  Google Scholar 

  • Jackson JO, DeFoliart GR (1970) Ixodes scapularis say in Northern Wisconsin. Journal of Medical Entomology 7:124-125

    CAS  Google Scholar 

  • Jones CJ, Kitron UD (2000) Populations of Ixodes scapularis (Acari : Ixodidae) are modulated by drought at a Lyme disease focus in Illinois. Journal of Medical Entomology 37:408-415

    Article  CAS  Google Scholar 

  • Keirans JE, Clifford CM (1978) The genus Ixodes in the United States: a scanning electron microscope study and key to the adults. Journal of Medical Entomology Supplements 2:1-149

    CAS  Google Scholar 

  • Kitron U, Jones CJ, Bouseman JK (1991) Spatial and temporal dispersion of immature Ixodes dammini on Peromyscus leucopus in northwestern Illinois. The Journal of Parasitology 77:945-949

    Article  CAS  Google Scholar 

  • Lindgren E, Gustafson R (2001) Tick-borne encephalitis in Sweden and climate change. The Lancet 358:16-18

    Article  CAS  Google Scholar 

  • Liveris D, Gazumyan A, Schwartz I (1995) Molecular typing of Borrelia burgdorferi sensu lato by PCR restriction fragment length polymorphism analysis. Journal of Clinical Microbiology 33:589-595

    CAS  Google Scholar 

  • Lord R, Humphreys J, Lord V, McLean R, Garland C (1992) Borrelia burgdorferi infection in white-footed mice (Peromyscus leucopus) in hemlock (Tsuga canadensis) habitat in western Pennsylvania. Journal of Wildlife Diseases 28:364-368

    CAS  Google Scholar 

  • Lord RD, Lord VR, Humphreys JG, McLean RG (1994) Distribution of Borrelia burgdorferi in host mice in Pennsylvania. Journal of Clinical Microbiology 32:2501-2504

    CAS  Google Scholar 

  • Madhav NK, Brownstein JS, Tsao JI, Fish D (2004) A dispersal model for the range expansion of blacklegged tick (Acari : Ixodidae). Journal of Medical Entomology 41:842-852

    Article  Google Scholar 

  • Magnarelli LA, Anderson JF, Durland F (1987). Transovarial transmission of Borrelia burgdorferi in Ixodes dammini (Acari:Ixodidae). The Journal of Infectious Diseases 156:234-236

    CAS  Google Scholar 

  • Marconi RT, Liveris D, Schwartz I (1995) Identification of novel insertion elements, restriction fragment length polymorphism patterns, and discontinuous 23S ribosomal RNA in Lyme disease spirochetes: phylogenetic analyses of ribosomal RNA genes and their intergenic spacers in Borrelia japonica sp. nov and genomic group (Borrelia andersonii sp nov) isolates. Journal of Clinical Microbiology 33:2427-2434

    CAS  Google Scholar 

  • Maupin GO, Gage KL, Piesman J, Montenieri J, Sviat SL, Vanderzanden L, Happ CM, Dolan M, Johnson BJ (1994). Discovery of an enzootic cycle of Borrelia burgdorferi in Neotoma mexicana and Ixodes spinipalpis from northern Colorado, an area where Lyme disease is nonendemic. Journal of Infectious Diseases 170:636-643

    CAS  Google Scholar 

  • MDNR (2002) Deer management history in Michigan. Michigan Department of Natural Resources. Available: http://www.michigan.gov/dnr/0,1607,7-153-10363_10856_10905-28543–,00.html. Accessed 1 Dec 2009

  • Ogden NH, Lindsay RL, Hanincova K, Barker IK, Bigras-Poulin M, Charron DF, Heagy A, Francis CM, O’Callaghan CJ, Schwartz I, Thompson RA (2008) Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Applied and Environmental Microbiology 74:3919-3919

    Article  CAS  Google Scholar 

  • Oliver JH, Lin T, Gao L, Clark KL, Banks CW, Durden LA, James AM, Chandler FW Jr (2003) An enzootic transmission cycle of Lyme borreliosis spirochetes in the southeastern United States. Proceedings of the National Academy of Sciences of the United States of America 100:11642-11645

    Article  CAS  Google Scholar 

  • Piesman J, Sinsky RJ (1988) Ability of Ixodes scapularis, Dermacentor variabilis, and Amblyomma americanum (Acari, Ixodidae) to acquire, maintain, and transmit Lyme disease spirochetes (Borrelia burgdorferi). Journal of Medical Entomology 25:336-339

    CAS  Google Scholar 

  • Pinger RR, Glancy T (1989) Ixodes dammini (Acari, Ixodidae) in Indiana. Journal of Medical Entomology 26:130-131

    CAS  Google Scholar 

  • Pinger RR, Timmons L, Karris K (1996) Spread of Ixodes scapularis (Acari: Ixodidae) in Indiana: collections of adults in 1991-1994 and description of a Borrelia burgdorferi-infected population. Journal of Medical Entomology 33:852-855

    CAS  Google Scholar 

  • Randolph SE (2004) Evidence that climate change has caused `emergence’ of tick-borne diseases in Europe? International Journal of Medical Microbiology Supplements 293:5-15

    Article  Google Scholar 

  • Ryder JW, Pinger RR, Glancy T (1992) Inability of Ixodes cookei and Amblyomma americanum nymphs (Acari, Ixodidae) to transmit Borrelia burgdorferI. Journal of Medical Entomology 29:525-530

    CAS  Google Scholar 

  • Schulze TL, Jordan RA, Hung RW (1998) Comparison of Ixodes scapularis (Acari: Ixodidae) populations and their habitats in established and emerging Lyme disease areas in New Jersey. Journal of Medical Entomology 35:64-70

    CAS  Google Scholar 

  • Schulze TL, Jordan RA, Hung RW (2001) Effects of selected meteorological factors on diurnal questing of Ixodes scapularis and Amblyomma americanum (Acari : Ixodidae). Journal of Medical Entomology 38:318-324

    Article  CAS  Google Scholar 

  • Schulze TL, Jordan RA, Hung RW, Puelle RS, Markowski D, Chomsky MS (2003) Prevalence of Borrelia burgdorferi (Spirochaetales : Spirochaetaceae) in Ixodes scapularis (Acari : Ixodidae) adults in New Jersey, 2000-2001. Journal of Medical Entomology 40:555-558

    Article  Google Scholar 

  • Sonenshine DE (1979) Ticks of Virginia. Virginia Polytechnic Institute and State University, College of Agriculture and Life Sciences, Blacksburg, VA

    Google Scholar 

  • Sonenshine DE, Ratzlaff RE, Troyer J, Demmerle S, Demmerle ER, Austin WE, et al. (1995) Borrelia burgdorferi in Eastern Virginia: comparison between a coastal and inland locality. American Journal of Tropical Medicine and Hygiene 53:123-133

    CAS  Google Scholar 

  • Stafford KC 3rd, Cartter ML, Magnarelli LA, Ertel SH, Mshar PA (1998) Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. Journal of Clinical Microbiology 36:1240-1244

    Google Scholar 

  • Steere AC, Coburn J, Glickstein L (2004) The emergence of Lyme disease. Journal of Clinical Investigation 113:1093-1101

    CAS  Google Scholar 

  • Strand MR, Walker ED, Merritt RW (1992) Field studies on Ixodes dammini in the Upper Peninsula of Michigan. Vector Control Bulletin of North Central States 1:11-18

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596-1599

    Article  CAS  Google Scholar 

  • Telford SR, Mather TN, Moore SI, Wilson ML, Spielman A (1988) Incompetence of deer as reservoirs of the Lyme disease spirochete. American Journal of Tropical Medicine and Hygiene 39:105-109

    Google Scholar 

  • Telford SR, Spielman A (1989a) Competence of a rabbit feeding Ixodes (Acari, Ixodidae) as a vector of the Lyme disease spirochete. Journal of Medical Entomology 26:118-121

    Google Scholar 

  • Telford SR, Spielman A (1989b) Enzootic transmission of the agent of Lyme disease in rabbits. American Journal of Tropical Medicine and Hygiene 41:482-490

    Google Scholar 

  • Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, Barbour AG (2004) An ecological approach to preventing human infection: Vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences of the United States of America 101:18159-18164

    Article  CAS  Google Scholar 

  • Walker ED, Stobierski MG, Poplar ML, Smith TW, Murphy AJ, Smith PC, Schmitt SM, Cooley TM, Kramer CM (1998) Geographic distribution of ticks (Acari : Ixodidae) in Michigan, with emphasis on Ixodes scapularis and Borrelia burgdorferI. Journal of Medical Entomology 35:872-882

    CAS  Google Scholar 

  • Wormser GP, Liveris D, Nowakowski J, Nadelman RB, Cavaliere LF, McKenna D, Holmgren D, Schwartz I (1999) Association of specific subtypes of Borrelia burgdorferi with hematogenous dissemination in early Lyme disease. The Journal of Infectious Diseases 180:720-725

    Article  CAS  Google Scholar 

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Acknowledgments

We thank M. Rosen, J. Sidge, T. Lickfett, N. Ochmanek, L. Alexander, E. Foster, G. Hamer, R. Henke, M. Kauffman, C. Niebuhr, P. Roy, and A. Rydecki for assistance with trapping, dragging, and laboratory work. J. Piesman and G. Dietrich at the Centers for Disease Control and Prevention provided infected ticks for use as controls. Two anonymous reviewers provided helpful comments. This study was funded by cooperative agreement no. cI00171-01 from the Centers for Disease Control and Prevention (graduate assistantship to SAH), and G. H. Lauff Research Award and the T. Wayne and Katherine Porter Fellowships from Kellogg Biological Station. This is Kellogg Biological Station Contribution no. 1552.

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Authors and Affiliations

  1. Department of Fisheries and Wildlife, Michigan State University, 13 Natural Resources Building, East Lansing, MI, 48824, USA

    Sarah A. Hamer & Jean I. Tsao

  2. Department of Large Animal Clinical Sciences, Michigan State University, East Lansing, MI, 48824, USA

    Jean I. Tsao

  3. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, 48824, USA

    Edward D. Walker

  4. Center for Wildlife Health/NIMBioS, The National Institute for Mathematical and Biological Synthesis, University of Tennessee, 1534 White Ave., Knoxville, TN, 37996-1527, USA

    Graham J. Hickling

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  1. Sarah A. Hamer
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Correspondence to Sarah A. Hamer.

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10393_2010_287_MOESM1_ESM.pdf

Supplementary material 1 (Bird-tick infestation prevalences on the inland and coastal transects in Lower Michigan, May–June, 2004–2008. Number of birds carrying larvae/nymphs/adults is indicated with the percent of birds infested with at least one tick of any life stage in parenthesis. All ticks were tested for Borrelia burgdorferi; those birds with infected ticks are indicated in Supplementary Material 2)

10393_2010_287_MOESM2_ESM.pdf

Supplementary material 2 (Infection prevalence of each species of tick removed from mammalian and avian hosts in Lower Michigan, May–June, 2004–2008. Infection prevalence is presented as the percent of ticks that tested positive with the sample size of ticks tested in parenthesis. Larval infection is reported as the minimum infection prevalence. LL = larvae; NN = nymph; AA = adult. Regarding birds, only those species with positive ticks are listed below; a complete list of all 56 bird species and associated ticks is provided in Supplementary Material 1)

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Hamer, S.A., Tsao, J.I., Walker, E.D. et al. Invasion of the Lyme Disease Vector Ixodes scapularis: Implications for Borrelia burgdorferi Endemicity. EcoHealth 7, 47–63 (2010). https://doi.org/10.1007/s10393-010-0287-0

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