Abstract
Lyme disease (LD), the most frequently reported vector-borne disease in the United States, requires that humans, infected vector ticks, and infected hosts all occur in close spatial proximity. Understanding the spatial dynamics of LD requires an understanding of the spatial determinants of each of these organisms. We review the literature on spatial patterns and environmental correlates of human cases of LD and the vector ticks, Ixodes scapularis in the northeastern and midwestern United States and Ixodes pacificus in the western United States. The results of this review highlight a need for a more standardized and comprehensive approach to studying the spatial dynamics of the LD system. Specifically, we found that the only environmental variable consistently associated with increased LD risk and incidence was the presence of forests. However, the reasons why some forests are associated with higher risk and incidence than others are still poorly understood. We suspect that the discordance among studies is due, in part, to the rapid developments in both conceptual and technological aspects of spatial ecology hastening the obsolescence of earlier approaches. Significant progress in identifying the determinants of spatial variation in LD risk and incidence requires that: (1) existing knowledge of the biology of the individual components of each LD system is utilized in the development of spatial models; (2) spatial data are collected over longer periods of time; (3) data collection and analysis among regions are more standardized; and (4) the effect of the same environmental variables is tested at multiple spatial scales.
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References
Allan BF, Keesing F, Ostfeld RS (2003) Effects of forest fragmentation on Lyme disease risk. Conservation Biology 17:267–272
Amerasinghe FP, Breisch NL, Azad LA, Gimpel WF, Greco M, Neidhardt K, et al. (1992) Distribution, density, and Lyme disease spirochete infection in Ixodes dammini (Acari: Ixodidae) on white-tailed deer in Maryland. Journal of Medical Entomology 29:54–61
Anderson JF, Russell RC, Magnarelli LA, Hyde FW, Myers JE (1987) Prevalence of Borrelia burgdorferi and Babesia microti in mice on islands inhabited by white-tailed deer. Applied and Environmental Microbiology 53:892–894
Belozerov VN (1982) Diapause and biological rhythms in ticks. In: Physiology of Ticks, Obenchain FD, Galun R (editors), New York: Pergamon Press, pp 469–500
Brisson D, Dykhuizen DE, Ostfeld RS (2008) Conspicuous impacts of inconspicuous hosts drive the human Lyme disease epidemic. Proceedings of the Royal Society of London. Series B: Biological Sciences (London)275:227–235
Brown RN, Lane RS (1992) Lyme disease in California: a novel enzootic transmission cycle of Borrelia burgdorferi. Science 256:1439–1442
Brown RN, Lane RS (1996) Reservoir competence of four chaparral-dwelling rodents for Borrelia burgdorferi in California. American Journal of Tropical Medicine and Hygiene 54:84–91
Brownstein JS, Holford TR, Fish D (2003) A climate-based model predicts the spatial distribution of the Lyme disease vector Ixodes scapularis in the United States. Environmental Health Perspectives 111:1152–1157
Brownstein JS, Skelly DK, Holford TR, Fish D (2005) Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146:469–475
Bunnell JE, Price SD, Das A, Shields TM, Glass GE (2003) Geographic information systems and spatial analysis of adult Ixodes scapularis (Acari: Ixodidae) in the Middle Atlantic region of the USA. Journal of Medical Entomology 40:570–576
Carroll JF, Kramer M (2001) Different activities and footwear influence exposure to host-seeking nymphs of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae). Journal of Medical Entomology 38:596–600
Centers for Disease Control, Prevention (CDC) (2007) Lyme disease—United States, 2003–2005. Morbidity and Mortality Weekly Report 56:573–576
Chen H, White DJ, Caraco TB, Stratton HH (2005) Epidemic and spatial dynamics of Lyme disease in New York State, 1990–2000. Journal of Medical Entomology 42:899–908
Connally NP, Ginsberg HS, Mather TN (2006) Assessing peridomestic entomological factors as predictors for Lyme disease. Journal of Vector Ecology 31:364–370
Cromley EK, Cartter ML, Mrozinski RD, Ertel SH (1998) Residential setting as a risk factor for Lyme disease in a hyperendemic region. American Journal of Epidemiology 147:472–477
Daniel M, Danielová V, Kríz B, Jirsa A, Nozicka J (2003) Shift of the tick Ixodes ricinus and tick-borne encephalitis to higher altitudes in Central Europe. European Journal of Clinical Microbiology and Infectious Disease 22:327–328
Dennis DT, Hayes EB (2002) Epidemiology of Lyme borreliosis. In: Gray JS, Kahl O, Lane RS, Stanek G (editors), Lyme Borreliosis Biology, Epidemiology and Control, New York: CABI Publishing, pp 251–280
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
Dister SW, Fish D, Bros SM, Frank DH, Wood BL (1997) Landscape characterization of peridomestic risk for Lyme disease using satellite imagery. American Journal of Tropical Medicine and Hygiene 57:687–692
Duik-Wasser MA, Gatewood AG, Cortinas MR, Yaremych-Hamer S, Tsao T, Kitron U, et al (2006) Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. Journal of Medical Entomology 43:166–176
Duffy DC, Clark DD, Campbell SR, Gurney S, Perello R, Simon N (1994) Landscape patterns of abundance of Ixodes-scapularis (Acari, Ixodidae) on Shelter Island, New York. Journal of Medical Entomology 31:875–879
Eisen RJ, 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. Environmental Entomology 32:1010–1018
Eisen RJ, Eisen L, Lane RS (2001) Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentalis) in northern California: temporal trends and environmental correlates. Journal of Parasitology 87:1301–1307
Eisen RJ, Eisen L, Lane RS (2006a) 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. American Journal of Tropical Medicine and Hygiene 74:632–640
Eisen RJ, Lane RS, Fritz CL, Eisen L (2006b) Spatial patterns of Lyme disease risk in California based on disease incidence data and modeling of vector-tick exposure. American Journal of Tropical Medicine and Hygiene 75:669–676
Estrada-Peña A (2001) Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in northern Spain. Journal of Medical Entomology 38:361–370
Estrada-Peña A (2002) Increasing habitat suitability in the United States for the tick that transmits Lyme disease: a remote sensing approach. Environmental Health Perspectives 110:635–640
Falco RC, Fish D (1988) Prevalence of Ixodes dammini near the homes of Lyme disease patients in Westchester County, New York. American Journal of Epidemiology 127:826–830
Fix AD, Peña CA, Strickland GT (2000) Racial differences in reported Lyme disease incidence. American Journal of Epidemiology 152:756–759
Frank DH, Fish D, Moy FH (1998) Landscape features associated with Lyme disease risk in a suburban residential environment. Landscape Ecology 13:27–36
Glass GE, Amerasinghe FP, Morgan JM, Scott TW (1994) Predicting Ixodes-scapularis abundance on white-tailed deer using geographic information-systems. American Journal of Tropical Medicine and Hygiene 51:538–544
Glass GE, Schwartz BS, Morgan JM, Johnson DT, Noy PM, Israel E (1995) Environmental risk-factors for Lyme-disease identified with geographic information-systems. American Journal of Public Health 85:944–948
Glavanakov S, White DJ, Caraco T, Lapenis A, Robinson GR, Szymanski BK, et al (2001) Lyme disease in New York State: spatial pattern at a regional scale. American Journal of Tropical Medicine and Hygiene 65:538–545
Goddard J (1992) Ecological studies of adult Ixodes scapularis in central Mississippi: questing activity in relation to time of year, vegetation type and meteorological conditions. Journal of Medical Entomology 29:501–506
Gray JS, Kahl O, Janetzki C, Stein J (1992) Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology 29:915–920
Guerra M, Walker E, Jones C, Paskewitz S, Cortinas MR, Stancil A et al (2002) Predicting the risk of Lyme disease: habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8:289–297
Horobik V, Keesing F, Ostfeld RS (2006) Abundance and Borrelia burgorferi-infection prevalence of nymphal Ixodes scapularis ticks along forest-field edges. EcoHealth 3:232–238
Jackson LE, Hilborn ED, Thomas JC (2006a) Towards landscape design guidelines for reducing Lyme disease risk. International Journal of Epidemiology 35:315–322
Jackson LE, Levine JF, Hilborn ED (2006b) A comparison of analysis units for associating Lyme disease with forest edge habitat. Community Ecology 7:189–197
Jensen PM, Hansen H, Frandsen F (2000) Spatial risk assessment for Lyme borreliosis in Denmark. Scandanavian Journal of Infectious Disease 32:545–550
Jordon RA, Schulze TL (2005) Deer browsing and the distribution of Ixodes scapularis (Acari: Ixodidae) in central New Jersey forests. Environmental Entomology 34:801–805
Jouda F, Perret J, Gern L (2004) Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. Journal of Medical Entomology 41:162–169
Kitron U, Kazmierczak JJ (1997) Spatial analysis of the distribution of Lyme disease on Wisconsin. American Journal of Epidemiology 145:558–566
Kitron U, Bouseman JK, Jones CJ (1991) Use of the Arc Info GIS to study the distribution of Lyme-disease ticks in an Illinois county. Preventive Veterinary Medicine 11:243–248
Knelle W, Rudolph D (1982) Humidity relationships and water balance of ticks. In: Obenchain FD, Galun R (editors), Physiology of Ticks, New York: Pergamon, pp 43–70
Lane RS (1990) Susceptibility of western fence lizard (Sceloporus occidentalis) to the Lyme borreliosis spirochete (Borrelia burgdorferi). American Journal of Tropical Medicine and Hygiene 42:75–82
Lane RS, Brown RN (1991) Wood rats and kangaroo rats: potential reservoirs of the Lyme disease spirochete in California. Journal of Medical Entomology 28:299–302
Lane RS, Loye JE (1989) Lyme disease in California: interrelationship of Ixodes pacificus (Acari: Ixodidae), the western fence lizard (Sceloporus occidentalis), and Borrelia burgdorferi. Journal of Medical Entomology 26:272–278
Lane RS, Quistad GB (1998) Borreliacidal factor in the blood of the western fence lizard (Scelaporus occidentalis). The Journal of Parasitology 84:29–34
Lane RS, Mun J, Eisen RJ, Eisen L (2005) Western gray squirrel (Rodential: Sciuridae): a primary reservoir host of Borrelia burgdorferi in California oak woodlands? Journal of Medical Entomology 42:388–396
Lane RS, Peavey CA, Padgett KA, Hendson M (1999) Life history of Ixodes (Ixodes) jellisoni (Acari: Ixodidae) and its vector competence for Borrelia burgdorferi sensu lato. Journal of Medical Entomology 36:329–340
Lane RS, Piesman J, Burgdorfer W (1991) Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annual Review of Entomology 36:587–609
Lane RS, Steinlein DB, Mun J (2004) Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. Journal of Medical Entomology 41:239–248
Li X, Peavey CA, Lane RS (2000) Density and spatial distribution of Ixodes pacificus (ACARI: IXODIDAE) in two recreational areas in north coastal California. American Journal of Tropical Medicine and Hygiene 62:415–422
Lindgren E, Jaenson TGT (2006) Lyme Borreliosis in Europe: Influences of Climate and Climate Change, Epidemiology, Ecology and Adaptation Measures, Copenhagen, Denmark: World Health Organization, p 34
Lindgren E, Tälleklint L, Polfeldt T (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinuns. Environmental Health Perspectives 108:119–123
LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceeding of the National Academy of Sciences 100:567–571
Lubelczyk CB, Elias SP, Rand PW, Holman MS, Lacombe EH, Smith RP Jr (2004) Habitat associations of Ixodes scapularis (Acari: Ixodidae) in Maine. Environmental Entomology 33:900–906
Mannelli A, Kitron U, Jones CJ, Slajchert TL (1994) Influence of season and habitat on Ixodes scapularis infestation on white-footed mice in northwestern Illinois. Journal of Parisitology 80:1038–1042
Mather TN, Wilson ML, Moore SI, Ribeiro JMC, Speilman A (1989) Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burdoreri). American Journal of Epidemiology 130:143–150
Maupin GO, Fish D, Zultowsky J, Campos EG, Piesman J (1991) Landscape ecology of Lyme disease in a residential area of Westchester County, New York. American Journal of Epidemiology 133:1105–1113
McCabe GJ, Bunnell JE (2004) Precipitation and the occurrence of Lyme disease in the northeastern United States. Vector-borne and Zoonotic Diseases 4:143–148
McEnroe WD (1977) The restriction of the species range of Ixodes scapularis, say, in Massachusetts by fall and winter temperature. Acarologia 18:618–625
McEnroe WD (1984) Winter survival and spring breeding by the fall tick, Ixodes dammini, in Massachusetts (Acarina: Ixodidae). Acarologia 25:223–229
Naleway AL, Belongia EA, Kazmierczak JJ, Greenlee RT, Davis JP (2002) Lyme disease incidence in Wisconsin: a comparison of state-reported rates and rates from a population-based cohort. American Journal of Epidemiology 155:1120–1127
Ogden NH, Digras-Poulin M, O’Callaghan CJ, Barker IK, Lindsay LR, Maarouf A et al (2005) A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. International Journal of Parasitology 35:375–389
Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed MG et al (2006) Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. International Journal for Parasitology 36:63–70
Orloski KA, Campbell GL, Genese CA, Beckley JW, Schriefer ME, Spitalny KC et al (1998) Emergence of Lyme disease in Hunterdon County, New Jersey, 1993: a case-control study of risk factors and evaluation of reporting patterns. American Journal of Epidemiology 147:391–397
Orloski KA, Hayes EB, Campbell GL, Dennis DT (2000) Surveillance for Lyme disease—United States, 1992–1998. Morbidity and Mortality Weekly Report 49:1–11
Ostfeld RS, Keesing F (2000) Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14:722–728
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 Biology 4:1058–1068
Ostfeld RS, Cepeda OM, Hazler KR, Miller MC (1995) Ecology of Lyme disease—habitat associations of ticks (Ixodes-scapularis) in a rural landscape. Ecological Applications 5:353–361
Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology & Evolution 20:328–336
Padgett KA, Lane RS (2001) Life cycle of Ixodes pacificus (Acari: Ixodidae): timing of developmental processes under field and laboratory conditions. Journal of Medical Entomology 38:684–693
Peavey CA, Lane RS (1995) Transmission of Borrlia burgdorferi by Ixodes pacificus nymphs and reservoir competence of deer mice (Peromyscus maniculatus) infected by tick-bite. Journal of Parasitology 81:175–178
Perkins SE, Cattadori IM, Tagliapietra V, Rizzoli AP, Hudson PJ (2006) Localized deer absence leads to tick amplification. Ecology 87:1981–1986
Prusinski MA, Chen H, Drobnack JM, Kogut SJ, Means RG, Howard JJ et al (2006) Habitat structure associated with Borrelia burgdorferi prevalence in small mammals in New York State. Environmental Entomology 35:308–319
Racz GR, Ban E, Ferenczi E, Berencsi G (2006) A simple spatial model to explain the distribution of human tick-borne encephalitis cases in Hungary. Vector-borne and Zoonotic Diseases 6:369–378
Randolph SE (2001) The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences (London) 356:1045–1056
Rand PW, Lubelczyk C, Lavigne GR, Elias S, Holman MS, Lacombe EH, Smith RP Jr (2003) Deer density and the abundance of Ixodes scapularis (Acari: Ixididae). Journal of Medical Entomology 40:179–184
Rodgers SE, Mather TN (2006) Evaluating satellite sensor-derived indices for Lyme disease risk prediction. Journal of Medical Entomology 43:337–343
Rodgers SE, Zolnik CP, Mather TN (2007) Duration of exposure to suboptimal atmospheric moisture affects nymphal blacklegged tick survival. Journal of Medical Entomology 44:372–375
Schauber EM, Ostfeld RS, Evans AS (2005) What is the best predictor of annual Lyme disease incidence: weather, mice or acorns? Ecological Applications 15:575–586
Schulze TL, Jordan RA, Hung RW (2001) Potential effects of animal activity on the spatial distribution of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae). Environmental Entomology 30:568–577
Stafford KC, Magnarelli LA (1993) Spatial and temporal patterns of Ixodes-scapularis (Acari, Ixodidae) in southeastern Connecticut. Journal of Medical Entomology 30:762–771
Subak S (2003) Effects of climate on variability in Lyme disease incidence in the northeastern United States. American Journal of Epidemiology 157:531–538
Tälleklint-Eisen L, Lane RS (2000) Spatial and temporal variation in the density of Ixodes pacificus (Acari: Ixodidae) nymphs. Environmental Entomology 29:272–280
Waller LA, Goodwin BJ, Wilson ML, Ostfeld RS, Marshall SL, Hayes EB (2007) Spatio-temporal patterns in county-level incidence and reporting of Lyme disease in the northeastern United States, 1990–2000. Environmental and Ecological Statistics 14:83–100
Westrom DR, Lane RS, Anderson JR (1985) Ixodes pacificus (Acari: Ixodidae): population dynamics and distribution on Columbian black-tailed deer (Odocoileus hemionus columbianus). Journal of Medical Entomology 22:507–511
Wilson ML, Adler GH, Speilman A (1985) Correlation between abundance of deer and that of the deer tick, Ixodes dammini (Acari: Ixodidae). Annals of the Entomological Society of America 78:172–176
Wilson ML, Ducey AM, Litwin TS, Gavin TA, Speilman A (1990) Microgeographic distribution of immature Ixodes dammini ticks correlated with that deer. Medical and Veterinary Entomology 4:151–159
Wilson ML, Telford SRI, Piesman J, Speilman A (1988) Reduced abundance of immature Ixodes dammini (Acari: Ixodidae) following removal of deer. Journal of Medical Entomology 25:224–228
Wright SA, Lane RS, Clover JR (1998) Infestation of the southern alligator lizard (Squamata: Anguidae) by Ixodes pacificus (Acari: Ixodidae) and its susceptibility to Borrelia burgdorferi. Journal of Medical Entomology 35:1044–1049
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This material is based upon work supported by the National Science Foundation under Grant No. EF-0525674.
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Killilea, M.E., Swei, A., Lane, R.S. et al. Spatial Dynamics of Lyme Disease: A Review. EcoHealth 5, 167–195 (2008). https://doi.org/10.1007/s10393-008-0171-3
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DOI: https://doi.org/10.1007/s10393-008-0171-3