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Disease Risk in a Dynamic Environment: The Spread of Tick-Borne Pathogens in Minnesota, USA

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Abstract

As humans and climate change alter the landscape, novel disease risk scenarios emerge. Understanding the complexities of pathogen emergence and subsequent spread as shaped by landscape heterogeneity is crucial to understanding disease emergence, pinpointing high-risk areas, and mitigating emerging disease threats in a dynamic environment. Tick-borne diseases present an important public health concern and incidence of many of these diseases are increasing in the United States. The complex epidemiology of tick-borne diseases includes strong ties with environmental factors that influence host availability, vector abundance, and pathogen transmission. Here, we used 16 years of case data from the Minnesota Department of Health to report spatial and temporal trends in Lyme disease (LD), human anaplasmosis, and babesiosis. We then used a spatial regression framework to evaluate the impact of landscape and climate factors on the spread of LD. Finally, we use the fitted model, and landscape and climate datasets projected under varying climate change scenarios, to predict future changes in tick-borne pathogen risk. Both forested habitat and temperature were important drivers of LD spread in Minnesota. Dramatic changes in future temperature regimes and forest communities predict rising risk of tick-borne disease.

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References

  • Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267-272.

    Article  Google Scholar 

  • Altizer S, Ostfeld RS, Johnson PT, Kutz S, Harvell CD (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514-519.

    Article  CAS  PubMed  Google Scholar 

  • Bacon RM, Kugeler KJ, Mead PS (2008) Surveillance for Lyme disease–United States, 1992–2006. Department of Health & Human Services, Centers for Disease Control and Prevention

  • Bivand R, Altman M, Anselin L, et al. (2011) R Package ‘spdep’: spatial dependence: weighting schemes, statistics and models. http://cran.r-project.org/web/packages/spdep/index.html

  • Brinkerhoff RJ, Folsom-O’Keefe CM, Tsao K, Diuk-Wasser MA (2009) Do birds affect Lyme disease risk? Range expansion of the vector-borne pathogen Borrelia burgdorferi. Frontiers in Ecology and the Environment 9, 103-110.

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. New York, NY: Springer

    Google Scholar 

  • Council of State and Territorial Epidemiologists (1997) Case definitions for infectious conditions under public health surveillance. MMWR 46 (No. RR-10)

  • Demma LJ, Holman RC, McQuiston JH, Krebs JW, Swerdlow DL (2005) Epidemiology of human ehrlichiosis and anaplasmosis in the United States, 2001-2002. The American journal of tropical medicine and hygiene 73, 400-409.

    PubMed  Google Scholar 

  • Diuk-Wasser MA, Liu Y, Steeves T, et al. (2014) Monitoring human Babesiosis emergence through vector surveillance New England, USA. Emerging Infectious Diseases 20, 225-231.

    Article  PubMed Central  PubMed  Google Scholar 

  • Diuk-Wasser MA, Vourc’h G, Cislo P, et al. (2010) Field and climate-based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne disease agents in the eastern United States. Global Ecology and Biogeography 19, 504-514.

    Google Scholar 

  • Dobson AD, Randolph SE (2011) Modelling the effects of recent changes in climate, host density and acaricide treatments on population dynamics of Ixodes ricinus in the UK. Journal of Applied Ecology 48, 1029-1037.

    Article  Google Scholar 

  • Duffy DC, Campbell SR, Clark D, DiMotta C, Gurney S (1994) Ixodes scapularis (Acari: Ixodidae) deer tick mesoscale populations in natural areas: effects of deer, area, and location. Journal of medical entomology 31, 152-158.

    Article  CAS  PubMed  Google Scholar 

  • Estrada-Pena 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gatewood AG, Liebman KA, Vourc’h Gl, et al. (2009) Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Applied and Environmental Microbiology 75, 2476-2483

    Article  PubMed Central  CAS  PubMed  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.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guerra M, Walker E, Jones C, 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamer SA, Tsao JI, Walker ED, Hickling GJ (2010) Invasion of the Lyme disease vector Ixodes scapularis: implications for Borrelia burgdorferi endemicity. EcoHealth 7, 47-63.

    Article  PubMed  Google Scholar 

  • Harrus S, Baneth G (2005) Drivers for the emergence and re-emergence of vector-borne protozoal and bacterial diseases. International journal for parasitology 35, 1309-1318.

    Article  CAS  PubMed  Google Scholar 

  • Harvell D, Altizer S, Cattadori IM, Harrington L, Weil E (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90, 912-920.

    Article  PubMed  Google Scholar 

  • Hayhoe K, VanDorn J, Croley II T, Schlegal N, Wuebbles D (2010) Regional climate change projections for Chicago and the US Great Lakes. Journal of Great Lakes Research 36, 7-21.

    Article  Google Scholar 

  • Hess G, Randolph S, Arneberg P, et al. (2002) Spatial aspects of disease dynamics. In: The ecology of wildlife diseases (ed. PJ Hudson AR, BT Grenfell, H Heesterbeek, AP Dobson), pp. 102-118. Oxford University Press, Oxford, UK

    Google Scholar 

  • Iverson LR, A. M. Prasad, S. N. Matthews, Peters M (2008) Estimating potential habitat for 134 eastern US tree species under six climate scenarios. Forest Ecology and Management 254, 390-406.

    Article  Google Scholar 

  • Jones C, Kitron U (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  PubMed  Google Scholar 

  • Killilea ME, Swei A, Lane RS, Briggs CJ, Ostfeld RS (2008) Spatial dynamics of Lyme disease: a review. EcoHealth 5, 167-195.

    Article  PubMed  Google Scholar 

  • Krause PJ, McKay K, Gadbaw J, et al. (2003) Increasing health burden of human babesiosis in endemic sites. The American journal of tropical medicine and hygiene 68, 431-436.

    PubMed  Google Scholar 

  • Kurtenbach K, Hanincova K, Tsao JI, et al. (2006) Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660-669.

    Article  CAS  PubMed  Google Scholar 

  • Lawson AB (2013) Statistical Methods in Spatial Epidemiology. New York: Wiley

    Google Scholar 

  • Leger E, Vourc’h G, Vial L, Chevillon C, McCoy KD (2013) Changing distributions of ticks: causes and consequences. Experimental and Applied Acarology 59, 219-244.

    Article  PubMed  Google Scholar 

  • Levi T, Kilpatrick AM, Mangel M, Wilmers CC (2012) Deer, predators, and the emergence of Lyme disease. Proceedings of the National Academy of Sciences 109, 10942-10947.

    Article  CAS  Google Scholar 

  • Lewellen RH, Vessey SH (1998) The effect of density dependence and weather on population size of a polyvoltine species. Ecological Monographs 68, 571-594.

    Article  Google Scholar 

  • Lindgren E, Talleklint L, Polfeldt T (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environmental health perspectives 108, 119.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lindsay LR, Barker IK, Surgeoner GA, et al. (1998) Survival and development of the different life stages of Ixodes scapularis (Acari: Ixodidae) held within four habitats on Long Point, Ontario, Canada. Journal of medical entomology 35, 189-199.

    Article  CAS  PubMed  Google Scholar 

  • Lindsay LR, Barker IK, Surgeoner GA, et al. (1995) Survival and development of Ixodes scapularis (Acari: Ixodidae) under various climatic conditions in Ontario, Canada. Journal of medical entomology 32, 143-152.

    Article  CAS  PubMed  Google Scholar 

  • 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. Proceedings of the National Academy of Sciences 100, 567-571.

    Article  CAS  Google Scholar 

  • Matthews JN (2005) Summary Measures Analysis of Longitudinal Data. Encyclopedia of Biostatistics. Wiley: New York

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Minnesota Department of Natural Resources. http://deli.dnr.state.mn.us/data_catalog.html. Accessed May 2013

  • MN State Climatology Office. http://climate.umn.edu/. Accessed May 2013

  • Nakicenovic N, Alcamo J, Davis G, et al. (2000) Special report on emissions scenarios: a special report of Working Group III of the Intergovernmental Panel on Climate Change. Pacific Northwest National Laboratory, Richland, WA (US), Environmental Molecular Sciences Laboratory (US).

    Google Scholar 

  • Nupp TE, Swihart RK (1998) Effects of forest fragmentation on population attributes of white-footed mice and eastern chipmunks. Journal of Mammalogy, 79:1234-1243

    Article  Google Scholar 

  • Ogden N, Bigras-Poulin M, Hanincova K, et al. (2008) Projected effects of climate change on tick phenology and fitness of pathogens transmitted by the North American tick Ixodes scapularis. Journal of Theoretical Biology 254, 621-632.

    Article  CAS  PubMed  Google Scholar 

  • Ogden N, Bigras-Poulin M, O’callaghan C, et al. (2005) A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. International journal for parasitology 35, 375-389.

    Article  CAS  PubMed  Google Scholar 

  • Ogden N, Lindsay L, Beauchamp G, et al. (2004) Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. Journal of medical entomology 41, 622-633.

    Article  CAS  PubMed  Google Scholar 

  • Ogden N, Maarouf A, Barker I, 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.

    Article  CAS  PubMed  Google Scholar 

  • Ogden NH, Lindsay LR, Leighton PA (2013) Predicting the rate of invasion of the agent of Lyme disease Borrelia burgdorferi. Journal of Applied Ecology 50, 510-518.

    Article  Google Scholar 

  • Ostfeld R, Cepeda O, Hazler K, Miller M (1995) Ecology of Lyme disease: habitat associations of ticks (Ixodes scapularis) in a rural landscape. Ecological Applications 5, 353-361.

    Article  Google Scholar 

  • Ostfeld R, Keesing F, LoGiudice K (2006) Community ecology meets epidemiology: the case of Lyme disease. In: Disease ecology: community structure and pathogen dynamics (eds. Collinge S, Ray C), pp. 28–40. Oxford University Press, Oxford, UK.

    Chapter  Google Scholar 

  • Perret J-L, Guigoz E, Rais O, Gern L (2000) Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitology Research 86, 554-557.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffle M, Littwin N, Muders SV, Petney TN (2013) The ecology of tick-borne diseases. International Journal for Parasitology 43:1059–1077

    Article  PubMed  Google Scholar 

  • Prasad AM, Iverson LR, Matthews S, Peters M (2007) A Climate Change Atlas for 134 Forest Tree Species of the Eastern United States [database]. Delaware, OH: Northern Research Station, USDA Forest Service. http://www.nrs.fs.fed.us/atlas/tree. Accessed May 2014

  • Pritt BS, Sloan LM, Johnson DKH, et al. (2011) Emergence of a new pathogenic Ehrlichia species, Wisconsin and Minnesota, 2009. New England Journal of Medicine 365, 422-429.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pryor S, Barthelmie R, Schoof J (2013) High-resolution projections of climate-related risks for the Midwestern USA. Climate research 56, 61-79.

    Article  Google Scholar 

  • Randolph S (1998) Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186-192.

    Article  CAS  PubMed  Google Scholar 

  • Randolph SE (2010) To what extent has climate change contributed to the recent epidemiology of tick-borne diseases? Veterinary parasitology 167, 92-94.

    Article  PubMed  Google Scholar 

  • Robinson C, Schumacker RE (2009) Interaction effects: centering, variance inflation factor, and interpretation issues. Multiple Linear Regression Viewpoints 35, 6-11.

    Google Scholar 

  • Rogers D, Randolph S (2006) Climate change and vector-borne diseases. Advances in Parasitology 62, 345-381.

    Article  CAS  PubMed  Google Scholar 

  • Schmid GP, Horsley R, Steere AC, et al. (1985) Surveillance of Lyme disease in the United States, 1982. Journal of Infectious Diseases 151, 1144-1149.

    Article  CAS  PubMed  Google Scholar 

  • Schulze TL, Jordan RA (2003) Meteorologically mediated diurnal questing of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) nymphs. Journal of medical entomology 40, 395-402.

    Article  PubMed  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  PubMed  Google Scholar 

  • Schwartz BS, Goldstein MD (1990) Lyme disease in outdoor workers: risk factors, preventive measures, and tick removal methods. American Journal of Epidemiology 131, 877-885.

    CAS  PubMed  Google Scholar 

  • Simon JA, Marrotte RR, Desrosiers N, et al. (2014) Climate change and habitat fragmentation drive the occurrence of Borrelia burgdorferi, the agent of Lyme disease, at the northeastern limit of its distribution. Evolutionary Applications 7:750–764

  • Steere AC, Malawista SE, Snydman DR, et al. (1977) An epidemic of oligoarticular arthritis in children and adults in three Connecticut communities. Arthritis & Rheumatism 20, 7-17.

    Article  CAS  Google Scholar 

  • Sumilo D, Bormane A, Asokliene L, et al. (2006) Tick-borne encephalitis in the Baltic States: identifying risk factors in space and time. International Journal of Medical Microbiology 296, 76-79.

    Article  PubMed  Google Scholar 

  • U.S. Census Bureau (2010) Data generated using American FactFinder. http://factfinder2.census.gov/faces/nav/jsf/pages/index.xhtml. Accessed May 2013

  • Vail SG, Smith G (2002) Vertical movement and posture of blacklegged tick (Acari: Ixodidae) nymphs as a function of temperature and relative humidity in laboratory experiments. Journal of medical entomology 39, 842-846.

    Article  PubMed  Google Scholar 

  • Wall MM (2004) A close look at the spatial structure implied by the CAR and SAR models. Journal of Statistical Planning and Inference 121, 311-324.

    Article  Google Scholar 

  • Waller LA, Gotway CA (2004) Applied spatial statistics for public health data. New York, NY: Wiley.

  • Wilson ML, Adler GH, Spielman 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.

    Article  Google Scholar 

  • Woolhouse ME, Gowtage-Sequeria S (2005) Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11, 1842.

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank the graduate student team at MDH for conducting TBP case follow-up. This work was supported by the University of Minnesota Institute on the Environment and Cooperative Agreements (U50/CCU510333-06). Partial support for UGM came from NIH Grant (R01AI042792).

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Authors and Affiliations

  1. University of Minnesota, St Paul, MN, USA

    Stacie J. Robinson, Meggan E. Craft, Karin E. Hamilton, David J. Mulla, Ulrike G. Munderloh, Patrick T. Redig, Jamie K. Umber & Katharine M. Pelican

  2. Minnesota Department of Health, St Paul, MN, USA

    David F. Neitzel & Kirk E. Smith

  3. University of Minnesota, Duluth, MN, USA

    Ronald A. Moen & Lucinda B. Johnson

  4. Minnesota Department of Natural Resources, St Paul, MN, USA

    Clarence L. Turner

  5. Ecosystem Health Initiative, Department of Veterinary Population Medicine, 368 Animal Science/Veterinary Medicine, University of Minnesota, 1365 Gortner Avenue, St Paul, MN, 55108, USA

    Stacie J. Robinson

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  1. Stacie J. Robinson
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  2. David F. Neitzel
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Correspondence to Stacie J. Robinson.

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Robinson, S.J., Neitzel, D.F., Moen, R.A. et al. Disease Risk in a Dynamic Environment: The Spread of Tick-Borne Pathogens in Minnesota, USA. EcoHealth 12, 152–163 (2015). https://doi.org/10.1007/s10393-014-0979-y

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  • DOI: https://doi.org/10.1007/s10393-014-0979-y

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