Skip to main content
Top

Open Access 04-05-2024 | Lyme Disease | Original Contribution

Opposing Patterns of Spatial Synchrony in Lyme Disease Incidence

Authors: Asad E. Ali, Allison M. Gardner, Herman H. Shugart, Jonathan A. Walter

Published in: EcoHealth

Login to get access

Abstract

Incidence of Lyme disease, a tick-borne illness prevalent in the US, is increasing in endemic regions and regions with no previous history of the disease, significantly impacting public health. We examined space–time patterns of Lyme disease incidence and the influence of ecological and social factors on spatial synchrony, i.e., correlated incidence fluctuations across US counties. Specifically, we addressed these questions: Does Lyme disease incidence exhibit spatial synchrony? If so, what geographic patterns does Lyme disease synchrony exhibit? Are geographic patterns of disease synchrony related to weather, land cover, access to health care, or tick-borne disease awareness? How do effects of these variables on Lyme disease synchrony differ geographically? We used network analysis and matrix regression to examine geographical patterns of Lyme disease synchrony and their potential mechanisms in 399 counties in the eastern and Midwestern US. We found two distinct regions of synchrony in Northeast and upper Midwest regions exhibiting opposing temporal fluctuations in incidence. Spatial patterns of Lyme disease synchrony were partly explained by land cover, weather, poverty, and awareness of tick-borne illness, with significant predictive variables changing regionally. However, the two regions may have become more synchronous over time, potentially leading to higher-amplitude nation-wide fluctuations in disease incidence.
Literature
go back to reference Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17(1):267–272CrossRef Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17(1):267–272CrossRef
go back to reference Anderson TL, Walter JA, Levine TD, Hendricks SP, Johnston KL, White DS, Reuman DC (2018) Using geography to infer the importance of dispersal for the synchrony of freshwater plankton. Oikos 127(3):403–414CrossRef Anderson TL, Walter JA, Levine TD, Hendricks SP, Johnston KL, White DS, Reuman DC (2018) Using geography to infer the importance of dispersal for the synchrony of freshwater plankton. Oikos 127(3):403–414CrossRef
go back to reference Bisanzio D, Fernández MP, Martello E, Reithinger R, Diuk-Wasser MA (2020) Current and future spatiotemporal patterns of Lyme disease reporting in the Northeastern United States. JAMA Network Open 3(3):e200319–e200319PubMedPubMedCentralCrossRef Bisanzio D, Fernández MP, Martello E, Reithinger R, Diuk-Wasser MA (2020) Current and future spatiotemporal patterns of Lyme disease reporting in the Northeastern United States. JAMA Network Open 3(3):e200319–e200319PubMedPubMedCentralCrossRef
go back to reference Bjørnstad ON, Liebhold AM, Johnson DM (2008) Transient synchronization following invasion: revisiting Moran’s model and a case study. Population Ecology 50(4):379–389CrossRef Bjørnstad ON, Liebhold AM, Johnson DM (2008) Transient synchronization following invasion: revisiting Moran’s model and a case study. Population Ecology 50(4):379–389CrossRef
go back to reference Burtis JC, Sullivan P, Levi T, Oggenfuss K, Fahey TJ, Ostfeld RS (2016) The impact of temperature and precipitation on blacklegged tick activity and Lyme disease incidence in endemic and emerging regions. Parasites & Vectors 9(1):1–10CrossRef Burtis JC, Sullivan P, Levi T, Oggenfuss K, Fahey TJ, Ostfeld RS (2016) The impact of temperature and precipitation on blacklegged tick activity and Lyme disease incidence in endemic and emerging regions. Parasites & Vectors 9(1):1–10CrossRef
go back to reference Conte CE, Leahy JE, Gardner AM (2021) Active Forest Management Reduces Blacklegged Tick and Tick-Borne Pathogen Exposure Risk. EcoHealth 18:1–12CrossRef Conte CE, Leahy JE, Gardner AM (2021) Active Forest Management Reduces Blacklegged Tick and Tick-Borne Pathogen Exposure Risk. EcoHealth 18:1–12CrossRef
go back to reference Couper LI, MacDonald AJ, Mordecai EA (2021) Impact of prior and projected climate change on US Lyme disease incidence. Global Change Biology 27(4):738–754PubMedCrossRef Couper LI, MacDonald AJ, Mordecai EA (2021) Impact of prior and projected climate change on US Lyme disease incidence. Global Change Biology 27(4):738–754PubMedCrossRef
go back to reference Diuk-Wasser MA, VanAcker MC, Fernandez MP (2021) Impact of land use changes and habitat fragmentation on the eco-epidemiology of tick-borne diseases. Journal of Medical Entomology 58(4):1546–1564PubMedCrossRef Diuk-Wasser MA, VanAcker MC, Fernandez MP (2021) Impact of land use changes and habitat fragmentation on the eco-epidemiology of tick-borne diseases. Journal of Medical Entomology 58(4):1546–1564PubMedCrossRef
go back to reference Eisen RJ, Eisen L, Beard CB (2016) County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. Journal of Medical Entomology 53(2):349–386PubMedCrossRef Eisen RJ, Eisen L, Beard CB (2016) County-scale distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental United States. Journal of Medical Entomology 53(2):349–386PubMedCrossRef
go back to reference Elias SP, Gardner AM, Maasch KA, Birkel SD, Anderson NT, Rand PW, Smith RP Jr (2021) A generalized additive model correlating blacklegged ticks with white-tailed deer density, temperature, and humidity in Maine, USA, 1990–2013. Journal of Medical Entomology 58(1):125–138PubMed Elias SP, Gardner AM, Maasch KA, Birkel SD, Anderson NT, Rand PW, Smith RP Jr (2021) A generalized additive model correlating blacklegged ticks with white-tailed deer density, temperature, and humidity in Maine, USA, 1990–2013. Journal of Medical Entomology 58(1):125–138PubMed
go back to reference Gardner AM, Pawlikowski NC, Hamer SA, Hickling GJ, Miller JR, Schotthoefer AM, Allan BF (2020) Landscape features predict the current and forecast the future geographic spread of Lyme disease. Proceedings of the Royal Society B 287(1941):20202278PubMedPubMedCentralCrossRef Gardner AM, Pawlikowski NC, Hamer SA, Hickling GJ, Miller JR, Schotthoefer AM, Allan BF (2020) Landscape features predict the current and forecast the future geographic spread of Lyme disease. Proceedings of the Royal Society B 287(1941):20202278PubMedPubMedCentralCrossRef
go back to reference Ginsberg HS, Zhioua E, Mitra S, Fischer J, Buckley PA, Verret F, Buckley FG (2004) Woodland type and spatial distribution of nymphal Ixodes scapularis (Acari: Ixodidae). Environmental Entomology 33(5):1266–1273CrossRef Ginsberg HS, Zhioua E, Mitra S, Fischer J, Buckley PA, Verret F, Buckley FG (2004) Woodland type and spatial distribution of nymphal Ixodes scapularis (Acari: Ixodidae). Environmental Entomology 33(5):1266–1273CrossRef
go back to reference Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22:1–19CrossRef Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22:1–19CrossRef
go back to reference Halsey SJ, Allan BF, Miller JR (2018) The role of Ixodes scapularis, Borrelia burgdorferi and wildlife hosts in Lyme disease prevalence: a quantitative review. Ticks and Tick-Borne Diseases 9(5):1103–1114PubMedCrossRef Halsey SJ, Allan BF, Miller JR (2018) The role of Ixodes scapularis, Borrelia burgdorferi and wildlife hosts in Lyme disease prevalence: a quantitative review. Ticks and Tick-Borne Diseases 9(5):1103–1114PubMedCrossRef
go back to reference Haynes KJ, Liebhold AM, Fearer TM, Wang G, Norman GW, Johnson DM (2009) Spatial synchrony propagates through a forest food web via consumer–resource interactions. Ecology 90(11):2974–2983PubMedCrossRef Haynes KJ, Liebhold AM, Fearer TM, Wang G, Norman GW, Johnson DM (2009) Spatial synchrony propagates through a forest food web via consumer–resource interactions. Ecology 90(11):2974–2983PubMedCrossRef
go back to reference Haynes KJ, Bjørnstad ON, Allstadt AJ, Liebhold AM (2013) Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers. Proceedings of the Royal Society B: Biological Sciences 280(1753):20122373PubMedCentralCrossRef Haynes KJ, Bjørnstad ON, Allstadt AJ, Liebhold AM (2013) Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers. Proceedings of the Royal Society B: Biological Sciences 280(1753):20122373PubMedCentralCrossRef
go back to reference Herrington JE, Campbell GL, Bailey RE, Cartter ML, Adams M, Frazier EL, Gensheimer KF (1997) Predisposing factors for individuals Lyme disease prevention practices: Connecticut, Maine, and Montana. American Journal of Public Health 87(12):2035–2038PubMedPubMedCentralCrossRef Herrington JE, Campbell GL, Bailey RE, Cartter ML, Adams M, Frazier EL, Gensheimer KF (1997) Predisposing factors for individuals Lyme disease prevention practices: Connecticut, Maine, and Montana. American Journal of Public Health 87(12):2035–2038PubMedPubMedCentralCrossRef
go back to reference Kilpatrick AM, Dobson ADM, Levi T, Salkeld DJ, Swei A, Ginsberg HS, Diuk-Wasser MA (2017) Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control. Philosophical Transactions of the Royal Society B: Biological Sciences 372(1722):20160117CrossRef Kilpatrick AM, Dobson ADM, Levi T, Salkeld DJ, Swei A, Ginsberg HS, Diuk-Wasser MA (2017) Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control. Philosophical Transactions of the Royal Society B: Biological Sciences 372(1722):20160117CrossRef
go back to reference Koenig WD, Liebhold AM (2016) Temporally increasing spatial synchrony of North American temperature and bird populations. Nature Climate Change 6(6):614–617CrossRef Koenig WD, Liebhold AM (2016) Temporally increasing spatial synchrony of North American temperature and bird populations. Nature Climate Change 6(6):614–617CrossRef
go back to reference Kotchi SO, Bouchard C, Brazeau S, Ogden NH (2021) Earth Observation-Informed Risk Maps of the Lyme Disease Vector Ixodes scapularis in Central and Eastern Canada. Remote Sensing 13(3):524CrossRef Kotchi SO, Bouchard C, Brazeau S, Ogden NH (2021) Earth Observation-Informed Risk Maps of the Lyme Disease Vector Ixodes scapularis in Central and Eastern Canada. Remote Sensing 13(3):524CrossRef
go back to reference Kugeler KJ, Farley GM, Forrester JD, Mead PS (2015) Geographic distribution and expansion of human Lyme disease. United States. Emerging Infectious Diseases 21(8):1455–1457PubMedCrossRef Kugeler KJ, Farley GM, Forrester JD, Mead PS (2015) Geographic distribution and expansion of human Lyme disease. United States. Emerging Infectious Diseases 21(8):1455–1457PubMedCrossRef
go back to reference Legendre P, Lapointe FJ, Casgrain P (1994) Modeling brain evolution from behavior: a permutational regression approach. Evolution 48(5):1487–1499PubMedCrossRef Legendre P, Lapointe FJ, Casgrain P (1994) Modeling brain evolution from behavior: a permutational regression approach. Evolution 48(5):1487–1499PubMedCrossRef
go back to reference 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(27):10942–10947CrossRef 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(27):10942–10947CrossRef
go back to reference Levi T, Keesing F, Oggenfuss K, Ostfeld RS (2015) Accelerated phenology of blacklegged ticks under climate warming. Philosophical Transactions of the Royal Society B: Biological Sciences 370(1665):20130556–20130556CrossRef Levi T, Keesing F, Oggenfuss K, Ostfeld RS (2015) Accelerated phenology of blacklegged ticks under climate warming. Philosophical Transactions of the Royal Society B: Biological Sciences 370(1665):20130556–20130556CrossRef
go back to reference Lichstein JW (2007) Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology 188(2):117–131CrossRef Lichstein JW (2007) Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology 188(2):117–131CrossRef
go back to reference Liebhold A, Koenig WD, Bjørnstad ON (2004) Spatial Synchrony in Population Dynamics. Annual Review of Ecology, Evolution, and Systematics 35(1):467–490CrossRef Liebhold A, Koenig WD, Bjørnstad ON (2004) Spatial Synchrony in Population Dynamics. Annual Review of Ecology, Evolution, and Systematics 35(1):467–490CrossRef
go back to reference Linske MA, Stafford KC, Williams SC, Lubelczyk CB, Welch M, Henderson EF (2019) Impacts of deciduous leaf litter and snow presence on nymphal Ixodes scapularis (Acari: Ixodidae) overwintering survival in coastal New England, USA. InSects 10(8):227PubMedPubMedCentralCrossRef Linske MA, Stafford KC, Williams SC, Lubelczyk CB, Welch M, Henderson EF (2019) Impacts of deciduous leaf litter and snow presence on nymphal Ixodes scapularis (Acari: Ixodidae) overwintering survival in coastal New England, USA. InSects 10(8):227PubMedPubMedCentralCrossRef
go back to reference 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(2):567–571CrossRef 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(2):567–571CrossRef
go back to reference López-Pérez AM, Plourde B, Smith K, Rubino F, Pascoe E, Smith O, Foley J (2021) Impacts of Timber Harvest on Communities of Small Mammals, Ticks, and Tick-Borne Pathogens in a High-Risk Landscape in Northern California. Journal of Medical Entomology 58(3):1171–1187PubMedCrossRef López-Pérez AM, Plourde B, Smith K, Rubino F, Pascoe E, Smith O, Foley J (2021) Impacts of Timber Harvest on Communities of Small Mammals, Ticks, and Tick-Borne Pathogens in a High-Risk Landscape in Northern California. Journal of Medical Entomology 58(3):1171–1187PubMedCrossRef
go back to reference MacDonald AJ, Hyon DW, Brewington JB, O’Connor KE, Swei A, Briggs CJ (2017) Lyme disease risk in southern California: abiotic and environmental drivers of Ixodes pacificus (Acari: Ixodidae) density and infection prevalence with Borrelia burgdorferi. Parasites & Vectors 10(1):1–16CrossRef MacDonald AJ, Hyon DW, Brewington JB, O’Connor KE, Swei A, Briggs CJ (2017) Lyme disease risk in southern California: abiotic and environmental drivers of Ixodes pacificus (Acari: Ixodidae) density and infection prevalence with Borrelia burgdorferi. Parasites & Vectors 10(1):1–16CrossRef
go back to reference Moustakas A, Evans MR, Daliakopoulos IN, Markonis Y (2018) Abrupt events and population synchrony in the dynamics of Bovine Tuberculosis. Nature Communications 9(1):2821PubMedPubMedCentralCrossRef Moustakas A, Evans MR, Daliakopoulos IN, Markonis Y (2018) Abrupt events and population synchrony in the dynamics of Bovine Tuberculosis. Nature Communications 9(1):2821PubMedPubMedCentralCrossRef
go back to reference Newman MEJ (2006) Modularity and community structure in networks. Proceedings of the National Academy of Sciences 103(23):8577–8582CrossRef Newman MEJ (2006) Modularity and community structure in networks. Proceedings of the National Academy of Sciences 103(23):8577–8582CrossRef
go back to reference Ostfeld RS, Brunner JL (2015) Climate change and Ixodes tick-borne diseases of humans. Philosophical Transactions of the Royal Society B: Biological Sciences 370(1665):20140051CrossRef Ostfeld RS, Brunner JL (2015) Climate change and Ixodes tick-borne diseases of humans. Philosophical Transactions of the Royal Society B: Biological Sciences 370(1665):20140051CrossRef
go back to reference Ostfeld RS, Levi T, Keesing F, Oggenfuss K, Canham CD (2018) Tick-borne disease risk in a forest food web. Ecology 99(7):1562–1573PubMedCrossRef Ostfeld RS, Levi T, Keesing F, Oggenfuss K, Canham CD (2018) Tick-borne disease risk in a forest food web. Ecology 99(7):1562–1573PubMedCrossRef
go back to reference Penczykowski RM, Walker E, Soubeyrand S, Laine AL (2015) Linking winter conditions to regional disease dynamics in a wild plant-pathogen metapopulation. New Phytologist 205(3):1142–1152PubMedCrossRef Penczykowski RM, Walker E, Soubeyrand S, Laine AL (2015) Linking winter conditions to regional disease dynamics in a wild plant-pathogen metapopulation. New Phytologist 205(3):1142–1152PubMedCrossRef
go back to reference Rohani P (1999) Opposite Patterns of Synchrony in Sympatric Disease Metapopulations. Science 286(5441):968–971PubMedCrossRef Rohani P (1999) Opposite Patterns of Synchrony in Sympatric Disease Metapopulations. Science 286(5441):968–971PubMedCrossRef
go back to reference Schwartz AM, Hinckley AF, Mead PS, Hook SA, Kugeler KJ (2017) Surveillance for Lyme Disease—United States, 2008–2015. MMWR. Surveillance Summaries 66(22):1–12PubMedCentralCrossRef Schwartz AM, Hinckley AF, Mead PS, Hook SA, Kugeler KJ (2017) Surveillance for Lyme Disease—United States, 2008–2015. MMWR. Surveillance Summaries 66(22):1–12PubMedCentralCrossRef
go back to reference Scott JD, Scott CM (2018) Lyme disease propelled by Borrelia burgdorferi-infected blacklegged ticks, wild birds and public awareness—Not climate change. J. Vet. Sci. Med 6(8) Scott JD, Scott CM (2018) Lyme disease propelled by Borrelia burgdorferi-infected blacklegged ticks, wild birds and public awareness—Not climate change. J. Vet. Sci. Med 6(8)
go back to reference Springer YP, Johnson PTJ (2018) Large-scale health disparities associated with Lyme disease and human monocytic ehrlichiosis in the United States, 2007–2013. Plos One 13(9):e0204606CrossRef Springer YP, Johnson PTJ (2018) Large-scale health disparities associated with Lyme disease and human monocytic ehrlichiosis in the United States, 2007–2013. Plos One 13(9):e0204606CrossRef
go back to reference Subak S (2003) Effects of climate on variability in Lyme disease incidence in the northeastern United States. American Journal of Epidemiology 157(6):531–538PubMedCrossRef Subak S (2003) Effects of climate on variability in Lyme disease incidence in the northeastern United States. American Journal of Epidemiology 157(6):531–538PubMedCrossRef
go back to reference VanAcker MC, Little EA, Molaei G, Bajwa WI, Diuk-Wasser MA (2019) Enhancement of risk for Lyme disease by landscape connectivity, New York, New York, USA. Emerging Infectious Diseases 25(6):1136PubMedPubMedCentralCrossRef VanAcker MC, Little EA, Molaei G, Bajwa WI, Diuk-Wasser MA (2019) Enhancement of risk for Lyme disease by landscape connectivity, New York, New York, USA. Emerging Infectious Diseases 25(6):1136PubMedPubMedCentralCrossRef
go back to reference Viboud C, Børnstad ON, Smith DL, Simonsen L, Miller MA, Grenfell BT (2006) Synchrony, Waves, and Spatial Hierarchies in the Spread of Influenza. Science 312(April):447–451PubMedCrossRef Viboud C, Børnstad ON, Smith DL, Simonsen L, Miller MA, Grenfell BT (2006) Synchrony, Waves, and Spatial Hierarchies in the Spread of Influenza. Science 312(April):447–451PubMedCrossRef
go back to reference Walter JA, Sheppard LW, Anderson TL, Kastens JH, Bjørnstad ON, Liebhold AM, Reuman DC (2017) The geography of spatial synchrony. Ecology Letters 20(7):801–814PubMedCrossRef Walter JA, Sheppard LW, Anderson TL, Kastens JH, Bjørnstad ON, Liebhold AM, Reuman DC (2017) The geography of spatial synchrony. Ecology Letters 20(7):801–814PubMedCrossRef
go back to reference Walter JA, Hallett LM, Sheppard LW, Anderson TL, Zhao L, Hobbs RJ, Reuman DC (2021) Micro-scale geography of synchrony in a serpentine plant community. Journal of Ecology 109(2):750–762CrossRef Walter JA, Hallett LM, Sheppard LW, Anderson TL, Zhao L, Hobbs RJ, Reuman DC (2021) Micro-scale geography of synchrony in a serpentine plant community. Journal of Ecology 109(2):750–762CrossRef
go back to reference Wang G, Wolff JO, Vessey SH, Slade NA, Witham JW, Merritt JF, Elias SP (2009) Comparative population dynamics of Peromyscus leucopus in North America: influences of climate, food, and density dependence. Population Ecology 51(1):133–142CrossRef Wang G, Wolff JO, Vessey SH, Slade NA, Witham JW, Merritt JF, Elias SP (2009) Comparative population dynamics of Peromyscus leucopus in North America: influences of climate, food, and density dependence. Population Ecology 51(1):133–142CrossRef
go back to reference Wood CL, Lafferty KD (2013) Biodiversity and disease: A synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28(4):239–247PubMedCrossRef Wood CL, Lafferty KD (2013) Biodiversity and disease: A synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28(4):239–247PubMedCrossRef
Metadata
Title
Opposing Patterns of Spatial Synchrony in Lyme Disease Incidence
Authors
Asad E. Ali
Allison M. Gardner
Herman H. Shugart
Jonathan A. Walter
Publication date
04-05-2024
Publisher
Springer US
Published in
EcoHealth
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-024-01677-8