Abstract
Interdisciplinary approaches are merited when attempting to understand the complex and idiosyncratic processes driving the spillover of pathogens from wildlife and vector species to human populations. Public health data are often available for zoonotic pathogens but can lead to erroneous conclusions if the data have been spatially or temporally aggregated. As an illustration, we use human Lyme disease incidence data as a case study to examine correlations between mammalian biodiversity, fried chicken restaurants and obesity rates on human disease incidence. We demonstrate that Lyme disease incidence is negatively correlated with mammalian biodiversity, the abundance of fried chicken restaurants and obesity rates. We argue, however, that these correlations are spurious, representing both an ‘ecologic fallacy’ and Simpson’s paradox, and are generated by the use of aggregated data. We argue that correlations based on aggregated data across large spatial scales must be rigorously examined before being invoked as proof of disease ecology theory or as a rationale for public health policy.
Similar content being viewed by others
References
Arsnoe IM, Hickling GJ, Ginsberg HS, McElreath R, Tsao JI (2015) Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human Lyme disease risk. PLoS ONE 10:e0127450
Bickel PJ, Hammel EA, O’Connell JW (1975) Sex bias in graduate admissions: data from Berkeley. Science 187:398–404
Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon T, Ortega CN, Sauer EL, Sehgal T, Young S, Rohr JR (2015) Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings National Academy Sciences, USA 112:8667–8671
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 53:349–386
Eisen RJ, Eisen L (2018) The blacklegged tick, Ixodes scapularis: an increasing public health concern. Trends in Parasitology 34:295–309
Forrester JD, Meiman J, Mullins J, Nelson R, Ertel S-H, Cartter M, Brown CM, Lijewski V, Schiffman E, Neitzel D, Daly ER, Mathewson AA, Howe W, Lowe LA, Kratz NR, Semple S, Backenson PB, White JL, Kurpiel PM, Rockwell R, Waller K, Johnson DH, Steward C, Batten B, Blau D, DeLeon-Carnes M, Drew C, Muehlenbachs A, Ritter J, Sanders J, Zaki SR, Molins C, Schriefer M, Perea A, Kugeler K, Nelson C, Hinckley A, Mead P (2014) Update on Lyme carditis, groups at high risk, and frequency of associated sudden cardiac death – United States. Morbidity and Mortality Weekly Report (MMWR) 63:982–983
Gascon M, Zijlema W, Vert C, White MP, Nieuwenhuijsen MJ (2017) Outdoor blue spaces, human health and well-being: A systematic review of quantitative studies. International Journal of Hygiene and Environmental Health 220:1207–1221
Gordis L (2009) Epidemiology, 4th edn., Philadelphia PA: Saunders Elsevier, p 375
Gotway CA, Young LJ (2002) Combining incompatible spatial data. Journal of the American Statistical Association 97:632–648
Halliday FW, Rohr JR (2019) Measuring the shape of the biodiversity-disease relationship across systems reveals new findings and key gaps. Nature Communications 10:5032
Hickman D, Jones MK, Zhu S, Kirkpatrick E, Ostrov DA, Wang X, Ukhanova M, Sun Y, Mai V, Salemi M, Karst SM (2014) The effect of malnutrition on norovirus infection. mBio 5(2):e01032–13
Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt R, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652
Kilpatrick AM, Salkeld DJ, Titcomb G, Hahn MB (2017) Conservation of biodiversity as a strategy for improving human health and well-being. Philosophical Transactions of the Royal Society, London B 372: 20160131
Levi T, Kilpatrick AM, Mangel M, Wilmers CC (2012) Deer, predators, and the emergence of Lyme disease. Proceedings National Academy Sciences, USA 109:10942–10947
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 National Academy Sciences, USA 100:567–571
Messerli FH (2012) Chocolate consumption, cognitive function, and Nobel laureates. New England Journal of Medicine 367:1562–1564
Millins C, Gilbert L, Johnson P, James M, Kilbride E, Birtles R, Biek R (2016) Heterogeneity in the abundance and distribution of Ixodes ricinus and Borrelia burgdorferi (sensu lato) in Scotland: implications for risk prediction. Parasites and Vectors 9:595
Nadelman RB, Wormser G (2005) Poly-ticks: blue state versus red state for Lyme disease. Lancet 356: 280
Nelson CA, Saha S, Kugeler KJ, Delorey MJ, Shankar MB, Hinckley AF, Mead PS (2015) Incidence of clinician-diagnosed Lyme disease, United States, 2005–2010. Emerging Infectious Diseases 21:1625–1631
Ogden NH, Tsao JI (2009) Biodiversity and Lyme disease: dilution or amplification. Epidemics 1:196–206
Ostfeld RS, Keesing F (2000) Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14:722–728
Pepin KM, Eisen RJ, Mead PS, Piesman J, Fish D, Hoen AG, Barbour AG, Hamer S, Diuk-Wasser MA (2012) Geographic variation in the relationship between human Lyme disease incidence and density of infected host-seeking Ixodes scapularis nymphs in the Eastern United States. American Journal of Tropical Medicine and Hygiene 86:1062–1071
Pollet TV, Tybur JM, Frankenhuis WE, Rickard IJ (2014) What can cross-cultural correlations teach us about human nature? Human Nature 25:410–429
Pollet TV, Stulp G, Henzi SP, Barrett L (2015) Taking the aggravation out of data aggregation: a conceptual guide to dealing with statistical issues related to the pooling of individual-level observational data. American Journal of Primatology 77:727–740
Pongsiri MJ, Roman J, Ezenwa VO, Goldberg TL, Koren HS, Newbold SC, Ostfeld RS, Pattanayak SK, Salkeld DJ (2009) Biodiversity loss and the new global disease ecology. BioScience 59:945–954
Porter WT, Motyka PJ, Wachara J, Barrand ZA, Hmood Z, McLaughlin M, Pemberton K, Nieto NC (2019) Citizen science informs human-tick exposure in the Northeastern United States. International Journal of Health Geographics 18:9
R Core Team (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/
Randolph SE, Dobson ADM (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 16:1–17
Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008) Evaluating the links between climate, disease spread, and amphibian declines. Proceedings National Academy Sciences, USA 105:17436–17441
Salkeld DJ, Leonhard S, Girard YA, Hahn N, Mun J, Padgett KA, Lane RS (2008) Identifying the reservoir hosts of the Lyme disease spirochete Borrelia burgdorferi in California: the role of the western gray squirrel (Sciurus griseus). American Journal of Tropical Medicine and Hygiene 79:535–540
Salkeld DJ, Padgett KA, Jones JH (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters 16:679–686
Salkeld DJ, Nieto NC, Carbajales-Dale P, Carbajales-Dale M, Cinkovich SS, Lambin EF (2015) Disease risk and landscape attributes of tick-borne Borrelia pathogens in the San Francisco Bay Area, California. PLoS ONE 10(8):e0134812
Salkeld DJ, Padgett KA, Jones JH, Antolin MF (2015) Public health perspective on patterns of biodiversity and zoonotic disease. Proceedings National Academy Sciences, USA 112:E6261
Salkeld DJ, Porter WT, Loh SM, Nieto NC (2019) Time of year and outdoor recreation affect human exposure to ticks in California, United States. Ticks and Tick-borne Diseases, 10:1113–1117
Schiffman EK, McLaughlin C, Ray JAE, Kemperman MM, Hinckley AF, Friedlander HG, Neitzel DF (2018) Underreporting of Lyme and other tick-borne diseases in residents of a high-incidence county, Minnesota, 2009. Zoonoses Public Health 65:230–237
Shortridge BG (2005) Apple stack cake for dessert: Appalachian regional foods. Journal of Geography 104:65–73.
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):e0204609
Stanek G, Wormser GP, Strle F (2012) Lyme borreliosis. Lancet 379:461–473
Strauss AT, Shocket MS, Civitello DJ, Hite JL, Penczykowski RM, Duffy MA, Cáceres CE, Hall SR (2016) Habitat, predators, and hosts regulate disease in Daphnia through direct and indirect pathways. Ecological Monographs 86:393–411
Sun Y, Liu B, Snetselaar LG, Robinson JG, Wallace RB, Peterson LL, Bao W (2019) Association of fried food consumption with all cause, cardiovascular, and cancer mortality: prospective cohort study. The BMJ, 364:k5420
Turney S, Gonzalez A, Millien V (2014) The negative relationship between mammal host diversity and Lyme disease incidence strengthens through time. Ecology 95, 3244–3250
Way JG, White BN (2013) Coyotes, red foxes, and the prevalence of Lyme disease. Northeastern Naturalist 20:655–665
Webb P, Bain C (2011) Essential epidemiology: an introduction for students and health professionals, 2nd ed., Cambridge: University Press, p 445
Wilkinson DA, Marshall JC, French NP, Hayman DTS (2018) Habitat fragmentation, biodiversity loss and the risk of novel infectious disease emergence. Journal of the Royal Society Interface 15:20180403
Wood CL, Lafferty KD (2013). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28:239–247
Acknowledgements
We wish to thank Anne Kjemtrup, Lynne Gaffikin, James Holland Jones and Mevin Hooten for fierce insights into ecology and epidemiology and especially Jean Tsao for her brilliant offhand remark that inspired this paper. We thank Virginie Millien for providing data and W. Tanner Porter for creating maps and Bay Area Lyme Foundation for financial support. This work is dedicated to the memory of Nate Nieto—a brilliant friend and scientist, one of the best, and loved to bits.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Salkeld, D.J., Antolin, M.F. Ecological Fallacy and Aggregated Data: A Case Study of Fried Chicken Restaurants, Obesity and Lyme Disease. EcoHealth 17, 4–12 (2020). https://doi.org/10.1007/s10393-020-01472-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-020-01472-1