Ambient soil cation exchange capacity inversely associates with infectious and parasitic disease risk in regional Australia.

Human contact with soil may be important for building and maintaining normal healthy immune defence mechanisms, however this idea remains untested at the population-level. In this continent-wide, cross-sectional study we examine the possible public health benefit of ambient exposures to soil of high cation exchange capacity (CEC), a surrogate for potential immunomodulatory soil microbial diversity. We compare distributions of normalized mean 2011/12-2012/13 age-standardized public hospital admission rates (cumulative incidence) for infectious and parasitic diseases across regional Australia (representing an average of 29,516 patients/year in 228 local government areas), within tertiles of socioeconomic status and soil exposure. To test the significance of soil CEC, we use probabilistic individual-level environmental exposure data (with or without soil), and group-level variables, in robust non-parametric multilevel modelling to predict disease rates in unseen groups. Our results show that in socioeconomically-deprived areas with high CEC soils, rates of infectious and parasitic disease are significantly lower than areas with low CEC soils. Also, health inequality (relative risk) due to socioeconomic status is significantly lower in areas with high CEC soils compared to low CEC soils (Δ relative risk = 0.47; 95% CI: 0.13, 0.82). Including soil exposure when modelling rates of infectious and parasitic disease significantly improves prediction performance, explaining an additional 7.5% (Δ r2 = 0.075; 95% CI: 0.05, 0.10) of variation in disease risk, in local government areas that were not used for model building. Our findings suggest that exposure to high CEC soils (typically high soil biodiversity) associates with reduced risk of infectious and parasitic diseases, particularly in lower socioeconomic areas.

[1]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[2]  S. Frey,et al.  Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls , 2016, Nature Communications.

[3]  A. Kabata-Pendias,et al.  Trace Elements from Soil to Human , 2007 .

[4]  P. Polymenakou Atmosphere: A Source of Pathogenic or Beneficial Microbes? , 2012 .

[5]  Nitin Kumar,et al.  Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation , 2016, Nature.

[6]  L. Jost Entropy and diversity , 2006 .

[7]  Neil McKenzie,et al.  Australian Soils and Landscapes: An Illustrated Compendium , 2004 .

[8]  L. Øvreås,et al.  Microbial diversity and function in soil: from genes to ecosystems. , 2002, Current opinion in microbiology.

[9]  H. Zahran Diversity, adaptation and activity of the bacterial flora in saline environments , 1997, Biology and Fertility of Soils.

[10]  R. Mitchell,et al.  Effect of exposure to natural environment on health inequalities: an observational population study , 2008, The Lancet.

[11]  R. Miller,et al.  Soil aggregate stabilization and carbon sequestration: Feedbacks through organomineral associations , 1996 .

[12]  P. Weinstein,et al.  Environmental Change and Human Health: Can Environmental Proxies Inform the Biodiversity Hypothesis for Protective Microbial–Human Contact? , 2016 .

[13]  D. Wall,et al.  VARIATION IN BIOGEOCHEMISTRY AND SOIL BIODIVERSITY ACROSS SPATIAL SCALES IN A POLAR DESERT ECOSYSTEM , 2004 .

[14]  T. Haahtela,et al.  Disconnection of man and the soil: reason for the asthma and atopy epidemic? , 2006, The Journal of allergy and clinical immunology.

[15]  D. Coleman,et al.  Fundamentals of Soil Ecology , 1996 .

[16]  Song Liang,et al.  Environmental Determinants of Infectious Disease: A Framework for Tracking Causal Links and Guiding Public Health Research , 1997, Environmental health perspectives.

[17]  I M Longini,et al.  The ecological effects of individual exposures and nonlinear disease dynamics in populations. , 1994, American journal of public health.

[18]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[19]  Y. Belkaid,et al.  Intestinal microbiota: shaping local and systemic immune responses. , 2012, Seminars in immunology.

[20]  D. Antonopoulos,et al.  Commensal bacteria protect against food allergen sensitization , 2014, Proceedings of the National Academy of Sciences.

[21]  Andrew J. Lowe,et al.  Urban habitat restoration provides a human health benefit through microbiome rewilding: the Microbiome Rewilding Hypothesis , 2017 .

[22]  Mark V Brown,et al.  Circular linkages between soil biodiversity, fertility and plant productivity are limited to topsoil at the continental scale. , 2017, The New phytologist.

[23]  Andrew J Lowe,et al.  Revegetation rewilds the soil bacterial microbiome of an old field , 2017, Molecular ecology.

[24]  J. Ord,et al.  Local Spatial Autocorrelation Statistics: Distributional Issues and an Application , 2010 .

[25]  Deforestation, Mosquitoes, and Ancient Rome: Lessons for Today , 2008 .

[26]  Tari Haahtela,et al.  Environmental biodiversity, human microbiota, and allergy are interrelated , 2012, Proceedings of the National Academy of Sciences.

[27]  M Susser,et al.  The logic in ecological: I. The logic of analysis. , 1994, American journal of public health.

[28]  J. Six,et al.  Soil biodiversity and human health , 2015, Nature.

[29]  Mike Grundy,et al.  Soil and landscape grid of Australia. , 2015 .

[30]  Korine N. Kolivras,et al.  Environmental vVariability and coccidioidomycosis (valley fever) , 2001 .

[31]  G. Rook Regulation of the immune system by biodiversity from the natural environment: An ecosystem service essential to health , 2013, Proceedings of the National Academy of Sciences.

[32]  L. Stanish,et al.  Key Edaphic Properties Largely Explain Temporal and Geographic Variation in Soil Microbial Communities across Four Biomes , 2015, PloS one.

[33]  Aaron D. Peacock,et al.  PLANT DIVERSITY, SOIL MICROBIAL COMMUNITIES, AND ECOSYSTEM FUNCTION: ARE THERE ANY LINKS? , 2003 .

[34]  M. Croon,et al.  Predicting group-level outcome variables from variables measured at the individual level: a latent variable multilevel model. , 2007, Psychological methods.

[35]  A Hyvärinen,et al.  Green areas around homes reduce atopic sensitization in children , 2015, Allergy.

[36]  Tari Haahtela,et al.  The biodiversity hypothesis and allergic disease: world allergy organization position statement , 2013, The World Allergy Organization journal.

[37]  D. J. Reuter,et al.  Soil Analysis: An Interpretation Manual , 1999 .

[38]  Carla M. Zammit,et al.  Introducing BASE: the Biomes of Australian Soil Environments soil microbial diversity database , 2016, GigaScience.

[39]  Erika von Mutius,et al.  Innate Immunity and Asthma Risk in Amish and Hutterite Farm Children. , 2016, The New England journal of medicine.

[40]  C. Belzer,et al.  The first thousand days – intestinal microbiology of early life: establishing a symbiosis , 2014, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[41]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[42]  I M Young,et al.  Interactions and Self-Organization in the Soil-Microbe Complex , 2004, Science.

[43]  William B. Karesh,et al.  Connecting global priorities: biodiversity and human health: a state of knowledge review. , 2015 .

[44]  D. Baumgardner Soil-Related Bacterial and Fungal Infections , 2012, The Journal of the American Board of Family Medicine.

[45]  A. Iwasaki,et al.  Microbiota regulates immune defense against respiratory tract influenza A virus infection , 2011, Proceedings of the National Academy of Sciences.

[46]  Jacob G. Mills,et al.  High-throughput eDNA monitoring of fungi to track functional recovery in ecological restoration , 2018 .

[47]  T. Haahtela,et al.  Natural immunity , 2011, EMBO reports.