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Regulation of the immune system by biodiversity from the natural environment: An ecosystem service essential to health
Open accessAbstract
Epidemiological studies suggest that living close to the natural environment is associated with long-term health benefits including reduced death rates, reduced cardiovascular disease, and reduced psychiatric problems. This is often attributed to psychological mechanisms, boosted by exercise, social interactions, and sunlight. Compared with urban environments, exposure to green spaces does indeed trigger rapid psychological, physiological, and endocrinological effects. However, there is little evidence that these rapid transient effects cause long-term health benefits or even that they are a specific property of natural environments. Meanwhile, the illnesses that are increasing in high-income countries are associated with failing immunoregulation and poorly regulated inflammatory responses, manifested as chronically raised C-reactive protein and proinflammatory cytokines. This failure of immunoregulation is partly attributable to a lack of exposure to organisms (“Old Friends”) from mankind’s evolutionary past that needed to be tolerated and therefore evolved roles in driving immunoregulatory mechanisms. Some Old Friends (such as helminths and infections picked up at birth that established carrier states) are almost eliminated from the urban environment. This increases our dependence on Old Friends derived from our mothers, other people, animals, and the environment. It is suggested that the requirement for microbial input from the environment to drive immunoregulation is a major component of the beneficial effect of green space, and a neglected ecosystem service that is essential for our well-being. This insight will allow green spaces to be designed to optimize health benefits and will provide impetus from health systems for the preservation of ecosystem biodiversity.
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“Beyond physiological benefits, natural environments foster mental well-being and social engagement, reducing anxiety, depression, and cognitive decline risks [52,53,54].”
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Cites
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823
De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccini, G., & Lionetti, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005963107 · Cited by 5,579
The rhizosphere microbiome and plant health
Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012) · Trends in Plant Science · doi:10.1016/j.tplants.2012.04.001 · Cited by 5,347
View Through a Window May Influence Recovery from Surgery
Ulrich, R. S. (1984) · Science · doi:10.1126/science.6143402 · Cited by 5,341
The gut microbiota shapes intestinal immune responses during health and disease
Round, J. L., & Mazmanian, S. K. (2009) · Nature Reviews Immunology · doi:10.1038/nri2515 · Cited by 5,029
Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species
Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., et al. (2011) · Science · doi:10.1126/science.1198469 · Cited by 3,752
Gut microbiota composition correlates with diet and health in the elderly
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O’Connor, E. M., Cusack, S., Harris, H. M. B., Coakley, M., Lakshminarayanan, B., O’Sullivan, O., et al. (2012) · Nature · doi:10.1038/nature11319 · Cited by 3,314
Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis.
Howren, M. B., Lamkin, D. M., & Suls, J. (2009) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181907c1b · Cited by 2,766
The Effect of Infections on Susceptibility to Autoimmune and Allergic Diseases
Bach, J. (2002) · New England Journal of Medicine · doi:10.1056/nejmra020100 · Cited by 2,723
Millennium Ecosystem Assessment
Sadler, B., & Dalal-Clayton, B. (2012) · Routledge eBooks · doi:10.4324/9781849772631-19 · Cited by 2,625
The cognitive benefits of interacting with nature.
Berman, M. G., Jonides, J., & Kaplan, S. (2008) · Psychological Science · doi:10.1111/j.1467-9280.2008.02225.x · Cited by 2,535
Gleeson, M., Bishop, N. C., Stensel, D. J., Lindley, M. R., Mastana, S. S., & Nimmo, M. A. (2011) · Nature Reviews Immunology · doi:10.1038/nri3041 · Cited by 2,470
Insights into the phylogeny and coding potential of microbial dark matter
Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N. N., Anderson, I. J., Cheng, J.-F., Darling, A., Malfatti, S., Swan, B. K., Gies, E. A., et al. (2013) · Nature · doi:10.1038/nature12352 · Cited by 2,394
Rosenthal, N. E. (1984) · Archives of General Psychiatry · doi:10.1001/archpsyc.1984.01790120076010 · Cited by 2,385
Dethlefsen, L., Huse, S., Sogin, M. L., & Relman, D. A. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060280 · Cited by 2,361
Effect of exposure to natural environment on health inequalities: an observational population study
Mitchell, R., & Popham, F. (2008) · The Lancet · doi:10.1016/s0140-6736(08)61689-x · Cited by 2,099
NLRP6 Inflammasome Regulates Colonic Microbial Ecology and Risk for Colitis
Elinav, E., Strowig, T., Kau, A. L., Henao-Mejia, J., Thaiss, C. A., Booth, C. J., Peaper, D. R., Bertin, J., Eisenbarth, S. C., Gordon, J. I., et al. (2011) · Cell · doi:10.1016/j.cell.2011.04.022 · Cited by 2,024
Green space, urbanity, and health: how strong is the relation?
Maas, J., Verheij, R. A., Groenewegen, P. P., de Vries, S., & Spreeuwenberg, P. (2006) · Journal of Epidemiology and Community Health · doi:10.1136/jech.2005.043125 · Cited by 1,976
Innate immunity and intestinal microbiota in the development of Type 1 diabetes
Wen, L., Ley, R. E., Volchkov, P. Y., Stranges, P. B., Avanesyan, L., Stonebraker, A. C., Hu, C., Wong, F. S., Szot, G. L., Bluestone, J. A., et al. (2008) · Nature · doi:10.1038/nature07336 · Cited by 1,921
The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota
Round, J. L., Lee, S. M., Li, J., Tran, G., Jabri, B., Chatila, T. A., & Mazmanian, S. K. (2011) · Science · doi:10.1126/science.1206095 · Cited by 1,604
Exposure to Environmental Microorganisms and Childhood Asthma
Ege, M. J., Mayer, M., Normand, A.-C., Genuneit, J., Cookson, W. O. C. M., Braun-Fahrländer, C., Heederik, D., Piarroux, R., & von Mutius, E. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1007302 · Cited by 1,529
Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey
Riedler, J., Braun-Fahrländer, C., Eder, W., Schreuer, M., Waser, M., Maisch, S., Carr, D., Schierl, R., Nowak, D., & von Mutius, E. (2001) · The Lancet · doi:10.1016/s0140-6736(01)06252-3 · Cited by 1,520
Thompson Coon, J., Boddy, K., Stein, K., Whear, R., Barton, J., & Depledge, M. H. (2011) · Environmental Science & Technology · doi:10.1021/es102947t · Cited by 1,391
de Vries, S., Verheij, R. A., Groenewegen, P. P., & Spreeuwenberg, P. (2003) · Environment and Planning A: Economy and Space · doi:10.1068/a35111 · Cited by 1,258
Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity
Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., & Weiser, J. N. (2010) · Nature Medicine · doi:10.1038/nm.2087 · Cited by 1,154
Morbidity is related to a green living environment
Maas, J., Verheij, R. A., de Vries, S., Spreeuwenberg, P., Schellevis, F. G., & Groenewegen, P. P. (2009) · Journal of Epidemiology and Community Health · doi:10.1136/jech.2008.079038 · Cited by 1,133
Cohabiting family members share microbiota with one another and with their dogs
Song, S. J., Lauber, C. L., Costello, E. K., Lozupone, C., Humphrey, G., Berg-Lyons, D., Caporaso, J. G., Knights, D., Clemente, J. C., Nakielny, S., et al. (2013) · eLife · doi:10.7554/elife.00458 · Cited by 1,120
Park, B. J., Tsunetsugu, Y., Kasetani, T., Kagawa, T., & Miyazaki, Y. (2010) · Environmental Health and Preventive Medicine · doi:10.1007/s12199-009-0086-9 · Cited by 1,116
Compartmentalized Control of Skin Immunity by Resident Commensals
Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M. J., Salcedo, R., Kastenmuller, W., Deming, C., Quinones, M., Koo, L., Conlan, S., et al. (2012) · Science · doi:10.1126/science.1225152 · Cited by 1,092
Hemarajata, P., & Versalovic, J. (2013) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x12459294 · Cited by 1,083
McGrath, J., Saha, S., Welham, J., El Saadi, O., MacCauley, C., & Chant, D. (2004) · BMC Medicine · doi:10.1186/1741-7015-2-13 · Cited by 1,072
The current status of urban‐rural differences in psychiatric disorders
Peen, J., Schoevers, R. A., Beekman, A. T. F., & Dekker, J. (2009) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2009.01438.x · Cited by 1,068
Environmental biodiversity, human microbiota, and allergy are interrelated
Hanski, I., von Hertzen, L., Fyhrquist, N., Koskinen, K., Torppa, K., Laatikainen, T., Karisola, P., Auvinen, P., Paulin, L., Mäkelä, M. J., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205624109 · Cited by 1,063
The genomic signature of dog domestication reveals adaptation to a starch-rich diet
Axelsson, E., Ratnakumar, A., Arendt, M.-L., Maqbool, K., Webster, M. T., Perloski, M., Liberg, O., Arnemo, J. M., Hedhammar, Å., & Lindblad-Toh, K. (2013) · Nature · doi:10.1038/nature11837 · Cited by 963
Smits, H. H., Engering, A. J., van der Kleij, D., de Jong, E. C., Schipper, K., van Capel, T. M. M., Zaat, B. A. J., Yazdanbakhsh, M., Wierenga, E. A., & van Kooyk, Y. (2005) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2005.03.036 · Cited by 778
Frumkin, H. (2001) · American Journal of Preventive Medicine · doi:10.1016/s0749-3797(00)00317-2 · Cited by 765
Ownby, D. R. (2002) · JAMA · doi:10.1001/jama.288.8.963 · Cited by 736
Fertile Ground for Community: Inner‐City Neighborhood Common Spaces
Kuo, F. E., SULLIVAN, W. C., Coley, R. L., & Brunson, L. (1998) · American Journal of Community Psychology · doi:10.1023/a:1022294028903 · Cited by 706
Multiple sclerosis: Geoepidemiology, genetics and the environment
Milo, R., & Kahana, E. (2009) · Autoimmunity Reviews · doi:10.1016/j.autrev.2009.11.010 · Cited by 681
A meta‐analysis of the association between Caesarean section and childhood asthma
Thavagnanam, S., Fleming, J., Bromley, A., Shields, M. D., & Cardwell, C. R. (2008) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2007.02780.x · Cited by 651
Urban aerosols harbor diverse and dynamic bacterial populations
Brodie, E., DeSantis, T. Z., Parker, J. M., Zubieta, I. X., Piceno, Y. M., & Andersen, G. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608255104 · Cited by 642
Bringing the ocean into the laboratory to probe the chemical complexity of sea spray aerosol
Prather, K. A., Bertram, T. H., Grassian, V. H., Deane, G. B., Stokes, M. D., DeMott, P. J., Aluwihare, L. I., Palenik, B. P., Azam, F., Seinfeld, J. H., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300262110 · Cited by 633
Kowalchuk, G. A., Buma, D. S., de Boer, W., Klinkhamer, P. G. L., & van Veen, J. A. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020565523615 · Cited by 624
Turner, T. R., Karunakaran, R., Walshaw, J., Heavens, D., Alston, M. J., Swarbreck, D., Osbourn, A., Grant, A., & Poole, P. S. (2013) · The ISME Journal · doi:10.1038/ismej.2013.119 · Cited by 582
The urban brain: Analysing outdoor physical activity with mobile EEG
Aspinall, P., Mavros, P., Coyne, R., & Roe, J. (2015) · British Journal of Sports Medicine · doi:10.1136/bjsports-2012-091877 · Cited by 574
Burrows, S. M., Elbert, W., Lawrence, M. G., & Pöschl, U. (2009) · Atmospheric chemistry and physics · doi:10.5194/acp-9-9263-2009 · Cited by 565
Gimeno, D., Kivimäki, M., Brunner, E. J., Elovainio, M., De Vogli, R., Steptoe, A., Kumari, M., Lowe, G. D. O., Rumley, A., Marmot, M. G., et al. (2009) · Psychological Medicine · doi:10.1017/s0033291708003723 · Cited by 561
Architectural design influences the diversity and structure of the built environment microbiome
Kembel, S. W., Jones, E. B. G., Kline, J., Northcutt, D., Stenson, J., Womack, A. M., Bohannan, B. J. M., Brown, G. Z., & Green, J. L. (2012) · The ISME Journal · doi:10.1038/ismej.2011.211 · Cited by 542
Zuany‐Amorim, C., Sawicka, E., Manlius, C., Moine, A. L., Brunet, L. R., Kemeny, D. M., Bowen, G., Rook, G. A. W., & Walker, C. (2002) · Nature Medicine · doi:10.1038/nm0602-625 · Cited by 514
Self-citationHildebrand, F., Nguyen, T. L. A., Brinkman, B. M. N., Yunta, R. G., Cauwe, B., Vandenabeele, P., Liston, A., & Raes, J. (2013) · Genome biology · doi:10.1186/gb-2013-14-1-r4 · Cited by 478
Grainger, J. R., Smith, K. A., Hewitson, J. P., McSorley, H. J., Harcus, Y., Filbey, K. J., Finney, C. A. M., Greenwood, E. J. D., Knox, D. P., Wilson, M. S., et al. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20101074 · Cited by 469
Association between parasite infection and immune responses in multiple sclerosis
Correale, J. D., & Farez, M. (2007) · Annals of Neurology · doi:10.1002/ana.21067 · Cited by 461
DeLeón-Rodriguez, N., Lathem, T. L., Rodriguez‐R, L. M., Barazesh, J. M., Anderson, B. E., Beyersdorf, A. J., Ziemba, L. D., Bergin, M., Nenes, A., & Konstantinidis, K. T. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1212089110 · Cited by 453
Urbanisation and incidence of psychosis and depression
Sundquist, K., Frank, G., & Sundquist, J. (2004) · The British Journal of Psychiatry · doi:10.1192/bjp.184.4.293 · Cited by 434
Virus-specific CD4(+) memory-phenotype T cells are abundant in unexposed adults
Su, L. F., Kidd, B. A., Han, A., Kotzin, J. J., & Davis, M. M. (2013) · Immunity · doi:10.1016/j.immuni.2012.10.021 · Cited by 429
Hygiene Hypothesis and Autoimmune Diseases
Rook, G. A. W. (2011) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-011-8285-8 · Cited by 419
Self-citationMaas, J., Verheij, R. A., Spreeuwenberg, P. M. M., & Groenewegen, P. (2008) · BMC Public Health · doi:10.1186/1471-2458-8-206 · Cited by 411
Tsunetsugu, Y., Park, B., & Miyazaki, Y. (2009) · Environmental Health and Preventive Medicine · doi:10.1007/s12199-009-0091-z · Cited by 402
Does living by the coast improve health and wellbeing?
Wheeler, B. W., White, M. P., Stahl-Timmins, W., & Depledge, M. H. (2012) · Health & Place · doi:10.1016/j.healthplace.2012.06.015 · Cited by 393
Karimi, K., Inman, M. D., Bienenstock, J., & Forsythe, P. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200806-951oc · Cited by 361
Lauritsen, M. B., Pedersen, C. B., & Mortensen, P. B. (2005) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2004.00391.x · Cited by 359
Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation?
MEYER, U., FELDON, J., & DAMMANN, O. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e318212c196 · Cited by 357
Home Life: Factors Structuring the Bacterial Diversity Found within and between Homes
Dunn, R. R., Fierer, N., Henley, J. B., Leff, J., & Menninger, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064133 · Cited by 354
Biodiversity and biogeography of the atmosphere
Womack, A. M., Bohannan, B. J. M., & Green, J. L. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0283 · Cited by 348
Rook, G. A. W. (2010) · Clinical and Experimental Immunology · doi:10.1111/j.1365-2249.2010.04133.x · Cited by 332
Self-citationMulder, I. E., Schmidt, B., Stokes, C., Lewis, M. C., Bailey, M., Aminov, R. I., Prosser, J. I., Gill, B. P., Pluske, J. R., Mayer, C., et al. (2009) · BMC Biology · doi:10.1186/1741-7007-7-79 · Cited by 311
Green space, health inequality and pregnancy
Dadvand, P., de Nazelle, A. J., Figueras, F., Basagaña, X., Su, J. G., Amoly, E., Jerrett, M., Vrijheid, M., Sunyer, J., & Nieuwenhuijsen, M. J. (2011) · Environment International · doi:10.1016/j.envint.2011.07.004 · Cited by 305
von Hertzen, L., Hanski, I., & Haahtela, T. (2011) · The EMBO Reports · doi:10.1038/embor.2011.195 · Cited by 304
Isotopic evidence of early hominin diets
Sponheimer, M., Alemseged, Z., Cerling, T. E., Grine, F. E., Kimbel, W. H., Leakey, M. G., Lee‐Thorp, J. A., Manthi, F. K., Reed, K. E., Wood, B. A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222579110 · Cited by 291
Migrant studies in multiple sclerosis
Galé, C. R., & Martyn, C. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)80008-v · Cited by 289
Leck, C., & Bigg, E. K. (2005) · Tellus B · doi:10.3402/tellusb.v57i4.16546 · Cited by 285
Debarry, J., Garn, H., Hanuszkiewicz, A., Dickgreber, N., Blümer, N., von Mutius, E., Bufe, A., Gatermann, S. G., Renz, H., Holst, O., et al. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.03.023 · Cited by 281
The association between low vitamin D and depressive disorders
Milaneschi, Y., Hoogendijk, W. J. G., Lips, P. T. A. M., Heijboer, A. C., Schoevers, R. A., van Hemert, A. M., Beekman, A. T. F., Smit, J. H., & Penninx, B. W. J. H. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.36 · Cited by 265
Microbial ‘Old Friends’, immunoregulation and stress resilience
Rook, G. A. W., Lowry, C. A., & Raison, C. L. (2013) · Evolution Medicine and Public Health · doi:10.1093/emph/eot004 · Cited by 258
Self-citationProbiotic helminth administration in relapsing–remitting multiple sclerosis: a phase 1 study
Fleming, J. O., Isaak, A., Lee, J., Luzzio, C. C., Carrithers, M. D., Cook, T., Field, A. S., Boland, J., & Fábry, Z. (2011) · Multiple Sclerosis Journal · doi:10.1177/1352458511398054 · Cited by 257
Use of Antibiotics during Pregnancy Increases the Risk of Asthma in Early Childhood
Stensballe, L. G., Simonsen, J., Jensen, S. M., Bønnelykke, K., & Bisgaard, H. F. (2012) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2012.09.049 · Cited by 248
Man's best friend? The effect of pet ownership on house dust microbial communities
Fujimura, K. E., Johnson, C. C., Ownby, D. R., Cox, M. J., Brodie, E., Havstad, S. L., Zoratti, E. M., Woodcroft, K. J., Bobbitt, K. R., Wegienka, G., et al. (2010) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2010.05.042 · Cited by 244
The impact of parasite infections on the course of multiple sclerosis
Correale, J. D., & Farez, M. (2011) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2011.01.002 · Cited by 237
Allergic disease in urban and rural populations: increasing prevalence with increasing urbanization
Nicolaou, N. C., Siddique, N., & Čustović, A. (2005) · Allergy · doi:10.1111/j.1398-9995.2005.00961.x · Cited by 237
Babu, S., Blauvelt, C. P., Kumaraswami, V., & Nutman, T. B. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.5.3248 · Cited by 230
Culturable Airborne Bacteria in Outdoor Environments in Beijing, China
Fang, Z., Ouyang, Z., Zheng, H., Wang, X., & Hu, L. (2007) · Microbial Ecology · doi:10.1007/s00248-007-9216-3 · Cited by 230
Vega, W. A., Sribney, W. M., Aguilar‐Gaxiola, S., & Kolody, B. (2004) · The Journal of Nervous and Mental Disease · doi:10.1097/01.nmd.0000135477.57357.b2 · Cited by 220
Oakes, J. M., Forsyth, A., & Schmitz, K. H. (2007) · Epidemiologic Perspectives & Innovations · doi:10.1186/1742-5573-4-16 · Cited by 216
Hou, J. K., El‐Serag, H. B., & Thirumurthi, S. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.190 · Cited by 210
Lowry, C. A., Hollis, J. H., de Vries, A., Pan, B., Brunet, L. R., Hunt, J. R. F., Paton, J. F. R., van Kampen, E., Knight, D. M., Evans, A. K., et al. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.01.067 · Cited by 199
Self-citationGreen cities and health: a question of scale?
Richardson, E. A., Mitchell, R., Hartig, T., de Vries, S., Astell‐Burt, T., & Frumkin, H. (2011) · Journal of Epidemiology & Community Health · doi:10.1136/jech.2011.137240 · Cited by 193
Prenatal exposure to a farm environment modifies atopic sensitization at birth
Ege, M. J., Herzum, I., Büchele, G., Krauss‐Etschmann, S., Lauener, R. P., Roponen, M., Hyvärinen, A., Vuitton, D. A., Riedler, J., Brunekreef, B., et al. (2008) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2008.06.011 · Cited by 181
Carr, I., & Mayberry, J. F. (1999) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.1999.01438.x · Cited by 179
A six‐fold gradient in the incidence of type 1 diabetes at the eastern border of Finland
Kondrashova, A., Reunanen, A., Romanov, A., Karvonen, A., Viskari, H., Vesikari, T., Ilonen, J., Knip, M., & Hyöty, H. (2005) · Annals of Medicine · doi:10.1080/07853890410018952 · Cited by 177
Does diversity of environmental microbial exposure matter for the occurrence of allergy and asthma?
Heederik, D. J. J., & von Mutius, E. (2012) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2012.01.067 · Cited by 175
Mooney, H. A., Cropper, A., & Reid, W. V. (2005) · Nature · doi:10.1038/434561a · Cited by 175
Aerosolized Red-Tide Toxins (Brevetoxins) and Asthma
Fleming, L. E., Kirkpatrick, B., Backer, L. C., Bean, J. A., Wanner, A., Reich, A., Zaias, J., Cheng, Y. S., Pierce, R., Naar, J. P., et al. (2007) · CHEST Journal · doi:10.1378/chest.06-1830 · Cited by 167
Breslau, J. A., Borges, G. L. G., Hagar, Y., Tancredi, D. J., & Gilman, S. E. (2008) · Psychological Medicine · doi:10.1017/s0033291708004698 · Cited by 164
McDade, T. W., Rutherford, J., Adair, L., & Kuzawa, C. W. (2010) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2009.1795 · Cited by 162
Studies on the natural history of multiple sclerosis
Beebe, G. W., Kurtzke, J. F., Kurland, L. T., Auth, T. L., & Nagler, B. (1967) · Neurology · doi:10.1212/wnl.17.1.1 · Cited by 159
Rehman, A., Lepage, P., Nolte, A., Hellmig, S., Schreiber, S., & Ott, S. J. (2010) · Journal of Medical Microbiology · doi:10.1099/jmm.0.021170-0 · Cited by 150
Radon, K., Windstetter, D., Poluda, A. L., Mueller, B., von Mutius, E., Koletzko, S., & Chronische Autoimmunerkrankungen und Kontakt zu Tieren (Chronic Autoimmune Disease and Animal Contact) Study Group (2007) · PEDIATRICS · doi:10.1542/peds.2006-3624 · Cited by 136
Adaptation and habitat selection in the eco-evolutionary process
Morris, D. W. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.0604 · Cited by 134
Epidemiologic Study of Multiple Sclerosis in Israel
ANTONOVSKY, A. (1965) · Archives of Neurology · doi:10.1001/archneur.1965.00470020073010 · Cited by 124
Predominance of Gram‐positive bacteria in house dust in the low‐allergy risk Russian Karelia
Pakarinen, J., Hyvärinen, A., Salkinoja-Salonen, M. S., Laitinen, S., Nevalainen, A. I., Mäkelä, M. J., Haahtela, T., & von Hertzen, L. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01723.x · Cited by 122
Is sunlight good for our heart?
Feelisch, M., Kolb-Bachofen, V., Liu, D., Lundberg, J. O., Revelo, L. P., Suschek, C. V., & Weller, R. (2010) · European Heart Journal · doi:10.1093/eurheartj/ehq069 · Cited by 113
Mcdade, T. W., Tallman, P. S., Madimenos, F. C., Liebert, M. A., Cepon, T. J., Sugiyama, L. S., & Snodgrass, J. J. (2012) · American Journal of Human Biology · doi:10.1002/ajhb.22296 · Cited by 113
STUDIES ON THE NATURAL HISTORY OF MULTIPLE SCLEROSIS
Nagler, B., Beebe, G. W., Kurtzke, J. F., Kurland, L. T., Auth, T. L., & Nefzger, M. D. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1966.tb02012.x · Cited by 107
Andersson, M. A., Mikkola, R., KROPPENSTEDT, R. M., Rainey, F. A., Peltola, J., Helin, J., Sivonen, K., & Salkinoja-Salonen, M. S. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.12.4767-4773.1998 · Cited by 106
Risk of inflammatory bowel disease in first- and second-generation immigrants in Sweden
Li, X., Sundquist, J., Hemminki, K., & Sundquist, K. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21535 · Cited by 97
Rottem, M., Szyper‐Kravitz, M., & Shoenfeld, Y. (2005) · International Archives of Allergy and Immunology · doi:10.1159/000083894 · Cited by 93
Significant changes in the skin microbiome mediated by the sport of roller derby
Meadow, J. F., Bateman, A. C., Herkert, K. M., O’Connor, T. K., & Green, J. L. (2013) · PeerJ · doi:10.7717/peerj.53 · Cited by 90
Söderström, U., Åman, J., & Hjern, A. (2012) · Acta Paediatrica · doi:10.1111/j.1651-2227.2011.02410.x · Cited by 88
Nehmé, B., Gilbert, Y., Létourneau, V., Forster, R. J., Veillette, M., Villemur, R., & Duchaine, C. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00726-09 · Cited by 88
Parasitic Helminths: New Weapons against Immunological Disorders
Osada, Y., & Kanazawa, T. (2010) · BioMed Research International · doi:10.1155/2010/743758 · Cited by 87
Repeated bouts of aerobic exercise enhance regulatory T cell responses in a murine asthma model
Lowder, T., Dugger, K. J., Deshane, J. S., Estell, K., & Schwiebert, L. M. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.09.011 · Cited by 86
McDade, T. W., Hoke, M., Borja, J. B., Adair, L. S., & Kuzawa, C. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.08.010 · Cited by 83
Hagner, S., Harb, H., Zhao, M., Stein, K., Holst, O., Ege, M. J., Mayer, M., Matthes, J., Bauer, J., von Mutius, E., et al. (2013) · Allergy · doi:10.1111/all.12094 · Cited by 79
Prenatal exposure to household pets influences fetal immunoglobulin E production
Aichbhaumik, N., Zoratti, E. M., Strickler, R. C., Wegienka, G., Ownby, D. R., Havstad, S. L., & Johnson, C. C. (2008) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2008.03079.x · Cited by 79
Exposure of Sink Drain Microcosms to Triclosan: Population Dynamics and Antimicrobial Susceptibility
McBain, A. J., Bartolo, R. G., Catrenich, C. E., Charbonneau, D. L., Ledder, R. G., Price, B. B., & Gilbert, P. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.9.5433-5442.2003 · Cited by 78
Vogel, K., Blümer, N., Korthals, M., Mittelstädt, J., Garn, H., Ege, M. J., von Mutius, E., Gatermann, S. G., Bufe, A., Goldmann, T., et al. (2008) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2008.05.016 · Cited by 71
Sunlight therapy and solar architecture
Hobday, R. A. (1997) · Medical History · doi:10.1017/s0025727300063043 · Cited by 68
Sick building syndrome in relation to domestic exposure in Sweden - A cohort study from 1991 to 2001
Sahlberg, B., Wieslander, G., & Norbäck, D. (2009) · Scandinavian Journal of Public Health · doi:10.1177/1403494809350517 · Cited by 66
Environmental changes and epidemiology of multiple sclerosis in the French West Indies
Cabre, P. (2009) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2009.04.039 · Cited by 62
Heydenreich, B., Bellinghausen, I., König, B., Becker, W. M., Grabbe, S., Petersen, A., & Saloga, J. (2011) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2011.03888.x · Cited by 59
Hunt, J. R. F., Martinelli, R., Adams, V., Rook, G. A. W., & Brunet, L. R. (2005) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2005.02239.x · Cited by 58
Self-citationA nationwide survey of the prevalence of multiple sclerosis in immigrant populations of Sweden
Ahlgren, C., Odén, A., & Lycke, J. (2011) · Multiple Sclerosis Journal · doi:10.1177/1352458511433062 · Cited by 55
Hjern, A., Rasmussen, F. E., & Hedlin, G. (1999) · Pediatric Allergy and Immunology · doi:10.1034/j.1399-3038.1999.00023.x · Cited by 51
High-Sensitive C-Reactive Protein: Universal Prognostic and Causative Biomarker in Heart Disease?
Rietzschel, E. R., & Buyzere, M. D. (2012) · Biomarkers in Medicine · doi:10.2217/bmm.11.108 · Cited by 49
Jansson, J. K., & Prosser, J. I. (2013) · Nature · doi:10.1038/494040a · Cited by 47
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Kuiper, J., van Puijvelde, G. H. M., van Wanrooij, E. J. A., van Es, T., Habets, K. L. L., Hauer, A. D., & van Berkel, T. J. C. (2007) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e3282efd0d4 · Cited by 45
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Lowis, G. W. (1990) · The Science of The Total Environment · doi:10.1016/0048-9697(90)90192-w · Cited by 36
Eldeirawi, K. M., McConnell, R., Furner, S. E., Freels, S. A., Stayner, L. T., Hernández, E., Amoruso, L., Torres, S., & Persky, V. (2009) · Journal of Asthma · doi:10.3109/02770900903114572 · Cited by 35
Kirkpatrick, B., Currier, R., Nierenberg, K., Reich, A., Backer, L. C., Stumpf, R. P., Fleming, L. E., & Kirkpatrick, G. J. (2008) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2008.03.032 · Cited by 35
MacNeill, S., Sozańska, B., Danielewicz, H., Dębińska, A., Kosmeda, A., Boznański, A., Illi, S., Depner, M., Strunz‐Lehner, C., Waser, M., et al. (2013) · Allergy · doi:10.1111/all.12141 · Cited by 34
Migration and multiple sclerosis: The French West Indies experience
Cabre, P. (2007) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2007.06.044 · Cited by 32
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Kovess–Masféty, V., Lecoutour, X., & Delavelle, S. (2005) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/s00127-005-0934-x · Cited by 31
Pereg, D., Tirosh, A., Lishner, M., Goldberg, A., Shochat, T., & Confino‐Cohen, R. (2008) · Allergy · doi:10.1111/j.1398-9995.2008.01661.x · Cited by 31
Nyqvist, F., Nygård, M., & Steenbeek, W. (2013) · International Journal of Behavioral Medicine · doi:10.1007/s12529-013-9307-0 · Cited by 28
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Metadata
- Authors
- Rook, G. A.
- Affiliations
- National Institute for Health and Care Research (GB)
- Corresponding author
- Rook, Graham A.
- ORCID
- Rook, Graham A.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-10-23
- Volume
- 110
- Issue
- 46
- Pages
- 18360-18367
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3831972
- OpenAlex
- W2051692047
- Cited by
- 760
- References
- 135
- Citations by year
- 2026: 65 · 2025: 56 · 2024: 71 · 2023: 62 · 2022: 69 · 2021: 69 · 2020: 57 · 2019: 61 · 2018: 103 · 2017: 41 · 2016: 46 · 2015: 37 · 2014: 22
- FWCI
- 4.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- NIHR Biomedical Research Centre, Royal Marsden NHS Foundation Trust/Institute of Cancer Research
- University College London
- National Institutes of Health
- Topics
- Social Sciences › Urban Studies › Urban Green Space and Health
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Asthma and respiratory diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- immune regulation, biodiversity, ecosystem services, green spaces, old friends hypothesis, helminths, microbial exposure, inflammation, C-reactive protein, inflammatory cytokines, mental health, cardiovascular disease, green space design, biodiversity conservation
- MeSH terms
- Environment, Humans, Biodiversity, Adaptive Immunity, Hygiene Hypothesis, Microbiota
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