Asthma and selective migration from farming environments in a three-generation cohort study

Abstract

Individuals raised on a farm appear to have less asthma than individual raised elsewhere. However, selective migration might contribute to this as may also the suggested protection from farm environment. This study investigated if parents with asthma are less likely to raise their children on a farm. This study involved three generations: 6045 participants in ECRHS/RHINE cohorts (born 1945–1973, denoted G1), their 10,121 parents (denoted G0) and their 8260 offspring participating in RHINESSA (born 1963–1998, denoted G2). G2-offspring provided information on parents not participating in ECRHS/RHINE. Asthma status and place of upbringing for all three generations were reported in questionnaires by G1 in 2010–2012 and by G2 in 2013–2016. Binary regressions with farm upbringing as outcome were performed to explore associations between parental asthma and offspring farm upbringing in G0–G1 and G1–G2. Having at least one parent with asthma was not associated with offspring farm upbringing, either in G1–G2 (RR 1.11, 95% CI 0.81–1.52) or in G0–G1 (RR 0.99, 0.85–1.15). G1 parents with asthma born in a city tended to move and raise their G2 offspring on a farm (RR 2.00, 1.12–3.55), while G1 parents with asthma born on a farm were less likely to raise their G2 offspring on a farm (RR 0.34, 0.11–1.06). This pattern was not observed in analyses of G0–G1. This study suggests that the protective effect from farm upbringing on subsequent asthma development could not be explained by selective migration. Intriguingly, asthmatic parents appeared to change environment when having children.

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References

  1. 1.

    Timm S, Frydenberg M, Janson C, Campbell B, Forsberg B, Gislason T, Holm M, Jogi R, Omenaas E, Sigsgaard T, Svanes C, Schlünssen V. The urban-rural gradient in asthma: a population-based study in Northern Europe. Int J Environ Res Public Health. 2015;13:1–14. https://doi.org/10.3390/ijerph13010093.

    Article  CAS  Google Scholar 

  2. 2.

    Ege M, Mayer M. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364:701–9.

    Article  CAS  PubMed  Google Scholar 

  3. 3.

    Von Ehrenstein OS, Von Mutius E, Illi S, Baumann L, Böhm O, Von Kries R. Reduced risk of hay fever and asthma among children of farmers. Clin Exp Allergy. 2000;30:187–93. https://doi.org/10.1046/j.1365-2222.2000.00801.x.

    Article  Google Scholar 

  4. 4.

    Bråbäck L, Hjern A, Rasmussen F. Trends in asthma, allergic rhinitis and eczema among Swedish conscripts from farming and non-farming environments. A nationwide study over three decades. Clin Exp Allergy. 2004;34:38–43.

    Article  PubMed  Google Scholar 

  5. 5.

    Heederik D, Von Mutius E. Does diversity of environmental microbial exposure matter for the occurrence of allergy and asthma? J Allergy Clin Immunol. 2012;130:44–50. https://doi.org/10.1016/j.jaci.2012.01.067.

    Article  PubMed  Google Scholar 

  6. 6.

    Strachan DP. Hay fever, hygiene and household size. BMJ. 1989;299:1259–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Ege MJ, Frei R, Bieli C, Schram-Bijkerk D, Waser M, Benz MR, Weiss G, Nyberg F, van Hage M, Pershagen G, Brunekreef B, Riedler J, Lauener R, Braun-Fahrländer C, von Mutius E. Not all farming environments protect against the development of asthma and wheeze in children. J Allergy Clin Immunol. 2007;119:1140–7. https://doi.org/10.1016/j.jaci.2007.01.037.

    Article  PubMed  Google Scholar 

  8. 8.

    Wlasiuk G, Vercelli D. The farm effect, or: when, what and how a farming environment protects from asthma and allergic disease. Curr Opin Allergy Clin Immunol. 2012;12:461–6. https://doi.org/10.1097/ACI.0b013e328357a3bc.

    Article  PubMed  Google Scholar 

  9. 9.

    Basinas I, Sigsgaard T, Kromhout H, Heederik D, Wouters IM, Schlünssen V. A comprehensive review of levels and determinants of personal exposure to dust and endotoxin in livestock farming. J Expo Sci Environ Epidemiol. 2013. https://doi.org/10.1038/jes.2013.83.

    Article  PubMed  Google Scholar 

  10. 10.

    Bråbäck L, Hjern A, Rasmussen F, Van Schayck CP, Knottnerus JA. Selective migration contributes to a healthy worker effect in the farming population. J Clin Epidemiol. 2006;59:102–3. https://doi.org/10.1016/j.jclinepi.2005.08.003.

    Article  PubMed  Google Scholar 

  11. 11.

    Vogelzang PFJ, van der Gulden JWJ, Tielen MJ, Folgering H, van Schayck CP. Health based selection for asthma, but not for chronic bronchitis, in pig farmers: an evidence based hypothesis. Eur Respir J. 1999;13:187. https://doi.org/10.1034/j.1399-3003.1999.13a34.x.

    Article  CAS  PubMed  Google Scholar 

  12. 12.

    Eduard W, Schlünssen V, Sigsgaard T, Omland Ø, Pearce N, Douwes J. Can selection explain the protective effects of farming on asthma? Ann Agric Environ Med. 2015;22:467–9. https://doi.org/10.5604/12321966.1167715.

    Article  PubMed  Google Scholar 

  13. 13.

    Klintberg B, Berglund N, Lilja G, Wickman M, van Hage-Hamsten M. Fewer allergic respiratory disorders among farmers’ children in a closed birth cohort from Sweden. Eur Respir J. 2001;17:1151–7. https://doi.org/10.1183/09031936.01.00027301.

    Article  CAS  PubMed  Google Scholar 

  14. 14.

    Burney PGJ, Luczynska C, Chinn S, Jarvis D. The European community respiratory health survey. Eur Respir J. 1994;7:954–60. https://doi.org/10.1183/09031936.94.07050954.

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Johannessen A, Verlato G, Benediktsdottir B, Forsberg B, Franklin K, Gislason T, Holm M, Janson C, Jögi R, Lindberg E, Macsali F, Omenaas E, Real FG, Saure EW, Schlünssen V, Sigsgaard T, Skorge TD, Svanes C, Torén K, Waatevik M, Nilsen RM, de Marco R. Longterm follow-up in European respiratory health studies—patterns and implications. BMC Pulm Med. 2014;14:63. https://doi.org/10.1186/1471-2466-14-63.

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Glymour MM, Greenland S. Causal diagrams. In: Rothmann K, Greenland S, Lash  T, editors. Modern Epidemiology. Lippincott Williams & Wilkins; 2012. p. 183–212.

  17. 17.

    Pekkanen J, Pearce N. Defining asthma in epidemiological studies. Eur Respir J. 1999;14:951–7. https://doi.org/10.1034/j.1399-3003.1999.14d37.x.

    Article  CAS  PubMed  Google Scholar 

  18. 18.

    Kuiper IN, Svanes C, Benediktsdottir B, Bertelsen RJ, Bråbäck L, Dharmage SC, Holm M, Jögi R. Agreement in reporting of asthma by parents or offspring—the RHINESSA generation study. BMC Pulm Med. 2018. https://doi.org/10.1186/s12890-018-0687-4.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Kjøller M, Thoning H. Characteristics of non-response in the Danish Health Interview Surveys, 1987–1994. Eur J Public Health. 2005;15:528–35. https://doi.org/10.1093/eurpub/cki023.

    Article  PubMed  Google Scholar 

  20. 20.

    Demarest S, Van Der Heyden J, Charafeddine R, Tafforeau J, Van Oyen H, Van Hal G. Socio-economic differences in participation of households in a Belgian national health survey. Eur J Public Health. 2013;23:981–5. https://doi.org/10.1093/eurpub/cks158.

    Article  PubMed  Google Scholar 

  21. 21.

    Christensen S, Timm S, Janson C, Benediktsdottir B, Forsberg B, Holm M, Jogi R, Johannessen A, Omenaas E, Sigsgaard T, Svanes C, Schlünssen V. A clear urban-rural gradient of allergic rhinitis in a population-based study in Northern Europe. Eur Clin Respir J. 2016;3:33463.

    Article  PubMed  Google Scholar 

  22. 22.

    Campbell B, Lodge C, Lowe A, Burgess J, Matheson M, Dharmage S. Exposure to ‘farming’ and objective markers of atopy: a systematic review and meta-analysis. Clin Exp Allergy. 2015;45:744–57. https://doi.org/10.1111/cea.12429.

    Article  CAS  PubMed  Google Scholar 

  23. 23.

    Svanes C, Zock J-P, Antó J, Dharmage S, Norbäck D, Jarvis D, De Marco R, Plana E, Raherison C, Sunyer J. Do asthma and allergy influence subsequent pet keeping? An analysis of childhood and adulthood. J Allergy Clin Immunol. 2006. https://doi.org/10.1016/j.jaci.2006.06.017.

    Article  PubMed  Google Scholar 

  24. 24.

    Bornehag CG, Sundell J, Hagerhed L, Janson S. Pet-keeping in early childhood and airway, nose and skin symptoms later in life. Allergy Eur J Allergy Clin Immunol. 2003;58:939–44. https://doi.org/10.1034/j.1398-9995.2003.00050.x.

    Article  CAS  Google Scholar 

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Funding

The ECRHS/RHINE/RHINESSA study was supported by grants from The Faculty of Health, Aarhus University, Denmark (Project No. 240008), The Wood Dust Foundation (Project No. 444508795), The Danish Lung Association, the Swedish Heart and Lung Foundation, the Swedish Association Against Asthma and Allergy, the Swedish Association against Heart and Lung Disease, the Swedish Council for Working Life and Social Research, The Bror Hjerpstedt Foundation, The Vårdal Foundation for Health Care and Allergic Research, The Norwegian Research Council (Grant Nos. 214123, 230827/F20, 228174 and 135773/330), The Norwegian Asthma and Allergy Association, HelseVest Norway (Grant No. 911 631), The Icelandic Research Council, The University of Iceland Research Fund, The Icelandic GP’s Research Fund, The Estonian Science Foundation (Grant No. 4350), The Estonian Research Council (Grant No. PUT562), Melbourne University, National Health & Medical Research Council of Australia, SEPAR Spain, Sociedad Española de Neumologia y Cirugía Toracica Spain and Horizon2020 PHC1 (Grant No. 633212). For further information about funding sources, please consult www.rhinessa.net. Vivi Schlünssen and Cecilie Svanes are members of the COST BM1201 network. Signe Timm received a PhD scholarship from Aarhus University, Denmark.

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Correspondence to Signe Timm.

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Michael Abramson has received investigator-initiated grants from Pfizer and Boehringer-Ingelheim for unrelated research. The other authors declare no conflict of interest.

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Timm, S., Frydenberg, M., Abramson, M.J. et al. Asthma and selective migration from farming environments in a three-generation cohort study. Eur J Epidemiol 34, 601–609 (2019). https://doi.org/10.1007/s10654-019-00491-9

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Keywords

  • Asthma
  • Farming
  • Selective migration
  • ECRHS
  • RHINE
  • RHINESSA