European Journal of Epidemiology

, Volume 34, Issue 6, pp 601–609 | Cite as

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

  • Signe TimmEmail author
  • Morten Frydenberg
  • Michael J. Abramson
  • Randi J. Bertelsen
  • Lennart Bråbäck
  • Bryndis Benediktsdottir
  • Thorarinn Gislason
  • Mathias Holm
  • Christer Janson
  • Rain Jogi
  • Ane Johannessen
  • Jeong-Lim Kim
  • Andrei Malinovschi
  • Gita Mishra
  • Jesús Moratalla
  • Torben Sigsgaard
  • Cecilie Svanes
  • Vivi Schlünssen


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.


Asthma Farming Selective migration ECRHS RHINE RHINESSA 



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 Vivi Schlünssen and Cecilie Svanes are members of the COST BM1201 network. Signe Timm received a PhD scholarship from Aarhus University, Denmark.

Compliance with ethical standards

Conflict of interest

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

Supplementary material

10654_2019_491_MOESM1_ESM.docx (449 kb)
Supplementary material 1 (DOCX 449 kb)


  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. Scholar
  2. 2.
    Ege M, Mayer M. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364:701–9.CrossRefPubMedGoogle 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. 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.CrossRefPubMedGoogle 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. Scholar
  6. 6.
    Strachan DP. Hay fever, hygiene and household size. BMJ. 1989;299:1259–60.CrossRefPubMedPubMedCentralGoogle 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. 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. 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. 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. 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. 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. 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. Scholar
  14. 14.
    Burney PGJ, Luczynska C, Chinn S, Jarvis D. The European community respiratory health survey. Eur Respir J. 1994;7:954–60. 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. 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.Google Scholar
  17. 17.
    Pekkanen J, Pearce N. Defining asthma in epidemiological studies. Eur Respir J. 1999;14:951–7. 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. 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. 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. 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.CrossRefPubMedGoogle 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. 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. 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. Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Signe Timm
    • 1
    Email author
  • Morten Frydenberg
    • 1
  • Michael J. Abramson
    • 2
  • Randi J. Bertelsen
    • 3
  • Lennart Bråbäck
    • 4
  • Bryndis Benediktsdottir
    • 5
    • 6
  • Thorarinn Gislason
    • 5
    • 7
  • Mathias Holm
    • 8
  • Christer Janson
    • 9
  • Rain Jogi
    • 10
  • Ane Johannessen
    • 11
    • 12
  • Jeong-Lim Kim
    • 13
  • Andrei Malinovschi
    • 14
  • Gita Mishra
    • 15
  • Jesús Moratalla
    • 16
  • Torben Sigsgaard
    • 1
  • Cecilie Svanes
    • 11
    • 12
  • Vivi Schlünssen
    • 1
    • 17
  1. 1.Department of Public Health, Danish Ramazzini CentreAarhus UniversityAarhus CDenmark
  2. 2.School of Public Health and Preventive MedicineMonash UniversityMelbourneAustralia
  3. 3.Institute of Clinical ScienceUniversity of BergenBergenNorway
  4. 4.Section of Sustainable Health, Department of Public Health and Clinical MedicineUmeå UniversityUmeåSweden
  5. 5.Medical FacultyUniversity of IcelandReykjavíkIceland
  6. 6.Primary Health Care CenterGardabaerIceland
  7. 7.Department of SleepLandspitali University HospitalReykjavíkIceland
  8. 8.Section of Occupational and Environmental MedicineSahlgrenska University HospitalGothenburgSweden
  9. 9.Department of Medical Sciences: Respiratory, Allergy and Sleep ResearchUppsala UniversityUppsalaSweden
  10. 10.Department of Pulmonology (ARKS)University of TartuTartuEstonia
  11. 11.Department of Global Public Health and Primary Care, Centre for International HealthUniversity of BergenBergenNorway
  12. 12.Department of Occupational MedicineHaukeland University HospitalBergenNorway
  13. 13.Section of Occupational and Environmental Medicine, The Sahlgrenska AcademyUniversity of GothenburgGothenburgSweden
  14. 14.Department of Medical Sciences, Clinical PhysiologyUppsala UniversityUppsalaSweden
  15. 15.School of Public HealthThe University of QueenslandBrisbaneAustralia
  16. 16.Department of Internal MedicineAlbacete University HospitalAlbaceteSpain
  17. 17.National Research Centre for The Working EnvironmentCopenhagenDenmark

Personalised recommendations