A three-generation study on the association of tobacco smoking with asthma
Open accessAbstract
Background: Mothers' smoking during pregnancy increases asthma risk in their offspring. There is some evidence that grandmothers' smoking may have a similar effect, and biological plausibility that fathers' smoking during adolescence may influence offspring's health through transmittable epigenetic changes in sperm precursor cells. We evaluated the three-generation associations of tobacco smoking with asthma. Methods: Between 2010 and 2013, at the European Community Respiratory Health Survey III clinical interview, 2233 mothers and 1964 fathers from 26 centres reported whether their offspring (aged ≤51 years) had ever had asthma and whether it had coexisted with nasal allergies or not. Mothers and fathers also provided information on their parents' (grandparents) and their own asthma, education and smoking history. Multilevel mediation models within a multicentre three-generation framework were fitted separately within the maternal (4666 offspring) and paternal (4192 offspring) lines. Results: Fathers' smoking before they were 15 [relative risk ratio (RRR) = 1.43, 95% confidence interval (CI): 1.01-2.01] and mothers' smoking during pregnancy (RRR = 1.27, 95% CI: 1.01-1.59) were associated with asthma without nasal allergies in their offspring. Grandmothers' smoking during pregnancy was associated with asthma in their daughters [odds ratio (OR) = 1.55, 95% CI: 1.17-2.06] and with asthma with nasal allergies in their grandchildren within the maternal line (RRR = 1.25, 95% CI: 1.02-1.55). Conclusions: Fathers' smoking during early adolescence and grandmothers' and mothers' smoking during pregnancy may independently increase asthma risk in offspring. Thus, risk factors for asthma should be sought in both parents and before conception. Funding: European Union (Horizon 2020, GA-633212).
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Grandmaternal smoking while the mother is in utero independently increases the risk of subsequent offspring childhood asthma.
“Recent evidence from multi-generational studies suggest that grandmaternal smoking while the mother is in utero and paternal smoking during his adolescence can independently increase the risk of subsequent offspring childhood asthma.”
From Epidemiology of Asthma in Children and Adults (2019) · cites this paper as [128]
Tobacco smoking may cause heritable modifications of the epigenome, which increase the risk of asthma in future generations.
“These findings suggest that tobacco smoking may cause heritable modifications of the epigenome, which increase the risk of asthma in future generations (128).”
From Epidemiology of Asthma in Children and Adults (2019) · cites this paper as [128]
Paternal smoking during his adolescence independently increases the risk of subsequent offspring childhood asthma.
“Recent evidence from multi-generational studies suggest that grandmaternal smoking while the mother is in utero and paternal smoking during his adolescence can independently increase the risk of subsequent offspring childhood asthma.”
From Epidemiology of Asthma in Children and Adults (2019) · cites this paper as [128]
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Epidemiology of Asthma in Children and Adults
Dharmage, S. C., Perret, J. L., & Custovic, A. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00246 · Cited by 1,200 · see citing works
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- Authors
- Accordini, S., Calciano, L., Johannessen, A., Portas, L., Benediktsdóttir, B., Bertelsen, R. J., Bråbäck, L., Carsin, A.-E., Dharmage, S. C., Dratva, J., Forsberg, B., Gomez Real, F., Heinrich, J., Holloway, J. W., Holm, M., Janson, C., Jögi, R., Leynaert, B., Malinovschi, A., Marcon, A., Martínez-Moratalla Rovira, J., Raherison, C., Sánchez-Ramos, J. L., Schlünssen, V., Bono, R., Corsico, A. G., Demoly, P., Dorado Arenas, S., Nowak, D., Pin, I., Weyler, J., Jarvis, D., Svanes, C., & Study, T. A. L. I. E. C. (.
- Affiliations
- University of Verona (IT)
- University of Bergen (NO)
- Faculty of Medicine, University of Iceland, Reykjavik, Iceland
- Haukeland University Hospital (NO)
- Umeå University (SE)
- Universitat Pompeu Fabra (ES)
- The University of Melbourne (AU)
- Swiss Tropical and Public Health Institute (CH)
- Department of Clinical Science, University of Bergen, Bergen, Norway
- LMU Klinikum (DE)
- University of Southampton (GB)
- University of Gothenburg (SE)
- Uppsala University (SE)
- Tartu University Hospital (EE)
- Inserm (FR)
- Department of Medical Sciences: Clinical Physiology, Uppsala University, Uppsala, Sweden
- Pneumology Service of the University Hospital Complex of Albacete (CHUA), Health Service of Castilla-La Mancha (SESCAM), Albacete, Spain
- INSERM U1219, Bordeaux University, Bordeaux, France
- Department of Nursing, University of Huelva, Huelva, Spain
- Aarhus University (DK)
- University of Turin (IT)
- University of Pavia (IT)
- Pulmonology Department, Galdakao-Usansolo Hospital, Biscay, Spain
- University of Antwerp (BE)
- MRC Centre for Environment and Health (GB)
- Corresponding author
- Accordini, Simone
- ORCID
- Accordini, Simone
- Calciano, Lucia
- Johannessen, Ane
- Portas, Laura
- Bertelsen, Randi Jacobsen
- Bråbäck, Lennart
- Carsin, Anne-Elie
- Dharmage, Shyamali C
- Dratva, Julia
- Forsberg, Bertil
- Gomez Real, Francisco
- Heinrich, Joachim
- Holloway, John W
- Holm, Mathias
- Janson, Christer
- Jögi, Rain
- Leynaert, Bénédicte
- Marcon, Alessandro
- Schlünssen, Vivi
- Bono, Roberto
- Corsico, Angelo G
- Demoly, Pascal
- Nowak, Dennis
- Pin, Isabelle
- Weyler, Joost
- Jarvis, Deborah
- Svanes, Cecilie
- Venue
- International Journal of Epidemiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-03-09
- Volume
- 47
- Issue
- 4
- Pages
- 1106-1117
- ISSN
- 0300-5771 (ISSN-L)
- 1464-3685
- PMC
- PMC6124624
- OpenAlex
- W2786338585
- Cited by
- 125
- References
- 50
- Citations by year
- 2026: 8 · 2025: 15 · 2024: 12 · 2023: 10 · 2022: 17 · 2021: 21 · 2020: 18 · 2019: 19 · 2018: 5
- FWCI
- 10.83
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- International Journal of Epidemiology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (publishedVersion, cc-by-nc)
- edoc (University of Basel) (acceptedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- HAL (submittedVersion, other-oa)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by-nc)
- DiVA at Umeå University (Umeå University) (submittedVersion, other-oa)
- KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
- Repositorio Institucional de la Universidad de Huelva (Universidad de Huelva) (submittedVersion)
- Zürcher Hochschule für Angewandte Wissenschaften digital collection (Zurich University of Applied Sciences) (submittedVersion, cc-by-nc-nd)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by-nc)
- Hispana (submittedVersion, cc-by-nc-nd)
- Opin vísindi (Opin vísindi) (submittedVersion, cc-by-nc)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion, cc-by-nc)
- Repositorio Institucional de la Universidad de Huelva (Universidad de Huelva) (submittedVersion, cc-by-nc-nd)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, cc-by-nc)
- Spiral (Imperial College London) (submittedVersion, cc-by-nc)
- Funders
- Ageing Lungs in European Cohorts
- ALEC
- European Union's Horizon 2020 (633212)
- European Community Respiratory Health Survey
- ECRHS
- European Commission
- Medical Research Council
- Topics
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
- Keywords
- asthma, smoking, smoking during pregnancy, paternal smoking, adolescent smoking, transgenerational epigenetic inheritance, sperm epigenetics, nasal allergy, three-generation study, mediation analysis
- MeSH terms
- Grandparents, Tobacco Smoking, Adolescent, Adult, Aged, Asthma, Australia, Child, Child, Preschool, Europe, Female, Health Surveys, Humans, Infant, Infant, Newborn, Male, Middle Aged, Parents, Pregnancy, Prenatal Exposure Delayed Effects, Regression Analysis, Risk Factors, Multilevel Analysis, Young Adult
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