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Prenatal and prepubertal exposures to tobacco smoke in men may cause lower lung function in future offspring: a three-generation study using a causal modelling approach

Simone Accordini, Lucia Calciano, Ane Johannessen, Bryndis Benediktsdóttir, Randi Jacobsen Bertelsen, Lennart Bråbäck, Shyamali C. Dharmage, Bertil Forsberg, Francisco Gómez Real, John W. Holloway, Mathias Holm, Christer Janson, Nils O. Jõgi, Rain Jõgi, Andrei Malinovschi, Alessandro Marcon, Jesús Martínez-Moratalla Rovira, José Luis Sánchez-Ramos, Vivi Schlünssen, Kjell Torén, Deborah Jarvis, Cecilie Svanes
European Respiratory Journal 2021; DOI: 10.1183/13993003.02791-2020
Simone Accordini
1Unit of Epidemiology and Medical Statistics, Department of Diagnostics and Public Health, University of Verona, Verona, Italy
19Equal contribution as first authors
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  • For correspondence: simone.accordini@univr.it
Lucia Calciano
1Unit of Epidemiology and Medical Statistics, Department of Diagnostics and Public Health, University of Verona, Verona, Italy
19Equal contribution as first authors
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Ane Johannessen
2Department of Global Public Health and Primary Care, Centre for International Health, University of Bergen, Bergen, Norway
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Bryndis Benediktsdóttir
3Faculty of Medicine, University of Iceland, Reykjavik, Iceland
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Randi Jacobsen Bertelsen
4Department of Clinical Science, University of Bergen, Bergen, Norway
5Oral Health Centre of Expertise in Western Norway/Vestland, Bergen, Norway
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  • ORCID record for Randi Jacobsen Bertelsen
Lennart Bråbäck
6Section of Sustainable Health, Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden
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Shyamali C. Dharmage
7Allergy and Lung Health Unit, School of Population and Global Health, University of Melbourne, Melbourne, Australia
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Bertil Forsberg
6Section of Sustainable Health, Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden
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  • ORCID record for Bertil Forsberg
Francisco Gómez Real
4Department of Clinical Science, University of Bergen, Bergen, Norway
8Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway
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John W. Holloway
9Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, United Kingdom
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Mathias Holm
10Occupational and Environmental Medicine, School of Public Health and Community Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
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Christer Janson
11Department of Medical Sciences: Respiratory, Allergy and Sleep Research, Uppsala University, Uppsala, Sweden
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Nils O. Jõgi
4Department of Clinical Science, University of Bergen, Bergen, Norway
12Lung Clinic, Tartu University Hospital, Tartu, Estonia
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Rain Jõgi
12Lung Clinic, Tartu University Hospital, Tartu, Estonia
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Andrei Malinovschi
13Department of Medical Sciences: Clinical Physiology, Uppsala University, Uppsala, Sweden
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Alessandro Marcon
1Unit of Epidemiology and Medical Statistics, Department of Diagnostics and Public Health, University of Verona, Verona, Italy
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Jesús Martínez-Moratalla Rovira
14Servicio de Neumología del Complejo Hospitalario Universitario de Albacete (CHUA), Servicio de Salud de Castilla-La Mancha (SESCAM), Albacete, Spain
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José Luis Sánchez-Ramos
15Department of Nursing, University of Huelva, Huelva, Spain
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Vivi Schlünssen
16Department of Public Health, Aarhus University, Aarhus, Denmark
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Kjell Torén
10Occupational and Environmental Medicine, School of Public Health and Community Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
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Deborah Jarvis
17Faculty of Medicine, National Heart & Lung Institute, Imperial College, London, United Kingdom
18MRC-PHE Centre for Environment and Health, Imperial College, London, United Kingdom
20Equal contribution as last authors
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Cecilie Svanes
2Department of Global Public Health and Primary Care, Centre for International Health, University of Bergen, Bergen, Norway
20Equal contribution as last authors
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Abstract

Mechanistic research suggests that lifestyle and environmental factors impact respiratory health across generations by epigenetic changes transmitted through male germ cells. Evidence from studies on humans is very limited.

We investigated multi-generation causal associations to estimate the causal effects of tobacco smoking on lung function within the paternal line. We analysed data from 383 adult offspring (age: 18–47; female: 52.0%) and their 274 fathers, who had participated in the ECRHS/RHINESSA generation study and had provided valid measures of pre-bronchodilator lung function. Two counterfactual-based, multi-level mediation models were developed with: paternal grandmothers’ smoking in pregnancy and fathers’ smoking initiation in prepuberty as exposures; fathers’ FEV1 and FVC, or FEV1/FVC z-scores as potential mediators (proxies of unobserved biological mechanisms that are true mediators); offspring's FEV1 and FVC, or FEV1/FVC z-scores as outcomes. All effects were summarised as differences in expected z-scores related to fathers’ and grandmothers’ smoking history.

Fathers’ smoking initiation in prepuberty had a negative direct effect on both offspring's FEV1 (−0.36; 95% confidence interval: −0.63, −0.10) and FVC (−0.50; −0.80, −0.20) compared to fathers’ never smoking. Paternal grandmothers’ smoking in pregnancy had a negative direct effect on fathers’ FEV1/FVC (−0.57; −1.09, −0.05) and a negative indirect effect on offspring's FEV1/FVC (−0.12; −0.21, −0.03) compared to grandmothers’ not smoking before fathers’ birth nor during fathers’ childhood.

Fathers’ smoking in prepuberty and paternal grandmothers’ smoking in pregnancy may cause lower lung function in offspring. Our results support the concept that lifestyle-related exposures during these susceptibility periods influence the health of future generations.

Footnotes

This manuscript has recently been accepted for publication in the European Respiratory Journal. It is published here in its accepted form prior to copyediting and typesetting by our production team. After these production processes are complete and the authors have approved the resulting proofs, the article will move to the latest issue of the ERJ online. Please open or download the PDF to view this article.

Conflict of interest: Prof. Accordini has nothing to disclose.

Conflict of interest: Dr. Calciano has nothing to disclose.

Conflict of interest: Dr. Johannessen has nothing to disclose.

Conflict of interest: Dr. Benediktsdóttir has nothing to disclose.

Conflict of interest: Dr. Bertelsen has nothing to disclose.

Conflict of interest: Dr. Bråbäck has nothing to disclose.

Conflict of interest: Dr. Dharmage has nothing to disclose.

Conflict of interest: Dr. Forsberg has nothing to disclose.

Conflict of interest: Dr. Gómez Real has nothing to disclose.

Conflict of interest: Dr. Holloway reports grants from European Union's Horizon 2020 research and innovation programme, grants from Research Council of Norway, during the conduct of the study.

Conflict of interest: Dr. Holm has nothing to disclose.

Conflict of interest: Dr. Janson has nothing to disclose.

Conflict of interest: Dr. Jõgi has nothing to disclose.

Conflict of interest: Dr. Rain Jõgi reports grants from Estonian Research Council Personal Research Grant no 562, during the conduct of the study; personal fees from Consultancy, grants from Grants/grants pending, personal fees from Payment for lectures, personal fees from Travel/acco

Conflict of interest: Dr. Malinovschi has nothing to disclose.

Conflict of interest: Dr. Marcon has nothing to disclose.

Conflict of interest: Dr. Martínez-Moratalla Rovira has nothing to disclose.

Conflict of interest: Dr. Sánchez-Ramos has nothing to disclose.

Conflict of interest: Dr. Schlünssen has nothing to disclose.

Conflict of interest: Dr. Torén has nothing to disclose.

Conflict of interest: Professor. Jarvis reports grants from EU, during the conduct of the study; .

Conflict of interest: Dr. Svanes has nothing to disclose.

This is a PDF-only article. Please click on the PDF link above to read it.

  • Received July 15, 2020.
  • Accepted March 11, 2021.
  • Copyright ©The authors 2021. For reproduction rights and permissions contact permissions{at}ersnet.org
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Prenatal and prepubertal exposures to tobacco smoke in men may cause lower lung function in future offspring: a three-generation study using a causal modelling approach
Simone Accordini, Lucia Calciano, Ane Johannessen, Bryndis Benediktsdóttir, Randi Jacobsen Bertelsen, Lennart Bråbäck, Shyamali C. Dharmage, Bertil Forsberg, Francisco Gómez Real, John W. Holloway, Mathias Holm, Christer Janson, Nils O. Jõgi, Rain Jõgi, Andrei Malinovschi, Alessandro Marcon, Jesús Martínez-Moratalla Rovira, José Luis Sánchez-Ramos, Vivi Schlünssen, Kjell Torén, Deborah Jarvis, Cecilie Svanes
European Respiratory Journal Jan 2021, 2002791; DOI: 10.1183/13993003.02791-2020

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Prenatal and prepubertal exposures to tobacco smoke in men may cause lower lung function in future offspring: a three-generation study using a causal modelling approach
Simone Accordini, Lucia Calciano, Ane Johannessen, Bryndis Benediktsdóttir, Randi Jacobsen Bertelsen, Lennart Bråbäck, Shyamali C. Dharmage, Bertil Forsberg, Francisco Gómez Real, John W. Holloway, Mathias Holm, Christer Janson, Nils O. Jõgi, Rain Jõgi, Andrei Malinovschi, Alessandro Marcon, Jesús Martínez-Moratalla Rovira, José Luis Sánchez-Ramos, Vivi Schlünssen, Kjell Torén, Deborah Jarvis, Cecilie Svanes
European Respiratory Journal Jan 2021, 2002791; DOI: 10.1183/13993003.02791-2020
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