A three-generation study on the association of tobacco smoking with asthma

Simone Accordini, Lucia Calciano, Ane Johannessen, Laura Portas, Bryndis Benediktsdóttir, Randi Jacobsen Bertelsen, Lennart Bråbäck, Anne Elie Carsin, Shyamali C. Dharmage, Julia Dratva, Bertil Forsberg, Francisco Gomez Real, Joachim Heinrich, John WHolloway, Mathias Holm, Christer Janson, Rain Jögi, Bénédicte Leynaert, Andrei Malinovschi, Alessandro MarconJesús Martínez Moratalla Rovira, Chantal Raherison, José Luis Sánchez-Ramos, Vivi Schlünssen, Roberto Bono, Angelo G. Corsico, Pascal Demoly, Sandra Dorado Arenas, Dennis Nowak, Isabelle Pin, Joost Weyler, Deborah Jarvis, Cecilie Svanes

Research output: Contribution to journalArticle

Abstract

© The Author(s) 2018. 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.
Original languageEnglish
Pages (from-to)1106-1117
Number of pages12
JournalInternational Journal of Epidemiology
Volume47
Issue number4
DOIs
Publication statusPublished - Jan 1 2018

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Asthma
Smoking
Mothers
Fathers
Odds Ratio
Nose
Confidence Intervals
Pregnancy
Hypersensitivity
Parents
European Union
Health Surveys
Nuclear Family
Epigenomics
Spermatozoa
History
Interviews
Education
Grandparents
Health

Keywords

  • Ageing Lungs in European Cohorts (ALEC) Study
  • Asthma
  • Fathers' smoking during puberty
  • Grandmothers' smoking during pregnancy
  • Mothers' smoking during pregnancy
  • Multilevel mediation model

Cite this

Accordini, S., Calciano, L., Johannessen, A., Portas, L., Benediktsdóttir, B., Bertelsen, R. J., ... Svanes, C. (2018). A three-generation study on the association of tobacco smoking with asthma. International Journal of Epidemiology, 47(4), 1106-1117. https://doi.org/10.1093/ije/dyy031

A three-generation study on the association of tobacco smoking with asthma. / Accordini, Simone; Calciano, Lucia; Johannessen, Ane; Portas, Laura; Benediktsdóttir, Bryndis; Bertelsen, Randi Jacobsen; Bråbäck, Lennart; Carsin, Anne Elie; Dharmage, Shyamali C.; Dratva, Julia; Forsberg, Bertil; Real, Francisco Gomez; Heinrich, Joachim; WHolloway, John; Holm, Mathias; Janson, Christer; Jögi, Rain; Leynaert, Bénédicte; Malinovschi, Andrei; Marcon, Alessandro; Rovira, Jesús Martínez Moratalla; Raherison, Chantal; Luis Sánchez-Ramos, José; Schlünssen, Vivi; Bono, Roberto; Corsico, Angelo G.; Demoly, Pascal; Arenas, Sandra Dorado; Nowak, Dennis; Pin, Isabelle; Weyler, Joost; Jarvis, Deborah; Svanes, Cecilie.

In: International Journal of Epidemiology, Vol. 47, No. 4, 01.01.2018, p. 1106-1117.

Research output: Contribution to journalArticle

Accordini, S, Calciano, L, Johannessen, A, Portas, L, Benediktsdóttir, B, Bertelsen, RJ, Bråbäck, L, Carsin, AE, Dharmage, SC, Dratva, J, Forsberg, B, Real, FG, Heinrich, J, WHolloway, J, Holm, M, Janson, C, Jögi, R, Leynaert, B, Malinovschi, A, Marcon, A, Rovira, JMM, Raherison, C, Luis Sánchez-Ramos, J, Schlünssen, V, Bono, R, Corsico, AG, Demoly, P, Arenas, SD, Nowak, D, Pin, I, Weyler, J, Jarvis, D & Svanes, C 2018, 'A three-generation study on the association of tobacco smoking with asthma', International Journal of Epidemiology, vol. 47, no. 4, pp. 1106-1117. https://doi.org/10.1093/ije/dyy031
Accordini S, Calciano L, Johannessen A, Portas L, Benediktsdóttir B, Bertelsen RJ et al. A three-generation study on the association of tobacco smoking with asthma. International Journal of Epidemiology. 2018 Jan 1;47(4):1106-1117. https://doi.org/10.1093/ije/dyy031
Accordini, Simone ; Calciano, Lucia ; Johannessen, Ane ; Portas, Laura ; Benediktsdóttir, Bryndis ; Bertelsen, Randi Jacobsen ; Bråbäck, Lennart ; Carsin, Anne Elie ; Dharmage, Shyamali C. ; Dratva, Julia ; Forsberg, Bertil ; Real, Francisco Gomez ; Heinrich, Joachim ; WHolloway, John ; Holm, Mathias ; Janson, Christer ; Jögi, Rain ; Leynaert, Bénédicte ; Malinovschi, Andrei ; Marcon, Alessandro ; Rovira, Jesús Martínez Moratalla ; Raherison, Chantal ; Luis Sánchez-Ramos, José ; Schlünssen, Vivi ; Bono, Roberto ; Corsico, Angelo G. ; Demoly, Pascal ; Arenas, Sandra Dorado ; Nowak, Dennis ; Pin, Isabelle ; Weyler, Joost ; Jarvis, Deborah ; Svanes, Cecilie. / A three-generation study on the association of tobacco smoking with asthma. In: International Journal of Epidemiology. 2018 ; Vol. 47, No. 4. pp. 1106-1117.
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abstract = "{\circledC} The Author(s) 2018. 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.",
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AU - Accordini, Simone

AU - Calciano, Lucia

AU - Johannessen, Ane

AU - Portas, Laura

AU - Benediktsdóttir, Bryndis

AU - Bertelsen, Randi Jacobsen

AU - Bråbäck, Lennart

AU - Carsin, Anne Elie

AU - Dharmage, Shyamali C.

AU - Dratva, Julia

AU - Forsberg, Bertil

AU - Real, Francisco Gomez

AU - Heinrich, Joachim

AU - WHolloway, John

AU - Holm, Mathias

AU - Janson, Christer

AU - Jögi, Rain

AU - Leynaert, Bénédicte

AU - Malinovschi, Andrei

AU - Marcon, Alessandro

AU - Rovira, Jesús Martínez Moratalla

AU - Raherison, Chantal

AU - Luis Sánchez-Ramos, José

AU - Schlünssen, Vivi

AU - Bono, Roberto

AU - Corsico, Angelo G.

AU - Demoly, Pascal

AU - Arenas, Sandra Dorado

AU - Nowak, Dennis

AU - Pin, Isabelle

AU - Weyler, Joost

AU - Jarvis, Deborah

AU - Svanes, Cecilie

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N2 - © The Author(s) 2018. 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.

AB - © The Author(s) 2018. 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.

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