Skip to main content
Top
Published in: Reproductive Health 1/2021

Open Access 01-12-2021 | Attention Deficit Hyperactivity Disorder | Review

The impact of paternal alcohol, tobacco, caffeine use and physical activity on offspring mental health: a systematic review and meta-analysis

Authors: Kayleigh E. Easey, Gemma C. Sharp

Published in: Reproductive Health | Issue 1/2021

Login to get access

Abstract

Background

There is some evidence that paternal health behaviours during and around pregnancy could be associated with offspring health outcomes. However, the impact that paternal health behaviours during pregnancy can have on offspring mental health is understudied and remains unclear.

Methods

We conducted a systematic review and meta-analysis of articles in PubMed describing studies of potentially modifiable paternal health behaviours (tobacco smoking, alcohol consumption, caffeine consumption and physical activity) in the prenatal period in relation to offspring mental health. GRADE was used to measure risk of bias.

Results

Eight studies were included and categorized by paternal health behaviour and offspring mental health outcome investigated. The narrative synthesis provided evidence of association between paternal health behaviours around pregnancy and offspring mental health problems, with the strongest evidence shown for tobacco use. Grouped by analysis type, two separate meta-analyses showed evidence of paternal smoking during pregnancy being associated with greater odds of ADHD in offspring (OR 1.42, 95% CI 1.02–1.99; HR 1.28, 95% CI 1.19–1.39).

Conclusions

The small number of studies that have investigated paternal prenatal effects on offspring mental health, and the limited sample sizes of those studies, makes it challenging to draw firm conclusions. Although existing studies suggest that paternal tobacco smoking and alcohol consumption in the prenatal period are associated with poorer offspring mental health, (particularly hyperactivity/ADHD), further investigation of potential paternal effects is required, using methods that allow stronger inference to determine whether associations are causal.
Appendix
Available only for authorised users
Literature
1.
go back to reference Easey KE, Dyer ML, Timpson NJ, Munafò MR. Prenatal alcohol exposure and offspring mental health: a systematic review. Drug Alcohol Depend. 2019;197:344–53.CrossRef Easey KE, Dyer ML, Timpson NJ, Munafò MR. Prenatal alcohol exposure and offspring mental health: a systematic review. Drug Alcohol Depend. 2019;197:344–53.CrossRef
2.
go back to reference Easey KE, Wootton RE, Sallis HM, Haan E, Schellhas L, Munafò MR, et al. Characterization of alcohol polygenic risk scores in the context of mental health outcomes: within-individual and intergenerational analyses in the Avon Longitudinal Study of Parents and Children. Drug Alcohol Depend. 2021;221:108654.CrossRef Easey KE, Wootton RE, Sallis HM, Haan E, Schellhas L, Munafò MR, et al. Characterization of alcohol polygenic risk scores in the context of mental health outcomes: within-individual and intergenerational analyses in the Avon Longitudinal Study of Parents and Children. Drug Alcohol Depend. 2021;221:108654.CrossRef
4.
go back to reference Sharp GC, Lawlor DA, Richardson SS. It’s the mother!: How assumptions about the causal primacy of maternal effects influence research on the developmental origins of health and disease. Soc Sci Med. 2018;213:20–7.CrossRef Sharp GC, Lawlor DA, Richardson SS. It’s the mother!: How assumptions about the causal primacy of maternal effects influence research on the developmental origins of health and disease. Soc Sci Med. 2018;213:20–7.CrossRef
6.
go back to reference Braun JM, Messerlian C, Hauser R. Fathers matter: why it’s time to consider the impact of paternal environmental exposures on children’s health. Curr Epidemiol Rep. 2017;4(1):46–55.CrossRef Braun JM, Messerlian C, Hauser R. Fathers matter: why it’s time to consider the impact of paternal environmental exposures on children’s health. Curr Epidemiol Rep. 2017;4(1):46–55.CrossRef
7.
go back to reference Sharp GC, Lawlor DA. Paternal impact on the life course development of obesity and type 2 diabetes in the offspring. Diabetologia. 2019;62(10):1802–10.CrossRef Sharp GC, Lawlor DA. Paternal impact on the life course development of obesity and type 2 diabetes in the offspring. Diabetologia. 2019;62(10):1802–10.CrossRef
8.
go back to reference Donkin I, Barrès R. Sperm epigenetics and influence of environmental factors. Mol Metab. 2018;14:1–11.CrossRef Donkin I, Barrès R. Sperm epigenetics and influence of environmental factors. Mol Metab. 2018;14:1–11.CrossRef
9.
go back to reference Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M. Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab. 2012;302(7):E768–80.CrossRef Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M. Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab. 2012;302(7):E768–80.CrossRef
11.
go back to reference Stevenson JG, Oliver JA, Hallyburton MB, Sweitzer MM, Conklin CA, McClernon FJ. Smoking environment cues reduce ability to resist smoking as measured by a delay to smoking task. Addict Behav. 2017;67:49–52.CrossRef Stevenson JG, Oliver JA, Hallyburton MB, Sweitzer MM, Conklin CA, McClernon FJ. Smoking environment cues reduce ability to resist smoking as measured by a delay to smoking task. Addict Behav. 2017;67:49–52.CrossRef
12.
go back to reference Scheffers-van Schayck T, Tuithof M, Otten R, Engels R, Kleinjan M. Smoking behavior of women before, during, and after pregnancy: indicators of smoking, quitting, and relapse. Eur Addict Res. 2019;25(3):132–44.CrossRef Scheffers-van Schayck T, Tuithof M, Otten R, Engels R, Kleinjan M. Smoking behavior of women before, during, and after pregnancy: indicators of smoking, quitting, and relapse. Eur Addict Res. 2019;25(3):132–44.CrossRef
13.
go back to reference Dejin-Karlsson E, Hanson BS, Ostergren PO, Ranstam J, Isacsson SO, Sjöberg NO. Psychosocial resources and persistent smoking in early pregnancy—a population study of women in their first pregnancy in Sweden. J Epidemiol Community Health. 1996;50(1):33–9.CrossRef Dejin-Karlsson E, Hanson BS, Ostergren PO, Ranstam J, Isacsson SO, Sjöberg NO. Psychosocial resources and persistent smoking in early pregnancy—a population study of women in their first pregnancy in Sweden. J Epidemiol Community Health. 1996;50(1):33–9.CrossRef
14.
go back to reference Gage SH, Munafò MR, Davey SG. Causal inference in developmental origins of health and disease (DOHaD) research. Annu Rev Psychol. 2016;67:567–85.CrossRef Gage SH, Munafò MR, Davey SG. Causal inference in developmental origins of health and disease (DOHaD) research. Annu Rev Psychol. 2016;67:567–85.CrossRef
15.
go back to reference Easey KE, Timpson NJ, Munafò MR. Association of prenatal alcohol exposure and offspring depression: a negative control analysis of maternal and partner consumption. Alcohol Clin Exp Res. 2020;44(5):1132–40.CrossRef Easey KE, Timpson NJ, Munafò MR. Association of prenatal alcohol exposure and offspring depression: a negative control analysis of maternal and partner consumption. Alcohol Clin Exp Res. 2020;44(5):1132–40.CrossRef
16.
go back to reference Taylor AE, Carslake D, de Mola CL, Rydell M, Nilsen TIL, Bjørngaard JH, et al. Maternal smoking in pregnancy and offspring depression: a cross cohort and negative control study. Sci Rep. 2017;7(1):12579.CrossRef Taylor AE, Carslake D, de Mola CL, Rydell M, Nilsen TIL, Bjørngaard JH, et al. Maternal smoking in pregnancy and offspring depression: a cross cohort and negative control study. Sci Rep. 2017;7(1):12579.CrossRef
18.
go back to reference Oldereid NB, Wennerholm UB, Pinborg A, Loft A, Laivuori H, Petzold M, et al. The effect of paternal factors on perinatal and paediatric outcomes: a systematic review and meta-analysis. Hum Reprod Update. 2018;24(3):320–89.CrossRef Oldereid NB, Wennerholm UB, Pinborg A, Loft A, Laivuori H, Petzold M, et al. The effect of paternal factors on perinatal and paediatric outcomes: a systematic review and meta-analysis. Hum Reprod Update. 2018;24(3):320–89.CrossRef
19.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9.CrossRef Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9.CrossRef
20.
go back to reference Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, Brozek J, et al. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol. 2011;64(4):383–94.CrossRef Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, Brozek J, et al. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol. 2011;64(4):383–94.CrossRef
22.
go back to reference Langley K, Heron J, Smith GD, Thapar A. Maternal and paternal smoking during pregnancy and risk of ADHD symptoms in offspring: testing for intrauterine effects. Am J Epidemiol. 2012;176(3):261–8.CrossRef Langley K, Heron J, Smith GD, Thapar A. Maternal and paternal smoking during pregnancy and risk of ADHD symptoms in offspring: testing for intrauterine effects. Am J Epidemiol. 2012;176(3):261–8.CrossRef
23.
go back to reference Zhu JL, Olsen J, Liew Z, Li J, Niclasen J, Obel C. Parental smoking during pregnancy and ADHD in children: the Danish national birth cohort. Pediatrics. 2014;134(2):e382–8.CrossRef Zhu JL, Olsen J, Liew Z, Li J, Niclasen J, Obel C. Parental smoking during pregnancy and ADHD in children: the Danish national birth cohort. Pediatrics. 2014;134(2):e382–8.CrossRef
24.
go back to reference Altink ME, Slaats-Willemse DI, Rommelse NN, Buschgens CJ, Fliers EA, Arias-Vásquez A, et al. Effects of maternal and paternal smoking on attentional control in children with and without ADHD. Eur Child Adolesc Psychiatry. 2009;18(8):465–75.CrossRef Altink ME, Slaats-Willemse DI, Rommelse NN, Buschgens CJ, Fliers EA, Arias-Vásquez A, et al. Effects of maternal and paternal smoking on attentional control in children with and without ADHD. Eur Child Adolesc Psychiatry. 2009;18(8):465–75.CrossRef
25.
go back to reference Nomura Y, Marks DJ, Halperin JM. Prenatal exposure to maternal and paternal smoking on attention deficit hyperactivity disorders symptoms and diagnosis in offspring. J Nerv Ment Dis. 2010;198(9):672–8.CrossRef Nomura Y, Marks DJ, Halperin JM. Prenatal exposure to maternal and paternal smoking on attention deficit hyperactivity disorders symptoms and diagnosis in offspring. J Nerv Ment Dis. 2010;198(9):672–8.CrossRef
26.
go back to reference Tiesler CM, Chen CM, Sausenthaler S, Herbarth O, Lehmann I, Schaaf B, et al. Passive smoking and behavioural problems in children: results from the LISAplus prospective birth cohort study. Environ Res. 2011;111(8):1173–9.CrossRef Tiesler CM, Chen CM, Sausenthaler S, Herbarth O, Lehmann I, Schaaf B, et al. Passive smoking and behavioural problems in children: results from the LISAplus prospective birth cohort study. Environ Res. 2011;111(8):1173–9.CrossRef
27.
go back to reference Biederman J, Fitzgerald M, Spencer TJ, Bhide PG, McCarthy DM, Woodworth KY, et al. Is Paternal smoking at conception a risk for ADHD? A controlled study in youth with and without ADHD. J Atten Disord. 2020;24(11):1493–6.CrossRef Biederman J, Fitzgerald M, Spencer TJ, Bhide PG, McCarthy DM, Woodworth KY, et al. Is Paternal smoking at conception a risk for ADHD? A controlled study in youth with and without ADHD. J Atten Disord. 2020;24(11):1493–6.CrossRef
28.
go back to reference Abel EL. Paternal alcohol exposure and hyperactivity in rat offspring: effects of amphetamine. Neurotoxicol Teratol. 1993;15(6):445–9.CrossRef Abel EL. Paternal alcohol exposure and hyperactivity in rat offspring: effects of amphetamine. Neurotoxicol Teratol. 1993;15(6):445–9.CrossRef
29.
go back to reference Short AK, Yeshurun S, Powell R, Perreau VM, Fox A, Kim JH, et al. Exercise alters mouse sperm small noncoding RNAs and induces a transgenerational modification of male offspring conditioned fear and anxiety. Transl Psychiatry. 2017;7(5):e1114.CrossRef Short AK, Yeshurun S, Powell R, Perreau VM, Fox A, Kim JH, et al. Exercise alters mouse sperm small noncoding RNAs and induces a transgenerational modification of male offspring conditioned fear and anxiety. Transl Psychiatry. 2017;7(5):e1114.CrossRef
31.
go back to reference Sharma A, Madaan V, Petty FD. Exercise for mental health. Prim Care Companion J Clin Psychiatry. 2006;8(2):106.CrossRef Sharma A, Madaan V, Petty FD. Exercise for mental health. Prim Care Companion J Clin Psychiatry. 2006;8(2):106.CrossRef
32.
go back to reference Chekroud SR, Gueorguieva R, Zheutlin AB, Paulus M, Krumholz HM, Krystal JH, et al. Association between physical exercise and mental health in 1·2 million individuals in the USA between 2011 and 2015: a cross-sectional study. Lancet Psychiatry. 2018;5(9):739–46.CrossRef Chekroud SR, Gueorguieva R, Zheutlin AB, Paulus M, Krumholz HM, Krystal JH, et al. Association between physical exercise and mental health in 1·2 million individuals in the USA between 2011 and 2015: a cross-sectional study. Lancet Psychiatry. 2018;5(9):739–46.CrossRef
33.
go back to reference Davey SG. Negative control exposures in epidemiologic studies. Epidemiology. 2012;23(2):350–1.CrossRef Davey SG. Negative control exposures in epidemiologic studies. Epidemiology. 2012;23(2):350–1.CrossRef
34.
go back to reference Lipsitch M, Tchetgen Tchetgen E, Cohen T. Negative controls: a tool for detecting confounding and bias in observational studies. Epidemiology. 2010;21(3):383–8.CrossRef Lipsitch M, Tchetgen Tchetgen E, Cohen T. Negative controls: a tool for detecting confounding and bias in observational studies. Epidemiology. 2010;21(3):383–8.CrossRef
35.
go back to reference van Enst WA, Scholten RJ, Whiting P, Zwinderman AH, Hooft L. Meta-epidemiologic analysis indicates that MEDLINE searches are sufficient for diagnostic test accuracy systematic reviews. J Clin Epidemiol. 2014;67(11):1192–9.CrossRef van Enst WA, Scholten RJ, Whiting P, Zwinderman AH, Hooft L. Meta-epidemiologic analysis indicates that MEDLINE searches are sufficient for diagnostic test accuracy systematic reviews. J Clin Epidemiol. 2014;67(11):1192–9.CrossRef
36.
go back to reference Rice DB, Kloda LA, Levis B, Qi B, Kingsland E, Thombs BD. Are MEDLINE searches sufficient for systematic reviews and meta-analyses of the diagnostic accuracy of depression screening tools? A review of meta-analyses. J Psychosom Res. 2016;87:7–13.CrossRef Rice DB, Kloda LA, Levis B, Qi B, Kingsland E, Thombs BD. Are MEDLINE searches sufficient for systematic reviews and meta-analyses of the diagnostic accuracy of depression screening tools? A review of meta-analyses. J Psychosom Res. 2016;87:7–13.CrossRef
37.
go back to reference Ross-White A, Godfrey C. Is there an optimum number needed to retrieve to justify inclusion of a database in a systematic review search? Health Info Libr J. 2017;34(3):217–24.CrossRef Ross-White A, Godfrey C. Is there an optimum number needed to retrieve to justify inclusion of a database in a systematic review search? Health Info Libr J. 2017;34(3):217–24.CrossRef
Metadata
Title
The impact of paternal alcohol, tobacco, caffeine use and physical activity on offspring mental health: a systematic review and meta-analysis
Authors
Kayleigh E. Easey
Gemma C. Sharp
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Reproductive Health / Issue 1/2021
Electronic ISSN: 1742-4755
DOI
https://doi.org/10.1186/s12978-021-01266-w

Other articles of this Issue 1/2021

Reproductive Health 1/2021 Go to the issue