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How much and why does the mum matter? Mechanisms explaining the intergenerational transmission of smoking
Advances in Life Course Research 40 (2019) 99–107
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How much and why does the mum matter? Mechanisms explaining the intergenerational transmission of smoking
T
M. Pasqualinia, , L. Pieronib, C. Tomassinic ⁎
a
Department of Statistical Science, University of Rome La Sapienza, Italy Department of Political Science, University of Perugia, Italy c Department of Economics, University of Molise, Italy b
ARTICLE INFO
ABSTRACT
Keywords: Childhood Adolescence Smoking Intergenerational transmission Antisocial behaviours Path analysis
Offspring whose mother smokes during pregnancy have higher risk of smoking themselves. In this study, epigenetics, antisocial behaviours, and social learning were investigated as potential mechanisms of mother-to-child transmission of smoking among a population sample drawn from the Birth Cohort Study 1970. Findings on daughters showed that the direct epigenetic hypothesis was mediated by social learning mechanisms, suggesting that exposure to maternal smoking across childhood and adolescence strongly explained why the smoking habits of mother and daughter correlate. However, prenatal smoking effects on sons were only partially explained by observational learning of mother smoking habits. Our estimates provided evidence concerning the potential role also played by the child's persistent antisocial behaviours. These results were confirmed after controlling for early life circumstances and current socioeconomic conditions. Policy implications of the results are discussed.
1. Introduction In the last decade, robust empirical findings on the intergenerational transmission of smoking have been reported. However, the literature has not reached a consensus on the nature and strength of this relationship. Different hypotheses have been formulated to explain the association between smoking during pregnancy and a child's subsequent smoking habit, distinguishing between direct and indirect routes. Previous studies have explored this relationship, assessing the earlier smoking initiation of the child, current smoking status, and its persistence over time (Al Mamun et al., 2006; Buka, Shenassa, & Niaura, 2003; Griesler, Kandel, & Davies, 1998; Oncken, McKee, Krishnan-Sarin, O’Malley, & Mazure, 2004). Some of these studies were supportive of the direct epigenetic explanation setting that the foetus inherits susceptibility to addiction since the nicotine is transmitted by the placenta and this predisposes the child to smoke (Kandel & Udry, 1999; Kandel, Wu, & Davies, 1994). Another way through which physiological mechanisms act is mediated by antisocial behaviours (Benowitz, 2001; Miles & Weden, 2012; Wakschlag et al., 2003; Wakschlag, Pickett, Cook, Benowitz, & Leventhal, 2002). According to this hypothesis, exposure to tobacco in utero neurologically affects the foetus in terms of behavioural problems (Wakschlag et al., 2002) that, in turn, sets in motion trajectories making the initiation and progression of smoking more likely (Miles & Weden, ⁎
2012). Finally, since mothers who smoke during pregnancy are very likely to continue smoking after birth (Miles & Weden, 2012), the direct effect may also be mediated by exposure to postnatal smoking. Exposure to parental smoking during childhood and adolescence has been proven to predict child adult smoking acting through a social learning process that reflects role modelling and operates through a supportive influence on pro-smoking norms and attitudes. This paper aims to identify the existence of a specific channel of smoking transmission by simultaneously testing direct and indirect mechanisms. Specifically, we assess whether smoking during pregnancy predicts offspring smoking habits at age 34 acting through a direct epigenetic route, a physiological effect on the child's behaviours, or a mechanism of socialisation. The choice of focusing on adult smoking habit, despite adolescent initiation, must be considered as a robustness of the tested hypothesis, since smoking initiation may be strongly affected by peers. In addition, taking advantage of the longitudinal design of our data, we accounted for the persistence of behaviours across the life course. Analyses were conducted separately by gender, testing potential differences between offspring's sex. To estimate the mother-tochild transmission of smoking, we propose an approach based on the structural equation model (SEM), drawing on data from the 1970 British Cohort Study (BCS70). Consistent with prior research, we hypothesise that smoking behaviour is transmitted from mother to child with some differences according to gender and provide empirical
Corresponding author at: Department of Statistical Science, University of Rome La Sapienza, Viale Regina Elena 295, Palazzina G, Roma, Italy. E-mail address: [email protected] (M. Pasqualini).
https://doi.org/10.1016/j.alcr.2019.03.004 Received 21 September 2017; Received in revised form 4 November 2018; Accepted 4 March 2019 Available online 08 March 2019 1040-2608/ © 2019 Elsevier Ltd. All rights reserved.
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findings to shed light on the mediating roles of both antisocial behaviours and social learning mechanisms. As a contribution to the growing literature on intergenerational transmissions, our empirical approach differs from most previous studies (Gilman et al., 2009; Melchior, Chastang, Mackinnon, Galera, & Fombonne, 2010; Otten, Engels, van de Ven, & Bricker, 2007; Wakschlag et al., 2002; Wickrama, Conger, Wallace, & Elder, 1999; Chassin, Presson, Rose, & Sherman, 1998; Griesler et al., 1998) because it considers adolescence as a mediation step instead of the time of transmission outcome.
functioning. In addition, the interaction between nicotine and hormones may explain apparent sexual differences in effects (Lichtensteiger & Schlumpf, 1993; Kandel & Udry, 1999). According to Fried et al. (1998), effects on neurological development due to exposure to cigarette smoke during pregnancy lead to antisocial manifestations early in life that, in turn, are associated with a higher probability of starting and continuing to smoke (Miles & Weden, 2012). Specifically, antisocial behaviour is defined as a heterogeneous concept encompassing physically aggressive behaviours (for example, bullying or fighting), rule breaking and oppositional behaviours (for example, destroying belongings and disobeying parents), and more severe problems associated with lack of empathy and guilt (Bonino, Cattelino, Ciairano, & Jessor, 2007; Donovan, Jessor, & Costa, 1991; Jessor & Jessor, 1977). According to Moffitt (1993), the age of onset may be considered one of the best-established methods to characterise the heterogeneity within antisocial behaviours and, therefore, to differentiate between the life course persistent (LCP) and adolescence limited (AL) antisocial subgroups. According to this definition, while adolescents often tend to behave antisocially, they do so only temporarily, but most children who develop early behavioural problems have a long history of antisocial conduct (as shown in Fig. 1).
2. Background Tobacco smoking shows a significant heritability (Chassin et al., 2005; Li, 2003; Melchior et al., 2010) because family members tend to resemble each other in terms of health behaviours, as explained by Schor and Menaghan (1995) for whom similarities reflect familial and genetic predisposition, shared physical, social, and emotional environments, and acquired health beliefs and values. Previous research investigating the relationship between mothers smoking during pregnancy and child smoking outcomes adopted different theoretical perspectives. This paper suggests three analytical mechanisms (epigenetic, antisocial behaviours, and social learning), that may contribute to identify both direct and indirect smoking outcomes.
2.3. The social-learning mechanism There is evidence that these physiological associations may be completely confounded by social and environmental factors, especially when there is no clear distinction between smoking during pregnancy and postnatal smoking habit (Brion et al., 2010; Knopik, 2009; Maughan, Taylor, Caspi, & Moffitt, 2004; Roza et al., 2009) that are strongly related. Indeed, mothers who smoke during pregnancy are very likely to continue after birth (Miles & Weden, 2012); thus, postnatal smoking may be another potential mediator of this relationship. Social learning theory (Bandura & Walters, 1977) demonstrated that behaviours can be assimilated through direct modelling by others and parental influence increases over time due to long-term attention and the retention processes of the child. According to this hypothesis, children learn by observing and modelling their parents’ behaviour. Previous studies showed that cigarette consumption among adults and adolescents correlated modestly but significantly with each other (Bricker et al., 2006; Chassin et al., 2005; Li, 2003; Wickrama et al., 1999). Some studies in the literature confirmed that maternal and paternal smoking equally influenced offspring tobacco use (Bailey, Ennett, & Ringwalt, 1993; Chassin, Presson, Rose, & Sherman, 1998; Darling & Cumsille, 2003; Hu, Davies, & Kandel, 2006; Peterson et al., 2006), whereas others showed that mothers who smoked had a stronger effect than fathers on adolescent smoking (Brenner & Scharrer, 1996; Herlitz & Westholm, 1996), although the opposite has also been reported (Shamsuddin & Haris, 2000).
2.1. The epigenetic mechanism One mechanism underlying the effect of prenatal smoking on offspring might be the impact of nicotine products on the developing brain of the foetus. Nicotine may encourage the action of the cholinergic neurons, increment nicotinic receptors in the brain, and enhance activity in the neural systems involved in addictive behaviour (Kandel & Udry, 1999; Lambers & Clark, 1996). According to this theory, nicotine, which enters through the placenta, may alter the nervous system and change its threshold (Kandel & Udry, 1999). Thus, during a critical prenatal period of brain development, exposure to maternal smoke may have direct effects on the foetus, predisposing the child to smoke and persist in smoking later in life (Kandel et al., 1994). This explanation is consistent with the hypothesis that addictive drugs can modify gene expression and therefore induce structural changes in the dopaminergic systems (Kandel et al., 1994). Relevant sex differences in the direct physiological effect of prenatal smoking on offspring have been explained by invoking the distinctive sexual hormonal dimorphism of the brain that emerges during foetal development (Kelly, 1991; Tallal & McEwen, 1991; Kandel et al., 1994). This hypothesis has been enforced by genetic studies that found how smoking is influenced by genetic factors such as testosterone. Indeed, in female foetuses, in contrast to male foetuses, testosterone levels are determined by the maternal genetic factors, which affect the central nervous system of women in utero and thus increase their daughters’ likelihood of smoking.
3. Empirical strategy Although there is strong evidence that both pre- and postnatal maternal smoking increases the risk of offspring smoking, some unresolved issues remain regarding the nature and strength of this association. Therefore, a more careful specification of the transmission paths is necessary that might to produce a clearer understanding of why and how much to what extent smoking mothers matter. Thus far, the literature has mainly distinguished between epigenetic, antisocial behaviours, and social learning oriented studies. However, there is a lack of comprehensive studies identifying the real contribution of each route of transmission. Thus, this paper aims to extend prior empirical evidence by simultaneously testing direct and indirect routes of mother-to-child transmission of smoking. Moreover, this research frames observations into a life course perspective controlling for the persistence of behaviours across life stages. Empirically, the pathways approach is used to distinguish different trajectories and
2.2. The antisocial behaviour mechanism Empirical findings have tested the effect of maternal smoking during pregnancy on children's psychological problems, including antisocial (Brion et al., 2010; Fried, Watkinson, & Gray, 1998; Miles & Weden, 2012; Wakschlag et al., 2002; Zoloto, Nagoshi, Presson, & Chassin, 2012) and problematic behaviours (Wakschlag et al., 2003). Previous evidence indicates that prenatal exposure to nicotine is associated with foetal neurotoxicity (Benowitz, 2001; Wakschlag et al., 2002) that might occur via hypoxic effects on the foetal-placental unit and via teratological effects on the foetal nervous system (Lichtensteiger & Schlumpf, 1993; Wakschlag et al., 2002). The nicotine effect is mainly due to its stimulation of nicotinic receptors in the brain that interact with genes, causing permanent alterations in cell 100
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Fig. 1. Hypothetical illustration of life course change in antisocial involvement. The figure is from Moffitt (1993).
Smoking during pregnancy is measured by asking whether the mother of the respondent smoked any kind of tobacco when she was pregnant (yes = 1, no = 0). Postnatal maternal smoking takes into account whether the mother smoked when the child was 5 and 16 years old (yes/no). Young antisocial behaviours are measured considering the same set of variables reported by the mother for both childhood and adolescence (at 5 and 16 years old). Since antisocial behaviours consist of a wide range of factors, we simplify this heterogeneous category by selecting five variables that, even if not exhaustive of antisocial behaviours, are the most used in the literature. According to Bonino et al. (2007), the antisocial mode should comprise physical or verbal aggression against peers, theft or vandalism, and telling lies. Hence, the variables were selected according to whether the child/adolescent fights with other peers, whether she/he sometimes destroys belongings, and whether she/he is often disobedient. Finally, the main outcome is an observed variable that was constructed based on smoking status at age 34. In this way, we are able to test the mother-to-child transmission of smoking, assessing the life course patterns of behaviours. A set of covariates were taken into account. Smoking at age 34 was also controlled for social class based on the Registrar General's classification (manual versus non-manual), education level (lower versus higher), marital status (single, widowed, or divorced versus married), and the father's smoking habits when the child was 5 and 16 years old. Antisocial behaviours at age 5 were controlled for a set variables related to the child's early life conditions. We measured the changes in the family structure (specifically, whether the family experienced divorce or a parent's death during the child's infancy), the single use of the bathroom for the family as a measure of home facilities and, finally, whether or not the father was employed in a manual job. In the empirical analyses, we used the structural equation model (SEM), which allows both latent and observed indicators to be considered within a single framework, since the observed variables are involved as indicators of the latent constructs (Kline, 2015). Moreover, the support of graphical representations (for example, the path analysis) makes it easier to identify the causal relationship among the latent constructs and their specifications by the observed variables 1 .
emphasise the differences between the direct and indirect effects of each life stage. Fig. 2 outlines the graphical model, which supports the following hypotheses: A. Maternal smoking during pregnancy may directly affect a child's probability of smoking at age 34 (epigenetic mechanism). B. Maternal smoking during pregnancy may indirectly affect a child's smoking habit at age 34 via the child's persistent problematic behaviours (antisocial behaviours mechanism). C. Maternal smoking during pregnancy indirectly affects a child's smoking habit at age 34 via subsequent maternal smoking behaviour (social learning mechanism). The model controls for a child's social class, level of education, marital status, and the father's smoking habit, while antisocial behaviours are controlled for some variables related to the household socioeconomic condition during the offspring's childhood, such as the single use of the bathroom, the father's employment skill, and any disruptive change in the family structure (divorce and/or parental deaths). 4. Data and method This paper used the 1970 British Cohort Study (BCS70) to estimate the intergenerational transmission of smoking habit. This database is an ongoing national longitudinal study that involves more than 17,000 individuals born in Great Britain in a given week in April 1970 (including stillbirths). This survey was conducted at regular intervals (the last wave was in 2012), providing more than 15,000 multidisciplinary variables. According to the Response and Deaths datasets, the level of attrition for mortality, migration, and missing answers varied across waves by 5–20%. However, the longitudinal nature of this research design avoids selection biases that may affect the analyses. This paper used the 1970, 1975, 1986, and 2004 waves. The sample was comprised of 6138 members (53% women) of the longitudinal target who participated in all of the selected waves. The birth cohort data contain detailed information at a micro level on the health, health-related behaviours, education, and social development of all cohort members as they passed through childhood and adolescence until they progressed into adult life. These data provide a picture of the entire generation and offer a unique opportunity to understand the origins of socioeconomic, health, and behavioural disparities from childhood to adulthood.
1
Model diagrams are represented in this article using symbols from the McArdle–McDonald reticular action model (RAM): observed variables are represented by rectangles, latent variables by circles or ellipses, and hypothesised directional direct effects of one variable to another by a line with a single arrowhead. 101
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Fig. 2. Theoretical model. Note: Latent variables are represented by ellipses and observed variables are represented by rectangles.
Estimates were carried out using the STATA 14 GSEM command. In this setting, the hypotheses were tested through the maximum likelihood estimation based on a two-step modelling approach: the multiple indicators measurement model and the structural analysis. Thus, path models can provide considerable insight into complex causal mechanisms by investigating the mediating role of young peoples’ antisocial behaviours. Specifically, it is possible to decompose the total effect of cigarette smoking transmission into direct and indirect components (Pickles & De Stavola, 2007) and test whether the introduction of antisocial latent constructs changes the effect of causality between the dependent (e.g. adult smoking behaviours) and the independent variables (e.g. smoking during pregnancy).2 In addition, gender differences in parameters were explicitly tested with the Wald chi-squared test of interaction. Tables 1 and 2 show the frequency distributions and missing values (in percentage) for each binary variable by gender.
associated items. Moreover, measurement errors associated with each observed indicator are hypothesised to be uncorrelated with each other and the latent variable. Because STATA GSEM does not provide goodness-of-fit statistics, the size of the estimated coefficients was used to determine the adequacy of the measurement model (see also Silverstein & Bengtson, 2018). 5.1. The intergenerational transmission of smoking in daughters Generalised structural equation modelling (GSEM) is an extension of SEM that allows the analysis of categorical data utilising a logistic link function that does not rely on linear assumptions to model relationships with dichotomous data. The odds ratios (O.R.), confidence intervals (C.I.), and p-values (p-v) are estimated and are listed in the figures. Fig. 3 lists the adjusted odds ratios for daughters. The findings indicate that smoking during pregnancy, early antisocial behaviours, postnatal maternal smoking, and offspring smoking habit at age 34 were significantly associated. However, some considerations occurred. Mothers who smoked during pregnancy were approximately two times more likely to continue smoking when their daughter was age 5 (O.R. = 2.01; C.I. = 1.96–2.05). Concomitantly, smoking during pregnancy significantly increased the daughters’ probability of engaging in antisocial behaviours at age 5 (O.R. = 1.05; C.I. = 1.03–1.07). However, the direct relationship between smoking during pregnancy and daughters’ smoking at age 34 was not statistically significant (O.R. = 0.99; C.I. = 0.94–1.05). Consistent with social learning theory, the exposure to maternal smoking when the daughter was adolescent significantly predicted her probability of smoking at age 34 of approximately 8% (O.R. = 1.08; C.I. = 1.02–1.15). However, daughters who were antisocial at age 16 were not significantly more likely to smoke in adulthood, even if the effect was high in magnitude (O.R. = 1.27; C.I. = 0.78–2.07). Finally, the persistence of behaviours was confirmed by estimates. Indeed, maternal smoking habit when the daughter was age 5 strongly increased maternal smoking 11 years later by approximately 94% (O.R. = 1.94; C.I. = 1.88–2.00) and, consistent with Moffitt's theory (1993), similar effects have been found for child antisocial behaviours between age 5 and 16 (O.R. = 01.21; C.I. = 1.15–1.27). The findings from the mediation analysis are shown in Table 4 and report the direct,
5. Results The factor loadings, as shown in Table 3, indicate the measure of correlation between the observed items (disobeying parents, fighting peers, and destroying belongings) and the latent construct (antisocial behaviours). Standardised loadings show satisfying measurement properties varying from 0.45 to 0.75, which is a good range compared to conventions of the loadings of 0.40 or greater. The positive loading signs indicate the direction of the effect of the constructs on the 2 According to Preacher and Leonardelli (2009), a variable may be considered a mediator when it carries the influence of a given independent variable to a given dependent variable. From the contributions of some authors (Baron & Kenny, 1986; James & Brett, 1984; Judd & Kenny, 1981), four criteria that must be followed to investigate whether mediation occurs: (1) the independent variable significantly affects the mediator, (2) the independent variable significantly affects the dependent variable in the absence of the mediator, (3) the mediator has a significant effect on the dependent variable, and (4) the effect of the independent variable on the dependent variable significantly decreases upon the addition of the mediator. Because all of the observed indicators are binary, the latent variables are linked to observed variables by probit regression models; this framework is also used to link the outcome of the latent and observed variables (Golini & Egidi, 2002).
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Table 1 Descriptive statistics in percentage for daughters. Variables
Total sample
1 = Yes
0 = No
Missing values
Smoking during pregnancy Father smoked when child was 5 years old Father smoked when child was 16 years old Mother smoked when child was 5 years old Mother smoked when child was 16 years old No single use of bathroom Change in family structure (divorce or a parent's death) Father is in the manual labour social class Fighting peers at age 5 Destroying belongings at age 5 Disobeying parents at age 5 Fighting peers at age 16 Destroying belongings at age 16 Disobeying parents at age 16 Smoking at age 34 Social class at age 34 (manual = 1) Education at age 34 (lowest = 1) Marital status age 34 (single, widowed, or separated = 1)
3258 3084 1980 3156 1976 3229 3253 2750 3240 3243 3238 2631 2644 2638 3260 2465 3258 3261
0.43 0.52 0.29 0.38 0.22 0.03 0.10 0.59 0.25 0.14 0.64 0.08 0.01 0.19 0.28 0.16 0.21 0.24
0.57 0.43 0.32 0.59 0.40 0.96 0.90 0.36 0.74 0.85 0.35 0.72 0.79 0.62 0.72 0.60 0.79 0.76
– 0.05 0.39 0.03 0.38 0.01 – 0.05 0.01 0.01 0.01 0.20 0.20 0.19 – 0.24 – –
Variables
Total sample
1 = Yes
0 = No
Missing values
Smoking during pregnancy Father smoked when child was 5 years old Father smoked when child was 16 years old Mother smoked when child was 5 years old Mother smoked when child was 16 years old No single use of bathroom Change in family structure (divorce or a parent's death) Father is in the manual labour social class Fighting peers at age 5 Destroying belongings at age 5 Disobeying parents at age 5 Fighting peers at age 16 Destroying belongings at age 16 Disobeying parents at age 16 Smoking at age 34 Social class at age 34 (manual = 1) Education at age 34 (lowest = 1) Marital status age 34 (single, widowed, or separated = 1)
2865 2750 1280 2770 1268 2837 2876 2754 2861 2861 2863 2252 2248 2251 2875 2642 2873 2877
0.42 0.50 0.20 0.38 0.16 0.03 0.10 0.57 0.41 0.26 0.72 0.07 0.04 0.22 0.41 0.37 0.25 0.26
0.57 0.45 0.25 0.58 0.29 0.96 0.90 0.38 0.58 0.73 0.27 0.71 0.74 0.57 0.69 0.54 0.75 0.74
0.01 0.05 0.55 0.04 0.55 0.01 – 0.05 0.01 0.01 0.01 0.22 0.22 0.21 – 0.09 – –
Table 2 Descriptive statistics in percentage for sons.
Sobel test (Sobel, 1982).3 Table 3 Standardised factor loadings of antisocial behaviour variables. Survey item
Sons
Daughters
Disobeying parents at age 5 Fighting peers at age 5 Destroying belongings at age 5 Disobeying parents at age 16 Fighting peers at age 16 Destroying belongings at age 16
0.58*** 0.71*** 0.71*** 0.59*** 0.72*** 0.72***
0.58*** 0.70*** 0.69*** 0.54*** 0.75*** 0.65***
5.2. The intergenerational transmission of smoking in sons The findings on sons are reported in Fig. 4. Smoking during pregnancy significantly increased subsequent maternal smoking when the son was age 5 by approximately double (O.R. = 2.02; C.I. = 1.97–2.07), which, in turn, predicted continuing smoking later in life (O.R. = 1.87; C.I. = 1.80–1.95). Prenatal smoking also increased the probability of developing antisocial behaviours at age 5 by 7% (O.R. = 1.07; C.I. = 1.04–1.09), which, in turn, predicted the persistence of behavioural difficulties at age 16 by approximately 35% (O.R. = 1.34; C.I. = 1.26–1.43). In addition, antisocial adolescents
Note: Each latent variable referring to antisocial behaviours (at 5 and 16 years old) is composed of three observed variables indicating whether the respondent tells lies, bullies peers, or steals things belonging to others. The asterisks show the levels of statistical significance of the corresponding factor loadings: (*** pvalue < 0.001, ** p-value < 0.01, * p-value < 0.05).
3 The Sobel test is a specialised t-test that provides a method to determine whether the reduction in the effect of the independent variable, after including the mediator in the model, is a significant reduction and, in turn, whether the mediation effect is statistically significant. This represents the change in the magnitude of the effect that the independent variable has on the dependent variable after controlling for the mediator. The Sobel test estimate is provided by:
indirect, and total effects for daughters. Estimates show that the intergenerational transmission of smoking for daughters was entirely explained by social learning mechanisms. Indeed, the cumulative effect of exposure to maternal smoking between the ages of 5 and 16 significantly increased the probability of becoming a smoker at age 34 by approximately 4% (O.R. = 1.04; C.I. = 1.00–1.06). The statistical significance of this mediated route was additionally confirmed by the
2 *SE 2 * 2 *SE 2
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(1)
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Fig. 3. Results for daughters showing the adjusted O.R. for the paths in the hypothesised model. Note: Odds ratios are reported with asterisks as indicators of the significance level: (***p-value < 0.001, **p-value < 0.01, *p-value < 0.05). LL = −7378.662, DF = 35, AIC = 14827.32, BIC = 15040.37. Table 4 Mediation analysis of daughters. Hypothesised sssociation
Direct effect
Indirect effects
Total effect
Sobel test
Mother smokes in pregnancy − > Cohort member smokes at 34
A. Epigenetic 0.99 (0.94–1.05)
B. Antisocial behaviours 1.00 (0.99–1.00) C. Social-learning 1.04(1.00–1.06)***
1.04 (0.97–1.09)
B. Antisocial behaviours 0.967 C. Social-learning 2.697***
Note: Odds ratios with confidence intervals in parentheses are reported with asterisks as indicators of the significance level: (***p-value < 0.001, ** p-value < 0.01, *p-value < 0.05).
Fig. 4. Results for sons showing the adjusted O.R. for the paths in the hypothesised model. Note: Odds ratios are reported with asterisks as indicators of the significance level: (***p-value < 0.001, **p-value < 0.01, *p-value < 0.05). LL = −8229.993, DF = 35, AIC = 16529.99, BIC = 16738.46.
were 74% more likely to smoke at age 34 (O.R. = 1.74; C.I. = 1.23–2.48). Also among sons, the direct association between smoking during pregnancy and their smoking habit was not statistically
significant (O.R. = 0.99; C.I. = 0.93–1.06), whereas exposure to maternal smoke during adolescence was significantly associated with the cohort member smoking habit, which increased by approximately 8% 104
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Table 5 Mediation analysis of sons. Hypothesised association
Direct effect
Indirect effects
Total effect
Sobel test
Mother smokes during pregnancy − > Cohort member smokes at 34
A. Epigenetic 0.99 (0.93–1.06)
B. Antisocial behaviours 1.01 (1.00–1.0)*** C. Social-learning 1.04 (1.00–1.07)**
1.05 (0.97–1.11)
B. Antisocial behaviours 2.693*** C. Social-learning 2.302**
Note: Odds ratios with confidence intervals in parentheses are reported with asterisks as indicators of the significance level: (***p-value < 0.001, ** p-value < 0.01, *p-value < 0.05).
behaviours and adolescence-limited problematic behaviours. Thus, our results highlight the importance of the persistence of antisocial behaviours in childhood as a potential precondition of recidivism in risktaking behaviours (such as smoking). These results clearly indicate that the main channel through which both boys and girls acquire maternal smoking habits is by observing and imitating their mothers’ behaviour since, according to social learning theory, children are inclined to consider tobacco consumption as a normal form of adult behaviour (Baric & Fisher, 1979). Therefore, children's reproduction of parental behaviours is consistent with social learning theory, which posits that habits toward cigarette smoking are learned through modelling parental conduct (Akers, Krohn, Lanza-Kaduce, & Radosevich, 1979; den Exter Blokland, Engels, Hale, Meeus, & Willemsen, 2004; Gilman et al., 2009). Contrary to some prior studies (Kandel et al., 1994; Kandel & Udry, 1999), the direct genetic hypothesis was not confirmed by our estimates. Indeed, despite the considerable literature providing evidence of the direct unique effects of being exposed to nicotine in pregnancy, the underlying biological processes may often be muddied due to the inability to separate tobacco exposure from other factors. Specifically, most existing studies provide only limited control for the fact that prenatal exposure is associated with parental behaviours that could act as proximal predictors in the transmission of behaviours to their offspring (Knopik, 2009). Indeed, the vast majority of existing research controlled only for postnatal smoking behaviours (Kandel et al., 1994) without hypothesising that, since postnatal smoking is strongly influenced by being used to smoke during pregnancy, it may be a suitable mediator of this relationship. Finally, some interesting considerations may involve differences in smoking behaviours between parents’ and children's generations. Even if the longitudinal structure of the data does not allow for a proper analysis able to detect the period effect, we can draw some conclusions by simply comparing proportions of smokers. According to the UK Office for National Statistics (ONS), while almost 55% of adults in the UK were smokers in the mid-1970s, the proportion of those reporting stable smoking habits in 2004 was substantially reduced (30% on average) with increasing differences between men and women compared to the 1970s pattern. These proportions are consistent with those reported by comparing parents’ and children's generations in our data.
(O.R. = 1.08; C.I. = 1.01–1.17). The direct, indirect, and total effects for sons are listed in Table 5. Estimates show that the intergenerational transmission of smoking in boys was partially explained by juvenile antisocial behaviours and partially by social learning mechanisms. Indeed, the effect of persistently showing an antisocial behaviour between the ages of 5 and 16 was positively associated with smoking at age 34 (O.R. = 1.01; C.I. = 1.00–1.01). Concomitantly, being continuously exposed to maternal smoking across childhood significantly increased the probability of becoming a smoker in adulthood by approximately 4% (O.R. = 1.04; C.I. = 1.00–1.07). Specifically, effect proportions indicate that persistent antisocial behaviours significantly mediated the relationship between smoking during pregnancy and sons’ smoking habits, explaining almost 22% of the total effect (ln 1.01/ln 1.05), whereas social learning mechanisms accounted for almost 78% of the entire effect (ln 1.04/ln 1.05). 6. Conclusions The aim of this paper was to identify the existence of a specific channel of intergenerational smoking transmission by simultaneously testing direct and indirect routes. Specifically, we assessed whether mothers who smoked during pregnancy predicted offspring smoking habits at age 34 acting through a direct epigenetic mechanism (A), through a mediation due to the child's antisocial behaviours (B), or through social learning mechanisms (C). Few studies have investigated the association between mother and offspring smoking habits by examining the persistence in antisocial behaviours and at postnatal smoking as potential mechanisms of transmission, adjusting analyses for early life and adult conditions as well as for fathers’ smoking habits. These findings uphold a statistically significant effect of maternal smoking during pregnancy on the problematic behaviours of offspring at age 5 with no significant differences with respect to gender (p > 0.1 for the test of interaction). Since we controlled for environmental factors that, as empirically confirmed, affect antisocial behaviours, the behavioural explanation was strongly supported by our results. However, its role in mediating the intergenerational transmission of smoking was confirmed only in boys, for whom antisocial behaviours in youth were strongly associated with their smoking habits in adulthood. The test of interaction confirmed a statistically significant difference in the effect of antisocial behaviours on adult smoking (chi-squared = 2.32; p < 0.1). Consistent with prior research (Windle, 1990), our findings demonstrated that antisocial behaviours may not be equally powerful predictors of adolescent (or adult) smoking or substance use for men and women. In men, antisocial and problematic behaviours are often combined with smoking and other substance use, since they are usually different manifestations of a broader pattern of behaviour that tends to eschew social norms (Jessor & Jessor, 1977; Wakschlag et al., 2002). In women, smoking has been associated more with internalising symptomatology (such as depression) rather than antisocial behaviours. The importance of identifying persistent paths of antisocial behaviour across the life course is suggested by psychosociological literature. Based on Moffitt (1993), age emerges as the best-established criterion to distinguish between life course persistent antisocial
7. Discussion These findings support the existence of specific life course channels of maternal smoking transmission with important differences according to a child's gender. Whereas findings on girls indisputably supported social learning mechanisms, with no evidence of direct epigenetic or antisocial hypotheses, results on sons provided indications concerning the potential role played by a child's persistent antisocial behaviours. With respect to previous studies, this paper contributes to the literature mainly through the identification of distinct paths within the life course in which the persistence of behaviours was conveyed through later health risks. However, some specific limitations should be listed. Whereas attrition due to mortality, migration, and missing answers could have marginally affected the estimation results, selectivity could be an issue due to the need to choose only individuals whose 105
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mothers and fathers were alive at the beginning of the study, even if such selection was limited. Other limitations refer mainly to potential biases in self-reporting; a more direct test of the prenatal smoking effect requires biological indicators of maternal smoking during pregnancy. In addition, the association between maternal smoking and child behavioural problems may also be partly confounded by genetic factors since mothers with behavioural problems are more likely to smoke and, via genetic transmission, have greater risk of having children with behavioural problems (Knopik, 2009). Previous literature has largely overlooked the lifelong influences of interpersonal, neighbourhood, community, cultural, institutional, and environmental spheres, whereas this paper focused only on individual-level factors. Regarding possible policy implications, this work is framed within a general goal of contributing to the elimination of disparities in health and behaviours, beginning with the description of family paths, which transmit inequalities among generations. From this perspective, broader knowledge in this field of study could provide a powerful instrument for policies to improve living conditions of children as a strategy for improving health and reducing health disparities across the entire life course. The findings of this study suggested that childhood and adolescence are key periods within life that shape adult behaviours, and so school and other exogenous factors, jointly with the family, seem to be strongly incisive. The well-known persistence feature of antisocial behaviours should convince policy makers to provide social investments during the early stages of life. Moreover, a deeper understanding of the intergenerational transmission of tobacco smoking can provide insights into health prevention, suggesting family-based interventions with the aim to reduce parental smoking and smoking in subsequent generations.
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How much and why does the mum matter? Mechanisms explaining the intergenerational transmission of smoking
T
M. Pasqualinia, , L. Pieronib, C. Tomassinic ⁎
a
Department of Statistical Science, University of Rome La Sapienza, Italy Department of Political Science, University of Perugia, Italy c Department of Economics, University of Molise, Italy b
ARTICLE INFO
ABSTRACT
Keywords: Childhood Adolescence Smoking Intergenerational transmission Antisocial behaviours Path analysis
Offspring whose mother smokes during pregnancy have higher risk of smoking themselves. In this study, epigenetics, antisocial behaviours, and social learning were investigated as potential mechanisms of mother-to-child transmission of smoking among a population sample drawn from the Birth Cohort Study 1970. Findings on daughters showed that the direct epigenetic hypothesis was mediated by social learning mechanisms, suggesting that exposure to maternal smoking across childhood and adolescence strongly explained why the smoking habits of mother and daughter correlate. However, prenatal smoking effects on sons were only partially explained by observational learning of mother smoking habits. Our estimates provided evidence concerning the potential role also played by the child's persistent antisocial behaviours. These results were confirmed after controlling for early life circumstances and current socioeconomic conditions. Policy implications of the results are discussed.
1. Introduction In the last decade, robust empirical findings on the intergenerational transmission of smoking have been reported. However, the literature has not reached a consensus on the nature and strength of this relationship. Different hypotheses have been formulated to explain the association between smoking during pregnancy and a child's subsequent smoking habit, distinguishing between direct and indirect routes. Previous studies have explored this relationship, assessing the earlier smoking initiation of the child, current smoking status, and its persistence over time (Al Mamun et al., 2006; Buka, Shenassa, & Niaura, 2003; Griesler, Kandel, & Davies, 1998; Oncken, McKee, Krishnan-Sarin, O’Malley, & Mazure, 2004). Some of these studies were supportive of the direct epigenetic explanation setting that the foetus inherits susceptibility to addiction since the nicotine is transmitted by the placenta and this predisposes the child to smoke (Kandel & Udry, 1999; Kandel, Wu, & Davies, 1994). Another way through which physiological mechanisms act is mediated by antisocial behaviours (Benowitz, 2001; Miles & Weden, 2012; Wakschlag et al., 2003; Wakschlag, Pickett, Cook, Benowitz, & Leventhal, 2002). According to this hypothesis, exposure to tobacco in utero neurologically affects the foetus in terms of behavioural problems (Wakschlag et al., 2002) that, in turn, sets in motion trajectories making the initiation and progression of smoking more likely (Miles & Weden, ⁎
2012). Finally, since mothers who smoke during pregnancy are very likely to continue smoking after birth (Miles & Weden, 2012), the direct effect may also be mediated by exposure to postnatal smoking. Exposure to parental smoking during childhood and adolescence has been proven to predict child adult smoking acting through a social learning process that reflects role modelling and operates through a supportive influence on pro-smoking norms and attitudes. This paper aims to identify the existence of a specific channel of smoking transmission by simultaneously testing direct and indirect mechanisms. Specifically, we assess whether smoking during pregnancy predicts offspring smoking habits at age 34 acting through a direct epigenetic route, a physiological effect on the child's behaviours, or a mechanism of socialisation. The choice of focusing on adult smoking habit, despite adolescent initiation, must be considered as a robustness of the tested hypothesis, since smoking initiation may be strongly affected by peers. In addition, taking advantage of the longitudinal design of our data, we accounted for the persistence of behaviours across the life course. Analyses were conducted separately by gender, testing potential differences between offspring's sex. To estimate the mother-tochild transmission of smoking, we propose an approach based on the structural equation model (SEM), drawing on data from the 1970 British Cohort Study (BCS70). Consistent with prior research, we hypothesise that smoking behaviour is transmitted from mother to child with some differences according to gender and provide empirical
Corresponding author at: Department of Statistical Science, University of Rome La Sapienza, Viale Regina Elena 295, Palazzina G, Roma, Italy. E-mail address: [email protected] (M. Pasqualini).
https://doi.org/10.1016/j.alcr.2019.03.004 Received 21 September 2017; Received in revised form 4 November 2018; Accepted 4 March 2019 Available online 08 March 2019 1040-2608/ © 2019 Elsevier Ltd. All rights reserved.
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findings to shed light on the mediating roles of both antisocial behaviours and social learning mechanisms. As a contribution to the growing literature on intergenerational transmissions, our empirical approach differs from most previous studies (Gilman et al., 2009; Melchior, Chastang, Mackinnon, Galera, & Fombonne, 2010; Otten, Engels, van de Ven, & Bricker, 2007; Wakschlag et al., 2002; Wickrama, Conger, Wallace, & Elder, 1999; Chassin, Presson, Rose, & Sherman, 1998; Griesler et al., 1998) because it considers adolescence as a mediation step instead of the time of transmission outcome.
functioning. In addition, the interaction between nicotine and hormones may explain apparent sexual differences in effects (Lichtensteiger & Schlumpf, 1993; Kandel & Udry, 1999). According to Fried et al. (1998), effects on neurological development due to exposure to cigarette smoke during pregnancy lead to antisocial manifestations early in life that, in turn, are associated with a higher probability of starting and continuing to smoke (Miles & Weden, 2012). Specifically, antisocial behaviour is defined as a heterogeneous concept encompassing physically aggressive behaviours (for example, bullying or fighting), rule breaking and oppositional behaviours (for example, destroying belongings and disobeying parents), and more severe problems associated with lack of empathy and guilt (Bonino, Cattelino, Ciairano, & Jessor, 2007; Donovan, Jessor, & Costa, 1991; Jessor & Jessor, 1977). According to Moffitt (1993), the age of onset may be considered one of the best-established methods to characterise the heterogeneity within antisocial behaviours and, therefore, to differentiate between the life course persistent (LCP) and adolescence limited (AL) antisocial subgroups. According to this definition, while adolescents often tend to behave antisocially, they do so only temporarily, but most children who develop early behavioural problems have a long history of antisocial conduct (as shown in Fig. 1).
2. Background Tobacco smoking shows a significant heritability (Chassin et al., 2005; Li, 2003; Melchior et al., 2010) because family members tend to resemble each other in terms of health behaviours, as explained by Schor and Menaghan (1995) for whom similarities reflect familial and genetic predisposition, shared physical, social, and emotional environments, and acquired health beliefs and values. Previous research investigating the relationship between mothers smoking during pregnancy and child smoking outcomes adopted different theoretical perspectives. This paper suggests three analytical mechanisms (epigenetic, antisocial behaviours, and social learning), that may contribute to identify both direct and indirect smoking outcomes.
2.3. The social-learning mechanism There is evidence that these physiological associations may be completely confounded by social and environmental factors, especially when there is no clear distinction between smoking during pregnancy and postnatal smoking habit (Brion et al., 2010; Knopik, 2009; Maughan, Taylor, Caspi, & Moffitt, 2004; Roza et al., 2009) that are strongly related. Indeed, mothers who smoke during pregnancy are very likely to continue after birth (Miles & Weden, 2012); thus, postnatal smoking may be another potential mediator of this relationship. Social learning theory (Bandura & Walters, 1977) demonstrated that behaviours can be assimilated through direct modelling by others and parental influence increases over time due to long-term attention and the retention processes of the child. According to this hypothesis, children learn by observing and modelling their parents’ behaviour. Previous studies showed that cigarette consumption among adults and adolescents correlated modestly but significantly with each other (Bricker et al., 2006; Chassin et al., 2005; Li, 2003; Wickrama et al., 1999). Some studies in the literature confirmed that maternal and paternal smoking equally influenced offspring tobacco use (Bailey, Ennett, & Ringwalt, 1993; Chassin, Presson, Rose, & Sherman, 1998; Darling & Cumsille, 2003; Hu, Davies, & Kandel, 2006; Peterson et al., 2006), whereas others showed that mothers who smoked had a stronger effect than fathers on adolescent smoking (Brenner & Scharrer, 1996; Herlitz & Westholm, 1996), although the opposite has also been reported (Shamsuddin & Haris, 2000).
2.1. The epigenetic mechanism One mechanism underlying the effect of prenatal smoking on offspring might be the impact of nicotine products on the developing brain of the foetus. Nicotine may encourage the action of the cholinergic neurons, increment nicotinic receptors in the brain, and enhance activity in the neural systems involved in addictive behaviour (Kandel & Udry, 1999; Lambers & Clark, 1996). According to this theory, nicotine, which enters through the placenta, may alter the nervous system and change its threshold (Kandel & Udry, 1999). Thus, during a critical prenatal period of brain development, exposure to maternal smoke may have direct effects on the foetus, predisposing the child to smoke and persist in smoking later in life (Kandel et al., 1994). This explanation is consistent with the hypothesis that addictive drugs can modify gene expression and therefore induce structural changes in the dopaminergic systems (Kandel et al., 1994). Relevant sex differences in the direct physiological effect of prenatal smoking on offspring have been explained by invoking the distinctive sexual hormonal dimorphism of the brain that emerges during foetal development (Kelly, 1991; Tallal & McEwen, 1991; Kandel et al., 1994). This hypothesis has been enforced by genetic studies that found how smoking is influenced by genetic factors such as testosterone. Indeed, in female foetuses, in contrast to male foetuses, testosterone levels are determined by the maternal genetic factors, which affect the central nervous system of women in utero and thus increase their daughters’ likelihood of smoking.
3. Empirical strategy Although there is strong evidence that both pre- and postnatal maternal smoking increases the risk of offspring smoking, some unresolved issues remain regarding the nature and strength of this association. Therefore, a more careful specification of the transmission paths is necessary that might to produce a clearer understanding of why and how much to what extent smoking mothers matter. Thus far, the literature has mainly distinguished between epigenetic, antisocial behaviours, and social learning oriented studies. However, there is a lack of comprehensive studies identifying the real contribution of each route of transmission. Thus, this paper aims to extend prior empirical evidence by simultaneously testing direct and indirect routes of mother-to-child transmission of smoking. Moreover, this research frames observations into a life course perspective controlling for the persistence of behaviours across life stages. Empirically, the pathways approach is used to distinguish different trajectories and
2.2. The antisocial behaviour mechanism Empirical findings have tested the effect of maternal smoking during pregnancy on children's psychological problems, including antisocial (Brion et al., 2010; Fried, Watkinson, & Gray, 1998; Miles & Weden, 2012; Wakschlag et al., 2002; Zoloto, Nagoshi, Presson, & Chassin, 2012) and problematic behaviours (Wakschlag et al., 2003). Previous evidence indicates that prenatal exposure to nicotine is associated with foetal neurotoxicity (Benowitz, 2001; Wakschlag et al., 2002) that might occur via hypoxic effects on the foetal-placental unit and via teratological effects on the foetal nervous system (Lichtensteiger & Schlumpf, 1993; Wakschlag et al., 2002). The nicotine effect is mainly due to its stimulation of nicotinic receptors in the brain that interact with genes, causing permanent alterations in cell 100
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Fig. 1. Hypothetical illustration of life course change in antisocial involvement. The figure is from Moffitt (1993).
Smoking during pregnancy is measured by asking whether the mother of the respondent smoked any kind of tobacco when she was pregnant (yes = 1, no = 0). Postnatal maternal smoking takes into account whether the mother smoked when the child was 5 and 16 years old (yes/no). Young antisocial behaviours are measured considering the same set of variables reported by the mother for both childhood and adolescence (at 5 and 16 years old). Since antisocial behaviours consist of a wide range of factors, we simplify this heterogeneous category by selecting five variables that, even if not exhaustive of antisocial behaviours, are the most used in the literature. According to Bonino et al. (2007), the antisocial mode should comprise physical or verbal aggression against peers, theft or vandalism, and telling lies. Hence, the variables were selected according to whether the child/adolescent fights with other peers, whether she/he sometimes destroys belongings, and whether she/he is often disobedient. Finally, the main outcome is an observed variable that was constructed based on smoking status at age 34. In this way, we are able to test the mother-to-child transmission of smoking, assessing the life course patterns of behaviours. A set of covariates were taken into account. Smoking at age 34 was also controlled for social class based on the Registrar General's classification (manual versus non-manual), education level (lower versus higher), marital status (single, widowed, or divorced versus married), and the father's smoking habits when the child was 5 and 16 years old. Antisocial behaviours at age 5 were controlled for a set variables related to the child's early life conditions. We measured the changes in the family structure (specifically, whether the family experienced divorce or a parent's death during the child's infancy), the single use of the bathroom for the family as a measure of home facilities and, finally, whether or not the father was employed in a manual job. In the empirical analyses, we used the structural equation model (SEM), which allows both latent and observed indicators to be considered within a single framework, since the observed variables are involved as indicators of the latent constructs (Kline, 2015). Moreover, the support of graphical representations (for example, the path analysis) makes it easier to identify the causal relationship among the latent constructs and their specifications by the observed variables 1 .
emphasise the differences between the direct and indirect effects of each life stage. Fig. 2 outlines the graphical model, which supports the following hypotheses: A. Maternal smoking during pregnancy may directly affect a child's probability of smoking at age 34 (epigenetic mechanism). B. Maternal smoking during pregnancy may indirectly affect a child's smoking habit at age 34 via the child's persistent problematic behaviours (antisocial behaviours mechanism). C. Maternal smoking during pregnancy indirectly affects a child's smoking habit at age 34 via subsequent maternal smoking behaviour (social learning mechanism). The model controls for a child's social class, level of education, marital status, and the father's smoking habit, while antisocial behaviours are controlled for some variables related to the household socioeconomic condition during the offspring's childhood, such as the single use of the bathroom, the father's employment skill, and any disruptive change in the family structure (divorce and/or parental deaths). 4. Data and method This paper used the 1970 British Cohort Study (BCS70) to estimate the intergenerational transmission of smoking habit. This database is an ongoing national longitudinal study that involves more than 17,000 individuals born in Great Britain in a given week in April 1970 (including stillbirths). This survey was conducted at regular intervals (the last wave was in 2012), providing more than 15,000 multidisciplinary variables. According to the Response and Deaths datasets, the level of attrition for mortality, migration, and missing answers varied across waves by 5–20%. However, the longitudinal nature of this research design avoids selection biases that may affect the analyses. This paper used the 1970, 1975, 1986, and 2004 waves. The sample was comprised of 6138 members (53% women) of the longitudinal target who participated in all of the selected waves. The birth cohort data contain detailed information at a micro level on the health, health-related behaviours, education, and social development of all cohort members as they passed through childhood and adolescence until they progressed into adult life. These data provide a picture of the entire generation and offer a unique opportunity to understand the origins of socioeconomic, health, and behavioural disparities from childhood to adulthood.
1
Model diagrams are represented in this article using symbols from the McArdle–McDonald reticular action model (RAM): observed variables are represented by rectangles, latent variables by circles or ellipses, and hypothesised directional direct effects of one variable to another by a line with a single arrowhead. 101
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Fig. 2. Theoretical model. Note: Latent variables are represented by ellipses and observed variables are represented by rectangles.
Estimates were carried out using the STATA 14 GSEM command. In this setting, the hypotheses were tested through the maximum likelihood estimation based on a two-step modelling approach: the multiple indicators measurement model and the structural analysis. Thus, path models can provide considerable insight into complex causal mechanisms by investigating the mediating role of young peoples’ antisocial behaviours. Specifically, it is possible to decompose the total effect of cigarette smoking transmission into direct and indirect components (Pickles & De Stavola, 2007) and test whether the introduction of antisocial latent constructs changes the effect of causality between the dependent (e.g. adult smoking behaviours) and the independent variables (e.g. smoking during pregnancy).2 In addition, gender differences in parameters were explicitly tested with the Wald chi-squared test of interaction. Tables 1 and 2 show the frequency distributions and missing values (in percentage) for each binary variable by gender.
associated items. Moreover, measurement errors associated with each observed indicator are hypothesised to be uncorrelated with each other and the latent variable. Because STATA GSEM does not provide goodness-of-fit statistics, the size of the estimated coefficients was used to determine the adequacy of the measurement model (see also Silverstein & Bengtson, 2018). 5.1. The intergenerational transmission of smoking in daughters Generalised structural equation modelling (GSEM) is an extension of SEM that allows the analysis of categorical data utilising a logistic link function that does not rely on linear assumptions to model relationships with dichotomous data. The odds ratios (O.R.), confidence intervals (C.I.), and p-values (p-v) are estimated and are listed in the figures. Fig. 3 lists the adjusted odds ratios for daughters. The findings indicate that smoking during pregnancy, early antisocial behaviours, postnatal maternal smoking, and offspring smoking habit at age 34 were significantly associated. However, some considerations occurred. Mothers who smoked during pregnancy were approximately two times more likely to continue smoking when their daughter was age 5 (O.R. = 2.01; C.I. = 1.96–2.05). Concomitantly, smoking during pregnancy significantly increased the daughters’ probability of engaging in antisocial behaviours at age 5 (O.R. = 1.05; C.I. = 1.03–1.07). However, the direct relationship between smoking during pregnancy and daughters’ smoking at age 34 was not statistically significant (O.R. = 0.99; C.I. = 0.94–1.05). Consistent with social learning theory, the exposure to maternal smoking when the daughter was adolescent significantly predicted her probability of smoking at age 34 of approximately 8% (O.R. = 1.08; C.I. = 1.02–1.15). However, daughters who were antisocial at age 16 were not significantly more likely to smoke in adulthood, even if the effect was high in magnitude (O.R. = 1.27; C.I. = 0.78–2.07). Finally, the persistence of behaviours was confirmed by estimates. Indeed, maternal smoking habit when the daughter was age 5 strongly increased maternal smoking 11 years later by approximately 94% (O.R. = 1.94; C.I. = 1.88–2.00) and, consistent with Moffitt's theory (1993), similar effects have been found for child antisocial behaviours between age 5 and 16 (O.R. = 01.21; C.I. = 1.15–1.27). The findings from the mediation analysis are shown in Table 4 and report the direct,
5. Results The factor loadings, as shown in Table 3, indicate the measure of correlation between the observed items (disobeying parents, fighting peers, and destroying belongings) and the latent construct (antisocial behaviours). Standardised loadings show satisfying measurement properties varying from 0.45 to 0.75, which is a good range compared to conventions of the loadings of 0.40 or greater. The positive loading signs indicate the direction of the effect of the constructs on the 2 According to Preacher and Leonardelli (2009), a variable may be considered a mediator when it carries the influence of a given independent variable to a given dependent variable. From the contributions of some authors (Baron & Kenny, 1986; James & Brett, 1984; Judd & Kenny, 1981), four criteria that must be followed to investigate whether mediation occurs: (1) the independent variable significantly affects the mediator, (2) the independent variable significantly affects the dependent variable in the absence of the mediator, (3) the mediator has a significant effect on the dependent variable, and (4) the effect of the independent variable on the dependent variable significantly decreases upon the addition of the mediator. Because all of the observed indicators are binary, the latent variables are linked to observed variables by probit regression models; this framework is also used to link the outcome of the latent and observed variables (Golini & Egidi, 2002).
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Table 1 Descriptive statistics in percentage for daughters. Variables
Total sample
1 = Yes
0 = No
Missing values
Smoking during pregnancy Father smoked when child was 5 years old Father smoked when child was 16 years old Mother smoked when child was 5 years old Mother smoked when child was 16 years old No single use of bathroom Change in family structure (divorce or a parent's death) Father is in the manual labour social class Fighting peers at age 5 Destroying belongings at age 5 Disobeying parents at age 5 Fighting peers at age 16 Destroying belongings at age 16 Disobeying parents at age 16 Smoking at age 34 Social class at age 34 (manual = 1) Education at age 34 (lowest = 1) Marital status age 34 (single, widowed, or separated = 1)
3258 3084 1980 3156 1976 3229 3253 2750 3240 3243 3238 2631 2644 2638 3260 2465 3258 3261
0.43 0.52 0.29 0.38 0.22 0.03 0.10 0.59 0.25 0.14 0.64 0.08 0.01 0.19 0.28 0.16 0.21 0.24
0.57 0.43 0.32 0.59 0.40 0.96 0.90 0.36 0.74 0.85 0.35 0.72 0.79 0.62 0.72 0.60 0.79 0.76
– 0.05 0.39 0.03 0.38 0.01 – 0.05 0.01 0.01 0.01 0.20 0.20 0.19 – 0.24 – –
Variables
Total sample
1 = Yes
0 = No
Missing values
Smoking during pregnancy Father smoked when child was 5 years old Father smoked when child was 16 years old Mother smoked when child was 5 years old Mother smoked when child was 16 years old No single use of bathroom Change in family structure (divorce or a parent's death) Father is in the manual labour social class Fighting peers at age 5 Destroying belongings at age 5 Disobeying parents at age 5 Fighting peers at age 16 Destroying belongings at age 16 Disobeying parents at age 16 Smoking at age 34 Social class at age 34 (manual = 1) Education at age 34 (lowest = 1) Marital status age 34 (single, widowed, or separated = 1)
2865 2750 1280 2770 1268 2837 2876 2754 2861 2861 2863 2252 2248 2251 2875 2642 2873 2877
0.42 0.50 0.20 0.38 0.16 0.03 0.10 0.57 0.41 0.26 0.72 0.07 0.04 0.22 0.41 0.37 0.25 0.26
0.57 0.45 0.25 0.58 0.29 0.96 0.90 0.38 0.58 0.73 0.27 0.71 0.74 0.57 0.69 0.54 0.75 0.74
0.01 0.05 0.55 0.04 0.55 0.01 – 0.05 0.01 0.01 0.01 0.22 0.22 0.21 – 0.09 – –
Table 2 Descriptive statistics in percentage for sons.
Sobel test (Sobel, 1982).3 Table 3 Standardised factor loadings of antisocial behaviour variables. Survey item
Sons
Daughters
Disobeying parents at age 5 Fighting peers at age 5 Destroying belongings at age 5 Disobeying parents at age 16 Fighting peers at age 16 Destroying belongings at age 16
0.58*** 0.71*** 0.71*** 0.59*** 0.72*** 0.72***
0.58*** 0.70*** 0.69*** 0.54*** 0.75*** 0.65***
5.2. The intergenerational transmission of smoking in sons The findings on sons are reported in Fig. 4. Smoking during pregnancy significantly increased subsequent maternal smoking when the son was age 5 by approximately double (O.R. = 2.02; C.I. = 1.97–2.07), which, in turn, predicted continuing smoking later in life (O.R. = 1.87; C.I. = 1.80–1.95). Prenatal smoking also increased the probability of developing antisocial behaviours at age 5 by 7% (O.R. = 1.07; C.I. = 1.04–1.09), which, in turn, predicted the persistence of behavioural difficulties at age 16 by approximately 35% (O.R. = 1.34; C.I. = 1.26–1.43). In addition, antisocial adolescents
Note: Each latent variable referring to antisocial behaviours (at 5 and 16 years old) is composed of three observed variables indicating whether the respondent tells lies, bullies peers, or steals things belonging to others. The asterisks show the levels of statistical significance of the corresponding factor loadings: (*** pvalue < 0.001, ** p-value < 0.01, * p-value < 0.05).
3 The Sobel test is a specialised t-test that provides a method to determine whether the reduction in the effect of the independent variable, after including the mediator in the model, is a significant reduction and, in turn, whether the mediation effect is statistically significant. This represents the change in the magnitude of the effect that the independent variable has on the dependent variable after controlling for the mediator. The Sobel test estimate is provided by:
indirect, and total effects for daughters. Estimates show that the intergenerational transmission of smoking for daughters was entirely explained by social learning mechanisms. Indeed, the cumulative effect of exposure to maternal smoking between the ages of 5 and 16 significantly increased the probability of becoming a smoker at age 34 by approximately 4% (O.R. = 1.04; C.I. = 1.00–1.06). The statistical significance of this mediated route was additionally confirmed by the
2 *SE 2 * 2 *SE 2
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Fig. 3. Results for daughters showing the adjusted O.R. for the paths in the hypothesised model. Note: Odds ratios are reported with asterisks as indicators of the significance level: (***p-value < 0.001, **p-value < 0.01, *p-value < 0.05). LL = −7378.662, DF = 35, AIC = 14827.32, BIC = 15040.37. Table 4 Mediation analysis of daughters. Hypothesised sssociation
Direct effect
Indirect effects
Total effect
Sobel test
Mother smokes in pregnancy − > Cohort member smokes at 34
A. Epigenetic 0.99 (0.94–1.05)
B. Antisocial behaviours 1.00 (0.99–1.00) C. Social-learning 1.04(1.00–1.06)***
1.04 (0.97–1.09)
B. Antisocial behaviours 0.967 C. Social-learning 2.697***
Note: Odds ratios with confidence intervals in parentheses are reported with asterisks as indicators of the significance level: (***p-value < 0.001, ** p-value < 0.01, *p-value < 0.05).
Fig. 4. Results for sons showing the adjusted O.R. for the paths in the hypothesised model. Note: Odds ratios are reported with asterisks as indicators of the significance level: (***p-value < 0.001, **p-value < 0.01, *p-value < 0.05). LL = −8229.993, DF = 35, AIC = 16529.99, BIC = 16738.46.
were 74% more likely to smoke at age 34 (O.R. = 1.74; C.I. = 1.23–2.48). Also among sons, the direct association between smoking during pregnancy and their smoking habit was not statistically
significant (O.R. = 0.99; C.I. = 0.93–1.06), whereas exposure to maternal smoke during adolescence was significantly associated with the cohort member smoking habit, which increased by approximately 8% 104
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Table 5 Mediation analysis of sons. Hypothesised association
Direct effect
Indirect effects
Total effect
Sobel test
Mother smokes during pregnancy − > Cohort member smokes at 34
A. Epigenetic 0.99 (0.93–1.06)
B. Antisocial behaviours 1.01 (1.00–1.0)*** C. Social-learning 1.04 (1.00–1.07)**
1.05 (0.97–1.11)
B. Antisocial behaviours 2.693*** C. Social-learning 2.302**
Note: Odds ratios with confidence intervals in parentheses are reported with asterisks as indicators of the significance level: (***p-value < 0.001, ** p-value < 0.01, *p-value < 0.05).
behaviours and adolescence-limited problematic behaviours. Thus, our results highlight the importance of the persistence of antisocial behaviours in childhood as a potential precondition of recidivism in risktaking behaviours (such as smoking). These results clearly indicate that the main channel through which both boys and girls acquire maternal smoking habits is by observing and imitating their mothers’ behaviour since, according to social learning theory, children are inclined to consider tobacco consumption as a normal form of adult behaviour (Baric & Fisher, 1979). Therefore, children's reproduction of parental behaviours is consistent with social learning theory, which posits that habits toward cigarette smoking are learned through modelling parental conduct (Akers, Krohn, Lanza-Kaduce, & Radosevich, 1979; den Exter Blokland, Engels, Hale, Meeus, & Willemsen, 2004; Gilman et al., 2009). Contrary to some prior studies (Kandel et al., 1994; Kandel & Udry, 1999), the direct genetic hypothesis was not confirmed by our estimates. Indeed, despite the considerable literature providing evidence of the direct unique effects of being exposed to nicotine in pregnancy, the underlying biological processes may often be muddied due to the inability to separate tobacco exposure from other factors. Specifically, most existing studies provide only limited control for the fact that prenatal exposure is associated with parental behaviours that could act as proximal predictors in the transmission of behaviours to their offspring (Knopik, 2009). Indeed, the vast majority of existing research controlled only for postnatal smoking behaviours (Kandel et al., 1994) without hypothesising that, since postnatal smoking is strongly influenced by being used to smoke during pregnancy, it may be a suitable mediator of this relationship. Finally, some interesting considerations may involve differences in smoking behaviours between parents’ and children's generations. Even if the longitudinal structure of the data does not allow for a proper analysis able to detect the period effect, we can draw some conclusions by simply comparing proportions of smokers. According to the UK Office for National Statistics (ONS), while almost 55% of adults in the UK were smokers in the mid-1970s, the proportion of those reporting stable smoking habits in 2004 was substantially reduced (30% on average) with increasing differences between men and women compared to the 1970s pattern. These proportions are consistent with those reported by comparing parents’ and children's generations in our data.
(O.R. = 1.08; C.I. = 1.01–1.17). The direct, indirect, and total effects for sons are listed in Table 5. Estimates show that the intergenerational transmission of smoking in boys was partially explained by juvenile antisocial behaviours and partially by social learning mechanisms. Indeed, the effect of persistently showing an antisocial behaviour between the ages of 5 and 16 was positively associated with smoking at age 34 (O.R. = 1.01; C.I. = 1.00–1.01). Concomitantly, being continuously exposed to maternal smoking across childhood significantly increased the probability of becoming a smoker in adulthood by approximately 4% (O.R. = 1.04; C.I. = 1.00–1.07). Specifically, effect proportions indicate that persistent antisocial behaviours significantly mediated the relationship between smoking during pregnancy and sons’ smoking habits, explaining almost 22% of the total effect (ln 1.01/ln 1.05), whereas social learning mechanisms accounted for almost 78% of the entire effect (ln 1.04/ln 1.05). 6. Conclusions The aim of this paper was to identify the existence of a specific channel of intergenerational smoking transmission by simultaneously testing direct and indirect routes. Specifically, we assessed whether mothers who smoked during pregnancy predicted offspring smoking habits at age 34 acting through a direct epigenetic mechanism (A), through a mediation due to the child's antisocial behaviours (B), or through social learning mechanisms (C). Few studies have investigated the association between mother and offspring smoking habits by examining the persistence in antisocial behaviours and at postnatal smoking as potential mechanisms of transmission, adjusting analyses for early life and adult conditions as well as for fathers’ smoking habits. These findings uphold a statistically significant effect of maternal smoking during pregnancy on the problematic behaviours of offspring at age 5 with no significant differences with respect to gender (p > 0.1 for the test of interaction). Since we controlled for environmental factors that, as empirically confirmed, affect antisocial behaviours, the behavioural explanation was strongly supported by our results. However, its role in mediating the intergenerational transmission of smoking was confirmed only in boys, for whom antisocial behaviours in youth were strongly associated with their smoking habits in adulthood. The test of interaction confirmed a statistically significant difference in the effect of antisocial behaviours on adult smoking (chi-squared = 2.32; p < 0.1). Consistent with prior research (Windle, 1990), our findings demonstrated that antisocial behaviours may not be equally powerful predictors of adolescent (or adult) smoking or substance use for men and women. In men, antisocial and problematic behaviours are often combined with smoking and other substance use, since they are usually different manifestations of a broader pattern of behaviour that tends to eschew social norms (Jessor & Jessor, 1977; Wakschlag et al., 2002). In women, smoking has been associated more with internalising symptomatology (such as depression) rather than antisocial behaviours. The importance of identifying persistent paths of antisocial behaviour across the life course is suggested by psychosociological literature. Based on Moffitt (1993), age emerges as the best-established criterion to distinguish between life course persistent antisocial
7. Discussion These findings support the existence of specific life course channels of maternal smoking transmission with important differences according to a child's gender. Whereas findings on girls indisputably supported social learning mechanisms, with no evidence of direct epigenetic or antisocial hypotheses, results on sons provided indications concerning the potential role played by a child's persistent antisocial behaviours. With respect to previous studies, this paper contributes to the literature mainly through the identification of distinct paths within the life course in which the persistence of behaviours was conveyed through later health risks. However, some specific limitations should be listed. Whereas attrition due to mortality, migration, and missing answers could have marginally affected the estimation results, selectivity could be an issue due to the need to choose only individuals whose 105
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mothers and fathers were alive at the beginning of the study, even if such selection was limited. Other limitations refer mainly to potential biases in self-reporting; a more direct test of the prenatal smoking effect requires biological indicators of maternal smoking during pregnancy. In addition, the association between maternal smoking and child behavioural problems may also be partly confounded by genetic factors since mothers with behavioural problems are more likely to smoke and, via genetic transmission, have greater risk of having children with behavioural problems (Knopik, 2009). Previous literature has largely overlooked the lifelong influences of interpersonal, neighbourhood, community, cultural, institutional, and environmental spheres, whereas this paper focused only on individual-level factors. Regarding possible policy implications, this work is framed within a general goal of contributing to the elimination of disparities in health and behaviours, beginning with the description of family paths, which transmit inequalities among generations. From this perspective, broader knowledge in this field of study could provide a powerful instrument for policies to improve living conditions of children as a strategy for improving health and reducing health disparities across the entire life course. The findings of this study suggested that childhood and adolescence are key periods within life that shape adult behaviours, and so school and other exogenous factors, jointly with the family, seem to be strongly incisive. The well-known persistence feature of antisocial behaviours should convince policy makers to provide social investments during the early stages of life. Moreover, a deeper understanding of the intergenerational transmission of tobacco smoking can provide insights into health prevention, suggesting family-based interventions with the aim to reduce parental smoking and smoking in subsequent generations.
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