Abstract
Abstract
Purpose:
There is little known about the association between breastfeeding and long-term child psychopathology. This study aimed to examine the impact of breastfeeding on child mental health and problem behavior at 14 years and whether this association is confounded by other variables.
Subjects and Methods:
Data were from a pre-birth prospective study that included mothers and their children followed up from pregnancy to 14 years of the child's age in Brisbane, Australia. The child's anxiety/depression, withdrawal problems, somatic complaints, social problems, thought problems, attention problems, aggression, and delinquency were measured using the Achenbach Youth Self Report at 14 years. Breastfeeding was prospectively assessed at the 6-month follow-up of the study. The analysis was based on 4,502 adolescents who responded to the YSR questionnaire and for whom prospective data were available on breastfeeding.
Results:
Breastfeeding as reported by mothers when the child was 6 months old predicted reduced symptoms of child mental health and problem behavior at 14 years. The impact of breastfeeding on the child's social problems, attention problems, and aggressive behavior remained statistically significant after controlling for the effect of other variables, such as unplanned pregnancy, maternal mental health, and substance use during pregnancy.
Conclusions:
Our data suggest that breastfeeding for at least 4 months can have a significant protective effect on a child's social, attention, and aggression problems in early adolescence. Given the limitations of the existing evidence, further research is needed to investigate the robustness of the findings of this study and the mechanisms of long-term association between breastfeeding and reduced social, attention, and aggression problems of the offspring in adolescence.
Introduction
To date, there have been few studies that have examined the relationship between breastfeeding and offspring's psychobehavioral development in childhood and early adolescence,8–13 although findings are not consistent across studies. The discrepancy between the results of these studies could be due to different methods of assessment of outcomes and/or level of control for potential confounders. For example, in a prospective study of 500 newborns in Spain, Julvez et al. 12 found that attention, hyperactivity, and social competency of 4-year-old children were associated with their duration of breastfeeding. In contrast, a longitudinal research from New Zealand 8 suggested that the influence of breastfeeding on a child's conduct problems was mainly due to confounding factors. In this study, scores of conduct disorder (for both maternal and teacher ratings) declined with increasing duration of breastfeeding. However, when potential confounding factors were taken into account, maternal (but not teacher) ratings of child conduct disorder remained significantly correlated with length of breastfeeding.
In one of the few longitudinal studies, Fergusson and Woodward 9 found no significant difference in self-reported rate of juvenile offending and court conviction and of DSM-IV substance use and mental health problems between breastfed and bottle-fed children. Consistently, a Brazilian cohort study found no association between breastfeeding and violent crimes resulting in conviction between 12 and 25 years. 14 However, a recent Australian cohort study found association between shorter duration of breastfeeding and increased symptoms of mental health problems. 13
Notwithstanding previous research, there is little known about the impact of breastfeeding on the mental health and behavior of the child as he or she progresses through the usual developmental stages. To our knowledge, there has been no research on the impact of breastfeeding on a wide range of child mental health and problem behaviors. This study aims to examine the prospective association between breastfeeding in the first 6 months after the birth of the child and that child's mental health and behavioral outcomes at 14 years. It also aims to explore whether background characteristics that are associated with both breastfeeding and offspring's outcomes confound their association. We hypothesize that longer duration of breastfeeding is associated with fewer adverse outcomes in early adolescence.
Subjects and Methods
Participants
The data were taken from the 21-year Mater-University of Queensland Study of Pregnancy (MUSP),15,16 a study of women enrolled at the Mater Misericordiae Hospital in Brisbane, Australia, between 1981 and 1983. The cohort comprised a sample recruited at the first antenatal visit involving 7,223 consecutive women who subsequently gave birth to a live singleton baby. The cohort was followed up at 3–5 days, 6 months, 5 years, and 14 years after the birth. Of those, 6,665 provided information about breastfeeding at the 6-month follow-up. The present study comprises 4,502 participants who completed the questionnaire at the 14-year follow-up and for whom data were available about breastfeeding and other covariates measured between pregnancy and 14 years. Written informed consent from each mother was obtained at all phases of data collection. Ethics committees at the Mater Hospital and The University of Queensland approved each phase of the study.
Adolescent outcomes
Outcomes measured when the child was 14 years old included Achenbach subscales of mental health and problem behaviors. The Youth Self Report (YSR) 17 of the Child Behavior Check List (CBCL) 18 was used at the 14-year follow-up. The YSR is a self-completed questionnaire about behavior in the previous 6 months that has been designed for individuals 11–18 years old. It consists of 112 items assessing eight subscales including aggression, delinquency, withdrawal, anxiety/depression, somatic complaints, social problems, attention problems, and thought problems. The YSR has the same format as the CBCL, except that YSR items are worded in the first person. The problem items are scored 0 if the behavior is “not true,” 1 if the behavior is “sometimes or somewhat true,” and 2 if the behavior is “very true or often true.” For the purpose of this study, anxiety/depression (Cronbach's α=0.84), aggression (Cronbach's α=0.84), delinquency (Cronbach's α=0.71), attention problems (Cronbach's α=0.73), withdrawal problems (Cronbach's α=0.62), somatic complaints (Cronbach's α=0.70), social problems (Cronbach's α=0.61), and thought problems (Cronbach's α=0.70) as well as internalizing behavior, externalizing behavior, and total problems are considered as outcomes of interest. Higher outcome scores indicate increased symptoms or poorer mental health.
Breastfeeding
Information on the duration of breastfeeding was obtained from the mothers at the 6-month follow-up assessment. Duration of breastfeeding (full or partial) was recorded in six categories: not at all, ≤2 weeks, 3–6 weeks, 7 weeks–3 months, 4–6 months, and still breastfeeding. Because 50% of those reporting still breastfeeding responded to their questionnaire at 5–6 months, the latter two categories were combined into ≥4 months. The remaining four categories were combined into not breastfed and breastfed <4 months, to contrast the absence of breastfeeding with other categories and to maximize numbers in each group.
Other covariates
Maternal sociodemographic background, including age, education (did not complete high school; completed high school; and post-high school education), and maternal marital status, were assessed at the first clinic visit. At the first clinic visit, women were asked three questions that were concerned with whether the pregnancy was planned/wanted (I planned to get pregnant at this time; I meant to avoid pregnancy at this time; and I wanted to get pregnant at this time). Options were no=1, unsure=2, and yes=3. The three-item scale had good internal reliability (Cronbach's α=0.86). Using the individual's total score for these three questions we created a variable ranging from 3 to 9, with higher scores indicating unplanned/unwanted pregnancy.
Maternal anxiety and depression at the first clinic visit were assessed using the short form of the Delusions-Symptoms-States Inventory (DSSI). 19 The DSSI has been widely used, and its validity has been established 20 against the DSM-III. 21 In the MUSP the DSSI items were administered to the mother in the form of a self-report questionnaire, which included the seven-item anxiety (Cronbach's α=0.76) and depression (Cronbach's α=0.79) subscales.
At entry to the study, mothers were asked to indicate the number of cigarettes they smoked per day during the last week. The mothers were subsequently categorized as non-smoker and smoker. In addition, the frequency and quantity of maternal alcohol consumption were measured with the following questions: “How often do you drink alcohol?” and “How much alcohol do you usually drink at those times?” Mothers were then categorized as either abstainer or drinker.
Statistical analysis
For this analysis, we included 4,502 adolescents (51.6% males and 48.4% females) who provided answers to YSR questions at 14 years and for whom data were available about maternal-reported breastfeeding at the 6-month follow-up. Initially, chi-square tests were used to compare the study population at the baseline and the subsample present at the 14-year follow-up according to background sociodemographic characteristics and other covariates. A series of analysis of variance tests were used to examine mean symptoms of YSR mental health and problem behavior for each category of breastfeeding and other covariates in the study. In addition, unadjusted and adjusted linear regression models were conducted to examine the association between breastfeeding and the child's outcomes at 14 years, with no breastfeeding being the reference category. Variables with p<0.05 in univariate analyses were included in the multivariate models. In the first adjusted model the association were controlled for child's gender and mother's age and education. The second model included variables in Model 1 plus maternal reported unplanned pregnancy, anxiety, and depression. The final adjustment model included the covariates in Model 2 plus mother's smoking and alcohol consumption during pregnancy.
In order to test the validity of our findings, a series of sensitivity analyses were conducted. First, unadjusted and adjusted logistic regression models were used to estimate the risk of high level (top 10%) of mental health and problem behaviors for each category of breastfeeding. Second, unadjusted and adjusted linear regression analyses were repeated using maternal-reported CBCL subscales as the outcome variables. Finally, Student's t test was used to compare mental health and problem behaviors of the offspring in the breastfeeding versus not breastfeeding groups. All analyses were conducted using STATA version 11.
Results
In the present data 19.2% of mothers reported they did not breastfeed at all, 37.9% breastfed less than 4 months, and 42.9% breastfed 4 months or longer. The average age of adolescents was 13.9 (SD=0.3) years. Table 1 compares the original sample with the follow-up subsample at age 14 years according to maternal reported breastfeeding and their sociodemographic background. Children who were breastfed for at least 4 months were more likely to respond to the 14-year follow-up questionnaire. Participants' maternal age, education, smoking, anxiety, and depression during pregnancy were significantly associated with loss to follow-up at 14 years. Children whose mothers were younger than 20 years old, had a lower level of education, were smokers, or had anxiety or depression at the first antenatal visit were more likely to be lost at the 14-year follow-up. However, the data in Table 1 show that the differences between the original sample and the follow-up subsample are quite small.
Significance level for difference in lost to follow-up between categories.
Table 2 presents the association between breastfeeding and other covariates, on the one hand, and the child's mental health and problem behaviors at the 14-year follow-up, on the other. Children who were breastfed for at least 4 months reported fewer symptoms of anxiety/depression, social problems, attention problems, aggression, and delinquency at 14 years. Male participants when compared with female participants had higher symptoms of social problems, attention problems, and delinquency, whereas females were more likely to report anxiety/depression, withdrawal symptoms, and somatic or thought problems. Participants whose mothers were younger than 20 years at pregnancy were more likely to report symptoms of aggressive and delinquent behavior, and less educated mothers had children with more symptoms of social, attention, aggression, and delinquent problems. Children who were the outcome of an unplanned pregnancy were more likely to reports symptoms of mental health and problem behavior at 14 years. It is also noted that anxious or depressed mothers, or those who smoked cigarettes or drank alcohol while pregnant, were more likely to have a 14-year-old child with symptoms of mental health and problem behavior.
Data are mean (SD) values unless otherwise indicated. Higher scores represent poorer outcomes.
The level of significance was derived from analysis of variance or Student's t tests: *p<0.05, **p<0.01, ***p<0.001.
RE (SD), regression coefficient (SD), derived from linear regression models.
Unadjusted and multivariate associations between breastfeeding and the child's outcomes are presented in Table 3. Unadjusted linear regression analyses show that when no breastfeeding was considered the reference category, children who were breastfed for at least 4 months reported fewer symptoms of anxiety/depression, social or attention problems, and aggressive or delinquent behavior at 14 years. The associations remained unaltered when the child's gender and mother's age and education were included in the regression models (Model 1). Further adjustment for unplanned pregnancy and the mother's anxiety and depression at first clinic visit slightly attenuated the magnitude of associations between breastfeeding and participants' YSR subscales (Model 2), although the relationships remained significant. For example, regression coefficients for anxiety/depression, attention problems, and aggressive behavior were reduced by 16.3%, 10.4%, and 15.7%, respectively.
Data are regression coefficient (95% confidence interval) derived from linear regression. Model 1 was adjusted for the child's gender and mother's age and education at first clinic visit, Model 2 was adjusted for Model 1 plus unplanned pregnancy and mother's anxiety and depression at first clinic visit, and Model 3 was adjusted for Model 2 plus mother's smoking and alcohol use at first clinic visit.
The level of significance derived from analysis of variance or Student's t tests: *p<0.05, **p<0.01, ***p<0.001.
In the fully adjusted model breastfeeding showed a significant relationship with the child's social, attention, and aggression problems at 14 years (Model 3), with those who were breastfed for at least 4 months reporting better mental health and behavioral outcomes. However, the association between breastfeeding and offspring's anxiety/depression and delinquency was no longer statistically significant. Inclusion of mother's smoking and alcohol consumption in the multivariate model led to a further 9.3% and 18.6% reduction in the regression coefficients for the child's attention problem and aggressive behavior at 14 years, respectively.
Sensitivity analysis
Using the 90 percentile cutoff of each subscale of YSR, we divided the participants into two groups, with those above the cutoff considered the cases. The findings of logistic regression models were consistent with those presented in Table 3. In unadjusted analyses, children who were breastfed for at least 4 months were statistically significantly less likely to exhibit extreme symptoms of anxiety/depression, social problems, attention problems, and aggressive behavior at 14 years. Some 8.2% and 6.5% of the children who breastfed at least for 4 months reported high levels of attention and aggression problems, respectively, compared with 10.6% and 10.2% of those who were not breastfed at all. However, inclusion of other covariates in the logistic regression model led to the association for anxiety/depression and delinquency becoming non-significant. Additional analyses were conducted to examine the association between duration of breastfeeding and subscales of the Achenbach CBCL (maternal report) measured at the 14-year follow-up. The findings of new analyses were not materially different from those presented here. Furthermore, independent Student's t tests showed that any breastfeeding was associated with fewer symptoms of problem behaviors in children at 14 years (data are not shown).
Discussion
Using population-based information from a large cohort of mothers and children we examined the association between breastfeeding in the first 6 months after the child's birth and his or her mental health and problem behavior at 14 years. Our study found that breastfeeding less than 4 months or not breastfeeding at all as prospectively reported by mothers at 6 months after the child's birth predicted increased symptoms of mental health impairment and problem behaviors in children at 14 years. Our data suggest that at least part of the associations between breastfeeding and the child's mental health and problem behavior at 14 years is explained by confounding factors such as mother's mental health and substance use during pregnancy. After adjustment for confounding variables, breastfeeding continued to be associated with offspring's social, attention, and aggression problems at 14 years.
To our knowledge there has been limited research on the relationship between breastfeeding and the offspring's mental health and problem behavior in childhood and early adolescence.8–13 Our finding that a shorter duration of breastfeeding is associated with the child's attention problems is consistent with the results of Julvez et al. 12 Our data also confirm the findings of previous studies that suggested the relationship between breastfeeding and child conduct problems or delinquency is due to the effect of confounding.8,14 In addition, the present study is in agreement with the research of Fergusson and Woodward 9 that found no significant association between breastfeeding and offspring's anxiety and depression between 16 and 18 years. However, it contradicts a recent cohort study by Oddy et al. 13 that found association between breastfeeding and adolescent internalizing problems at 14 years. The discrepancy between the findings of the two studies might be due to the difference in length of breastfeeding (4 months in this study vs. 6 months in that by Oddy et al. 13 ) and measurement of the offspring's mental health. In this study the adolescent psychopathology was self-reported (YSR) by the participants, whereas Oddy et al. 13 used the maternal-report version of the Achenbach CBCL.
Our findings suggest that breastfeeding for at least 4 months is associated with fewer social, attention, and aggression problems in offspring compared with no breastfeeding at all. The additional analysis also confirms the positive impact of any breastfeeding versus not breastfeeding at all.
Mechanisms of association
One possible explanation for the association between breastfeeding and reduced social, attention, and aggression problems in children is that they are both correlated with other factors that may confound the associations observed here. In the present study, we controlled for a selected group of potential confounders such as maternal sociodemographic background, unplanned pregnancy, maternal mental health, and substance use. In our data the impact of breastfeeding on improved anxiety/depression and delinquent behaviors of the child was mainly due to the confounding, but the protective effect of breastfeeding on the child's social, attention, and aggression problems remained significant after adjustments. Although the present findings suggest an association between breastfeeding and long-term social, attention, and aggression problems of the child when allowance was made for a range of confounders, the possibility remains that the association found in this study arises from the effect of unobserved/unmeasured confounders.
A second possibility is that the impact of breastfeeding in the early stages of child development on that a child's long-term psychopathology is mediated by the child–mother relationship and interaction. 9 Research suggests that parental bonding and attachment are linked to better child psychological development, 22 including attention problems. 23 On the other hand, research has shown that longer duration of breastfeeding is associated with less child maltreatment perpetrated by the mother. 24 There is a need to investigate whether the child–mother relationship and the maltreatment of the child during the child's development explain the association between breastfeeding and the offspring's reduced social, attention, and aggression problems.
Limitations
The findings of this study should be interpreted in the light of a few limitations. The main limitation of this study is that it is an observational study, and there remains a possibility that many unmeasured variables are likely correlated with both breastfeeding and the child's mental well-being and might explain the observed associations. Other potential confounding variables include birth history, type of delivery, length of gestation, birth weight, maternal body mass index, and pre-eclampsia.
Second, there was sizeable reduction in the sample between the assessment of breastfeeding at the child's 6-month and 14-year follow-ups. Of the 6,665 subjects for whom we collected information related to breastfeeding at the 6-month follow-up, only 73.0% responded to the 14-year phase. Over the 14-year follow-up, children whose mothers were younger than 20 years, less educated, or anxious, depressed, or smoking cigarettes during pregnancy were more likely to be lost to follow-up (p<0.001). Loss to follow-up was also more common among children who were not breastfed compared with those who were breastfed less than 4 months and longer (40.1%, 34.4%, and 26.4%, respectively). Loss to follow-up may influence our results in two possible ways. If the association between breastfeeding and the child's outcomes in those lost to follow-up was stronger than in the study group, our findings would underestimate the true association. The main threat to the validity of our findings is if the association we have observed is not evident or is in the opposite direction among those lost to follow-up. Given the likely causal pathways and the positive association reported by other authors, this latter possibility seems very unlikely.
A third limitation is that, in this study, we used self-reported maternal smoking and alcohol consumption during pregnancy, and the child's symptoms of psychopathology were assessed by the Achenbach YSR. It would have been ideal if nicotine levels were measured at the baseline. The YSR is a well-validated measure of adolescents' mental health and problem behavior. In addition, our sensitivity analysis using CBCL's maternal report produced the same results as YSR. However, the YSR and CBCL do not represent a clinical diagnosis of mental illnesses but rather measure the symptoms of impaired mental health and problem behaviors.
Conclusions
Along with existing evidence on health benefits of breastfeeding our data suggest that breastfeeding in the early stages of child development has a long-term protective effect on the mental health and behavior of the child. If the observed relationships are independent of other factors, effective programs that encourage breastfeeding can help improve the offspring's social, attention, and aggression problems by at least 9.0% later in their life. There is a need for further research to test the robustness of our findings by measurement of other potential confounding variables, and also to investigate possible pathways that can explain the association between a shorter duration of breastfeeding and the child's mental health and problem behavior.
Footnotes
Acknowledgments
Over time the study has been funded primarily by the National Health and Medical Research Council. We thank all participants in the study, the MUSP data collection team, and Greg Shuttlewood, University of Queensland, who has helped to manage the data for the MUSP.
Disclosure Statement
No competing financial interests exist.
