Infant Breastfeeding and Behavioral Disorders in School-Age Children

Abstract

Objective:

To explore the effects of breastfeeding on behavioral disorders of school-age children.

Materials and Methods:

Totally 1,979 children of 6–11 years old from three primary schools in Xiamen, China, were assessed and included for further analysis. The Pearson chi-square test and multivariable logistic regression model were used to analyze the effects of breastfeeding on internalizing behaviors such as depression, withdrawn, and somatic complaints, and externalizing behaviors such as aggression and rule-breaking behavior.

Results:

The Pearson chi-square test revealed that the percentages in internalizing behavioral problems (χ² = 21.693, p < 0.001), depression (χ² = 12.713, p = 0.002), and somatic complains (χ² = 12.850, p = 0.002) were significantly lower with the decrease of the duration of breastfeeding. However, there were no statistically significant differences in externalizing behavioral problems. After adjusting the potential covariates, children who were breastfed for >6 months were significantly associated with the reduced risk of internalizing behavioral problems (Odds ratio = 0.446, 95%CI: 0.228–0.873) and depression (Odds ratio = 0.452, 95% CI: 0.225–0.906) compared with those who were never breastfed, whereas differences were not found in externalizing behavioral problems.

Conclusion:

Increased duration of breastfeeding (≥6 months) could help lower internalizing behavioral problems, particularly depression, in school-age children. Breastfeeding with longer duration will play an important role to prevent and reduce children's internalizing behavioral disorders.

Introduction

Many health benefits are associated with breastfeeding in children, such as a reduction in the risk of acute otitis media, nonspecific gastroenteritis, severe lower respiratory tract infections, atopic dermatitis, asthma (young children), obesity, type 1 and 2 diabetes, childhood leukemia, and so on.¹ In the past two decades, scholars have increasingly studied the association between breastfeeding and children's behavior problems. However, there have been inconsistent findings. Some studies have found that breastfeeding is associated with children's behavioral problems. For example, a large cohort study of Irish children at 9 months of age showed a positive effect of any breastfeeding on gross motor, fine motor, problem solving, and personal–social skills, and these remained after adjustment for a range of confounding variables.² Yorifuji observed a dose–response relationship between breastfeeding status and inability to perform age-appropriate behaviors in Japanese children at age 2.5 and 5.5 years.³ Subin⁴ found that a lack of breastfeeding was associated with increased overall behavioral problems in Korean children, whereas others with the same aim have not observed any association.^5,6 Meanwhile, most of the previous studies focused on the effects of breastfeeding on overall behavioral problems and tend to focus on infancy and early childhood.

The purpose of this study is to evaluate whether breastfeeding is related to a lower risk of internalizing or externalizing behavioral disorders in school-age children through a large number of data, which, in turn, may encourage proper breastfeeding.

Materials and Methods

Study sample

Participants in this study were recruited from three primary schools in Xiamen City, Fujian Province, China. A letter inviting participation in the study was sent to first to fourth grade children (aged 6–11 years old) and their parents. After informed consent of the parents, a total of 2,443 children were invited to participate in child behavior assessment and questionnaire survey. The inclusion criteria for selecting subjects for data analyses were as follows: (a) completed both behavior assessment and valid questionnaires, (b) information on breastfeeding was complete, (c) children were born full of moon (≥37 weeks), (d) no reported psychoses or neurologic diseases since birth, and (e) birth weight was >2,500 g. This study was approved by the Ethics Committee of Children's Hospital of Fudan University Xiamen Branch.

Child behavior assessment

The parents were invited to finish a Child Behavior Checklist (CBCL) (the version for 4–18 years of age) scale to assess child potential behavior problems. The CBCL composes of 113 items rated on a three-step response scale ranging from 0 (absent) to 2 (very often present), which consists of nine syndrome scales: depression, withdrawn, somatic complaints, rule-breaking behavior, aggression, attention problems, obsessive behavior, social problems, and immaturity (boy)/sexual problems (girl), and two composite scales: internalizing behavioral problems (sum of the scores on the depression, withdrawn, and somatic complaints scales) and externalizing behavioral problems (sum of the scores on the aggression and rule-breaking behavior). Through CBCL survey, a raw score would yield to measure the degree of problems on the specified syndrome and composite scales, with higher scores corresponding to more problems.

Questionnaire survey

Breastfeeding and the possible risk factors of behavioral disorders were collected through the General Status of Children Questionnaire that was self-designed. The questionnaire included questions such as breastfeeding (breastfed or not, breastfeeding duration), child and neonatal factors (gender, birth weight, birth age and medical history, etc.), parental factors (parent education background, alcohol and tobacco consumption, family income, upbringing style, etc.), and prenatal factors (X-ray exposure during pregnancy, maternal alcohol use and smoking during pregnancy, maternal medication use during pregnancy, delivery method, etc.).

Statistical analysis

Statistical analyses were performed with SPSS version 17.0. First, differences between the children included and excluded in the analysis were estimated with Pearson chi-square test. Second, T-scores for the specific syndromes and composite scales of CBCL were standardized to a mean = 50 and SD = 10, and dichotomized into two groups for each syndrome: abnormal (T-score ≥60) and normal (T-score <60). Next, Pearson chi-square test was used to assess the differences of various duration of breastfeeding in each syndrome and composite scales. Finally, logistic regression analysis model was used for multifactors analysis so as to further explore the association between breastfeeding and children's behavioral problems. Thirteen independent variables were analyzed in the model: age (years), gender (0 = female, 1 = male), educational attainment of children's mother (0 = ≤ primary school, 1 = middle school, 2 = high school, 3 = technical school, 4 = ≥ college/university), educational attainment of children's father (0 = ≤ primary school, 1 = middle school, 2 = high school, 3 = technical school, 4 = ≥ college/university), family income (0 = 5,000 yuan/month, 1 = 5,000 yuan/month～, 2 = 10,000 yuan/month～, 3 = 15,000 yuan/month～, 4 = 20,000 yuan/month～), parents upbringing style (0 = education mainly, 1 = blame mainly), delivery method (0 = vaginal delivery, 1 = abdominal delivery), passive smoking (0 = no, 1 = yes), history of poor pregnancy of mother (0 = no, 1 = yes), maternal medicine use during pregnancy (0 = no, 1 = yes), maternal alcohol drinking during pregnancy (0 = no, 1 = yes), X-ray exposure during pregnancy (0 = no, 1 = yes), and duration of breastfeeding (0 = never breastfed, 1 = breastfed <6 months, 2 = breastfed ≥6 months). As a study variable, duration of breastfeeding was entered into the model forcibly, and the other variables were screened by backward regression method with p < 0.15 as variable inclusion and exclusion criteria as potential confounds.

Result

Sociodemographic characteristics of participants

Among 2,443 subjects who were invited to participate in this study, 2,257 had completed both behavior assessment and valid questionnaires. Of these subjects, 278 were excluded from final analysis for the following reasons: preterm birth (182 children), low birth weight (81 children), no complete information about breastfeeding (14 children), and history of epilepsy (1 child). Overall, 1,979 children were eligible for data analyses.

Table 1 compares characteristics for participants who entered the data analyses with those excluded. There were no significant differences between the two groups, which suggested that excluding some participants did not result in confounding in this study.

Table 1.

Comparison of Characteristics of Participants Included in the Data Analyses and Those Excluded

		Participants		Nonparticipants
Characteristics	Category	n	%	n	%	χ ²	p
Age (years old)	6	183	9.25	32	11.51	4.832	0.437
	7	274	13.85	43	15.47
	8	481	24.31	66	23.74
	9	503	25.42	72	25.90
	10	337	17.03	35	12.59
	11	201	10.16	30	10.79
Gender	Male	910	45.98	130	46.76	0.060	0.807
Gender	Female	1069	54.02	148	53.24	0.060	0.807
Educational attainment of mothers	≤Primary school	299	15.11	39	14.03	5.449	0.244
	Middle school	685	34.61	80	28.78
	High school	472	23.85	75	26.98
	Technical school	284	14.35	49	17.63
	≥College/university	239	12.08	35	12.59
Educational attainment of fathers	≤Primary school	111	5.61	15	5.40	3.355	0.500
	Middle school	603	30.47	71	25.54
	High school	633	31.99	92	33.09
	Technical school	265	13.39	41	14.75
	≥College/university	367	18.54	59	21.22
Family income (Yuan/month)	<5,000	214	10.81	30	10.79	7.000	0.136
	5,000～	527	26.63	89	32.01
	10,000～	594	30.02	67	24.10
	15,000～	421	21.27	66	23.74
	≥20,000	223	11.27	26	9.35

n, the number of children in this category; %, the proportion of corresponding children among participants/nonparticipants in each category.

Among these 1,979 subjects, 1,921(97.07%) children were breastfed (either partially or fully breastfed) and 58 (2.93%) were not breastfed. Reported breastfeeding duration was 8.30 ± 3.12 months (range 0–21 months). Duration was categorized into three levels: never breastfed (2.93%), breastfed <6 months (16.57%), and ≥6 months (80.50%).

Behavioral outcomes

As is given in Table 2, the percentages in internalizing behavioral problems, depression, somatic complains, and withdrawn were lower with the decrease of the duration of breastfeeding, and significant group differences were found in internalizing behavioral problems (χ² = 21.693, p < 0.001), depression (χ² = 12.713, p = 0.002), and somatic complains (χ² = 12.850, p = 0.002). The results also revealed significant group difference for aggression (χ² = 9.966, p = 0.007). However, there were no statistically significant differences in externalizing behavioral problems and rule-breaking behavior.

Table 2.

Differences of Various Duration of Breastfeeding in Children's Behavioral Problems

Behavioral problems	Never breastfed (n = 58), %	Breastfed <6 months (n = 328), %	Breastfed ≥6 months (n = 1,593), %	χ ²	p
Internalizing behavioral disorders	20.69	18.60	10.36	21.693	<0.001
Depression	18.97	16.16	10.23	12.713	0.002
Withdrawn	18.97	14.63	11.68	4.583	0.101
Somatic complaints	15.52	15.24	9.10	12.850	0.002
Externalizing behavioral disorders	10.34	15.24	12.18	2.599	0.273
Rule-breaking behavior	6.90	8.54	9.98	1.171	0.557
Aggression	13.79	18.60	12.12	9.966	0.007

Significant results are highlighted in bold.

n, the number of children in this category.

Table 3 presents the results of logistic regression analyses. Total of nine covariates were included in the seven models. Educational attainment of mothers and parents and upbringing style were shown in all models, which indicated that children's behavioral problems were significantly associated with family environment. Maternal alcohol drinking and maternal medicine use during pregnancy were also included in five models, which suggested the risk of exposure to harmful factors during pregnancy. Passive smoking was a key factor for increasing risk of the behavioral problems of somatic complaints, externalizing behavioral problems, aggression, and rule-breaking behavior. Children's gender, age, and history of poor pregnancy of mothers were also included in some models. More importantly, after adjusted the potential covariates, children who were breastfed >6 months were significantly associated with the reduced risk of internalizing behavioral problems (Odds ratio = 0.446, 95%CI = 0.228–0.873) and depression (Odds ratio = 0.452, 95%CI = 0.225–0.906) compared with those who were never breastfed, whereas differences were not found in children who breastfed <6 months.

Table 3.

Results of Logistic Regression Model

Dependent variables	Adjusted odds ratio (95%CI)	p	Other variables in the model
Internalizing behavioral disorders
Never breastfed	1 (reference)		Gender (p = 0.145), educational attainment of mothers (p = 0.029), parents upbringing style^a (p < 0.001), maternal alcohol drinking durings pregnancy (p = 0.014), maternal medicine use during pregnancy^b (p = 0.129)
Breastfed <6 months	0.702 (0.425–1.780)	0.803
Breastfed ≥6 months	0.446 (0.228–0.873)	0.018
Withdrawn
Never breastfed	1 (reference)		Age (p = 0.061), educational attainment of mothers (p = 0.009), parents upbringing style (p = 0.007)
Breastfed <6 months	0.927 (0.439–1.959)	0.844
Breastfed ≥6 months	0.597 (0.299–1.189)	0.142
Depression
Never breastfed	1 (reference)		Educational attainment of mothers (p = 0.003), maternal medicine use during pregnancy (p = 0.042), parents upbringing style (p < 0.001), maternal alcohol drinking during pregnancy (p = 0.056)
Breastfed <6 months	0.789 (0.374–1.665)	0.534
Breastfed ≥6 months	0.452 (0.225–0.906)	0.025
Somatic complaints
Never breastfed	1 (reference)		Gender (p = 0.003), educational attainment of mothers (p = 0.065), parents upbringing style (p = 0.002), passive smoking^c (p = 0.085)
Breastfed <6 months	0.946 (0.428–2.093)	0.892
Breastfed ≥6 months	0.569 (0.270–1.199)	0.138
Externalizing behavioral disorders
Never breastfed	1 (reference)		Educational attainment of mothers (p < 0.001), maternal medicine use during pregnancy (p < 0.001), parents upbringing style (p < 0.001), passive smoking (p = 0.032), maternal alcohol drinking during pregnancy (p = 0.054)
Breastfed <6 months	1.613 (0.391–1.771)	0.634
Breastfed ≥6 months	1.203 (0.498–2.903)	0.681
Aggression
Never breastfed	1 (reference)		Educational attainment of mothers (p = 0.020), maternal medicine use during pregnancy (p = <0.001), parents upbringing style (p < 0.001), history of poor pregnancy of mother^d (p = 0.052), passive smoking (p = 0.069), maternal alcohol drinking during pregnancy (p = 0.012)
Breastfed <6 months	1.378 (0.606–3.132)	0.444
Breastfed ≥6 months	0.857 (0.394–1.868)	0.698
Rule-breaking behavior
Never breastfed	1 (reference)		Gender (p = 0.002), educational attainment of mothers (p = 0.115), maternal medicine use during pregnancy (p = 0.014), parents upbringing style (p = 0.022), maternal alcohol drinking during pregnancy (p = 0.027), passive smoking (p = 0.054)
Breastfed <6 months	1.438 (0.474–4.365)	0.521
Breastfed ≥6 months	1.571 (0.554–4.456)	0.396

Significant results are highlighted in bold.

No blaming the child or blaming the child ≤1 times every week identified as “education mainly,” while blaming the child ≥2 times every week identified as “blame mainly.”

Including unprescribed or prescribed antiviral and antibiotic medicine.

One or both parents smoke in the home.

Including abortion, premature birth, stillbirth.

Discussion

Externalizing behaviors describe a range of disruptive and dysregulated behaviors such as hyperactivity, aggression, and delinquency. In contrast, internalizing behaviors are indicative of inwardly directed distress related to depression and withdrawn.⁷ Externalizing and internalizing behaviors in children are key health issues in childhood and adolescence. This study explored whether breastfeeding is related to a lower risk of internalizing or externalizing behavioral disorders in children of 6–11 years old. In our unadjusted analyses, we observed that the percentages of internalizing behavioral problems and its three subscales were lower with the increase of the duration of breastfeeding, whereas these associations were not found in externalizing behavioral problems and its two subscales. After adjusting for the potential confounding factors, children who were breastfed for >6 months were significantly associated with the reduced risk of internalizing behavioral problems, particularly depression, compared with those who were never breastfed, whereas differences were not found in externalizing behavioral problems.

Previous studies on the association between breastfeeding and behavioral disorders tended to focus on infancy and early childhood and limited in older age groups. Positive effects of breastfeeding at infancy and early childhood included well gross motor and fine motor,² better motor maturity and alertness during social interactions,⁸ fewer abnormal reflexes, signs of depression, and withdrawal.⁹ In this study, the included population was the children of 6–11 years age in primary schools, and the results showed children who were breastfed for >6 months exhibited lower internalizing behavioral problems. Our result was consistent with some previous studies, which focus on school-age children. A study of Hong Kong Chinese children aged 11–13 years showed that breastfeeding for any length of time or exclusive breastfeeding for <3 months was associated with poorer behavior (higher Rutter z-score (0.10, 95% CI 0.05–0.16)) and lower self-esteem (−0.09, 95% CI −0.14 to −0.04).¹⁰ Oddy team followed the live births for 14 years and found that breastfeeding for <6 months compared with that for 6 months or longer was an independent predictor of mental health problems through childhood and into adolescence.¹¹ These outcomes indicated a long-term effect of breastfeeding on behavioral problems in school-age children.

In this study, we explore the effects of breastfeeding on the specific syndromes of behavioral disorders. Consistent with previous studies by Liu¹² and Oddy,¹¹ we found a significant association between longer breastfeeding duration and internalizing behavioral problems, particularly depression. It was estimated that about 20% of children and adolescents had been affected by childhood internalizing disorders.¹³ Internalizing behavioral problems have become key health issues in childhood and adolescence. Therefore, it is important to indentify breastfeeding as a protective factor for children's internalizing behavioral disorders. Breast milk is the perfect nutrition for infants, a result of millions of years of evolution, finely attuning it to the requirements of the infant. It contains a variety of nutrients that play an important role in the brain development of infants and children, which, in turn, promote the psychological and neurobehavioral development of children. Docosahexaenoic acid omega-3 fats and eicosapentaenoic acid fats in breast milk may reduce the risk for affective disorders, including depression and bipolar disorders.^14,15 What is more, indirect benefit for a child's mental health from breastfeeding will be obtained through enhancing the mother–infant bonding process through active talking, eye contact, and skin-to-skin touch. Dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis has been found to be related to internalizing symptoms in children.¹⁶ The HPA axis regulates cortisol production and the organism's capacity to respond to stressors. Internalizing behavioral disorders had a negative association between cortisol increase (β = −0.199, p < 0.05),¹⁷ and almost continuous skin-to-skin contact from mother would decrease infants' cortisol reactivity.¹⁸

It was indicated that prenatal risk and HPA functioning may, in part, be mechanisms of genetic and environmental influences for internalizing but not for externalizing behavioral problems during early childhood.¹⁹ In our study, the result also revealed no association between externalizing behavior disorders in school-age children.

There are several limitations in this study. First, although maternal recall of breastfeeding duration is relatively accurate,²⁰ recall bias may be existed due to the use of retrospective data in this study. Second, we did not obtain information on breastfeeding patterns (exclusive, predominant, or partial) and classified breastfeeding only according to duration, which led to the inability to evaluate the differences of various breastfeeding patterns. Furthermore, backward regression method was used to screen variables in logistic model in this study. One of the weaknesses of this method is that the coefficient tested for significance in a stepwise algorithm evaluates only the relationship between the potential confounders and the outcome, but ignores the relationship between the potential confounders and the exposure, which may result in the inclusion of variables that were not confounding or omit variables that were confounding.²¹ Therefore a larger and long-term epidemiological study should be conducted for further study to explore the association between breastfeeding and internalizing or externalizing behavioral disorders of school-age children.

Conclusions

Our findings indicated that increased duration of breastfeeding (≥6 months) could help lower internalizing behavioral problems, particularly depression in school-age children, which provide strong evidence of long-term protective effect of prolonged breastfeeding with regard to children's internalizing behavioral problems.

Footnotes

Acknowledgment

This study was supported by Project of Xiamen Science and Technology Bureau, Fujian Province in China (grant no.: 3502Z20164071).

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