The Possible Effects of Breastfeeding on Infant Development at 3 Months: A Case

Abstract

Objective:

To examine the influence of exclusive breastfeeding on infant development among 3-month-old infants in a Chinese population.

Methods:

Mothers and their 3-month-old infants were recruited from four maternal and child health hospitals from April 2018 to March 2019. Based on the infants' feeding patterns, the mother-infant dyads were divided into two groups: exclusive breastfeeding and formula feeding groups. Infant development was evaluated using the Chinese version of the Ages and Stages Questionnaires, 3rd edition (ASQ-C), and maternal depression, parenting confidence, and infant temperament were also assessed using the relevant scales/questionnaires. Multivariate logistic regression analysis was conducted to explore the effects of feeding patterns on infant development at 3 months.

Results:

The data from 417 mother-infant dyads were analyzed. For the breastfeeding group and formula feeding group, the risk of developmental delay measured by the ASQ-C was 4.1% (10/244) and 9.3% (16/173) respectively for the communication domain; 5.7% (14/244) and 8.1% (14/173) for problem-solving domain and 6.2% (15/244) and 12.1% (21/173) for personal-social domain, respectively. Compared with exclusive breastfeeding, formula feeding was a risk factor for delayed development of communication (adjusted odd ratio [aOR] = 2.60, 95% confidence interval [CI] = 1.42–4.75) problem-solving (aOR = 1.91, 95% CI = 1.06–3.45), and personal-social skills (aOR = 1.96, 95% CI = 1.12–3.42).

Conclusions:

Exclusive breastfeeding is important for infant communication, problem solving, and social interaction at the age of 3 months. Formula-fed infants may be at a higher risk of developmental delay than exclusively breast-fed infants. It is necessary to encourage mothers to establish and continuous breastfeeding.

Introduction

Early childhood is a critical period for the growth and development of a child. From birth to age three, every system develops rapidly, especially the brain.¹ The developmental progress of a child is jointly influenced by hereditary factors, environmental factors, and living experience. Good nutrition during the first 2 years of life provides a strong foundation for the physical and mental development of an infant.² Breastfeeding is accepted as the best way to provide ideal nutrition that meets the developmental needs of infants.³ Exploring the potential relationship between breastfeeding and early infant development can provide theoretical evidence to underpin the study of childhood development.

Numerous studies have shown the benefits of breastfeeding for infant.^4,5 Exclusively breast-fed infants have a lower mortality rate and are at a lower risk of infection-related death.⁶ Breastfeeding has been associated with a reduction in diarrhea,⁷ acute otitis media,⁸ and a reduced risk of infant hospital admissions for respiratory infections as well.⁹ Some evidence has shown that breastfeeding in infancy has been shown to reduce the risk of type 2 diabetes¹⁰ and cardiovascular diseases in adulthood.¹¹ There is growing evidence that breastfeeding has been emphasized as a protective factor in the growth and development of infants.¹² As early as 1929, the relationship between breastfeeding and childhood development was studied by Hoefer and Hardy, who found a positive relationship between breastfeeding and intelligence among children aged 7–13 years.¹³ Many subsequent studies have explored the relationship between breastfeeding and childhood development. Quigley et al. suggested that breast-fed children would be 1–6 months ahead in cognitive development than formula-fed children at the age of 5 years.¹⁴ In a survey of children aged 0–5 years in the United States, Dee et al. found that breastfeeding may protect children against delays in language and motor skill development; the survey also showed that breastfeeding for 3–5.9 months may foster a stronger relationship between the mother and the child.¹⁵ Grace et al. also reported similar findings that infants who were breastfed for >6 months had better motor development in late childhood and adolescence (10, 14, and 17 years old).¹⁶ The results of many longitudinal studies on larger populations suggest that breastfeeding is beneficial to the development of language,¹⁵ cognitive,^15,17 and motor skills.¹⁶

However, in some studies, the link between breastfeeding and childhood development was no longer significant after adjusting for sociodemographic confounders. Taylor suggested that the characteristics of children should be taken into account, as the observed protective effect of breastfeeding on the cognitive development of children may be an artifact of sociodemographic confounding rather than a true association.¹⁸ Silva et al. found that the link between developmental outcomes and breastfeeding is actually attributable to maternal educational level and social status.¹⁹ A review by Der et al. showed that the significant association between breastfeeding and cognitive development is overestimated by the confounding effect of maternal intelligence and environment.²⁰ We have reason to believe that the influence of socioeconomic status (such as parental income and educational background) is the main confounding factor influencing the association between breastfeeding and childhood development.

The outcome of an ideal observational study that explores the association between breastfeeding and developmental outcomes depends on how the confounding effects are minimized. The confounding factors associated with both exposure (feeding pattern) and outcome (developmental outcomes) are not associated with causality.²¹ In many studies, parenting style was reported to have an impact on the development of cognition and intelligence in children as well.^21,22 Mothers who choose to breastfeed their babies may be inclined to adopt a positive nurturing relationship with their babies. The temperament, personal emotional expression, and activity level of an infant²³ may influence communication with the parents and affect the development of social learning skills.²⁴ Mothers with depressive symptoms may not communicate and make eye contact with their babies; this may limit maternal caregiving behavior and influence the process of breastfeeding and the interaction and communication skills of the child.^25,26 Parenting efficacy may mediate the quality of parental caregiving and affect the child's behavior and developmental outcomes.^27,28 Therefore, it is necessary to control sociodemographic factors and parenting factors (such as infant temperament, maternal emotion, and parenting efficacy) on the relationship between feeding pattern and developmental outcomes.

Presently, many studies on the relationship between breastfeeding and infant development can be found in the available literature, but the findings of these studies are controversial^21,29; therefore, the effect of breastfeeding on the development of cognition and intelligence in infants cannot not be ascertained. Most of the studies were conducted to determine the dose–response relationship and long-term effect of breastfeeding on childhood development by adopting a longitudinal study design, in which the participants were followed up for 1 year or more.³⁰ However, infant development may be influenced by some socioeconomic factors; this may have contributed to the differences in their results. Girard et al. suggested that the benefits of breastfeeding are apparent during early childhood but not when children get older.¹⁷ However, researches involving children younger than 1 year is limited. Hart reported that the neurobehavioral functioning of 1-week-old infants is differentiated by feeding patterns.³¹ Vestergaard et al. found that exclusive breastfeeding benefited developmental milestones (i.e., crawling, pincer grip, and polysyllable babbling) at the age of 8 months.³² McCrory and Murray found that breastfeeding has a positive effect on gross motor development (odds ratio [OR] = 1.59, 95% confidence interval [CI] = 1.42–1.79), fine motor development (OR = 1.32, 95% CI = 1.14–1.53), problem-solving skills (OR = 1.38, 95% CI = 1.23–1.54), and personal-social skills (OR = 1.38, 95% CI = 1.23–1.54) of infants at the age of 9 months.³³ These findings show that it is necessary to explore the association between breastfeeding and development in early infancy.

We hypothesized that breast-fed infants have a lower risk of developmental delay than formula-fed infants. Accordingly, the aim of this study was to explore the relationship between exclusive breastfeeding at 3 months and infant communication, gross motor skills, fine motor skills, problem-solving, and personal-social development in a Chinese population while controlling for the confounding effects of sociodemographic factors, infant temperament, and mother's emotional and parenting confidence.

Methods

Participants

This study was a part of a multicenter cohort study of mother-infant interaction. The study was approved by the Institutional Review Board (Approval No. 2018A202) and the Ethics Review Committee of the National Center for Women and Children's Health, Chinese Center for Disease Control and Prevention (Approval No. of Ethics Committee: FY2017–2018). The mothers and their 3-month-old infants were recruited from four city-level Maternal and Child Health Hospitals in Chongqing, Tsingtao, Maanshan and Liuzhou from April 2018 to March 2019. All mothers provided written informed consent. The inclusion criteria were (1) 3 months old (±7 days); (2) gestational age ≥37 weeks; (3) birth weight ≥2,500 g; (4) infant and mother having no serious illnesses or chronic health problems; and (5) infants who were exclusively breastfed or wholly formula-fed at 3 months.

Exposures

In this study, exclusive breastfeeding was defined as receiving only breast milk and nothing else (except for medicines and vitamins) over the last 24 hours, and breast milk intake accounted for >90% of infant feeding during the first 3 months after birth. Wholly formula feeding was defined as no breastfeeding in the past 24 hours, and breastfeeding accounting for <10% of the infants' total food intake during the first 3 months after birth. Based on the self-reported information the mothers provided regarding feeding patterns, the mother-infant dyads were categorized into groups: 244 mother-infant dyads were in the exclusive breastfeeding group and 173 dyads were in the wholly formula feeding group.

Infant development outcome

Infant development was assessed by using the Chinese version of the Ages and Stages Questionnaires, 3rd edition (ASQ-C).³⁴ The ASQ-C is a parent-reported development screening tool for children aged 1–66 months. The questionnaire for each age group has 30 items covering five domains: communication, gross motor, fine motor, problem-solving, and personal-social domains.³⁵ Every item has three answers: “yes,” “sometimes,” and “not yet,” which can be converted to 10, 5, and 0 points, respectively. All items in each domain are summed to obtain the total points. Based on the scores in each domain, infant development outcomes are categorized into three groups: “risk of delay,” “suspected risk of delay,” and “normal.”³⁶ For the Chinese version, the Cronbach's α coefficient is 0.8, test-retest reliability is 0.8, sensitivity is 87.5%, and specificity is 84.5% (Ref.³⁴).

Confounding factors

In this study, infant and maternal sociodemographic factors, parenting factors, and psychological characteristics were considered confounding factors. Sociodemographic factors included infant's gender, infant's ethnicity, mode of delivery, mother's age and educational level, one-child family, family structure, family income, and location. Parenting factors and psychological factors included main caregiver, feeding done by mother, parenting confidence, maternal depression, and infant temperament, which were measured using scales as follows:

Maternal depression was measured using the Edinburgh Postnatal Depression Scale (EPDS).^37,38 The EPDS is a 4-point Likert scale with 10 items. The items are scored 0–3 points based on symptom severity, which range from “No” to “Very severe.” Some items are reversed questions. The scores of all items are summed to obtain the total points. Higher scores indicate more serious depression.³⁹ The Cronbach's α coefficient for the EPDS is 0.79, the split-half reliability is 0.76, and test-retest reliability is 0.85 (Ref.⁴⁰).

Parenting confidence was assessed with the Karitane Parenting Confidence Scale (KPCS).⁴¹ KPCS is a 15-item scale used to assess the perceived self-efficacy of parents with infants aged 0–12 months. Items are assessed on a 4-point scale from 0 (almost impossible) to 3 (frequently), and some are reversed questions. A total score of <40 points indicates “lack of parental confidence.”⁴² The Cronbach's α coefficient for the KPCS is 0.81, test-retest consistency is 0.88, sensitivity is 86%, and specificity is 89% (Ref.⁴¹).

Infant temperament was measured with the Early Infancy Temperament Questionnaire (EITQ).⁴³ The EITQ is a parent-reported temperament scale for 1- to 4-month-old infants. It has 76 questions, and each item has 6-point Likert ratings. Infant behaviors are categorized into nine temperament dimensions (including Adaptability, Approach, Rhythmicity, Intensity, Mood, Activity level, Persistence, and Distractibility)⁴⁴ and five types (easy, difficult, intermediate-easy, intermediate-difficult, and slow-to-warm-up types).⁴⁵ The Cronbach's α coefficient for the EITQ is 0.42–0.76, and test-retest reliability is 0.43–0.87 (Ref.⁴³).

Statistical analyses

Data were entered into EpiData 3.1 and analyzed with SAS 9.4. The sociodemographic, parenting, and psychological characteristics of the mother-infant dyads were described. Bivariate analysis was used to compare the sociodemographic factors, parenting, and psychological characteristics between the two feeding pattern groups; the Chi-squared test was used for categorical variables and t-test or Wilcoxon rank-sum test was used for continuous variables. Multivariate logistic regression analysis was conducted using three models (all variables met proportional odds assumption) to explore the association between feeding pattern and infant development. The outcomes of the five ASQ development domains were used as the dependent variables (risk of delay = 2, suspected risk of delay = 1, and normal = 0), whereas feeding patterns were used as the independent variables (exclusive breastfeeding = 1, formula feeding = 0). Model 1: No variables were adjusted. Model 2: Sociodemographic factors, including infant's gender, ethnicity, mode of delivery, mother's age, maternal educational level, family structure, family income, one-child family, and location, were adjusted. Model 3: In addition to the factors in Model 2, parenting and psychological characteristics, including main caregiver, feeding done by mother, maternal depression, maternal parental confidence, and infant temperament, were adjusted. Binary variables (such as gender, mode of delivery), ordered category variables (such as maternal educational level, family income), and continuous variables (such as mother's age, depression score) were entered into the model in a raw form, whereas unordered categorical variables (such as family structure, location, and infant temperament type) were converted into dummy variables. No variables were found to be collinear, and p < 0.05 was considered significant. Both unadjusted and aORs and 95% CIs were calculated.

Results

Sociodemographic characteristics

Survey invitations were sent out to 421 people and all responded. Proportions of missing data were <10% and four questionnaires were removed. The rate of completion was 99.1%. The response rate was about 80% in the breastfeeding group (∼40 responses for every 50 invitations sent) and 85% in the formula feeding group (∼43 responses for every 50 invitations sent). Four hundred and seventeen infants aged 3 months old and their mothers were assessed. Sixty-five dyads were from Qingdao, 117 were from Chongqing, 119 from Liuzhou, and 116 from Maanshan; 244 (58.5%) of the infants were exclusively breastfed and 173 (41.5%) were wholly formula-fed. Two hundred twenty-three (53.5%) of the infants were boys and 151 (36.4%) were from one-child families. The mean age of the mothers was 30.4 ± 4.5 years, and 69.8% of the mothers had college-level education or higher. More than half (56.1%) of the infants were from stem families, whereas 37.9% were from nuclear families. More than 60% of the families earned a monthly income of over $699 per-capita. There were no significant differences between the exclusive breastfeeding group and the formula feeding group regarding gender, ethnicity, one-child family, mother's age, maternal education level, family structure, and family income.

Parenting characteristics and psychological characteristics of mothers and infants

The mean EPDS score of the mothers was 10.22 ± 3.80, whereas the mean KPCS score of mothers was 40.06 ± 4.14. Up to 50% of the infants had an easy type of temperament (Table 1). In the exclusive breastfeeding group, only two mothers were not the child's main caregiver and did not feed the infant themselves. In the formula feeding group, 32.3% of the mothers did not do all the feeding by themselves, whereas 9.3% of the mothers were not the child's main caregiver. There were no significant differences between the maternal depression scores of the two groups (p = 0.194). The results of the analysis of infant temperament types (p < 0.001), main caregiver (p < 0.001) and feeding done by mother (p < 0.001), and maternal confidence scores (p = 0.041) were significantly different between the two groups (Table 1).

Table 1.

Comparison of the Characteristics of Mother-Infant Dyads in Different Feeding Pattern Groups

	Total (n = 417)	Group		χ²/t/Z^*	p
	Total (n = 417)	Breastfeeding (n = 244)	Formula feeding (n = 173)	χ²/t/Z^*	p
Characteristics of infants
Gender (boy)	223 (53.48)	127 (52.05)	96 (55.49)	0.482	0.487
Han nationality	334 (80.10)	196 (80.33)	138 (79.77)	0.020	0.888
One-child family	151 (36.39)	89 (36.78)	62 (35.84)	0.038	0.845
Vaginal delivery	231 (55.40)	150 (61.48)	81 (46.82)	8.798	0.003
Mother as main caregiver	399 (95.68)	242 (99.18)	157 (90.75)	17.413	<0.001
Feeding done mother	355 (86.17)	240 (99.17)	115 (67.65)	83.349	<0.001
Infant temperament type (EITQ)				21.697	<0.001
Easy	204 (49.04)	116 (47.74)	88 (50.87)
Intermediate-easy	139 (33.41)	92 (37.86)	47 (27.17)
Slow-to-warm-up	33 (7.93)	22 (9.05)	11 (6.36)
Intermediate-difficult	11 (2.64)	7 (2.88)	4 (2.31)
Difficult	29 (6.97)	6 (2.47)	23 (13.29)
Characteristics of mother
Age (years)	30.40 ± 4.49	30.14 ± 4.02	30.76 ± 5.08	−1.238	0.216
Educational level				5.432	0.143
Junior school or below	52 (12.47)	24 (9.84)	28 (16.18)
High school/polytechnic school	74 (17.75)	40 (16.39)	34 (19.65)
Junior college	113 (27.10)	68 (27.87)	45 (26.01)
Bachelor or above	178 (42.69)	112 (45.90)	66 (38.15)
Maternal depression (EPDS)	7.00 (4.00–10.00)	7.00 (4.00–10.00)	7.00 (5.00–11.00)	−1.300	0.194
Parenting confidence (KPCS)	41.00 (38.00–43.00)	41.00 (39.00–43.00)	41.00 (37.00–43.00)	−2.046	0.041
Characteristics of family
Family structure^a				1.510	0.470
Nuclear family	158 (37.89)	98 (40.16)	60 (34.68)
Stem family	234 (56.12)	133 (54.51)	101 (58.38)
Joint family	21 (5.04)	11 (4.51)	10 (5.78)
Divorced family	4 (0.96)	2 (0.82)	2 (1.16)
Family monthly income (per-capita)^b				3.272	0.513
Under $441	50 (12.02)	27 (11.07)	23 (13.37)
$441–735	100 (24.04)	53 (21.72)	47 (27.33)
$735–1,029	92 (22.12)	54 (22.13)	38 (22.09)
$1,029–1,470	67 (16.11)	42 (17.21)	25 (14.53)
Over $1,470	107 (25.72)	68 (27.87)	39 (22.67)
Location				23.844	<0.001
Qingdao	65 (15.59)	55 (22.54)	10 (5.78)
Chongqin	117 (28.06)	69 (28.28)	48 (27.75)
Liuzhou	119 (28.54)	59 (24.18)	60 (34.68)
Maanshan	116 (27.82)	61 (25.00)	55 (31.79)

Data are shown as n (%) and mean ± standard deviation.

Chi-squared test was used for categorical variables, t-test was used for normally distributed data (mother's age), and the Wilcoxon rank-sum test for not normally distributed data (EPDS scores and KPCS scores).

Family structure: nuclear family: a family group that consists only parents and children; stem family: a family group that consists grandparents, parents, and children; joint family: a family that includes not only parents and children but also the grandparents, aunts, uncles, cousins, and other relatives; divorced family: one of the parents divorced.

Family monthly income were converted into U.S. dollar.

EITQ, Early Infancy Temperament Questionnaire; EPDS, Edinburgh Postnatal Depression Scale; KPCS, Karitane Parenting Confidence Scale.

Infant development

As shown in Table 2, for the breastfeeding group and the formula feeding group, the risk of developmental delay measured with the ASQ-C was 4.1% (10/244) and 9.3% (16/173) for the communication domain, 5.7% (14/244) and 8.1% (14/173) for the problem-solving domain, and 6.2% (15/244) and 12.1% (21/173) for the personal-social domain, respectively. There were no statistically significant differences between gross motor development and fine motor development in both groups (p > 0.05). The ASQ-C scores of breastfed infants were higher (230.67 ± 39.07) than those of formula-fed infants (217.69 ± 45.75) (t = 3.030, p = 0.003).

Table 2.

Comparison of Ages and Stages Questionnaires Scores of Mother-Infant Dyads

In different feeding pattern groups	Total	Group		t/Z^*	p
In different feeding pattern groups	Total	Breastfeeding	Formula feeding	t/Z^*	p
Total ASQ score	225.28 ± 42.40	230.67 ± 39.07	217.69 ± 45.75	3.030	0.003
Communication				2.689	0.007
Suspected risk	66 (15.83)	33 (13.52)	33 (19.08)
Risk	26 (6.24)	10 (4.10)	16 (9.25)
Gross motor				0.920	0.358
Suspected risk	48 (11.51)	30 (12.30)	18 (10.40)
Risk	13 (3.12)	3 (1.23)	10 (5.78)
Fine motor				1.744	0.081
Suspected risk	90 (21.58)	45 (18.44)	45 (26.01)
Risk	14 (3.36)	8 (3.28)	6 (3.47)
Problem-solving				2.155	0.031
Suspected risk	70 (16.79)	34 (13.93)	36 (20.81)
Risk	28 (6.71)	14 (5.74)	14 (8.09)
Personal-social				2.001	0.045
Suspected risk	77 (18.47)	43 (17.62)	34 (19.65)
Risk	36 (8.63)	15 (6.15)	21 (12.14)

Five domains: communication, gross motor, fine motor, problem-solving, and personal-social.

t-Test and Wilcoxon rank-sum rank test were used.

ASQ, Ages and Stages Questionnaires, Chinese version.

Association between feeding pattern and infant development

Bivariate analysis revealed that breast-fed infants were less likely than formula-fed infants to be at risk for having developmental delay in communication (OR = 1.88, 95% CI = 1.19–2.99), problem-solving (OR = 1.64, 95% CI = 1.04–2.58), and personal-social development (OR = 1.55, 95% CI = 1.01–2.39) (Table 3, Model 1).

Table 3.

Associations Between Breastfeeding and the Five Domains of the Ages and Stages Questionnaires Among Infants Aged 3 Months Old

Model	Communication	Gross motor	Fine motor	Problem-solving	Personal-social
Model 1
Breastfeeding	1.000	1.000	1.000	1.000	1.000
Formula feeding	1.883 (1.185–2.994)^**	1.293 (0.571–2.227)	1.483 (0.951–2.313)	1.640 (1.044–2.578)^*	1.553 (1.011–2.387)^*
Model 2
Breastfeeding	1.000	1.000	1.000	1.000	1.000
Formula feeding	1.863 (1.110–3.129)^*	1.528 (0.824–2.834)	1.466 (0.901–2.386)	1.858 (1.123–3.072)^*	1.806 (1.122–2.908)^*
Model 3
Breastfeeding	1.000	1.000	1.000	1.000	1.000
Formula feeding	2.598 (1.420–4.753)^**	1.610 (0.782–3.318)	1.757 (0.994–3.105)	1.909 (1.058–3.445)^*	1.956 (1.118–3.424)^*

Model 1: no variables were adjusted; Model 2: sociodemographic factors such as gender, ethnicity, one-child family, mode of delivery, mother's age, mother's level of education, monthly household income, family structure, and location were adjusted; Model 3: In addition to the sociodemographic factors in Model 2, parenting factors and psychological characteristics, such as main caregiver, feeding done by mother, maternal depression, parenting confidence, and infant temperament types were also adjusted.

p < 0.05, ^**p < 0.01.

Compared with the unadjusted model (Model 1), after adjusting for sociodemographic factors (Model 2), communication, problem-solving and personal-social development were significantly associated with feeding pattern. Formula-fed infants had a higher risk of development delay than breastfed infants.

In Model 3, there were significant differences in the personal-social (aOR = 1.96, 95% CI = 1.12–3.42), communication (aOR = 2.60, 95% CI = 1.42–4.75), and problem-solving (aOR = 1.91, 95% CI = 1.06–3.45) domains. After adjustment, the aOR of the communication and problem-solving domains were higher than those of Model 2. After adjustment for multiple confounders, neither gross motor (aOR = 1.61, 95% CI = 0.78–3.32) nor fine motor skills (aOR = 1.76, 95% CI = 0.99–3.11) were statistically significant at the age of 3 months.

Discussion

This study focused on evaluating the effects of exclusive breastfeeding during early infancy in an urban Chinese population. Based on information in the available literature, we controlled the confounding effects of sociodemographic factors, parenting characteristics, and psychological characteristics of infants and mothers to obtain a clearer picture of the relationship between exclusive breastfeeding and infant development.

In this study, we collected information about infant temperament and maternal mental health, both of which are associated with both feeding pattern and infant developmental outcomes. Our findings showed that the development level of breast-fed infants is better than that of formula-fed infants. We also found that breastfeeding may protect against the risk of developmental delay in infant communication, problem-solving, and personal-social skills; the associations between feeding pattern and developmental outcomes were also found to be stronger after adjusting for multiple confounding factors. These results agree with most existing studies. In a follow-up study, Choi et al. found that compared with children breastfed for 4 months, children breastfed for less than 4 months were more likely to be at risk for having developmental delays in communication and social interaction at 6 months.⁴⁶ Oddy et al. also reported a similar conclusion for a cohort study: after adjustment, they found that infants who were breast-fed for more than 4 months were found to have gained a better development among 1- to 3-year-old children.⁴⁷ We also found significant effects in the problem-solving domain after adjusting for confounding variables; this finding is in agreement with those of some other studies. Bernard et al. showed that the longer the duration of breastfeeding, the better the problem-solving development performance (higher points on ASQ) for 3-year-old children.⁴⁸ Ali et al. also found a better performance in this domain among 3-year-old children who were exclusively breastfed for more than 6 months than among children who were breastfed for less than 6 months.⁴⁹

Two theories may support the results of the present study. One theory suggests that breast milk has a direct impact on infant brain development by providing specific nutrients such as long-chain polyunsaturated fatty acids, especially docosahexaenoic acid (DHA) and arachidonic acid (ARA).⁵⁰ Both DHA and ARA are involved in visual development and neurodevelopment of infants by promoting neuronal maturation, which is essential for the cognitive ability of children.⁵¹ An alternative theory is that breastfeeding promotes mother-infant interaction,⁵² which may improve the cognitive development of infants indirectly.⁵³ As a result of sensory feedback during breastfeeding, the mother may be more sensitive to the infant's needs and can respond in a timely and appropriate manner.⁵⁴ During breastfeeding, close physical contact and interactions such as gaze behavior and vocalization may provide infants with sensory stimuli, which may improve the development of social skills.⁵⁵ Breastfeeding can facilitate the gradual growth of a safe relationship between mother and infant, which will help the infant's emotional development and enable the infant to explore the environment more. Breastfeeding benefits cognitive development by way of great mother-infant interactions.⁵⁵ These findings confirm that breastfeeding has positive effects on communication and problem-solving skills.

We did not find any positive effects of breastfeeding on the motor development of infant; a finding that is inconsistent with those of some studies. Sacker et al. found that the chance of delay in motor development among 9-month-old breastfed children may be 50% higher than that of children who were never breastfed.⁵⁶ In a Taiwanese childbirth cohort study, Chiu et al. reported that breastfeeding for more than 6 months had a positive effect on the gross motor and fine motor development of children at the age of 18 months.⁵⁷ Ali et al. also found that among a rural Indian population, breastfeeding for more than 6 months may lead to scoring higher in the gross motor and fine motor domains of the ASQ.⁴⁹ The differences in these results may be due to inconsistent research designs, including unspecific definition of breastfeeding and formula feeding, differences in the measurements of outcome variables, and/or variation in the adjustment of confounding factors.^21,58 In the study by Ali et al., no confounding variable was adjusted, and feeding data were obtained after 3 years of life, making the details more susceptible to recall bias.⁴⁹ The complexity of measuring childhood development outcomes is also one causes of the inconsistent results⁵⁹; for example, the Denver developmental screening test was used in the studies by Sacker et al.⁵⁶ and Chiu et al.⁵⁷ The sensitivity and specificity of the measurements and dimensions may affect the evaluation of the study outcomes. Another reason may be the age of which developmental testing was conducted. In the present study, we measured development at 3 months of age; at such an early age, the benefit of only a few months of breastfeeding may not be observed. A study of 1-year-old Korean children showed that infants who were exclusively breastfed until they were 4 months old had improved cognitive ability at 12 months, whereas breastfeeding did not have any apparent impact on the outcomes at 6 months.⁴⁶

The main strength of our study was the research design. First, the participants were healthy and full-term infants and mothers who had no severe diseases or pregnancy complications; thus, the potential confounding effect of various diseases was excluded. Second, data were collected in early infancy, which can minimize exposures to certain factors such as family environment or parenting practice, and improve the quality of feeding data by reducing or eliminating the risk of recall bias and misclassification. Third, the ASQ was used to examine the developmental outcome of our study.⁶⁰ The ASQ fully or partially covers the common domains of children's developmental milestones. Moreover, compared with other commonly used development screening tools, the ASQ is less affected by the sociodemographic characteristics of subjects.⁶⁰

There were some limitations in this study. First, the participants were all from urban areas; therefore, the study conclusion cannot be extrapolated to a rural population. Second, some potential factors such as maternal intelligence and parenting environment were not included in this study, due to the limitations of data collection. Third, this was a case–control study and a mixed-feeding group was not included; thus, it may not be sufficient to provide a conclusion about the causal relationship between exclusive breastfeeding and infant development. Therefore, a future follow-up study investigating infant development associated with different feeding patterns should include mix-feeding groups.

Conclusions

Our results show that a positive relationship exists between breastfeeding and infant's communication ability, problem-solving skill, and social development at the age of 3 months. These results support the promotion of exclusive and continuous breastfeeding, which has major public health implications. Once the benefit of breastfeeding presents early in life as expected, the promotion of breastfeeding would gain more public support.

Footnotes

Acknowledgments

We appreciate all the mothers and infants enrolled in this study, as well as all medical staff who helped to complete this study. We thank Prof. Mike Woolridge for English language editing.

Disclosure Statement

All the authors declare no competing financial interests.

Funding Information

This work was supported by the Youth Program of National Natural Science Foundation of China (Grant Number 81803249) and the Youth Scholar Scientific Research Foundation of Chinese Center for Disease Control and Prevention (Grant Number 2018A202).

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The Possible Effects of Breastfeeding on Infant Development at 3 Months: A Case–Control Study