Comparison of the Effect of Direct Breastfeeding,Expressed Human Milk,and Infant Formula Feeding on Infant Weight Trajectories: A Systematic Review

Abstract

Background:

Formula and breastfeeding are known factors associated with infant weight trajectories. Evidence exploring the effect of expressed human milk feeding on infant weight in the community setting has not been well synthesized.

Objectives:

This systematic review examined (1) weight changes among infants fed expressed human milk and (2) differences in weight change between infants fed expressed human milk and infants fed at the breast or infant formula via bottle.

Methods:

A comprehensive search of the literature was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. The quality of each study was appraised using the Joanna Briggs Critical Appraisal Tools.

Results:

A total of six studies met the eligibility criteria and included a total of 5,152 infants. The within-subject analysis identified only 31 infants strictly or predominantly fed expressed human milk. The between-subject analysis comparing expressed human milk feeding to the available comparison groups (formula-fed or direct at the breastfed) revealed that higher weight gains were observed in the weight trajectories among infants in the bottle or formula-fed conditions in four of the six included studies.

Conclusions:

Findings from the few studies included in this review found a difference in the infant weight gain patterns among expressed human milk-fed infants when compared with their respective feeding groups (directly breastfed or formula-fed). Further research is needed to corroborate these findings and elucidate the clinical significance of the differences in weight gain patterns observed across infant feeding groups.

Introduction

Infant weight trajectories that deviate from the projected percentile curve for age and sex are of concern. Inadequate infant weight gain can be a marker of an underlying pathology, such as a metabolic disorder.¹ In addition, inadequate infant weight gain can increase maternal anxiety regarding milk supply and negatively impact breastfeeding duration.² Weight change patterns during infancy are important indicators of future disease risk. Several studies have cited rapid weight gain during infancy as a risk factor for later-life obesity.^3,4 For example, in the study conducted by Zheng et al.,³ infants with rapid weight gain, defined as a change in weight-for-age z-score (WAZ) greater than 0.67 standard deviations, had a 3.7 times increased risk of childhood obesity compared with infants without rapid weight gain. Nutrition during infancy has been cited to play an influential role in the risk of rapid weight gain. A longitudinal study revealed infants who were breastfed, compared with infants who were formula-fed, exhibited the lowest risk of rapid weight gain during the first year of life.⁵ Further, Appleton et al.⁶ found it plausible that formula feeding practices contribute to the risk of rapid weight gain. Given the high prevalence of childhood obesity, risk factors related to rapid weight gain are important to identify.

Two meta-analyses found that breastfeeding is protective against later-life obesity.^7,8 Both the composition of human milk, relative to infant formula, and the feeding practices associated with feeding at the breast, compared with feeding via a bottle, have been hypothesized to influence infant weight gain patterns. The bioactive nutrient profile of human milk differs from that of infant formula. In particular, human milk is higher in fat composition but lower in protein and energy.⁹ The early protein hypothesis posits that the lower protein content in human milk may protect against childhood obesity via growth and adipogenic activity through modulation of insulin and insulin-like growth factor 1 secretion.^10,11 Further, the literature has cited that the bioactive components in human milk, such as leptin and adiponectin, play a critical role in modulating infant weight gain trajectories.^12,13 Leptin and adiponectin levels in human milk have been found to regulate fat storage and blood glucose levels, respectively.^12,14,15

Key differences in the delivery of human milk (e.g., breast or bottle) raise important considerations between the two feeding modes. For example, human milk composition and caloric content are known to change both throughout the day (e.g., circadian variation)¹⁶ and throughout each feeding (e.g., foremilk versus hindmilk).¹⁷ This highlights potential differences in the feeding experiences among infants fed human milk directly at the breast compared with infants fed expressed milk via a bottle. Further, the composition of expressed human milk feeding is dependent on several additional factors, such as the storage (e.g., refrigeration and freezer) and handling processes (e.g., warming and thawing) of the expressed milk. The literature examining the impact of circadian rhythms and storage and handling processes on the composition of expressed human milk is a complex, emerging area of research.^16,18,19

The mode of milk delivery has also been shown to influence infant feeding practices. Feeding at the breast has been hypothesized to foster more responsive, infant-led feeding styles when compared with infants fed via a bottle.^20,21 For example, infants fed directly at the breast were found to exhibit higher levels of engagement and disengagement cues during feeding sessions compared with formula-fed infants.²² Finally, infants fed via bottle have been cited to have higher milk intake and a higher risk for rapid weight gain compared with their fed-at-the-breast counterparts.^23–25

For these reasons, the breastfeeding recommendations set forth by the American Academy of Pediatrics (AAP) and the World Health Organization (WHO) underscore human milk as the best source of nutrition for infants but highlight the need for closer examination of the potential effect of human milk delivery mode.^26,27 To date, the growth patterns of nonhospitalized infants bottle-fed expressed human milk have not been well synthesized in the literature.²⁸ Surveillance efforts in the United States to gauge the prevalence of expressed human milk feeding are limited to predominantly White, non-Hispanic populations.^29,30 The Infant Feeding Practices Study II cited that 85% of women fed their infants some expressed human milk within the first 4.5 months of life.²⁹ This prevalence estimate was collected between 2005 and 2007 among a sample with higher rates of employment and education than nationally representative samples in the United States.^29,30 In a more recent analysis of participants in the Special Supplemental Nutrition Program for Women, Infants, and Children, almost three-fourths (70%) of participants expressed human milk in the first 13 months following birth.³⁰ Globally, prevalence rates of expressed human milk feeding ranged from 5% to 20% in Hong Kong in the first 6 months of life,³¹ 16.5% in Singapore in the first 3 months of life,³² and 69% in Australia in the first 6 weeks of life.³³ Thus, based on prevalence reports in the available literature, engagement in expressed human milk feeding among nonhospitalized infants in a community setting is a widespread feeding method practiced globally.

The global reach of this feeding practice accentuates the need to synthesize the effect of expressed human milk feeding on infant weight trajectories compared with the weight trajectories of directly breastfed and formula-fed infants. Previously conducted reviews found insufficient evidence to understand the association between expressed human milk feeding and infant weight trajectories.^34–36 Thus, the aim of the current systematic review was to describe infant growth patterns among infants fed expressed human milk and identify potential differences in growth patterns among infants based on feeding mode (expressed human milk-fed compared with infants fed at the breast or fed infant formula via bottle).

Methods

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines were used to develop the methods of this systematic review.³⁷ For the purposes of this review, the following terminology and definitions were used: (1) “infants” represent children between birth and 2 years of age; (2) milk type was divided into (a) human milk and (b) nonhuman milk comprising infant formulas (cow-based, soy-based, and preterm formulations); (3) mode of feeding was divided into (a) fed at the breast and (b) fed via bottle; and (4) infant growth patterns included measures of infant weight (e.g., crude weight and weight-for-age percentiles) and function of weight measurements (e.g., weight-for-length [WLZ] or body mass index z-scores [BMIz]). Similar to a prior systematic review, the umbrella term “human milk” was used to encompass the variability in the definition and use of the term “breast milk.”³⁸ This method permits human milk to reference human milk fed directly at the breast and expressed human milk fed via a bottle.

Eligibility criteria

Inclusion criteria were that studies reported on weight outcomes following expressed human milk feeding among infants between birth and 2 years of age. This time frame was selected to stay consistent with the WHO and AAP’s guidance for the duration of breastfeeding.^26,27 Given the previous focus of the literature on hospitalized preterm or low-birth-weight infants, no limitation on birth weight or gestational age was applied to capture all infants following hospital discharge.^39,40 Studies not written in English, occurring in low- or medium-income countries (LMICs), and not original, empirical research published in peer-reviewed journals were excluded. LMICs were defined using the Human Development Index⁴¹ and were excluded from the present review given the high prevalence of malnutrition in these countries; 99% of the world’s children affected by child growth failure, defined as underweight, stunting, and wasting, inhabit these countries.⁴²

Search strategy

A comprehensive search of the literature was conducted in PubMed, Embase, Scopus, Cumulative Index to Nursing and Allied Health Literature, and Cochrane Library. Following a thorough review of the literature, no other systematic review conducted on the present research question was identified. Therefore, no date restriction was applied in the search strategy. The general search term categories used across databases are outlined in Table 1. The search was conducted and last consulted in October 2022.

Table 1.

General Search Strategy Terms

	Weight change terms	Mode of milkdelivery terms	Milk type terms	Milk expression terms
Example Search Terms	Adiposity	Breastfeeding	Human milk	Breast milk expression
	Pediatric obesity	Breastfeeding	Breast milk	Human milk expression
	Rapid or excessive or accelerated and weight gain	Bottle feeding		Breast pumps
	Body weight changes			Expressed milk

Study selection

Search results were exported into an RIS file using Zotero software⁴³ and imported into Covidence for screening and organization.⁴⁴ Study selection occurred in two phases. In phase one, the title and abstract of each article were screened using a screening tool adapted from Polanin et al.⁴⁵ by C.N.S. and N.A.J. and based on the aforementioned eligibility criteria. The screening tool was pilot tested on 20 studies and underwent two modifications to arrive at the final screening tool used to screen all titles and abstracts. In phase two, full-text articles were screened against the eligibility criteria by C.N.S. and N.A.J. This review was limited to studies that reported weight change measures on infants fed expressed human milk separately from infants fed at the breast. This strategy was used to better understand and isolate the effect of expressed human milk feeding on infant weight change. However, this approach eliminated studies that explored expressed human milk but combined all human milk or all bottle feedings into a single variable.^25,46,47

Data extraction and synthesis

Data were extracted from the included articles by C.N.S. and N.A.J. using a data extraction checklist informed by Denison et al.⁴⁸ Data extracted for synthesis included author name and year of publication, location and setting of the study, study design, exposure of interest including study time points and methods used for measurement, outcomes of interest including measurement type and study time points and methods used for measurement, key findings, confounding factors considered, and statistical techniques used. During the analysis, data were grouped by the comparison arm and synthesized based on the trajectory of the outcome measure. Studies that reported statistical analysis findings on within-subject changes were synthesized to assess the effect of expressed human milk on infant weight trajectories. Studies that provided a comparison, fed at breast or fed infant formula via bottle, were grouped by the comparison arm and compared to groups fed expressed human milk. When applicable, missing data were searched for in the article, supplemental material, and referenced prior work. Missing data that were not identified through searching were operationalized as not collected in the present review.

Quality assessment

The Joanna Briggs Institute (JBI) Critical Appraisal Tool was used to assess study quality.⁴⁹ This tool was also used to assess the risk for bias in the design, conduct, or analysis of each study and the quality of the methodological approach.⁵⁰ Quality assessment was performed only with extracted data applicable to the aims of this review. The JBI checklist for cohort studies has a total of 11 items with the following response options: “yes,” “no,” “unclear,” and “NA.”⁴⁹ Each “yes” response was scored as a value of one. Each “no,” “unclear,” and “NA” response was scored with a value of zero. Studies with a score of nine or higher were deemed “excellent.” Studies with a score between six and eight were deemed “moderate.” Studies with a score of five or below were deemed “poor.”

Results

Search results

Overall, 1,720 studies were identified. The Covidence software identified and removed 657 duplicate records. Title and abstract screening excluded 924 studies not meeting eligibility criteria. During the full-text review, a further 133 articles were excluded. This resulted in six studies meeting the eligibility criteria.

Study characteristics

All included studies took place in the United States, with the exception of one study conducted in Canada.⁵¹ The study designs included three retrospective and three prospective cohort studies.^23,51–55 See Table 2 for a summary of study characteristics. Most studies recruited participants within a specified geographical area.^51–55 Final follow-up of the included studies varied from 4 months corrected age to beyond 2 years of age. Sample size varied across studies with two studies having over 1,000 participants.^23,51 See Table 3 for a summary of participant characteristics. Four of the included studies included both fed at the breast and fed nonhuman milk as comparators.^23,51,53,55 Gehl et al.⁵⁴ compared fortified human milk with nonfortified human milk-supplemented infant formula. Whereas Bartok⁵² divided participants into two groups, infants primarily fed at the breast and infants primarily fed human milk via a bottle. The amount of infant formula permitted was restricted a priori in each group in this research study.⁵² The outcome of interest was the primary aim in four of the six studies.^23,51–53 Two of the included studies analyzed weight as a secondary aim.^54,55 In terms of the outcome measurement, the number of studies that reported on the following measurements included three studies reporting on BMIz, two studies measuring WLZ, four studies providing WAZ, and two studies reporting weight percentiles.^23,51–55 Each of the studies reported on the following measures: weight measured in grams, weight gain velocity, weight-for-height z-score (WHZ), fat mass, and fat-free mass.^23,51–55 See Table 4 for a summary of outcome measurement characteristics.

Table 2.

Study Characteristics

First author (year) Location/setting	Study design	Exposure and measurement	Comparator	Outcome Measurement collection	Key findings
Maskarinec et al.⁵³	Retrospective, longitudinal study	Expressed milk feeding	HM feeding	Abstracted from medical record (birth to 6 years)	No association between duration of feeding method and risk of excess weight at any time point
United States		Self-report survey; collected at 12 months	Excl HM feeding
			Feeding at breast
			Excl feeding at breast
			Formula feeding
Gehl et al.⁵⁴	Retrospective, longitudinal study	Fortified HM	- None	4 Months CA	BM-F infants were smaller (kg) than BM-S infants at 4 months CA
United States		HM supplemented with formula			More BM-S infants above the 50th percentile
		Feeding type measured at hospital discharge
Azad et al.⁵¹	Prospective, longitudinal study	BF only, some expressed milk	BF only, all direct	Measurements collected via CHILD staff at 12 months of age	BMIz and change in WAZ: No BF or Partial BF > BF + HM > BF, all direct at 12 months of age
Canada		Self-report by mothers at 3, 6, 12, 18, and 24 months of age	Partial BF with formula
			No BF
Li et al.²³	Prospective, longitudinal study	HM by bottle only	BF only	Weight measurements reported on 3-, 5-, 7-, and 12-month surveys	Bottle-fed infants gained more weight (g) per month than BF only
United States		BF and HM by bottle	BF and NHM by bottle		HM-fed-only infants gained more weight with higher bottle feedings compared with lower bottle feedings
		HM and NHM by bottle	NHM by bottle only
		Self-report; postpartum survey (1, 2, 3, 4, 5, 6, 7, 9, 10, and 12 months of age)
DiSantis et al.⁵⁵	Retrospective, longitudinal study	HM via bottle	BF direct	Growth measures from 6, 12, 24 months collected from medical records	No differences in mean WLZ across feeding groups at 6, 12, and 24 months
United States		Self-report; first 3 months of life	Formula via bottle		Feeding method unable to predict weight change trajectories
Bartok⁵²	Prospective, longitudinal study	HM via bottle	Fed at breast	Weight measured at monthly visits	Direct BF group
United States		Self-report, monthly visit 1–6 months	Self-report, monthly visit 1–6 months	Body composition measured at 1, 3, and 6 months	Lower WLZ at 1 and 2 months
					Lower BMIz at 1 month
					No significant differences between groups for weight, WAZ, FM, %FM, FFM

BF, breastfed; BM-F, fortified breast milk; BMIz, body mass index z-score; BM-S, breast milk supplemented with infant formula; CA, corrected age; Excl, exclusive; FFM: fat-free mass; FM: fat mass; %FM: fat mass percentage; HM, human milk; NHM, nonhuman milk; WAZ: weight-for-age z score; WHZ, weight-for-height z-score; WLZ: weight-for-length z-score.

Table 3.

Participant Characteristics

First author (year)	Sample (N)	Female (infant) (%)	Gestational age	Birth weight	Race/ethnicity (Maternal) (%)
Maskarinec et al.⁵³	269	48	Preterm (n): 21	kg, mean ± SD:	White: 84; Black: 8;
			Term (n): 248	3.43 ± 1.76	Other: 8; Hispanic: 5;
			Weeks, mean ± SD	g, mean ± SD	Non-Hispanic: 95
Gehl et al.⁵⁴	285	BM-F: 56	BM-F: 28.8 ± 2.8	BM-F: 1145 ± 334	White BM-F: 49;
		BM-S: 47	BM-S: 29.3 ± 2.6	BM-S: 1230 ± 316	White BM-S: 69
Azad et al.⁵¹	2553	47.9	Weeks, mean ± SD	g, mean ± SD	Asian: 14.6; White 75.1; First Nations: 3.7; Other 6.6
			39.9 ± 1.0	3509 ± 443
Li et al.²³	1899	51.82	Weeks, mean ± SD	kg, mean ± SD	White: 86.99; Black: 3.32; Hispanic: 5.21; Other: 4.48
			39.31 ± 1.25	3.48 ± 0.46
Disantis et al.⁵⁵	109	51.4	Not reported	Not reported	White 84.4; Black: 10.1; Other: 5.5
Bartok⁵²	37	NG: 61	Weeks, mean ± SD	kg, mean ± SD	NG: American Indian: 5; Asian: 5; White: 90; Hispanic: 20; Non-Hispanic: 80
		BG: 55	NG: 39.7 ± 1.2	NG: 3.48 ± 0.41	BG: Asian: 11; White: 89; Non-Hispanic: 100
			BG: 39.4 ± 1.0	BG: 3.41 ± 0.43

BF, breastfed; BM-F, fortified breast milk; BM-S, breast milk supplemented with infant formula; NG, nursing group; BG, bottle-fed expressed milk group; SD, standard deviation.

Table 4.

Outcome Comparison

	Outcome measure					Growth chart type
First author (year)	WAZ	WHZ/WLZ	BMIz	Weight	Weight Percentile	WHO	CDC	Fenton
Maskarinec et al.⁵³	x	x	x	x		x
Gehl et al.⁵⁴				x	x	x		x
Azad et al.⁵¹	x		x	x		x
Li et al.²³				x			x
DiSantis et al.⁵⁵	x	x		x			x
Bartok⁵²	x	x	x	x	x	x

BMIz, body mass index z-score; CDC, Centers for Disease Control and Prevention; WAZ, weight-for-age z score; WHO, World Health Organization; WHZ, weight-for-height z-score; WLZ, weight-for-length z-score.

Quality assessment

Overall, five of the six studies included in this review were appraised as “moderate” to “excellent” quality. Of the six studies included in this review, three studies were appraised as excellent with a score of 9 out of a total of 11 points.^23,51,52 Two studies were appraised as “moderate” with scores ranging from 7 to 8 out of 11 points.^53,55 One study was appraised as “poor” with a score of 4 out of 11 points.⁵⁴ Major areas that downrated the quality of the included studies were participant groups were not similar in demographic characteristics or were not recruited from the same population (n = 5), did not identify confounding variables in the analysis of the primary outcome of interest (n = 1), did not implement strategies for confounding variables in analysis of the primary outcome of interest (n = 1), outcomes were not measured using valid and reliable methodology (n = 4), follow-up was not completed or adequately described (n = 4), and strategies to address incomplete follow-up were not outlined (n = 3). See Table 5 for a quality assessment summary of the included studies. The areas that downrated the quality assessment across the included studies greatly increased the risk of bias in the published results. In regard to design, five studies were found to have differences between study groups.^{23,51,53–55} Three studies reported statistically significant differences in demographic characteristics across feeding groups.^51,54,55 Li et al.²³ and Maskarinec et al.⁵³ provided only total sample demographic characteristics. Thus, differences between groups could not be fully analyzed. In the study conducted by Gehl et al.,⁵⁴ confounding variables and the analysis approach for weight outcomes were not outlined. Three of the included studies did not provide a strategy for incomplete follow-up.^53–55 Finally, four studies did not utilize trained research staff to directly collect outcome measurements.^23,53–55 In particular, Maskarinec et al.⁵³ and DiSantis et al.⁵⁵ relied on measures collected from medical records. Li et al.²³ used self-report measurements collected via survey from caregivers. Whereas Gehl et al.⁵⁴ did not specify how the weight measurements were collected.

Table 5.

Summary of Critical Assessment of Included Studies

	Maskarinec et al.⁵³	Gehl et al.⁵⁴	Azad et al.⁵¹	Li et al.²³	DiSantis et al.⁵⁵	Bartok⁵²
Similar groups	x	x	x	x	x	✓
Similar measures for exposure between groups	✓	✓	✓	✓	✓	✓
Valid and reliable exposure measures	✓	✓	✓	✓	✓	✓
Identified confounding variables	✓	x	✓	✓	✓	✓
Strategies for confounding factors	✓	x	✓	✓	✓	✓
Participants free of outcomes	✓	✓	✓	✓	✓	x
Valid and reliable outcomes measurement	x	x	✓	x	x	✓
Sufficient follow-up time	✓	✓	✓	✓	✓	✓
Completed follow-up time	x	x	x	✓	✓	x
Strategies for incomplete follow-up	x	x	✓	✓	x	✓
Appropriate statistical analysis	✓	x	✓	✓	✓	✓

Synthesis of results

Outcomes were grouped by the overarching finding and infant weight or function of weight (e.g., WLZ or BMIz) measurement categories for both within and between subjects. Table 6 provides a synopsis of findings in each weight or function of weight category.

Table 6.

Synthesis of Results

Category	Findings
Within-subject comparisons	No evidence of weight faltering/different weight trajectories	Evidence of different weight trajectories
Crude weight	No unexpected deviations in the average weight gain trajectories (measured in kilograms) between baseline and follow-up measurements⁵²	Crude weight gain: 1,024 g at birth to 3 months, 634 g at >3–5 months, 561 g at >5–7 months, and 438 g at >7–12 months²³
Between-subject comparisons	No evidence of weight faltering or different weight trajectories	Evidence of different weight trajectories
Crude weight	No differences in weight gain (kg) trajectories between 1 and 6 months of age⁵²	All bottle groups gained more crude weight (g) than direct breastfed group²³
Weight-for-age percentile	No major differences between infants below the 10th percentile for weight between groups at 4 months corrected age⁵⁴	More formula-supplemented infants above the 50th percentile for weight than fortified expressed group⁵⁴
Weight-for-age z-score (WAZ)	Three studies found no differences between WAZ and feeding methods^52,53,55	No breastfeeding > expressed human milk > direct breastfeeding at 12 months⁵¹
Weight-for-Length z-score (WLZ)	Two studies found no differences between WLZ and feeding methods^53,55	Direct breastfeeding < expressed human milk at 1 and 2 months⁵²
Body Mass Index z-score (BMIz)	One study found no differences between BMIz and feeding methods⁵³	Direct breastfeeding < expressed human milk at 1 month of age⁵²
		No breastfeeding > expressed human milk > direct breastfeeding at 12 months⁵¹

Effect of expressed human milk consumption: No evidence of weight faltering or differences in weight trajectory based on infant feeding mode comparisons

Infants fed expressed human milk demonstrated weight gain trajectories assessed with different measurement modalities (e.g., crude weight gain measured in grams and weight-for-age percentiles) that did not falter below the expected range or found no differences for each respective quantification modality.

Effect of expressed human milk consumption on infant weight trajectories: Within-subject analysis

Two of the identified studies provided data for analysis of within-subject weight gain trajectories among expressed human milk-fed infants.^23,52 One of these two studies reported no difference in within-subject infant weight trajectories when compared with established weight trajectory patterns.⁵² In particular, Bartok⁵² examined the average standard error of mean weight gain trajectories measured in kilograms of male and female infants fed expressed human milk between baseline and follow-up measurements. The author reported that “expected, steady patterns” of weight gain were observed among infants fed expressed human milk across the study period.⁵² Weight gain trajectories lines were represented in the study graphically without the accompanying numerical reporting.⁵²

Effect of expressed human milk consumption on weight and weight percentile: Between-subject (directly breastfed or infant formula-fed) analysis

Two of the three studies that examined the effect of expressed human milk feeding on infant weight or weight percentile did not find a difference in weight change trajectories when compared with their respective comparison feeding groups.^52,54 Specifically, Bartok⁵² found no significant difference in weight gain trajectories measured in kilograms between 1 and 6 months of age among infants fed expressed human milk via bottle compared with infants fed directly at the breast. Results were predicted using mixed model analyses and reported graphically.⁵² In the study conducted by Gehl et al.,⁵⁴ infants were fed fortified expressed human milk or expressed human milk supplemented with infant formula. No statistically significant difference was found in infants below the 10th percentile at 4 months corrected age between the two feeding groups.⁵⁴

Effect of expressed human milk consumption on WAZ: Between-subject (directly breastfed or infant formula-fed) analysis

Three of the four included studies that examined the effect of expressed human milk feeding on WAZ found no statistically significant difference between weight outcomes and the feeding methods compared.^52,53,55 Among these studies, Maskarinec et al.⁵³ and Bartok⁵² both used direct breastfeeding as a comparison group, whereas DiSantis et al.⁵⁵ used both direct breastfeeding and formula feeding via bottle as comparison groups. Maskarinec et al.⁵³ reported no statistically significant differences in WAZ (β: 0.13 [95% confidence interval (CI): −0.17 to 0.43] and β: −0.03 [95% CI: −0.27 to 0.21]) among expressed human milk-fed infants measured at 3–6 months and 6–12 months of age, respectively. DiSantis et al.⁵⁵ found in latent growth models that direct breastfeeding compared with expressed human milk (slope [standard error]: 0.02 [0.02] intercept [standard error]: 0.18 [0.23]) or formula feeding (slope [standard error]: 0.00 [0.02] intercept [standard error]: 0.07 [0.28]) via bottle did not predict WAZ. Finally, Bartok⁵² reported no statistically significant differences in WAZ in graphical reports using quadratic model analyses.

Effect of expressed human milk consumption on WLZ and WHZ: Between-subject (directly breastfed or infant formula-fed) analysis

Two of the three studies that examined the effect of expressed human milk feeding on WLZ/WHZ found no statistically significant difference between WLZ/WHZ and the feeding methods compared.^53,55 DiSantis et al.⁵⁵ examined mean WLZ at 6, 12, and 24 months of age based on the feeding method used in the first 3 months of life. No significant differences in mean WLZ were observed between infants fed human milk at the breast (mean standard deviation [SD] at 6 months: 0.68 [1.01], 12 months: 0.45 [1.15], and 24 months: 0.23 [1.17]) compared with infants fed human milk via bottle (mean [SD] at 6 months: 0.61 [0.91], 12 months: 0.57 [0.82], and 24 months: 0.36 [1.15]) at any of the study time points.⁵⁵ Maskarinec et al.⁵³ found no statistically significant WHZ (β: −0.28 [95% CI: −0.59 to 0.03] and β: −0.17 [95% CI: −0.41 to 0.08]) among expressed human milk-fed infants measured at 3–6 months and 6–12 months of age, respectively.

Effect of expressed human milk consumption on BMIz: Between-subject (directly breastfed or infant formula-fed) analysis

One of the three studies that examined the effect of expressed human milk feeding via bottle on BMIz found no statistically significant difference between BMIz and the feeding methods compared.⁵³ Specifically, Maskarinec et al.⁵³ found no statistically significant association between the human milk feeding method and the BMIz measured at 3–6 months (β: −0.23 [95% CI: −0.60 to 0.15]) and 6–12 months of age (β: −0.09 [95% CI: −0.39 to 0.20]), respectively.

Effect of expressed human milk consumption: Evidence of differences in weight trajectory based on infant feeding mode comparisons

Evidence supporting differences in infant weight gain trajectories among infants fed expressed human milk compared with infants fed infant formula or fed directly at the breast was observed in four of the six studies identified in this review. Weight change trajectories across the included studies, for all feeding modes, were measured using different measurement modalities (e.g., crude weight gain measured in grams and weight-for-age percentiles).

Effect of expressed human milk consumption on infant weight trajectories (within-subject analysis)

One of the two studies²³ that examined the effect of expressed human milk feeding on infant weight trajectories across time found differences within the studied weight trajectories. This study compared the crude weight gain measured in grams per month among each feeding group across the first year of life divided into the following intervals: birth to 3 months, >3–5 months, >5–7 months, and >7–12 months.²³ Crude mean weight gain for infants fed expressed human milk was 1,024 g at birth to 3 months, 634 g at >3–5 months, 561 g at >5–7 months, and 438 g at >7–12 months.²³

Effect of expressed human milk consumption on weight and weight percentile: Between-subject (directly breastfed or infant formula-fed) analysis

Two of the three studies that examined the effect of expressed human milk feeding on infant weight gain trajectories found differing patterns of weight trajectories based on the feeding method.^23,54 In particular, Li et al.²³ found a statistically significant difference in weight gain (g) per month in infants fed at the breast compared with infants fed expressed human milk or infant formula via bottle. Infants fed expressed human milk via bottle gained 89 g more per month (p = 0.02) when compared with infants fed directly at the breast only.²³ Similarly, infants fed infant formula via bottle gained 71 g more weight per month (p < 0.001) than their directly breastfed counterparts. In addition, in this study, infants fed expressed human milk gained more crude weight (measured in grams per month) than infants fed directly at the breast at birth to 3 months (mean difference: 87 g), >5–7 months (mean difference: 128 g), and >7–12 months (mean difference: 163 g). Whereas infants fed human milk via bottle gained more crude weight during the birth to 3-month (mean difference: 111 g) and >7–12-month (mean difference: 92 g) intervals than infants fed nonhuman milk via bottle. Finally, among infants fed only human milk, infants categorized as having high bottle feedings gained more grams per month (780 g/month) compared with infants categorized as having low bottle feedings (729 g/month).²³

In the study conducted by Gehl et al.,⁵⁴ it was found that human milk feeds supplemented with bottles of infant formula exhibited higher weight gain (measured via kilograms) than infants fed fortified human milk feeds at 4 months corrected age. The infant group fed expressed human milk supplemented with infant formula had significantly more infants above the 50th percentile for weight at 4 months corrected age compared with infants fed fortified expressed milk.⁵⁴

Effect of expressed human milk consumption on WAZ: Between-subject (directly breastfed or infant formula-fed) analysis

One of the four studies examining WAZ found differing weight change patterns among infants fed expressed human milk compared with their formula-fed and fed-at-the-breast counterparts.⁵¹ Specifically, Azad et al.⁵¹ found an “intermediate” change in WAZ measured using both descriptive statistics and regression modeling techniques. Three-month-old infants fed expressed human milk via the bottle exhibited a lower weight gain velocity (β: 0.14 [95% CI: 0.05–0.24]; mean [SD]: −0.17 ± 1.02) compared with infants fed formula (β: 0.51 [95% CI: 0.38–0.64]; mean [SD]: 0.21 ± 1.14) but a higher weight gain velocity compared with infants fed directly at the breast (β: 0.00 reference group; mean [SD]: −0.37 ± 1.03).⁵¹

Effect of expressed human milk consumption on WLZ and WHZ: Between-subject (directly breastfed or infant formula-fed) analysis

The study conducted by Bartok⁵² is one of the three studies that examined WLZ/WHZ and found that compared with infants fed human milk via bottle, infants fed at the breast had a statistically significant lower WLZ at 1 (p = 0.006) and 2 months (p = 0.01) of age.

Effect of expressed human milk consumption on BMIz: Between-subject (directly breastfed or infant formula-fed) analysis

Two of the three studies that examined the effect of expressed human milk feeding via bottle on BMIz scores found differing BMIz scores among infants fed expressed human milk compared with their formula-fed and fed-at-the-breast counterparts.^51,52 Bartok⁵² found that compared with infants fed human milk via bottle, infants fed at the breast had statistically significant lower BMIz at 1 month (p = 0.03) of age. Azad et al.⁵¹ found infants fed expressed human milk had higher BMIz at 12 months of age (β: 0.12 [95% CI: 0.01–0.23]; mean [SD]: 0.14 ± 1.00) compared with infants fed directly at the breast only (β: 0.00 [reference group]; mean [SD]: −0.02 ± 1.06) and lower BMIz at 12 months of age compared with infants fed formula only (β: 0.45 [95% CI: 0.30–0.59]; mean [SD]: 0.56 ± 1.08).

Discussion

This review identified only six studies that examined the relationship between expressed human milk feeding and infant growth patterns. Only two of the six included studies published data permitting the within-subject analysis of changes in infant growth patterns.^23,52 These studies found no evidence of weight faltering or weight trajectories deviating below the expected range of the measurement modality utilized among the 31 infants strictly or predominantly fed expressed human milk.^23,52 However, there is insufficient evidence to draw overall conclusions about infant weight trajectories among strictly or predominantly expressed human milk-fed infants over time. Four of the included studies supplied data to analyze infant growth patterns between subjects (e.g., expressed human milk versus formula or direct breastfeeding) and found statistically significant differences in their selected outcome measurements across feeding groups.^23,51,52,54 Overall, synthesis efforts were complicated by the significant heterogeneity in the form of outcome measurement and the type of comparison groups (direct breastfeeding, infant formula feeding, or both) used across these studies. Overall, findings from this review must be interpreted within the context that there is a paucity of existing research in this area (only six studies identified) and that the heterogeneity of the comparison groups and outcome measurements restricted synthesis efforts.

The within-subject analysis revealed no evidence of weight trajectories below the expected ranges of the reported measurement modalities among the 31 infants strictly fed expressed human milk across these two studies but provided insufficient evidence for the synthesis of generalizable growth patterns of infants fed expressed human milk over time. Infants are expected to gain an average of 30 g per day in the first 3 months of life, 15 g per day between 3 and 6 months, and 10 g between 6 and 12 months of life.⁵⁶ Li et al.²³ compared crude weight gain measured in grams per month across feeding groups. Crude weight gain for infants fed only expressed human milk was above the established, expected weight trajectory.^23,56 In the study conducted by Bartok,⁵² growth trajectories of infants fed expressed human milk demonstrated weight gain trajectories without unexpected deviations on graphical reporting during the study period. Additional research in large, nationally representative samples is critically needed to corroborate these tentative findings.

The between-subject analysis provided some evidence in the evaluation of infant growth patterns among expressed human milk-fed infants compared with formula-fed or directly breastfed infants. Four of the included studies found differences in their respective outcome measurements across feeding groups. Li et al.,²³ in a prospective, longitudinal study with a large sample size, found that both bottle delivery, regardless of bottle contents, and bottle feeding frequency were associated with more weight gain measured in grams per month. Whereas Gehl et al.⁵⁴ found that the preterm infant group that was supplemented with infant formula had significantly more infants above the 50th percentile and exhibited higher rates of weight gain (kilograms/day) than infants fed fortified expressed human milk. A prospective cohort study with a large sample size found infants fed expressed human milk at 3 months of life exhibited WAZ and BMIz lower than infants fed infant formula but higher than infants fed directly at the breast at 12 months of life.⁵¹ In the fourth study that identified differences in reported outcome measurements across feeding groups, infants fed expressed human milk, compared with infants fed directly at the breast, exhibited higher BMIz and WLZ at 1 month and within the first 2 months of life, respectively.⁵² Higher weight gain measurements were observed in the weight trajectories among infants in the bottle-fed or in the formula-fed conditions across these four studies. However, these findings are complicated by several limitations, including the heterogeneity in outcome measurements reported, the heterogeneity in comparison groups (direct breastfeeding, infant formula feeding, or both) used across studies, and the small sample sizes in studies with a strictly expressed human milk-fed grouping.^23,52

Among the studies that did not find any statistically significant associations between infant weight change and feeding methods, two of the three studies used a retrospective design with a 12-month or longer recall period for feeding exposure.^53,55 Further, the study conducted by DiSantis et al.⁵⁵ included a small sample size of infants fed formula starting at birth and therefore may have been underpowered to detect differences between only formula-fed and human milk-fed infants. The other study, conducted by Bartok,⁵² was also underpowered to detect differences between feeding methods and weight gain velocity curves exceeding the 85th percentile for weight on WHO growth charts. A post-hoc power analysis conducted by the author revealed that 75 infants per group would be needed to reach statistical significance at 4–6 months of age between the two feeding groups studied (expressed human milk via bottle vs. direct breastfeeding).⁵²

Overall, the findings in support of a difference in infant weight trajectories among infants receiving expressed human milk via bottle in this review are congruent with prior research examining the association between patterns of infant growth and bottle-feeding behaviors and infant formula feeding. Prior evidence supports that an earlier introduction to the bottle, regardless of milk type, may disrupt self-regulation of intake and increase the likelihood of bottle-emptying behaviors in late infancy.⁴⁷ In addition, higher levels of milk intake have been noted among bottle-fed infants in the literature.^23–25 Infant formula feeding has been associated with higher rates of rapid infant weight gain compared with their breastfed counterparts.⁵ However, further research in large, longitudinal cohort studies is still needed to corroborate these findings as none of the included studies collected the age of bottle introduction or measured the amount consumed at each feeding for any of the feeding modes.

Additional considerations for the discrepancies in the results found across the retained studies include the limited diversity in race/ethnicity of participants and the variation in outcome measurement reported across studies. Four out of the six studies had sample groups that consisted of 80% or higher White participants.^23,52,53,55 Social and health care inequities prevalent among disproportionately affected groups are known to hinder breastfeeding initiation and duration rates and increase the risk of negative health outcomes in childhood, such as obesity.^57,58 The variation in weight outcome measurement reported across studies complicated synthesis efforts in the present review. Research from a large cohort study found BMIz, compared to WLZ, measured during early infancy had higher predictive power for subsequent obesity risk.⁵⁹ In addition, two systematic reviews have highlighted the clinical utility of WAZ as a measure of rapid infant weight gain.^60,61 Therefore, future work should report growth findings in both WAZ and BMIz to enhance interpretability and generalizability. Finally, the variation in the groups used for comparison (direct breastfeeding, infant formula feeding, or both) across the included studies further complicated the synthesis efforts of the present review. Most of the included studies (four of six studies), utilized both fed at the breast and fed infant formula as comparators.^23,51,53,55 The two remaining studies had only infant formula⁵⁴ or fed directly at the breast as the comparators.⁵² Large, nationally representative samples of both infants fed infant formula and fed directly at the breast are needed in future research to better elucidate the effect of expressed human milk feeding on infant weight trajectories.

Strengths and limitations

This review has several strengths. The literature search was conducted using multiple databases, search term development was done in consultation with a librarian, and the screening, initial analysis, and quality assessment portions of this review were conducted independently by two reviewers using evidence-informed and validated tools. The review, however, also has several limitations. This review excluded publications in the gray literature, such as dissertations and conference abstracts, and therefore is subject to publication bias.^62,63 There was limited diversity among the included samples and significant heterogeneity in reported weight-related outcomes and comparison groups utilized, which greatly limited the comparison and synthesis of findings across studies.

Future directions for health policy and research

Additional research among infants receiving expressed human milk via bottle is essential to helping mothers meet the WHO and AAP’s recommendations for exclusive breastfeeding. Labiner-Wolfe et al.²⁹ reported working mothers were four to six times more likely to engage in expressing human milk than nonworking mothers. Globally, half of working-age women were employed outside of the household in 2020.⁶⁴ Further, women were found to provide half or more of the earnings in roughly one-third and 41% of households in the United States⁶⁵ and Canada, respectively.⁶⁶ This highlights a critical need for changes in health policy to lengthen parental leave and provide lactation support at work.

Based on findings from this review, it is plausible that expressed human milk feeding may exhibit different weight gain trajectories or function of weight (e.g., WAZ) measurements than their formula-fed and fed-at-the-breast counterparts. Azad et al.⁵¹ described infants fed expressed human milk exhibited BMIz and weight gain velocities (measured via change in WAZ) at 12 months of age that were “intermediate” or in-between infants fed infant formula or fed directly at the breast. The pilot study conducted by Bartok⁵² found a higher percentage of infants above the 85th percentile for weight on WHO growth charts among infants fed human milk via bottle compared with infants fed directly at the breast. The results of the pilot study did not reach statistical significance; however, a post-hoc analysis revealed that larger infant feeding groups in both feeding conditions would reach significance. Finally, Li et al.²³ found that among infants fed only human milk, infants grouped into having “high bottle feedings” gained more weight, measured in grams per month, than infants grouped into having “low bottle feedings.” Future research with comparison groups of both formula and fed directly at the breast is needed to determine if these patterns can be corroborated and if they are clinically meaningful.

The current review highlights significant gaps in the literature. High-quality, longitudinal cohort studies with large sample sizes that observe weight change patterns from birth throughout childhood are needed to better understand the effect of expressed human milk feeding on infant weight trajectories. Further, the included studies used various definitions to define expressed human milk feeding groups with some studies grouping expressed human milk-fed infants with partially human milk-fed infants. In future studies, it is important to fully separate or define the amount of expressed milk feedings. Finally, the current review can serve as a call for action for researchers exploring infant nutrition in relation to health outcomes. In order to best understand the benefits of human milk, the complexity of human milk feeding must be accounted for in future study designs. Infant feeding is a dyadic, complex interaction that will require future studies to account for variations in feeding styles and intake in addition to the milk content and delivery mode.

Conclusions

The current review identified six studies exploring the association between infant weight change among infants fed expressed human milk. The synthesis from the few studies included in this review supports a difference in infant weight gain patterns observed among expressed human milk-fed infants when compared with their respective feeding groups (directly breastfed or formula-fed). What is unclear at this time is if the difference in infant weight gain patterns among infants who are fed expressed human milk exclusively or the majority of the time results in a unique, “intermediate” pattern of weight gain when compared with their breastfed and formula-fed counterparts or in patterns of infant weight gain similar to the patterns observed among infants fed formula. This could be concerning if infants fed expressed human milk via a bottle therefore might have a higher propensity for obesity later in life, similar to the risk seen among formula-fed infants via a bottle.⁶² There is some evidence that suggests metabolic hormones in human milk (e.g., adiponectin)¹⁹ have been found to be unaffected by storage and handling processes and thus may be protective even when an infant is fed expressed milk via bottle.

This research could serve as a call to action for clinicians to accurately document infant feeding practices in the pediatric primary care setting. Two of the authors of this article work(ed) in these settings and are critically aware that there is a lack of detailed description of infant feeding practices. Explicit documentation of the route of feeding (at breast, bottle, or other mode) and what is being fed in the bottle (human milk and/or formula) is crucial in order to conduct future research to truly understand the clinical significance of differences in weight patterns.

Footnotes

Acknowledgments

The authors wish to acknowledge Richard James, former Penn Nursing Liaison Librarian, for his insightful commentary and feedback during the development of the literature search strategy.

Authors’ Contributions

C.N.S. and A.M.C. contributed to the conceptualization and methodology of this work. C.N.S. and N.A.J. contributed to the formal analysis of this work. A.M.C. contributed to the supervision of this work. All authors substantially contributed to drafting or revising the article. All authors approved the final version of this article and took responsibility for its content.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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