Abstract.
Breastfeeding is recommended as the ideal nutrient source for infants, with the benefit of reducing future metabolic risk. Rapid catch-up growth in infancy has been associated with increased later adiposity and cardiometabolic risk. Few studies have evaluated growth and feeding patterns in Japanese infants. This study aimed to clarify growth and feeding patterns in Japanese infants. Participants were children enrolled in the Japan Environment and Children’s Study cohort. Height, weight, and body mass index (BMI) at 3–4 and 8–12 mo, and 1, 1.5, 2, 2.5, and 3 yr were compared between three feeding patterns at 6 mo: breast-, formula-, and combination-feeding. The breast-, combination-, and formula-feeding groups comprised 19,987, 8,804, and 5,071 infants, respectively. In the combination-feeding group, measured indices at 3–4 mo were lower than in the breastfeeding group (p < 0.0001), although combination-fed infants showed catch-up growth from 8–12 mo to 1 yr (p < 0.05). Breastfed infants showed rapid growth and high BMI from birth to 3–4 mo, and slow growth and low BMI after 8–12 mo. Combination- and formula-fed infants showed slow growth in early infancy then rapid growth. Catch-up pattern observed in combination- and formula-fed infants warrants growth monitoring and access to individualized feeding support.
Keywords: breastfeeding, infant formula, body mass index, body weight, height
Highlights
● Growth and feeding patterns were analyzed in Japanese infants.
● Breastfed infants grow rapidly early, then slow after 8–12 mo.
● Combination- and formula-fed infants grow slowly, then rapidly catch up.
Introduction
Breast milk provides the ideal balance of nutrients for infants and contains many bioactive ingredients, such as immunoglobulins, hormones, and oligosaccharides (1). These ingredients help infants’ body and brain development (2), shape gut microbiota (3), reduce allergic disease risk (4), promote appropriate weight gain (5), and reduce the risk of becoming overweight (6,7,8,9). Breastfeeding offers a natural way for infants to ingest milk, with the benefit of reducing the future metabolic risk (10,11,12).
Early growth trajectories are also relevant to later metabolic health: rapid infancy weight gain or catch-up growth has been consistently associated with increased risk of later obesity (10, 13), and early-life nutrition in the first 1,000 days may program later cardiometabolic risk (14, 15). Therefore, clarifying how early feeding patterns relate to growth trajectories provides clinically meaningful context for later metabolic risk.
The benefits of breastfeeding are well known. However, breastfeeding is sometimes impossible because of certain factors, and formula milk may be substituted for or added to breast milk. However, because mothers have difficulty assessing the amount of breast milk their infant receives, they cannot control the total amount of breast and formula milk (16). Clarifying growth patterns among infants receiving breastfeeding, formula-feeding, and combination breast- and formula-feeding (combination-feeding) is necessary to assess adequate growth and growth patterns for each feeding pattern. Because there are differences in infant growth among different ethnicities (17,18,19), data for the growth of Japanese infants are needed to assess growth patterns according to breastfeeding pattern in Japan.
In this study, we aimed to compare the growth of infants who were fed breast milk, formula milk, and combination breast and formula milk using data from a large birth cohort. We also aimed to show the characteristics of the patterns of growth indices for Japanese infants and clarify how breastfeeding patterns during early infancy influence children’s growth.
Methods
Enrollment
Data were collected from the Japan Environment and Children’s Study (JECS) (20). A total of 104,062 infants were registered between January 2011 and March 2014 from 15 regional centers across Japan (21). We used JECS data for “jecs-ta-20190930-qsn,” in this study.
Exposure and outcome variables
The JECS questionnaire was provided directly or sent by mail to caregivers when the enrolled children were aged 1 and 6 mo, and 1, 1.5, 2, 2.5, and 3 yr. The questionnaire collected anthropometric data, and the type of milk fed at age 6 mo. The infants’ height and weight data for early infancy were provided at birth (in the 1-mo survey) and 3–4 mo (in the 6-mo survey), and data for middle infancy (8–12 mo) were provided in the 1-yr survey. The height and weight data of the surveys at 1.5, 2, 2.5, and 3 yr of age were the most recent data at 1.5, 2, 2.5, and 3 yr of age, respectively.
The study population comprised singleton infants with the following characteristics: gestational age: 37 wk 0 d to 41 wk 6 d and birth weight 2500–4000 g, based on pregnancy history and maternal information reported at 1 mo; available height and weight measurements at six time points: birth and 3–4 mo (early infancy) and 8–12 mo of age (middle infancy), and 1.5, 2, 2.5, and 3 yr of age; and mothers without type 1 or type 2 diabetes, gestational diabetes, or thyroid disease.
The infants were categorized into three groups on the basis of the information provided for 6 mo of age as breastfeeding, formula-feeding, and combination-feeding (combined breast- and formula-feeding). We enrolled 19,987, 8804, and 5071 children as the breast-, combination-, and formula-feeding groups, respectively.
We compared trajectories for height, weight, and body mass index (BMI) among the three groups at the six assessment points to assess growth outcomes. BMI was calculated as weight in kilograms divided by height in meters squared. We compared the growth indices between the three groups by sex to exclude sex differences in growth. We also compared growth indices among the three groups in all infants in the JECS cohort.
Statistical analysis
We used t-tests or chi-square tests to compare anthropometric data and the proportions of specific variables in the breastfeeding group with the formula- and combination-feeding groups. We also evaluated differences in anthropometrics between the formula-feeding and combination-feeding groups versus the breastfeeding group. P < 0.05 was considered statistically significant, and all statistical tests and descriptive analyses were performed using SAS statistical software (version 9.4; SAS Institute Inc., Cary, NC, USA).
Ethics approval
The JECS protocol was reviewed and approved by the Ministry of the Environment’s Institutional Review Board on Epidemiological Studies (approval no. 100910001) and the Ethics Committees of all participating institutions. The study was performed in accordance with the ethical guidelines of the Declaration of Helsinki. Written informed consent was obtained from all parents for the use of their infants’ data.
Results
The number of infants (percentage of boys) in the breastfeeding, combination-feeding, and formula-feeding groups was 19,987 (50.8%), 8804 (52.7%), and 5071 (51.3%), respectively (Table 1). The proportion of infants for whom weaning began at 6 mo was highest in the combination-feeding group (91.7%), followed by the formula-feeding (90.3%) and breastfeeding (90.2%) groups.
Table 1. Characteristics of term singleton normal birth weight infants divided into the breast-, combination-, and formula-feeding groups.
Tables 2 and 3 show the average weight, height, and BMI for each group and age time point. At 3–4 mo, the combination-feeding group showed a lower mean weight and BMI than the breastfeeding group. In contrast, from 1.5 to 3 yr, weight and height were generally higher in the combination- and formula-feeding groups than those in the breastfeeding group, with small between-group differences in BMI. The combination-feeding group had the lowest mean BMI at ages 3–4 mo and 8–12 mo. The mean BMI in the breastfeeding group was highest at 3–4 mo and lowest at 1–2 yr of age. We also constructed three tables for all infants in the JECS cohort, corresponding to Supplementary Tables 1, 2, 3.
Table 2. Physical indices for term singleton normal birth weight boys divided into the breast-, combination-, and formula-feeding groups.
Table 3. Physical indices for term singleton normal birth weight girls by the breast-, combination-, and formula-feeding groups.
Figure 1 shows the mean differences in weight, height, and BMI between the three groups from 3–4 mo to 3 yr of age. The mean height and BMI for boys and girls in the combination-feeding group were significantly lower versus the breastfeeding group at 3–4 mo and 8–12 mo in boys, and 3–4 mo in girls (p < 0.0001).
Fig. 1.
Mean difference in height, weight, and body mass index in term singleton normal birth weight infants for the formula- and combination-feeding groups compared with the breastfeeding group. a) Mean weight in boys compared with breastfeeding; b) Mean weight in girls compared with breastfeeding; c) Mean height in boys compared with breastfeeding; d) Mean height in girls compared with breastfeeding; e) Mean BMI in boys compared with breastfeeding; f) Mean BMI in girls compared with breastfeeding. Gray line, combination-feeding group; Dashed line, formula-feeding group. BMI, body mass index. * < 0.05, ** < 0.001 vs. the breastfeeding group; t-test.
Discussion
This study showed that infants’ growth patterns differed depending on feeding pattern (breastfeeding, formula-feeding, or combination-feeding). Breastfed infants showed higher BMI than the other two feeding groups at 3–4 mo of age. The formula- and combination-feeding groups showed slow growth until 3–4 mo or 8–12 mo of age and rapid growth after 1 yr of age. The strengths of this study include the large nationwide birth cohort, restriction to term singleton infants with normal birth weight, and evaluation of three feeding patterns (breast-, formula-, and combination-feeding), enabling description of growth trajectories that reflect real-world childcare practices.
Breastfeeding reduces the risk of obesity and diabetes compared with formula-feeding (6,7,8,9). Notably, the different growth patterns seen in the combination-feeding group in our study may indicate the same metabolic risk as that with formula-feeding (6,7,8,9).
There are conflicting reports regarding growth rates in breastfed infants, with some studies indicating rapid growth (22, 23), and others slow growth (5, 23, 24). Previous studies in White populations reported that breastfed infants showed slower growth than formula-fed infants, and this trend continued after the start of weaning (5, 23, 24). However, in the current study, growth to at least 1 yr of age was better in the breastfed group, although the rate slowed after 1 yr. Notably, previous reports compared breastfeeding and formula-feeding, with few reports on combination-feeding.
There are several possible explanations for the mechanism underlying the growth pattern in our study. First, formula- and combination-feeding may not explain the slow growth because slow growth might have been the reason for formula- or combination-feeding. Infants who did not obtain sufficient breast milk and who were supplemented with formula milk were included in the formula-feeding and combination-feeding groups, whereas the breastfeeding group might have included those who gained sufficient weight with breast milk only. However, our findings indicated appropriate growth in the breastfeeding group and a risk for inadequate growth in the combination-feeding group. Second, low birth weight infants, and multiple birth infants, might have influenced the growth rate and delayed the onset of rapid growth, as has been reported among small for gestational age infants (25). In our study, although we limited our analysis to gestational age, birth weight, and singleton births, a similar trend was observed (Supplementary Tables 1, 2, 3). Third, there may be ethnic differences in neonatal feeding and growth. Studies from Brazil (22), Italy (23), and Japan (17) reported different growth patterns compared with growth standards in the USA (26) and those of the World Health Organization (27).
The persistence of between-group differences after the transition to complementary feeding is consistent with the concept that early-life nutrition, particularly during the first 1,000 days, which can have long-term implications for growth and metabolic health (11). In line with this perspective, it is reported that infant feeding patterns and breastfeeding duration influence subsequent BMI more significantly than the timing of weaning initiation (13).
Several factors may contribute to rapid growth in breastfed infants. Breast milk has a low metabolic load (28, 29) because it has the optimum composition for infants. Additionally, breast milk may contribute to infants’ health by reducing the onset and severity of infectious diseases (29). Breastfed infants may also obtain sufficient milk, which promotes growth.
Regarding BMI at 3 yr in boys, the mean BMI values were very close across groups (Table 2), suggesting convergence by age 3 yr. The slightly lower mean BMI in the formula-feeding group compared with that in the breastfeeding and combination-feeding groups may reflect minor differences in linear growth and unmeasured dietary patterns post age 6 mo; the clinical importance of this small difference is unclear and requires confirmation (10, 11, 13).
The formula- and combination-feeding groups initially showed slow growth, followed by rapid growth. The combination-feeding group showed slow growth until 3–4 mo of age, but higher BMI after 2 yr of age. This group might have included infants who had difficulty gaining weight because of insufficient breastmilk feeding (30). Although infants in the combination-feeding group were also breastfed, undernutrition may lead to a subsequent predictive adaptive response. In our opinion, rapid growth in breastfed infants up to age 3–4 mo can be considered normal for Japanese infants and does not reflect excessive breast milk intake.
Our study has several limitations. First, the questionnaire time points and the time points for the anthropometric indices were not the same. However, because the infants’ ages were the same in all feeding groups, we consider that the time difference did not affect the group comparisons. Second, fully breastfed infants at age 3–4 mo might have been able to grow sufficiently with breastfeeding alone, and infants whose breastfeeding was interrupted (e.g., because of illness) might have been classified as non-breastfed infants. Third, previous reports evaluated feeding patterns at age 3 mo; however, we examined feeding data from age 6 mo. Therefore, direct comparisons of our findings with those in previous reports may be difficult. The proportion of breastfed infants at age 6 mo was similar to that reported by the national nutrition survey on preschool children, which evaluated 3-mo-old infants (56.6% vs. 54.7%, respectively) (16). However, it is possible that the feeding patterns evaluated in this study could be divided more accurately by the age in mo when the feeding amount was increased. Fourth, we classified feeding pattern by the type of milk and did not evaluate the amounts fed. Therefore, we could compare growth patterns only by breast-, formula-, combination-feeding. Given these limitations, our findings should be interpreted as describing associations rather than causation. Nevertheless, the catch-up growth pattern observed in the combination-feeding group suggests that some infants may benefit from careful growth monitoring and timely access to individualized feeding support, particularly when early weight gain is suboptimal (30).
In this study, breastfed infants showed rapid growth and high BMI until 3–4 mo of age and slow growth and low BMI after 8–12 mo of age. Combination- and formula-fed infants showed slow growth until 3–4 mo of age, then rapid growth. These findings suggest that the milk amounts in combination-fed infants may be inadequate. Although mothers who breastfeed often have a strong desire to continue breastfeeding and avoid formula feeding (31), medically indicated supplemental feeding is necessary in certain situations, and inappropriate avoidance of supplementation may compromise newborn safety (30). Therefore, breastfeeding guidance may be needed on the basis of an infant’s weight gain.
In conclusion, the growth patterns of Japanese infants differed depending on the type of milk fed at age 6 mo. Breastfed infants initially showed rapid growth, and formula- and combination-fed infants showed catch-up growth, with a higher BMI at 2–3 yr of age. Careful follow-up of subsequent growth may be necessary regarding metabolic risks and catch-up compensatory growth in combination-fed infants, as for formula-fed infants.
Conflicts of interests
The authors declare no conflicts of interest.
Supplementary
Acknowledgements
The authors are grateful to the participants of the JECS. The findings and conclusions of this study are solely the responsibility of the authors and do not represent the official views of the Ministry of the Environment, Japan. Members of the JECS Group as of 2024: Michihiro Kamijima (Principal Investigator, Nagoya City University, Nagoya, Japan), Shin Yamazaki (National Institute for Environmental Studies, Tsukuba, Japan), Maki Fukami (National Center for Child Health and Development, Tokyo, Japan), Reiko Kishi (Hokkaido University, Sapporo, Japan), Chiharu Ota (Tohoku University, Sendai, Japan), Koichi Hashimoto (Fukushima Medical University, Fukushima, Japan), Chisato Mori (Chiba University, Chiba, Japan), Shuichi Ito (Yokohama City University, Yokohama, Japan), Ryoji Shinohara (University of Yamanashi, Chuo, Japan), Hidekuni Inadera (University of Toyama, Toyama, Japan), Takeo Nakayama (Kyoto University, Kyoto, Japan), Ryo Kawasaki (Osaka University, Suita, Japan), Yasuhiro Takeshima (Hyogo Medical University, Nishinomiya, Japan), Seiji Kageyama (Tottori University, Yonago, Japan), Narufumi Suganuma (Kochi University, Nankoku, Japan), Shoichi Ohga (Kyushu University, Fukuoka, Japan), and Takahiko Katoh (Kumamoto University, Kumamoto, Japan).
References
- 1.Wiciński M, Sawicka E, Gębalski J, Kubiak K, Malinowski B. Human milk oligosaccharides: health benefits, potential applications in infant formulas, and pharmacology. Nutrients 2020;12: 266. doi: 10.3390/nu12010266 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Clapp M, Aurora N, Herrera L, Bhatia M, Wilen E, Wakefield S. Gut microbiota’s effect on mental health: The gut-brain axis. Clin Pract 2017;7: 987. doi: 10.4081/cp.2017.987 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Planer JD, Peng Y, Kau AL, Blanton LV, Ndao IM, Tarr PI, et al. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature 2016;534: 263–6. doi: 10.1038/nature17940 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Viggiano C, Occhinegro A, Siano MA, Mandato C, Adinolfi M, Nardacci A, et al. Analgesic effects of breast-and formula feeding during routine childhood immunizations up to 1 year of age. Pediatr Res 2021;89: 1179–84. [DOI] [PubMed] [Google Scholar]
- 5.Azad MB, Vehling L, Chan D, Klopp A, Nickel NC, McGavock JM, et al. CHILD Study InvestigatorsInfant feeding and weight gain: separating breast milk from breastfeeding and formula from food. Pediatrics 2018;142: e20181092. doi: 10.1542/peds.2018-1092 [DOI] [PubMed] [Google Scholar]
- 6.Ziegler EE. Growth of breast-fed and formula-fed infants. Protein and energy requirements in infancy and childhood. 58: Karger Publishers; 2006. p. 51-64. [Google Scholar]
- 7.Mueller E, Blaser M. Breast milk, formula, the microbiome and overweight. Nat Rev Endocrinol 2018;14: 510–1. doi: 10.1038/s41574-018-0066-5 [DOI] [PubMed] [Google Scholar]
- 8.Yan J, Liu L, Zhu Y, Huang G, Wang PP. The association between breastfeeding and childhood obesity: a meta-analysis. BMC Public Health 2014;14: 1267. doi: 10.1186/1471-2458-14-1267 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Arenz S, Rückerl R, Koletzko B, von Kries R. Breast-feeding and childhood obesity--a systematic review. Int J Obes Relat Metab Disord 2004;28: 1247–56. doi: 10.1038/sj.ijo.0802758 [DOI] [PubMed] [Google Scholar]
- 10.Monteiro POA, Victora CG. Rapid growth in infancy and childhood and obesity in later life--a systematic review. Obes Rev 2005;6: 143–54. doi: 10.1111/j.1467-789X.2005.00183.x [DOI] [PubMed] [Google Scholar]
- 11.Zheng M, Campbell KJ, Baur L, Rissel C, Wen LM. Infant feeding and growth trajectories in early childhood: the application and comparison of two longitudinal modelling approaches. Int J Obes (Lond) 2021;45: 2230–7. doi: 10.1038/s41366-021-00892-5 [DOI] [PubMed] [Google Scholar]
- 12.Victora CG, Bahl R, Barros AJD, França GVA, Horton S, Krasevec J, et al. Lancet Breastfeeding Series Group.Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 2016;387: 475–90. doi: 10.1016/S0140-6736(15)01024-7 [DOI] [PubMed] [Google Scholar]
- 13.Woo Baidal JA, Locks LM, Cheng ER, Blake-Lamb TL, Perkins ME, Taveras EM. Risk factors for childhood obesity in the first 1,000 days: A systematic review. Am J Prev Med 2016;50: 761–79. doi: 10.1016/j.amepre.2015.11.012 [DOI] [PubMed] [Google Scholar]
- 14.Schwarzenberg SJ, Georgieff MK. Advocacy for improving nutrition in the first 1,000 days to support childhood development and adult health. Pediatrics 2018;141: e20173716. doi: 10.1542/peds.2017-3716 [DOI] [PubMed] [Google Scholar]
- 15.Meek JY, Noble L, Section on Breastfeeding. Policy Statement: Breastfeeding and the Use of Human Milk. Pediatrics 2022;150: e2022057988. doi: 10.1542/peds.2022-057988 [DOI] [PubMed] [Google Scholar]
- 16.The Ministry of Health Labour and Welfare. National nutrition survey on preschool children in 2015. 2016.
- 17.Tanaka H, Ishii H, Yamada T, Akazawa K, Nagata S, Yamashiro Y. Growth of Japanese breastfed infants compared to national references and World Health Organization growth standards. Acta Paediatr 2013;102: 739–43. doi: 10.1111/apa.12262 [DOI] [PubMed] [Google Scholar]
- 18.Anstey EH, Chen J, Elam-Evans LD, Perrine CG. Racial and geographic differences in breastfeeding - United States, 2011-2015. MMWR Morb Mortal Wkly Rep 2017;66: 723–7. doi: 10.15585/mmwr.mm6627a3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Grummer-Strawn L, Krebs NF, Reinold CM. Use of World Health Organization and CDC growth charts for children aged 0-59 months in the United States. 2009. [PubMed]
- 20.Kawamoto T, Nitta H, Murata K, Toda E, Tsukamoto N, Hasegawa M, et al. Working Group of the Epidemiological Research for Children’s Environmental Health. Rationale and study design of the Japan environment and children’s study (JECS). BMC Public Health 2014;14: 25. doi: 10.1186/1471-2458-14-25 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Iwai-Shimada M, Nakayama SF, Isobe T, Michikawa T, Yamazaki S, Nitta H, et al. Japan Environment and Children’s Study Group. Questionnaire results on exposure characteristics of pregnant women participating in the Japan Environment and Children Study (JECS). Environ Health Prev Med 2018;23: 45. doi: 10.1186/s12199-018-0733-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Victora CG, Morris SS, Barros FC, de Onis M, Yip R. The NCHS reference and the growth of breast- and bottle-fed infants. J Nutr 1998;128: 1134–8. doi: 10.1093/jn/128.7.1134 [DOI] [PubMed] [Google Scholar]
- 23.Agostoni C, Grandi F, Giannì ML, Silano M, Torcoletti M, Giovannini M, et al. Growth patterns of breast fed and formula fed infants in the first 12 months of life: an Italian study. Arch Dis Child 1999;81: 395–9. doi: 10.1136/adc.81.5.395 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Dewey KG. Growth characteristics of breast-fed compared to formula-fed infants. Biol Neonate 1998;74: 94–105. doi: 10.1159/000014016 [DOI] [PubMed] [Google Scholar]
- 25.Ong KK. Catch-up growth in small for gestational age babies: good or bad? Curr Opin Endocrinol Diabetes Obes 2007;14: 30–4. doi: 10.1097/MED.0b013e328013da6c [DOI] [PubMed] [Google Scholar]
- 26.Hamill PV, Drizd TA, Johnson CL, Reed RB, Roche AF. NCHS growth curves for children birth-18 years. Department of Health Education and Welfare Washington DC; 1977. [PubMed]
- 27.World Health Organization. WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development: World Health Organization; 2006.
- 28.Andreas NJ, Kampmann B, Mehring Le-Doare K. Human breast milk: A review on its composition and bioactivity. Early Hum Dev 2015;91: 629–35. doi: 10.1016/j.earlhumdev.2015.08.013 [DOI] [PubMed] [Google Scholar]
- 29.Hanson LA, Korotkova M. The role of breastfeeding in prevention of neonatal infection. Semin Neonatol 2002;7: 275–81. doi: 10.1053/siny.2002.0124 [DOI] [PubMed] [Google Scholar]
- 30.Kellams A, Harrel C, Omage S, Gregory C, Rosen-Carole C. ABM clinical protocol #3: supplementary feedings in the healthy term breastfed neonate, revised 2017. Breastfeed Med 2017;12: 188–98. doi: 10.1089/bfm.2017.29038.ajk [DOI] [PubMed] [Google Scholar]
- 31.Ayton J, Hansen E, Quinn S, Nelson M. Women’s experiences of ceasing exclusive breastfeeding: a qualitative study. BMJ Open 2019;9: e026234. doi: 10.1136/bmjopen-2018-026234 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.