Next Article in Journal
Nutritional Status of Children with Newly Diagnosed Food Allergies
Previous Article in Journal
A Systematic Review of Clinical Practice Guidelines for Neonatal Abstinence Syndrome
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Children
Volume 10
Issue 10
10.3390/children10101686
children-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Breast and Formula Milk and Early Puberty Onset

by
Valeria Calcaterra
1,2,†,
Hellas Cena
3,4,*,†,
Francesca Sottotetti
3,
Virginia Rossi
2,
Federica Loperfido
3 and
Gianvincenzo Zuccotti
2,5
1
Department of Internal Medicine and Therapeutics, University of Pavia, 27100 Pavia, Italy
2
Pediatric Department, Buzzi Children’s Hospital, 20154 Milano, Italy
3
Laboratory of Dietetics and Clinical Nutrition, Department of Public Health, Experimental and Forensic Medicine, University of Pavia, 27100 Pavia, Italy
4
Clinical Nutrition Unit, General Medicine, Istituti Clinici Scientifici Maugeri IRCCS, 27100 Pavia, Italy
5
Department of Biomedical and Clinical Science, University of Milano, 20157 Milano, Italy
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Children 2023, 10(10), 1686; https://doi.org/10.3390/children10101686
Submission received: 10 September 2023 / Revised: 12 October 2023 / Accepted: 12 October 2023 / Published: 14 October 2023
(This article belongs to the Section Pediatric Gastroenterology and Nutrition)
Browse Figure
Versions Notes

Abstract

:
Nutrients have an enormous impact on many hormonal systems and aspects of health, and nutrition status is a crucial regulator of growth and pubertal development in children and adolescents. In this narrative review, we explore the connection between these feeding methods and the timing of puberty to provide a clearer understanding of how infant nutrition might contribute to the early development of puberty. Puberty is a key stage in the transition from childhood to adulthood and the timing of puberty represents a significant biological milestone of growth. Breast milk seems to have a pivotal role in puberty onset, mainly due to its dynamism, which shape indirectly the gut microbiota in early life, besides direct exposure of the baby to the milk microbiota through gut–breast axis. Concerning breast and formula milk and their effects on the onset of puberty, a protective role of the former occurs. As for the potential harmful effects of soy-based formulas and the isoflavones that they contain, the studies reported demonstrate conflicting opinions, underlining the need for further research on this topic. A healthy and well-nourished diet from the earliest stages of life has significant preventive potential for overall well-being, reducing the risk of many health problems later in life.

1. Introduction

Nutrients have an enormous impact on many hormonal systems and aspects of health and nutrition status is a crucial regulator of growth and pubertal development in children and adolescents [1,2,3].
Puberty is a key stage in the transition from childhood to adulthood and the timing of puberty represents a significant biological milestone of growth [4,5]. Puberty timing is influenced by a range of factors, including nutrition, genetics, body mass index (BMI), endocrine disrupting chemicals [6]. Recent studies have sparked interest in investigating the impact of early childhood feeding practices, particularly breast milk and formula milk, on the onset of puberty.
Regarding breastfeeding, the World Health Organization (WHO) recommends it at least up to 6 months because of the positive impact on both mother and newborn health [7,8]. It is in fact known that breastfed infants have a lower risk of incurring respiratory, allergic, gastroenterological and endocrinological pathologies, compared to non-breastfed ones [9] However, since breastfeeding might not always be possible, infant formulae (IF) have been developed over the years and companies attempt to make it as similar as possible to breast milk, even if the latter presents a unique composition that is difficult to reproduce [10].
In this narrative review, we explore the characteristics of breast milk and formula milk and the connection between these feeding methods and the timing of puberty to provide a clearer understanding of how infant nutrition might contribute to the early development of puberty. This review seeks to shed light on the practical implications of early life nutrition in shaping pubertal patterns, considering both physiological and social aspects of this intricate relationship.

2. Methods

To conduct the narrative review, specific inclusion criteria were established: articles written in English, meta-analyses, clinical trials, and reviews focusing on the subject within the last twenty years were considered. Case reports and series were excluded. The review utilized the electronic databases PubMed, Scopus, and Web of Science. Relevant keywords were used either individually or in combination. The key words used for this research alone or/and in association were breastfeeding, formula feeding, infant formula, milk, puberty, early puberty onset, and precocious puberty. The time period for conducting keyword search was 2003–2023. Starting with a total of 190 papers, the authors independently assessed abstracts (n = 142) and then examined full texts to identify potentially relevant studies (n = 98) from the literature (Figure 1). Additionally, the reference lists of all articles were reviewed to find pertinent studies.

3. Breast Milk and Early Puberty Onset

Nutrition plays a pivotal role in the development of puberty [1]. The connection between nutrition and the puberty onset is closely linked to the relationship between the amount of food intake and weight gain pattern, sometimes leading to obesity [2,3]. Early life nutrition, before two years of age, splits into breastfeeding or formula feeding and, later, complementary foods [6].
Breast milk is the ideal initial food for newborns, with recommendations from the WHO) [8], the Academy of Nutrition and Dietetics [11] and the American Academy of Pediatrics (AAP) supporting exclusive breastfeeding for at least the first six months [12]. This recommendation is aligned with guidelines from the American College of Obstetricians and Gynecologists and the Canadian Pediatric Society [13,14]. Furthermore, the Academy of Nutrition and Dietetics recommends associating breastfeeding with the gradual introduction of complementary foods until 12 months of age [11] and the AAP advocates continuing breastfeeding, along with appropriate complementary foods introduced at about 6 months, as long as the mother and baby mutually desire it, for 2 years or more [12].
Early life nutrition continues to have a lasting positive impact on health well into adulthood. Numerous data confirm that breastfed infants experience lower occurrences of various acute and chronic pediatric disorders, such as respiratory, allergologic, gastroenterologic, and endocrinologic conditions, as compared to non-breastfed infants [9]. This beneficial effect may be attributed to the unique biological composition of human milk. Additionally, breastfeeding mothers themselves enjoy a reduced risk of developing type 2 diabetes mellitus, as well as breast, ovarian, and endometrial cancer, and hypertension [9].
Different studies have examined the influence of breastfeeding on pubertal development, but the findings are not always consistent.
Breastfeeding’s influence on the timing of puberty appears to yield varying outcomes based on several studies. Hvidt et al.’s population-based cohort study [15], focusing on 13,511 boys and girls from the Puberty Cohort nested within the Danish National Birth Cohort, found intriguing gender disparities. In boys, the absence of breastfeeding was linked to accelerated pubertal timing. However, for girls, breastfeeding did not show a significant association with pubertal development. Similarly, Al-Sahab et al. [16] found in their population-based cohort study, drawing data from the Cebu Longitudinal Health and Nutrition Survey, that exclusive breastfeeding was negatively associated with early menarche. In contrast, Karaolis-Danckert et al.’s cohort study [17] conducted in Germany suggested that intrauterine and early postnatal growth factors, including full breastfeeding for at least 4 months, influenced markers of puberty onset in both boys and girls independently of prepubertal body composition. Aghaee et al. [18], in their prospective cohort study involving a multiethnic cohort of mother–daughter pairs, reported that the absence of breastfeeding was linked to earlier onset of breast and pubic hair development in girls compared to those breastfed for at least 6 months. Kale et al. [19], in their prospective study encompassing diverse girls across geographic locations, found mixed effects. Mainly breastfed or mixed-fed girls had a delayed breast development onset compared to formula-fed peers, while breastfeeding’s impact on pubic hair development onset was not significant. In contrast, Kwok et al.’s observational cohort study [20] involving the “Children of 1997” cohort from Hong Kong indicated that neither breastfeeding nor childhood milk consumption had a connection with the timing of pubertal onset. Morris et al.’s cohort study [21] in the UK’s Breast Cancer Generations Study showed that breastfeeding correlated with a delayed onset of menarche in women. The Thousand Families Study by Blell et al. [22], a prospective longitudinal cohort study in the UK, revealed that the timing of menarche was not associated with the duration of breastfeeding. On the other hand, Ong et al. [23] demonstrated in the Avon Longitudinal Study of Parents and Children (ALSPAC) cohort that breast milk might act protectively against earlier menarche in girls. Lee et al. [24], in their prospective observational study in South Korea, found that children breastfed for 6 months or more exhibited a protective link against early puberty.
Overall, these studies highlight the complex and sometimes inconsistent role of breastfeeding in influencing the timing of puberty. The outcomes appear to be influenced by factors such as gender, duration of breastfeeding, and other contextual variables, underlining the need for further investigation to better understand these relationships. Table 1 summarizes the results of these studies, selected for their significance.
A plausible link between early life nutrition, breastfeeding duration (if applicable), and the timing of puberty has been elucidated, particularly in relation to the correlation between overweight/obesity and the risk of early puberty. Breastfeeding during the first year of life is a notable factor implied in a reduction of childhood overweight likelihood by 15% in comparison to formula feeding [25]. This protective attribute is linked to divergent growth patterns between breastfed and formula-fed infants [6,26,27]. Breastfed babies typically follow a slower growth curve, a characteristic that appears to safeguard against later-life obesity [6,28,29]. Even after accounting for birth weight, the correlation between rapid weight gain, known as ‘catch-up growth’, and obesity retains significance [30].
The linkage between early life nutrition and the timing of puberty draws from the association between increased weight gain during early childhood and higher childhood BMI, both of which have been linked to an earlier onset of puberty [3,31]. This correlation finds support in the interconnected factors that contribute to the relationship between breast milk and the prevention of excessive weight gain and early puberty. These elements encompass insulin-like growth factor (IGF)-1 levels, leptin levels, bioactive nutrients present in both human and formula milk, the composition of the microbiome, and the aptitude for self-regulated feeding [6,32,33,34]. Elevated IGF-1 levels manifest both in formula-fed infants [32] and infants experiencing swift weight gain in early months [35]. Importantly, increased IGF-1 levels correlate with enhanced sex steroid production, which facilitates secretion of GnRH and subsequent pubertal development [36].
Rapid weight gain during infancy, as shown by Emmett PM et al. [37], associates with increased risk of obesity at five and eight years, coupled with heightened insulin resistance, advanced adrenarche, and reduced sex hormone-binding globulin levels. Notably, Zheng [30] highlighted substantial connections between swift weight gain and obesity, even after birth weight adjustment, thereby suggesting an influence on puberty timing. Li et al. [38] confirmed that breastfeeding was inversely associated with the risk of childhood obesity from 2 to 6 years old, and there was a trend from mixed feeding to exclusive breastfeeding; infant exclusive formula feeding might be a risk factor for childhood underweight at preschool time [38].
Across various nonhuman species, the timing of puberty is influenced by the social environment, carrying implications for reproductive success and behavioral patterns [39]. Within the realm of human beings, although variations in pubertal timing have not yet been systematically investigated concerning social environmental factors, it is noteworthy that their psychological consequences have been documented.
For instance, the quality of child–parent attachment has shown a positive correlation with breastfeeding, and it appears to exert an influence on reproductive development during later stages of life [40,41]. Conversely, maternal depression, which exhibits a negative association with breastfeeding, has been linked to an increased likelihood of early pubertal onset in girls [5,6,42].

4. Formula Milk and Early Puberty Onset

As we already underlined, over the years, it has been studied how early childhood nutrition can influence the pubertal process [5]. Specifically, attention is increasingly directed to the difference between breast milk and formula milk and the effects that these may have on pubertal development [19]. In a study conducted by Novotny R. et al., a sample of girls residing on the island of Oahu was evaluated based on their feeding during early childhood; of the 349 girls enrolled, 59 (17%) were breastfed only, while 242 (71%) were formula fed. The authors concluded that the formula-fed girls were shorter and heavier than the breast-fed ones, resulting in early attainment of menarche [43]. In 2012, a study compared mental, motor, and language development between breastfed infants and infants fed with milk-based formula or soy protein-based formula during the first year of life. The results showed that there were no significant differences between the infants fed with the two types of formulas. However, breastfed infants showed an improved cognitive and psychomotor development compared to formula-fed infants [44]. A prospective cohort investigation revealed that among a sample of 1237 girls aged 6 to 8 years, those mainly nourished through breastfeeding experienced a delayed initiation of breast development compared to those who were formula fed. Moreover, breastfeeding duration was also directly associated with age at the onset breast initiation development [19]. Finally, a randomized controlled trial conducted in 2018 compared a significant group of infants fed cow’s milk formula (CMF) with children who received extensively hydrolyzed formula (EHF). There was a significant difference in the rate of weight gain velocity from 0.75 to 4.5 months (p = 0.002) between the two groups being compared. Specifically, the EHF group gained weight on average by 25.1 ± 0.9 g/d, while the CMF group by 29.0 ± 1.0 g/day. However, there was no difference in length increase [45]. In this scenario, opinions about the use of soy-based formulas are also conflicting, due to the presence of high concentrations of isoflavones and its potential estrogenic effect on infant development [6]. Isoflavones constitute a cluster of phytoestrogens encompassing three primary compounds (genistein, daidzein, and glycitein) with a chemical composition and hormonal effects similar to estradiol [46]. Indeed, a study involving 2920 girls has observed that about 2% had started introducing soy-based formula at or before the age of 4 months. The study’s overall findings revealed that the median age at which the girls experienced menarche was around 12.8 years. However, the girls fed with soy-based formulae experienced menarche by 4 months earlier (12.4 years). Moreover, the girls who consumed soy products had a 25% higher risk of experiencing early onset menarche than girls who were fed formula or non-soy milk (Hazard Ratio of 1.25 (95% confidence interval, 0.92, 1.71)). The authors concluded that exposure to soy isoflavones may have mild endocrine-disrupting effects, potentially leading to the early onset of puberty. Nevertheless, they highlighted that their study had some limitations, primarily due to the relatively small sample size [47]. Otherwise, Sinai et al. found no significant differences in pubertal development, growth, or BMI values in a nested case–control study in which they examined the possible association between soy formula feeding and early pubertal manifestation [48]. More recently, another case–control study demonstrated that exclusive breastfeeding up to 6 months of age was an important protective factor for CPP; instead, soy consumption was positively correlated (r = 0.2; p < 0.01) [46]. Thus, although the association between early soy exposure and early menarche is biologically plausible, different studies have produced conflicting results and further research is needed to elucidate this topic. Table 2 summarizes the papers referring to formula milk and early puberty onset.

5. Conclusions

Nutrition plays a central role in human growth and development, particularly in relation to childhood obesity and the long-term impact of early life nutrition.
Breast milk is a unique source of beneficial bacteria and compounds that shape an infant’s microbiota and influence various bodily functions’ development, such as gastrointestinal, immunological, and neurological.
The timing of puberty is a significant milestone in growth, influenced by early nutrition and breastfeeding, which is associated with lower rates of pediatric disorders. The HPG axis plays a key role in regulating puberty onset, and breast milk’s dynamic composition indirectly affects the gut microbiota, further influencing this process.
Breast milk is believed to have a protective role in puberty onset, while soy-based formulas containing isoflavones have conflicting research findings regarding their potential harmful effects, which require further investigation.
This manuscript, being a narrative review, takes a less formal methodologic approach than systematic reviews, but provides an analysis of how feeding practices during the first stages of life may contribute to infants’ growth processes, including pubertal patterns.
Overall, it emphasizes the importance of a well-nourished diet in early childhood that promotes healthy growth, prevents chronic diseases and supports mental well-being. Establishing healthy dietary habits early in life is considered a key tool for improving long-term health and reducing the burden of chronic disease for both individuals and health systems.

Author Contributions

Conceptualization, V.C., H.C. and G.Z.; methodology, V.C., H.C., V.R., F.S., F.L. and G.Z.; writing—original draft preparation, V.C., H.C., V.R., F.S. and F.L.; writing—review and editing, V.C. and H.C.; supervision, V.C., H.C. and G.Z. All authors have read and agreed to the published version of the manuscript.

Funding

Project funded under the National Recovery and resilience Plan (NRRP), Mission 4 Component 2 Investment 1.3-Call for proposal No. 341 of 15 March 2022 of Italian Ministry of University and Research funded by the European Union-NextGenerationEU. Project code PE00000003, Concession Decree No. 1550 of 11 October 2022 adopted by the Italian Ministry of University and Research, CUP D93C22000890001, Project title “ON Foods-Research and innovation network on food and nutrition Sustainability, Safety and Security-Working ON Foods”.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Soliman, A.; De Sanctis, V.; Elalaily, R. Nutrition and Pubertal Development. Indian J. Endocr. Metab. 2014, 18, 39. [Google Scholar] [CrossRef]
  2. Hong, Y.H.; Woo, Y.J.; Lee, J.H.; Shin, Y.-L.; Lim, H.-S. Association between Dietary Habits and Parental Health with Obesity among Children with Precocious Puberty. Children 2020, 7, 220. [Google Scholar] [CrossRef]
  3. Huang, A.; Roth, C.L. The Link between Obesity and Puberty: What Is New? Curr. Opin. Pediatr. 2021, 33, 449–457. [Google Scholar] [CrossRef]
  4. Abreu, A.P.; Kaiser, U.B. Pubertal Development and Regulation. Lancet Diabetes Endocrinol. 2016, 4, 254–264. [Google Scholar] [CrossRef] [PubMed]
  5. Calcaterra, V.; Cena, H.; Regalbuto, C.; Vinci, F.; Porri, D.; Verduci, E.; Mameli, C.; Zuccotti, G.V. The Role of Fetal, Infant, and Childhood Nutrition in the Timing of Sexual Maturation. Nutrients 2021, 13, 419. [Google Scholar] [CrossRef]
  6. Calcaterra, V.; Verduci, E.; Magenes, V.C.; Pascuzzi, M.C.; Rossi, V.; Sangiorgio, A.; Bosetti, A.; Zuccotti, G.; Mameli, C. The Role of Pediatric Nutrition as a Modifiable Risk Factor for Precocious Puberty. Life 2021, 11, 1353. [Google Scholar] [CrossRef]
  7. Unicef Breastfeeding. Available online: https://data.unicef.org/topic/nutrition/breastfeeding/ (accessed on 15 July 2023).
  8. World Health Organization (WHO) Breastfeeding. Available online: https://www.who.int/health-topics/breastfeeding#tab=tab_1 (accessed on 15 July 2023).
  9. Stoody, E.E.; Spahn, J.M.; Casavale, K.O. The Pregnancy and Birth to 24 Months Project: A Series of Systematic Reviews on Diet and Health. Am. J. Clin. Nutr. 2019, 109, 685S–697S. [Google Scholar] [CrossRef] [PubMed]
  10. Verduci, E.; D’Elios, S.; Cerrato, L.; Comberiati, P.; Calvani, M.; Palazzo, S.; Martelli, A.; Landi, M.; Trikamjee, T.; Peroni, D.G. Cow’s Milk Substitutes for Children: Nutritional Aspects of Milk from Different Mammalian Species, Special Formula and Plant-Based Beverages. Nutrients 2019, 11, 1739. [Google Scholar] [CrossRef] [PubMed]
  11. Lessen, R.; Kavanagh, K. Position of the Academy of Nutrition and Dietetics: Promoting and Supporting Breastfeeding. J. Acad. Nutr. Diet. 2015, 115, 444–449. [Google Scholar] [CrossRef]
  12. Meek, J.Y.; Noble, L. Section on Breastfeeding Policy Statement: Breastfeeding and the Use of Human Milk. Pediatrics 2022, 150, e2022057988. [Google Scholar] [CrossRef]
  13. ACOG Committee Opinion No. 756: Optimizing Support for Breastfeeding as Part of Obstetric Practice. Obstet. Gynecol. 2018, 132, e187–e196. [CrossRef]
  14. Critch, J.N. Canadian Paediatric Society; Nutrition and Gastroenterology Committee Nutrition for Healthy Term Infants, Six to 24 Months: An Overview. Paediatr. Child. Health 2014, 19, 547–552. [Google Scholar]
  15. Hvidt, J.J.; Brix, N.; Ernst, A.; Lunddorf, L.L.H.; Ramlau-Hansen, C.H. Breast Feeding and Timing of Puberty in Boys and Girls: A Nationwide Cohort Study. Paediatr. Perinat. Epidemiol. 2021, 35, 578–589. [Google Scholar] [CrossRef] [PubMed]
  16. Al-Sahab, B.; Adair, L.; Hamadeh, M.J.; Ardern, C.I.; Tamim, H. Impact of Breastfeeding Duration on Age at Menarche. Am. J. Epidemiol. 2011, 173, 971–977. [Google Scholar] [CrossRef] [PubMed]
  17. Karaolis-Danckert, N.; Buyken, A.E.; Sonntag, A.; Kroke, A. Birth and Early Life Influences on the Timing of Puberty Onset: Results from the DONALD (DOrtmund Nutritional and Anthropometric Longitudinally Designed) Study. Am. J. Clin. Nutr. 2009, 90, 1559–1565. [Google Scholar] [CrossRef]
  18. Aghaee, S.; Deardorff, J.; Greenspan, L.C.; Quesenberry, C.P.; Kushi, L.H.; Kubo, A. Breastfeeding and Timing of Pubertal Onset in Girls: A Multiethnic Population-Based Prospective Cohort Study. BMC Pediatr. 2019, 19, 277. [Google Scholar] [CrossRef]
  19. Kale, A.; Deardorff, J.; Lahiff, M.; Laurent, C.; Greenspan, L.C.; Hiatt, R.A.; Windham, G.; Galvez, M.P.; Biro, F.M.; Pinney, S.M.; et al. Breastfeeding Versus Formula-Feeding and Girls’ Pubertal Development. Matern. Child. Health J. 2015, 19, 519–527. [Google Scholar] [CrossRef]
  20. Kwok, M.K.; Leung, G.M.; Lam, T.H.; Schooling, C.M. Breastfeeding, Childhood Milk Consumption, and Onset of Puberty. Pediatrics 2012, 130, e631–e639. [Google Scholar] [CrossRef] [PubMed]
  21. Morris, D.H.; Jones, M.E.; Schoemaker, M.J.; Ashworth, A.; Swerdlow, A.J. Determinants of Age at Menarche in the UK: Analyses from the Breakthrough Generations Study. Br. J. Cancer 2010, 103, 1760–1764. [Google Scholar] [CrossRef]
  22. Blell, M.; Pollard, T.M.; Pearce, M.S. Predictors of Age at Menarche in the Newcastle Thousand Families Study. J. Biosoc. Sci. 2008, 40, 563–575. [Google Scholar] [CrossRef]
  23. Ong, K.K.; Emmett, P.; Northstone, K.; Golding, J.; Rogers, I.; Ness, A.R.; Wells, J.C.; Dunger, D.B. Infancy Weight Gain Predicts Childhood Body Fat and Age at Menarche in Girls. J. Clin. Endocrinol. Metab. 2009, 94, 1527–1532. [Google Scholar] [CrossRef]
  24. Lee, H.A.; Kim, Y.J.; Lee, H.; Gwak, H.S.; Hong, Y.S.; Kim, H.S.; Park, E.A.; Cho, S.J.; Ha, E.H.; Park, H. The Preventive Effect of Breast-Feeding for Longer than 6 Months on Early Pubertal Development among Children Aged 7–9 Years in Korea. Public Health Nutr. 2015, 18, 3300–3307. [Google Scholar] [CrossRef]
  25. Weng, S.F.; Redsell, S.A.; Swift, J.A.; Yang, M.; Glazebrook, C.P. Systematic Review and Meta-Analyses of Risk Factors for Childhood Overweight Identifiable during Infancy. Arch. Dis. Child. 2012, 97, 1019–1026. [Google Scholar] [CrossRef]
  26. Koletzko, B.; Von Kries, R.; Monasterolo, R.C.; Subías, J.E.; Scaglioni, S.; Giovannini, M.; Beyer, J.; Demmelmair, H.; Anton, B.; Gruszfeld, D.; et al. Can Infant Feeding Choices Modulate Later Obesity Risk? Am. J. Clin. Nutr. 2009, 89, 1502S–1508S. [Google Scholar] [CrossRef]
  27. Juul, F.; Chang, V.W.; Brar, P.; Parekh, N. Birth Weight, Early Life Weight Gain and Age at Menarche: A Systematic Review of Longitudinal Studies: Birth Weight Early Life Weight Gain and Age at Menarche. Obes. Rev. 2017, 18, 1272–1288. [Google Scholar] [CrossRef] [PubMed]
  28. Morgen, C.S.; Larsson, M.W.; Ängquist, L.; Sørensen, T.I.A.; Michaelsen, K.F. Overweight in Childhood of Exclusively Breastfed Infants with a High Weight at 5 Months. Matern. Child. Nutr. 2021, 17. [Google Scholar] [CrossRef] [PubMed]
  29. Uwaezuoke, S.N.; Eneh, C.I.; Ndu, I.K. Relationship Between Exclusive Breastfeeding and Lower Risk of Childhood Obesity: A Narrative Review of Published Evidence. Clin. Med. Insights Pediatr. 2017, 11, 117955651769019. [Google Scholar] [CrossRef]
  30. Zheng, M.; Lamb, K.E.; Grimes, C.; Laws, R.; Bolton, K.; Ong, K.K.; Campbell, K. Rapid Weight Gain during Infancy and Subsequent Adiposity: A Systematic Review and Meta-Analysis of Evidence. Obes. Rev. 2018, 19, 321–332. [Google Scholar] [CrossRef]
  31. Wagner, I.V.; Sabin, M.A.; Pfäffle, R.W.; Hiemisch, A.; Sergeyev, E.; Körner, A.; Kiess, W. Effects of Obesity on Human Sexual Development. Nat. Rev. Endocrinol. 2012, 8, 246–254. [Google Scholar] [CrossRef] [PubMed]
  32. Larnkjær, A.; Mølgaard, C.; Michaelsen, K.F. Early Nutrition Impact on the Insulin-like Growth Factor Axis and Later Health Consequences. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15, 285–292. [Google Scholar] [CrossRef]
  33. Tang, J.; Xue, P.; Huang, X.; Lin, C.; Liu, S. Diet and Nutrients Intakes during Infancy and Childhood in Relation to Early Puberty: A Systematic Review and Meta-Analysis. Nutrients 2022, 14, 5004. [Google Scholar] [CrossRef] [PubMed]
  34. Mameli, C.; Mazzantini, S.; Zuccotti, G.V. Nutrition in the First 1000 Days: The Origin of Childhood Obesity. Int. J. Environ. Res. Public Health 2016, 13, 838. [Google Scholar] [CrossRef]
  35. Lyons-Reid, J.; Albert, B.B.; Kenealy, T.; Cutfield, W.S. Birth Size and Rapid Infant Weight Gain-Where Does the Obesity Risk Lie? J. Pediatr. 2021, 230, 238–243. [Google Scholar] [CrossRef]
  36. Wolfe, A.; Divall, S.; Wu, S. The Regulation of Reproductive Neuroendocrine Function by Insulin and Insulin-like Growth Factor-1 (IGF-1). Front. Neuroendocrinol. 2014, 35, 558–572. [Google Scholar] [CrossRef] [PubMed]
  37. Emmett, P.M.; Jones, L.R. Diet, Growth, and Obesity Development throughout Childhood in the Avon Longitudinal Study of Parents and Children. Nutr. Rev. 2015, 73, 175–206. [Google Scholar] [CrossRef]
  38. Li, W.; Yuan, J.; Wang, L.; Qiao, Y.; Liu, E.; Wang, S.; Leng, J. The Association between Breastfeeding and Childhood Obesity/Underweight: A Population-Based Birth Cohort Study with Repeated Measured Data. Int. Breastfeed. J. 2022, 17, 82. [Google Scholar] [CrossRef] [PubMed]
  39. Pham, H.T.; DiLalla, L.F.; Corley, R.P.; Dorn, L.D.; Berenbaum, S.A. Family Environmental Antecedents of Pubertal Timing in Girls and Boys: A Review and Open Questions. Horm. Behav. 2022, 138, 105101. [Google Scholar] [CrossRef]
  40. Belsky, J.; Houts, R.M.; Fearon, R.M.P. Infant Attachment Security and the Timing of Puberty: Testing an Evolutionary Hypothesis. Psychol. Sci. 2010, 21, 1195–1201. [Google Scholar] [CrossRef]
  41. Tharner, A.; Luijk, M.P.C.M.; Raat, H.; IJzendoorn, M.H.; Bakermans-Kranenburg, M.J.; Moll, H.A.; Jaddoe, V.W.V.; Hofman, A.; Verhulst, F.C.; Tiemeier, H. Breastfeeding and Its Relation to Maternal Sensitivity and Infant Attachment. J. Dev. Behav. Pediatr. 2012, 33, 396–404. [Google Scholar] [CrossRef]
  42. Grigoriadis, S.; VonderPorten, E.H.; Mamisashvili, L.; Tomlinson, G.; Dennis, C.-L.; Koren, G.; Steiner, M.; Mousmanis, P.; Cheung, A.; Radford, K.; et al. The Impact of Maternal Depression during Pregnancy on Perinatal Outcomes: A Systematic Review and Meta-Analysis. J. Clin. Psychiatry 2013, 74, e321–e341. [Google Scholar] [CrossRef] [PubMed]
  43. Novotny, R.; Daida, Y.G.; Grove, J.S.; Acharya, S.; Vogt, T.M. Formula Feeding in Infancy Is Associated with Adolescent Body Fat and Earlier Menarche. Cell. Mol. Biol. (Noisy-Le-Grand) 2003, 49, 1289–1293. [Google Scholar] [PubMed]
  44. Andres, A.; Cleves, M.A.; Bellando, J.B.; Pivik, R.T.; Casey, P.H.; Badger, T.M. Developmental Status of 1-Year-Old Infants Fed Breast Milk, Cow’s Milk Formula, or Soy Formula. Pediatrics 2012, 129, 1134–1140. [Google Scholar] [CrossRef]
  45. Mennella, J.A.; Inamdar, L.; Pressman, N.; Schall, J.I.; Papas, M.A.; Schoeller, D.; Stallings, V.A.; Trabulsi, J.C. Type of Infant Formula Increases Early Weight Gain and Impacts Energy Balance: A Randomized Controlled Trial. Am. J. Clin. Nutr. 2018, 108, 1015–1025. [Google Scholar] [CrossRef] [PubMed]
  46. Felício, J.S.; De Alcântara, A.L.; Janaú, L.C.; De Moraes, L.V.; De Oliveira, M.C.N.I.; De Lemos, M.N.; De Souza Neto, N.J.K.; Neto, J.F.A.; Da Silva, W.M.; De Souza, Í.J.A.; et al. Association of Soy and Exclusive Breastfeeding with Central Precocious Puberty: A Case-Control Study. Front. Endocrinol. 2021, 12, 667029. [Google Scholar] [CrossRef]
  47. Adgent, M.A.; Daniels, J.L.; Rogan, W.J.; Adair, L.; Edwards, L.J.; Westreich, D.; Maisonet, M.; Marcus, M. Early-Life Soy Exposure and Age at Menarche. Paediatr. Perinat. Epidemiol. 2012, 26, 163–175. [Google Scholar] [CrossRef]
  48. Sinai, T.; Ben-Avraham, S.; Guelmann-Mizrahi, I.; Goldberg, M.R.; Naugolni, L.; Askapa, G.; Katz, Y.; Rachmiel, M. Consumption of Soy-Based Infant Formula Is Not Associated with Early Onset of Puberty. Eur. J. Nutr. 2019, 58, 681–687. [Google Scholar] [CrossRef] [PubMed]
Children 10 01686 g001
Figure 1. Diagram graphically showing the process of paper selection and exclusion used in writing this narrative review.
Figure 1. Diagram graphically showing the process of paper selection and exclusion used in writing this narrative review.
Children 10 01686 g001
Table 1. Summary of the papers referred to breastfeeding and early puberty onset.
Table 1. Summary of the papers referred to breastfeeding and early puberty onset.
Author, YearStudy DesignCohortResults
Hvidt et al., 2021 [15]Population-based cohort studyIn total, 13,511 boys and girls from the Puberty Cohort nested within the Danish National Birth Cohort.YES.
Absence of breastfeeding accelerate pubertal
timing in boys; in girls, breastfeeding was not associated with pubertal development.
Al-Sahab et al., 2011 [16] Population-based cohort studyData was taken from the Cebu Longitudinal Health and Nutrition Survey, initiated in 1981 to examine the feeding patterns of infants in the Metro Cebu Area, Philippines, recruiting pregnant women who gave birth between May 1983 and April 1984. Follow-up studies were conducted when the girls reached ages 8–9, 11–12, and 14–15 years.NO.
Negative association between exclusive breastfeeding and early menarche.
Karaolis-Danckert et al., 2009 [17]Cohort study conducted
by the Research Institute of Child Nutrition in Dortmund,
Germany		German girls and boys between 6 and 13 years.
Only term (37–42 wk of
gestation) singletons with a birth weight 2500 g who fulfilled
the following minimum requirement were selected.		YES.
In both boys and girls, intrauterine and early postnatal
growth factors (including full breastfeeding, >= 4 months) appear to influence both early and later markers
of puberty onset independently of prepubertal body composition.
Aghaee et al., 2019 [18]Prospective cohortThis study considered a multiethnic cohort, eventually including 3331 mother–daughter pairs (girls born between 2004 and 2006).YES.
Absence of breastfeeding has been linked to an earlier onset of breast and pubic hair development, as compared to a breastfeeding period lasting at least 6 months.
Kale et al., 2015 [19]Prospective studyThis study considered a population of 1237 socio-economically and ethnically diverse girls
across three geographic locations (New York City, Cincinnati, and the San Francisco Bay Area).		YES and NO.
The effect of breastfeeding on pubertal onset varies by study site. Mainly breastfed or mixed-fed girls had a later onset of breast development compared to formula-fed peers; breastfeeding’s link to pubic hair development onset was not significant.
Kwok et al., 2012 [20]Observational cohoty study“Children of 1997” cohort from Hong Kong.NO.
Neither breastfeeding nor childhood milk consumption had a connection with the timing of pubertal onset.
Morris et al., 2010 [21]Cohort studyThe study cohort comprises women aged 16 and above from the UK who joined the Breast Cancer Generations Study. It started in 2003 with 111,595 participants. The final analysis included 81,606 women.YES.
Women who received breastfeeding experienced a delayed onset of menarche compared to those who were not breastfed.
Blell et al., 2008 [22]Prospective longitudinal cohort studyThe cohort in the Thousand Families Study includes all 1142 children who were born in May and June 1947 to mothers residing in Newcastle-upon-Tyne, UK. Out of the original cohort, a total of 832 individuals were successfully traced.NO.
Timing of menarche was not associated with the duration of breast-feeding.
Ong et al., 2009 [23]Prospective cohort studyThe cohort of the Avon Longitudinal Study of Parents and Children (ALSPAC) study is formed by 14,541 pregnant women who resided in one of three Bristol-based health districts in the former County of Avon.YES.
Breast milk appears to be protective against earlier menarche in girls.
Lee et al., 2015 [24]Prospective observational studyThe study involves the Ewha Birth & Growth Cohort (2001–2006, South Korea). It follows mothers and their children, with clinical assessments performed at ages 3, 5, 7, 8, and 9. The 2011 follow-up included 260 participants aged 9, focusing on puberty.YES.
Children breastfed for 6 months or more exhibited a protective link against early puberty
Table 2. Summary of the papers referred to formula milk and early puberty onset.
Table 2. Summary of the papers referred to formula milk and early puberty onset.
Author, YearStudy DesignCohortResults
Novotny R. et al., 2003 [43]Comparative studyGirls residing on the island of Oahu were evaluated based on their feeding during early childhood; of the 349 girls enrolled, 59 (17%) were breastfed only, while 242 (71%) were formula fed.YES
Formula-fed girls exhibited shorter stature and greater weight compared to the breastfed ones, leading to an earlier onset of menarche.
Andres A. et al., 2012 [44] Clinical trialOverall, 391 Healthy infants were divided in 3 groups: breastfed (BF), milk-based formula-fed (MF), or soy protein-based formula-fed (SF). Development was evaluated (at ages 3, 6, 9, and 12 months) by using the Bayley Scales of Infant Development and the Preschool Language Scale-3.NO
No significant differences between the infants fed with the two types of formulas.
YES
Breastfed infants showed an improved cognitive and psychomotor development than formula-fed infants.
Kale A. et al., 2015 [19]Prospective cohort studyOverall, 1237 girls (age between 6 and 8) were enrolled from three different regions: New York City, Cincinnati, and the San Francisco Bay Area. The study evaluated breastfeeding habits through self-administered questionnaires or interviews conducted with the caregiver.YES
Girls who were predominantly breastfed had a later onset of breast development compared with those who were formula-fed.
Breastfeeding duration was also directly associated with age at the onset of breast development.
Mennella JA et al., 2018 [45] Randomized controlled trialA comparison between a significant group of infants fed cow’s milk formula (CMF) with children who received extensively hydrolysed formula (EHF).YES
Significant difference in the rate of weight gain velocity from 0.75 to 4.5 months (p = 0.002) between the two groups being compared. Specifically, the EHF group gained weight on average by 25.1 ± 0.9 g/d, while the CMF group by 29.0 ± 1.0 g/day.
No difference in length increase.
Adgent MA et al., 2012 [47]Prospective, longitudinal studyA sample of 2920 girls; approximately 2% had introduced soy-based formula at 4 months of age or earlier. YES
Girls fed soy products had a 25% higher risk of developing premature menarche than girls fed formula or non-soy milk (Hazard Ratio 1.25 (95% confidence interval, 0.92, 1.71)).
The presence of mild endocrine disrupting effects of soy isoflavone exposure, may lead to an early onset of puberty. However, the research was limited to a few subjects exposed to soy
Sinai et al., 2019 [48]Nested case–control studyA cohort of children was followed prospectively from birth to age 3; during this period, their eating habits and the possible appearance of IgE-mediated cow’s milk allergy were evaluated. Two groups were created: one included infants who consumed only soy-based infant formula (soy group: 29 participants, 17 males), the other group was randomly selected from those without IgE-CMA and who did not receive milk soy-based artificial (control group: 60 participants, 27 males).NO
No significant differences in pubertal development, growth, or BMI values.
Felício JS et al., 2021 [46]Case-control studyThe study involved 161 girls, of which 84 were patients diagnosed with CPP (case group), the remaining 77 did not have a diagnosis of CPP (control group).YES
Exclusive breastfeeding up to 6 months of age, was an important protective factor for CPP; instead, soy consumption was positively correlated (r = 0.2; p < 0.01).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Calcaterra, V.; Cena, H.; Sottotetti, F.; Rossi, V.; Loperfido, F.; Zuccotti, G. Breast and Formula Milk and Early Puberty Onset. Children 2023, 10, 1686. https://doi.org/10.3390/children10101686

AMA Style

Calcaterra V, Cena H, Sottotetti F, Rossi V, Loperfido F, Zuccotti G. Breast and Formula Milk and Early Puberty Onset. Children. 2023; 10(10):1686. https://doi.org/10.3390/children10101686

Chicago/Turabian Style

Calcaterra, Valeria, Hellas Cena, Francesca Sottotetti, Virginia Rossi, Federica Loperfido, and Gianvincenzo Zuccotti. 2023. "Breast and Formula Milk and Early Puberty Onset" Children 10, no. 10: 1686. https://doi.org/10.3390/children10101686

APA Style

Calcaterra, V., Cena, H., Sottotetti, F., Rossi, V., Loperfido, F., & Zuccotti, G. (2023). Breast and Formula Milk and Early Puberty Onset. Children, 10(10), 1686. https://doi.org/10.3390/children10101686

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop