- Breastfeeding on demand leads to successful lactation and better infant appetite control.
- Factors involved in appetite control that are present only in breastmilk, such as leptin, appear to influence regulation of milk intake in breastfed infants.
- Breastmilk appetite control factors likely influence physiological processes such as hypothalamic development and gastric emptying.
- The mode of feeding affects milk intake and appetite regulation such that bottle feeding allows greater milk consumption and lower appetite control compared to breastfeeding.
‘Slow down, Mama!’ – In contrast to breastfeeding, which allows infants to feed on demand, bottle feeding enables parents to provide set volumes of milk to babies. Latest evidence shows that breastfed babies control their appetite better than formula-fed babies, and although the mechanisms through which this occurs are not yet clear, it has been shown that this has long-term effects on appetite regulation and weight control into adulthood. Perhaps it is time to start seriously considering breastfeeding as an intervention window against the obesity epidemic.
Exclusively breastfed infants self-regulate their nutrient intake1, 2. Breastfeeding on demand facilitates this. In 1986, a study demonstrated that when mothers stimulated an increase of milk supply by daily milk expression, their babies did not consume the extra milk after cessation of the stimulation phase3. We have shown that breastfed infants rarely consume 100% of the available breastmilk, with the average consumption being 67% of available breastmilk4. Ultrasound imaging studies of milk ejection in the breast of lactating women have shown that in 39% of the mothers who had multiple milk ejections, the infant terminated the breastfeed during a milk ejection even though milk was readily available5, demonstrating active short-term appetite control.
In addition, breastfeeding results in long-term appetite control not otherwise seen in formula-fed infants, with a significant body of evidence demonstrating that breastfed infants have a lower risk of becoming obese in childhood and adulthood6, 7. A number of large epidemiological studies in different areas around the world have reported a negative, dose-response relationship between the duration of breastfeeding and the incidence of obesity later in life, after controlling for confounding factors8-10. These findings are quite remarkable considering that the only nutritional measurements made were whether the infant received breastmilk and the duration of breastfeeding, hardly acceptable measures of dietary intake in light of the large variation between mother/infant dyads in daily milk production, intake, and composition4, 11-13.
Appetite control factors in breastmilk
The consistent beneficial effects of breastfeeding on short- and long-term appetite control in babies are bound to be multifactorial and are not yet well understood. One piece of the puzzle may be found in the components of breastmilk, which are absent or present in lower amounts in artificial formula. In 1994, leptin was discovered, a signalling peptide regulating energy intake and expenditure in adults14. Since then, a series of other bioactive factors involved in adult energy metabolism have been identified, including adiponectin, an orexigenic (stimulating food intake) peptide; ghrelin, which stimulates food intake and has an adipogenic activity; resistin, a cytokine secreted by adipocytes, and many others. What is fascinating is that many of these factors that control appetite in adults are also present in breastmilk! As can be expected, studies are emerging linking them with appetite regulation in breastfed babies.
Increasing leptin concentration in breastmilk has been associated with lower infant weight, still within the normal range, at two years15. Moreover, animal studies have shown that leptin contributes to the development of neural circuits associated with appetite regulation16. Other hormones in breastmilk may also confer appetite control in breastfed infants. Breastmilk adiponectin has been shown to positively correlate with the incidence of being overweight at two years of age17. Breastmilk IGF-I positively correlates with BMI in the first five months of life18. Although these and many other appetite control factors are present in breastmilk, they have only recently been identified, and their role in neonate physiology, infant growth, and short- and long-term appetite control is elusive, thus deserving close attention. In addition to these hormones, other components of the nutrition the infant receives early on may regulate appetite. Protein intake is a serious candidate.
The protein content of a food is known to influence appetite and its regulation22, 23. The protein content of mature human milk is very low, three times less than that of bovine milk24, yet it is optimal for the growth requirements of the human term infant. Noticeably, this is the period of maximal growth rate across the total lifespan. Animal milk-based artificial formulas typically contain higher amounts of protein, different ratios of protein types (e.g., caseins versus whey proteins), as well as a different composition of protein, all of which may affect infant development and appetite regulation. Therefore, it becomes clear that further knowledge on how the specific composition of the early infant nutrition influences development of appetite mechanisms in the infant is paramount. In this connection, factors such as the maternal diet and BMI, which may affect breastmilk composition in appetite controllers, merit further investigation.
Infant suckling and gastric emptying
Whilst breastfed infants display good appetite regulation, there may be other influencing factors apart from the vast array of appetite control factors in breastmilk. A recent study suggests that the ‘container’ from which milk is delivered (breast or bottle) may also play a role. Li et al. (2012)19 showed that bottle feeding is positively associated with increased weight gain in the first year of life irrespectively of whether breastmilk or formula was fed. The researchers speculated that infants are more active in controlling the volume of milk taken during a breastfeed and that changes in breastmilk composition occurring during a breastfeed, such as the increase in fat as the feed progresses, may provide a signal that the feeding is nearing completion. Bottle feeding in comparison, is more likely influenced by the caregivers who are more likely to lengthen the feed if they believe the infant has not consumed enough of the milk in the bottle.
Interestingly, breastfed infants display a wide range of feeding patterns and volumes that may also relate to breastmilk composition in terms of appetite regulating factors. For example, the main source of leptin in the first six months of life is breastmilk where it is absorbed from the stomach and enters the infant’s circulation. In contrast, there is little to no leptin in artificial formulas. This may explain in part why breastfed infants feed more frequently and consume less milk than their formula-fed counterparts.
In addition to feeding patterns, differences exist in how food is processed by the infant’s gastrointestinal tract depending on whether it is breastmilk or formula. Formula, being bovine milk-based, empties slower in the stomach because of its higher casein-whey ratio compared to breastmilk20. Moreover, preliminary evidence supports the notion that appetite control factors, such as leptin, which are present in breastmilk but are absent in formula, may also influence gastric emptying20, 21. These differences in gastric emptying and nutrient processing may not only influence growth and appetite regulation in the short-term, but may also have appetite programming effects and thus long-term consequences.
Breastmilk as a model for optimum nutrition in later life
Popular opinion and accumulating evidence suggests that the ‘window’ of early feeding has an impact on adult health by influencing functional programming. Indeed, given the enormous increase in obesity and obesity-related diseases, the breastfeeding period is an important public health initiative and an opportunity to influence long-term health25. Whilst breastfeeding is often shown to be protective against obesity, a proportion of infants still become overweight later in life despite being breastfed. This indicates that the weaning period may also be critical to appetite control. The transition from consuming breastmilk at a frequency and quantity largely of the infant’s choosing to being encouraged to consume food to meet the expectations of the parents and health professionals is a period which, if not well managed, may have detrimental effects on the infant’s appetite control mechanisms that developed during breastfeeding. Thus, in addition to investigating how appetite is regulated during the breastfeeding period, we should perhaps start thinking of the composition of human milk as an optimum guide for the introduction of solid foods in infancy and the lasting effects into adulthood.
1. Taveras EM, Scanlon KS, Birch L, Rifas-Shiman SL, Rich-Edwards JW, Gillman MW. (2004) Association of breastfeeding with maternal control of infant feeding at age 1 year. Pediatrics 114:e577-583.
2. Savino F, Liguori SA, Fissore MF, Oggero R. (2009) Breast milk hormones and their protective effect on obesity. Int J Pediatr Endocrinol 2009:327505.
3. Dewey KG & Lonnerdal B. (1986) Infant self-regulation of breast milk intake. Acta Paediatr Scand 75:893-898.
4. Kent JC, Mitoulas LR, Cregan MD, Ramsay DT, Doherty DA, Hartmann PE. (2006) Volume and frequency of breastfeedings and fat content of breast milk throughout the day. Pediatrics 117:e387-395.
5. Ramsay DT, Kent JC, Owens RA, Hartmann PE. (2004) Ultrasound imaging of milk ejection in the breast of lactating women. Pediatrics 113:361-367.
6. Stettler N. (2011) Infant feeding practices and subsequent development of adipose tissue. Nestle Nutr Workshop Ser Pediatr Program 68:215-221; discussion 222-215.
7. Pirila S, Saarinen-Pihkala UM, Viljakainen H, Turanlahti M, Kajosaari M, Makitie O, Taskinen M. (2012). Breastfeeding and determinants of adult body composition: a prospective study from birth to young adulthood. Horm Res Paediatr 77:281-290.
8. Dewey KG, Wesseling W, Heinig MJ. (1995) Do infant intake and growth rate change after termination of breastfeeding in the second year of life? FASEB Journal 9:A755.
9. Arenz S, Ruckerl R, Koletzko B, von Kries R. (2004) Breast-feeding and childhood obesity–a systematic review. Int J Obes Relat Metab Disord 28:1247-1256.
10. Harder T, Bergmann R, Kallischnigg G, Plagemann A. (2005) Duration of breastfeeding and risk of overweight: a meta-analysis. Am J Epidemiol 162:397-403.
11. Mitoulas LR, Kent JC, Cox DB, Owens RA, Sherriff JL, Hartmann PE (2002) Variation in fat, lactose and protein in human milk over 24 h and throughout the first year of lactation. Br J Nutr 88:29-37.
12. Ogra PL & Greene HL. (1982) Human milk and breast feeding: an update on the state of the art. Pediatr Res 16:266-271.
13. Butte NF, Garza C, Smith EO, Nichols BL. (1984) Human milk intake and growth in exclusively breast-fed infants. J Pediatr 104:187-195.
14. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425-432.
15. Miralles O, Sanchez J, Palou A, Pico C. (2006) A physiological role of breast milk leptin in body weight control in developing infants. Obesity (Silver Spring) 14:1371-1377.
16. Bouret SG & Simerly RB. (2006) Developmental programming of hypothalamic feeding circuits. Clin Genet 70:295-301.
17. Weyermann M, Brenner H, Rothenbacher D. (2007) Adipokines in human milk and risk of overweight in early childhood: a prospective cohort study. Epidemiology 18:722-729.
18. Savino F, Fissore MF, Grassino EC, Nanni GE, Oggero R, Silvestro L. (2005) Ghrelin, leptin and IGF-I levels in breast-fed and formula-fed infants in the first years of life. Acta Paediatr 94:531-537.
19. Li R, Magadia J, Fein SB, Grummer-Strawn LM. (2012) Risk of bottle-feeding for rapid weight gain during the first year of life. Arch Pediatr Adolesc Med 166:431-436.
20. Van Den Driessche M, Peeters K, Marien P, Ghoos Y, Devlieger H, Veereman-Wauters G. (1999) Gastric emptying in formula-fed and breast-fed infants measured with the 13C-octanoic acid breath test. J Pediatr Gastroenterol Nutr 29:46-51.
21. Yarandi SS, Hebbar G, Sauer CG, Cole CR, Ziegler TR. (2011) Diverse roles of leptin in the gastrointestinal tract: modulation of motility, absorption, growth, and inflammation. Nutrition 27:269-275.
22. Abete I, Astrup A, Martinez JA, Thorsdottir I, Zulet MA. (2010) Obesity and the metabolic syndrome: role of different dietary macronutrient distribution patterns and specific nutritional components on weight loss and maintenance. Nutr Rev 68:214-231.
23. Michaelsen KF, Larnkjaer A, Molgaard C. (2012) Amount and quality of dietary proteins during the first two years of life in relation to NCD risk in adulthood. Nutr Metab Cardiovasc Dis 22:781-786.
24. Frank A, Bruhn JC, Lawrence CM. (1988) Distribution of protein in California milk in 1983. J Dairy Sci 71:2373.
25. Geddes DT & Prescott SL. (2013) Developmental origins of health and disease: the role of human milk in preventing disease in the 21st century. J Hum Lact 29:123-127.
Prof. Foteini Hassiotou & Prof. Donna Geddes
Hartmann Human Lactation Research Group
The University of Western Australia