Document Detail

Is the macronutrient intake of formula-fed infants greater than breast-fed infants in early infancy?
Jump to Full Text
MedLine Citation:
PMID:  23056929     Owner:  NLM     Status:  PubMed-not-MEDLINE    
Faster weight gain early in infancy may contribute to a greater risk of later obesity in formula-fed compared to breast-fed infants. One potential explanation for the difference in weight gain is higher macronutrient intake in formula-fed infants during the first weeks of life. A systematic review was conducted using Medline to assess the macronutrient and energy content plus volume of intake in breast-fed and formula-fed infants in early infancy. All studies from healthy, term, singleton infants reporting values for the composition of breast milk during the first month of life were included. The energy content of colostrum (mean, SEM: 53.6 ± 2.5 kcal/100 mL), transitional milk (57.7 ± 4.2 kcal/100 mL), and mature milk (65.2 ± 1.1 kcal/100 mL) was lower than conventional infant formula (67 kcal/100 mL) on all days analyzed. The protein concentration of colostrum (2.5 ± 0.2 g/100 mL) and transitional milk (1.7 ± 0.1 g/100 mL) was higher than formula (1.4 g/100 mL), while the protein content of mature milk (1.3 ± 0.1 g/100 mL) was slightly lower. Formula-fed infants consume a higher volume and more energy dense milk in early life leading to faster growth which could potentially program a greater risk of long-term obesity.
Shelly N Hester; Deborah S Hustead; Amy D Mackey; Atul Singhal; Barbara J Marriage
Related Documents :
7143179 - Cranial blood volume changes during mechanical ventilation and spontaneous breathing in...
24963369 - The survival of a 580 g infant conceived by in vitro.
23299229 - Evaluation of sigmoidal maturation and allometric models: prediction of propofol cleara...
25003169 - Differences in birthweight outcomes: a longitudinal study based on siblings.
7075229 - Lack of response to bronchodilator of airway obstruction after mechanical ventilation i...
18972409 - Nasal nitric oxide in infants before and after extubation.
7259259 - Cytotoxicity of lymphocytes in the newborn.
8625729 - And baby makes four: predictors of attachment security among preschool-age firstborns d...
12405509 - Impaired processing of brief, rapidly presented auditory cues in infants with a family ...
Publication Detail:
Type:  Journal Article     Date:  2012-09-27
Journal Detail:
Title:  Journal of nutrition and metabolism     Volume:  2012     ISSN:  2090-0732     ISO Abbreviation:  J Nutr Metab     Publication Date:  2012  
Date Detail:
Created Date:  2012-10-11     Completed Date:  2012-10-12     Revised Date:  2014-02-20    
Medline Journal Info:
Nlm Unique ID:  101526296     Medline TA:  J Nutr Metab     Country:  United States    
Other Details:
Languages:  eng     Pagination:  891201     Citation Subset:  -    
Export Citation:
APA/MLA Format     Download EndNote     Download BibTex
MeSH Terms
Grant Support
G0700349//Medical Research Council

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-ta): J Nutr Metab
Journal ID (iso-abbrev): J Nutr Metab
Journal ID (publisher-id): JNUME
ISSN: 2090-0724
ISSN: 2090-0732
Publisher: Hindawi Publishing Corporation
Article Information
Download PDF
Copyright © 2012 Shelly N. Hester et al.
Received Day: 25 Month: 4 Year: 2012
Accepted Day: 21 Month: 8 Year: 2012
Print publication date: Year: 2012
Electronic publication date: Day: 27 Month: 9 Year: 2012
Volume: 2012E-location ID: 891201
ID: 3463945
PubMed Id: 23056929
DOI: 10.1155/2012/891201

Is the Macronutrient Intake of Formula-Fed Infants Greater Than Breast-Fed Infants in Early Infancy?
Shelly N. Hester1
Deborah S. Hustead2
Amy D. Mackey2
Atul Singhal3
Barbara J. Marriage2*
1Abbott Nutrition, Champaign-Urbana, IL 61820, USA
2Abbott Nutrition, 3300 Stelzer Road, Columbus, OH 43219, USA
3Institute of Child Health, University College London, London WC1N 1EH, UK
Correspondence: *Barbara J. Marriage:
[other] Academic Editor: Patricia Helen C. Rondó

1. Introduction

Breastfeeding has a number of short- and long-term benefits for health, but the underlying mechanisms for its effects on long-term outcomes are uncertain. One of the most widely cited advantages of breastfeeding is a lower risk of long-term obesity [14] and cardiovascular disease [57], but whether these effects are due to sociobiological differences between infants breast- or formula-fed or to the nutritional composition and intake of breast milk remains controversial. Several mechanisms for the long-term advantages of breastfeeding have been proposed, but recently we suggested that these effects were a consequence of slower early growth in breast-fed compared to formula-fed infants—the growth acceleration hypothesis [6].

More than twenty-five studies now support the hypothesis that faster weight gain (upward centile crossing for weight) in infancy influences, or programs, a greater risk of long-term obesity [8, 9] and cardiovascular disease [6, 810]. This association has been seen for obesity in adults and children, in high-income and low-income countries [810] and is consistent for cohorts over the last 80 years [8]. The “critical window” for the effects of growth is not known, but slower weight gain in the first few weeks (regardless of gestation or birth weight) is associated with a lower risk of later obesity [11, 12], insulin resistance [13], endothelial dysfunction [5], and adult obesity [14]. Therefore, differences in weight gain between formula- and breast-fed infants in the first postnatal weeks, when breast-fed babies often lose weight compared to weight gain in babies given formula [15, 16], could partially explain long-term programming advantages of breastfeeding [6].

The difference in early weight gain between formula-fed and breast-fed infants is likely to be related to differences between formula and breast milk in both the composition and volume of intake of colostrum (days 1–5) and transitional breast milk (days 6–14). In fact, in contrast to the composition of human milk which varies with the age of the infant, formula composition is constant and designed to meet the nutrient requirements for the whole of the first six to 12 months of life. However, while there has been extensive research on the nutritional composition of human milk, relatively few studies have focused on the composition and volume of intake during the first few weeks after birth. We therefore conducted a systematic review of the literature and meta-analysis of available data on the macronutrient content of human milk and the volume of milk intake in breast-fed and formula-fed infants in the first weeks of life. Such data could help our understanding of the possible mechanisms by which breastfeeding benefits long-term health and helps in the primary prevention of obesity and cardiovascular disease, and in the development of preventative strategies for obesity in formula-fed infants.

2. Methods
2.1. Search Strategy

A literature search investigating the macronutrient and energy content of human milk and volume of milk intake in breast-fed and formula-fed infants in the first two weeks of life was conducted using the National Library of Medicine (MEDLINE). Additional studies were identified from a hand-search of relevant journals and a search of references from identified studies. Details of the search strategy used are shown in Table 1. Since most published studies were observational, a meta-analysis was conducted as described by Stroup et al. [17]. This method was used previously to investigate metabolizable energy (ME) intake in older breast-fed infants [39].

All studies that reported breast milk energy and macronutrient concentration during the first month of life from mothers who were exclusively breastfeeding healthy, term, singleton infants were included. Only volumes of milk intake for either exclusively breast-fed or formula-fed infants were included in the analysis, only studies which reported original data were eligible, and duplicate publications (e.g., in reviews) were excluded. Studies only reporting graphical data were excluded, since estimating values from graphs would increase error in the meta-analysis. Energy and macronutrient values of breast milk were arbitrarily divided into three categories; colostrum (1–5 days), transitional milk (6–14 days), and mature milk (>14 days).

Studies were excluded if they used methods to analyze the macronutrient and energy content of breast milk previously shown to be invalid. For example, studies using nonspecific methods to analyze carbohydrates were not used since they may overestimate lactose concentration, compared to lactose-specific methods [40]. Also, since breast milk energy content varies due to both diurnal variation and variation between fore milk and hind milk [31], only studies that used acceptable sampling methods (e.g., collecting a complete feed, a mid feed, or at the beginning and end of a feed) were included [19].

Estimates of breast milk intake expressed as g/day were converted to mL/day using a correction for the density of human milk of 1.031 g/mL [49]. The meta-analysis values for gross energy content of breast milk were converted into metabolizable energy (ME) levels by multiplying the classic Atwater factors 4, 4, 9 kcal/g for carbohydrate, protein, lipid, respectively, and by assuming 93% of gross breast milk energy reported by bomb calorimetry methods is metabolizable [39]. The conversion of breast milk gross energy values to metabolizable energy allows for a more direct comparison of formula and breast milk energy as labeling of infant formulas utilizes metabolizable energy.

Since triacylglycerols account for 98% of the lipids, data from studies reporting total triacylglycerols concentrations were analyzed as total lipid content [50]. The carbohydrate content of breast milk was taken as the total lactose content, since lactose is the main carbohydrate in breast milk. The oligosaccharides and other sugars were not included in the estimation of carbohydrate in human milk. The calculation of protein included nonprotein nitrogen which includes components such as free amino acids, urea, uric acid, and nucleotides as these components make up 20 to 25% of the total nitrogen in milk [51].

Comprehensive Meta-Analysis, version 2 (Biostat, Inc., NJ, USA), was used to perform a meta-analysis of the macronutrient and energy content of breast milk and volume intake of both formula and breast milk by infants during the first weeks of life. Random effects models were used to calculate summary means and SEM for each of the parameters. All data reported from the individual studies are expressed as mean ± SEM.

3. Results
3.1. Macronutrients in Breast Milk
3.1.1. Lipids

Our literature search identified 25 potentially eligible papers. After screening these for eligibility, 20 studies were included with a total of 390, 257, and 567 breast milk samples available for analysis of colostrum, transitional milk, and mature milk, respectively. The mean lipid content of breast milk increased from 2.2 ± 0.2 g/100 mL (range 1.0 to 3.0 g/100 mL) in colostrum, to 3.0 ± 0.1 g/100 mL (range 2.5 to 3.8 g/100 mL) in transitional milk, and 3.8 ± 0.1 g/100 mL (range 2.8 to 4.9 g/100 mL) in mature milk (Table 2). Lipid concentrations of both colostrum and transitional milk were lower than that commonly found in formula (3.7 g/100 mL) but similar to lipid concentrations in mature milk.

3.1.2. Carbohydrates

Our literature search identified 30 potentially eligible papers. We identified 21 eligible studies with 265, 337, and 476 breast milk samples for analysis of colostrum, transitional milk, and mature milk, respectively. Average carbohydrate content of breast milk increased from 5.6 ± 0.6 g/100 mL (range 2.6 to 7.6 g/100 mL) in colostrum to 5.9 ± 0.4 g/100 mL (4.1 to 6.8 g/100 mL) in transitional milk and to 6.7 ± 0.2 g/100 mL (5.0 to 8.3 g/100 mL) in mature milk (Table 3). The carbohydrate content of human milk at all stages of lactation was less than that of formula (commonly 7.6 g/100 mL).

3.1.3. Protein

We identified 29 potentially eligible papers, and 21 were included with a total of 433, 308, and 415 breast milk samples available for colostrum, transitional milk, and mature milk, respectively. Mean milk protein concentration declined with duration of lactation (Table 4) from 2.5 ± 0.2 g/100 mL (range 1.4 to 6.5 g/100 mL) in colostrum to 1.7 ± 0.1 g/100 mL (1.3 to 2.5 g/100 mL) in transitional milk and 1.3 ± 0.1 g/100 mL (0.8 to 2.1 g/100 mL) in mature milk. Protein concentration in colostrum and transitional milk was greater than commonly found in formula (1.4 g/100 mL), while the protein content of mature milk was slightly lower.

3.2. Intake of Breast Milk and Formula

Our literature search identified 31 potentially eligible papers for breast milk intake. We screened these for eligibility, and 25 were included with a total of 148, 123, 109, 109, 139, 132, and 407 intake values for day 1, day 2, day 3, day 4, day 5, day 7, and >14 days, respectively. We identified 12 potentially eligible papers for infant formula intake, and 9 were included with a total of 157, 157, 129, 128, 128, 126, 188, and 136 formula intake values available for day 1, day 2, day 3, day 4, day 5, day 6, day 7, and >14 days, respectively. To ensure that values for breastmilk and formula intake were comparable between the two groups and to focus on early feeding, the upper age limit was established at 6 weeks. The range of intake was from 15 days to 6 weeks with the majority of the data at 1 month of age.

Most studies measured the total volume of breast milk intake by weighing the infant before and after a breastfeed and taking the increase in infant weight as the weight of milk consumed by the infant. Although there was considerable variation in breast milk intakes during the first few days of life (Table 5), breast milk intake tended to increase from 21.5 ± 4.2 mL/day on day 1 to 495.3 ± 33.4 mL/day on day 7 to 673.6 ± 29 mL/day after 14 days.

Formula intake is generally measured by weighing the bottle weight before and after a feed and taking into account any spillage during feeding. Few studies reported formula intake during the first week of life, and hence meta-analyses were performed only for days 1, 2, and after 14 days since there were three or more studies for each of these times. Infant formula intake increased from 170.5 ± 55.8 mL/day on day 1 to 265.0 ± 67.7 mL/day on day 2 and to 761.8 ± 18 mL/day after 14 days (Table 6) and was greater than the volume of breast milk intake on all days analyzed.

3.3. Energy Content of Breast Milk

Of the 25 potentially eligible papers identified by our literature search, 22 met the entry criteria, and these had a total of 387, 155, and 1088 breast milk samples for colostrum, transitional milk, and mature milk, respectively. The energy content of colostrum (53.6 ± 2.5 kcal/100 mL), transitional milk (57.7 ± 4.2 kcal/100 mL), and mature milk (65.2 ± 1.1 kcal/100 mL) was less than that commonly found in formula (67 kcal/100 mL), shown in Table 7.

3.4. Macronutrient Intake in Breast-Fed and Formula-Fed Infants

The average volume of infant formula consumed was substantially higher than the volume of breast milk on all days analyzed. Due to the greater volume of milk intake by formula-fed infants and higher energy content of formula, (67 kcal/100 mL), average energy intake on the first day of life was 114 kcal/day in formula-fed infants compared to 12 kcal/day in breast-fed infants (a 9.5-fold difference). From day 14 up to 6 weeks of life, average energy intake in formula-fed infants remained higher at 513 kcal/day compared to 440 kcal/day in the breast-fed infants (a 1.2-fold difference). In addition, the greater volume of formula intake compared to breast milk intake led to an average protein intake on the first day to be 2.4 g in formula-fed infants compared to only 0.5 g in breast-fed infants (a 4.8-fold difference). By day 14, protein intake in formula-fed infants (10.7 g/day) was still slightly higher than that of breast-fed infants (8.8 g/day) (a 1.2-fold difference). A similar pattern of increased intake of carbohydrate and fat in the formula-fed infants compared to breast-fed infants was also observed.

4. Discussion

To our knowledge, this is the first meta-analysis of the macronutrient content of human milk which includes milk from early lactation. We found that, depending on number of days from birth, in the first two weeks of life, formula-fed infants have a 1.2- to 9.5-fold greater energy intake and a 1.2- to 4.8-fold greater protein intake than those breastfed. This difference is due to the higher energy and protein content of formula and a greater volume of intake which may contribute to greater weight gain in formula-fed compared to breast-fed infants during early infancy. These data are therefore consistent with the hypothesis that formula-fed infants may be overfed early in infancy during a possible critical period of growth that may lead to programming of long-term obesity [6, 810], and have implications for the optimal composition of infant formulas.

Ideally, the energy content of formula should be equivalent to corresponding energy content of human milk at different stages of lactation. However, formula is designed to be appropriate for the first year of life and most commercially available products have an energy density of approximately 67 kcal/100 mL, far greater than the energy content of early breast milk. We found the metabolizable energy content of mature milk (65.2 kcal/100 mL) was also slightly lower than infant formula (67 kcal/100 mL) and within the range reported by Neville (60.1 kcal/100 mL to 77.6 kcal/100 mL) [82]. Similarly, in a review of 25 studies, Reilly et al. reported a mean ME of mature human milk as 63.9 kcal/100 mL [39], while a doubly labeled water study demonstrated that the energy content of breast milk at five and 11 weeks was 57.4 kcal/100 mL and 59.8 kcal/100 mL, respectively [79]. Therefore, our findings suggest that formula-fed infants could have a higher energy intake in the first six months of life and could partially explain greater weight gain in infants given formula compared to breast milk.

Along with the increase in energy density at all stages of lactation, the volume of intake of formula-fed infants was greater than those breast fed on all days analyzed and in particular in the first days of life. There are several potential explanations for this. First, it is likely that milk supply is limited in the first 24–48 hours postpartum which was confirmed by this analysis. Breast-fed infants receive approximately 25 to 100 mL per day in the first two days of life. Second, mothers of formula-fed infants may encourage finishing of the bottle even though appetite has been satisfied, hence a greater volume of intake. The capacity of the stomach of the newborn is very small in the first two days of life and increases in volume capacity after three to four days of life [83].

In support of this, in a pilot study designed to test the hypothesis that a higher nutrient intake in the first postnatal week may increase later obesity risk, infants fed a lower energy formula did not compensate by consuming more volume [18]. These results are similar to that reported by Fomon et al. who illustrated that between eight and 41 days of life the volume consumed was not different between a calorically dense (100 kcal/100 mL) or calorically dilute (54 kcal/mL) formula. This leads to a greater energy intake and rate of growth in the infants consuming a more concentrated formula [84]. It is evident that during the early weeks of life infants drink to volume, not to energy needs.

After this critical period, infants appear to regulate their volume of intake better during ad libitum feedings to meet caloric needs for growth. For instance, at about 6 weeks of age, infants fed either a calorically dilute (54 kcal/100 mL) or calorically dense (100 kcal/100 mL) formula modified their volume of intake so that energy intake was similar to that of infants fed a conventional formula (67 kcal/100 mL) [85]. Other studies provide support for this hypothesis. Small for gestation infants fed either a standard formula (65 kcal/100 mL) or calorically dense (87 kcal/mL) formula had similar intakes by two months of age [86].

The ability of an older infant (after 41 days) to regulate intake based on growth needs was validated by the fact that the mean weight gain between the two groups (calorically dilute and dense) during the “caloric matching phase” was nearly identical, 24.6 ± 4.6 and 24.9 ± 5.3 g/day [84]. Interestingly, during the “early window” where infants consumed similar volumes, there was a significant difference in weight gain between infants fed calorically dilute or dense formula. Infants consuming a calorically dense formula had a mean weight gain 1.4-fold greater (29.8 ± 4.9 versus 41 ± 10.4 g/day, P < 0.01) than those consuming the dilute formula which may be explained by a greater gain in percentage fat. The overall weight gain between the two groups up to 112 days was significantly different (26.3 ± 3.8 versus 30.2 ± 5.8, P < 0.05) which appears to be due to the initial difference in the early feeding period window [84]. Therefore, infants in the first weeks of life do not seem to compensate for getting less energy dense milk by drinking more (i.e., during the early weeks of life they drink to volume, not to energy needs). Hence, making the energy content of formula closer to that of breast milk may help reduce rapid weight gain of formula-fed infants in the critical window in the first weeks after birth.

In addition to differences in energy intake between breast-fed and formula-fed infants, protein intake varies considerably between the two groups. Protein concentration of human milk is highest during the initial, colostrum period because it contains large amounts of immunoglobulins and lactoferrin which gradually decline to relatively low levels in mature milk. However, despite this higher protein concentration, the greater volume of milk intake by formula-fed infants means that formula-fed infants have up to a 5-fold higher protein intake in the first two weeks of life compared to those breast fed, a difference which is likely to contribute to faster weight gain in formula-fed compared to breast-fed infants [87].

This faster weight gain in formula-fed infants compared to breast-fed infants is already evident in the first week of life. In two separate studies, healthy term breast-fed infants lost a mean 6.4% to 6.6% of birth weight before starting to gain weight compared to formula fed infants who only lost 3.5% to 3.7% [15, 16]. Breast-fed infants may not regain their birth weight by eight days of life; however, formula-fed infants generally exceed birth weight at eight days of age by 50–100 g [88, 89].

Importantly, several observational studies have demonstrated that faster postnatal weight gain in infancy leads to increased childhood and adult overweight status [17, 9093], hypertension risk [94], and insulin resistance [91]. This has been shown across several different population groups including those of European [14] and Asian [94] decent. The critical window for these programming effects is not known, but recent experimental evidence [95] now supports observational data [14] suggesting that weight gain in the first week of life may be particularly influential for increasing the later risk of obesity. In a small pilot study, infants randomly assigned to receive a lower nutrient formula, designed to mimic the intake of the breast-fed infant for the first seven postnatal days, had lower weight and sum of skin-fold thicknesses at age six and 18 months than those given standard formula [95]. Nutrition and growth during a critical window in the first week of life could therefore influence the long-term risk of obesity.

Limitations of this meta-analysis include the relative heterogeneity of the studies used, the small sample size of several studies, and limited data from the first few days of life. A lack of stable isotope studies to measure the energy content of early breast milk, which are difficult to perform in the first weeks of life, is another key limitation. The measurement of breast milk volume (test weighing of infants) may be less accurate than measurement of formula intake. Despite these limitations, a consistent pattern of lower macronutrient intake in breast-fed babies is supported by the data demonstrating a slower rate of weight gain in breast-fed compared to formula-fed infants.

Breastfeeding is clearly the most optimal nutrition for an infant and has major advantages for health. Although clearly it is not possible to replicate these benefits in infant formula, research should continue to strive to mimic, as close as possible, the composition and intake of the breastfed infant to provide similar health benefits to infants who cannot be breastfed. This could possibly be achieved either by reducing energy and/or protein content of formula; or by reducing the volume of intake. Volume of formula intake is more difficult to manipulate safely and could lead to hypernatremia, hypoglycemia, unintended weight loss, and undue stress on the caregiver. Infants fed formula consume larger volumes than those breast fed in the early postnatal period. Therefore, a formula designed to achieve a growth rate similar to that of the breast-fed infant would need a lower protein and energy content than that in breast milk, to compensate for the higher volume of intake.

Here we demonstrate that the energy and macronutrient content of infant formula, as well as the volume of formula intake, may be increased compared to human milk. This difference, particularly in the first weeks of life, could contribute to a faster weight gain. This provides an opportunity to modify the energy content of current infant formulas to more closely match the intake of the breast-fed infant, a strategy that could help in the long-term prevention of obesity, metabolic disease, and cardiovascular disease.

Conflict of Interests

A. Singhal has received honoraria for lectures for Danone, Pfizer, Nestle, and Abbott Nutrition. A. Singhal and coworkers at University College London have developed intellectual property based on the concept of lower nutrient intake in infants during the first weeks of life.


Christina Sherry, Ph.D., RD, is acknowledged for editorial and technical assistance. This work was funded by Abbott Nutrition, Columbus, OH, USA.

1. Arenz S,Ruckerl R,Koletzko B,et al. Breast-feeding and childhood obesity—a systematic reviewInternational Journal of Obesity and Related Metabolic DisordersYear: 2004281247125615314625
2. Harder T,Bergmann R,Kallischnigg G,Plagemann A. Duration of breastfeeding and risk of overweight: a meta-analysisAmerican Journal of EpidemiologyYear: 200516253974032-s2.0-2394445265816076830
3. Owen CG,Martin RM,Whincup PH,Davey-Smith G,Gillman MW,Cook DG. The effect of breastfeeding on mean body mass index throughout life: a quantitative review of published and unpublished observational evidenceAmerican Journal of Clinical NutritionYear: 2005826129813072-s2.0-3214445385916332664
4. Owen CG,Martin RM,Whincup PH,Smith GD,Cook DG. Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidencePediatricsYear: 20051155136713772-s2.0-2514450396115867049
5. Singhal A,Cole TJ,Fewtrell M,Deanfield J,Lucas A. Is slower early growth beneficial for long-term cardiovascular health?CirculationYear: 20041099110811132-s2.0-154240991214993136
6. Singhal A,Lucas A. Early origins of cardiovascular disease: is there a unifying hypothesis?The LancetYear: 20043639421164216452-s2.0-2442479898
7. Singhal A,Wells J,Cole TJ,Fewtrell M,Lucas A. Programming of lean body mass: a link between birth weight, obesity, and cardiovascular disease?American Journal of Clinical NutritionYear: 20037737267302-s2.0-003736961712600868
8. Baird J,Fisher D,Lucas P,Kleijnen J,Roberts H,Law C. Being big or growing fast: systematic review of size and growth in infancy and later obesityBritish Medical JournalYear: 200533175229299312-s2.0-2714454577116227306
9. Ong KKL,Preece MA,Emmett PM,Ahmed ML,Dunger DB. Size at birth and early childhood growth in relation to maternal smoking, parity and infant breast-feeding: longitudinal birth cohort study and analysisPediatric ResearchYear: 20025268638672-s2.0-003689204212438662
10. Monteiro POA,Victora CG. Rapid growth in infancy and childhood and obesity in later life—a systematic reviewObesity ReviewsYear: 2005621431542-s2.0-1804439206315836465
11. Durmus B,Mook-Kanamori DO,Holzhauer S,et al. Growth in foetal life and infancy is associated with abdominal adiposity at the age of 2 years: the generation R studyClinical EndocrinologyYear: 20107263364019769622
12. Holzhauer S,Hokken Koelega ACS,Ridder MD,et al. Effect of birth weight and postnatal weight gain on body composition in early infancy. The Generation R StudyEarly Human DevelopmentYear: 20098552852902-s2.0-6474910653419091495
13. Singhal A,Fewtrell M,Cole TJ,Lucas A. Low nutrient intake and early growth for later insulin resistance in adolescents born pretermThe LancetYear: 20033619363108910972-s2.0-0037471833
14. Stettler N,Stallings VA,Troxel AB,et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formulaCirculationYear: 200511115189719032-s2.0-1764440320515837942
15. Crossland DS,Richmond S,Hudson M,Smith K,Abu-Harb M. Weight change in the term baby in the first 2 weeks of lifeActa PaediatricaYear: 20089744254292-s2.0-4114917478218363951
16. Macdonald PD,Ross SRM,Grant L,Young D. Neonatal weight loss in breast and formula fed infantsArchives of Disease in ChildhoodYear: 2003886F472F4762-s2.0-034537754414602693
17. Stroup DF,Berlin JA,Morton SC,et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) groupThe Journal of the American MedicalYear: 200028320082012
18. Singhal A. Optigrow pilot study In press.
19. Allen JC,Keller RP,Archer P,Neville MC. Studies in human lactation: milk composition and daily secretion rates of macronutrients in the first year of lactationAmerican Journal of Clinical NutritionYear: 199154169802-s2.0-00258712492058590
20. Anderson GH,Atkinson SA,Bryan MH. Energy and macronutrient content of human milk during early lactation from mothers giving birth prematurely and at termAmerican Journal of Clinical NutritionYear: 19813422582652-s2.0-00193668387211727
21. Boersma ER,Offringa PJ,Muskiet FAJ,Chase WM,Simmons IJ. Vitamin E, lipid fractions, and fatty acid composition of colostrum, transitional milk, and mature milk: an international comparative studyAmerican Journal of Clinical NutritionYear: 1991535119712042-s2.0-00258913172021129
22. Carias D,Velásquez G,Cioccia AM,Piñero D,Inciarte H,Hevia P. The effect of lactation time on the macronutrient and mineral composition of milk from Venezuelan womenArchivos Latinoamericanos de NutricionYear: 19974721101172-s2.0-00311512139659423
23. Corvaglia L,Battistini B,Paoletti V,Aceti A,Capretti MG,Faldella G. Near-infrared reflectance analysis to evaluate the nitrogen and fat content of human milk in neonatal intensive care unitsArchives of Disease in ChildhoodYear: 2008935F372F3752-s2.0-5144909178018192331
24. Dewey KG,Lonnerdal B. Milk and nutrient intake of breast-fed infants from 1 to 6 months: relation to growth and fatnessJournal of Pediatric Gastroenterology and NutritionYear: 1983234975062-s2.0-00205543076620057
25. Ferris AM,Dotts MA,Clark RM,Ezrin M,Jensen RG. Macronutrients in human milk at 2, 12, and 16 weeks postpartumJournal of the American Dietetic AssociationYear: 19888866946972-s2.0-00238998983372922
26. Gross SJ,David RJ,Bauman L,Tomarelli RM. Nutritional composition of milk produced by mothers delivering pretermJournal of PediatricsYear: 19809646416442-s2.0-00189015387359266
27. Hosoi S,Honma K,Daimatsu T,Kiyokawa M,Aikawa T,Watanabe S. Lower energy content of human milk than calculated using conversion factorsPediatrics InternationalYear: 2005471792-s2.0-1464439791915693858
28. Jackson MB,Lammi-Keefe CJ,Jensen RG,Couch SC,Ferris AM. Total lipid and fatty acid composition of milk from women with and without insulin-dependent diabetes mellitusAmerican Journal of Clinical NutritionYear: 19946033533612-s2.0-00279669048074065
29. Kent JC,Mitoulas LR,Cregan MD,Ramsay DT,Doherty DA,Hartmann PE. Volume and frequency of breastfeedings and fat content of breast milk throughout the dayPediatricsYear: 20061173e387e3952-s2.0-3364502800216510619
30. Marquis GS,Penny ME,Zimmer JP,Díaz JM,Marín RM. An overlap of breastfeeding during late pregnancy is associated with subsequent changes in colostrum composition and morbidity rates among peruvian infants and their mothersJournal of NutritionYear: 20031338258525912-s2.0-004220986512888642
31. Mitoulas LR,Kent JC,Cox DB,Owens RA,Sherriff JL,Hartmann PE. Variation in fat, lactose and protein in human milk over 24 h and throughout the first year of lactationBritish Journal of NutritionYear: 200288129372-s2.0-003630720612117425
32. Narang APS,Bains HS,Kansal S,Singh D. Serial composition of human milk in preterm and term mothersIndian Journal of Clinical BiochemistryYear: 200621189942-s2.0-33644886377
33. Ruegg M,Blanc B. The fat globule size distribution in human milkBiochimica et Biophysica ActaYear: 198166617142-s2.0-00197714207295765
34. Saarela T,Kokkonen J,Koivisto M. Macronutrient and energy contents of human milk fractions during the first six months of lactationActa PaediatricaYear: 2005949117611812-s2.0-2714444812216203669
35. Shehadeh N,Aslih N,Shihab S,Werman MJ,Sheinman R,Shamir R. Human milk beyond one year post-partum: lower content of protein, calcium, and saturated very long-chain fatty acidsJournal of PediatricsYear: 200614811221242-s2.0-3074443390116423611
36. Van Beusekom CM,Zeegers TA,Martini IA,et al. Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid compositionAmerican Journal of Clinical NutritionYear: 19935769389432-s2.0-00272122458503365
37. Wan ZX,Wang XL,Xu L,Geng Q,Zhang Y. Lipid content and fatty acids composition of mature human milk in rural North ChinaBritish Journal of NutritionYear: 201010369139162-s2.0-7795034665119825220
38. Yamawaki N,Yamada M,Kan-no T,Kojima T,Kaneko T,Yonekubo A. Macronutrient, mineral and trace element composition of breast milk from Japanese womenJournal of Trace Elements in Medicine and BiologyYear: 2005192-31711812-s2.0-2774459101516325533
39. Reilly JJ,Ashworth S,Wells JCK. Metabolisable energy consumption in the exclusively breast-fed infant aged 3–6 months from the developed world: a systematic reviewBritish Journal of NutritionYear: 200594156632-s2.0-2544453035316115333
40. Newburg DS,Neubauer SH. Jensen RGCarbohydrates in milk: analysis, quantities and significanceHandbook of Milk CompositionYear: 1995San Diego, Calif, USAAcademic Press273338
41. Arthur PG,Kent JC,Hartmann PE. Metabolites of lactose synthesis in milk from diabetic and nondiabetic women during lactogenesis IIJournal of Pediatric Gastroenterology and NutritionYear: 19941911001082-s2.0-00280703777965458
42. Chen DC,Nommsen-Rivers L,Dewey KG,Lönnerdal B. Stress during labor and delivery and early lactation performanceAmerican Journal of Clinical NutritionYear: 19986823353442-s2.0-00318692139701191
43. Coppa GV,Gabrielli O,Pierani P,Catassi C,Carlucci A,Giorgi PL. Changes in carbohydrate composition in human milk over 4 months of lactationPediatricsYear: 19939136376412-s2.0-00275185838441573
44. Kulski JK,Hartmann PE. Changes in human milk composition during the initiation of lactationAustralian Journal of Experimental Biology & Medical ScienceYear: 1981591011147236122
45. Lonnerdal B,Forsum E,Hambraeus L. A longitudinal study of the protein, nitrogen, and lactose contents of human milk from Swedish well nourished mothersAmerican Journal of Clinical NutritionYear: 19762910112711332-s2.0-0017058795973601
46. Mohammad MA,Sunehag AL,Haymond MW. Effect of dietary macronutrient composition under moderate hypocaloric intake on maternal adaptation during lactationAmerican Journal of Clinical NutritionYear: 2009896182118272-s2.0-6684911191319386740
47. Neubauer SH,Ferris AM,Chase CG,et al. Delayed lactogenesis in women with insulin-dependent diabetes mellitusAmerican Journal of Clinical NutritionYear: 199358154602-s2.0-00272883668317390
48. Viverge D,Grimmonprez L,Cassanas G,Bardet L,Solere M. Variations in oligosaccharides and lactose in human milk during the first week of lactationJournal of Pediatric Gastroenterology and NutritionYear: 19901133613642-s2.0-00250030042246719
49. Neville MC,Keller R,Seacat J,et al. Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactationAmerican Journal of Clinical NutritionYear: 1988486137513862-s2.0-00242377183202087
50. Bitman J,Carlson SE,Couch SC,et al. Jensen RGMilk lipidsHandbook of Milk CompositionYear: 1995San Diego, Calif, USAAcademic Press495573
51. Atkinson SA,Lonnerdal B. Jensen RGNitrogenous components of milkHandbook of Milk CompositionYear: 1995San Diego, Calif, USAAcademic Press369385
52. Chao JCJ,Tseng HP,Chang CW,et al. Chicken extract affects colostrum protein compositions in lactating womenJournal of Nutritional BiochemistryYear: 200415137442-s2.0-034573600514711459
53. Cregan MD,De Mello TR,Kershaw D,McDougall K,Hartmann PE. Initiation of lactation in women after preterm deliveryActa Obstetricia et Gynecologica ScandinavicaYear: 20028198708772-s2.0-003671542012225305
54. Davis TA,Nguyen HV,Garcia-Bravo R,et al. Amino acid composition of human milk is not uniqueJournal of NutritionYear: 19941247112611322-s2.0-00283214658027865
55. Lonnerdal B,Woodhouse LR,Glazier C. Compartmentalization and quantitation of protein in human milkJournal of NutritionYear: 19871178138513952-s2.0-00231983593498019
56. Sanchez-Pozo A,Lopez J,Pita ML. Changes in the protein fractions of human milk during lactationAnnals of Nutrition and MetabolismYear: 198630115202-s2.0-00226434123954320
57. Butte NF,Garza C,O’Brian Smith E,Nichols BL. Human milk intake and growth in exclusively breast-fed infantsJournal of PediatricsYear: 198410421871952-s2.0-00213445596694010
58. Butte NF,Wong WW,Klein PD,Garza C. Measurement of milk intake: tracer-to-infant deuterium dilution methodBritish Journal of NutritionYear: 19916513142-s2.0-00260709421997129
59. Butte NF,Wong WW,Ferlic L,O’Brian Smith E,Klein PD,Garza C. Energy expenditure and deposition of breast-fed and formula-fed infants during early infancyPediatric ResearchYear: 19902866316402-s2.0-00252256802284162
60. Casey CE,Neifert MR,Seacat JM,Neville MC. Nutrient intake by breast-fed infants during the first five days after birthAmerican Journal of Diseases of ChildrenYear: 198614099339362-s2.0-00224925833740001
61. Davies PSW,Wells JCK,Lucas A. Adjusting milk intake for body size in early infancyEarly Human DevelopmentYear: 199436161672-s2.0-00280144018026365
62. De Bruin NC,Degenhart HJ,Gàl S,Westerterp KR,Stijnen T,Visser HKA. Energy utilization and growth in breast-fed and formula-fed infants measured prospectively during the first year of lifeAmerican Journal of Clinical NutritionYear: 19986758858962-s2.0-00319802819583846
63. Dollberg S,Lahav S,Mimouni FB. A comparison of intakes of breast-fed and bottle-fed infants during the first two days of lifeJournal of the American College of NutritionYear: 20012032092112-s2.0-003495646511444415
64. Evans KC,Evans RG,Royal R,Esterman AJ,James SL. Effect of caesarean section on breast milk transfer to the normal term newborn over the first week of lifeArchives of Disease in ChildhoodYear: 2003885F380F3822-s2.0-004276276012937041
65. Goldberg GR,Prentice AM,Coward WA,et al. Longitudinal assessment of the components of energy balance in well-nourished lactating womenAmerican Journal of Clinical NutritionYear: 19915457887982-s2.0-00260056291951148
66. Krebs NF,Reidinger CJ,Robertson AD,Hambidge KM. Growth and intakes of energy and zinc in infants fed human milkJournal of PediatricsYear: 1994124132392-s2.0-00280144378283374
67. Michaelsen KF,Larsen PS,Thomsen BL,Samuelson G. The Copenhagen Cohort Study on infant nutrition and growth: breast-milk intake, human milk macronutrient content, and influencing factorsAmerican Journal of Clinical NutritionYear: 19945936006112-s2.0-00282659348116536
68. Motil KJ,Sheng HP,Montandon CM,Wong WW. Human milk protein does not limit growth of breast-fed infantsJournal of Pediatric Gastroenterology and NutritionYear: 199724110172-s2.0-00309449449093980
69. Pao EM,Himes JM,Roche AF. Milk intakes and feeding patterns of breast-fed infantsJournal of the American Dietetic AssociationYear: 19807755405452-s2.0-00190872037430508
70. Santoro W Jr.,Martinez FE,Ricco RG,Jorge SM. Colostrum ingested during the first day of life by exclusively breastfed healthy newborn infantsJournal of PediatricsYear: 2010156129322-s2.0-7204908551619783000
71. Van Raaij JMA,Schonk CM,Vermaat-Miedema SH,Peek MEM,Hautvast JGAJ. Energy cost of lactation, and energy balances of well-nourished Dutch lactating women: reappraisal of the extra energy requirements of lactationAmerican Journal of Clinical NutritionYear: 19915336126192-s2.0-00258701872000814
72. Wood CS,Isaacs PC,Jensen M,Hilton HG. Exclusively breast-fed infants: growth and caloric intakePediatric nursingYear: 19881421171242-s2.0-00239682143353137
73. Butte NF,Wong WW,Garza C,et al. Energy requirements of breast-fed infantsJournal of the American College of NutritionYear: 1991101901951894876
74. Lloyd B,Halter RJ,Kuchan MJ,Baggs GE,Ryan AS,Masor ML. Formula tolerance in postbreastfed and exclusively formula-fed infantsPediatricsYear: 19991031p. E72-s2.0-17144458789
75. James RJA,James A,Drewett RF,Cheetham TD. Milk intake and feeding behavior in the first week of life and its relationship to cord blood ghrelin, leptin, and insulin concentrationsPediatric ResearchYear: 20076266956992-s2.0-3634897405817957153
76. Montandon CM,Wills C,Garza C. Formula intake of 1- and 4-month-old infantsJournal of Pediatric Gastroenterology and NutritionYear: 1986534344382-s2.0-00228700113723264
77. Garza C,Butte NF. Energy concentration of human milk estimated from 24-h pools and various abbreviated sampling schemesJournal of Pediatric Gastroenterology and NutritionYear: 1986569439482-s2.0-00229194933794916
78. Lepage G,Collet S,Bougle D. The composition of preterm milk in relation to the degree of prematurityAmerican Journal of Clinical NutritionYear: 1984405104210492-s2.0-00217502396496384
79. Lucas A,Ewing G,Roberts SB,Coward WA. How much energy does the breast fed infant consume and expand?British Medical JournalYear: 1987295659075772-s2.0-00231957423113642
80. Powe CE,Knott CD,Conklin-Brittain N. Infant sex predicts breast milk energy contentAmerican Journal of Human BiologyYear: 201022150542-s2.0-7534909716919533619
81. Wojcik KY,Rechtman DJ,Lee ML,Montoya A,Medo ET. Macronutrient analysis of a nationwide sample of donor breast milkJournal of the American Dietetic AssociationYear: 200910911371402-s2.0-5764922068019103335
82. Neville MC. Jensen RGVolume and caloric density of human milkHandbook of Milk CompositionYear: 1995San Diego, Calif, USAAcademic Press99111
83. Zangen S,Di Lorenzo C,Zangen T,Mertz H,Schwankovsky L,Hyman PE. Rapid maturation of gastric relaxation in newborn infantsPediatric ResearchYear: 20015056296322-s2.0-003477971611641459
84. Fomon SJ,Filer LJ,Thomas LN. Influence of formula concentration on caloric intake and growth of normal infantsActa Paediatrica ScandinavicaYear: 19756421721812-s2.0-00166395171168981
85. Fomon SJ. Nutritional requirements in relation to growthMonatsschr KinderheilkdYear: 1974122supplement 52362394414865
86. Brooke OG,Kinsey JM. High energy feeding in small for gestation infantsArchives of Disease in ChildhoodYear: 198560142462-s2.0-00219118013882059
87. Koletzko B,Von Kries R,Closa R,et al. Lower protein in infant formula is associated with lower weight up to age 2 y: a randomized clinical trialAmerican Journal of Clinical NutritionYear: 2009896183618452-s2.0-6684913860619386747
88. Fomon SJ,Thomas LN,Filer LJ,Ziegler EE,Leonard MT. Food consumption and growth of normal infants fed milk-based formulasActa Paediatrica Scandinavica, SupplementYear: 19712231362-s2.0-00151697225291969
89. Ziegler EE. Growth of breast-fed and formula-fed infantsNestle Nutrition Workshop Series: Paediatric Programme.Year: 200658516316902325
90. Dubois L,Girard M. Early determinants of overweight at 4.5 years in a population-based longitudinal studyInternational Journal of ObesityYear: 20063046106172-s2.0-3364546548316570091
91. Leunissen RWJ,Kerkhof GF,Stijnen T,Hokken-Koelega A. Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic risk profile in early adulthoodJournal of the American Medical AssociationYear: 200930121223422422-s2.0-6644911409319491185
92. Stettler N,Zemel BS,Kumanyika S,Stallings VA. Infant weight gain and childhood overweight status in a multicenter, cohort studyPediatricsYear: 200210921941992-s2.0-003616375511826195
93. Taveras EM,Rifas-Shiman SL,Belfort MB,Kleinman KP,Oken E,Gillman MW. Weight status in the first 6 months of life and obesity at 3 years of agePediatricsYear: 20091234117711832-s2.0-6534919439019336378
94. Bowers K,Liu G,Wang P,et al. Birth weight, postnatal weight change, and risk for high blood pressure among Chinese childrenPediatricsYear: 20111275e1272e12792-s2.0-7995550696721502227
95. Singhal A,Lanigan J,Mackey A,et al. Early Nutrition and Later Risk of ObesityYear: 2010San Diego, Calif, USAObesity Society

Article Categories:
  • Review Article

Previous Document:  Maternal and Early Childhood Risk Factors for Overweight and Obesity among Low-Income Predominantly ...
Next Document:  Alcohol Consumption, Beverage Preference, and Diet in Middle-Aged Men from the STANISLAS Study.