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A systematic review and meta-analysis of the nutrient content of preterm and term breast milk

BMC Pediatrics201414:216

DOI: 10.1186/1471-2431-14-216

Received: 1 May 2014

Accepted: 22 August 2014

Published: 30 August 2014

Abstract

Background

Breast milk nutrient content varies with prematurity and postnatal age. Our aims were to conduct a meta-analysis of preterm and term breast milk nutrient content (energy, protein, lactose, oligosaccharides, fat, calcium, and phosphorus); and to assess the influence of gestational and postnatal age. Additionally we assessed for differences by laboratory methods for: energy (measured vs. calculated estimates) and protein (true protein measurement vs. the total nitrogen estimates).

Methods

Systematic review results were summarized graphically to illustrate the changes in composition over time for term and preterm milk. Since breast milk fat content varies within feeds and diurnally, to obtain accurate estimates we limited the meta-analyses for fat and energy to 24-hour breast milk collections.

Results

Forty-one studies met the inclusion criteria: 26 (843 mothers) preterm studies and 30 (2299 mothers) term studies of breast milk composition. Preterm milk was higher in true protein than term milk, with differences up to 35% (0.7 g/dL) in colostrum, however, after postnatal day 3, most of the differences in true protein between preterm and term milk were within 0.2 g/dL, and the week 10–12 estimates suggested that term milk may be the same as preterm milk by that age. Colostrum was higher than mature milk for protein, and lower than mature milk for energy, fat and lactose for both preterm and term milk. Breast milk composition was relatively stable between 2 and 12 weeks. With milk maturation, there was a narrowing of the protein variance. Energy estimates differed whether measured or calculated, from −9 to 13%; true protein measurement vs. the total nitrogen estimates differed by 1 to 37%.

Conclusions

Although breast milk is highly variable between individuals, postnatal age and gestational stage (preterm versus term) were found to be important predictors of breast milk content. Energy content of breast milk calculated from the macronutrients provides poor estimates of measured energy, and protein estimated from the nitrogen over-estimates the protein milk content. When breast milk energy, macronutrient and mineral content cannot be directly measured the average values from these meta-analyses may provide useful estimates of mother’s milk energy and nutrient content.

Keywords

Human milk Lactation Breast milk Infant Premature

Background

Breast milk composition is variable. While breast milk is the recommended feeding for all infants [13], including preterm infants [2, 4, 5], its variable composition makes estimating nutrient intakes difficult. Milk produced by mothers who deliver prematurely is well known to be higher in protein [4, 5]. Milk composition changes with postnatal age; protein content decreases over weeks after birth [6]. Breast milk fat and energy content varies from the start to the end of a feeding, and follows a diurnal pattern in both term [7, 8] and preterm milk [8, 9].

In addition, there are several reasons for the variability in the values of breast milk composition due to laboratory methods used for the analysis. Two approaches have been used to quantify energy in breast milk: a) direct energy quantification by combusting in a bomb calorimetry and b) calculated energy estimates using Atwater energy multiplication factors for the macronutrients: protein, fat, and carbohydrate [10]. Two methods used to estimate protein content include a) direct quantification of the true protein content and b) quantification of the nitrogen (assuming that all nitrogen is protein, rather than recognition that some is in non-protein nitrogen compounds [1113].

Thus we conducted a systematic review and meta-analysis of observational studies on the composition of breast milk nutrient content (energy, macronutrient (protein, lactose, fat)) and mineral content (calcium, phosphorus). We hypothesized that the composition of breast milk depends on four variables, which include: gestational stage (premature birth), postnatal age, calculated versus measured energy estimates, and protein method (true protein versus total nitrogen). We conducted the meta-analyses of breast milk composition stratified by these 4 factors (gestational stage; postnatal age; energy estimation method [measurement vs. calculation]; and protein estimation method [true protein versus total nitrogen]), to determine whether any or all of these factors should be considered when estimating breast milk nutrient content.

Methods

Literature search

In an attempt to find all published literature on the topic, studies relating to breast milk content in premature and mature milk were identified through computerized searches. First searches were conducted in MedLine and Embase for studies published in any language using the following Medical Subject Headings and text words: human, milk, lactation, breast milk, breast milk, protein, energy calories, lactose, oligosaccharide(s), fat, calcium, phosphorus, and infant, premature, preterm, neonate, or newborn, independently by the two investigators (DG and TRF) in March 2014. In an effort to include all available studies, a Web of Science search was conducted for all papers that cited the references Schanler et al. 1980 [14] and Atkinson SA et al. 1980 [15] (by DG). A grey literature search was also conducted to avoid reporting bias and look for unpublished literature (by DG) in March 2014. We reviewed the reference lists of included papers.

The inclusion criteria were: studies that reported on analysis of energy, macronutrient (protein, fat, lactose) and/or mineral (calcium, phosphorus) content in the breast milk of healthy, term (37–42 wk of gestation) and preterm (<37 wk of gestation) infants, if the data were reported categorized by postnatal age and term versus preterm status. Review articles and commentaries were excluded. Studies conducted in developing countries (i.e. outside North America, Europe, Australia, Israel and Japan [16]) were excluded in an attempt to exclude mothers with suboptimal nutritional status. The Meta-analysis Of Observational Studies in Epidemiology (MOOSE) Proposal for Reporting [17] was used to guide this study.

Data extraction

All article titles were examined for potential fit to the inclusion criteria by the two reviewers (DG and TRF). When the title was not clear regarding the potential fit, then the abstract was reviewed; when the abstract was not clear whether the study fit the inclusion criteria, the paper was reviewed. In studies where the data was presented in a non-numerical format, and thus not possible to include in a meta-analysis, efforts were made (by DG) to contact the author to obtain these data. If no response was received to the request or the author was unable to provide additional data, the study was not included in the meta-analysis. Data were extracted by DG and checked for accuracy by TRF.

Since breast milk fat content varies between fore and hind milk [6, 7] and diurnally between early and later in the day [79], to obtain accurate estimates we limited the meta-analyses for energy and fat to 24-hour breast milk collections. This requirement was not placed on the other analyses since the differences between fore and hind milk and diurnally in protein are not of an important magnitude [6, 7].

Analysis

Meta-analyses were carried out on studies that reported the following outcomes in either healthy, term or preterm delivering mothers: total energy (kcal/dL), protein (g/dL), fat (g/dL), lactose content (kcal/dL), calcium (mg/dL), and phosphate (mg/dL). Data was grouped into the following time points: 1–3 days (representing colostrum), 4 to 7 days, week 2 (day 8–14), week 3–4 (days 15–28), week 5–6 (days 29–42), week 7–9 (days 43 – 63), week 10–12 (days 64 – 84). We continued the meta-analyses to 12 weeks since age-specific data was sparse for the analyses after this age.

To examine whether the two energy measures, bomb calorimetry and calculation methods, estimated different energy contents, separate meta-analyses were prepared for each energy estimation method and compared. Energy reported as kilojoules was converted to kilocalories by dividing by 4.184.

Historically, protein in breast milk has been estimated in two different ways: including or excluding the non-protein nitrogen. Thus, we conducted two meta-analyses of protein for the available data: an estimate of protein based on the assumption that all of the nitrogen is protein and a true protein estimate which excludes the non-protein nitrogen. When only total protein was only reported in terms of total nitrogen, total protein was calculated by multiplying the nitrogen by 6.25 [1214, 1823].

Mineral data reported as millimoles was converted to milligrams by multiplying by the molecular weight. Breast milk data reported per kilogram was converted to per liter by dividing by 1.032 [24].

The nutrient content meta-analyses were calculated as weighted averages and pooled standard deviation for each time period, for preterm and term breast milk. For statistical comparisons, t-tests were used to compare preterm and term milk composition. Given the multiple comparisons made in this study, an approximate Bonferroni adjustment was made, and the p-value for statistical significance used was 0.001.

Results

A total of 41 studies were included in the analysis: 26 (843 mothers) and 30 (2299 mothers) studies reporting on preterm and term breast milk composition, respectively (Table 1). Attempts were made to contact authors of nine studies, we received replies from four, but no additional information was received for the meta-analyses. Ninety-nine studies were excluded for reasons provided in Figure 1: no original data/review articles [2539], studies performed in developing countries [4048], no numerical results [4959], not 24-hour milk collection/pooled milk (required only for energy and fat contents) [79, 6070], no report of macro/micronutrient contents [36, 71107], did not report time frames used in the meta-analyses [108116], other [117, 118]. Energy was estimated in 11 studies using bomb calorimetry [11, 12, 18, 119126] and in five studies by calculation using values for the energy contributions from fat, protein, and carbohydrate [6, 19, 22, 121, 127]. Protein was estimated based on total nitrogen in 23 studies [6, 1114, 1823, 120, 122, 123, 125, 128135] and as a true protein estimate in 15 studies [1114, 18, 19, 121123, 127129, 136139]. A summary of the meta-analyses breast milk composition at various postnatal ages for energy, protein, fat, calcium and phosphorus is outlined in Table 2.
Table 1

Studies included in the meta-analysis

Reference

Site

Subjects

Reported outcomes

  

  Preterm

 n

  Term

 n

 

Anderson et al., 1983 [18]

US

28-36 weeks

14

37-42 weeks

9

E, Pro, fat

Arnold et al., 1987 [130]

Australia

26-33 weeks

6

38-40 weeks

7

Pro, lactose

Atkinson et al., 1980 [15]

Canada

26-33 weeks

13

38-40 weeks

10

Ca, P

Atkinson et al., 1981 [19]

Canada

BW < 1300 g

7

-

 

E, Pro, lactose, fat

Bejiers et al., 1992 [128]

Netherlands

25.7–30.9 weeks

30

-

 

Pro

Britton et al., 1986 [137]

US

25-35 weeks

70

38-42 weeks

38

Pro

Butte et al., 1984 [13]

US

< 37 weeks

8

≥ 37 weeks

13

Pro, Ca, P

Butte et al., 1984 [122]

US

-

 

Term

40

E, Pro, fat

Butte NF et al., 1990 [123]

US

-

 

39.9 ± 0.9 weeks

40

E, Pro, lactose, fat

Coppa et al., 1993 [140]

Italy

-

 

Term

46

Lactose, oligo

Coppa et al., 1997 [141]

Italy

27-35 weeks

26

-

 

Oligo

Corvaglia et al., 2008 [20]

Italy

26-32 weeks

55

37-41 weeks

69

Pro

Cregan MD, 2002 [135]

Australia

31-35 weeks

22

> 38 weeks

16

Pro, lactose

Ehrenkranz et al., 1984 [142]

US

26-33 weeks

21

-

 

fat

Faerk et al., 2001 [133]

Denmark

< 32 weeks

101

-

 

Pro

Ferris et al., 1988 [21]

US

-

 

> 37 weeks

12

Pro, lactose

Garza et al., [124]

US

-

 

Term

10

E

Gabrielli et al., 2011 [143]

Italy

25-30 weeks

63

-

 

Lactose, oligo

Gross et al., 1980 [131]

US

28-36 weeks

33

38-42 weeks

18

Pro, lactose, Ca

Guerrini et al., 1981 [144]

Italy

29-37 weeks

25

38-42 weeks

47

fat

Hibberd et al., 1982 [11]

UK, Germany

-

 

> 37 weeks

10

E, Pro, lactose, fat, Ca

Hosoi et al., 2005 [134]

Japan

-

 

Term

114

Pro

Hurgoiu et al., 1986 [145]

Romania

27-34 weeks

28

-

 

Ca

Itabashi et al., 1999 [129]

Japan

26-33 weeks

15

-

 

Pro, lactose, Ca, P

Lepage et al., 1984 [120]

Canada, US

26-36 weeks

32

> 37 weeks

19

E, Pro

Lemons et al., 1982 [12]

US

27-37 weeks

20

39-41 weeks

7

E, Pro, lactose, fat, Ca, P

Maas et al., 1998 [22]

Netherlands

25-29 weeks

79

-

 

E, Pro, lactose, fat

Michaelsen et al., 1994 [139]

Denmark

-

 

37-41weeks

91

Pro, fat, lactose

Montagne et al., 1999 [136]

France

< 37 weeks

46

> 37 weeks

28

Pro

Motil et al., 1997 [125]

US

-

 

38-42 weeks

10

E, Pro

Nommsen et al., 1991 [127]

US

-

 

Term

58

E, Pro, fat

Reinken et al., 1985 [132]

Germany

28-33 weeks

16

38-40 weeks

24

Pro

Saarela et al., 2005 [6]

Finland

31.4 ± 3 weeks

36

40.2 ± 1.4 weeks

53

E, Pro, lactose, fat

Sadurskis et al., 1998 [119]

Sweden

  

Term

23

E

Sanchez-Pozo et al., 1986 [138]

Spain

  

Term

209

Protein

Sann et al., 1981 [146]

France

26-35 weeks

41

38-41 weeks

61

Pro, lactose, fat, Ca, P,

Schanler et al., 1980 [14]

US

29.7 ± 0.5 weeks

16

-

 

Pro, Ca

Thomas et al., 1986 [121]

US

30-34 weeks

20

-

 

E, Pro, lactose, fat

Yamawaki et al., 2005 [23]

Japan

-

 

BW > 2500 g

1180

Pro, lactose, Ca, P

Viverge et al., 1990 [147]

France

-

 

Term

15

Lactose, oligo

Wood et al., 1988 [126]

US

-

 

37-42 weeks

22

E

Total

  

843

 

2299

 

E = energy, Pro = protein, oligo = oligosaccharides, Ca = calcium, P = phosphate, BW = birth weight, g = gram, UK = United Kingdom, US = United States.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig1_HTML.jpg
Figure 1

Flow diagram of the literature search process.

Table 2

Meta-analysis summary estimates of breast milk composition per 100 milliliters at various postnatal ages (mean (+/−2 standard deviations))

Preterm

Energy (kcal)

Protein (g)

Fat (g)

Calcium (mg)

Phosphorus (mg)

1st week

60 (45–75)

2.2 (0.3-4.1)

2.6 (0.5-4.7)

26 (9–43)

11 (1–22)

2nd week

71 (49–94)

1.5 (0.8-2.3)

3.5 (1.2-5.7)

25 (11–39)

15 (8–21)

Week 3/4

77 (61–92)

1.4 (0.6-2.2)

3.5 (1.6-5.5)

25 (13–36)

14 (8–20)

Week 10/12

66 (39–94)

1.0 (0.6-1.4)

3.7 (0.8-6.5)

29 (19–38)

12 (8–15)

Term

Energy (kcal)

Protein (g)

Fat (g)

Calcium (mg)

Phosphorus (mg)

1st week

60 (44–77)

1.8 (0.4-3.2)

2.2 (0.7-3.7)

26 (16–36)

12 (6–18)

2nd week

67 (47–86)

1.3 (0.8-1.8)

3.0 (1.2-4.8)

28 (14–42)

17 (8–27)

Week 3/4

66 (48–85)

1.2 (0.8-1.6)

3.3 (1.6-5.1)

27 (18–36)

16 (10–22)

Week 10/12

68 (50–86)

0.9 (0.6-1.2)

3.4 (1.6-5.2)

26 (14–38)

16 (9–22)

Estimates as +/− 2 standard deviations assumed no skew. Energy values were bomb calorimeter measured values except for 10–12 weeks, which were calculated values. Protein values are true measured protein, not based on total nitrogen content.

Energy measurement vs. calculation from the macronutrients

In the comparison between measured and calculated energy contents of milk, measured estimates were −6 to 10 kcal/dL (−9 to 13%) greater than the calculated analyses (Table 3, Figures 2 and 3), but only four differences (preterm milk at weeks 3–4 and 7–9, term milk at weeks 7–9 and 10–12 weeks) met the adjusted statistical significance criteria (i.e. p < 0.001). Most of the preterm measured energy estimates had less than 30 subjects (Table 3), and while the calculated energy estimates generally had higher numbers; none of the studies that reported calculated energy estimates had any data for the first few postnatal days (Figure 2 and 3, Table 3).
Table 3

Meta-analysis results of preterm and term breast milk energy content over time from measured and calculated estimates

Comparison: Bomb calorimetry energy measurement (kcal/dL)♦

 

Preterm

  

Term

  

Preterm & term compared

Time frame:

mean

SD

n

Mean

SD

n

% difference

p-value

d 1-3

49

7

12

54

8

19

−10

0.34

d 4-7

71

9

52

66

9

37

7

0.02

week 2

71

12

53

66

9

34

7

0.04

week 3-4

77

8

27

66

8

97

16

< 0.00001*

week 5-6

70

5

14

63

7

40

11

< 0.00001*

week 7-9

76

8

11

63

7

77

21

< 0.00001*

week 10-12

-

-

-

63

8

83

-

-

Energy meta-analysis was limited to 24 hour collections

References: [11, 12, 18, 119126]

Comparison: Calculated energy content (kcal/dL)♦♦

 

Preterm

  

Term

  

Preterm & term compared

Time frame:

mean

SD

n

Mean

SD

n

% difference

p-value

d 1-3

-

-

-

-

-

-

  

d 4-7

65

13

41

68

9.6

48

−5

0.21

week 2

70

14

95

-

-

-

  

week 3-4

68

8.0

135

70

9.3

46

−2

0.26

week 5-6

67

6.9

79

-

-

-

  

week 7-9

66

8.9

63

69

9.9

43

−4

0.16

week 10-12

66

14

14

68

9.0

95

−3

0.50

♦♦ References: [6, 19, 22, 121, 127]

Comparison: Measured vs. calculated energy

 

Preterm

 

Term

     
 

Difference

% difference

p-value

Difference

% difference

p-value

  

d 1-3

 

-

-

 

-

-

  

d 4-7

6

−9%

0.009

−2

2%

0.350

  

week 2

1

−2%

0.66

     

week 3-4

9

−11%

< 0.00001*

−3

5%

0.007

  

week 5-6

3

−5%

0.11

     

week 7-9

10

−13%

0.0009*

−6

9%

0.0003*

  

week 10-12

   

−5

9%

0.0002*

  

*Statistically significant difference. In compensation for multiple comparisons, an approximate Bonferroni adjustment was made and the p-value for statistical significance was < 0.001.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig2_HTML.jpg
Figure 2

Measured Energy distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig3_HTML.jpg
Figure 3

Calculated Energy estimates distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

Protein estimation method [true protein versus total nitrogen estimate]

Almost all of the differences in protein content, between the estimates of protein based on total nitrogen content and the measured true protein estimates were statistically significantly lower for the true protein measures for most time periods, for both term and preterm milk, (Table 4, Figures 4 and 5). The most common differences in quantity between the total nitrogen and true protein estimates was 0.3 g/dL (Table 4).
Table 4

Meta-analysis results of preterm and term breast milk protein content over time

Comparison: True protein comparisons: Preterm vs. term (g/dL)♦

 

Preterm

Term

Preterm & term compared

Time frame:

mean

SD

n

mean

SD

n

% difference

p-values

d 1-3

2.7

1.5

141

2.0

0.9

108

35

< 0.00001*

d 4-7

1.7

0.5

165

1.6

0.3

185

7

0.005

week 2

1.5

0.4

191

1.3

0.2

256

16

< 0.00001*

week 3-4

1.4

0.4

92

1.1

0.2

194

27

< 0.00001*

week 5-6

1.1

0.2

38

1.0

0.1

85

7

0.0003

week 7-9

1.1

0.2

30

0.9

0.1

113

20

< 0.00001*

week 10-12

1.0

0.2

25

1.0

0.1

221

2

0.37

References: [1114, 18, 19, 121123, 127129, 136139]

Comparison: Total protein comparisons: Preterm vs. term (g/dL)♦♦

 

Preterm

Term

Preterm & term compared

Time frame:

mean

SD

n

mean

SD

n

% difference

p-values

d 1-3

2.8

1.1

94

2.0

0.6

168

37

< 0.00001*

d 4-7

2.1

0.5

244

2.0

0.5

229

4

0.04

week 2

1.9

0.4

253

1.8

0.4

192

8

< 0.00001*

week 3-4

1.6

0.4

439

1.5

0.3

210

9

0.01

week 5-6

1.4

0.3

268

1.1

0.2

357

18

< 0.00001*

week 7-9

1.1

0.2

183

1.3

0.2

453

−10

< 0.00001*

week 10-12

1.3

0.3

18

1.2

0.2

109

12

0.07

♦♦ References: [6, 1114, 1823, 120, 122, 123, 125, 128135]

Comparisons: True vs. Total protein ♦♦♦

 

Difference

% difference

p-value

Difference

% difference

p-value

  

d 1-3

0.1

4%

0.60

0

1%

0.91

  

d 4-7

0.3

20%

< 0.00001*

0.4

24%

< 0.00001*

  

week 2

0.4

26%

< 0.00001*

0.5

36%

< 0.00001*

  

week 3-4

0.2

12%

< 0.00001*

0.4

31%

< 0.00001*

  

week 5-6

0.3

27%

< 0.00001*

0.1

11%

< 0.00001*

  

week 7-9

0

3%

0.35

0.3

37%

< 0.00001*

  

week 10-12

0.3

32%

0.0002

0.2

20%

< 0.00001*

  

♦♦♦Estimates based on true protein content versus the assumption that all nitrogen is protein.

*Statistically significant difference. In compensation for multiple comparisons, an approximate Bonferroni adjustment was made and the p-value for statistical significance was < 0.001.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig4_HTML.jpg
Figure 4

True Protein content distribution of preterm and term breast milk in by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig5_HTML.jpg
Figure 5

Fat content distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

Gestational stage effect: preterm milk compared to term milk

In a comparison of the term versus preterm milk, most of the analytes (with the exception of fat and calculated energy) had some differences between the preterm and term milk composition that were statistically significant (Tables 3, 4, 5, 6, 7).
Table 5

Meta-analysis results of preterm and term breast milk fat, lactose and oligosaccharide content over time

 

Preterm

Term

Preterm & term compared

Fat (g/dL)♦

Time frame:

mean

SD

n

mean

SD

n

% difference

p-value

d 1-3

2.2

0.9

76

1.8

0.7

74

23

0.002

d 4-7

3.0

1.2

111

2.6

0.8

136

16

0.002

week 2

3.5

1.1

158

3.0

0.9

48

15

0.01

week 3-4

3.5

1.0

180

3.4

0.8

127

5

0.12

week 5-6

3.2

0.8

95

3.6

1.1

20

−11

0.07

week 7-9

3.3

0.9

120

3.4

0.8

83

−3

0.38

week 10-12

3.7

1.5

22

3.4

0.9

95

7

0.31

Fat meta-analysis was limited to 24 hour collections.

References: [6, 11, 12, 18, 19, 22, 121123, 125, 127, 142, 144, 146]

Lactose (kcal/dL)♦♦

Time frame:

mean

SD

n

mean

SD

n

% difference

p-value

d 1-3

5.1

0.7

95

5.6

0.6

59

−9

< 0.00001*

d 4-7

6.3

1.1

114

6.0

1.0

281

4

0.009

week 2

5.7

0.8

231

6.2

0.6

100

−8

< 0.00001*

week 3-4

6.0

0.5

225

6.7

0.7

193

−10

< 0.00001*

week 5-6

5.8

0.6

104

6.1

1.0

22

−6

0.06

week 7-9

6.3

0.4

123

6.5

0.5

646

−2

< 0.00001*

week 10-12

6.8

0.3

28

6.7

0.7

58

2

0.47

♦♦References: [6, 11, 12, 19, 2123, 121, 123, 129131, 135, 140, 143, 146, 147]

Oligosaccharides (g/dL) ♦♦♦

    

Time frame:

mean

SD

n

mean

SD

n

% difference

p-value

d 1-3

-

-

-

1.6

0.2

9

-

-

days 4-7

2.1

0.4

89

1.9

0.4

93

12

0.0009

week 2 (days 7–14)

2.1

0.5

89

1.9

0.4

54

7

0.004

week 3–4 (days 15–30)

1.7

0.3

152

1.6

0.3

46

12

0.27

week 5-6

-

-

-

1.4

0.3

46

-

-

week 7-9

-

-

-

1.3

0.3

46

-

-

week 10-12

-

-

-

-

-

-

-

-

♦♦♦References: [140, 141, 143, 147].

*Statistically significant difference. In compensation for multiple comparisons, an approximate Bonferroni adjustment was made and the p-value for statistical significance was < 0.001.

Table 6

Meta-analysis results of preterm and term breast milk mineral content over time

 

Preterm

Term

Preterm & term compared

Calcium (mg/dL)♦

Time frame:

mean

SD

n

mean

SD

n

% difference

p-value

d 1-3

25

9

50

26

6

26

−3

0.6

d 4-7

27

9

88

26

4

86

5

0.34

week 2

25

7

116

28

7

100

−10

0.002

week 3-4

25

6

108

27

5

85

−8

0.01

week 5-6

28

6

41

25

6

223

11

0.004

week 7-9

30

6

37

26

6

363

15

0.0002*

week 10-12

29

5

30

27

3

13

6

0.17

References: [1115, 23, 88, 129, 131, 145, 146]

Phosphate (mg/dL)♦♦

Time frame:

mean

SD

n

mean

SD

n

% difference

p-value

d 1-3

10

7

7

11

3

6

−14

0.62

d 4-7

13

4

79

13

4

86

3

0.50

week 2

15

3

67

15

4

90

−4

0.44

week 3-4

14

3

56

16

3

75

−14

0.0004*

week 5-6

13

2

33

16

3

213

−16

< 0.0001*

week 7-9

14

2

29

16

3

363

−13

0.002

week 10-12

12

2

22

14

3

13

−19

0.03

♦♦ References: [12, 13, 15, 23, 88, 129, 131, 146]

*Statistically significant difference. In compensation for multiple comparisons, an approximate Bonferroni adjustment was made and the p-value for statistical significance was < 0.001.

Table 7

The milk maturity effect: Comparison of colostrum versus mature milk

 

Energy (measured)

Protein (true protein)

Fat

Lactose

 

Preterm

Term

Preterm

Term

Preterm

Term

Preterm

Term

Colostrum

49

54

2.7

2.0

2.2

1.8

5.1

5.6

Mature milk

73

63

1.1

1.0

3.3

3.4

6.2

6.5

Difference

49%

16%

−61%

−52%

50%

93%

21%

16%

p-value

<0.00001*

<0.00001*

<0.00001*

<0.00001*

<0.00001*

<0.00001*

<0.00001*

<0.00001*

 

Calcium

Phosphate

 
 

Preterm

Term

Preterm

Term

Colostrum

25

26

9.5

11

Mature milk

29

26

12.8

16

Difference

13%

−2%

35%

41%

p-value

0.003

0.62

0.002

0.001

*met our approximate Bonferroni adjusted p-value criteria for statistical significance was < 0.001.

Colostrum was milk collected in the first 3 days, mature milk was collected between 5 to 12 weeks. The difference values less than 100% reflect lower values for mature milk, differences greater than 100% reflect higher values for colostrum compared to mature milk.

The energy content of preterm milk was similar to term milk at all postnatal ages, with three significant differences for the bomb calorimetric methods between 3 to 9 weeks; with differences of −10-21% (Table 3, Figures 2 and 3). We found no measured energy content data on preterm milk after 9 weeks.

Preterm milk was higher in true protein than term milk, with maximum mean differences up to 35% (0.7 g/dl) in the first few days after birth (Table 4, Figure 4). However, after postnatal day 3, most of the differences in true protein between preterm and term milk were within 0.2 g/dL or less, and the week 10–12 estimates suggested that term milk may be the same as preterm milk by that age. The estimates of protein based on total nitrogen suggested differences between preterm and term milk as high as 37% (0.8 g/dl) in the first few days, however after day 3, the most common difference between preterm and term protein estimates based on total nitrogen was 0.1 g/dL (Table 4).

The fat content of the preterm milk did not differ statistically (all p-values > 0.001) between preterm and term milk at any point in time, even though preterm milk was 23% higher than term milk (non-significant) in the first few days of life (Table 5, Figure 5).

Lactose was significantly lower in preterm milk compared to term milk, in the first 3 days and at a few later time points (Table 5, Figure 6). The general pattern of oligosaccharides showed similarities between preterm and term milk, although there was limited data for preterm milk (data only on days 4 – week 4) (Table 5, Figure 7). One difference was statistically significant for days 4–7 when preterm milk was 12% higher than term milk.
https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig6_HTML.jpg
Figure 6

Lactose content distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig7_HTML.jpg
Figure 7

Oligosaccharide content distribution of preterm and term breast milk oligosaccharide content in by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

The minerals, calcium and phosphate, were mostly similar between preterm and term milk. (Table 6, Figures 8 and 9).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig8_HTML.jpg
Figure 8

Calcium content distribution of preterm and term breast milk calcium content in by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2431-14-216/MediaObjects/12887_2014_Article_1248_Fig9_HTML.jpg
Figure 9

Phosphate content distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

The milk maturity effect

In general, the meta-analyses of breast milk composition revealed relatively stable milk content between 2 and 12 weeks, after the initial fluctuations as the milk changed from colostrum to more mature milk (Tables 3, 4, 5, 6 and 7, Figures 2, 3, 4, 5, 6, 7, 8 and 9). The composition of colostrum compared to more mature milk (5 to 12 weeks) differed for all of the macronutrients by 16% or more (Table 2, Figures 2, 3, 4, 5, 6 and 7). Compared to colostrum, mature milk protein content decreased dramatically while fat increased by approximately one half in preterm milk or doubled in term milk. Measured energy and lactose were higher in mature milk compared to colostrum (Tables 3 and 5 Figures 2 and 6).

With milk maturation, there was a notable narrowing of the true protein variance in preterm milk, from the wide estimated 0 to 5.7 g/dL reference interval (+/− 2 standard deviations) in colostrum to the narrower mature milk estimated 0.6 to 1.4 g/dL at 12 weeks.

Discussion

Much has been written about the differences between preterm and term breast milk, particularly about the nutritional superiority of preterm milk. This meta-analysis revealed more similarities than differences between preterm and term milk for energy, fat, oligosaccharides, calcium, and phosphorus. Gestational age (preterm vs term milk); postnatal age; protein estimation method [true protein versus total nitrogen estimate] and energy estimation method [measured versus calculated] were each found to identify important differences in breast milk content. Thus these factors should be considered when estimating breast milk nutrient content and in designing future studies to analyze breast milk nutrient content.

For energy, the differences between measured and calculated estimates of breast milk composition were only significantly different at three time points for preterm milk, however, the differences were as high as 10 kcal/dL (13%), which are likely clinically important differences. This data suggests that measured energy content of breast milk is superior to calculated methods.

It is possible that errors in the calculation of energy content of milk could be due to the various conversion factors used to calculate the energy contributions of the macronutrients and also from assuming that all of the nitrogen was protein [6, 19, 22] and that the only carbohydrate was lactose [6, 19, 121], which would contribute to an over- and an under-estimation, respectively, of the energy content of the milk [6].

The mean protein in early preterm milk was higher than in term milk at some time points during the first weeks, but also of importance, the variability of the protein content in preterm milk was twice that of term milk at most time points. The decrease in protein content and variance with postnatal age for preterm and term milk were similar over time. Although the differences in protein content between preterm and term milk were statistically significant for several time points, the differences may be only likely of clinical importance in the first few postnatal days. The meta-analysis revealed that protein content of preterm early milk may be very low in some mothers, based on the calculated reference intervals (mean +/− two (1.96) standard deviations, assuming that the milk composition was not skewed) of 0 to 5.6 g/dl. However biological parameters often are skewed. Further research is needed to describe the preterm milk protein distribution, range, and distribution symmetry.

The most dramatic changes from colostrum to mature milk was the decrease in protein and increase in fat, in both preterm and term milk, as well as the increase in energy in preterm milk (Table 7). There is evidence that the protein content of breast milk continues to decrease over time after birth, as revealed by analyses of donor breast milk reports that donated breast milk contains on average 0.9 grams of protein per 100 mL [110, 113, 148]. One of these studies of donated milk assessed the milk protein content at 8 months of postnatal age, and found the protein was 0.7 g/dL [110]. These studies did not meet our inclusion criteria since the milk from both preterm and term delivering mothers were combined [110, 113, 148].

Some researchers presented their estimates of breast milk protein content based on the total nitrogen, assuming that all of the nitrogen represented protein [6, 1114, 1823, 120, 122, 123, 125, 128135], some presented both protein estimates [1114, 18, 128, 129], while other researchers reported only true protein estimates [1114, 18, 19, 121123, 127129, 136139]. The protein meta-analysis estimates based on total protein were almost uniformly higher than the true protein estimates, which suggest that these two approaches should not be averaged together. It has been suggested that the higher protein content of colostrum and early milk compared with later postnatal ages may not be digestible since much of this early non-protein nitrogen is non-digestible lactoferrin and IgA [128, 149]. If some of this “protein” is not digestible, then it would not be available to meet nutritional protein needs.

This study was limited by the availability of results from the individual studies, and the various milk collection and analysis methods used. The minor undulations in the graphs may not represent real changes in breast milk nutrient content, but be due to differences between the studies and their methods. Another limitation was the limited sample sizes for some of the analyses.

Conclusion

The protein content of breast milk decreases after birth to be less than half of the colostrum content by 6 weeks. Most of the differences in true protein between preterm and term milk were within 0.2 g/dL, and by 3 months of age, term milk may have the same protein content as preterm milk. The four parameters assessed in this study (postnatal age, gestational stage (preterm versus term), protein estimated from nitrogen versus measured protein content, and energy calculated from macronutrients versus measured using bomb calorimetry) were all found to be important predictors of breast milk content.

This meta-analysis evidence revealed that breast milk is highly variable between individuals. If breast milk energy macronutrient and mineral content cannot be directly analyzed for the individual mother and infant, the average values from these meta-analyses may provide useful estimates of the milk content.

For future research, our meta-analyses suggest that breast milk energy content calculated from the macronutrients provide poor estimates of measured energy and that protein estimated from the nitrogen over-estimates the true protein milk content.

Declarations

Authors’ Affiliations

(1)
Department of Pediatrics, University of Calgary
(2)
Nutrition Services, Alberta Health Services, Department of Community Health Sciences, Alberta Children’s Hospital Research Institute, Faculty of Medicine, University of Calgary

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