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by Ann Prentice, United Nations University

Abstract

Breastmilk contains all the nutrients required by the newborn baby. It also contains non-nutritional components that may promote infant health, growth, and development, such as antimicrobial factors, digestive enzymes, hormones, trophic factors, and growth modulators. Human milk has a unique composition, which differs from that of other mammals in its ingredients and their concentrations.

Breastmilk composition is not constant and varies with stage of lactation, breastfeeding pattern, season, and parity. It also differs among individuals and among communities, for reasons that are not well understood. Studies have demonstrated that the total concentrations of fat, protein, and lactose are relatively insensitive to current dietary intake and nutritional status, whereas the fatty acid profile and the concentrations of several micronutrients, particularly water-soluble vitamins, are responsive to maternal diet.

After other foods are added to the diet, breastmilk continues to be a valuable nutrient source and to provide non-nutritional factors even for older children. Consequently, breastfeeding for one to two or more years as part of a mixed diet has many advantages for children.

Introduction

Breastmilk is a complex fluid, rich in nutrients and in non-nutritional bioactive components.

Nutritional and non-nutritional components

Breastmilk contains all of the nutrients needed by the newborn baby during the first weeks of life. These include the metabolic fuels (fat, protein, carbohydrate), water, and the raw materials for tissue growth and development, such as fatty acids, amino acids, minerals, vitamins, and trace elements.

More than 98% of the fat in breastmilk is in the form of triglycerides, constructed within the mammary epithelial cell from medium- and long-chain fatty acids derived either from the maternal circulation (carbon chain lengths ≤ 16) or manufactured locally (carbon chain lengths ≥ 16) [5]. Short-chain fatty acids (carbon chain length ≤ 8) are only present in trace amounts. Oleic acid (18:1) and palmitic acid (16:0) are the most abundant fatty acids in breastmilk triglycerides, with comparatively high proportions of the essential fatty acids, linoleic acid (18: 2ω6) and linolenic acid (18: 3ω3). Comparatively high proportions of other long-chain polyunsaturated fatty acids, such as arachidonic acid (20: 4ω6) and docosahexaenoic acid (22: 6ω3), are also present [5]. These long-chain fatty acids are constituents of brain and neural tissue and are needed in early life for mental and visual development [6]. At least half of the triglyceride molecules in breastmilk contain palmitic acid attached to the central carbon of the glycerol component, a property that increases digestibility, absorption, and mineral balance [5, 7]. The lipid component of breastmilk is the transport vehicle for fat-soluble micronutrients such as prostaglandins and vitamins A, D, E, and K.

Proteins account for approximately 75 % of the nitrogen-containing compounds in breastmilk. Non-protein nitrogen substances include urea, nucleotides, peptides, free amino acids, and DNA. The proteins of breastmilk can be divided into two categories: micellar caseins and aqueous whey proteins, present in the ratio of about 40:60 [8]. The predominant casein of human milk is β casein, which forms micelles of relatively small volume and produces a soft, flocculent curd in the infant’s stomach. The major whey proteins are -lactalbumin, lactoferrin, secretory IgA, and serum albumin [8], with a large number of other proteins present in smaller amounts. Secretory IgA is the principal immunoglobulin of breastmilk. It is synthesized in the mammary epithelial cell by the coupling of two IgA molecules, produced locally by lymphocytes resident in the breast tissue, with two proteins, J-chain and secretory component [8]. The specificity of breastmilk secretory IgA antibodies reflects the mother’s exposure to mucosal infection and is independent of the specificity profile of blood-borne IgA [9]. Many of the proteins in breastmilk have a multitude of potential functions. Lactoferrin, for example, transports and promotes the absorption of iron, is bacteriostatic to a range of organisms, and acts as a nutritional protein, producing amino acids for absorption on digestion [8, 10].The principal carbohydrate of human milk is lactose, a β-disaccharide manufactured in the mammary epithelial cell from glucose by a reaction involving -lactalbumin [11]. In addition, breastmilk contains significant quantities of oligosaccharides, predominantly lactose-N-tetraose and its monofucosylated derivatives, representing about 10% of total milk carbohydrate. The oligosaccharide composition reflects the Lewis blood group and secretor status of the mother [12].

In addition to the nutritional components, breastmilk contains a wealth of bioactive components that may have beneficial non-nutritional functions [8, 9, 13, 14]. These include a wide range of specific and non-specific antimicrobial factors; cytokines and anti-inflammatory substances; and hormones, growth modulators, and digestive enzymes (table 1), many of which have multiple activities. These components may be of particular importance for young infants because of the immaturity of the host defence and digestive systems early in life. The physiological significance of many of these substances has yet to be determined, and some may be present merely as “spillover” or excretory products from metabolic processes occurring within the mammary epithelial cell. For those with established significance, the site of action may be within the mother’s breast, within the infant’s alimentary canal, or, after absorption, within the infant’s body. Some antimicrobial components, for example, are active both within the breast, minimizing the risk of breast infection and mastitis [15], and within the baby’s gastrointestinal and respiratory tracts, protecting the mucosal surfaces from infection by bacteria, viruses, and parasites [9]. By contrast, the site of action of the peptide feedback inhibitor of lacation (FIL) is within the breast, its function being the autocrine regulation of milk production [16]. On the other hand, casomorphins, opioid-like substances that may affect infant behaviour and mood in addition to a range of other functions, are produced in the baby’s intestines by the degradation of breastmilk casein [17]. Many bioactive substances are also valuable nutrient sources and ultimately are digested and absorbed in the normal way. Protease inhibitors in breastmilk may afford a degree of protection from digestion for some breastmilk components [8]. A sufficient proportion of antimicrobial proteins, for example, escape digestion and emerge in the faeces, suggesting that antimicrobial activity continues throughout the length of the infant’s gastrointestinal tract [10].

Comparison with animal milks

Breastmilk contains a unique combination of ingredients, differing from the milks of other mammals in both the concentration and the nature of its many components. In common with the milk of other primates, human milk has low energy and nutrient density compared with the milks of most other mammals, except for a high density of carbohydrates [4]. In addition, the daily output of the major nutrients in milk relative to the size of the mother is lower in humans than in other mammals, especially dairy and laboratory species [29].

The composition of cow’s milk, the basis of most breastmilk substitutes over the centuries, is compared with that of human milk in table 2. In addition to the obvious concentration differences, the milks differ considerably in the structure of many of the milk fractions [30]. For example, in cow’s milk the major proteins are α-casein and , β lactoglobulin; the ratio of casein to whey protein is 80:20; the casein micellar volume is double that of human milk, and the curd formed is hard; the principal milk immunoglobulin is IgG; and lactoferrin and Iysozyme are present only in small amounts [30]. Cow’s milk triglycerides contain a higher proportion of short chain fatty acids and a lower proportion of long chain and polyunsaturated fatty acids; furthermore, the positional distribution of fatty acids on the glycerol molecule is different [30]. In addition, many of the non-nutritional factors found in human milk are absent from cow’s milk or are present only in trace amounts. For the human baby, these differences affect the digestibility and absorption of nutrients, the bioavailability of micronutrients, and the potential benefits from non-nutritional factors.

TABLE 1. Examples of the non-nutritional components of breastmilk
Antimicrobial factors
secretory IgA, IgM, IgG lactoferrin lysozyme complement C3 leucocytes bifidus factor lipids and fatty acids antiviral mucins, GAGs oligosaccharides
Growth factors
epidermal (EGF) nerve (NGF) insulin-like (IGF) transforming (TGF) taurine polyamines
Cytokines and anti-inflammatory factors
tumour necrosis factor interleukins interferon- prostaglandins α1-antichymotrypsin α1-antitrypsin platelet-activating factor: acetyl hydrolase
Digestive enzymes
amylase bile acid-stimulating esterase bile acid-stimulating lipases lipoprotein lipase
Hormones
feedback inhibitor of lactation (FIL) insulin prolactin thyroid hormones corticosteroids, ACTH oxytocin calcitonin parathyroid hormone erythropoietin
Transporters
lactoferrin (Fe) folate binder cobalamin binder IgF binder thyroxine binder corticosteroid binder
Others
casomorphinsδ -sleep peptides nucleotides DNA, RNA
Introduction

The composition of breastmilk is not uniform, and the concentrations of many of its constituents change during the lactation period and differ between individual mothers. As variations in concentration are not necessarily inversely related to breastmilk volume, differences in breastmilk composition affect the daily intakes of milk components by the breastfed child. There are several factors that are known to influence the concentration of breastmilk constituents in predictable ways [31]. These include stage of lactation; breastfeeding routine; parity, age, and other maternal characteristics; regional differences; and, in some situations, season of the year and maternal diet. These are discussed in detail below.

Stage of lactation

Human lactation can be divided into four phases that differ in the composition and volume of milk produced: colostral, transitional, mature, and involutional. Colostrum is secreted for the first three to five days after delivery, transitional milk until the end of the second week, mature milk during full lactation, and involutional milk at the end of lactation. These definitions are arbitrary; the timing varies from one mother to another, and composition does not change abruptly. Typical concentrations of selected milk constituents are shown in table 3 [29, 32-35]. Notably, colostrum is rich in secretory IgA, lactoferrin, vitamin A, and sodium compared with mature milk but has relatively low concentrations of fat, lactose, and vitamin B1. Involutional milk is characterized by low lactose content and high concentrations of protein, fat, and sodium [11, 36]. Because milk volume is low during the colostral phase, rising slowly during the first week to the higher levels of established lactation [37-39], the daily intake of most milk components by breastfed babies increases after birth, reaching a peak after several weeks (table 4). The exception is secretory IgA and, hence, total protein intake, which is maximal in the first week (table 4). Mature breastmilk composition also changes during the course of lactation, although not as markedly as in the early weeks [31, 36, 40]. Many nutrients show a gradual decrease in concentration of around 10% to 30% during the first year of lactation, often reaching a low plateau thereafter. A greater decrease occurs for some components, such as zinc [41]. Some components show little change, especially those involved in osmoregulation, including lactose and sodium, whereas a few, notably Iysozyme, increase.

Breastfeeding routine

Breastmilk composition can vary during the day and from the beginning to the end of a feeding. This is most pronounced for fat and fat-soluble components such as vitamin A and zinc [5, 42]. The fat content of breastmilk can change by as much as fivefold during the course of a feeding [42]. The fat concentration is influenced by the breastfeeding routine of the mother, and short-term variations are related to the volume of milk produced per feeding and the time interval between feedings [42]. Differences in breastfeeding routine can affect the diurnal variation in fat concentration. In the Gambia, for example, where mothers feed on demand and sleep with their infants who suckle during the night, the highest breastmilk fat concentration tends to occur in the early morning, whereas in Western societies, with different feeding schedules, the early morning is associated with the lowest fat concentration of the day [42]. Other constituents, such as protein, may show small but consistent changes from the beginning to the end of a feeding and during the day [36, 43], whereas others, such as calcium, are unaffected [44].

TABLE 2. Examples of the non-nutritional components of breastmilk
Contents
Fat
Human milk
Cow’s milk
secretory IgA, IgM, IgG
4.2
3.8
fatty acids 8C (% )
trace
6
polyunsaturated fatty acids (%)
14
3
Protein (g/100 ml)
total
1.1
3.3
casein 0.4
0.3
2.5
lactalbumin
0.3
0.1
casein 0.4
0.3
2.5
lactoferrin
0.2
trace
IgA
0.1
0.003
ysozyme
0.05
trace
serum albumin
0.05
0.03
ß-lactoglobulin
0.3
Carbohydrate (g/100 ml)
lactose
7.0
4.8
oligosaccharides
0.5 0.
005
Minerals (g/100 ml)
calcium
0.030
0.125
phosphorus
0.014
0.093
sodium
0.015
0.047
potassium
0.055
0.155
chlorine
0.043
0.103
TABLE 3. Typical contents of 100 ml breastmilk produced on days 1-5 (colostrum) and more than 15 days (mature milk) post-partum
Contents
Fat
Human milk
Cow’s milk
secretory IgA, IgM, IgG
4.2
3.8
fatty acids 8C (% )
trace
6
polyunsaturated fatty acids (%)
14
3
Protein (g/100 ml)
total
1.1
3.3
casein 0.4
0.3
2.5
lactalbumin
0.3
0.1
casein 0.4
0.3
2.5
lactoferrin
0.2
trace
IgA
0.1
0.003
ysozyme
0.05
trace
serum albumin
0.05
0.03
ß-lactoglobulin
0.3
Carbohydrate (g/100 ml)
lactose
7.0
4.8
oligosaccharides
0.5 0.
005
Minerals (g/100 ml)
calcium
0.030
0.125
phosphorus
0.014
0.093
sodium
0.015
0.047
potassium
0.055
0.155
chlorine
0.043
0.103

a. Percentage ratio of concentrations in colostrum and mature milk.

b. Considerably higher on days 1-3.

Maternal parity and age

Breastmilk composition may be influenced by the parity and age of the mother. In the Gambia young, primiparous mothers have higher concentrations of several constituents, especially fat, total protein, and immunoproteins, whereas older mothers of very high parity (nine or more children) tend to produce milk with reduced quality [45-48]. Other components, such as calcium, do not change with parity [44]. Similar observations have been made in some studies elsewhere [36], but not in others, and the mechanisms involved remain elusive.

Season

The season can influence breastmilk composition. In subSahelian Africa, where food availability, infection rates, farm work, and child-care patterns vary between seasons, variations in the concentrations of some constituents, such as fat, immunoproteins, and watersoluble vitamins, have been observed [45, 49, 50]. The changes may be related, in pan, to alterations in the mother’s diet or breastfeeding behaviour. Milk ascorbate level, for example, closely parallels maternal plasma ascorbate concentration and vitamin C intake, and is high during the season when mangoes are plentiful but low for the rest of the year [50].

Region

Differences in breastmilk composition have been reported between urban and rural populations, and between different socio-economic, geographic, and ethnic groups. Failure to consider differences in duration of lactation, breastfeeding practices, maternal parity and age, sampling protocols, and assay techniques may have contributed to the impression of marked regional differences. A recent evaluation of the available data suggests that the similarities between regions are more striking than the differences, particularly with respect to the major nutrients [31]. Nevertheless, some distinct regional differences are evident, particularly in the concentrations of certain protein components, minerals, vitamins, and trace elements [31, 44, 51]. The reasons are largely unknown but may be related, in part, to the maternal diet and the local environment.

Maternal diet and nutritional status

In the past it was commonly believed that poorly nourished mothers had reduced lactational performance, in both the amount and the quality of breastmilk produced. This view has now been shown to be largely incorrect [4]. A recent examination of the world literature could not demonstrate any convincing relationships between maternal nutritional status, as indicated by body mass index (BMI), defined as weight/height2, and either breastmilk output or energy content, even in very thin mothers (BMI less than 18.5 kg/m2).

Calculated intakes assume the following daily milk volumes: day 1 (0-24 h), 40 ml; day 3 (48-72 h), 200 ml; day 8, 600 ml; 3 months, 750 ml [1, 38, 52]. concentration data from table 3 and other references in the text. Direct dietary supplementation studies mostly support this view. In a Gambian study, where poorly nourished lactating mothers were given a high-energy, nutritionally balanced supplement that provided a net energy gain of 3 MJ/day, there was no impact on breastmilk volume [4, 37]. Breastmilk fat and protein concentrations were increased slightly by the supplement, but lactose levels fell, resulting in only a marginal effect on total breastmilk energy. A review of other intervention studies concluded that there was no persuasive evidence for the positive effects of diet on breastmilk energy output [53]. Although breastmilk fat concentration has been correlated with various aspects of maternal fatness in a number of studies [4, 36], including those in the Gambia [45], this observation is not universal; in some populations negative relationships have been reported [4]. Lactation, therefore, appears to be relatively robust in the face of poor nutrition. Maternal diet can, however, affect the breastmilk concentrations of many minor constituents, particularly long-chain polyunsaturated fatty acids, some vitamins, zinc, selenium, iodine, and fluorine [51]. The profile of fatty acids in the mother’s diet and adipose tissue stores is reflected in the fatty acids of breastmilk [5, 47]. The concentrations of two water-soluble vitamins, riboflavin (vitamin B2) and ascorbic acid (vitamin C), show rapid, dose-related responses to maternal supplementation [4, 50]. The fat-soluble vitamins A, D, E, and K are less responsive to diet because of the buffering action of maternal stores and carrier proteins, but large supplements can result in increased breastmilk concentrations, occasionally to potentially toxic levels [51]. Maternal zinc supplementation may slow the decline in breastmilk zinc concentration during lactation, although the magnitude of this effect and its significance for the breastfed child are still uncertain [41, 54]. Worldwide variations in breastmilk composition have suggested that poor maternal calcium intake may be a factor in determining breastmilk calcium concentration [55]. Mothers in the Gambia, for example, where the diet contains little calcium, have an average breastmilk calcium concentration more than 20% lower than that of British women [44, 56]. A recent supplementation study, however, which tripled the calcium intake of Gambian women for the first year of lactation, had no impact on breastmilk calcium concentration [56]. Intriguingly, a possible link with calcium intake during the preceding pregnancy emerged during this study, an observation that deserves further investigation [57].

Differences between mothers

Even when these various influences are taken into consideration, breastmilk composition varies considerably from one mother to another in the same population. Typically, major constituents such as fat, protein, and calcium can differ by two- to threefold between mothers at the same stage of lactation [44], and the concentrations and activities of some of the minor constituents can be highly variable [48]. At the same stage of lactation, breastmilk volume also varies between mothers [37]. In general, between-mother differences in composition and volume are maintained throughout lactation and are not necessarily related to each other [36, 37, 45, 48, 53, 58]. As a consequence, the intakes of breastmilk components are also highly variable, and some infants consistently receive substantially more or less from breastmilk than others of the same age. It is, therefore, important, when assessing the adequacy of breastfeeding for individual children, that measurements be made of both breastmilk intake and breastmilk composition.

Contribution of breastmilk to infant nutrition

Breastmilk makes substantial contributions to infant nutrition for many months after the introduction of other foods [40, 60]. Older, partially breastfed children obtain more than two-thirds of their vitamin A and fat from breastmilk [60]. The contribution of breastmilk to vitamin A nutrition may be the reason why prolonged breastfeeding protects against xerophthalmia and eye disorders in regions where vitamin A deficiency is common [60]. In addition, significant quantities of many of the non-nutritional factors continue to be ingested by the partially breastfed older child [60]. The many beneficial effects of prolonged breastfeeding on nutrition, health, birth spacing, and the family economy [61)] strongly suggest that breastfeeding for one to two or more years should be encouraged as part of a mixed diet.

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