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HM composition has generally been regarded as a gold standard for deriving infant nutritional requirements – for instance in situations where artificial feeding is required. This has certainly been a most helpful concept.

However, for breast milk to be a valid gold standard, it is critical that accurate data are obtained using appropriate methodology. This latter aspect is the one that is discussed in this section since it will be argued that despite intensive work on the composition of breast milk, misleading data have been derived in the past that have misdirected nutrition practice in ways that have had adverse impact on babies and their long-term health.

In 1953, Hoobler et al. [7] were able to summarize no less than 1,500 scientific publications on the composition of HM. In 1977, the UK Department of Health added further to this list: an official publication on the nutrient content of breast milk obtained by complete expression of one breast in mothers from 4 UK cities [8]. These data were proposed to provide a basis for infant nutritional needs and a model for the design of infant formulas. It was at this stage that this and past studies on breast milk composition were challenged as methodologically flawed [9].

One major difficulty in the study of breast milk content is obtaining representative samples of breast milk for analysis. Breast milk fat, and hence energy content, varies greatly during a feed, between breasts, and throughout lactation. Our own data show that during the course of a breastfeed, breast milk fat content doubles, and milk flow, statistically at least, decreases in a curvilinear manner [10]. We suggested that obtaining representative values for milk fat might be best derived by studying milk composition and milk flow during the feeding process, yet this had never been done. In the absence of such knowledge, we hypothesized that milk obtained for analysis in the traditional manner by unphysiological manual or mechanical expression of the breast – so-called expressed breast milk (EBM) – might differ greatly in its fat and energy content compared to the milk obtained by the baby during physiological breastfeeding – termed by Lucas “suckled breast milk” (SBM) [11]. This difference could occur, for instance, if expression of the breast removed more high-fat hind milk than would be obtained by the baby if the breast was not fully emptied during feeding.

In order to study SBM, a milk sampling system was devised by modifying a clinical nipple shield worn on the breast during breastfeeding. The modified nipple shield contained a milk sampling line so that milk could be sampled continuously during a breastfeed, and it also contained a flowmeter in the tip. Initial research using the nipple shield sampling system showed that SBM fat content was around 2.5 g/100 mL versus a figure of around 4.0 g/100 mL obtained in a vast number of prior studies on EBM composition [8, 11]. Thus, if valid, our data suggested that using EBM, it was possible to overestimate milk fat content by 60% compared to SBM obtained during normal feeding. We estimated the energy content of SBM to be 58 kcal/100 mL compared to around 71 kcal/100 mL based on over 1,500 prior publications. This would equate to a methodological error in measuring milk energy content of over 20% when studying EBM versus SBM.

When these data on SBM were published, they were too radically different to those published previously using EBM to be widely accepted. So, to confirm our findings on the energy content of breast milk, we used the doubly labeled water method in a novel way. In this method, 2 naturally occurring stable isotopes: deuterium (heavy hydrogen, ²H) and heavy oxygen (¹⁸O) are given orally producing enrichment of these isotopes in body fluids. Decline in these isotope enrichments back towards baseline is measured in urine or saliva over several days. The slope of the decline in ²H can be used to measure water output (since hydrogen is lost as water), which in steady state reflects water intake, and, from this, milk volume intake can be derived. The decline in ¹⁸O is faster since oxygen can be lost in both water and carbon dioxide. Hence, the difference in the decline in ²H and ¹⁸O is the CO₂ production rate, from which energy expenditure can be derived – and hence metabolizable energy intake. Thus, over several representative days, milk volume intake and energy intake can be estimated, and, by dividing the latter by the former, the energy content of breast milk is derived without any recourse to breast milk sampling. This approach produced values for energy content of breast milk according to postnatal age of 57–61 kcal/100 mL, thus confirming our previous values using the nipple shield system [12]. Later work has confirmed our finding that breast milk energy content had been greatly overestimated in past EBM studies.

One importance of these findings is that formula manufacturers based their products, and still do, on the composition of EBM, which emerges as the wrong model.

In addition to errors in prior estimation of breast milk fat and energy, breast milk protein content was also overestimated by using analytic methodology developed by the dairy industry. In cow’s milk (CM), there is little nitrogen that is not part of protein so that it is possible to estimate protein content by multiplying nitrogen content by a constant (6.38) [13]. This was used inappropriately for human breast milk in which there is a high content of nonprotein nitrogen (e.g., urea), which should not be counted as protein. Thus, more recent work shows that the true protein content of breast milk is significantly lower than previously thought [14], and this is one reason why infant formulas have substantially higher protein content than breast milk.

Thus, as a result of flawed methodology for breast milk compositional analysis, a generation of babies were fed on formulas modeled on EBM composition unphysiologically high in fat, energy, and protein. This constituted in an inadvertent experiment in early overfeeding, and animal studies since the 1960s show early overfeeding increases later cardiovascular risk factors [15].

The higher nutrient intake of the formula-fed infants is believed to be a major factor in the faster early growth of formula- rather than breastfed infants. So, does it matter that formula-fed babies grow faster? In 2004, based on our nutritional intervention trials and animal evidence, we published our postnatal growth acceleration hypothesis, which proposes that faster early growth increases the risk for later obesity and CVD [15]. In that publication, the known increased risk of obesity and cardiovascular risk markers with formula feeding was proposed to relate to the faster growth rate. Since then, over 60 studies, including randomized trials, have supported the postnatal growth acceleration hypothesis.

Thus, flaws in research on breast milk composition were indirectly partly responsible for the major modern epidemic of CVD and obesity – a salutary example of the importance of methodology in science. The field has now become a priority for research on both breastfeeding and formula feeding.