MILK: THE BIOLOGY OF LACTATION

Maureen MinchinAllergies, Book Reviews, Bottle Feeding, breastmilk, Child Health, Commentary, Complementary Feeding, epigenetics, evolution, Growth, HIV, Immunology, Infant Formula, Infant Health, Lactation, Maternal Health, Microbiome, Milk Hypothesis, Pregnancy, Weaning

MILK: THE BIOLOGY OF LACTATION
by Michael L Power and Jay Schulkin (Johns Hopkins Press, 2016)

This relatively small book aims to inform, stimulate and even challenge thought about milk and lactation, its evolution, and its importance to modern life. It achieves those aims. The structure is clear, the authors adhere to it, and summarise succinctly at the end of each of its four sections and 13 chapters. (You can look inside and see the Table of Contents at Amazon
https://www.amazon.com.au/Milk-Lactation-Michael-L-Power/dp/1421420422/

I loved this book, learned a lot from it, and was at times vastly entertained in the process, though much of the detail will not remain in my memory banks. It is a brilliant book, and I’ve written to tell the authors so.

Yet I come from a different context, and so see some things differently, both what is there and how it may be read and misunderstood. And for the most part this review is for a different audience, those dealing clinically with lactation. Many may never read the book itself, so I will try to give an overview and address issues of possible clinical significance, as well as some relevant omissions. Be warned: this is a long read, but much shorter than the book!

CONTENTS OVERVIEW
What is in the book? The first part covers the evolution of milk from prehistory, in which it preceded placental mammals and live birth; the second, milk as a food: the lactation strategies of different mammals and their links to milk nutrient differences; the third part, milk as a developmental regulator and the concept of the developmental origins of health and disease, (DOHaD); the fourth section, the interaction between milk and human evolution, and a discussion of breastfeeding, history and health. A huge agenda, as each part could be a substantial book in itself.

The authors’ thesis is that “the evolution of lactation allowed maternal biochemical signalling to influence the growth and development of offspring across an extended period of time, a characteristic and unique feature of modern mammalian biology.” They explore what was known, by 2015, about how this is achieved, and so in general the book is an implicit argument for societal change that enables universal breastfeeding. However, the authors do make what I see as needless concessions to current societal reality- concessions which may reduce the impetus for change to that reality, more’s the pity.

The first section, The Birth of Milk, chapters 1-4, discusses a variety of animal modes of feeding their young, then explores the evolution of milk from a skin secretion keeping eggs moist to what we mammals now know it to be, via a fascinating discussion of the molecules of milk, and the evolution of two lactation hormones oxytocin and prolactin, developed from ancient molecules with different functions.

Chapter 3, the Molecules of Milk, looks at a few of the novel molecules, found only in mammals, that are central to lactation: the casein proteins, some of the whey proteins such as alpha lactalbumin, and the sugar lactose, which alpha lactalbumin helped create. The book records that under certain conditions alpha-lactalbumin can be transformed by stomach acid into HAMLET (human alpha-lactalbumin made lethal to tumour cells). Something the authors could not have known when the book went to press is that HAMLET has since been shown to cause bladder cancer cells to explode on contact, and be excreted, without harming other bladder cells. This is now being scaled up for clinical trials. http://hamletpharma.com/en/hamlet/research/  AND https://vimeo.com/281383705

Curdling by stomach acid is needed for milk digestion, and casein curds travel through the gut at a different rate from the proteins in liquid whey, which has implications for both breastmilk research and clinical practice. As they discuss here, and later in chapter 12, the action of the neonate’s digestive tract is needed to activate certain functions of peptides, the breakdown products of those milk proteins. To me, this immediately raises questions about the wisdom and effects of doctors prescribing powerful off label acid-suppressant or neutralising medications for young infants.

The second part, chapters 5 to 7, discusses milk as food. It “aims to give the reader a good understanding of the extent of variation in nutrient compositions of milk between different species, as well as within species, in terms of variation across lactation and between individuals, as well as the types of constraints on milk composition. Not all combinations of fat protein and sugar can be found in milk. Some are biochemically impossible (or at least extremely unlikely) others would not be able to support mammalian life and growth. Milk composition may vary widely but there are patterns and apparent constraints… Mother’s milk represents an evolved compromise between many selection pressures.” In my view, evolution has achieved a highly successful compromise whereby mother and child and community benefit: it is remarkable that to date no study has proved better outcomes from formula feeding than breastfeeding. Remarkable because it was not until the second half of the 20th century that breastfeeding became associated with advantage; in the first half it was disadvantaged women who breastfed. Of course the excess body mass sometimes generated by early formulas was once taken as proof of superiority, and grossly fat babies won prizes, but in fact that was the beginning of the WEIRD obesity epidemic.

One of the selection pressures is obviously maternal survival and health. Lactation is seen as a burden and decreased inter-birth intervals as a benefit for women. Throughout the book there is emphasis on the nutrient demands on mothers. But there is no mention of the highly evolved metabolic efficiency of lactation, which means that a mother absorbs for example, three times as much calcium from the same volume of food. Both pregnancy and lactation involve shifts in maternal metabolic efficiency that are protective of the mother living in food scarcity conditions for at least some seasons.

Elsewhere, the authors say “The evidence does not support a strong benefit for exclusive breastfeeding after six months of age and there are some risks; by one year of age supplemental foods are considered necessary for human babies. And subsequently there is a recommendation supposedly from modern medicine for exclusive breastfeeding through 4 to 6 months of age at which time cereals and other supplementary foods may be given.” In my opinion, “modern medicine” is still getting this wrong, thanks to strong lobbying from vested interests. In fact WHO recommends exclusive breastfeeding to around six months of age – which can mean slightly before or slightly after. Among breastfeeding groups, it’s not uncommon for exclusive breastfeeding to be the baby’s choice for up to 9 months or even longer with no detrimental effects. In lived reality, the introduction of other foods begins the process of weaning the child, and reduces the protection against pregnancy that lactational amenorrhoea offers the mother. The unnaturally early introduction of cereals is likely to be detrimental to both mother and child, especially in communities where high calorie foods are scarce and carbohydrate staples the norm. Ther’s much more about this on my website in a number of posts.

Chapter 5 is titled Not Quite Perfection. This is a clue to the authors’ perspective, as well as the likely contents of the later summary chapters about women’s milk. It would obviously be irrational to expect milk to have evolved to deal with problems created by conditions that had never before existed on the planet. If that is what is required for perfection, milk is necessarily imperfect, and will always be a work in progress, as is evolution. But I think vested interests will seize on the negative perspective and tone of that chapter title, and the discussion that follows. (It echoes the dominant American approach to breastmilk, which has to prove beyond doubt – impossible- its superiority and safety before any claims can be made, while formula, provided at taxpayer expense to half its American users, is simply assumed to be completely safe. If formula were to be invented now it is doubtful clinical trials would ever be permitted, given what is known about milk that goes beyond it nutrient composition.)
So what is considered by the authors as less than perfection in breastmilk? Two substances: iron and Vitamin D. Is human milk imperfect because “marginal or deficient” in either iron and vitamin D? Deficient by what standard and for whom? And is the less than perfect element the milk, or is it the child, or the environment?

IRON
Discussions of iron really should not focus on the highly bioavailable and protectively low iron content of breast milk, acknowledged in chapter 12 of this book. In the period during which babies are normally exclusively breastfed, till at least six months of age, there is no shortage of iron for the full term infant who has not lost blood. In fact one Swedish study showed that the majority of infants exclusively breastfed to 9 months were still iron-sufficient, although 36% showed some subclinical deficiency when their blood was examined (none were symptomatic). Failure to add appropriate complementary foods containing iron before 9 months is responsible for iron deficiency in full term infants. Or else occult blood loss, usually as a result of gut damage due to allergy. Once unknown in fully breastfed babies, food protein intolerant eosinophilic syndrome (FPIES) can produce such outcomes. (However, giving iron to prevent deficiency may well increase the risk of causing FPIES, as well as sepsis.)

It should be noted that in the first half of the 20th century, when doctors were more familiar with breastfeeding, the period 6-9 months was seen purely as a time of ‘educational diet”, allowing infants to explore tastes and textures, try a variety of foods, but with breastmilk as the main diet. Then between 9-12 months the infant was moved on to the family diet, and complete weaning (sevrage) was expected – unless poverty made continued breastfeeding an important part of infant diet. In the United States, where the canned babyfood industry had developed in 1920s, there was more emphasis on pureed mixes in handy lead-soldered, or later plastic-lined, cans and glass jars. There the introduction of other foods became ridiculously early, with some doctors boasting about infants being fed meat by a few weeks of age. By the 1970s, AAP and AMA journals included advertising by Gerber stating 3 months of age or 10 lbs in weight, whichever came first, as the age to introduce iron-fortified cereal. Not until 1980 did the AAP Committee on Nutrition advise 4 months as the minimum age for all infants. That soon became the global norm in the WEIRD world, and was associated with that world’s rapid increase in food allergy.

Breastmilk iron is appropriately low, and appropriately bioavailable for the period of exclusive breastfeeding. Levels drop in response to infectious challenges, so starving the pathogens, as the authors later note. And no discussion of infancy iron should fail to condemn the cultural practices of Immediate cord clamping and cord blood harvesting, which robs infants of the physiological iron stores that would prevent deficiency even to 9 months of age. My conclusion on the iron issue is that breastmilk is not imperfect or deficient, but that obstetric practices need to change.

The authors may not be aware that concerns about iron deficiency in infancy arose from the epidemics in formula fed infants up until the 1960s, due to the protracted difficulty of finding safe, shelf-stable, and bioavailable iron sources for infant formulas. And of course, industry defended its truly-deficient product, as it often does, by turning the tables on breastmilk via intensive and subtle advertising campaigns, with company representatives giving literature to thousands of health professional workers and sites. Concerns about formula iron became concerns about breastmilk iron, while companies marketed with impunity products whose iron content ranged from deficient (1mg/L) to excessive (12mg/L) levels. This complex topic is discussed in my book Milk matters: infant feeding and immune disorder, http://www.infantfeedingmatters.com/  at some length. As I reference there (p.377 ) “A 1983 study found that the actual range of iron in infant formulas then on sale was from zero to 57.5mg/L. The range of iron allowed in 2013 in first infant formulas was still 1-21mg/L in the USA, 2-8mg/L in Europe, 3-13mg/L in the UK.” I am unaware of any later independent assessment of the reality. Eminent nutritionist Professor Bo Lonnerdal thinks 2mg/L adequate, being a thousandfold the amount in breastmilk.

VITAMIN D
It’s similarly inappropriate to consider breastmilk imperfect because of the occurrence of vitamin D deficiency in older infants that are never sun-exposed or adequately fed by vitamin D replete mothers. Rickets will occur wherever mothers and children are not appropriately sun exposed. From the early 20th century onwards the importance of sun baths for infants was understood, and cod liver oil was used to provide vitamin D where this was impossible. Cultural habits and clothing need to be addressed, and breastmilk should not be considered “a poor source of vitamin D”. Indeed, the authors state that “a solely breastfed infant has enough stored vitamin D to avoid frank deficiency for months.” And complementary foods need to include sources of vitamin D after the normal period of exclusive breastfeeding. Babies are in fact born with enough vitamin D to last them several months, i.e. through the entire period of exclusive breastfeeding.

All of the above information about Vitamin D is contained in the discussion in chapter 5, but in the context of saying that breastmilk is “marginal if not deficient in iron and vitamin D.” No, it’s not. Our skin readily makes much more than we need, excess is toxic, and our body has ways of preventing it all being absorbed. Humans just need small amounts of sun exposure, at times when UV levels are not excessive.

So breastmilk is not generally deficient in iron or vitamin D, although once again, formula marketing in the 1970s and 1980s especially couched the discussion in those terms. Health professionals such as the authors fail to notice how they are always being nudged into framing breastmilk as deficient, as a problem. Cases where breastmilk might be truly deficient, thanks to cultural practices and/or maternal deficiencies, do not justify either wholesale interventions or criticism of breastmilk as imperfect. The US practice of universal Vitamin D supplementation is not replicated in Australia, and cases of rickets remain uncommon except where produced by cultural habits, largely among dark-skinned or covered women. While health professionals don’t have to claim or prove breastmilk to be nutritionally perfect – it is just the normal highly evolved incredibly bioactive infant human diet – we also MUST NOT undermine women’s confidence in their own milk, and support industry by suggesting or accepting that breastmilk is deficient.

So is it perfect? Breastmilk IS the most perfect of all diets for the period for which it evolved to be the sole diet, i.e. to around 6 months, when infant teeth start to appear and infants start reaching for other foods and can digest them. But breastmilk is not a perfect sole diet for infants past the age when they should naturally get some sunlight and start to move on to the whole family diet. However, it is a uniquely valuable personalised part of infancy and childhood diet for as long as it available. Which in human evolutionary history, and among advantaged Australian women is often for years, not months or days, just as it was for their ancestral foremothers. That needs saying clearly.

Yes, there are children with inherited metabolic problems for whom breastmilk is unsuited or even lethal. Galactosaemics. No question breastmilk is unsuitable for them, and a special diet is warranted. But not PKU sufferers. Researchers eventually found that the best outcomes came from a diet of breastmilk supplemented with enough phenylalanine-free food to keep blood phenylalanine levels low, so that children achieved unprecedented levels of cognitive function, not known when solely fed phenylalanine-free formulas. Breastmilk as a sole diet is not perfect for such a child, and our ability to keep such children alive is an advance – if the life they achieve is one worth living. But the imperfect child is the problem in these cases, not the breastmilk.

One last example that needs to be mentioned: HIV. The publication of this book predated the revised WHO guidelines on HIV and breastfeeding https://www.who.int/maternal_child_adolescent/documents/hiv-infant-feeding-2016/en/ The authors seem to assume that breastfeeding is contraindicated in cases of HIV infection. This is not so. In fact infant formula is contraindicated for the infants of HIV-positive mothers on antiretroviral therapy. More children died because breastfeeding was banned than would have died had it been encouraged, even before drugs were available. Many other species have developed the ability to deal with retroviruses, presumably through the existence of survivors who then gestate and feed the subsequent generation, passing on their immune repertoire. Being exposed and surviving is what we need as a species, and breastmilk makes that much more likely. The American attitude to milk with drugs or infectious agents has always been to presume that formula would be safer., because of their blind trust in formula. While of course there can be risks, a proper risk/benefit analysis almost always reveals that even in these cases breastfeeding is the safest option, while abrupt weaning or never breastfeeding increases risks.

GROWTH AND SELECTIVE PRESSURES
Of course I agree with the argument of chapter 5, that mammalian milk is the result of many, sometimes conflicting, selective pressures. But I don’t think that iron and vitamin D bolster that theoretical argument. Rather, for me, they strengthen a later statement in the book, that “the composition of a species milk may not have evolved to maximise growth of the offspring, but rather to support appropriate growth.” Growth not only of the infant, but of the microbiome which feeds and protects the infant, and which alters without the right amounts of both iron and vitamin D. Maximising bodily growth is almost certainly an inappropriate goal, yet it was the main measure used to assess the suitability of early infant formulas. Only now is research looking at more complex measures of biological growth, such as brain and reproductive and organ development, and finding significant deviations from the breastfed norm in infants not receiving breastmilk, or even not being breastfed. Less testicular tissue/more ovarian growth at 4months of age shown by utrasound, MRI-revealed differences in brain white matter development under twelve months, a thymus half the size, differences in all bodily organs measured to date, more chromosomal breaks and DNA damage, double the risk of SUDI/SIDS: these and more physical differences indicate that infant formula is indeed far from a perfect whole diet. That is the context within which infant diets need to be discussed. For any suggestion that breastmilk is less than perfect influences decisions in the WEIRD societies in which synthetic alternatives are assumed to be totally safe and equivalent, and in which women feel under-confident about the value of their own milk. (more on this later.)

NUTRIENTS OF MILK
Chapter 6, The Milk Spectrum, is fascinating reading. There is more in it about rhinoceros milk than human, but the discussions of milk fat sugar and protein are interesting and informative, and cover a wide range of mammals, from giant anteaters to pangolins.. fascinating. Chapter 7, Lactation Strategies highlights the interaction between our evolutionary origins, milk composition, patterns of feeding, length of lactation and development. For us primates, the strategy is frequent suckling, relatively dilute milk, and a long lactation period, and it is becoming clear that longer duration than is now usual is important for human babies. At the other extreme, an equally effective lactation strategy is the incredibly short 4 day lactation of the hooded seal. The impacts of nursing frequency, maternal fasting and food availability, and allo-nursing are all discussed, This second section concludes that “Milk serves multiple functions in regulating and supporting the growth and development of the neonate. Nutrition must be balanced by immune function and developmental signalling. What is best is a complex multidimensional problem that evolution may not be able to solve for the simple reason that there may be no single best.” On a species scale or on the individual scale, that remains true.

MORE THAN FOOD
The third section, More Than Food, chapters 8 to 11, covers some of the “the known nutritive molecules in milk that affect everything, from priming the neonatal immune system to gut development, to helping to establish the gut microbiota”. Milk protects, guides, and regulates (the chapter titles) and these three chapters are an excellent introductory summary of how that occurs. Any second edition will doubtless include more about milk’s pluripotent stem cells, given the post-publication proof that these do indeed reach bodily organs beyond the gut. The citation (p.88) of a mouse study where a single stem cell developed a complete functioning mammary gland indicates the potential importance of such stem cells for human infants.

There is a huge amount that is interesting and valuable in these three chapters. Important methodological concerns about research are raised too. I would hope to see a second edition of the book update this In the light of ongoing research, ideally from studies where the definitions of breastfeeding include reliable records of truly exclusive breastfeeding from birth, ascertained prospectively, rather than from retrospective maternal report, or replies to a simple yes/no choice of ever breastfed. And since each generation produces the next, how parents and grandparents were fed needs to be recorded. The long term and potential intergenerational significance of neonatal exposure to infant formula is only now being realised, although studies from many decades ago recorded its long-term impact on the gut microbiome.

MIND YOUR LANGUAGE!
However it’s within these chapters that some unconscious cultural bias begins to warp the strictly scientific discussion. To say that “feeding preterm infants human milk reduces the risk of developing NEC” reflects the truly WEIRD cultural unwillingness to state that exposure to infant formula in fact increases risk. Health authorities do not state that not smoking reduces the risk of cancer; they say that smoking increases the risk. Similarly, breastfeeding does not halve the risk of SIDS; formula doubles it. The co-evolved physiological norm for infant feeding is human milk; as the book outlines so clearly. Breastmilk’s absence increases risk. And so, separately, does formula’s presence. Powell and Schulkin hypothesise that NEC arises from the lack of ‘signal provided by the mother, first by amniotic fluid, and after birth by milk’ which results in pathologic development of gut cells. It is common in WEIRD nations for disease to be discussed in relation to the presence or absence of breast milk, with little or no reflection on the actual impact of the presence of infant formula (and until recently, antibiotics prescribed to reduce the risks of needlessly high surgical birth rates.) Yet Professor Paula Meier has documented the direct cytotoxic effects of formula on intestinal mucosa and human gut cells and the impact on gut barrier functions. That is harm from the presence of formula, not made possible by the simple absence of breastmilk: starvation is the outcome of breastmilk absence. The authors acknowledge that breastfed babies develop a different intestinal microbiota compared to formula-fed babies, along with lower inflammatory states related to different patterns of gene expression. But nowhere do they emphasise that not just the lack of breastmilk, but also neonatal exposure to ultra-processed foods, increases risk. Perhaps that seemed beyond the remit of the book, but people other than scientists will be reading this book and need to make that connection. The e-Learning for Health https://www.e-lfh.org.uk Infant Formula education module approved for all UK NHS workers by the Royal College of Paediatrics and Child Health says “”The only accepted alternative to breast milk for infants up to 6 months of age is infant formula [1] which supports bodily growth along parameters different from those of the breast-fed child, and provides no immunity against disease. Many of the health outcomes of breastfeeding compared to formula feeding are dose-related: that is, better outcomes are associated with longer duration and exclusive breastfeeding, or less exposure to infant formula. For infants, formula will always be an inferior choice to breast milk.”

For some that last sentence will be shocking. Language is important. Language can create awareness or minimize it. Minimising language is often ‘justified’ by a desire not to upset existing formula users. (Or not to suffer the consequences of sometimes rabid trolling.) Or not to create pressure for radical societal change to enable breastfeeding. I will never forget the senior FDA scientist who, when excusing suppression of certain recalls in a plagiarised paper, justified it by saying, “You have to understand. We (FDA) need to reassure parents that formula is safe, because American society depends on bottle feeding.” Indeed it does. But WEIRD societies needn’t, and wouldn’t, if scientists told all the truth in ways people could hear.

PRESENT AND INTERGENERATIONAL EFFECTS ON WOMEN
And breastfeeding mothers suffer as a result that widespread, unscientific cultural instinct to protect the feelings (not the health) of current and past infant formula users even at the expense of future babies and families. The authors seem unaware that mothers will be powerfully affected by any hypothesis that it is their bodies’ failure to provide a necessary signal that has caused a devastating disease like NEC.

WEIGHTY PROBLEMS                                                                                     Further, the authors emphasise that ‘obesity in adults is associated with an altered gut microbial population’, that obese women produce milk that creates an aberrant biome associated with increased disease risk in infants.’ Yet they do not raise the possibility that this parental obesity is an intergenerational legacy of the almost universal exposure to infant formula in WEIRD hospitals from the 1960s onwards. (Formula which we have known for over a century produces “aberrant biomes” without telling parents that fact.) Maternal obesity in pregnancy may be the consequence of that mother’s in-infancy exposure to, or feeding with, the high-protein formulas common until very recently, and still used in many places. (Paternal obesity or allergy may also affect infants via miRNAs in sperm.)

Mothers made aware of the intergenerational and biparental impact of formula exposure shed debilitating feelings of guilt, and place responsibility where it truly lies, in hospital practices undermining breastfeeding – practices that obstetricians and paediatricians formulated and allowed to become universal.

The authors rightly state that obese mothers may pass on an obesogenic microbiome via breastfeeding, but seem unaware of the harm this can cause in societies where it is (wrongly) assumed that infant formula is tightly regulated, totally safe, and non-obesogenic. Many mothers lack confidence in their own milk, being aware of their less than perfect lives and diets. Some breastmilk may indeed be more obesogenic than other breastmilk. But none of it will be as damaging as infant formula, so that any suggestion of a mother’s own milk being possibly less than ideal needs to be accompanied by simultaneous reassurance that it is still far superior to the best infant formula. (Saying that “mother’s milk is more likely to produce a healthy outcome” could be considered damning with faint praise, not strong reassurance.)

Given that the authors are both deeply involved with the American College of Obstetrics and Gynecology, this was a missed opportunity to influence clinical practice and parental education and so reduce risk. The altered microbiomes readily attributed to surgical births per se may be largely a consequence of the greater likelihood of formula feeding after surgical birth. If rates of needless surgery cannot be reduced, it justifies strenuous ACOG efforts to ensure not only an end to instant cord clamping, but truly exclusive breastmilk feeding from birth, preferably maternal breastfeeding, and promote it for considerably longer than three months. In some countries obstetricians have not been prominent in programmes to improve hospital practice.

As an aside, I want to note that the increasing focus on maternal BMI in pregnancy is already having some adverse clinical consequences perhaps not apparent to academic researchers. Weight gain in pregnancy is indeed another obesogenic factor, and mothers are being strongly encouraged not to exceed limits set by medical authorities. Where this is not easy or feasible (perhaps due to the mother’s metabolic programming from infancy, rather than any failure of will or effort on her part) mothers feel bullied and become stressed. Stress itself has serious adverse impacts on normal infant development, so urging women to lose weight or not gain it in pregnancy, when this may be quite impossible, is perhaps another example of what the authors neatly describe as “well-intentioned but biologically unsound” clinical practice. There’s a lot of that about in infant feeding.

DOHaD
Chapter 11, the last chapter of Section 3, is an elegant outline of DOHaD and the regulatory influence on infant development of maternal signalling through gestation and lactation. This is not discussed intergenerationally, although the infant was once an egg inside his mother when she was being gestated inside her mother, and working with allergy families makes it clear that there are intergenerational epigenetic influences on current infants. The authors describes the interactions as “Mothers and babies are ‘speaking’ to each other at a fundamental biological level from the moment of implantation”, and there is continuity between pre and post birth signalling from, for example, growth factors in both amniotic fluid and milk..

They go on to say “These signals have evolved to assist the infant’s adaptation to the postbirth environment. But nowadays, signals coming to many modern infants from their mothers may be well outside of the normative ranges under which our species evolved. The infant’s metabolism and physiology will still adjust in response to those signals, but the adjustments may no longer represent an adaptive response; or at least may not result in long-term good health. The mammalian adaptation of extensive and long-term maternal influence on development that we hypothesise began with the evolution of lactation may underlie many modern human metabolic diseases. The modern human pathologies associated with DOHaD may represent the failure of an adaptive response due to an inappropriate environment.’

Such free-ranginging speculation is justified, but an appropriate diet is a critical part of any potential adaptation to post-birth life: why focus on “signals coming to many modern infants from their mothers” when those signals are being overridden by direct exposure to alien substances that never existed in evolution, like infant formulas and of course antibiotics? These certainly are way outside the normative ranges of what infant physiology has evolved to cope with. Even if the book is about milk, the possible threats need to be put into context.

OUR MOTHERS’ MILK
Part 4, Chapters 11 and 12, is titled Our Mother’s Milk and consists of two chapters, Milk and Human Evolution, and Breastfeeding, History and Health. The introduction to this section again hints at what I see (rightly or wrongly!) as some culturally-driven concern to reassure about infant formula. This is despite the authors’ cataloguing the enormous importance of breastfeeding and breastmilk to child development. And despite some strong later statements affirming the importance of breastmilk to humans. ‘No formula can match what evolution has produced. But that does not mean that breast milk is always best; there are circumstances where breastfeeding may be contraindicated.” True, but biological reasons remain rare exceptions that would not sustain a $50billion industry!

The authors also say, “The evidence that mother’s silk delivers tangible benefits is strong, but mother’s milk is not necessary, and a child is not doomed if his mother cannot or chooses not to breastfeed.” Well, of course not. Formula is not poison, just an ultra-prcessed dehydrated mixture of foods. But the fact that the child is “not doomed” is not usually seen as a valid justification of any decision to use home-made rather than proprietary brand of infant formula! Of course breastmilk is not (always) necessary if simple survival is the only criterion. Humans are omnivores; feeding the child pretty much anything will see some survive, as the old pap mixtures and an Icelandic diet of raw fish and cream proved.

  1. But contrast that attitude with that of researchers looking at infant immune development: “Breast milk stimulates the proliferation of a well balanced and diverse microbiota which initially influences a switch from an intrauterine Th2 predominant to aTh1/Th2 balanced response and with activation of T-regulatory cells by breast milk-stimulated specific organisms … The breast milk influence on initial intestinal microbiota also prevents expression of immune-mediated diseases (asthma, IBD, type 1 diabetes) later in life through a balanced initial immune response, underscoring the necessity of breast feeding as the first source of nutrition.” Necessity, no less, for normal immune development.    https://www.nature.com/articles/pr2014160

I absolutely agree with the  authors that “recommendations to women regarding breastfeeding need to be firmly grounded in evidence.” Recommendations about infant feeding in general need to be, and those about formula feeding are generally not. I know of few by-brand and by-product comparison studies despite the differences between brands. I could not find even outcome studies between infants fed evaporated milk mixtures, home-made formulas, and those fed formulas, all current options that don’t kill all exposed children. It is just assumed that any industrial formula meeting a wide-ranging standard produces good outcomes, equal to breastfeeding on any important level. And meanwhile, epidemics of colic and reflux and FPIES and gut distress and allergy expand in both the formula fed and the breastfed exposed to bovine prodcuts via gestation or hospital formula. Is that not evidence that we are getting some things very wrong? That species-specific milk just might be necessary to health, even if most children can survive such horrors? Families often don’t survive them: marital breakup is very common when both parents are stressed by infant health issues. And they increase the risk of physical and psychological abuse of children.

SPECULATING ABOUT EVOLUTION, BRAINS AND MILKS
Chapter 12 “attempts to recreate the evolutionary history of human milk: how it has changed from the milk of the common ancestor of great apes and humans over the last 4 to 6 million years to become the modern human milk of today.’ There is an interesting discussion as to whether and how human milk evolved to include higher fat levels than other primates in order to support the growth of the larger human brain. To do so, human diet had to change to higher quality foods providing more energy and possibly more nutrients per gram. As they say, “The large relative size of the human brain means that there is proportionately greater requirement for lipids to grow the brain. Although myelination of neurons begins in the 14th week of gestation most myelination occurs after birth, fuelled by milk.”

That fact makes me wonder why there is so little well-researched information about the brain development of infants. There was a period in WEIRD nations, from about 1960/70 to the end of the century, even 2010, when the majority of infants and their mothers had too little of necessary brain fats. DHA and ARA are always present in breastmilk because endogenously synthesized, but levels are affected by maternal diet. Formula fed infants were less fortunate. Cod liver oil was no longer given once 1960s formulas claimed to be a complete food, but the formula fat blends often lacked DHA and ARA right up until the 1990s, when fungi and algae were genetically modified by Martek to produce synthetic analogues of these fats. (Using eggs and peanut oil in some formulas was not a success, but the outcomes are not on the public record.) Although the authors wonder “if dietary DHA is a limitation on human brain development under natural conditions”, they do not allude to this key deficiency of American infant diet in the 20th century, the century in which America first identified autism and watched it become an epidemic. We now know from MRI studies that brain white matter development in not-breastfed infants is significantly different. And that the fat blends have an effect. And that children with autism have altered brain white matter. Which may all be coincidence. Or not. We’ll never know, if we don’t look carefully for fear of upsetting a minority of vocal advantaged parents. Science takes courage.

Drinking the milk of other animals: pregnancy and lactation
Unusually, and perhaps bravely, the book raises questions about the effects of human consumption of the milk of other mammals. That inappropriate environment discussed earlier in relation to obese women may include not only changed maternal characteristics, BMI and diet, but also maternal and fetal exposure to bovine milk in both pregnancy and lactation, and through three or more generations. It seems unlikely to be coincidence that the world’s tallest people are the Dutch, who for centuries have been the largest per capita consumers of bovine milk products.

And it’s not surprising (to me, anyway!) that cows milk allergy is the most common allergen in communities where pregnant and lactating women have been urged to drink excessive amounts of cows’ milk, and/or infants have been predominantly formula fed through generations: by 1970 as few as 20% of infants were ever-breastfed in some western nations, and mostly for very short durations. 1970s mothers were themselves drinking a litre of bovine milk daily. And by the 1970s the allergy epidemic had arrived in WEIRD nations: all had parent-led groups trying (often vainly) to convince the medical profession that their children were allergic, in the original sense of that word.

Despite the risks, every major formula company seems now to have launched a campaign to persuade pregnant women to drink their expensive milk products, many containing probiotics. This pre-birth colonisation of mothers will influence the breastfed infant microbiome, making it more like the microbiome of babies fed formula with the same probiotics, and so justifying claims that formula is closer to breastmilk – because breastmilk is closer to formula, in fact. This is particularly concerning in the booming formula markets of Asia, where milk is not a traditional food and tolerance will be an issue. Some women have found that pregnancy hyperemesis disappears when they stiop consuming bovine products, the very foods they are urged to consume in excess during pregnancy.

Not surprisingly, the authors do not discuss those issues, but do say that
“..milk for many species evolved to support growth and development of the neonates of that species. Milk evolved as a signalling mechanism as well as a nutrient delivery device. Consumption of milk and milk products from other species may expose us to signals designed to influence growth and development that are different from our evolved adaptive maternal milk signals. This is an area of current research. At present the data are sparse and the evidence indirect. But it is worth some speculation as to the extent that the signalling ability of milk might affect our physiology and metabolism when we consume another species milk. Milk may be a food that comes closest in truth to the old saying you are what you eat.…

Pasteurisation and homogenisation of milk deactivates some, but not all, of the bioactive molecules. The actual evidence for effects of signalling molecules in store-bought milk affecting the physiology of the humans who consume it is still sparse, but not to be discounted…

Micro RNAs from cow milk can be absorbed into circulation after people consume a glass of milk, and can be taken up by cells and affect gene expression. These findings are fascinating indications that milk has the potential to exert regulatory effect even on adults. The study was small and needs replicating… The use of other species milk may still be influencing our growth patterns from in utero through childhood, and may affect our vulnerability, both positively and negatively, to certain diseases.”

This needs urgent study, given the past and present WEIRD heavy emphasis on cows milk consumption during human pregnancy, and its known associations (with greater maternal weight gain, higher infant birthweight with an increase in fetal growth in the third trimester, and increased placental weight) along with the potential for anti-antibody formation by the mother increasing the child’s allergy risk or severity.

CONFLICTING MESSAGES?
The final chapter, Breastfeeding History and Health, is confusing. On the basis of the evidence previously cited, the authors strongly advocate breastfeeding as a public health measure, and express awareness of its value, and its impacts on lifelong health. A couple of forthright excerpts illustrate this.

“When a mother breastfeeds her baby she is engaging in one of the most intimate interactions with another person. She is feeding her baby with the product of her own body, but she is doing more than giving her child nutrition. She is transferring a wealth of bioactive molecules that will influence her baby’s immune system, developmental patterns, and eventual adult physiology. It has only been in the last few hundred years that a brief interlude of human arrogance questioned the primary importance of breast milk and suggested that humans could devise something better that unfortunate episode of history can be encapsulated by two famous lines from Alexander Pope’s 1709 an essay on criticism “a little learning is a dangerous thing” and fools rush in where angels fear to tread.”

“The biochemical complexity of milk with its numerous and as yet not completely characterised suite of bioactive molecules that could have developmental effects on babies, strongly suggests that there will be no complete substitutes for human milk any time soon. Technology continues to advance, but millions of years of evolution have given human breast milk a substantial advantage over any formula human beings might devise as a substitute. The hubris of early 20th century scientists who believed they could do better than evolution has been shown to be nothing more than hubris.”

Pretty strong stuff for American writers. And absolutely truthful. But then, the authors go on to say “human and technological progress has reduced the importance of breast milk for modern babies. Women have more choices now for how to feed their babies – exclusive breastfeeding, breastmilk by both breast and bottle, mixture of breastfeeding, formula and other supplemental foods, or no breast milk at all. All these options can be successfully employed.”

“Successfully employed” if you are using the basic 1800s criteria of staying alive, growing, and falling within the wide range of human competence? Yes, for most people, not for some. And almost all of those are living in that tiny part of the world where parents have reliable access to clean water, and power and can afford all the equipment and product needed, or have it supplied by the taxpayer (as in the United States).

But “successfully employed” if you are trying for optimal child development and health, and reduced public health costs? No. Clearly not. They’ve made clear why.

Yet the authors say elsewhere that “breastfeeding is not required. Formula-fed babies will grow up to be competent fully functional adults.” Of course that’s true for most, and it’s likely the authors themselves, their wives or their families, fall into that category. (Which is why I believe those writing or speaking in this field should declare their own history, as emotional influences and conflicts of interest are just as powerful as financial ones.)

But equally of course, some babies will not grow up at all; in every country some people die as a direct result both of not being breastfed, and of being formula fed. Not only the infants who die of NEC, or the children who die of anaphylaxis to cows milk protein, or those women who will die early of reproductive cancers who would not have done so had they breastfed their children. And who knows what levels of functioning and competence are being curtailed, for any individual, in any society? Survival proves little, but is a tribute to mammalian omnivore flexibility. Comparative mortality rates are only one marker of harm. Damaged survivors may damage future children an grandchildren.

As the authors say, “Have we managed to produce a satisfactory milk replacer formula? Based on the criteria of the 1800s the answer would be yes. Deaths among formula-fed babies are low. Formula-fed babies are likely to grow up to live normal healthy lives.” No one would dispute that.

But they go on to say, “Our expectations have also increased however. Breastfed babies still appear to have measurable advantages. Modern milk replacer formulas still lack important bioactive ingredients and cannot match the biological effects of breastmilk.”

To me, there’s a “have one’s cake and eat it too” feel about this last chapter and indeed the whole book. There’s a clear desire to catalogue the science that says those not breastfed or breastfeeding will deviate from human physiological norms, that milk is important. But there’s also a strong desire not to upset anyone, to reassure that this doesn’t matter that much, most formula fed humans are not badly affected. Given the levels of inflammatory disease in WEIRD communities, and their rapid emergence in every country where formula use increases, the latter position seems to me hard to maintain. But if you don’t look, you won’t see. And until recently, virtually all the money for research was industry money. And used feeding definions that inevitably minimised outcome differences. And followed industry marketing in talk of respecting women’s choices.

CHOICE?
However, talk of choice in infant feeding utterly enrages those of us who work with women, and know how constrained any choice is. Choice is non-existent for most, especially where governments actively subsidise the supply of formula to half the population, and pay for childcare by strangers, but never financially reward breastfeeding women or protect their ability to re-enter the workforce only when they feel ready to do so, meaning that those families bear the cost of optimal care for their children in decreased superannuation and longterm financial security.

Only a tiny minority of advantaged women can make any choice about feeding mode. And then it is an uninformed choice, as knowledge of infant formula and artificial feeding realities are buried under a mountain of poorly regulated marketing and horror stories about breastfeeding, in a society where for a mother to want to be with her baby is considered retrograde and punished.

CONCLUSIONS: THE PERFECT FORMULA IS??
Ever since industry began making formulas a century ago, it has made the claim that formula nowadays is just perfect, a complete food, that meets all nutritional needs, so close to breastmilk as to make no important difference. As these eminent scientists make clear, that’s simply untrue. Milk protects, guides, regulates.

When gene expression is clearly affected by nutrition and the microbiome it creates, all babies not breastfed will have, must have, deviated to a greater or lesser degree from what would have been their genomic physiological developmental trajectories. That is making a big difference. Such deviation is unlikely to be a benefit, and is probably a harm. Though of course the degree of harm will follow a bell curve outline, and may be unnoticeable, both because the harm has become usual, and because some genomes are more robust than others. Usual harms are seen as normal wherever formula has become the norm. Western concepts of the normal infant are not universal truths, for instance: prolonged excessive crying would not have helped the survival of early humans, and is rare, and considered a sign of poor parenting in traditional breastfeeding communities.

Knowledge of infant formula, its history and current reality, is the missing piece in most discussions of women’s milk and breastfeeding. Believe the propaganda, trust the regulatory authories who depend for their information on industry, assume it to be safe because it does not result in visually obvious harms – and you will write differently about breastmilk than if you think about what it means to lack that highly evolved bridge between the womb and the world. Why do we worry about the few IQ points lost to low-level lead exposure, but not those same few points (or in the case of preterms, up to 12 IQ points) when it is the absence of breastfeeding and the presence of formula which causes the cognitive loss?

Why is this public health issue constantly ignored, and effective societal education campaigns suppressed? $2billion total world formula sales in 1980; sales are projected to reach $70billion in the next few years, and more is spent on marketing than research. Everyone who uncritically accepts industry propaganda is responsible. The small advantaged army of breastfeeding deniers and formula apologists is very vocal and intimidating, and dominates media reporting. Industry has made itself almost indispensable to health professionals and their associations. Curing the blind spot all this has created will be slow and painful.

So it’s maybe not surprising that eminent as they are, and excellent as their book is, the authors have fallen into the trap of not being scientific and critical enough when it comes to the dominant mode and accepted practices of infant feeding in North America. And I believe that this has influenced what these men say about lactation, breastfeeding, and breast milk. I hope they will forgive my temerity in crticising such an original and interesting book. I do so because I value it highly and hope to influence the  second edition that the book deserves to run to! For, as all Cow and Gate formula tins used to say truly, “What we feed them now matters forever.”

Maureen Minchin
www.infantfeedingmatters.com

Read the book and judge for yourself. It’s well worth the time and effort, even if it costs as much as my Milk Matters: Infant Feeding and Immune Disorder and is less than a third of the size! (And my book is the cure for formula blindness, and should also be read.)
Find their book on Amazon at https://www.amazon.com.au/Milk-Lactation-Michael-L-Power/dp/1421420422/