- Allomaternal nursing is widespread across mammals and human cultures.
- The practice of wet-nursing was associated with infant mortality and economic exploitation.
- Natural selection may have favored allomaternal nursing.
- High demand for “grey” market milk is not without costs and concerns.
Allomaternal nursing, the practice of infants suckling from a female not their mother, takes many forms. This behavior is not unique to humans and is widespread among mammalian species. Allomaternal nursing is thought to increase the fitness of females and infants, which would be favored by natural selection, but little research effort is directed to the topic. More recently, modern technologies of plastic containers, cold storage, and rapid shipping have created opportunities for milk sharing and milk selling widely among women. Some researchers and clinicians consider this unregulated trade of human milk a cause for concern–especially the risk of disease and toxin transmission to developing babies. Before that, though, let’s consider allomaternal nursing through historical, cultural, and evolutionary perspectives.
Wet-nursing was a prevalent practice before the advent of commercial formula. Throughout the Renaissance and into the early 20th century, poor women were hired to nurse the infants of wealthy women. Physiologically, the period of lactation, especially early and peak lactation, requires the mobilization of maternal body fat and skeletal minerals. When mothers are losing weight, ovarian function is suppressed and women do not experience a menstrual cycle (Valeggia & Ellison, 2009). Once mothers recover from this “depletion” of their bodily stores, they can conceive. In this way, interbirth intervals are often correlated with the duration of exclusive breastfeeding. By hiring wet nurses, wealthy women could shorten interbirth intervals and produce large families by forgoing the biological costs of lactation. The employment of wet nurses may have also been desirable because it allowed mothers to sleep through the night or/and attend long-lasting social functions in which infants were not welcome. In contrast, the poor women hired as wet nurses would often neglect their own infants and bias nursing behavior toward “paying customers.” The mortality rate for the biological infants of wet nurses was estimated to be quite high (Hrdy, 1992). Disentangling infant mortality due to wet-nursing from the immuno-socio-politico-economic context in which it occurred is tricky, especially when relying on historical records. Take home message: wet-nursing was contingent on wealth disparity and generally had the potential to have high costs for the wet nurses.
The practice of allomaternal nursing goes far beyond wet-nursing and is much more widespread among human populations than generally acknowledged. Within Islamic culture, there is the practice of “milk kinship.” This is a familial relationship, analogous in many ways to “godparents” among Catholics. In such instances, infants are nursed by a woman not their mother and consider her biological children “milk brothers” and “milk sisters.” In this way, lifelong social bonds are established and maintained throughout childhood, adolescence, and adulthood. And these relationships are in place in the event of the death of the biological parents (Parkes, 2005). Additionally, allomaternal lactation has been reported to be routine among many peoples including the Efe, Beng, and Aka in equatorial Africa, the Ongee of the Andaman Islands, and the Trobriand Islanders (Hrdy, 2009). Cross-nursing, when two women reciprocally nurse each other’s infants, is much less studied, but is known to occur among mothers in modern Western societies (Shaw, 2007).
Allomaternal nursing among mammals
Allomaternal nursing is not just a cultural invention of humans but has been observed in many other mammals, over 70 species at last count. Roulin (2002) reviewed the prevalence of the behavior, although our knowledge could do with some updating from new research in the last decade. Identifying the benefits of allomaternal nursing is crucial because synthesizing milk is costly. Why would natural selection favor mothers who nourished young not their own?
Some species are characterized by cooperative breeding in which related or unrelated adults contribute to rearing infants of a dominant breeding pair. Contributions can include provisioning breeding females (and pups as they are weaned), babysitting, territorial defense, and in some species, females will nurse the dominant female’s infants. Among meerkats, pups will suckle from allo-lactators who have lost their litter, have spontaneously started lactating, or are also attempting to rear their own litters (Scantlebury et al., 2002). The benefit to the pup is clear but for the allo-lactators is less so. The pups may be related to the allo-lactator and care toward them can evolve via kin selection. Similarly, living in a group has benefits–territorial defense from other groups and more eyes to spot predators–and allolactation may be a tactic for being allowed to stay in the group. Among some house mice, two females will share a nest and take turns between going on foraging expeditions and staying behind to protect and nurse all the pups at the nest. The females nurse their pups and the other pups equivalently. About half the time the two females are sisters, but these reciprocal arrangements are just as often between unrelated females. Moreover, the arrangement can be stable across multiple birthing seasons (Weidt et al., 2008). Allonursing has also been documented in capuchin and squirrel monkeys (Baldovino and Bitetti, 2007; Perry, 1996; Williams et al., 1994). These species are not officially considered cooperative breeders but habitually allow infants not their own to suckle. A single report from squirrel monkeys indicates that allo-lactators produce lower fat concentrations in milk than do biological mothers (Milligan et al., 2008). In that study, the allo-lactators’ infants had died; it’s unclear if low-quality milk may have contributed to infant mortality or if the reduction in milk demand changed milk synthesis.
Mother’s milk is not only nutritive but is an integral component to defending the infant against pathogens and entraining the infant’s developing immune system. Milk includes maternal antibodies, hormones, commensal bacteria, and special sugars for beneficial bacteria to consume. Infants who suckle from multiple females may be boosting their immune system from the diverse exposures they get from allomaternal milk. Cross-nursing among mothers allows for all infants to benefit without increasing the net costs of milk synthesis to the individual mothers.
Milk-sharing in WEIRD people: Dangers & demand
(Westernized, Educated, Industrialized, Rich, Democratic Nations (Henrich et al., 2010))
Many of the beneficial constituents in breast milk are not available in commercial formulas. As a result, there is increasing demand for donor milk in neonatal intensive care units and among mothers seeking alternatives to formula. A recent meta-analysis of randomized, controlled trials revealed that premature babies that consumed commercial formula were four times more likely to develop the dangerous infection necrotizing entercolitis than were premature infants that consumed donor milk (Ben et al., 2012). A number of nonprofit and commercial entities have developed milk banks that rely on donated milk from women screened for health and lifestyle. After donation, milk undergoes processing to make it safer (e.g., pasteurization). These processes, while important for protecting the recipient, can also neutralize some of the beneficial bioactive constituents in milk. Moreover, the overhead costs and clinical applications of these milk banks limit the general public’s access to donated human breast milk.
Those in the general public clamoring for raw, unpasteurized human breast milk have turned to a vast online “grey” market for sharing and purchasing milk among strangers (Geraghty et al., 2011; Gribble, 2013). This generates a number of concerns for the health of the recipient and also the donor and the donor’s infant. Milk can include viruses, pathogenic bacteria, drugs, and poisonous toxins. HIV, E. coli, and methamphetamine can also be present in expressed breast milk; although rare, the probability is above zero. And lots of potentially dangerous things in milk aren’t quite so rare–such as BPA, cytomegalovirus, and over-the-counter drugs. Moreover, contamination can result from poor collection, storage, and transport methods. These concerns led the Food and Drug Administration to release a statement of the risks and state in 2010 that the “FDA recommends against feeding your baby breast milk acquired directly from individuals or through the Internet” (Use of Donor Human Milk, 2010). A recent survey of 41 recipients and 97 donors by Gribble (2013) revealed that although 85% of recipients of shared milk were aware that milk posed the risk of infectious disease, less than half of respondents were aware of drug or other kinds of contamination. In contrast, recipients named a number of their concerns with commercial infant formula that compelled their interest in purchasing human milk. Less than half of recipients had discussed milk-sharing with their health care provider. Although nearly all “donors” washed their milk pump before and after pumping, other tactics to prevent contamination were often overlooked, such as washing hands, nipples, freezing milk after expression, recording date of expressed milk on container, etc. (Gribble, 2013). Less than a third of milk donors had discussed milk donation with any clinician.
Problematically, the value of human breast milk when sold online is contingent on volume, not composition. This leads to a number of concerns. Additional income may induce women to upregulate milk synthesis through pumping, potentially compromising their own health and the composition of milk available for their own baby, as happened historically with wet nurses. The composition–or quality–of the milk can’t be evaluated by the recipient. The complex biochemistry involved in measuring the concentration of constituents–including contaminants–is restricted to a handful of highly specialized laboratories. I expect that most people are providing healthy, safe milk via the internet. But when profit is involved, some people may exploit the system. Just as the unscrupulous drug dealer cuts cocaine with talcum powder, internet milk may be padded with cow’s milk or tap water. Although we know that in general milk contains hundreds, maybe thousands, of bioactive molecules, a systematic description of everything in human milk does not exist (Neville et al., 2012). Studies have shown that concentrations of constituents in milk vary across lactation within mother or among mothers at any given time, but we don’t entirely know how much or why (Hinde & Milligan, 2011). Some constituents may vary in relation to the woman’s physical and psychological health, the sex of her infant, and other things we still don’t know. Although there may be benefits to allomother’s milk from an evolutionary perspective as discussed above, when observed in other mammals, allomother’s milk usually supplements mother’s milk; it is not usually a replacement.
Online milk selling exists at the intersection of socio-political context, economic factors, feminist perspectives, and medical consequences (both beneficial and detrimental for developing infants). These are complex issues and require substantial consideration and discussion. Just as in every domain of milk research, answers and solutions are never simple or easily determined.
So what are some possible solutions? Expand the current national network of milk banks, donor programs, and private industry that mirrors the management of our national blood supply. (American Red Cross, I am looking in your direction.) Just as many hands make light work, many mammaries produce substantial volumes of life-saving donor milk at low cost per lactating woman. This would generate a larger supply of donor milk. Such a plan would have to guard against potential problems of the commercialization of human fluids (very tricky). This solution also requires the improvement of processing techniques so as to retain the bioactivity of milk constituents. We also need to responsibly increase awareness of the risks involved with online milk sharing both for donors and recipients. A key element of this is not just educating parents but also health care providers to be able to effectively, and with nuance, discuss milk sharing with their patients. Parents who want to feed their baby breast milk are buying internet milk because they don’t want to use formula. If a formula more representative of human milk were available (cost effectively), perhaps fewer parents would take the risk of internet breast milk. Commercial infant formulas need to better reflect the complex biofluid that is human milk. Advantageously, many companies are interested in doing just that.
And we need to do more for families who steadfastly demand breast milk for their babies. We need to establish, with the reality of online exchanges in mind, best practices for milk handling from collection to storage to shipping to preparing for feeding. Some websites that host milk-sharing profiles include “tips,” but these fall far short of best practices. The reality is that milk sharing is part of our evolutionary and cultural heritage because, as with all aspects of child-rearing, infant feeding takes a village–the lactation biologists unlocking nature’s milk recipes, the food scientists formulating alternatives, clinicians caring for vulnerable patients, employers providing maternity leave and pumping stations, and healthy women donating their over-supply; all of these people contribute to optimizing infant health. This is our modern village, and we can do more to support all of our neighbors.
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Prof. Katie Hinde
Department of Human Evolutionary Biology