When to Wean

So many directions to go after that essay title. My pithy kneejerk response is “whenever the eff makes sense for you and your life, moms!” but then I recall I’ve been trying to cut back on my sailor mouth. 

I could quote the World Health Organization recommendations “continue frequent, on-demand breastfeeding until two years of age or beyond” or the American Academy of Pediatrics “for as long as is mutually desired by the mother and baby” or United Nations Children’s Fund (UNICEF), or the United States Center for Disease Control, or… or… or… or… Just like the beat, the list of evidence-based public health recommendations goes on.

Alternatively I can have my face melted by looking into the Ark of the Covenant that is the comment thread of Barbara King’s NPR post “What's Right About A 6-Year-Old Who Breast-Feeds”

When Barbara contacted me to provide comments for her thoughtful piece on very prolonged breastfeeding in response to the Mirror’s report on Denise Sumpter and the accompanying brouhaha, I groaned.  And then I groaned some more. Hornets nests. Viper Pits. Thin ice. These over-used metaphors can’t capture what awaits those who wade into mommy war waters.

I would rather face the orcs and trolls who pour through the Black Gates.

And to do justice to discussions of breast-feeding, particularly very prolonged breast-feeding in humans, we need to consider life history theory, biocultural reproduction, gene-culture coevolution, comparative primatology, individual and population levels of analysis, cultural relativism, the naturalistic fallacy, ecological context, global health, developmental programming, public policy, and maternal psychology. The complexities of these intersecting topics don’t lend themselves to quotable quotes.

And while I am getting better at public outreach, providing unambiguous, stand-alone, nuanced messages that will resonate across parents, lactivists, clinicians, colleagues, and the “cover-up! cover-up your breasts!” types... well that is just not in my wheelhouse yet. Also, I was in Davis, CA doing milk research and so punted by discussing gene-culture co-evolution. But also knew a comprehensive blogpost would have to roll out too, using the rhetorical device of myth-debunking to explore these topics.

Myth: Humans are adapted to wean at a specific age.

Sometimes folks will posit that this adaptive sweet spot is at 2 years old, at 2.5 years, at 4 years, 5 years, or some even 7 years.

Nope, nope, nope.

First of all, weaning is not an event, it is a process, so it can’t happen AT a time. When that process begins and how long mothers and infants negotiate milk transfer is going to vary across mother-infant dyads (Borries et al. 2014, Lee 1996 and see my previous post on weaning). As a general rule, for these types of behavioral biology traits there is no precise one size fits all adaptive set-point. And we’ll come back to whose adaptive optima- mom’s or kiddo’s- is being considered in the discussion of parent-offspring conflict below.

“Age at weaning” is found in the literature derived from behavioral observations. Sometimes it is the introduction of non-maternal foods- even though many primates have a period of complementary feeding of mother’s milk and solid foods. Perhaps the date of last nipple contact- but sometimes milk isn’t transferred, or milk is transferred in very very small volume. Do we make some absurd criteria like Monty Python instructions for the holy hand grenade of Antioch: “when less than 5% of daily caloric intake derives from mother’s milk for 14 consecutive days then the infant will be considered weaned- not 6%, not 5% for 13 days. 12 days is RIGHT OUT!”

We can awesomely look for isotopic signatures of milk consumption in poo and teeth, but those data are currently accumulating and not yet available for broad comparative analyses (Reitsema 2012, Austin et al. 2013).

Harrowell, Austin, Arora

Speaking of teeth, some scholars posit that by looking at tooth eruption patterns, particularly first molar, we know when young are adapted to transition to eating solid foods. But research is suggesting that inferences from tooth eruption schedules have notable challenges (Smith 2013 & see Wendy Dirks comment below!). In part this is because average tooth eruption patterns were linked to averages for “weaning age” at the species level, but that tells us little about the variation WITHIN SPECIES… which can be substantial. In an AWESOME OPEN ACCESS paper, Carola Borries and colleagues explain why we need to be cautious about aggregated life history tables. 

In a recent study of wild-living chimpanzees, Tanya Smith and colleagues found that “first molar emergence in these chimpanzees does not directly or consistently predict the introduction of solid foods, resumption of maternal estrous cycling, cessation of nursing, or maternal inter-birth intervals.” 

Chimpanzee tooth eruption, Andrew Bernard.

This gets us to lifetime reproductive success and parent-offspring conflict. Natural selection has shaped mothers to produce a series of offspring across a reproductive career, and has favored adaptations to transition from current reproduction to the next reproductive event. Individual offspring, being entirely related to oneself and only partially related to siblings- in terms of probabilities of shared genes- have been selected to want more resources from the mother than she has been selected to provide (Trivers 1974). This is why I find the AAP recommendation of “for as long as is mutually desired by the mother and baby” suboptimal, since parent-offspring conflict theory tells us that adaptive optima for mothers and offspring are expected to differ.

Anyone who has tangled with a weaning tantrum 

knows about parent offspring conflict.

Something that potentially provides insights into an adaptive timing of weaning is the production of lactase. Baby mammals are able to digest mother’s milk because they produce the enzyme lactase. This lactase enzyme breaks down lactose, the primary sugar in mammalian milk. The gene expression that controls the production of lactase shuts down during development as infants transition into juveniles. Scholars have hypothesized that the genetically programmed down-regulation of lactase is an aspect of the push-pull of parent-offspring conflict- if kiddo can’t digest mother’s milk, kiddo isn’t demanding it, and mom can allocate milk & energy to the next kiddo (Krebs 2009).

But many humans have “lactase persistence genes” that express well into adulthood. These genes have been favored by a cultural context of dairying. Individuals who continued to express lactase post-weaning living in populations that had cows, goats, camels, mares, and sheep were able to digest animal milks gaining protein and fat in their diet. This complex interplay between the human genome and cultural practices is known as gene-culture coevolution. This complicates the inferences we can make about the duration of breastfeeding and weaning times. Selective favoring of lactase persistence due to the cultural practice of animal herding (pastoralism) may have, as a byproduct, facilitated very prolonged breastfeeding in some populations. Interestingly use of domesticated animals across cultures is associated with a later age of introducing solids, but not breastfeeding duration (Sellen and Smay 2001)

Notably, not all humans have genes for lactase persistence. Where reported, the timed onset of declining lactase production occurs around 2 years of age. As stated by Wang and colleagues, “genetically programmed down-regulation of the lactase gene is detectable in children from the second year of life, although the onset and extent are somewhat variable” (1991). However, the end of any lactase production occurs by age 5 or as maybe as late as age 10, depending on the population being studied (Swallow 2003). Which means that human kiddos without lactase persistence have a pretty wide and variable window for digesting mother’s milk… 2-10 years.

Last cautionary note: adaptations reflect selection on traits in ancestral populations... not the current environment. And beware the lure of the naturalistic fallacies.

MYTH: We totes know the systematic effects of very prolonged breastfeeding.

Extensive research has demonstrated that exclusive breastfeeding the first months of life contributes to optimal infant health and development. Most research effort has been directed to understanding the effects of exclusive breastfeeding the first 4-6 months (current recommendations are exclusive breastfeeding for the first 6 months)… but on the other end of lactation, we know relatively little.

We don’t even systematically know what the milk composition is in mothers who sustain lactation for multiple years.

Mandel and colleagues recruited women who continued to breastfeed after the first-year. They sampled milk from 34 mothers who varied in how long they were lactating between 12 and 39 months of infant age and found that percent milk fat was higher the longer lactation had been sustained but they didn’t measure the amount of milk produced (2005). They stated that the “The long-term effects of such high fat intake have not been studied.” Kay Dewey’s 1984 study on breast milk composition from 12-20 months was able to look many more aspects of milk including many minerals. In general, the milk composition is similar in the second year of lactation as in the first year, when mothers are producing more that 500 mls of milk a day. However very few of these mothers were producing that much (N=4), most had significantly decreased their milk production.

Dewey et al. 1984

Those two studies above were conducted in “WEIRD” populations- Westernized, educated, industrialized, rich, & democratic, but most people aren’t WEIRD (Henrich et al. 2010). 

But before them, in 1978, Jeliffe and Jeliffe reviewed milk production across multiple populations, including poorly nourished communities in the Global South. Milk volume is seemingly much lower as lactation progresses. This is to be expected, as young consume solid foods and suckle less often, milk flow through in the mammary gland decreases causing a down-regulation of lactose synthesis. The lactose is responsible for pulling water into the mammary gland (yay osmotic pressure!), so as lactose synthesis decreases, milk volume decreases. Recently, Quinn showed among Filipino women breastfeeding up to 18 months of infant age that milk produced for older infants was higher in fat content and lower in lactose, consistent with expectations of the weaning process (Quinn et al. 2012).

Jeliffe and Jeliffe 1978 

These studies looked at milk primarily up to 2 years of infant age, 3-4 years of age tops. And they investigated macro-constituents in milk; percent fat, percent protein. What about the specific fatty acids? The specific proteins? And what about hormones? cells? immunofactors? bacteria? oligosaccharides? There are hundreds, if not thousands, of constituents in milk that we are still describing during the period of exclusive breast-feeding much less milk during complementary feeding. We are still unlocking what these constituents do when ingested by the newborn, much less toddlers and children. The information of very prolonged breastfeeding of 5+ years comes from rare self-selected cases, an extreme tail end of a continuous distribution of weaning ages.

Irwin Bernstein said it best, “The plural of anecdote is not data.” 

MYTH: The effects of breastfeeding are the same for all moms & infants in all places always.

Most of what we know about the effects of breast milk come from studies comparing formula and breast milk feeding or comparisons of duration of exclusive breastfeeding. As already mentioned above. The AMOUNT of the differences between formula and breastmilk groups depends on many things that also influence infant risk and development- key features of the environment. For the very low-birth weight, premature infant in the neonatal intensive care unit at high risk of necrotizing enterocolitis, breast milk can potentially mean the difference between life and death, can influence the length of hospital stay, and the hospital costs (Repa et al. 2014; Parker et al. 2012). For kiddos in communities with high prevalence of infectious diseases, limited access to clean drinking water, and risk of malnutrition… breast milk can reduce the risk of lethal diarrheal disease.

Global Diarrheal Disease

For the typically developing full term infant growing up WEIRD, the effect sizes of breast milk are often statistically and biologically significant. Though the effects are going to be less dramatic than in other settings. 

Similarly, since nutritional and environmental impacts have the strongest impacts earlier in development, as kiddos age the expected effect size of breast milk on cognition, health, behavior, growth is expected to decrease. This is the crux of developmental programming. When as kiddos age the benefits of breastfeeding go to zero though… we don’t have data to know. And whether or not continued breastfeeding should cross zero to detrimental consequences… well I am not aware of any research that supports those claims either.

MYTH: Moms have all the options.

We need to stop pretending that all mothers have all options. They don’t. Aside from the increasingly common medical conditions that prevent breastfeeding, many mothers can not meet their breast-feeding goals because of economic realities, lack of social support, cultural barriers, and limitations in medical training. 

Less than 250 hospitals in the US are designated “baby friendly” by offering “an optimal level of care for infant feeding and mother/baby bonding.” Some states don’t have ANY baby friendly hospitals. The recommendations for exclusive breast-feeding for six months is challenging when one lives in a country without paid maternity leave. The Affordable Care Act mandates insurance coverage for high quality pumps, break time and break space for pumping, and storage space for collected breast milk… but employers are differentially compliant with these protections. 

We owe mothers better support and better options, including better formulas that include more bioactive features of breast milk.

Wonder Woman as a Renaissance painting by Flashdaz

Messaging that undermines the women who are successfully breastfeeding for however long frustrates me. Just as messaging that undermines mothers whose lives and lived experiences limit their breastfeeding options. There are many ways to nurture our babies, our toddlers, our children, our teens, and our adult offspring. We are more than our mammary glands.

Words have power. Words chastise, words shame, words bolster, and words buffer. So what do we do, as clinicians, as biologists, as friends, when a single statement about breastfeeding, pro or con, exerts each of those outcomes depending on the person reading and hearing them?

I imagine the mother who desperately wants to breastfeed for any amount of time but the particular economic, medical, cultural, or social context doesn’t allow it. By emphasizing the importance of breastfeeding, without breaking down the barriers to breastfeeding, we are setting up mothers for failure and guilt.

I think about the precocious and wonderful18-month old Lulu whose mother gets dirty looks for continuing to nurse her daughter in full accordance with CDC and WHO recommendations.

LULU! (full disclosure r= 0.0625)

I remember the mother who is breastfeeding her 4-year old who is recovering from neurosurgery.

I worry about the elected officials and policymakers who read above about small effect sizes and foolishly think breastfeeding is not important because they don't understand that small effect sizes aggregated across a district, state, or nation translates into MILLIONS of public health dollars and a healthier society.

Krysten Ritter. Best eyeroll ever.

____________________

So where does this leave us?

In 2005, Dror Mandel and colleagues began their paper with the following sentence “The optimal duration of breastfeeding is unknown.” Given the wide range of variation and continued limitations in the state of our knowledge the idea that there is a specific adaptive age for weaning is not supported. There is no one way; there is no one size fits all.

So many people approach breast-feeding topics as black and white. But biology is entirely shades of gray- and way more than 50. Biological systems are exquisitely complex. Humans as biocultural organisms are confronted by the realities of the cultural and individual contexts in which we produce and rear our young.

Women of the World

Grappling with that complexity, as I do professionally as a scientist, precludes excessive claims relying on either logical fallacies or intuitions or non-existent data. And I am looking in both directions at folks who are intensely, aggressively pro- OR anti- prolonged breastfeeding. Whatever your arguments may be, they are predicated on “all else being equal.” But all else is never equal, and how any given mother weighs each of her considerations will ALWAYS be specific to her individual situation.

So proscriptive attitudes about what women should and shouldn’t do with their bodies can suck it.

Citations and Further Reading

Austin, Christine, et al. "Barium distributions in teeth reveal early-life dietary transitions in primates." Nature 498.7453 (2013): 216-219.

Bernstein, IS. "Cognitive capacities of Old World monkeys based on studies of social behavior." Old world monkeys (2000): 368.

Borries, C., Gordon, A. D., & Koenig, A. (2013). Beware of primate life history data: a plea for data standards and a repository. PloS one, 8(6), e67200.

Borries, C., Lu, A., Ossi‐Lupo, K., Larney, E., & Koenig, A. (2014). The meaning of weaning in wild Phayre's leaf monkeys: Last nipple contact, survival, and independence. American journal of physical anthropology, 154(2), 291-301.

Dewey, K. G., Finley, D. A., & Lönnerdal, B. (1984). Breast Milk Volume and Composition During Late Lactation (7-20 Months). Journal of pediatric gastroenterology and nutrition, 3(5), 713-720.

Henrich, J., Heine, S. J., & Norenzayan, A. (2010). Most people are not WEIRD. Nature, 466(7302), 29-29.

Jelliffe, D. B., & Jelliffe, E. F. (1978). The volume and composition of human milk in poorly nourished communities. A review. The American journal of clinical nutrition, 31(3), 492.

Kramer, M. S., Kakuma, R., & World Health Organization. (2001). The optimal duration of exclusive breastfeeding: a systematic review.

Krebs, J. R. (2009). The gourmet ape: evolution and human food preferences. The American journal of clinical nutrition, 90(3), 707S-711S.

Lee, P. C. (1996). The meanings of weaning: growth, lactation, and life history. Evolutionary Anthropology: Issues, News, and Reviews, 5(3), 87-98.

Mandel, D., Lubetzky, R., Dollberg, S., Barak, S., & Mimouni, F. B. (2005). Fat and energy contents of expressed human breast milk in prolonged lactation. Pediatrics, 116(3), e432-e435.

Parker, L. A., Krueger, C., Sullivan, S., Kelechi, T., & Mueller, M. (2012). Effect of breast milk on hospital costs and length of stay among very low-birth-weight infants in the NICU. Advances in Neonatal Care, 12(4), 254-259.

Quinn, E. A., Largado, F., Power, M., & Kuzawa, C. W. (2012). Predictors of breast milk macronutrient composition in Filipino mothers. American Journal of Human Biology, 24(4), 533-540.

Reitsema, L. J. (2012). Introducing fecal stable isotope analysis in primate weaning studies. American journal of primatology, 74(10), 926-939.

Repa, A., Thanhaeuser, M., Endress, D., Weber, M., Kreissl, A., Binder, C., ... & Haiden, N. (2014). Probiotics (Lactobacillus acidophilus and Bifidobacterium bifidum) prevent NEC in VLBW infants fed breast milk but not formula. Pediatric research.

Sellen, D. W., & Smay, D. B. (2001). Relationship between subsistence and age at weaning in “preindustrial” societies. Human Nature, 12(1), 47-87.

Smith TM. 2013. Teeth and Human Life-History Evolution. Ann Rev Anthropol. 42: 191-208.

Smith, T. M., Machanda, Z., Bernard, A. B., Donovan, R. M., Papakyrikos, A. M., Muller, M. N., & Wrangham, R. (2013). First molar eruption, weaning, and life history in living wild chimpanzees. Proceedings of the National Academy of Sciences, 110(8), 2787-2791.

Swallow, D. M. (2003). Genetics of lactase persistence and lactose intolerance. Annual review of genetics, 37(1), 197-219.

Trivers, R. L. (1974). Parent-offspring conflict. American zoologist, 14(1), 249-264.

Wang, Y., Harvey, C. B., Hollox, E. J., Phillips, A. D., Poulter, M., Clay, P., ... & Swallow, D. M. (1998). The genetically programmed down-regulation of lactase in children. Gastroenterology, 114(6), 1230-1236.

UPDATE 1/18/2015 13:15 PST: It has come to my attention that I have unwittingly replicated the title of a published paper:

Dettwyler, K. A. (2004). When to wean: biological versus cultural perspectives. Clinical obstetrics and gynecology, 47(3), 712-723. 

UPDATE 1/19/2015 12:54 PST: Added text about supplemental feeding and breastfeeding duration cross-culturally citing Sellen & Smay 2001, a great paper that can be read here.

Anyone who has relevant papers on this topic, please leave a comment. Also, comments will be moderated.