Professional Documents
Culture Documents
Miriam Erick
PII: S0306-9877(17)30649-7
DOI: https://doi.org/10.1016/j.mehy.2017.12.020
Reference: YMEHY 8757
Please cite this article as: M. Erick, Breast milk is conditionally perfect, Medical Hypotheses (2017), doi: https://
doi.org/10.1016/j.mehy.2017.12.020
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers
we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and
review of the resulting proof before it is published in its final form. Please note that during the production process
errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Breast milk is conditionally perfect (YMEHY_2017_571)
(c) 2017
Abstract
Breast milk is the universal preferred nutrition for the newborn human infant. New mother
have been encouraged to exclusively breastfeed by health care professionals and consumer-
advocacy forums for years, citing “breast milk is the perfect food”. The benefits are numerous
Human milk is a composite of nutritional choices of the mother, commencing in the pre-
conceptual era. Events influencing the eventual nutritional profile of breast milk for the
neonate start with pre-conceptual dietary habits through pregnancy and finally to postpartum.
It is not known who coined the phrase “breast milk is the perfect food” but it is widely
prevalent in the literature. While breast milk is highly nutritive, containing important
immunological and growth factors, scientific investigation reveals a few short-falls. Overall,
human breast milk has been found to be low in certain nutrients in developed countries:
vitamin D, iodine, iron, and vitamin K. Additional nutrient deficiencies have been documented
1
Given these findings, isn’t it more accurate to describe breast milk as “conditionally perfect”?
Here, we explore the nutritional status of groups of young women; some of whom will become
pregnant and eventually produce breast milk. We will review the available literature profiling
vitamin, mineral, protein and caloric content of breast milk. We highlight pre-existing
While alternative forms of infant nutrition carry standard product labels of nutrient adequacy,
this information does not apply universally to all breast milk. Infant formulas are fortified with
omega 3 fatty acids and any important new nutritional finding. Infant formulas are
manufactured to be consistent in composition and are monitored closely for quality. Not true
Any nutrient deficiency existing in pregnancy will ultimately be carried forward via lactation. It
is a biological impossibility for a lactating woman to transfer nutrients via breast milk she does
not have!
2
3
Introduction
Breast milk is the universal preferred nutrition for the newborn human infant. New mothers
have been encouraged to exclusively breastfeed by health care professionals and consumer-
advocacy forums for years globally, citing “breast milk is the perfect food”. The benefits are
Human milk is a composite of nutritional choices of the mother, starting in the pre-conceptual
era. Events that influence the nutritional profile of breast milk for the neonate include pre-
conceptual dietary habits, through pregnancy and finally to postpartum and lactation. Food
While alternative forms of infant nutrition carry standard product labels of nutrient adequacy,
this information does not apply universally to all breast milk. Infant formulas are fortified with
omega 3 fatty acids and other relevant factors from current studies. Alternative infant formulas
are consistent in composition and monitored closely to ensure quality. This is not universally
This paper presents findings from the literature regarding the potential compromised
nutritional status of women from various global communities. Some of these women are in
the pre-conceptual stage of life, some are pregnant and some postpartum and breast feeding.
4
Where nutrient deficits exist, the importance for effective nutrition intervention for the
postpartum needs of the new mother is critical. Only when the new mother is adequately
nourished can she provide optimal nourishment via breast milk to the neonate who has a
Hypothesis
It is not known who first coined the phrase “breast milk is the perfect food for the infant” but it
is widely prevalent in the literature. While breast milk is highly nutritive and contains
important immunological and growth factors, scientific investigation reveals a few short-falls.
Overall, human breast milk has been found to be low in certain nutrients in developed
countries: vitamin D, (3) (4 ) iodine (5), iron (6) (7) (8) and vitamin K. (9) (10). Additional
nutrient deficiencies have been documented in resource-poor countries: vitamin A (11) (12),
vitamin B 12 (13), (14), (15), (16), zinc (11), (12), and vitamin B 1/ thiamin. (17 ), (18).
Given these findings, isn’t it more accurate to describe breast milk as “conditionally perfect”?
5
We explore the nutritional status of groups of young women; some of whom will become
pregnant and eventually produce breast milk. We will review the available literature profiling
Expanding on the Barker Hypotheses, maintaining that adult diseases begin in utero we present
examples. What we know is frank iodine deficiency in pregnancy reduces fetal/neonatal IQ,
which is a cognitive injury. We also know that pre-conceptual folic acid deficiency results in
neural tube defect, a physical injury. Our last example is iron; a deficiency in pregnancy
reduces fetal myelin development which is associated with reduced attention span, and also
implicated in small for gestational age (SGA) neonates; resulting in both a cognitive and physical
Central to our hypothesis is that there are likely nutrients; vitamins, minerals, protein and fat; in
the human brain, as extrapolated from reference data on nutrients in animal brain used for
food. The data on nutrients in animal brain likely represents the by-product of optimal
nutrition to develop the flesh of animals for consumption. (19) Nutrients in the brain are
conveyed from the dietary intake of the subject. In pregnancy, the maternal intake would be
the vehicle in which nutrients are conveyed to the developing fetal brain. Not all pregnant
Nutrient deficiencies existing in pregnancy will be carried forward via lactation. It is a biological
impossibility for the lactating woman with any nutrient deficiency to transfer that nutrient to
6
breast milk. The newborn brain develops rapidly and requires optimal substrate to meet
optimization. Nutritional shortfalls in the neonate are not immediately apparent. Remediation,
however, after a defect is discovered may not remedy the insult. The window of opportunity
Table 1 highlights several situations which may present in a woman’s life that can impact her
nutritional status. Column 1 lists potential conditions which need attention pre-conceptually.
Nutrient deficits, pre-existing and if not corrected, will likely continue on their established
not uncommon. Wide-spread folic acid insufficiency, a form of malnourishment, points to only
one example of inadequate nutrient intake which had documented adverse implications for
pregnancy outcome. The action which resulted as a result of this knowledge was a universal
recommendation to take supplemental folic acid at least 3 month prior to conception. (46)
difficult one, especially in the obese. In the early 1970’s hospital malnutrition was
(48)(49) Malnutrition in pregnancy is also among the unrecognized “skeletons in the closet”.
7
Preconception
deficiencies which contribute to significant public health issues, negatively affecting maternal
and infant/child health outcomes. (36). A study of 4,983 rural women of reproductive age in
estimated average requirement was 25% for iron, 16% for zinc, 54% for folate, 64% for vitamin
B 12 and 27% for vitamin A. Each of these nutrient shortfalls has repercussions in the
developing embryo.
In more affluence countries, unidentified eating disorders affect pregnancy. Anorexia nervosa,
bulimia nervosa and binge eating disorders have lifetime prevalence estimates of .9%, 1.5%,
and 3.5% among women. It is estimated that only a minority of cases seek treatment. (21) (22)
Bariatric surgery for obesity has many benefits and a few caveats. Adequate oral contraception
after bariatric contraception ensures the woman has had enough time to stabilize weight and
optimize nutritional status. (35) Weight loss alters the hormonal balance between testosterone
and estrogen which increases fertility potential. Becoming pregnancy within a year of weight
loss surgery is not advised due to concerns over nutritional adequacy for fetal development.
Bariatric surgery has the potential to alter oral contraceptive agent (OCA) efficacy. Absorption
of OCA after bariatric surgery can be reduced if intestinal length has been altered. Experts
8
recommend adding a secondary agent such as barrier methods to prevent unintended
subjects after six months procedure and compliance found to be 30%. (26) While most of these
study persons were male and fully employed, this observation raises concern for women in the
reproductive years.
Paradoxically even with obesity, micronutrient malnutrition also co-exists. The American
Society for Metabolic and Bariatric Surgery reviewed the prevalence of pre-weight loss surgery
(WLS) micronutrient deficiency as well as post WLS nutrient deficiencies. (25) These findings
are presented in Table 2. Multiple nutrient deficiencies can exist in a single individual.
Pregnancy
Despite various recommendations for nutrient increases for pregnancy, not all women enter
pregnancy nutritionally replete. (23) Recommended Dietary Allowances (RDA’s) for pregnancy
for micronutrients (vitamins and minerals) remain constant throughout the trimesters except
for calories. (50 IOM) Maternal nutritional assessment is not routine hence nutritional
Prenatal supplemental vitamin tablets are regularly prescribed, however the compositions of
supplemental nutrients vary widely and none includes protein or energy components. Until
recently some prenatal supplements lack iodine, an essential nutrient. This decision was the
9
result of focus data from women having an adverse reaction to pyleogram (IVP) dye and/or
A 2002 study from Newark, New Jersey Baker et al identified at least 5 sub-clinical nutrient
deficiencies in a population of randomly selected 563 women, all enrolled in the WIC (Women,
Infant and Children) Program. (51) All women were compliant with prenatal supplementation
and assessed by registered dietitians as having adequate diets. Twelve nutrients were
assessed by different trimester: Niacin, thiamin, vitamin A, vitamin B 12, vitamin B 6, folic acid,
biotin, pantothenic acid, riboflavin, vitamin C, carotenes and vitamin E. Eighty three non-
pregnant women, aged 24-36, provided reference values for these nutrients. Details are
Baker’s group concluded an average of 20-30% of pregnant women suffer from a vitamin
author, include increased fetal requirement corresponding to growth and development in the
setting of decreased intake due to reduced maternal gastric space and early satiety, both
prevalent in advanced gestation. Of the 563 women included in this study, 53 neonates were
of low birth weight, less than 1500 grams. While they attempted to correlate low birth weights
as well as parity, gestational age with changes in the deficient nutrients, e.g. niacin, thiamin,
vitamin A, vitamin B 12, they found no statistical correlation using the Wilcoxon’s rank sum test.
Baker’s group theorized perhaps clearer correlations with factors involving pregnancy outcome
10
with hypovitaminemias might have emerged without prenatal supplements. However they felt
pregnant women found 1 in 20 women were biochemically deficient for vitamin B 12 in early
pregnancy. Another study involving pregnant adolescents revealed 50% had suboptimal
Deficiencies in other nutrients, such as iron, vitamin K, folate and calcium can result in both
maternal complications such as severe anemia and fetal complications such as congenital
abnormalities, intrauterine growth restriction (IUGR) and failure to thrive (FTT). (40 Guelinckx).
Vitamin K embryopathy, found in some severe HG cases, affects bone and cartilage
recommendations have been provided for twins and triplets. (54) (55). Studies shows higher
rates of preterm infants and small for gestation age (SGA) neonates born to women suffering
from extremely poor nutritional intake due to severe hyperemesis gravidarum (37 ) (38) with
higher rates of learning disorders in these children. There is speculation early nutrient
deficiencies might play a role in the development of autism. (56) (57) A relationship between
11
An evaluation from the WIC (Women, Infants and Children Supplemental Feeding Program)
demonstrated that with continuation of the prenatal vitamin during lactation, with targeted
nutrition education and vouchers for healthy food, the rate of autism among the children of
Bariatric surgery has known consequences in persons poorly compliant with nutritional
protocols. If the non-compliant person is a pregnant woman, nutrient deficits impact the
developing fetus. (40) Compliance to bariatric nutritional protocols and follow up evaluations
are variable and can be associated with insurance issues. (24) Providers who counsel women
pre-conceptually should inquire about changes in memory, mood and skin changes, night
vision, and hair loss along and frequency of bariatric follow up.
Despite compliant, adequate nutrient levels cannot always be achieved. (44) One case report
7 years before pregnancy was fund to have severe, maternal hypovitaminosis A during
gestation, manifesting a night blindness. The infant was born with undetectable serum vitamin
A levels, microphthalmia, inferior adherent leukoma and optic nerve hypoplasia. At 9 months
Night blindness, due to inadequate vitamin A intake in an impoverished pregnant woman, will
also affect the visual acuity of the fetus and increases risk for infection in the neonate. In
addition sub-optimal zinc intake during pregnancy is associated with SGA infants who also have
12
reduced immune capacity and an increased risk for infection. Data are provided in Tables 4 and
5. (12)
Postpartum
benefit, is a physiologically and metabolically demanding activity which occurs after the delivery
of an infant.
The informative and detailed summary of nutrient content of human breast milk of well-
review of the literature suggests the nutritional content of human breast milk is not uniform
but dynamic, reflecting maternal dietary intake. (1) (3) (8) (11) (14) (15) (16) (18) (41) (61)
Breast milk has been assumed to provide 20 kilocalories/ounce. However, a study of breast
milk from lactating mothers of NICU infants, producing milk in excess of their infants’ needs,
showed high variability in nutrient content and an average 17.9 kilocalories/ounce. (70)
Phrynoderma and acquired acrodermatitis enteropathica, both skin lesions, were reported in
two women following Roux-en-Y gastric bypass surgeries. One woman was diagnosed with a
vitamin A deficiency and the second with zinc deficiency. (45) While both women experienced
symptoms during pregnancy, clinicians felt the additional metabolic demands associated with
13
lactation further depleted nutrient stores, worsened lesions which drove women to specialists
for treatment.
Human breast milk has very little iron- 0.4 mg/L. (6) Iron supplementation of exclusively
breast fed infants needs to occur by 4 months if the mother had an uncomplicated healthy
pregnancy as the neonatal stores will be depleted. (6)(7). In study of 68 late preterm infants
born between 32 and 35 weeks of gestation, iron depletion and iron depletion anemia were
present in 38.2% and 30.9% of the infants by 6 weeks post natal life. Early supplementation for
the late preterm infant with a low birth weight (< 1830 g) and a low serum ferritin (< 155 ug/l)
in the absence of infection in the first week of life is needed to avoid iron depletion which may
Vitamin B 12, a key nutrient for neurological development, is low in breast milk of impoverished
women whose diet is low in animal protein, those with un-supplemented vegan diets as well as
some after bariatric procedures with poor compliance to nutritional protocols. (14) (15) (16)
(26) (61)
The vitamin D concentration in breast milk of women taking 400 international units (IU) of
vitamin D per day in pregnancy is relatively low, leading to vitamin D deficiency in breastfed
infants. The vitamin D activity in normal lactating women is known to be in the range of 5 to 80
IU depending method of assay. Supplementation with vitamin D to the nursing infant has been
endorsed by the American Academy of Pediatricians (AAP) and the Institute of Medicine (IOM).
14
Compliance to this practice is poor, ranging from 2-19%. (3) In a US study supplementing
nursing mothers with 400, 2400 or 6400 IU vitamin D3 daily for 6 months showed
supplementation with 6400 IU/day safely supplied breast milk with adequate vitamin D to meet
infant requirements and offered an alternative strategy to direct infant supplementation. (3)
Breast milk is low in vitamin K. (7) (10) Infants who are exclusively breastfed and who do not
receive intramuscular (IM) vitamin K at birth are at risk for hemorrhagic disease (HDN) of the
newborn. In a case report, a four week old infant, exclusively breastfed, presented to an
emergency department with lethargy and a grossly dilated right pupil. Trauma was ruled out.
A CT scan revealed a right-sided subdural hematoma with mid-line shift. The infant’s
international normalized ratio (INR) was over 10.9 and his prothrombin time (PT) was over 120
seconds. Vitamin K was administered and the infant underwent emergency surgery.
The estimated basal metabolic requirement (BMR) of the infant brain, which weighs 10-11% of
total body weight, requires 50%-60% of total daily energy. (71) (72) which is far greater than
other mammals. An approximation of vitamins and minerals of animal brains provided in food
composition tables proxies the nutritional composition of human brain (20). The rapidly
A report of 10 infants (mean gestational age: 30 weeks; range 25-40 weeks) with zinc deficiency
to gestational age of 41.4 weeks) was reported from Hamburg, Germany. Initially the cutaneous
15
lesions were misdiagnosed as eczema or impetigo in 8 of the 10 infants and treated with topical
cortico-steroids for a mean of 4 weeks before the correct diagnosis was established by
decreased serum zinc levels. All infants were exclusively breast-fed. Due to the infants rapid
growth, there was in acceleration in zinc requirement. All 10 infants had serum zinc levels
below the normal range of 720-1570 ug/L, ranging from 159 to 567 ug/L. Breast milk zinc levels
were found to be below the normal range of 784-2416 ug/L in 3 of the mothers and 7 of the
mothers did not have levels drawn. Two of the 3 mothers had serum zinc levels below the
normal range of 600-900ug/L; the first with 416 ug/L and the second mother with 548 ug/L.
Symptoms resolved with oral zinc supplementation. The zinc levels of mature breast milk are
lower than zinc in cow’s milk (1.18 mg/L vs. 3.9 mg/L) and further decrease during lactation.
(73)
From a study of 158 infants, aged 6 months, the prevalence of zinc deficiency was investigated
by feeding modality: exclusively breast fed, formula fed and mixed fed. Investigators found
14.9% zinc deficient in breast fed infants, 5.3% in formula bed infants and 2.9% in mixed fed
infants. A higher proportion of mothers of breast fed infants were found to be zinc deficient.
(74)
milk from undernourished mothers was studied. Forty samples of breast milk were obtained
from 20 undernourished mothers and 20 well-nourished mothers who had children, aged 15
16
days to 6 months, in the Emergency room of a pediatric ward. (62 Alvarez) Data are provided
in Table 7. This study was a prospective study with no experimental and comparative analysis
between the mothers’ nutritional condition and the macronutrients found in breast milk of two
groups of women. (62) However, breast milk of poorly nourished mothers provided 20%
Pregnant women in resource-poor areas are at risk for multiple micronutrient deficiencies and
indicators of low vitamin B-12 status have been associated with adverse pregnancy outcomes,
including anemia, low birth weight and IUGR. To evaluate whether a daily oral vitamin B-12
supplementation during pregnancy increases maternal and infant measures of vitamin B-12
status, researchers in Bangalore, India randomly assigned women to either a Vitamin B-12
supplement or placebo. Women in both groups received iron and folic acid supplements.
In a clinical report from Ankara, Turkey, 20 infants (11 girls, 9 boys) with a mean age of 6.65
+/- 4.5 months were evaluated for vitamin B 12 statuses. All infants were breast fed,
documented to be vitamin B-12 deficient and presented with various symptoms: 30% had
infections; 25% presented with pallor; hypotonia and neuro-developmental delay were
identified in 25%, 20% refused solid food and/or to suck, failure to thrive was found in 15% and
fatigue in 10%. All mothers were identified to be vitamin B 12 deficient due to low socio-
economics, living in resource-poor rural areas. (15) Vitamin B 12 can present as failure to
17
thrive (FTT) in the infant in as short a time as 2 months postnatal life in the full term infant
Experts suggest it is useful to categorize nutrients into 2 groups during lactation. Group I
nutrients (thiamin, riboflavin, vitamin B-6, choline, retinol, vitamin A, vitamin D, selenium and
iodine) are of the most interest in public health nutrition because their secretion into milk is
supplementation with these nutrients can increase breast milk concentrations and improve
infant status. In contrast, the concentration of Group II nutrients (folate, calcium, iron, copper
and zinc) in breast milk is relatively unaffected by maternal intake or status; the mother
gradually becomes more depleted when intake is less than the amount secreted in milk, add
maternal supplementation benefits the mother rather than the infant. (2)
Breast milk output is lower in malnourished women by 30%. This reduction corresponds to a
lower ingestion of immunoglobulins by the infants of malnourished women. (69). The serum
and human milk antimicrobial antibody titers were measured longitudinally in 17 malnourished
and 14 control Zairian women during 6 to 18 months of lactation to test whether malnutrition
was associated with an impaired secretory antibody response. No decrease in antibody content
was found in the malnourished women when compared with controls. (69) Improving the
18
During a prospective evaluation of a malaria prophylaxis program in a refugee population in
north western Thailand between 1987 and 1990 an extremely high infant mortality rate (18%)
was documented despite good access to health care. Infantile beriberi (thiamine deficiency)
was identified as causing 40% of all infant mortality. The likely cause was thiaminase activity
from raw fish, a typical dietary item, consumed by the lactating women. Vitamin B1 deficiency
was detected in 60% of the plasma samples of the breastfeeding mothers. Other sources of
thiaminase include betel nuts and ferns besides raw fish and raw shellfish. (17)
Vegan diets are known to be deficient in several key nutrients. In a review of the literature of
ranged from 17 to 39%, dependent on the trimester. (61) The deficiency prevalence among
In a report from a hospital in Prague, Czech Republic, pediatricians followed 40 children who
were referred for FTT. Serum vitamin B 12 (Cbl) of the 40 lactating asymptomatic women
showed levels at 122 +/-52 ng/L (normal range 250-900 ng/L) with breast milk levels of vitamin
B 12 at 64+/- 17 ng/L. Seventeen infants who were profoundly deficient in Cbl with serum
levels of 69 +/-17 ng/L and 23 infants with mild Cbl deficiency serum levels were noted to have
levels at 167 +/- 40 ng/L. Maternal Cbl deficiency may be caused by achlorhydria, Helicobacter
pylori infection, celiac disease, Crohn’s disease, and pancreatic insufficiency, treatment with
proton pump inhibitors or insufficient vitamin B12 from servings of animal proteins or a vegan
diet. (75) Cbl deficiency in adults may present as megaloblastic anemia, polyneuropathy, and
19
subacute combined neuro-degeneration of the spinal cord, dementia or depression. The
clinical impairment of the adult nervous system develops slowly over months or years. In
contrast vitamin B 12 deficiency can cause severe impairment in the neonate who is undergoing
rapid growth and may present within weeks. Anthropometrics- weight and length- begins to
decline long before other clinical presentation appears. FTT was present in 15 of the 17
severely deficient infants. Maternal Cbl deficiency can also be caused by insufficient Cbl
absorption. In this group of subjects only 6 (15%) of mothers were vegetarian. (16)
An investigation by Dijkhuizen (11) et al in West Java, Indonesia of 155 lactating mothers and
their healthy infants were assessed anthropometrically and biochemically via serum, urine and
breast milk samples for vitamin A and zinc. They demonstrated nutritional deficiencies in the
mother and infant do not have parallel biochemical parameters. The infants on physical
examinations were designated as appearing “healthy”. Data are provided in Table 9. (11)
Encouraging healthy omega 3 fats alters the saturated fatty acid profile of milk and can improve
omega 3 fatty acid delivery to the breast-fed infant. (1) (64) (65) Supplementation with
vitamin C and E also improves the total antioxidant content of human breast milk. (66)
Maternal diet influences iodine content of breast milk and is highly variable. (67). While
efforts to eradicate iodine deficiency have been successful with the use of iodized salt, pockets
20
Research demonstrates food flavors are transmitted via amniotic fluid during pregnancy and
postpartum, via breast milk. (77). There is a high probability that alcohol ingestion during
lactation is also influences the neonatal palate as well as the reward centers in the brain.
There is genuine concern that the additive properties of alcohol begin early and increase the
risk of alcohol addiction later in life. (78) (79) (80) Alcohol has been shown to disrupt the
hormonal milieu of the lactating woman which diminishes the milk supply. (81) A small
amount of alcohol before breast feeding was once thought beneficial however this practice is
no longer endorsed.
about the functions of this preprohormone indicate the potential to reduce the incidence of
preeclampsia, a major morbid condition of pregnancy and preterm birth, as well as later
supplementation with vitamin D is likely to become as health-enhancing as folic acid was in the
early 1990’s.
As a result of our review of the literature, we suggest that human breast milk is more accurately
termed “conditionally perfect” rather than “perfect” and the condition is based on the maternal
diet. It would be hoped that all persons have an adequate food intake which would enhance
health and prevent disease however the evidence this does not happen is well appreciated.
21
What is known about dietary improvement is that some of the most motivated persons are
When the question is asked: How can breast milk contain all the required nutrients for the
neonate from a woman who suffered from some degree of uncorrected gestational
malnutrition?
Honest answer: Breast milk can’t deliver adequate amounts of nutrients and energy to the
developing neonate without an aggressive nutritional repletion plan for the mother.
Women have heard the message “breast milk is perfect infant nutrition” and have no reason to
believe differently; but armed with knowledge that what they eat makes the crucial difference
At risk mothers include those who have experienced HG, have multiple gestations, previously
bariatric surgery or those with financial hardship or other situations of nutritional compromise
not included herein. Nutrient deficiencies are cumulative nutritional insults which are quietly
bestowed to the conceptus and then to the newborn as well as cognitive functioning and brain
growth. It is conceivable these deficits underlie the origins of autism, an expensive public
22
It is important the lactating woman and all health care professionals be cognizant of current
science regarding breast milk’s level of vitamin D, iron, iodine, vitamin K and other nutrients.
(1 ) (3) (4) (5) (6) (7)(9) (68) (74) (81) (82) Perpetuating the myth that all breast milk is
23
Breast milk is conditionally perfect
(c) 2017
References
nutrition on breast-milk composition: a systematic review. Am J Clin Nutr 2016 Sep; 104 (3):
646-62.
2. Allen, LH. B vitamins in breast milk: relative importance of maternal status and intake, and
3. Hollis BW, Wagner CL, Howard CR, et al. Maternal versus infant Vitamin D supplementation
4. Ziegler EE, Nelson SE, Jeter JM. Vitamin D supplementation of breastfed infants: a
5. Mulrine HM, Skeaff SA, Ferguson EL, Gray AR, Valeix P. Breast-milk iodine concentration
declines over the first 6 mo postpartum in iodine-deficient women. Am J Clin Nutr. 2010 Oct; 92
(4): 849-56.
6. Friel JK. There is No Iron in Human Milk. J Pediatr Gastroenterol Nutr 2016 Aug 4
7. Greer FR. How much iron is needed for breastfeeding infants? Curr Pediatr Rev. 2015; 11
(4): 298-304.
24
8. Akkermans MD, Uijterschout L, Abbink M, et al. Predictive factors of iron depletion in late
preterm infants at the postnatal age of 6 weeks. Eur J Clin Nutr. 2016 Aug: 70 (8): 941-6.
9. Greer FR. Are breast-fed infants vitamin K deficient? Adv Exp Med Biol 2001; 501: 391-5.
10. Enz R, Anderson RS, Jr. A blown pupil and intracranial hemorrhage in a 4 week old: a case
of delayed onset vitamin K bleeding, a rare “Can’t miss” diagnosis. J Emerg Med 2016 Aug 51
(2): 164-7.
11. Dijkhusizen MA, Wieringa FT, West CE, Muherdiyantiningsih, Muhilal. Concurrent
micronutrient deficiencies in lactating mothers and their infants in Indonesia. Am J Clin Nutr.
12. Biesalski K. Hidden Hunger- consequences for brain development. Bread and Brain,
Education and Poverty. Pontifical Academy of Sciences, Scripta Varia 125, Vatican City 2014.
www.pas.va/content/dam/accademia/pdf/sv125/sv125-biesalski.pdf.
13. Demir N, Koc A, Ustyol L, Peker E, Abuhandan M. Clinical and neurological findings of severe
vitamin B12 deficiency in infancy and importance of early diagnosis and treatment. J Paediatric
14. Pawlak R, Lester SE, Babtunde T. The prevalence of cobalamin deficiency among vegetarians
assessed by serum vitamin B12: a review of literature. Eur J Clin Nutr 2014 May; 68 (5): 541-8.
15. Akcaboy M, Malbora B, Zorlu P, Altmel E, Oguz MM, Senel S. Vitamin B12 deficiency in
25
16. Honzik T, Adamovicova M, Smolka V, Magner M, Hruba E, Zeman J. Clinical presentation
and metabolic consequences in 40 breastfed infants with nutritional vitamin B12 deficiency-
what have we learned? Eur J Padediatri Neurol 2010 Nov; 14 (6): 488-95.
17. Luxembruger C, White NJ, ter Kuile F, et al. Beri-beri: the major cause of infant mortality in
Karen refugees. Trans R Soc Trop Med Hyg. 2003 Mar-Apr; 97 (2): 251-5.
18. McGready R, Simpson JA, Arunjerdja R, et al. Delayed visual maturation in Karen refugee
19. Pennington JAT. Bowes & Church’s Food Values of Portions Commonly Used. 17th edition.
20. Hughes R. Food insecurity: the skeleton in the national closet. Public Health Nutr. 2009 Nov;
21. Dyer F. Understanding eating disorders in midwifery practice. Pract Midwifery 2016 Jul-
22. Hudson JI, Hiripi E, Pope HG, Jr, Kessler RC. The prevalence and correlates of eating
disorders in the National Comorbidity Survey Replication. Biol Psychiatry. 2007 Feb 1; 61 (3):
348-58.
23. Mmbaga N, Luk L. The impact of preconceptual diet on the outcome of reproductive
26
24. Wilson ER, Kyle TK, Nadglowski JF, Stanford FC. Obesity coverage gap: consumers perceive
low coverage for obesity treatments even when workplace wellness programs target BMI.
25. Parrot J, Frank L, Rabena R, Craggs-Dino L, Isom KA, Greiman L. American Society for
Metabolic and Bariatric Surgery Integrated Health National Guidelines for the Surgical Weight
Loss Patient 2016 Update: Micronutrients. Surg Ob Rel Dis. 2017 (in press)
26. Sunil S, Santiago VA, Gougeon L, et al. Predictors of vitamin adherence after bariatric
27. Boldery R, Fielding G, Rafter t, Pascoe AL, Scalia GM. Nutritional deficiency of selenium
gastric bypass and gastric banding surgery. Obes Surg 2012 Nov; 22 (11): 1660-5.
29. Kumar P, Hamza N, Madhok B, et al. Copper deficiency after gastric bypass for morbid
30. Goodman JC. Neurological complications of bariatric surgery. Curr Neurol Neurosci Rep.
31. Moss, HE. Bariatric surgery and the neuro-ophthalmolgist. J Neuroophthalmol. 2016. Mar;
36 (1): 78-84.
27
32. Al Hassany AA. Night blindness due to vitamin A deficiency associated with copper
deficiency myelopathy secondary to bowel bypass surgery. BMJ Case Rep. 2014 Apr 29; 2014.
Pii: bcr2013202478
33. Wilson HO, Datta DB. Complications from micronutrient deficiency following bariatric
34. Jen M, Yan AC. Syndromes associated with nutritional deficiencies and excess. Clin
35. Merhi ZO. Challenging oral contraception after weight loss by bariatric surgery. Gynecol
36. Nguygen PH, Nguyen H, Gonzalez-Casanova I, et al. Micronutrient intake among women of
reproductive age in Vietnam. PLoS One. 2014 Feb 21; 9 (2): e 89504. Doi:
10.1371/journal.pone. 008950
37. Fejzo MS, Poursharif B, Korst LM, et al. Symptoms and pregnancy outcomes with extreme
weight loss among women with hyperemesis gravidarum. J Womens Health (Larchmt). 2009
38. Fejzo MS, Magtira A, Schoenberg FP, Macgibbon K, Mullin PM. Neurodevelopmental delay
in children exposed in utero to hyperemesis gravidarum. Eur J Obstet Gynecol Reprod Biol
28
39. Aghajafari F, Field CJ, Kaplan BJ, et al. The current recommended Vitamin D intake guideline
for diet and supplements during pregnancy is not adequate to achieve Vitamin D sufficiency for
40. Guelinckx I, Devlieger R, Vansant G. Reproductive outcome after bariatric surgery: a critical
41. Jans G, Matthys C, Bogarets A, Lannoo M, et al. Maternal micronutrient deficiencies and
related adverse neonatal outcomes after bariatric surgery: a systematic review. Adv Nutr 2015
42. Machado SN, Pereira S. Saboya C, Saunders C, Ramalho A. Influence of roux-en-y gastric
bypass on nutritional status of vitamin A in pregnant women: a comparative study. Obes Surg
43. Gadgil MD, Chang HY, Richards TM, et al. Laboratory testing for and diagnosis of nutritional
deficiencies before and after bariatric surgery. J Womens Health (Larchmt). 2014 Feb; 23 (2):
129-37.
44. Gilchrist H, Taranath DA, Gole GA. Ocular malformation in a newborn secondary to
and acquired acrodermatitis enteropathica in breast feeding women after bariatric surgery. J
29
46. Ma R, Wang L, Jin L, Li Z, Ren A. Plasma folate levels and associated factors in women
planning to become pregnant in a population with high prevalence f neural tube defects. Birth
Defects Res. 2017 Jun 1. Doi: 10.1002/bbdr2.1040 (accessed Jun 21, 2017)
47. Butterworth CE. The skeleton in the closet. Nutr 1974. Sep-Oct; 10 95): 435-41.
48. Sousa TT, Sturion CJ, Faintuch J. Is the skeleton still in the hospital closet? A review of
hospital malnutrition emphasizing health economic aspects. Clin Nutr. 2015 Dec; 34 (6): 1088-
49. Cederholm T, Jensen GL. To create a consensus on malnutrition diagnostic criteria. JPEN
50. Institute of Medicine (IOM). Food and Nutrition Board: Dietary reference intakes for
energy, macronutrients, carbohydrates, fiber, fat and fatty acids. Washington, DC. 2002.
51. Baker H, DeAngelis B, Holland B, Gittens-Williams L, Barrett T Jr. Vitamin profile of 563
gravidas during trimesters of pregnancy. J Am Coll Nutr. 2002 Feb; 21 (1): 33-7.
53. Toriello HV, Erick M, Alessandri JL, et al. Maternal vitamin K deficient embryopathy:
association with hyper emesis gravid arum and Cohn disease. Am J Med Genet A. 2013 Mar;
30
54. Luke B. Nutrition for multiples. Clin Obstet Gynecol. 2015 Sep; 58 (3): 585-610.
55. Goodnight W, Newman R. Optimal nutrition for improved twin pregnancy outcome. Obstet
56. Chen J, Xin K, Wei J, Zhang K, Xiao M. Lower maternal serum 25 (OH) D in first trimester
associated with higher autism risk in Chinese offspring. J Psychosom Res 2016 Oct: 89: 98-101.
57. Al-Farsi YM, Waly MI, Deth RD, et al. Low folate and vitamin B12 nourishment is common in
Omani children with newly diagnosed autism. Nutr. 2013 Mar; 29 93): 537-41.
58. Anderson GH. Diet, neurotransmitters and brain function. Br Med Bulletin 1981 37 (1); 95-
100.
59. Shamberger RJ. Autism rates associated with nutrition and the WIC program. Amer Col
60. Lawrence RA, Lawrence RM. Breastfeeding: a guide for the medical profession. Lawrence
61. Roed C, Skovby F, Lund AM. Severe vitamin B 12 deficiency in infants breastfed by vegans.
Ugeskr Laeger 2009 Oct 19; 171 (43): 3099-101. Article in Danish.
31
63. Duggan C, Srinivasan K, Thomas T, et al. Vitamin B12 supplementation during pregnancy
and early lactation increases maternal, breast milk, and infant measures of vitamin B-12 status.
64. Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr
65. Maas C, Franz AR, Shunova A, et al. Choline and polyunsaturated fatty acids in preterm
66. Zarban A, Toroghi MM, Asli M, Jafari M, Veijdan M, Sharifzadeh G. Effect of vitamin C and E
supplementation on total antioxidant content of human breast milk and infant urine.
67. Dorea JG. Iodine nutrition and breastfeeding. J Trace Elem Med Biol. 2002; 16 (4): 207-20
68. Vio Streym S, Hojskov CS, Moller UK, et al. Vitamin D content in human breast milk: a 9-mo
69. Brussow H, Barclay D, Sidoti J, et al. Effect of malnutrition on serum and milk antibodies in
Zairian women. Clin Diagnos Lab Immunolo 1996 Jan; 3 (1): 37-41.
70. Sauer CW, Boutin MA, Kim JH. Wide variability in caloric density of expressed human milk
can lead to major underestimation or overestimation of nutrient content. J Hum Lact 2017.
33(2) 341-350.
71. Grande Covian F. [Energy metabolism of the brain in children (author’s transl)]. Article in
32
72. Georgieff M, Brunette KE, Tran PV. Early life nutrition and neural plasticity. Dev
73. Kienast A, Roth B, Bossier C, Hojabri C, Hoeger PH. Zinc-deficiency dermatitis in breast-fed
associated with breast milk zinc concentration and zinc status in breastfed infants aged 4-6
75. Matok I, Levy A, Wiznitzer A, Uziel E, Koren G, Gordischer R. The safety of fetal exposure to
proton-pump inhibitors during pregnancy. Dig Dis Sci 2012 Mar; 57 (3) 699-705.
76. Vanderpump MP. Epidemiology of iodine deficiency. Minerva Med. 2017 Apr; 108 (2): 116-
123.
77. Ventura AK, Worobey J. Early influences on the development of food preferences. Curr
78. Chang GQ, Karatayev O, Leibowitz SF. Prenatal exposure to ethanol stimulates
orexigenic peptide neurons and ethanol drinking in adolescent offspring. Neuroscience. 2015
33
79. Fabio MC, March SM, Molina JC, Nizhnikov ME, Spear NE, Pautassi RM. Prenatal ethanol
exposure increases ethanol intake and reduces c-Fos expression in intra-limbic cortex of
adolescent rats. Pharmacol Biochem Behav. 2013 Feb; 103 (4): 842-52. Doi: 10.1016/j.pbb.
80. Spear NE, Molina JC. Fetal or infantile exposure to ethanol promotes ethanol ingestion in
adolescence and adulthood: a theoretical review. Alc Clin Exp Res. 2005. Jun; 29 (6): 909-29.
81. Mennella JA, Pepino MY, Teff KL. Acute alcohol consumption disrupts the hormonal milieu
birth outcome and complications through direct genomic alteration. Mol Cell Endocrinol 2017
Sep 15; 453: 113-130. Doi: 10.1016/j.mce 2017.01.039. Epub 2017 Feb 7.
Author extends appreciation to Jean T. Cox, MS RD, University of New Mexico, Albuquerque,
34
Table 1 Lifestyle factors which impact the nutritional status of females
Planning for
pregnancy with Multiple gestation:
inadequate twins, triplets,
nutritional quadruplets,
supplementation: Quintuplets, sextuplets
folic acid. Other:
choline, iron, DHA,
iodine, vitamin D
(23) Hyperemesis
gravidarum (37 Fejzo)
Not at desirable (38 Fejzo)
body weight
Pregnancy (39)
Nutrient deficiencies Nutrient deficiencies Nutrient deficiencies
related to bariatric related to bariatric related to bariatric
surgery (24-34) surgery (40-43) surgery when
commencing
Inadequate oral lactation (44-45)
contraception after Complications arising
bariatric surgery during pregnancy (e.g.
(35) gallstones, trauma)
35
Poorly controlled Women who are
maternal medical pregnant and also
conditions: (e.g. breast feeding another
Crohn’s disease, child
ulcerative colitis,
metabolic disorders -
PKU, MSUD
Significant food
allergies without
supplementation
36
Table 2. Micronutrient status of persons before and after weight loss surgery (WLS) (25)
(abbreviations:
37
Table 3 Nutrient means considered deficient during pregnancy
(51)
38
Table 4 Incidence of night blindness in pregnant women globally
Region of the World % night blindness in pregnant Serum retinol < 0.70 umol/L
women
Globally 7.8% 15.3%
(6.5-9.1) (6.0-24.6)
Africa 9.4% 14.3%
(8.1-10.7) (9.7-19.0)
Americas and the Caribbean 4.4% 2.0%
(2.7-6.2) (0.4-3.6)
Asia 7.8% 18.4%
(6.6-9.0) (5.4-31.4)
Europe 2.9% 2.2%
1.1-4.6) (0.0-4.3)
Oceania (islands in the Pacific 9.2% 1.4%
Ocean) (10.3-18.2 (0.0-4.0)
(12)
39
Table 5 Incidence of Iodine, zinc and iron deficiencies in pregnant women globally
(12)
40
Table 6 Nutritional composition of human milk from well-nourished women
41
Potassium (mg) 74 64 57
Sodium 48 29 15
Zinc (ug) 540 n/a 120
OTHER
Carnitine nmol/mL 115 n/a 70-95
Cholesterol (mg) 27 16
Calories 57– 58 63 65
Adapted from (60)
Table 7 Maternal dietary intake and nutritional profile of breast milk from poorly nourished
breastfeeding women (62)
42
Table 8 Impact of maternal Vitamin B-12 supplementation on breast milk and infant serum
(63)
43
Table 9 Comparison of maternal vs. neonate nutritional deficiencies
(11)
44
Miriam Erick Conflict of Interest
Miriam Erick is also a book author and receives royalties from Managing Morning Sickness and Take Two
Crackers and Call Me in the Morning! a real-life guide for surviving morning sickness. She also receives
Honoria for presentations.
45