The Vegetarian Breastfeeding Mothers
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A collaborative of web resources of the vegetarian breastfeeding mothers. Targeting on diets plan during breastfeeding. Nutrients deficiency to a child and more insights.

A collaborative of web resources of the vegetarian breastfeeding mothers. Targeting on diets plan during breastfeeding. Nutrients deficiency to a child and more insights.

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The Vegetarian Breastfeeding Mothers The Vegetarian Breastfeeding Mothers Document Transcript

  • The Vegetarian Breastfeeding Mother Collaborate by Karen Ho, dated 16 August 2013
  • INDEX 2. Vitamin B12 and Vegetarian Diets • Vitamin B12 Deficiency • Digestion and absorption of Vitamin B12 • Vegetarians and Vitamin B12 status • Vegetarians infants and Vitamin B12 status • Vitamin B12 in the vegetarian diets • Vegetarian meal plan and food sources 1. Know Your Option. Know Your Right • Traditional After-Birth Care Theory and Nutrition • Case Study Valerie Lynn Post Pregnancy Wellness Coach Collaborate and prepare by Karen Ho, Interaction Designer, IT Medical Journal of Australia 3. A balanced vegetarian diest supports healthy breasfeeding • Calories Needs and Weigh Loss • High calorie, high nutrient foods • Fluids Needs • Meal plannning guidelines for breastfeeding vegetarians • Important nutrients Vegetarian Diets During Lactation
  • INDEX 5. The Vegetarian Breastfeeding Mothers • Vegan and Types of Vegan • Breastfeeding Mothers on vegan diets 4. Healthy eating for vegan pregnant and breastfeeding mothers Queensland Dietitians Last reviewed: June 2013 Leaders, USA 6. A balanced vegetarian diest supports healthy breasfeeding • Infants Formulas • Formula Milk and Soya Milk • The Best Diets for Breastfeeding • Weigh Loss and Milk Loss • Protein Requirement Vegan Baby and Children The Vegan Society 7. Breastfeeding Mothers and Fenugreek Breastfeeding and Herbs Collaborate and prepare by Karen Ho, Interaction Designer, IT
  • INDEX 9. Prenatal and Postnatal Care, Feeding and Dietary 8. Nutrient Adequacy of Exclusive Breastfeeding for the Term Infant During the First Six Month of Life World Health Organization Geneva WHO 2002 Pre-Post Natal Care 10. How much milk do my baby need? Estimating and Calculation of Expressed Milk Collaborate and prepare by Karen Ho, Interaction Designer, IT
  • Know your option, know your right Traditional After-Birth Care Theory and Nutrition By Choicesinchildbirth Valerie Lynn is American’s first Post-pregnancy Well- ness Coach and founder of the Post-pregnancy Well- ness Company. She is introducing an entirely new paradigm regard- ing after birth care in the United States based on Eastern influences. Her book, The Mommy Plan, Re- storing Your Post-pregnancy Body Naturally Using Women’s Tradi- tional Wisdom, is gaining global recognition in the child birth industry as she has explained core tenants of traditional after birth guidelines surrounding a mother’s diet, activities and personal care during the first 6-8 weeks after child birth. Valerie is the International Country Co- ordinator of Malaysia, for Postpartum Support International (PSI); and is on the Board of Advisors for the After Birth Project, a documentary- in-the-making on the lack of after birth support in the United States and the social effects. Valerie is the first foreigner, in Malaysia, to be university strained in traditional after birth care and is a practicing Tra- ditional Postpartum Practitioner. She offers training in traditional after birth care, herbal body treatments, massage and abdominal wrapping, and is the Sole US distributor of a unique traditional Postnatal Care Set. Resources: By Valerie Lynn, Author, The Mommy Plan This entry was posted on March 7, 2013 at 3:06 pm and is filed under Postpartum Health Website URL: http://choicesinchildbirth.wordpress.com/category/postpartum-health/
  • Know your option, know your right Traditional After-Birth Care Theory and Nutrition By Choicesinchildbirth Case Study: By Valerie Lynn, Author, The Mommy Plan In May 2007, I returned to the U.S. after living in Asia for ten years. That same month, I gave birth to my son, Jordan. I quickly realized that in the United States specific, structured care for mothers after delivery didn’t exist – and still doesn’t today. I’ve asked myself why this is the case many times over the years. Care during the first six weeks post-natally is deemed as a crucial healing period to at least three billion people around the globe. Why is this period not deemed as equally important in my own country, where we have at least 4 million births per year? I at- tribute this to the medicalization of birth and the diminished role of the midwife, beginning in the early 1900s. Our heritage of after-birth care has been lost. There is no longer an understanding of the transition of a woman’s body back to a non-pregnant state and the intense healing pro- cess that goes on in those first few weeks. The Humoral Theory of Medicine All after-birth traditions, practices, and guidelines are based on one of the oldest scientific theories in the world, the Humoral Theory of Medi- cine. According to this ancient theory, there are four conditions in the human body: hot, cold, moist, and dry, and they must remain in balance. The Humoral Theory of Pregnancy states that a woman’s body is out of balance and in a hot state while pregnant, as her body primarily func- tions as an incubator to support a growing and developing baby. The hot state is due to additional sources of heat, such as: raised level of hor- mones, baby’s body heat, the placenta and amniotic fluid, as well as a 50% increase in the volume of blood. All of these factors combine to raise a mother’s body temperature throughout pregnancy by 1-1.5°F. In fact, the first scientific pregnancy test was an elevated temperature for two weeks outside of the menstruation period. When a baby is born, a mother’s body temperature drops the same amount, 1-1.5°F below the normal body temperature. The decrease is due to the loss of heat sources, namely the baby’s body heat, the pla- centa, amniotic fluid, and blood, along with exhaustion from labor. At this time the mother’s body shifts into a cold state and the Humoral Theory of Medicine can be applied to the post-pregnancy period, when the body is again out of balance.
  • Know your option, know your right Traditional After-Birth Care Theory and Nutrition By Choicesinchildbirth Case Study: By Valerie Lynn, Author, The Mommy Plan Sustaining & Raising Body Temperature Traditional post-pregnancy recovery guidelines emphasize the impor- tance of raising a mother’s internal body temperature at a consistent pace over the six weeks after delivery. Therefore, all guidelines sur- rounding a mother’s diet and beverage intake, personal care, and activ- ity during this time are based on the notion that, due to the mother’s body being in a cold state, the remaining heat must be protected and maintained, ensuring no body heat escapes. In addition, a post-baby body has specific nutritional and energetic temperament needs than when it was in a pregnant state, which can be met by consuming nutrient dense healing foods. Heaty foods are Healing Foods A traditional after birth diet, whether from Asia, Latin America or else- where, is one where food is used as medicine to help accelerate the body’s natural healing capabilities. Since a mama’s body is in a cold state after delivery, only heaty foods should be consumed. The word ‘heaty’ refers to the capacity of a particular food, herb or spice to gener- ate a “hot sensation” and warming within the body. This is not to be con- fused with food being overly spicy, a taste sensation that provides a sharp spicy taste and causes sweating. That sort of heat is not good for a mama’s recovering body. Foods deemed as having a cold temperament should not be consumed during the healing period after delivery, as this may delay the natural in- crease in body temperature and shock the body’s digestive system. In turn, this could interrupt the healing process, lower body temperature further, and prolong the recovery process. Most vegetables are considered to have a cold temperament and theo- retically shouldn’t be consumed at this time. However, the coldness may be counteracted by the way the vegetables are prepared. For example, adding fresh ginger root while cooking makes vegetables “warm,” thus acceptable to eat and good for recuperation. A nutritious, wholesome, and natural diet should always be encouraged. However, even good foods can be trouble for the digestive system during the immediate post-pregnancy period due to the unique state of a mama’s body after delivery.
  • Know your option, know your right Traditional After-Birth Care Theory and Nutrition By Choicesinchildbirth Case Study: By Valerie Lynn, Author, The Mommy Plan Some of the traditional foods to avoid are nutritious and healthy such as broccoli, tomatoes and cauliflower. Please take note that it is only during the post-birth recovery period, when the body is in a weakened state, that specific foods should be avoided; by no means are they per- manent recommendations. Post-pregnancy Dietary Plan After childbirth you should continue to eat well. One hour after the pla- centa is birthed the body begins its transition back to a non-pregnant state. Over the first six weeks postpartum a mama’s body goes through an intense internal workout as a significant amount of healing takes place. Pregnancy is approximately 259 – 280 days or 37-40 weeks, and in just 42 days or six weeks, (medically speaking) the physical shrink- age of the perinatal organs is back to normal and most of the loss of re- tained water, fat, and gas takes place. This healing time equates to 15% of the total amount of time spent in a pregnant state. With this in mind, don’t you think a post-pregnancy dietary plan is just as important as a dietary plan during pregnancy? Three billion people around the globe do. By avoiding foods that interfere with the healing process you allow your body to have a stronger and more balanced recovery in a shorter period of time. Don’t Underestimate Traditional Post-Pregnancy Care The childbirth industry is in transition as more mothers are searching for ways to help speed up their recovery after childbirth. The United States is one of only four countries in the world that does not require employ- ers to provide paid maternity care. Women therefore need to return to work as soon as they are able. Western countries are no longer under- estimating the effectiveness of traditional post-pregnancy care, but trying to understand them. As women across the world are embracing more natural products and services into their lifestyles, western mamas are searching for natural ways to recover from childbirth. Post-pregnan- cy care that facilitates healing at a faster rate is becoming increasingly valued in modern cultures where women must resume their normal lives within weeks after delivery.
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 1/11 Advanced Search Clinical focus Vitamin B12 and vegetarian diets Carol L Zeuschner, Bevan D Hokin, Kate A Marsh, Angela V Saunders, Michelle A Reid and Melinda R Ramsay MJA Open 2012; 1 Suppl 2: 27-32. doi:10.5694/mjao11.11509 Abstract Vitamin B12 is found almost exclusively in animal-based foods and is therefore a nutrient of potential concern for those following a vegetarian or vegan diet. Vegans, and anyone who significantly limits intake of animal-based foods, require vitamin B12-fortified foods or supplements. Vitamin B12 deficiency has several stages and may be present even if a person does not have anaemia. Anyone following a vegan or vegetarian diet should have their vitamin B12 status regularly assessed to identify a potential problem. A useful process for assessing vitamin B12 status in clinical practice is the combination of taking a diet history, testing serum vitamin B12 level and testing homocysteine, holotranscobalamin II or methylmalonic acid serum levels. Pregnant and lactating vegan or vegetarian women should ensure an adequate intake of vitamin B12 to provide for their developing baby. In people who can absorb vitamin B12, small amounts (in line with the recommended dietary intake) and frequent (daily) doses appear to be more effective than infrequent large doses, including intramuscular injections. Fortification of a wider range of foods products with vitamin B12, particularly foods commonly consumed by vegetarians, is likely to be beneficial, and the feasibility of this should be explored by relevant food authorities. Vitamin B12 (cobalamin) is an essential vitamin, required for DNA synthesis (and ultimately cell division) and for maintaining nerve myelin integrity. It is found almost exclusively in animal-based products including red meats, poultry, seafood, milk, cheese and eggs. As vitamin B12 is produced by bacteria in the large intestines of animals, plant-based foods are generally not a source of vitamin B12. It is therefore a nutrient of concern for vegetarians and particularly for vegans who choose an entirely plant-based diet. A cross-sectional analysis study involving 689 men found that more than half of vegans and 7% of vegetarians were deficient in vitamin B12. Vitamin B12 deficiency Vitamin B12 deficiency is a serious health problem that can result in megaloblastic anaemia, inhibition of cell division, and neurological disorders. Folate deficiency can also cause megaloblastic anaemia and, although a high folate intake may correct anaemia from a vitamin B12 deficiency, subtle neurological symptoms driven by the vitamin B12 deficiency may arise. Loss of intrinsic factor, gastric acid or other protein-digesting enzymes contributes to 95% of known cases of vitamin B12 deficiency. Other factors that may contribute to vitamin B12 deficiency are listed in Box 1. However, in vegetarian and vegan populations, dietary insufficiency is the major cause. Furthermore, high levels of folate can mask vitamin B12 deficiency — a concern for vegetarians and vegans whose folate intake is generally high while vitamin B12 intake is low. The addition of vitamin B12 to any foods fortified with folate has been advocated to prevent masking of haematological and neurological manifestations of vitamin B12 deficiency. Subtle neurological damage (even in the absence of anaemia) may be more likely in vegans because of their increased folate levels preventing early detection of vitamin B12 deficiency. Vitamin B12 deficiency can also lead to demyelinisation of peripheral nerves, the spinal cord, cranial nerves and the brain, resulting in nerve damage and neuropsychiatric abnormalities. Neurological symptoms of vitamin B12 deficiency include numbness and tingling of the hands and feet, decreased sensation, difficulties walking, loss of bowel and bladder control, memory loss, dementia, depression, general weakness and psychosis. Unless detected and treated early, these symptoms can be irreversible. 1 2 3 4 13 4 14 4 3,4
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 2/11 Digestion and absorption of vitamin B12 The digestion of vitamin B12 begins in the stomach, where gastric secretions and proteases split vitamin B12 from peptides. Vitamin B12 is then free to bind to R-factor found in saliva. Pancreatic secretions partially degrade the R-factor, and vitamin B12 is then bound to intrinsic factor. Intrinsic factor binds to the ileal brush border and facilitates the absorption of vitamin B12. Box 2 illustrates the process of vitamin B12 digestion and absorption. Vitamin B12 absorption may decrease if intrinsic factor production decreases. There are many well documented factors causing protein-bound vitamin B12 malabsorption, including gastric resection, atrophic gastritis, and the use of medications that suppress acid secretion (see Box 1). Up to 89% of vitamin B12 consumed in the diet is absorbed, although as little as 9% is absorbed from some foods (including eggs). This relatively high rate of absorption, combined with low daily requirements and the body’s extremely efficient enterohepatic circulation of vitamin B12, contributes to the long period, often years, for a deficiency to become evident. Studies have been inconsistent in linking the duration of following an unsupplemented vegan diet with low serum levels of vitamin B12. Intestinal absorption is estimated to be saturated at about 1.5–2.0 µg per meal, and bioavailability significantly decreases as intake increases. Ageing causes a decreased level of proteases, as well as a reduced level of acid in the stomach. As a result, vitamin B12 is less effectively removed from the food proteins to which it is attached, and food-bound vitamin B12 absorption is diminished. The Framingham Offspring Study found that the vitamin B12 from supplements and fortified foods may be more efficiently absorbed than that from meat, fish and poultry. While low vitamin B12 status in vegetarians and vegans is predominantly due to inadequate intake, some cases of pernicious anaemia are attributable to inadequate production of intrinsic factor. Under the law of mass action, about 1% of vitamin B12 from large oral doses can be absorbed across the intestinal wall, even in the absence of adequate intrinsic factor. Assessing vitamin B12 status Taking a simple diet history can be a useful indicator of vitamin B12 intake and adequacy. However, laboratory analyses provide a much more accurate assessment. Measurement of serum vitamin B12 levels is a common and low-cost method of assessing vitamin B12 status. The earlier method of measuring vitamin B12 using biological assays was unreliable, as both the active and inactive analogues of vitamin B12 were detected, so levels were often overestimated. Modern radio isotope and immunoassay methods reliably measure biologically available analogues of vitamin B12. The early measured ranges of acceptable levels of serum vitamin B12 were determined using individuals who were apparently healthy but had potentially marginal levels of vitamin B12. This has resulted in reference intervals probably being set too low to provide a reliable clinical decision. To improve the ability to predict marginal vitamin B12 status, a higher reference interval (> 360 pmol/L) has been proposed. Objective measures of neurological damage have been found in patients with vitamin B12 levels below 258 pmol/L. However, the usual reference interval for vitamin B12 deficiency is < 220 pmol/L. Achieving national and international agreement on the definition of serum vitamin B12 deficiency would provide some clarity for comparison of studies and reduce variability in defining those at risk of deficiency. Internationally, the cut-off for vitamin B12 varies markedly between < 130 pmol/L and < 258 pmol/L. Serum vitamin B12 levels alone do not provide a measure of a person’s reserves of the vitamin. It is recommended that a metabolic marker of vitamin B12 reserves, such as serum homocysteine, also be determined. Elevated homocysteine levels can be a useful indicator for vitamin B12 deficiency, because serum homocysteine levels increase as vitamin B12 stores fall. While serum homocysteine levels greater than 9 µmol/L suggest the beginning of depleted vitamin B12 reserves, standard laboratory reference intervals suggest levels greater than 15 µmol/L as a marker for depleted vitamin B12 reserves. Although homocysteine levels may also increase with folate or vitamin B6 deficiency, these deficiencies are likely to be rare in vegetarians and vegans. Other markers for vitamin B12 deficiency include serum holotranscobalamin II (TC2) and urinary or serum methylmalonic acid (MMA). TC2 is the protein that transports vitamin B12 in blood, and its levels fall in vitamin B12 deficiency. Testing for this carrier protein can identify low vitamin B12 status before total serum vitamin B12 levels drop. Vitamin B12 is the only coenzyme required in the conversion of methylmalonyl-CoA to succinyl-CoA, so methylmalonyl-CoA levels increase with vitamin B12 deficiency. As it is toxic, methylmalonyl-CoA is converted to MMA, which accumulates in the blood and is excreted in the urine, enabling either urinary or serum MMA to be a useful measure of vitamin B12 reserves. Because TC2 15 17,18 2,19 18 4 20 21 17 4,22 23 24 25 Need website help? Contact us now!
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 3/11 is one of the earliest markers of vitamin B12 deficiency, it may be one of the better means of assessing vitamin B12 status. Requirements Box 3 shows the vitamin B12 nutrient reference values for Australia and New Zealand. As no recommended dietary intakes (RDIs) are available for infants under 12 months of age, an adequate intake is recommended instead. Vegans at all stages of the life cycle need to ensure an adequate and reliable source of vitamin B12 from fortified foods, or they will require supplementation equivalent to the RDI. Vegetarians and vitamin B12 status While reported cases of frank vitamin B12 deficiency in vegetarians or vegans are rare, several studies have found lower vitamin B12 levels in vegans and vegetarians compared with the general population. The European Prospective Investigation into Cancer and Nutrition (EPIC)-Oxford cohort study found that 121 of 232 vegans (52%), 16 of 231 vegetarians (7%) and one of 226 omnivores (0.4%) were classed as vitamin B12-deficient. There was no significant association between age or duration of subjects’ adherence to a vegetarian or vegan diet and the serum levels of vitamin B12. Intuitively, it is assumed that prevalence of deficiency increases with a longer duration of vegetarian diet. Although it can take years for deficiency to occur, it is likely that all vegans and anyone who does not regularly consume animal- based foods, and whose diets are unsupplemented or unfortified, will eventually develop vitamin B12 deficiency. Vegetarians and vegans should have their vitamin B12 status regularly assessed to enable early intervention if levels fall too low. Vegetarian infants and vitamin B12 status The risk of a breastfed infant becoming deficient in vitamin B12 depends on three factors: the vitamin B12 status of the mother during pregnancy; the vitamin B12 stores of the infant at birth; and the vitamin B12 status of the breastfeeding mother. The fetus obtains its initial store of vitamin B12 via the placenta, with newly absorbed vitamin B12 (rather than maternal stores) being readily transported across the placenta. Under normal conditions, full-term infants will have enough stored vitamin B12 at birth to last for about 3 months when the maternal diet does not contain vitamin B12. An infant born to a vegetarian or vegan mother is at high risk of deficiency if the mother’s vitamin B12 intake is inadequate and her stores are low. Vegetarian women who have repeated pregnancies place infants at greater risk, because their vitamin B12 stores are likely to have been depleted by earlier pregnancies. Vegetarian or vegan women must have a balanced diet, including adequate intake of vitamin B12, to provide for their babies during both pregnancy and lactation. Recent studies suggest that maternal stores of vitamin B12 are also reflected in breastmilk. When maternal serum vitamin B12 levels are low, vitamin B12 levels in breastmilk will also be low, and the infant will not receive an adequate vitamin B12 intake. There have been reports of deficiency in the breastfed infants of vegan (or “strict vegetarian”) mothers who did not supplement their diets with vitamin B12, because of the smaller stores of vitamin B12 gained by the infant during pregnancy and the low vitamin B12 content of breastmilk (reflective of the mothers’ serum levels). Infants have presented with a range of symptoms, often initially signalled by developmental delay. Lack of vitamin B12 in the maternal diet during pregnancy has been shown to cause severe retardation of myelination in the nervous system of the infant. Visible signs of vitamin B12 deficiency in infants may include involuntary motor movements, dystrophy, weakness, muscular atrophy, loss of tendon reflexes, psychomotor regression, cerebral atrophy, hypotonia and haematological abnormalities. While supplementation with vitamin B12 results in rapid improvements in laboratory measures of vitamin B12 status, there is continuing research about the long-term effects of deficiency in infants. Vitamin B12 in the vegetarian diet Lacto-ovo-vegetarians will have a reliable source of vitamin B12 in their diet, provided they consume adequate amounts of dairy products and eggs, although their intake is likely to be lower than in meat eaters. However, those who follow a vegan diet will not have a reliable intake unless they consume foods fortified with vitamin B12 or take a supplement. It was once thought that some plant foods, such as spirulina, and fermented soy products, including tempeh and miso, were dietary sources of vitamin B12, but this has been proven incorrect. Recent research has found traces of vitamin B12 in white button mushrooms and Korean purple laver (nori), but the quantity in a typical serving means that they are not a significant dietary source of this vitamin. An average serving of mushrooms contains about 5% of the RDI, making the quantity required to supply adequate amounts of vitamin B12 to vegetarians impractical. Further, use of 22 26 27,28 2 2 29 30 31 32 33,34 35 36 37,38 37 39 40 41 40,41
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 4/11 Korean laver is unlikely to be widespread in the Australian diet. With the unique exception of these two plant foods, any vitamin B12 detected in other plant foods is likely to be the inactive analogue, which is of no use to the body and can actually interfere with the absorption of the active form. Box 4 shows a sample vegetarian meal plan for a 19–50-year-old woman, which includes food sources typical in a Western-style diet and meets the RDI of vitamin B12 and requirements for other key nutrients (except vitamin D and long- chain omega-3 fatty acids). Excluding or limiting dairy foods or fortified soy milk from the vegetarian diet would necessitate the need for vitamin B12 supplements. Fortified foods In contrast to the United States, where foods are extensively fortified with vitamin B12, Food Standards Australia New Zealand permits only a limited number of foods to be fortified with vitamin B12. This includes selected soy milks, yeast spread, and vegetarian meat analogues such as soy-based burgers and sausages. Examples of the vitamin B12 content of foods suitable for vegetarians are shown in Box 5. Vitamin B12 added to foods is highly bioavailable, especially in people with vitamin B12 deficiency caused by inadequate dietary intake. An unpublished Australian study (Hokin BD. Vitamin B12 deficiency issues in selected at-risk populations [PhD thesis]. Newcastle: University of Newcastle, 2003) compared the effectiveness of fortified soy milk (two servings of 250 mL/day), soy-based meat analogues (one serving/day), vitamin B12 supplements (one low-dose tablet/day or one high-dose tablet/week) and vitamin B12 intramuscular injections (one injection/month) in raising serum vitamin B12 levels in subjects with deficiency. The study found that fortified foods were superior to the traditional methods of supplementation (intramuscular injections and tablets). Further research would be beneficial to confirm these findings. With inadequate dietary intake being a risk for vegetarians and vegans, further fortification of foods commonly consumed by this population with vitamin B12 would be beneficial and should be considered by the relevant authorities. Supplements In a vegan diet, using a supplement or consuming fortified foods is the only way to obtain vitamin B12. As the body can only absorb a limited amount of vitamin B12 at any one time, it is better to take small doses more often, instead of large doses less often. One study found that small doses of vitamin B12 in the range of 0.1–0.5 µg resulted in absorption ranging between 52% and 97%; doses of 1 µg and 5 µg resulted in mean absorption of 56% and 28%, respectively, while higher doses had even lower absorption, with 10 µg and 50 µg doses resulting in 16% and 3%, respectively, being absorbed. While sublingual supplements are often promoted as being more efficiently absorbed, there is no evidence to show that this form of supplement is superior to regular oral vitamin B12. Vitamin B12 supplements are not made from animal-based products and are suitable for inclusion in a vegan diet. Conclusion Vitamin B12 deficiency is a potential concern for anyone with insufficient dietary intake of vitamin B12, including those adhering to a vegan or vegetarian diet or significantly restricting animal-based foods. Studies have found that vegetarians, particularly vegans, have lower serum vitamin B12 levels, and it is likely that anyone avoiding animal-based foods will eventually become deficient if their diet is not supplemented. All vegans, and lacto-ovo-vegetarians who don’t consume adequate amounts of dairy products or eggs to provide sufficient vitamin B12, should therefore supplement their diet with vitamin B12 from fortified foods or supplements. It is particularly important that pregnant or breastfeeding vegan and vegetarian women consume a reliable source of vitamin B12 to reduce the risk of their baby developing a vitamin B12 deficiency. 40,41 42 17 44 Box 1 – Causes of vitamin B12 deficiency, with contributing factors (#) Inadequate dietary intake Restrictive diet or dieting; vegetarian or vegan diets without supplementation or use of fortified foods Inadequate absorption or impaired utilisation Loss of intrinsic factor, loss of gastric acid and/or other protein-digesting enzymes (contributes to 95% of known cases) Use of medications that suppress acid secretion, including somatostatin, cholecystokinin, atrial natriuretic peptide, 4 5
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 5/11 and nitric oxide Pancreatic disease Gastric resection, sleeve or banding surgery Ileal disease or ileal resection (secondary to Crohn’s disease) Use of metformin (oral hypoglycaemic agent) Use of angiotensin-converting enzyme inhibitor Use of levodopa and catechol-O-methyltransferase inhibitors Autoimmunity to intrinsic factor Gastric infection with Helicobacter pylori Ileocystoplasty Atrophic gastritis Increased requirements During pregnancy and lactation Increased excretion Alcoholism 5 6 7 6 9 10 11 12 Box 2 – Diagram illustrating vitamin B12 digestion and absorption (#)15 ,16 Box 3 – Recommended dietary intake (RDI)* and estimated average requirement (EAR) of vitamin B12 per day (#) † 26 Sex and age group RDI EAR Men = 19 years 2.4 µg 2.0 µg Women = 19 years 2.4 µg 2.0 µg Pregnant women 2.6 µg 2.2 µg Lactating women 2.8 µg 2.4 µg
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 6/11 Children 0–6 months 0.4 µg 7–12 months 0.5 µg 1–3 years 0.9 µg 0.7 µg 4–8 years 1.2 µg 1.0 µg 9–13 years 1.8 µg 1.5 µg 14–18 years 2.4 µg 2.0 µg * The RDI is the average daily dietary intake level that is sufficient to meet the nutrient requirements of nearly all healthy individuals (97%–98%) of a particular sex and life stage. The EAR is a daily nutrient level estimated to meet the requirements of half the healthy individuals of a particular sex and life stage. These values are adequate intakes, which are the average daily nutrient intake levels based on observed or experimentally determined approximations or estimates of nutrient intake by a group (or groups) of apparently healthy people that are assumed to be adequate. ‡ ‡ † ‡ Box 4 – A sample vegetarian meal plan designed to meet requirements for vitamin B12 and other key nutrients for a 19–50-year-old woman, showing vitamin B12 content of the foods* (#) Meal Vitamin B12 content Breakfast Bowl of cereal with fruit, and poached egg on toast 2 wholegrain wheat biscuits 0.0 µg 4 strawberries 0.0 µg 10 g chia seeds 0.0 µg 1/2 cup low-fat fortified soy milk (or dairy milk) 0.5 µg (0.8 µg) 1 slice multigrain toast 0.0 µg 1 poached egg 0.9 µg Snack Nuts and dried fruit 30 g cashews 0.0 µg 6 dried apricot halves 0.0 µg Lunch Chickpea falafel wrap 1 wholemeal pita flatbread 0.0 µg 1 chickpea falafel 0.0 µg 30 g hummus 0.0 µg 1/2 cup tabouli 0.0 µg Salad 0.0 µg †
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 7/11 Provenance: Commissioned by supplement editors; externally peer reviewed. Snack Banana and wheatgerm smoothie 3/4 cup low-fat fortified soy milk (or dairy milk) 0.8 µg (1.1 µg) 2 teaspoons wheatgerm 0.0 µg 1 banana 0.0 µg Dinner Stir-fry greens with tofu and rice 100 g tofu 0.0 µg 2 spears asparagus, 1/3 cup bok choy and 25 g snow peas 0.0 µg 1 cup cooked brown rice 0.0 µg Snack Fortified malted chocolate beverage 1 cup low-fat fortified soy milk (or dairy milk) 1.0 µg (1.5 µg) 10 g malted chocolate powder 0.0 µg Total vitamin B12 3.2 µg (4.3 µg) * Source: FoodWorks 2009 (incorporating Food Standards Australia New Zealand’s AUSNUT [Australian Food and Nutrient Database] 1999), Xyris Software, Brisbane, Qld. Figures are for soy milk (dairy milk). † † † † Box 5 – Vitamin B12 content of lacto-ovo-vegetarian food sources* (#) Vegetarian sources Vitamin B12 per 100 g Sausage, vegetarian style, fortified 2.0 µg Cheese, cheddar, reduced fat (16%) 1.8 µg Egg (chicken), whole, poached 1.7 µg Milk, cow, fluid, regular or reduced fat 0.6 µg Soy beverage, unflavoured, regular fat, fortified 0.9 µg Soy beverage, unflavoured, reduced fat (1.5%), fortified 0.9 µg Soy beverage, unflavoured, low fat, (0.5%), fortified 0.3 µg Yoghurt dessert, regular fat, flavoured 0.2 µg * From Food Standards Australia New Zealand. NUTTAB 2010 online searchable database.43
  • 8/15/13 Vitamin B12 and vegetarian diets | Medical Journal of Australia https://www.mja.com.au/open/2012/1/2/vitamin-b12-and-vegetarian-diets 8/11 Correspondence: carol.zeuschner@sah.org.au (mailto:carol.zeuschner@sah.org.au) Acknowledgements: We acknowledge the assistance of dietitians Sue Radd and Rebecca Prior in the early development stages of this article. Competing Interests: Kate Marsh previously consulted for Nuts for Life (Horticulture Australia), who are providing a contribution towards the cost of publishing this supplement. Angela Saunders, Michelle Reid and Melinda Ramsay are employed by Sanitarium Health and Wellbeing, sponsor of this supplement. 1. Cameron DG, Townsend SR, English A. Pernicious anaemia II: maintenance treatment with crystalline vitamin B12. Can Med Assoc J 1954; 70: 398-400. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? cmd=Retrieve&db=PubMed&list_uids=13150272&dopt=Abstract) 2. Gilsing AM, Crowe FL, Lloyd-Wright Z, et al. Serum concentrations of vitamin B12 and folate in British male omnivores, vegetarians and vegans: results from a cross-sectional analysis of the EPIC-Oxford cohort study. Eur J Clin Nutr 2010; 64: 933-939. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=20648045&dopt=Abstract) 3. Allen RH, Stabler SP, Savage DG, Lindenbaum J. Metabolic abnormalities in cobalamin (vitamin B12) and folate deficiency. FASEB J 1993; 7: 1344-1353. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? cmd=Retrieve&db=PubMed&list_uids=7901104&dopt=Abstract) 4. Mangels R, Messina V, Messina M. The dietitians’ guide to vegetarian diets: issues and applications. 3rd ed. Sudbury, MA: Jones & Bartlett Learning, 2010. 5. Schubert ML. Gastric secretion. Curr Opin Gastroenterol 2007; 23: 595-601. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=17906434&dopt=Abstract) 6. Aarts EO, Janssen IM, Berends FJ. The gastric sleeve: losing weight as fast as micronutrients? Obes Surg 2011; 21: 207-211. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=21088925&dopt=Abstract) 7. Yakut M, Ustün Y, Kabaçam G, Soykan I. Serum vitamin B12 and folate status in patients with inflammatory bowel diseases. Eur J Intern Med 2010; 21: 320-323. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? cmd=Retrieve&db=PubMed&list_uids=20603044&dopt=Abstract) 8. De Jager J, Kooy A, Lehert P, et al. Long term treatment with metformin in patients with type 2 diabetes and risk of vitamin B-12 deficiency: randomised placebo controlled trial. BMJ 2010; 340: c2181. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=20488910&dopt=Abstract) 9. Tal S, Shavit Y, Stern F, Malnick S. Association between vitamin B12 levels and mortality in hospitalized older adults. J Am Geriatr Soc 2010; 58: 523-526. <PubMed> (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? cmd=Retrieve&db=PubMed&list_uids=20158555&dopt=Abstract) 10. Triantafyllou NI, Kararizou E, Angelopoulos E, et al. The influence of levodopa and the COMT inhibitor on serum vitamin B12 and folate levels in Parkinson’s disease patients. Eur Neurol 2007; 58: 96-99. <PubMed> Carol L Zeuschner, BSc, MSc, APD, Manager of Nutrition and Dietetics Bevan D Hokin, BSc, MAppSc, PhD, Director of Pathology Kate A Marsh, AdvAPD, MNutrDiet, PhD, Director and Senior Dietitian Angela V Saunders, BS(Dietetics), MA(Ldshp&Mgmt–HS), APD, Senior Dietitian, Science and Advocacy Michelle A Reid, BND, APD, AN, Senior Dietitian, Nutrition Marketing Melinda R Ramsay, BMedSci, MNutrDiet, APD, Project Coordinator 1 Sydney Adventist Hospital, Sydney, NSW. 2 Northside Nutrition and Dietetics, Sydney, NSW. 3 Corporate Nutrition, Sanitarium Health and Wellbeing, Berkeley Vale, NSW. 4 Sanitarium Health and Wellbeing Services, Sanitarium Health and Wellbeing, Sydney, NSW. 1 1 2 3 3 4
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  • Vegetarian Diets During Lactation RD Resources for Consumers: A balanced vegetarian diet supports healthy breastfeeding. Lower levels of environmental toxins are found in milk from women who follow a vegetarian diet. Breastfed children of well-nourished vegetarian mothers grow and develop normally. Benefits of Breastfeeding Breast milk is best. It provides all the nutrients a growing infant needs in the most digestible form. Breastfeeding is free, convenient and supports mother-child bonding. The most benefits are gained when children are breastfed for at least the first 6 months after birth. Children build stronger immune systems, suffer from less allergies, and have reduced risk of obesity later in life. Mothers reduce their risk of some cancers, and type 2 diabetes. Calorie Needs and Weight Loss The body uses extra calories when producing breast milk. Increased calorie needs are based on the amount of milk produced. On average, women use 330 more calories each day for the first 6 months of breastfeeding. During the second 6 months, they use an additional 400 calories. While this will aid in healthy weight loss after pregnancy, extra calorie intake will also be needed. To meet higher calorie needs, consume plenty of whole-grains, fruits, vegetables, legumes, nuts, and seeds. Visit http://www.mypyramid.gov/mypyramidmoms/ breastfeeding_weight_loss.html for more information. Tandem Nursing When a woman nurses two children of different ages it is called“tandem nursing.”Producing milk for two children requires more calories and nutrients than needed to feed one. High calorie and high nutrient foods in snacks and meals provide good sources of additional calorie intake. Remaining hydrated, by drinking extra water, is also highly recommended. High calorie, High nutrient foods • Avocado • Nuts & nut butters • Seeds & seed butters • Dried fruits • Full-fat soy products • Bean spreads • Fruit juices 300-Calorie Snack Ideas • Whole-grain toast with 1½ tbsp. almond butter topped with sliced banana and strawberries • ½ cup hummus with 1 cup of raw carrots and bell peppers • Fruit smoothie with 1 cup frozen mango, ½ cup frozen pineapple, 1 cup soymilk • ¼ cup guacamole with 1/3 cup baked tortilla chips • ¼ cup of trail mix Fluid Needs Fluid needs increase while breastfeeding, therefore staying hydrated is key. Drink water throughout the day and while nursing. Low-fat or non-fat milk, 100% fruit juices, and soups are also good sources of fluid. tip
  • Important Nutrients Protein (.59 g/lb.) Example: A woman who weighs 150 lbs. would need approximately 89 g of protein per day (150 lbs x .59 g/lb = 88.5 g) • Dried beans • Tofu & Tempeh • Nuts & nut butters • Eggs • Soymilk • Whole-grains • Dairy products Omega-3 Fatty Acid-DHA • Eggs from chickens fed a DHA-rich diet • Foods fortified with microalgae-derived DHA Vegetarian & Vegan-friendly DHA supplements may be used. Vitamin B12 (2.6 mcg/day) • Fortified cereals • Fortified soymilk • Vitamin B12-fortified nutritional yeast • Milk and yogurt • Eggs Calcium (1,000 mg/day) • Fortified soymilk or rice milk • Dairy products • Calcium-set tofu • Some dark green leafy vegetables (e.g. broccoli, kale, collard greens, bok choy) • Soybeans • Almonds • Figs • Fortified orange juice Vitamin D (200 IU/day) • Cow’s milk • Fortified cereals • Vitamin D-fortified soymilk • Skin exposure to sunlight Breastfed infants should be given a 400 IU vitamin D supplement daily. tip tip RD Resources are a project of the Vegetarian Nutrition Dietetic Practice Group. More topics available at www.VegetarianNutrition.net. Professional resources also available for members at www.VNDPG.org. © 2010 by VN DPG. Written by: Christine Creighton, MS, RD Expires April 2015. RD Resources for Consumers: Vegetarian Diets During Lactation Choose high calcium foods from each of the food groups (e.g. calcium-fortified breakfast cereals, bok choy, broccoli, collards, Chinese cabbage, kale, mustard greens, okra, calcium-fortified orange juice, dairy products, calcium-fortified soy milk, tempeh, calcium-set tofu, almonds). tip Resources MyPyramid for Pregnancy & Breastfeeding, http://www.mypyramid.gov/mypyramidmoms/ index.html Raising Vegetarian Children by Joanne Stepaniak and Vesanto Melina Simply Vegan, 4th ed. by Debra Wasserman and Reed Mangels The Vegetarian Mother’s Cookbook by Cathe Olson Meal Planning Guidelines for Breastfeeding Vegetarians Food Group Grains Vegetables Fruits Legumes, nuts, seeds, milks Fats # of Svgs. 6 4 2 7 2 Serving Size 1 slice bread; ½ cup cooked cereal or pasta; ¾ - 1 cup ready-to-eat cereal ½ cup cooked vegetables; 1 cup raw vegetables; ¾ cup vegetable juice ½ cup canned fruit; 1 medium fruit; ¾ cup fruit juice ½ cup cooked beans, tofu, tempeh, textured vegetable protein (TVP); 3 ounces meat analog; 2 tbsp. nuts, seeds, nut or seed butter; 1 cup fortified soy or rice milk; 1 cup cow’s milk; 1 cup yogurt 1 tsp. oil or margarine Comments Choose whole or enriched grains Choose these calcium-rich foods often: dark green leafy vegetables (kale, collards, and mustard greens), broccoli, bok choy, Chinese cabbage, okra Choose these calcium-rich foods often: calcium- fortified juice, figs Choose these calcium-rich foods often: calcium- fortified soymilk, cow’s milk, yogurt, calcium-set tofu, almond butter, tahini, tempeh, almonds, cheese, soybeans The MyPyramid for Pregnancy and Breastfeeding Web site (www.mypyramid.gov/tips_resources/vegetarian_diets.html) provides meal plans that can be adapt for breastfeeding women who follow lacto-ovo and lacto vegetarian diets. MyPyramid for Pregnancy and Breastfeeding offers limited information for women following vegan diets. The following meal plan can be used for pregnant vegans. These guidelines are the suggested minimum number of servings for breastfeeding women. Some women may need additional servings and/or added fats to maintain desirable body weight.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Healthy eating for vegan pregnant and breastfeeding mothers Healthy eating is important at all stages of life, especially during pregnancy. Your choices of what to eat and drink at this time can affect your health and the health of your baby for many years to come. A well planned vegan diet is able to meet nutrition requirements for pregnancy and breastfeeding. There is only a small increase in the amount of food you need to eat while you are pregnant. However, you do need more of certain nutrients, so it is very important that you make good choices for a nutritious diet. This is important so you and your baby get all you need for healthy growth and a healthy pregnancy. Healthy eating is important when you are breastfeeding. Your body has a greater need for most nutrients. Some of the extra energy required for breastfeeding comes from body fat stored during pregnancy. To meet your extra nutrient needs, it is important to eat a variety of nutritious foods. Your daily food group requirements during pregnancy and breastfeeding are outlined in the table on the next page. Use the numbers in the middle column to guide how many serves to eat from each food group per day. One serve is equal to each of the foods in the column on the right. For example, one serve of fruit is equal to 2 small plums. One serve of grain (cereal) foods is equal to ½ cup of cooked pasta.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Food Group Number of Serves 1 serve Vegetables and legumes/ beans Pregnant 5 Breast Feeding 7½ ½ cup cooked green or orange vegetables (e.g. broccoli, carrot, pumpkin or spinach) ½ cup cooked, dried or canned beans, chickpeas or lentils (no added salt) 1 cup raw leafy green vegetables ½ medium potato, or other starchy vegetable (sweet potato, taro, or cassava) ½ cup sweet corn 75 g other vegetables e.g. 1 small- medium tomato Fruit Pregnant 2 Breast Feeding 2 1 piece medium sized fruit (e.g. apple, banana, orange, pear) 2 pieces smaller fruit (e.g. apricot, kiwi fruit, plums) 1 cup diced, cooked or canned fruit ½ cup 100% juice 30 g dried fruit (e.g. 1½ tbsp sultanas, 4 dried apricot halves) Grain (cereal) foods Pregnant 8½ Breast Feeding 9 1 slice of bread ½ medium bread roll or flat bread ½ cup cooked rice, pasta, noodles, polenta, quinoa, barley, porridge, buckwheat, semolina, cornmeal ⅔ cup breakfast cereal flakes ¼ cup muesli 3 crisp breads 1 crumpet or 1 small English muffin or scone Nuts, seeds and legumes Pregnant 3½ Breast Feeding 2½ 1 cup (170 g) cooked dried beans, lentils, chickpeas, split peas, canned beans 170 g tofu 1/3 cup (30 g) unsalted nuts, seeds or paste, no added salt Dairy alternatives Pregnant 2½ Breast Feeding 2½ 1 cup (250 ml) calcium fortified soy milk 200 g (3/4 cup) calcium fortified soy yoghurt 2 (40 g) slices of soy cheese Additional serves for taller or more active women 0–2½ 3–4 sweet biscuits 30 g potato crisps 2 scoops soy ice-cream 1 Tbsp (20 g) dairy-free butter, margarine, oil
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Protein Pregnant or breastfeeding women should aim to include protein sources at each meal such as nuts, seeds, soy products and dried beans and peas. Folate or Folic acid during pregnancy Folate (or folic acid) is needed for the growth and development of your baby. It is especially important in the month before you fall pregnant and the first trimester (three months) of pregnancy. A good intake of folate reduces the risks of your baby being born with some abnormalities such as spina bifida (a disorder where the baby’s spinal cord does not form properly). Dietary sources high in folate include green vegetables such as broccoli, spinach and salad greens, some fruits and fortified cereals. All women planning a pregnancy and in the early stages of pregnancy should eat a variety of folate-containing foods (e.g. green leafy vegetables such as spinach, broccoli, bok choy, and foods fortified with folic acid— fruit juice, bread, breakfast cereal). You should also take a folic acid supplement of 400 micrograms per day at least one month before and three months after you become pregnant. Iron during pregnancy Iron is needed to form the red blood cells for you and your baby. It helps carry oxygen in your blood and is needed for your baby to grow. During pregnancy you need a lot more iron than when you are not pregnant so for women who follow a vegan diet an iron supplement is highly recommended. Good sources of additional dietary iron are legumes, (e.g. beans, peas, lentils) dark green vegetables, dried fruits, nuts, fortified soy milks, breakfast cereals and wholemeal breads. Vitamin C will help its absorption, so combine it with citrus fruit, berries, juice or tomato. Talk to your dietitian or midwife to make sure you are getting enough iron from your diet. What you eat or drink can stop your body using iron from your diet. You should limit your intake of these. They include: • drinking tea or coffee with meals • eating more than 2 tablespoons of unprocessed bran. You can help your body get iron from the food you eat or drink by: • including vitamin C with meals (e.g. citrus foods, tomato, capsicum) • using antacids sparingly.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Iodine Adequate iodine in pregnancy is essential for your baby’s growth and brain development. Iodine is needed in higher amounts during pregnancy. It is now recommended that all pregnant women should take a supplement containing 150 micrograms of iodine. You still need to consume good food sources of iodine in addition to this supplement. These food sources include: - iodised salt (look for green label) - bread with added iodine - fortified margarine. Fluid When you are breastfeeding you need more to drink to replace the fluid used in breast milk (~700 ml/day). It is a good idea to have a drink, such as a glass of water or fat reduced milk (within your nutrition needs) every time your baby feeds. You will also need to drink more fluid at other times during the day too. Multivitamin supplements A folate supplement is important during the first trimester of pregnancy. You may also need to take an iron supplement if your iron levels are low. However, a multivitamin during pregnancy is not necessary unless you do not have a balanced diet – compare what you are eating with the table on the first page of this sheet. If you choose to take a vitamin or mineral supplement during pregnancy, choose one that is specifically designed for pregnancy. Always check with your doctor before taking any supplements as an excessive intake of these can be harmful and reduce the absorption of other nutrients. Calcium Calcium fortified soy products are important to meet calcium requirements whilst pregnant. Also include tofu, almonds, sesame seeds and tahini. Vitamin B12 Significant amounts of B12 are usually found in animal products, so your intake will be limited. A good amount can be consumed by having at least two serves of soy milk fortified with B12 daily. Food fermented by micro-organisms (soy sauce, miso, tempeh), manure-grown mushrooms, spirulina and yeast may contain small amounts of vitamin B12, but this is not sufficient to meet your requirements for vitamin B12. Discuss your vitamin B12 levels and requirements with your doctor or midwife.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Zinc Good sources for vegans include beans and lentils, yeast, nuts, seeds and wholegrain cereals. Pumpkin seeds provide one of the most concentrated vegan food sources of zinc. Weight Gain The amount of weight to gain during pregnancy will depend on what your weight was before you became pregnant. Your midwife or dietitian will be able to calculate your body mass index (BMI) (a measure of your weight for height) to help you work this out. If your pre-pregnancy BMI was… You should gain… Less than 18.5 kg/m² 18.5 to 24.9 kg/m² 25 to 29.9 kg/m² Above 30 kg/m² 12½ to 18kg 11½ to 16kg 7 to 11½ kg 5 to 9kg As well as having an overall weight gain goal for your pregnancy, there is a trimester by trimester guideline to follow, as well. How much should I gain in my first trimester? All women can expect to gain one or two kilograms in the first three months of pregnancy. How much should I gain in my second and third trimesters? This depends on your pre-pregnancy BMI. Refer to the table below to see your goal. If your pre-pregnancy BMI was… You should gain… Less than 18.5 kg/m² ½ kg/week 18.5 to 24.9 kg/m² 400g/week Above 25kg/m² Less than 300g/ week It is important to keep your weight gain in this range for both your health and the health of your baby. Not gaining enough weight means your baby may miss out on some important nutrients. This can cause problems later in life. Insufficient weight gain is also linked with preterm birth. Gaining too much weight during pregnancy can also cause problems such as high blood pressure, gestational diabetes, complications in delivery, and longer hospital stays for you or your baby. These problems can be harmful to both you and your baby.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Food safety during pregnancy Hormonal changes during pregnancy may make your immune system weaker. This can make it harder to fight infections. Foods are sometimes a source of infections so protecting yourself from food poisoning is important. Listeria Listeria is a bacteria found in some foods, which can cause an infection called listeriosis. If passed on to your unborn baby it can cause premature birth, miscarriage or damage. The risk is the same through your whole pregnancy. Always keep your food ‘safe’ by: • Choose freshly cooked and freshly prepared food. • Thawing food in the fridge or defrosting food in the microwave. • Cooling left over food in the fridge rather than the bench. • Wash your hands, chopping boards and knives after handling raw foods. • Make sure hot foods are hot (above 60 degrees Celsius) and cold foods are cold (below 5 degrees Celsius), both at home and when eating out. • Make sure all food is fresh, used within the used-by date. • Eat left overs within 24 hours and reheat foods to steaming hot. • Heat leftovers to above 74 degrees for over 2 minutes. • Never re-freeze food once it has been thawed. • Ready-to-eat salads (from salad bars, buffets, supermarkets etc.) are foods that may contain Listeria and should be avoided. Some other bacteria and parasites can be harmful to your unborn baby. In addition to the precautions above: • Wear gloves when gardening and wash hands afterwards. • Avoid contact with cats and use gloves when handling cat litter (cats can be a source of Toxoplasmosis– a serious infection that can cause defects or death in your baby).
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Special Considerations during Pregnancy Caffeine During pregnancy caffeine takes longer to break down in your body. Generally 2–3 cups of coffee or up to 4 cups of tea a day are okay, but decaffeinated drinks are a better alternative. Try to limit your intake of caffeine containing drinks and foods. Alcohol Alcohol crosses the placenta and can lead to physical, growth and mental problems in babies. There is no known safe level of alcohol consumption during pregnancy. The safest option is not to drink during your pregnancy. Nausea and vomiting Many women suffer from sickness, usually in early pregnancy. Morning sickness is usually caused by the hormonal changes of pregnancy, and can affect you at any time of the day. By the end of the 4th month of pregnancy, symptoms usually disappear or become much milder. Some tips to help morning sickness: • Eat small amounts every two hours — an empty stomach can cause nausea. • Avoid smells and foods that make your sickness worse. • Eat more nutritious carbohydrate foods: try dry toasts or crackers, breakfast cereals and fruit. • Eat less fatty and sugary foods. Heartburn Heartburn, or reflux, is a burning feeling in the middle of the chest that can also affect the back of the throat. It is caused when acid moves from the stomach, back up the oesophagus. This happens because hormonal changes during pregnancy relax stomach muscles, and also because as the baby grows, more pressure is put on your stomach. Some tips to reduce heartburn: • eat small regular meals more often • avoid fatty, fried or spicy foods • avoid tea, coffee, cola drinks, chocolate drinks and alcohol • sit up straight while eating • do not bend after meals or wear tight clothes • sleep propped up on a couple of pillows.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Constipation Constipation is common during pregnancy. Hormone changes may relax the muscles in your bowel, which together with pressure from the growing baby can slow down your bowel movements. It is important to have enough fibre, fluid and exercise to avoid constipation. Good sources of dietary fibre include; vegetables, fruit, wholegrain and high fibre breakfast cereals, wholegrain bread, nuts, seeds and legumes. Water is the best drink. Now that you are up to date on healthy eating for yourself you need to start thinking about nutrition for you baby when he or she arrives. Mothers & Babies are designed for Breastfeeding Breastfeeding is the natural, normal way to feed your baby. Breastmilk is a complex food. It changes to meet the particular needs of each child from the very premature baby to the older toddler. Food for Health Breastfeeding has an amazingly positive effect on the health of both mothers and babies. For this reason, the World Health Organisation (WHO) and the Australian Department of Health recommend that all babies are breastfed exclusively (ie. no other food or drinks) for around the first 6 months and then continue to receive breastmilk (along with complementary food and drink) into the child’s 2nd year and beyond. Research shows that the longer the breastfeeding relationship continues, the greater the positive health effects. Breastmilk provides: Protection for baby from infections such as ear, stomach, chest and urinary tract; diabetes, obesity, heart disease, some cancers, some allergies and asthma. Protection for mother from breast and ovarian cancers, osteoporosis and other illnesses. Healthier communities & environment.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Preparing to Succeed Research shows that nearly all of women are able to meet the breastmilk needs of their babies. Ask the midwife to put your baby skin to skin on your chest as soon as possible after birth. Take the midwife up on her offer to help your baby lead attachment to your breast. Talk to your family, friends and workplace about your decision to breastfeed so they are ready to support you once your baby has arrived. Avoiding certain foods during breastfeeding Mothers may be told to avoid certain foods when breastfeeding. However, there is no evidence to support the claims that either colic or allergic reactions in infants are caused by the mother’s diet. Allergic reactions are rare in breast fed babies. If this does occur, the mother’s diet should only be modified in consultation with her doctor and dietitian Trying to lose weight while breastfeeding Breast feeding helps you shape up. The greatest amount of weight loss generally occurs in the first 3 months after birth and then continues at a slow and steady rate until 6 months after birth. Breastfeeding your baby should help you return to your pre-pregnancy weight, as some of the fat stores you laid down during pregnancy are used as fuel to make breast milk. Continue breastfeeding for at least 12 months, into the second year of life and for as long as you and your baby & are happy to continue. When you are trying to lose your pregnancy weight, it is important you do not follow a very restrictive diet plan. You need to make nutritious breast milk and stay healthy yourself. Try these helpful hints: • Follow the meal plan in this handout or similar. • Do not skip meals. • Limit foods high in fat and sugar such as lollies, chocolate, soft drinks, cakes, sweet biscuits, chips and fatty take-away food. • Use healthy cooking methods such as steaming, boiling, microwaving, grilling and stir frying. • Do some gentle exercise such as taking your baby for a walk. If available attend physiotherapy postnatal classes. • Plan your healthy meals and snacks ahead of time.
  • This is a consensus document by Queensland Dietitians. Last reviewed: June 2013 Disclaimer: http://www.health.qld.gov.au/masters/copyright.asp Review: June 2015 Are you losing weight too quickly? If you are losing too much weight when you are breastfeeding it is important you do not stop breastfeeding. Instead, find ways to eat more nutritious foods. Try these suggestions: • Don’t skip meals. • Have three main meals and three between-meal snacks. • Keep easy to prepare nutritious snacks on hand (e.g. crisp-breads and cheese, fresh fruit, soy yoghurt, nuts, seeds, dried fruit, canned beans, fruit smoothies, breakfast cereals and soy milk). • Prepare a packed lunch or variety of snacks to have in a container beside you when breastfeeding. • Prepare and freeze meals in advance when possible (or ask your friends/family to help). • Plan your healthy meals & snacks ahead of time. For further breastfeeding information go to www.health.qld.gov.au/breastfeeding/ Things I can do to improve my diet for a healthy pregnancy and/or while breastfeeding: 1. 2. 3. 4. For further information contact your Dietitian or Nutritionist:_____________________ References: 1. Eat for Health Australian Dietary Guidelines. 2013. Commonwealth of Australia. 2. Foods Standards Australia and New Zealand, Listeria and food fact sheet, 2005. 3. Food Standards Australia and New Zealand, Mercury in Fish fact sheet, 2004. 4. Institute of Medicine (2009). Weight Gain During Pregnancy: Re-examining the Guidelines, National Academies Press. 5. National Health and Medical Research Council (2010), Public Statement, Iodine Supplementation for pregnant and breastfeeding women. 6. National Health and Medical Research Council (2006). Nutrient Reference Values for Australia and New Zealand Executive Summary. Dept. Health and Ageing. Canberra, Commonwealth of Australia. 7. Queensland Health. Optimal infant nutrition: evidence-based guidelines 2003-2008.Queensland Health Brisbane 2003. 8. World Health Organisation. Global Strategy for Infant and Young Child Feeding. World Health Organisation, 2003. 9. World Health Organisation. Infant Feeding: The Physiological Basis. 1996. James Akre (ed), WHO, Geneva. 10. Zimmermann M, Delange F. Iodine supplementation of pregnant women in Europe: a review and recommendations. Eur JClin Nutr 2004;58:979-984.
  • The Vegetarian Breastfeeding Mother Mel Wolk St. Peters, Missouri, USA From: LEAVEN, Vol. 33 No. 3, June-July 1997, p. 69 We provide articles from our publications from previous years for reference for our Leaders and members. Readers are cautioned to remember that research and medical information change over time. Ed. Note: From time to time, Leaders receive questions about diet from vegetarian mothers. The BREASTFEEDING ANSWER BOOK is a helpful resource. Vegetarian diets include several variations: Vegan - no flesh foods (red meat, poultry, fish), milk products or eggs. Ovo-lacto vegetarian - no flesh foods but milk products and eggs are allowed. Ovo vegetarian - no flesh foods or milk prod- ucts, but eggs are allowed. Lacto vegetarian - no flesh foods or eggs, but milk products are al- lowed. Vegetarian diets that contain no animal protein may require vitamin B12 supplementation to avoid a deficiency in mother or baby. In babies, symptoms may include loss of appetite, regression in motor development, lethargy, muscle atrophy, vomiting or blood abnormalities. Mothers of babies with symptoms may or may not exhibit symptoms themselves. Mothers on vegan diets who do not consume animal products do have alternatives. They can ask their health care provider about using a vitamin B12 supplement or adding fermented soybean foods and yeast (both contain some vitamin B12) to their diets. Another option would be to ask their health care provider about the need to supplement the baby with vitamin B12. Even though one study showed vegetarian mothers tend to consume less calcium than other mothers, levels of calcium in human milk were not affected. This is believed to be caused by the fact that vegetarians consume less protein and therefore need less calcium. Vegetarian mothers who do not consume milk or other dairy products will want to take special care to eat foods rich in calcium. One cup (227 grams) of cooked bok choy, a type of cabbage, will provide 86% of the calcium in one cup (240 ml.) Of milk. One half cup (113 grams) of ground sesame seeds contains twice as much calcium as one cup (240 ml.) of milk. Other sources of calcium include blackstrap molasses, tofu, collard greens, spinach, broccoli, turnip greens, kale, almonds and Brazil nuts. While vegetarian mothers in the same study had low vitamin D levels, supplements are not usu- ally recommended because most mothers and babies receive adequate vitamin D through expo- sure to the sun. Research suggests that women with dark skin, or those who wear traditional, en- veloping clothing that allows little exposure of skin to sunlight may need to consider a vitamin D supplement for themselves or their babies. The milk of vegetarian mothers is lower in environmental contaminants than the milk of non- vegetarian mothers. Environmental contaminants are stored mainly in fat. Vegetarian diets tend to be lower in fat than those containing animal products, so there is less transfer into human milk. Leaders can assure vegetarian mothers that their diet should not present a problem when breast- feeding their babies.
  • References Dagnelie P. et al. Nutrients and contaminants in human milk from mothers on macrobiotic and ominivorous diets. European Journal of Clinical Nutrition 1992; 46:355-66. Fuhrman, J. Osteoperosis: how to get it and how to avoid it. Health Science Jan/Feb 1992; 8-11. Kuhn, T. et al. Maternal vegan diet causing a serious infantile neurological disorder due to vitamin B12 defi- ciency. European Journal of Clinical Nutrition 1991; 150:205-08. Lawrence, R. Breastfeeding: A Guide for the Medical Profession, 4th ed. St. Louis: Mosby; 1994, pp. 104-15, 290-91, 300-02, 657. Specker, B. Nutritional concerns of lactating women consuming vegetarian diets. American Journal of Clinical Nutrition 1994; 54(Suppl): 1182S-86S.
  • Infant Formulas Unfortunately there is currently no infant formula available which is suitable for vegans. There are soya formulas on the market, such as SMA’s Wysoy and Cow and Gate’s Infasoy, but these are not 100% vegan as they are fortified with vitamin D3, which is made from lanolin (a grease produced by sheep’s skin and extracted from their wool). The vegan-suitable formula which was previously available, Heinz Nurture Soya (formerly Farley’s Soya), is no longer manufactured as Heinz no longer produce any infant formulas. Formula Milk & Soya Milk Some concern has been expressed regarding the relationship between the glucose content of soya formula and tooth decay in children. The energy content is based on glucose syrup rather than lactose (milk sugar) and it has been thought to have a greater potential to contribute to dental caries than cow's milk formulas. No studies have shown that soya infant formula is any more harmful to teeth than dairy infant for- mula. Feeds from a bottle, feeding at bedtime, prolonged sucking, may be the most important factors in predicting caries development (Moynham et al 1996). If normal weaning practices are adopted, infant formulas should not cause harm to teeth. When bottle feeding, do not allow prolonged or frequent contact of milk feeds with your baby's teeth since this increases the risk of tooth decay. As soon as the first tooth erupts (usually appears any time between 6 and 12 months although they may come through sooner or later than this) brush twice daily. Make sure your baby's teeth are cleaned after the last feed at night and try to wean your baby off the bottle by the age of one. Glucose syrup has several properties that make its use in soya formulas appropriate. It is easily absorbed and utilised by infants even when the gut mucosa is damaged. The use of glucose syrup as the carbohydrate in a soya formula ensures a similar osmolal- ity to breast milk. Glucose syrup is easily mixed with water, which is essential for home preparation, and the naturally bitter taste of soya protein is effectively masked by glu- cose syrup without causing undue sweetness. Formula should be fed from a feeding bottle. However, between the ages of six and 12 months a beaker or cup should be increasingly used. The use of a bottle should not be prolonged and teeth should be cleaned after feeds. Regarding tooth decay, evidence indicates that the quantity of sugar eaten is less important than the time taken to con- sume them and the interval before further sugar is eaten. If sugary foods or drinks are consumed, it is better to ensure they are finished relatively quickly rather than eaten over several hours as the mouth pH can be restored within 30 minutes. It is important that ordinary soya milk should not substituted for soya infant formula as it does not contain the proper ratio of protein, fat, carbohydrate, nor the vitamins and minerals required to be used as a sole food. Soya milk should also not be substituted to babies under 6 months of age because it has levels of protein which are too high and excessive protein intake is thought to be medically undesirable at this stage.
  • Breastfeeding and Fenugreek Betty H. Greenman: Posted on Wednesday, July 10, 2013 3:06 PM Many moms are interested in increasing their milk supply. The number one choice is Fenugreek. Fenugreek is an herb that many moms say that it increases their milk supply in only a few days. Fenugreek comes in capsule, powder seed or tea form. Some moms even get creative and bake cookis with Fenugreek in them. You should discuss using Fenugreek with your doctor before you get started taking this. If you have a history of diabetes, hypoglycemia, asthma, abnormal menstrual cycles, peanut or chickpea allergies, migraines, blood pressure problems, or heart disease, Fenugreek is not for you. When the mother takes large amounts of Fenugreek, sometimes she smells like maple syrup. Also, the baby can smell like maple syrup. Sometimes this can be misleading because there is a serious metabolic disorder that babies can be misdiagnosed as having. Also, Fenugreek is an herb related to the peanut family. Therefore, people who have allergies to peanuts, need to stay away. Some babies may have upset stomachs or even diarrhea when mom takes Fenugreek. Some women experience upset stomachs as well. Although herbs are natural, they are not always safe to use. Therefore, breastfeeding moms should be cau- tious when taking Fenugreek. The Food and Drug Administration (FDA) is mandated to control medications and infant formulas in the United States. However, they do not control herbs. Therefore, there are no requirements to list ingredients on the label. Furthermore, some herbs interfere with other medications so speak to your doctor before taking Fenugreek. In conclusion, always discuss any supplemental herbs you are taking while breastfeeding with your doctor. Many women today take Fenugreek in a pill form. Most vitamins and many supermarkets carry this product.If you or your baby are experiencing any side effects, stop taking Fenugreek immediately. Resources: http://bit.ly/1b0Gdrc
  • DEPARTMENT OF NUTRITION FOR HEALTH AND DEVELOPMENT DEPARTMENT OF CHILD AND ADOLESCENT HEALTH AND DEVELOPMENT WORLD HEALTH ORGANIZATION NUTRIENT ADEQUACY OF EXCLUSIVE BREASTFEEDING FOR THE TERM INFANT DURING THE FIRST SIX MONTHS OF LIFE
  • The World Health Organization was established in 1948 as a specialized agency of the United Nations serving as the directing and coordinating authority for international health matters and public health. One of WHO’s constitutional functions is to provide objective and reliable information and advice in the field of human health, a responsibility that it fulfils in part through its extensive programme of publications. The Organization seeks through its publications to support national health strategies and address the most pressing public health concerns of populations around the world. To respond to the needs of Member States at all levels of development, WHO publishes practical manuals, handbooks and training material for specific categories of health workers; internationally applicable guidelines and standards; reviews and analyses of health policies, programmes and research; and state-of-the-art consensus reports that offer technical advice and recommendations for decision-makers. These books are closely tied to the Organization’s priority activities, encompassing disease prevention and control, the development of equitable health systems based on primary health care, and health promotion for individuals and communities. Progress towards better health for all also demands the global dissemination and exchange of information that draws on the knowledge and experience of all WHO’s Member countries and the collaboration of world leaders in public health and the biomedical sciences. To ensure the widest possible availability of authoritative information and guidance on health matters, WHO secures the broad international distribution of its publications and encourages their translation and adaptation. By helping to promote and protect health and prevent and control disease throughout the world, WHO’s books contribute to achieving the Organization’s principal objective — the attainment by all people of the highest possible level of health.
  • GENEVA WORLD HEALTH ORGANIZATION 2002 NUTRIENT ADEQUACY OF EXCLUSIVE BREASTFEEDING FOR THE TERM INFANT DURING THE FIRST SIX MONTHS OF LIFE NANCY F. BUTTE, PHD USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA MARDIA G. LOPEZ-ALARCON, MD, PHD Nutrition Investigation Unit, Pediatric Hospital, CMN, Mexico City, Mexico CUTBERTO GARZA, MD, PHD Division of Nutritional Sciences, Cornell University, Ithaca, NY, USA
  • WHO Library Cataloguing-in-Publication Data Butte, Nancy F. Nutrient adequacy of exclusive breastfeeding for the term infant during the first six months of life / Nancy F. Butte, Mardia G. Lopez-Alarcon, Cutberto Garza. 1.Breastfeeding 2.Milk, Human – chemistry 3.Nutritive value 4.Nutritional requirements 5.Infant I.Lopez-Alarcon, Mardia G. II.Garza, Cutberto III.Expert Consultation on the Optimal Duration of Exclusive Breastfeeding (2001 : Geneva, Switzerland) IV.Title. ISBN 92 4 156211 0 (NLM Classification: WS 125) © World Health Organization 2002 All rights reserved. Publications of the World Health Organization can be obtained from Marketing and Dissemination, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland (tel: +41 22 791 2476; fax: +41 22 791 4857; email: bookorders@who.int). Requests for permission to reproduce or translate WHO publications – whether for sale or for non- commercial distribution – should be addressed to Publications, at the above address (fax: +41 22 791 4806; email: permissions@who.int). The designations employed and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines on maps represent approximate border lines for which there may not yet be full agreement. The mention of specific companies or of certain manufacturers’ products does not imply that they are endorsed or recommended by the World Health Organization in preference to others of a similar nature that are not mentioned. Errors and omissions excepted, the names of proprietary products are distinguished by initial capital letters. The World Health Organization does not warrant that the information contained in this publication is complete and correct and shall not be liable for any damages incurred as a result of its use. The named authors alone are responsible for the views expressed in this publication. Designed by minimum graphics Printed in France
  • Contents iii R E F E R E N C E S Abbreviations & acronyms v Foreword vii Executive summary 1 1. Conceptual framework 3 1.1 Introduction 3 1.2 Using ad libitum intakes to assess adequate nutrient levels 3 1.3 Factorial approaches 4 1.4 Balance methods 5 1.5 Other issues 6 1.5.1 Morbidity patterns 6 1.5.2 Non-continuous growth 6 1.5.3 Estimating the proportion of a group at risk for specific nutrient deficiencies 6 1.5.4 Summary 7 2. Human-milk intake during exclusive breastfeeding in the first year of life 8 2.1 Human-milk intakes 8 2.2 Nutrient intakes of exclusively breastfed infants 8 2.3 Duration of exclusive breastfeeding 8 2.4 Summary 14 3. Energy and specific nutrients 15 3.1 Energy 15 3.1.1 Energy content of human milk 15 3.1.2 Estimates of energy requirements 15 3.1.3 Summary 15 3.2 Proteins 16 3.2.1 Dietary proteins 16 3.2.2 Protein composition of human milk 16 3.2.3 Total nitrogen content of human milk 17 3.2.4 Approaches used to estimate protein requirements 17 3.2.5 Protein intake and growth 20 3.2.6 Plasma amino acids 21 3.2.7 Immune function 21 3.2.8 Infant behaviour 22 3.2.9 Summary 22
  • 3.3 Vitamin A 22 3.3.1 Introduction 22 3.3.2 Vitamin A in human milk 22 3.3.3 Estimates of vitamin A requirements 23 3.3.4 Plasma retinol 23 3.3.5 Functional end-points 24 3.3.6 Summary 26 3.4 Vitamin D 26 3.4.1 Introduction 26 3.4.2 Factors influencing the vitamin D content of human milk 26 3.4.3 Estimates of vitamin D requirements 27 3.4.4 Vitamin D status and rickets 29 3.4.5 Vitamin D and growth in young infants 29 3.4.6 Vitamin D and growth in older infants 30 3.4.7 Summary 30 3.5 Vitamin B6 30 3.5.1 Introduction 30 3.5.2 Vitamin B6 content in human milk 30 3.5.3 Approaches used to estimate vitamin B6 requirements 31 3.5.4 Estimates of requirements 31 3.5.5 Vitamin B6 status of breastfed infants and lactating women 31 3.5.6 Growth of breastfed infants in relation to vitamin B6 status 32 3.5.7 Summary 32 3.6 Calcium 32 3.6.1 Human milk composition 32 3.6.2 Estimates of calcium requirements 32 3.6.3 Summary 33 3.7 Iron 34 3.7.1 Human milk composition 34 3.7.2 Estimates of iron requirements 34 3.7.3 Summary 35 3.8 Zinc 35 3.8.1 Human milk composition 35 3.8.2 Estimates of zinc requirements 35 3.8.3 Summary 37 References 38 N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E iv
  • v R E F E R E N C E S Abbreviations & acronyms AI Adequate intake BMD Bone mineral density BMC Bone mineral content CDC Centers for Disease Control and Prevention (USA) DPT Triple vaccine against diphtheria, pertussis and tetanus DXA Dual-energy X-ray absorptiometry EAR Estimated average requirement EAST Erythrocyte aspartate transaminase EPLP Erythrocyte pyridoxal phosphate ESPGAN European Society of Paediatric Gastroenterology FAO Food and Agriculture Organization of the United Nations IDECG International Dietary Energy Consultative Group IU International units NCHS National Center for Health Statistics (USA) NPN Non-protein nitrogen PLP Pyridoxal phosphate PMP Pyridoxamine phosphate PNP Pyridoxine phosphate PTH Parathyroid hormone RE Retinol equivalents SD Standard deviation SDS Standard deviation score UNICEF United Nations Children’s Fund UNU United Nations University WHO World Health Organization
  • Foreword vii R E F E R E N C E S This review, which was prepared as part of the back- ground documentation for a WHO expert consultation,1 evaluates the nutrient adequacy of exclusive breast- feeding for term infants during the first 6 months of life. Nutrient intakes provided by human milk are compared with infant nutrient requirements. To avoid circular arguments, biochemical and physiological methods, independent of human milk, are used to define these requirements. The review focuses on human-milk nutrients, which may become growth limiting, and on nutrients for which there is a high prevalence of maternal dietary deficiency in some parts of the world; it assesses the adequacy of energy, protein, calcium, iron, zinc, and vitamins A, B6, and D. This task is confounded by the fact that the physiological needs for vitamins A and D, iron, zinc – and possibly other nutrients – are met by the combined availability of nutrients in human milk and endogenous nutrient stores. In evaluating the nutrient adequacy of exclusive breast- feeding, infant nutrient requirements are assessed in terms of relevant functional outcomes. Nutrient adequacy is most commonly evaluated in terms of growth, but other functional outcomes, e.g. immune response and neurodevelopment, are also considered to the extent that available data permit. This review is limited to the nutrient needs of infants. It does not evaluate functional outcomes that depend on other bioactive factors in human milk, or behaviours and practices that are inseparable from breastfeeding, nor does it consider consequences for mothers. In determining the optimal duration of exclusive breast- feeding in specific contexts, it is important that func- tional outcomes, e.g. infant morbidity and mortality, also are taken into consideration. The authors would like to thank the World Health Organization for the opportunity to participate in the expert consultation;1 and Nancy Krebs, Kim Michaelson, Sean Lynch, Donald McCormick, Paul Pencharz, Mary Frances Picciano, Ann Prentice, Bonny Specker and Barbara Underwood for reviewing the draft manuscript. They also express special appreciation for the financial support provided by the United Nations University. 1 Expert consultation on the optimal duration of exclusive breastfeeding, Geneva, World Health Organization, 28–30 March 2001.
  • 1 Executive summary The dual dependency on exogenous dietary sources and endogenous stores to meet requirements needs to be borne in mind particularly when assessing the adequacy of iron and zinc in human milk. Human milk, which is a poor source of iron and zinc, cannot be altered by maternal supplementation with these two nutrients. It is clear that the estimated iron requirements of infants cannot be met by human milk alone at any stage of infancy. The iron endowment at birth meets the iron needs of the breastfed infant in the first half of infancy, i.e. 0 to 6 months. If an exogenous source of iron is not provided, exclusively breastfed infants are at risk of becoming iron deficient during the second half of infancy. Net zinc absorption from human milk falls short of zinc needs, which appear to be subsidized by prenatal stores. In the absence of studies specifically designed to evaluate the time at which prenatal stores become depleted, circumstantial evidence has to be used. Available evidence suggests that the older the exclusively breastfed infant the greater the risk of specific nutrient deficiencies. The inability to estimate the proportion of exclusively breastfed infants at risk of specific deficiencies is a major drawback in terms of developing appropriate public health policies. Conventional methodologies require that a nutrient’s average dietary requirement and its distribution are known along with the mean and distribution of intakes and endogenous stores. Moreover, exclusive breastfeeding at 6 months is not a common practice in developed countries, and it is rarer still in developing countries. There is a serious lack of measurement, which impedes evaluation, of the human- milk intakes of 6-month-old exclusively breastfed infants from developing countries. The marked attrition rates in exclusive breastfeeding through 6 months postpartum, even among women who are both well nourished and highly motivated, is a major gap in our understanding of the biological, cultural and social determinants of the duration of exclusive breastfeeding. A limitation to promoting exclusive breastfeeding for the first 6 months of life is our lack of understanding of the reasons for the attrition rates. Improved understanding of the biological, socioeconomic and E X E C U T I V E S U M M A R Y In this review nutrient adequacy of exclusive breastfeeding is most commonly evaluated in terms of growth. Other functional outcomes, e.g. immune response and neurodevelopment, are considered when data are available. The dual dependency on exogenous dietary sources and endogenous stores for meeting requirements is also considered in evaluating human milk’s nutrient adequacy. When evaluating the nutrient adequacy of human milk, it is essential to recognize the incomplete knowledge of infant nutrient requirements in terms of relevant functional outcomes. Particularly evident is the inadequacy of crucial data for evaluating the nutrient adequacy of exclusive breastfeeding for the first 4 to 6 months. Mean intakes of human milk provide sufficient energy and protein to meet mean requirements during the first 6 months of infancy. Since infant growth potential drives milk production, the distribution of intakes likely matches the distribution of energy and protein requirements. The adequacy of vitamin A and vitamin B6 in human milk is highly dependent upon maternal diet and nutritional status. In well-nourished populations the amounts of vitamins A and B6 in human milk are adequate to meet the requirements for infants during the first 6 months of life. In populations deficient in vitamins A and B6, the amount of these vitamins in human milk will be sub-optimal and corrective measures are called for, either through maternal and/or infant supplementation, or complementary feeding for infants. The vitamin D content of human milk is insufficient to meet infant requirements. Infants depend on sunlight exposure or exogenous intakes of vitamin D; if these are inadequate, the risk of vitamin D deficiency rises with age as stores become depleted in the exclusively breastfed infant. The calcium content of human milk is fairly constant throughout lactation and is not influenced by maternal diet. Based on the estimated calcium intakes of exclusively breastfed infants and an estimated absorption efficiency of > 70%, human milk meets the calcium requirements of infants during the first 6 months of life.
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 2 cultural factors influencing the timing of supplemen- tation of the breastfed infant’s diet is an important part of advocating a globally uniform infant-feeding policy that accurately weighs both this policy’s benefits and possible negative outcomes. It is important to recognize that this review is limited to the nutrient needs of infants. No attempt has been made to evaluate functional outcomes that depend on other bioactive factors in human milk, or behaviours and practices that are inseparable from breastfeeding. Neither have the consequences, positive or negative, for mothers been considered. It is important that functional outcomes, e.g. infant morbidity and mortality, be taken carefully into account in determining the optimal duration of exclusive breastfeeding in specific environments. This review was prepared parallel to, but separate from, a systematic review of the scientific literature on the optimal duration of exclusive breastfeeding.1 These assessments served as the basis for discussion during an expert consultation (Geneva, 28–30 March 2001), whose report is found elsewhere.2 1 Kramer MS, Kakuma R. The optimal duration of exclusive breastfeeding: a systematic review. Geneva, World Health Organization, document WHO/NHD/01.08–WHO/FCH/CAH/ 01.23, 2001. 2 The optimal duration of exclusive breastfeeding: report of an expert consultation. Geneva, World Health Organization, document WHO/NHD/01.09–WHO/FCH/CAH/01.24, 2001.
  • 3 1. Conceptual framework A and D, and zinc). It is becoming increasingly clear that this is likely the case for iron, zinc and possibly calcium. Calcium is included because the physiological significance of the transient lower bone mineral content observed in breastfed infants, compared to their formula- fed counterparts, is not understood. Assessing nutrient needs without acknowledging this dual dependency likely leads to faulty conclusions. To make matters yet more complicated, it is clear that there is a range between clear deficiency and “optimal” adequacy within which humans adapt. The closer one is to deficiency within that range, the more vulnerable one is to common stresses (e.g. infections) and the less one is able to meet increased physiological demands (e.g. growth spurts). Perhaps the best examples of the conceptual difficulties that arise due to the capacity of humans to “adapt” to a range of intakes are debates that swirl around the “small is beautiful” proposition and the “adaptation to lower energy intakes” viewpoint. The former has been discredited fairly conclusively while the latter has been abandoned in recent estimates of energy needs; this is in recognition of the fact that humans can adapt to a range of energy intakes, but at a cost whenever there are sustained deviations from requirement levels (2, 3). Thus, energy requirements are estimated on the basis of multiples of basal metabolic rate to ensure that needs are met for both maintenance and socially acceptable and necessary levels of physical activity (3). 1.2 Using ad libitum intakes to assess adequate nutrient levels The paucity of available functional measures of optimal intakes compared to functional measures of deficiency leads most investigators interested in assessing infant nutrient requirements to base their estimates on data concerning nutrient intakes by presumably healthy, exclusively breastfed infants, i.e. those with no overt evidence of deficiency. This exercise generally relies on estimates of intake volumes and human milk nutrient composition. For some studies, estimates of both have been obtained in the same infant-mother dyad. In most cases, either milk volume or milk composition is 1 . C O N C E P T U A L F R A M E W O R K 1.1 Introduction Dietary surveys of presumably healthy populations, factorial approaches (summing needs imposed by growth and maintenance requirements), and balance techniques (measuring “inputs and outputs”) are the methods used most often to estimate nutrient requirements. None are particularly satisfactory because they seldom adequately address growing concerns that nutrient intakes support long-term health and optimal functional capacities rather than just avoid acute deficiency states. These concerns are most evident when considering the nutrient needs of infants because of the paucity of data for estimating most nutrient requirements and the limited number of functionally relevant outcome measures for this age group. As these limitations apply to nearly all the sections that follow, they will not be repeated. Growth is the most commonly used functional outcome measure of nutrient adequacy. This outcome is particularly useful for screening purposes because the normal progression of growth is dependent on many needs being met and many physiological processes proceeding normally. However, this strength also betrays this outcome’s principal weakness since abnormal growth is highly non-specific. The single or multiple etiologies of abnormal growth are usually difficult to ascertain confidently. This is most apparent in the differential diagnosis of failure to thrive found in most standard paediatric texts (1). Yet, this outcome is key to present approaches for interpreting dietary surveys, calculating factorial estimates and evaluating outcomes of balance studies. Specific issues, which relate to dependence on growth for estimating nutrient needs by each of the above-listed methods, are considered in most of the sections that follow. Another problem that is almost unique to infancy (possible exceptions may be found in specific processes during pregnancy and lactation) is that the normal progression of growth and development during this life stage likely relies on both exogenous sources and endogenous stores of nutrients. For exclusively breastfed infants, these are met by human milk and endogenous nutrient stores transferred to the infant from the mother during gestation (see sections below on iron, vitamins
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 4 assumed. Data on day-to-day variability for either measure are available for only a few studies. The most notable exceptions to these generalities are require- ment estimates for energy (4), protein (5) and iron (6). Factorial approaches are used most commonly to estimate average requirements for energy and these two nutrients. Generally speaking, estimates of nutrient requirements for the first year of life are based on measured intakes of human milk during the first 6 months. Estimated needs during the second 6 months are sometimes determined by extrapolating from these intake measures. The reasons for selecting the first 6 months appear arbitrary. One can offer physiological milestones as a reason for selecting this age, e.g. changes in growth velocities, stability in nutrient concentrations in human milk, disappearance of the extrusion reflex, teething, and enhanced chewing capabilities. However, the variability in the ages at which these milestones are reached is far greater than the specificity that the cut-off suggests. As noted above, growth may be used to justify selecting the first 6 months as a basis for estimating nutrient requirements, although its use this way has severe limitations. Waterlow & Thomson (7), for example, concluded that exclusive breastfeeding sustained normal growth for only approximately 3 months. WHO and others have questioned the present international reference used to reach this and other conclusions related to the maintenance of adequate growth (8). At present, there is no universally accepted reference or standard that is used for assessing the normality of either attained growth or growth velocity in infants. In the absence of such a reference or standard, rationales used in this review that rely on growth are based on WHO data (8) for attained growth and growth velocity. The composition of human milk changes dramatically in the postpartum period as secretions evolve from colostrum to mature milk. The stages of lactation correspond roughly to the following times postpartum: colostrum (0–5 days), transitional milk (6–14 days), and mature milk (15–30 days). Changes in human-milk composition are summarized in Table 1. The first 3 to 4 months of lactation appear to be the period of most rapid change in the concentrations of most nutrients. After that period nutrient concentrations appear to be fairly stable as long as mammary gland involution has not begun (9, 10). However, few studies assess the dietary and physiological factors that determine either the rate of change in nutrient concentrations or inter- individual variability. Intake data appearing in subsequent sections are presented in monthly intervals. All intake estimates are derived from nutrient concentrations and human-milk volumes obtained in studies of self-selected or opportunistic populations. In no case are randomly representative data available for these types of assessments. When data are available, variability of milk volume and composition are estimated by pooled weighted variances of specific studies cited for each nutrient. Unless otherwise stated only studies of “exclusively” or “predominantly” breastfed infants were used to make these estimates. To the extent possible no cross-sectional data of milk volumes and milk composition have been used in subsequent sections in order to minimize self-selection biases that such data present (11). However, it should be noted that most longitudinally designed studies have significant attrition rates as lactation progresses. Thus, these data also present special problems that are difficult to overcome. 1.3 Factorial approaches Factorial approaches are generally based on estimates of maintenance needs, nutrient accretion that accompanies growth, measures of digestibility and/or absorption (bioavailability), and utilization efficiency. The sum of maintenance needs and accretion could be used to estimate requirement levels if dietary nutrients were absorbed and utilized with 100% efficiency. Since this does not occur, however, the sum is corrected to account for absorption rates and utilization efficiency. Generally speaking, with the exception of protein, only maintenance, bioavailability and accretion rates will be of concern in the application of factorial approaches that target nutrient needs of exclusively human-milk fed infants. Thus, again with the exception of protein, in the sections that follow the efficiency of utilization of absorbed nutrients will be assumed to be 100%. The utilization of absorbed nutrients is determined by the nutrient’s biological value, which relates to the efficiency with which a target nutrient (e.g. protein) is assimilated or converted to some functionally active form (e.g. efficiency of use of β-carotene compared to retinol). Maintenance needs reflect endogenous losses related to cellular turnover (e.g. skin desquamation and intestinal epithelial shedding) and unavoidable meta- bolic inefficiency (e.g. endogenous urinary and biliary losses) of endogenous nutrient sources. Maintenance needs for young infants are known with greatest certainty where energy is concerned. Basal and resting metabolic rates generally are accepted as the best
  • 5 measure of energy maintenance needs. There are no unassailable estimates of protein maintenance needs of infants, whether or not breastfed, nor, for that matter, are there reliable estimates for any other nutrient. In adults, endogenous losses are estimated from data collected under conditions that limit the target nutrient’s content in the diet to approximately zero. Accretion rates are related to nutrient accumulations that accompany growth. In infancy, these rates are estimated from measured growth velocities and estimates of the composition of tissues gained as part of growth. Bioavailability generally relates to the availability of nutrients for intestinal absorption (e.g. of ferric versus ferrous iron and the various forms of calcium commonly found in foodstuffs). The determinants of absorption are too nutrient-specific to be considered in this general introduction. Generally, the host’s physiological state and the physical characteristics of nutrients as consumed are among the principal determinants of absorption. In addition to a nutrient’s obligatory losses that occur even when the target nutrient level falls to approximately zero, unavoidable losses are expected to increase as intake levels rise substantially above zero to meet physiological needs. This inefficiency is considered inconsistently in applications of factorial approaches, especially where the nutrient needs of infants are concerned. In the segments that follow, no allowance is made for this highly probable inefficiency other than in consideration of protein needs, and to the extent that iron absorption rates are affected by the status of iron stores. For iron and other minerals, endogenous or unavoidable losses and the bioavailability of dietary sources are measurable simultaneously by multiple-tracer stable-isotope methods. Because these measurements are made at nutrient intakes above zero, estimates of bioavailability and endogenous losses include the unavoidable inefficiencies in both absorption and utilization that are incurred as intakes rise. 1.4 Balance methods Balance methodologies also have been used to estimate nutrient needs and utilization. The general strengths and weaknesses of balance methods have been reviewed extensively and thus will not be repeated (12). For present purposes it is sufficient to acknowledge two characteristics of balance methods. The first is that their interpretation often relies heavily on estimates derived by factorial approaches, that is the appropriateness of retained quantities of target nutrients is determined by comparison with expected retention based on estimates derived by factorial methods. Thus, estimates of growth velocity and tissue composition are key to interpreting balance results. The second characteristic is that balance results are complicated by the unidirectional biases that are inherent in the method. These biases always favour overestimation of retention for two reasons. Firstly, intakes are generally overestimated (i.e. even if balance experiments are carefully carried out, it is much easier to miss “spills” than it is to “overfeed”) and, secondly, 1 . C O N C E P T U A L F R A M E W O R K Table 1. Human milk composition Age Energy Protein Vitamin A Vitamin D Vitamin B6 Calcium Iron Zinc (months) (kcalth/g)a (g/l)a (µmol/l)b (ng/l)c (mg/l)d (mg/l)a (mg/l)a (mg/l)a 1 0.67 11 1.7 645 0.13 266 0.5 2.1 2 0.67 9 1.7 645 0.13 259 0.4 2 3 0.67 9 1.7 645 0.13 253 0.4 1.5 4 0.67 8 1.7 645 0.13 247 0.35 1.2 5 0.67 8 1.7 645 0.13 241 0.35 1 6 0.67 8 1.7 645 0.13 234 0.3 1 7 0.67 8 1.7 645 0.13 228 0.3 0.75 8 0.67 8 1.7 645 0.13 222 0.3 0.75 9 0.67 8 1.7 645 0.13 215 0.3 0.75 10 0.67 8 1.7 645 0.13 209 0.3 0.5 11 0.67 8 1.7 645 0.13 203 0.3 0.5 12 0.67 8 1.7 645 0.13 197 0.3 0.5 a Reference 40. b Reference 6. c Reference 122. d Reference 150.
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 6 underestimating losses is much likelier than over- estimating them (i.e. it is easier to under- than to over- collect urine, faeces and skin losses). 1.5 Other issues 1.5.1 Morbidity patterns Three other issues should also be considered, the first of which is the estimation of common morbidity patterns. Although estimates of nutrient requirements reflect needs during health, it is increasingly recognized that accumulated deficits resulting from infections – due to decreased intakes and increased metabolic needs and losses – must be replenished during convalescence. Thus, it is generally important to consider safety margins in estimating nutrient needs. In the case of exclusive breastfeeding, the estimates presented below assume that infants will demand additional milk to redress accumulated energy deficits, that the nursing mother is able to respond to these increased demands, and that the increased micronutrient and protein intakes accompanying transient increases in total milk intake correct shortfalls accumulated during periods of illness. These assumptions are based on the generally recognized well-being of successfully breastfed infants, who experience occasional infections and live under favourable conditions. We recognize that no direct data are available to evaluate these assumptions under less favourable circumstances and that not enough is known to estimate the effects of possible constraints on maternal abilities to respond to transient increased demands by infants or constraints imposed by inadequate nutrient stores. 1.5.2 Non-continuous growth The second issue is the possibility of non-continuous growth evaluated by Lampl, Veldhuis & Johnson (13). Estimates of nutrient needs based on factorial approaches assume steady, continuous growth. The literature reports observations in support of the possibility that growth occurs in spurts during infancy. Non-continuous growth’s potential demands on nutrient stores and/or exogenous intakes have not been examined sufficiently, and thus no allowance for “non- continuous” growth needs is made in these assessments. 1.5.3 Estimating the proportion of a group at risk for specific nutrient deficiencies The third issue relates to the challenges of estimating the proportion of exclusively breastfed infants at risk of specific nutrient deficiencies using either the “probability approach” (14) or the simplified estimated average requirement (EAR) cut-point method described by Beaton (15). The probability approach estimates the proportion of a target group at risk for a specific nutrient deficiency/inadequacy based on the distributions of the target group’s average estimated nutrient requirement and the group’s ad libitum intake of the nutrient of interest. To use this approach, intakes and requirements should not be correlated and the distributions of requirements and intakes should be known. The EAR cut-point method is a simplified application of the probability approach; it can be used to estimate the proportion of a population at risk when ad libitum intakes and requirements are not correlated, inter- individual variation in the EAR is symmetrically distributed around the mean, and variance of intakes is substantially greater than the variance of the EAR. The dependence of both approaches on a lack of correlation between intakes and requirements presents some difficulties to the extent that the energy intakes, nutrient requirements and ad libitum milk intakes of exclusively breastfed infants are related to each other. This difficulty arises because milk production is driven by the infant’s energy demands and by maternal abilities to meet them. Thus, as energy requirements rise, so should the intakes of all human-milk constituents. The nature of the expected correlation can be illustrated by interrelationships between milk composition and energy and protein requirements imposed by growth. The protein-to-energy ratio of mature human milk is approximately 0.013 g protein/kcalth (16).1 The energy cost of growth is approximately 19 kcalth/kg, 12 kcalth/ kg, 9 kcalth/kg and 5 kcalth/kg for the age intervals 3–4 months, 4–5 months, 5–6 months and 6–9 months, respectively (4). To the degree that increased energy requirements imposed by growth drive increased human- milk consumption, the corresponding increase in protein intakes will be, respectively, 0.25, 0.15, 0.12 and 0.06 g protein/kg for the four above-mentioned age intervals. These values will increase to the extent that non-protein nitrogen (NPN) in human milk is utilizable (see section 3.2.3). The protein deposited per kg of body weight appears fairly stable, approximately 0.24 g/kg from 4 to 9 months of age (4). If we assume a net absorption rate of 0.85 for human-milk protein and an efficiency of dietary protein utilization of 0.73, the mean dietary protein requirement for growth is approximately1 1000 kcalth is equivalent to 4.18 MJ.
  • 7 0.39 g protein/kg (see section 3.2.3). Thus, although increased energy needs imposed by growth should simultaneously drive protein intakes upward, human milk becomes less likely to meet the infant’s need for protein unless energy requirements for activity increase in a manner that corrects the asynchrony described above. In the absence of such an adjustment, as long as human milk remains the only source of protein the growing infant becomes increasingly dependent upon stable or enhanced efficiencies in protein utilization. These types of correlations can be dealt with, in part, by suitable statistical techniques, as was demonstrated in the report of the International Dietary Energy Consultative Group (IDECG) evaluating protein and energy requirements (4, 5). However, the challenges presented by relationships among milk intakes and micronutrient requirements and intakes are more problematic. Theoretically, the same type of relationship exists among energy and micronutrient intakes and requirements as described above for protein but with an added complication. As will be evident in the sections that follow, it is clear that physiological needs for vitamin A, vitamin D, iron, zinc and possibly other nutrients are met by the combined availability of nutrients from human milk and nutrient stores transferred from mother to infant during late gestation. Thus, dietary nutrient requirements vary with the adequacy of those stores. As a consequence there is inadequate information to estimate “true” physiological requirements (i.e. the optimal amounts of a nutrient that should be derived from human milk and from stores accumulated during gestation). We therefore have inadequate information to estimate what the dietary EAR is for any of the nutrients for which there is a co-dependency on stores and an exogenous supply to meet physiological needs. Arriving at an EAR for specific nutrients based on the intakes of healthy breastfed infants assumes, by definition, “optimal” nutrient stores. However, this assumption grows progressively more precarious as the nutritional status of pregnant women becomes increasingly questionable. 1.5.4 Summary None of the available methods for assessing the nutrient needs of infants are entirely satisfactory because they address only short-term outcomes rather than short- and longer-term consequences for health. Of particular concern is the heavy dependence of most methods on growth in the absence of acceptable references/standards of normal attained growth and velocity, and their normal variability. A similar observation can be made regarding the paucity of information on the causes of the high attrition occurring in nearly all longitudinal studies of exclusive breastfeeding in the period of interest, i.e. beyond the first 4 months of life. Similarly, poor understanding of the determinants of inter- individual variability in the nutrient content of human milk creates significant problems in assessing key questions related to the assessment of present methods for estimating nutrient requirements in the first year of life. The infant’s co-dependence on nutrient stores acquired during gestation and nutrients from human milk further complicates estimation of nutrient requirements. This is particularly vexing in applying methods for assessing population rates of inadequacy that require estimates of average nutrient requirements. 1 . C O N C E P T U A L F R A M E W O R K
  • 2. Human-milk intake during exclusive breastfeeding in the first year of life 2.3 Duration of exclusive breastfeeding Although reasons for supplementation are not always discernible from the literature, evidence to date clearly indicates that few women exclusively breastfeed beyond 4 months. Numerous socioeconomic and cultural factors influence the decision to supplement human milk, including medical advice, maternal work demands, family pressures and commercial advertising. Biological factors including infant size, sex, development, interest/ desire, growth rate, appetite, physical activity and maternal lactational capacity also determine the need and timing of complementary feeding. However, neither socioeconomic nor cultural nor biological factors have received adequate systematic attention. In a longitudinal study in the USA, human-milk intake of infants was measured from 4 to 9 months through the transitional feeding period (26). Complementary feeding was started at the discretion of the mother in consultation with the child’s paediatrician. Forty-two per cent (19/45) of the infants were exclusively breastfed until 5 months of age, 40% (18/45) until 6 months, and 18% (8/45) until 7 months. In a Finnish study (25), 198 women intended to breastfeed for 10 months. The number of exclusively breastfed infants was 116 (58%) at 6 months, 71 (36%) at 7.5 months, 36 (18%) at 9 months, and 7 (4%) at 12 months. The reason given for introducing complemen- tary feeding before the age of 4 to 6 months was the infant’s demand appeared greater than the supply of human milk. This was decided by the mother in 77 cases and by the investigators in 7 cases. Complementary feeding reversed the progressive decline in the standard deviation score (SDS) for length from −0.52 to −0.32 (p=0.07) during the 6 to 9-month period. These authors concluded that, although some infants can thrive on exclusive breastfeeding until 9 to 12 months of age, on a population level prolonged exclusive breastfeeding carries a risk of nutritional deficiency even in privileged populations. In a study in the USA of growth and intakes of energy and zinc in infants fed human milk, despite intentions to exclusively breastfeed for 5 months, 23% of mothers added solids to their infant’s diet at 4.5 months; 55% 2.1 Human-milk intakes Human-milk intakes of exclusively and partially breastfed infants during the first year of life in developed and developing countries are presented in Table 2 and Table 3, respectively. Studies conducted in presumably well-nourished populations from developed countries and in under-privileged populations from developing countries in the 1980s–1990s were compiled. In most of these studies, human-milk intake was assessed using the 24-hour test-weighing method. However, the 12- hour test-weighing method (17, 18) and the deuterium dilution method (19–21) were also used in a few cases. If details were not provided in the publication regarding the exclusivity of feeding, partial breastfeeding was assumed. The overall mean human-milk intakes were weighted for sample sizes and a pooled standard deviation (SD) was calculated across studies. Mean human milk intake of exclusively breastfed infants, reared under favourable environmental conditions, increases gradually throughout infancy from 699 g/day at 1 month, to 854 g/day at 6 months and to 910 g/day at 11 months of age. The mean coefficient of variation across all ages was 16% in exclusively breastfed infants compared to 34% in partially breastfed infants. Milk intakes among the partially breastfed hovered around 675 g/day in the first 6 months of life and 530 g/ day in the second 6 months. There is a notable decrease in sample size in studies encompassing the transitional period from exclusive breastfeeding to partial breastfeeding (22–27). 2.2 Nutrient intakes of exclusively breastfed infants Nutrient intakes derived from human milk were calculated (Table 4) based on the mean milk intakes of exclusively breastfed infants from developed countries (Table 2) and human milk composition from well- nourished women (Table 1). The small samples of exclusively breastfed infants between 7 and 12 months of age limit the general applicability of these calculations for older breastfed infants. N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 8
  • 2 . H U M A N - M I L K I N T A K E D U R I N G E X C L U S I V E B R E A S T F E E D I N G I N T H E F I R S T Y E A R O F L I F E 9 Table 2. Human-milk intake of infants from developed countries Age (months) 1 2 3 4 5 6 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Exclusively breastfed infants Butte et al. (19) USA 691 141 8 724 117 14 Butte et al. (16) USA 751 130 37 725 131 40 723 114 37 740 128 41 Chandra (22) Canada 793 71 33 856 99 31 925 112 28 Dewey & Lönnerdal (23) USA 673 192 16 756 170 19 782 172 16 810 142 13 805 117 11 896 122 11 Dewey et al. (29) USA (boys) 856 129 34 Dewey et al. (29) USA (girls) 775 125 39 Goldberg et al. (212) UK 802 179 10 792 177 10 Hofvander et al. (213) Sweden 656 25 773 25 776 25 Janas et al. (214) USA 701 11 709 11 Krebs et al. (28) USA 690 110 71 Köhler et al. (215) Sweden 746 101 26 726 143 21 Lönnerdal et al. (216) Sweden 724 117 11 752 177 12 756 140 12 Michaelsen et al. (40) Denmark 754 167 60 827 139 36 Neville et al. (24) USA 668 117 12 694 98 12 734 114 10 711 100 12 838 134 12 820 79 9 Pao et al. (217) USA 600 159 11 833 2 682 1 Picciano et al. (218) USA 606 135 26 601 123 26 626 117 26 Rattigan et al. (219) Australia 1187 217 5 1238 168 5 Salmenperä et al. (61) Finland 790 140 12 800 120 31 Stuff et al. (220) USA 735 65 9 Stuff & Nichols (26) USA 792 111 19 Stuff & Nichols (26) USA 792 111 19 Stuff & Nichols (26) USA 734 150 18 729 165 18 Stuff & Nichols (26) USA 792 189 8 769 198 8 818 166 8 van Raaij et al. (221) Netherlands 692 122 16 718 122 16 van Raaij et al. (221) Netherlands 745 131 40 Whitehead & Paul (27) UK (boys) 791 116 27 820 187 23 829 168 18 790 113 5 922 1 Whitehead & Paul (27) UK (girls) 677 87 20 742 119 17 775 138 14 814 113 6 838 88 4 Wood et al. (222) USA 688 137 17 729 178 20 758 201 21 793 215 19 789 195 19 Mean, weighted for sample size 699 731 751 780 796 854 Pooled SD 134 132 130 138 141 118 N 186 354 376 257 131 93 Number of study groups 11 14 17 13 10 8
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 10 Table 2. Human-milk intake of infants from developed countries (continued) Age (months) 1 2 3 4 5 6 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Partially breastfed Infants Dewey et al. (29) USA (boys) 814 183 27 Dewey et al. (29) USA (girls) 733 155 33 Köhler et al. (215) Sweden 722 114 13 689 120 12 Krebs et al. (28) USA 720 130 16 Michaelsen et al. (40) Denmark 488 232 16 531 277 26 Pao et al. (217) USA 485 79 4 467 100 11 395 175 6 Paul et al. (223) UK 787 157 28 824 176 28 813 168 28 717 192 25 593 207 26 Paul et al. (223) UK 676 87 20 728 141 19 741 182 20 716 233 17 572 225 19 Prentice et al. (224) UK 741 142 48 785 168 47 783 176 48 717 207 42 588 206 45 Rattigan et al. (219) Australia 1128216.9 5 Stuff et al. (220) USA 640 94 17 Stuff & Nichols (26) USA 703 156 19 595 181 19 Stuff & Nichols (26) USA 648 196 18 van Raaij et al. (221) Netherlands 746 175 16 Whitehead & Paul (27) UK (boys) 648 1 833 123 5 787 172 10 699 204 20 587 188 25 Whitehead & Paul (27) UK (girls) 601 2 664 258 6 662 267 11 500 194 15 WHO (225) Hungary 607 123 84 673 144 86 681 147 85 631 168 85 539 150 85 WHO (225) Sweden 642 149 28 745 148 28 776 95 28 791 131 28 560 208 28 Mean, weighted for sample size 611 697 730 704 710 612 Pooled SD 129 150 149 184 194 180 N 116 227 241 251 163 380 Number of study groups 3 7 9 8 8 15 Age (months) 7 8 9 10 11 12 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Exclusively breastfed Infants Chandra (22) Canada 872 126 27 815 97 24 Neville et al. (24) USA 848 63 6 818 158 3 Salmenperä et al. (61) Finland 890 140 16 910 133 10 Whitehead & Paul (27) UK 854 1 Mean, weighted for sample size 867 815 890 910 Pooled SD 118 103 140 133 N 34 27 16 10 Number of study groups 3 2 1 1
  • 11 2 . H U M A N - M I L K I N T A K E D U R I N G E X C L U S I V E B R E A S T F E E D I N G I N T H E F I R S T Y E A R O F L I F E Table 2. Human-milk intake of infants from developed countries (continued) Age (months) 7 8 9 10 11 12 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Partially breastfed Infants Dewey et al. (43) USA 875 142 8 834 99 7 774 180 5 691 233 5 516 215 6 759 28 2 Dewey et al. (29) USA (boys) 687 233 25 499 270 20 Dewey et al. (29) USA (girls) 605 197 25 402 228 22 Krebs et al. (28) USA 640 150 71 Michaelsen et al. (40) Denmark 318 201 18 Pao et al. (217) USA 554 3 Paul et al. (223) UK 484 182 21 340 206 18 251 274 12 Paul et al. (223) UK 506 255 16 367 266 12 443 319 7 Prentice et al. (224) UK 493 216 38 342 228 31 328 292 19 Rattigan et al. (219) Australia 884 252 4 880 74 4 Stuff & Nichols (26) USA 551 142 19 Stuff & Nichols (26) USA 602 186 18 522 246 18 Stuff & Nichols (26) USA 677 242 8 645 250 8 565 164 8 van Raaij et al. (221) Netherlands 573 187 16 Whitehead & Paul (27) UK (boys) 484 181 21 342 203 18 Whitehead & Paul (27) UK (girls) 481 246 15 329 242 11 WHO (225) Sweden 452 301 28 Mean, weighted for sample size 569 417 497 691 516 497 Pooled SD 188 226 249 233 215 238 N 251 123 154 5 6 48 Number of study groups 11 8 11 1 1 4 Table 3. Human-milk intake of infants from developing countries Age (months) 1 2 3 4 5 6 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Exclusively breastfed infants Butte et al. (20) Mexico 885 146 15 Cohen et al. (30) Honduras 806 50 824 50 823 50 Gonzalez-Cossio et al. (226) Guatemala 661 135 27 749 143 27 776 153 27 Naing & Co (18) Myanmar 423 20 29 480 20 29 556 30 29 616 16 24 655 27 17 751 15 6 van Steenbergen et al. (227) Indonesia 828 41 5 862 184 6 732 90 5 768 109 6 728 101 3 727 224 8 Mean, weighted for sample size 562 634 582 768 778 804 Pooled SD 92 110 42 63 83 76 N 61 62 34 95 97 64 Number of study groups 3 3 2 4 4 3
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 12 Table 3. Human-milk intake of infants from developing countries (continued) Age (months) 1 2 3 4 5 6 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Partially breastfed Infants Butte et al. (20) Mexico 869 150 15 Cohen et al. (30) Honduras 799 47 688 47 699 47 Cohen et al. (30) Honduras 787 44 731 44 725 44 Coward et al. (21) Papua New Guinea 670 190 17 de Kanashiro et al. (17) Peru 685 245129 690 240126 655 226113 Frigerio et al. (228) Gambia 738 47 16 Gonzalez-Cossio et al. (226) Guatemala 655 198 26 726 153 26 721 166 26 720 165 26 Gonzalez-Cossio et al. (226) Guatemala 719 138 22 789 112 22 804 128 22 776 121 22 Gonzalez-Cossio et al. (226) Guatemala 887 125 27 727 113 27 769 128 27 771 117 27 Hennart & Vis (229) Central Africa 517 169 8 605 78 22 525 95 29 Prentice et al. (224) Gambia 649 113 7 705 183 8 782 168 6 582 169 10 643 149 17 van Steenbergen et al. (228) Kenya 778 180 7 619 197 13 573 208 9 van Steenbergen et al. (227) Indonesia 693 138 32 691 117 31 712 118 29 725 131 30 691 97 31 664 109 26 WHO (225) Guatemala (urban) 524 246 32 561 222 30 653 255 28 WHO (225) Philippines (urban) 336 191 34 404 242 25 320 200 20 344 244 10 374 117 16 WHO (225) Guatemala (urban) 519 186 28 548 173 30 586 185 28 WHO (225) Philippines (urban) 502 176 32 577 154 23 693 117 32 586 167 27 597 214 30 WHO (225) Guatemala (rural) 543 131 28 686 151 27 588 142 28 WHO (225) Philippines (rural) 571 187 27 689 216 30 622 221 28 613 201 23 589 136 29 WHO (225) Zaire (urban) 609 244 135 656 256156 588 202 99 607 185 58 641 198115 WHO (225) Zaire (rural) 338 159 52 355 132 50 356 173 57 368 147 66 357 170 99 Mean, weighted for sample size 568 636 574 634 714 611 Pooled SD 196 212 182 177 107 166 N 497 590 391 441 223 694 Number of study groups 15 14 12 10 8 16 Age (months) 7 8 9 10 11 12 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Exclusively breastfed infants van Steenbergen et al. (227) Indonesia 740 7 2 691 143 6 Mean, weighted for sample size 740 691 Pooled SD 7 143 N 2 6 Number of study groups 1 1
  • 13 2 . H U M A N - M I L K I N T A K E D U R I N G E X C L U S I V E B R E A S T F E E D I N G I N T H E F I R S T Y E A R O F L I F E Table 4. Nutrient intakes derived from human milka Human Human milk milk intake, Energy Vitamin Vitamin Vitamin Age intake corrected for (kcalth/ Protein A D B6 Calcium Iron Zinc (month) (g/day) IWLb (g/day) day) (g/day) (µmol/day) (ng/day) (mg/day) (mg/day) (mg/day) (mg/day) 1 699 734 492 8.1 1.25 473 0.1 195 0.37 1.54 2 731 768 514 6.9 1.3 495 0.1 199 0.31 1.54 3 751 803 538 7.2 1.37 518 0.1 203 0.32 1.20 4 780 819 549 6.6 1.39 528 0.11 202 0.29 0.98 5 796 836 560 6.7 1.42 539 0.11 201 0.29 0.84 6 854 897 601 7.2 1.52 578 0.12 210 0.27 0.90 7 867 910 610 7.3 1.55 587 0.12 208 0.27 0.68 8 815 856 573 6.8 1.45 552 0.11 190 0.26 0.64 9 890 935 626 7.5 1.59 603 0.12 201 0.28 0.70 10 900 945 633 7.6 1.61 610 0.12 198 0.28 0.47 11 910 956 640 7.6 1.62 616 0.12 194 0.29 0.48 a Nutrient intakes calculated based on the mean milk intakes of exclusively breastfed infants from developed countries (Table 2) and human milk composition from well-nourished women (Table 1). b IWL = insensible water losses. Table 3. Human-milk intake of infants from developing countries (continued) Age (months) 7 8 9 10 11 12 Reference Country Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Mean SD N Partially breastfed Infants Coward et al. (21) Papua New Guinea 936 173 8 de Kanashiro et al. (17) Peru 624 219 110 565 208 100 Hennart & Vis (229) Central Africa 580 73 39 582 55 43 van Steenbergen et al. (227) Indonesia 617 80 28 635 149 23 WHO (225) Philippines (urban) 321 156 16 WHO (225) Philippines (urban) 558 183 31 548 158 29 WHO (225) Guatemala (urban) 587 186 28 WHO (225) Zaire (urban) 613 193 72 593 192 60 WHO (225) Guatemala (rural) 602 187 28 WHO (225) Philippines (rural) 534 176 32 502 185 26 WHO (225) Zaire (rural) 378 153 91 407 174 85 Mean, weighted for sample size 688 635 516 565 511 Pooled SD 106 149 167 208 164 N 36 23 337 100 243 Number of study groups 2 1 8 1 5
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 14 added solids at 6 months and 93% added solids at 7 months (28). In a Canadian study, the growth performance of 36 exclusively breastfed infants was monitored (22). The number (percent) of children displaying growth faltering – defined as below the NCHS 10th weight-for-age percentile – increased from 3 (8.3%) at 4 months to 5 (13.6%) at 5 months, 8 (22.2%) at 6 months, 9 (25%) at 7 months, and 12 (33.3%) at 8 months. Even in well- nourished women, exclusive breastfeeding did not sustain growth beyond 4 months of age according to the 1977 growth curves; furthermore, growth faltering was associated with higher rates of infectious morbidity. Breastfed boys consistently consumed more human milk than breastfed girls did (29, 27). Girls tended to be exclusively breastfed longer than boys were; comp- lementary foods were offered to boys at 4.1 months and to girls at 4.9 months (27). In the same study, after 4 months only 20% of the boys and 35% of the girls were exclusively breastfed. Complementary feeding resulted in some increase in total energy intake in boys but not in girls. Since exclusive breastfeeding is rare in developing countries, the number of observational studies on human-milk intakes of exclusively breastfed infants is limited. An intervention study was conducted in Honduras where one group (n=50) was required to breastfeed exclusively for 6 months (30). Although this is an important study, it may not be totally represen- tative of all mothers and infants in that community. Sixty-four women were ineligible to participate because they did not maintain exclusive breastfeeding through 16 weeks for the following reasons: insufficient milk (n=26), personal choice (n=16), maternal health (n=12), and family pressure not to breastfeed exclusively (n=10). Weight gain (1092 ± 356 g) in the exclusively breastfed group was similar to the supplemented groups; however, the SD (± 409 g) of weight gain of exclusively breastfed infants of mothers with low BMI was greater than the supplemented infants in both groups. It is unclear whether all infants were growing satisfactorily. Based on this limited number of studies, intakes of exclusively breastfed infants were, on average, similar to those of infants between 4 and 6 months of age from developed countries. More recently, encouraging results have accrued from community-based breastfeeding promotion programmes in developing countries. For example, an intervention conducted in Mexico to promote exclusive breastfeeding succeeded in increasing rates of predominant breast- feeding above controls at 3 months postpartum from 12% in controls to 50% and 67% in the experimental groups (31). Rates of exclusive breastfeeding were 12% in controls and 38–50% in experimental groups. Although the programme succeeded in promoting exclusive breastfeeding, it did not approach the goal of exclusive breastfeeding for 6 months. Meanwhile, in Dhaka, Bangladesh, counsellors – local mothers who received 10 days’ training – paid 15 home- based counselling visits (2 in the last trimester of pregnancy, 3 early postpartum, and fortnightly until infants were 5months old) in the intervention group (32). For the primary outcome, the prevalence of exclusive breastfeeding at 5 months was 202/228 (70%) for the intervention group and 17/285 (6%) for the control group. For the secondary outcomes, mothers in the intervention group initiated breastfeeding earlier than control mothers and were less likely to give prelacteal and postlacteal foods. At day 4, significantly more mothers in the intervention group breastfed exclusively than controls. 2.4 Summary Longitudinal studies conducted among well-nourished women indicate that, during exclusive breastfeeding, human-milk production rates gradually increase from ~700 g/day to 850 g/day at 6 months. Because of the high attrition rates in these studies, the corresponding milk-production rates represent only a select group of women and thus do not reflect the population variability in milk production and infant nutrient requirements. Exclusive breastfeeding at 6 months is not a common practice in developed countries and appears to be rarer still in developing countries. Moreover, there is a serious lack of documentation and evaluation of human-milk intakes of 6-month-old exclusively breastfed infants from developing countries. A limitation to the uniform recommendation of exclusive breastfeeding for the first 6 months of life is the lack of understanding of reasons for the marked attrition rates in exclusive breastfeeding, even among highly motivated women, in the lactation period of interest. The limited relevant evidence suggests that sufficiency of exclusive breastfeeding is infant-specific (e.g. based on sex, size and growth potential), in addition to being linked to maternal lactational capacity and environ- mental factors that may affect an infant’s nutritional needs and a mother’s ability to respond to them. Nevertheless, recent intervention studies suggest that these variables are amenable to improvement in the presence of adequate support.
  • 15 3. Energy and specific nutrients Total energy requirements of breastfed infants (Table 5) were estimated using weight at the 50th percentile of the WHO pooled breastfed data set (8). An allowance for growth was derived from the weight gains at the 50th percentile of the WHO pooled breastfed data set (8), the rates of fat and protein accretion, and the energy equivalents of protein and fat deposition taken as 5.65 kcalth/g and 9.25 kcalth/g, respectively (37). The TEE of breastfed infants (36) was predicted at monthly intervals using the equation TEE (kcalth/day) = 92.8 * Weight (kg) – 151.7. Energy intakes based on the mean milk intakes of exclusively breastfed infants appeared to meet mean energy requirements during the first 6 months of life. Since infant size and growth potential drive energy intake, it is reasonable to assume a positive relationship between energy intake and energy requirements. Positive correlations between energy intake and infant weight, and energy intake and weight gain, have been reported (37–39). The matching of intake to require- ments for energy is unique in this regard. Thus, it is likely that infant energy needs can be met for 6 months, and possibly longer, by women wishing to breastfeed exclusively this long. The major shortcoming appears to be the marked attrition rates in exclusive breast- feeding, even among women who seem to be highly motivated and who have presumably good support networks. There is a major gap in our understanding of the role – and the relative positive or negative contribution – of biological and social determinants of observed attrition rates. 3.1.3 Summary Energy requirements derived from the sum of total energy expenditure and energy deposition were used to evaluate the adequacy of human milk to support the energy needs of exclusively breastfed infants. Energy intakes based on the mean milk intakes of exclusively breastfed infants appear to meet mean energy requirements during the first 6 months of life. Since infant growth potential drives milk production, it is likely that the distribution of energy intakes matches the distribution of energy requirements. Women who 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S 3.1 Energy 3.1.1 Energy content of human milk Proteins, carbohydrates and lipids are the major contributors to the energy content of human milk (33). Protein and carbohydrate concentrations change with duration of lactation, but they are relatively invariable between women at any given stage of lactation. In contrast, lipid concentrations vary significantly between both individual women and populations, which accounts for the variation observed in the energy content of human milk. Differences in milk sampling and analytical methods also contribute to the variation in milk energy (34, 35). Within-day, within-feeding, and between-breast variations in milk composition; interference with milk “let-down”; and individual feeding patterns affect the energy content of human milk. In the present context, two milk-sampling approaches have been used to estimate the energy content of human milk – expression of the entire contents of one or both breasts at a specific time or for a 24-hour period, and collection of small aliquots of milk at different intervals during a feed. Human milk’s energy content was determined directly from its heat of combustion measured in an adiabatic calorimeter, or indirectly from the application of physiological fuel values to the proximate analysis of milk protein, lactose and fat. The mean energy content of human milk ranges from 0.62 kcalth/g to 0.80 kcalth/g (33). For present purposes, a value of 0.67 kcalth/g has been assumed. 3.1.2 Estimates of energy requirements The energy requirements of infants may be derived from total energy expenditure and energy deposition (4). Total energy expenditure was measured by using the doubly labelled water method and energy deposition from protein and fat accretion in breastfed and formula- fed infants at 3, 6, 9, 12, 18 and 24 months of age (36). In this study, the mean coefficient of variation for total energy expenditure (TEE) and total energy requirements were 18% and 17%, respectively, across all ages.
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 16 wish to breastfeed exclusively can meet their infants’ energy needs for 6 months. 3.2 Proteins 3.2.1 Dietary proteins Dietary proteins provide approximately 8% of the exclusively breastfed infant’s energy requirements and the essential amino acids necessary for protein synthesis. Thus, the quantity and quality of proteins are both important. Because protein may serve as a source of energy, failure to meet energy needs decreases the efficiency of protein utilization for tissue accretion and other metabolic functions. Protein undernutrition produces long-term negative effects on growth and neurodevelopment. 3.2.2 Protein composition of human milk The protein content of mature human milk is approx- imately 8–10 g/l (33). The concentration of protein changes as lactation progresses. By the second week postpartum, when the transition from colostrum to mature milk is nearly complete, the concentration of protein is approximately 12.7 g/l (40). This value drops to 9 g/l by the second month, and to 8 g/l by the fourth month where it appears to remain until well into the weaning process when milk volumes fall substantially. At this point protein concentrations increase as involution of the mammary gland progresses. The inter- individual variation of the protein content of human milk, whose basis is unknown (41), is approximately 15%. Several methods have been used to analyse the protein content of human milk and each has yielded different results with implications for the physiology and Table 5. Energy requirements of breastfed Infants Weight Total energy Energy Energy Weight velocity expenditure deposition requirement (kg)a (g/day)a (kcalth/day)b (kcalth/day)c (kcalth/day) Boys 1 4.58 35.2 273 211 485 2 5.50 30.4 359 183 541 3 6.28 23.2 431 139 570 4 6.94 19.1 492 53 546 5 7.48 16.1 542 45 588 6 7.93 12.8 584 36 620 7 8.3 11 619 17 635 8 8.62 10.4 648 16 664 9 8.89 9 673 14 687 10 9.13 7.9 696 21 717 11 9.37 7.7 718 21 739 12 9.62 8.2 741 22 763 Girls 1 4.35 28.3 252 178 430 2 5.14 25.5 325 161 486 3 5.82 21.2 388 134 522 4 6.41 18.4 443 68 511 5 6.92 15.5 490 57 548 6 7.35 12.8 530 47 578 7 7.71 11 564 20 584 8 8.03 9.2 593 17 610 9 8.31 8.4 619 15 635 10 8.55 7.7 642 18 660 11 8.73 6.6 663 15 678 12 9 6.3 684 14 698 a Reference 8. b Reference 36. c Reference 37.
  • 17 nutrition of the breastfed infant (42). Direct analyses include the determination of total nitrogen by the Kjeldahl method and total amino-acid analysis. To derive the protein nitrogen content by the Kjeldahl method, the NPN fraction is separated by acid precipitation. Indirect analyses based on the protein molecule’s characteristics include the Biuret method (peptide bond), Coomassie-Blue/BioRad, BCA method (dye-binding sites) and the Lowry method (tyrosine and phenylalanine content). The Biuret method, whose results conflict with the BCA method, is not recommended for use in human milk because of high background interference. The Lowry method, although efficient, is subject to technical difficulties (e.g. spectrophotometric interference by lipids and cells, differential reaction of proteins in human milk with the colour reagent, and appropriate protein standard representative of complex, changing mixture). The protein content of mature human milk is approximately 9 g/l by the Kjeldahl method (33), and approximately 12–14 g/l by the Lowry and BCA methods (43, 23, 44). The 25% higher values obtained by the Lowry method have been attributed to using bovine serum albumin (BSA), which has fewer aromatic amino acids than human milk, as the standard. As a result, some investi- gators have adjusted milk-protein concentrations determined by the Lowry method (45). Although it is known that the stage of lactation influences the content and relative amounts of protein in human milk, the physiological mechanisms that regulate their levels have not been identified nor has the role of diet been well defined. Based on field studies, human milk’s total protein concentration does not appear to differ among populations at distinct levels of nutritional risk. However, difficulties arise in interpreting published data because total protein content often has been estimated from measurements of total nitrogen. This presents problems because in well-nourished populations approximately 25% of nitrogen is not bound to protein. However, in contrast to conclusions reached in field studies, when dietary protein was increased from 8 to 20% of energy consumption in metabolically controlled studies, protein N concentrations increased by approximately 8%, and 24-hour outputs of protein N increased by approximately 21%, in the milk of well-nourished women (46). Extrapolation from metabolically controlled studies to free-living subjects requires caution. Results from field studies may reflect chronic adaptations; those from shorter-term laboratory studies may represent acute responses to dietary change. There also is a lack of consensus in the literature as to whether low-protein diets result in reduced milk volumes, and therefore in reduced protein outputs (47, 46, 48). Longer-term studies are needed in diverse populations to help resolve these gaps in knowledge. 3.2.3 Total nitrogen content of human milk Human milk’s total nitrogen content, which appears to depend on the stage of lactation and dietary intakes, ranges from 1700 to 3700 mg/l. Eighteen to 30% of the total nitrogen in milk is non-protein nitrogen (NPN). Approximately 30% of NPN are amino acids (5, 49) and thus should be fully available to the infant. As much as 50% of NPN may be bound to urea (5, 49) and the remaining approximately 20% is found in a wide range of compounds such as nitrogen-containing carbo- hydrates, choline, nucleotides and creatinine (50). Changes in the relative composition of non-protein nitrogen, as lactation progresses, are not well described. From the limited information available, NPN appears to decrease by approximately 30% over the first 3 months of lactation (51). If this nitrogen fraction behaves similarly to protein, it should remain stable thereafter until possibly weaning is well under way. 3.2.4 Approaches used to estimate protein requirements Several approaches have been used to estimate protein requirements for infants and children. At present the protein intake of breastfed infants from 0 to 6 months of age is considered the standard for reasons reviewed by the 1994 IDECG report on protein and energy requirements (5). However, two other approaches also have been used to assess the protein requirements of infants – balance methods and factorial estimations. The 1985 FAO/WHO/UNU Report on Energy and Protein Requirements (52) states the rationale for using the protein intakes of exclusively breastfed infants from 0 to 6 months of age to estimate requirements: “The protein needs of an infant will be met if its energy needs are met and the food providing the energy contains protein in quantity and quality equivalent to that of breast milk.” This assumes that decreases in the protein content of human milk are synchronous with decreases in energy requirements expressed per kg of body weight from 0 to 6 months of age, and that the apparently high efficiency of protein utilization in early infancy is sustained at and beyond 6 months of age. There is no scientific evidence that seriously questions these assumptions in relation to utilization efficiency (see 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 18 Table 6), but changes in energy and protein requirements for growth do not appear to be proportionately synchronous. Evolutionary arguments presented for or against the adequacy of exclusive breastfeeding are equally unconvincing because of their basic teleological character. As will be evident below, the absence of sounder physiological data makes the use of human milk intakes during this age interval the best available choice. The 1996 IDECG report on energy and protein requirements (5) reviewed the flaws in the 1985 FAO/ WHO/UNU protein requirement estimates for infants (52). These are the assumption that at 1 month of lactation protein concentrations in milk are sustained (indeed, as discussed above, they fall); possible underestimation of milk-intake volumes (because some investigators decided not to measure insensible water losses when milk intakes are determined by test- weighing techniques, although this probably represents a trivial source of error); and failures to account for either the non-protein component of human milk or the possible under-utilization of some of the milk’s protein constituents because of their resistance to digestion. The following reasons are posited for these inaccurate estimates. Discomfort with reliance on intake data collected mostly under “opportunistic” situations has led to comparing estimates based on ad libitum intakes with nitrogen balance data, and “armchair estimates” based on the factorial approach. Of the two bases for comparisons, balance data are less satisfactory. Many of the difficulties with balance data arise because often they have been obtained from undernourished infants during repletion, or from premature infants. In either case these infants’ Table 6. Efficiency of protein utilization: growth and body composition of breastfed infants and infants consuming infant formula with varying protein concentrations Reference N Age Type of Growth LBM Efficiency of (months) feeding protein utilization Butte & Garza (58) 40 0–4 BF 60th percentile W/L Heinig et al. (45) 71 3–12 BFa Similar to FF Higher in FF Higher in BF 46 FF Motil et al. (231) 10 1.5–6 BF 60 pct Similar to FF Similar to FF 10 FF Similar to FF Salmenperä et al. (61) 202 4–12 BF FF Åkeson et al. (62) 27b 6 BF Similar among 10 FF-13 groups 9 FF-15 8 FF-18 Nielsen et al. (232) 339 10 BF> 7 months 13.7 g/day BF< 7 months 12.5 g/day Butte et al. (20) 15 4 BF Drop growth 15 6 velocity Dewey et al. (63) 50 5–6 BF Similar weight 91 Partial BF and length gain Abbreviations: W/L: weight-for-length percentile of the NCHS reference, 1977 LBM: lean body mass BF: breastfed FF: formula-fed a Breastfeeding and solids after 6 months. b Sample size varies because breastfed infants were changed to formula.
  • 19 physiological condition renders difficult extrapolation to healthy term infants. Moreover, the complexities imposed by relationships between energy intake and efficiencies of protein utilization, and by differences in utilization efficiencies due to the varying biological values and amounts of proteins fed in balance studies, significantly lessen the value of balance results for the purpose of directly estimating protein requirements for healthy term infants. Thus, the factorial approach, which requires estimating maintenance needs, protein accreted during growth and efficiency of utilization, appears more attractive than balance methods. Maintenance needs are based on obligatory losses and the progressive loss of efficiency in protein utilization as levels of protein increase. Utilization efficiency is believed to be maximal below requirement levels and to become progressively less efficient as requirement levels are approached and surpassed. The 1996 IDECG report used results from multiple studies to estimate maintenance needs (5). This estimate was calculated by extrapolating relationships between nitrogen intake and retention to a y intercept of 10 mg N/kg per day to account for integumental losses, and by adjusting relationships between intake and retention to an assumed slope of 0.73. In the report the maintenance requirement was estimated to be 90 mg N/kg per day. An alternative approach, which requires fewer assumptions and less manipulation of experimental data, is the use of basal metabolism to estimate obligatory losses (53). Although this approach was abandoned in the 1985 report because of inconsistent ratios across several ages, it appears reasonably consistent in the age range of interest, i.e. the range of values in published studies of children 4 to 15 months of age is 1.2 to 1.5 mg N per “basal” kcalth (53). For 1- and 4-month-old exclusively breastfed infants, minimal observable energy expenditure rates are approximately 45 kcalth/kg per day (54). If one uses 1.5 mg N per “basal” kcalth as a conservative estimate, obligatory losses are 68 mg N/kg per day and extrapo- lations of this value to 6 or 8 months present no substantial problems since major changes in basal metabolism are not anticipated at these ages. The mean protein gain between 4 and 8 months of age for exclusively breastfed infants is 0.24 g protein/kg of body weight/day or 38 mg N/kg per day. The sum of nitrogen needs for maintenance and growth is 106 mg N/kg per day. However, this sum must be corrected for the absorption rate of human-milk proteins and the rate of protein utilization for growth in the intake range of interest. Most studies that have examined the absorption of human-milk nitrogen and specific human milk-protein components have been preformed among premature infants (55, 56). In examining this issue, Donovan et al. (55) reported apparent absorption rates of 85%, which confirmed earlier data published by Schanler et al. (56). These rates of absorption are remarkably similar to those summarized by Fomon (57) for infants fed various types of cow’s milk-based formulas. These estimates all include losses of both dietary and endogenous nitrogen, thus available data likely underestimate “true” dietary absorption rates. If we nevertheless accept the value for purposes of estimating dietary N requirements, the figure adjusted for absorption is 125 mg N/kg per day. Taking this “conservative” approach, however, is not as unbalanced as it may first appear. The absorption of human milk’s immunological components has been a major concern because of their functional role and putative resistance to digestion. Studies examining this issue also have been performed principally in preterm infants (55, 56). Analyses by Donovan et al. (55) for specific components suggested a maximum absorption rate of 75% for SIgA and 91% for lactoferrin. The apparent absorption rates for lactoferrin reported by these investigators agree with the earlier studies published by Schanler et al. (56). However, the SIgA values in the two studies are quite different. Schanler et al. (56) reported total apparent SIgA absorption rates of 91% compared to the mean of 75% by Donovan et al. (55). This disparity likely reflects the different analytical methods used for measuring SIgA. The estimated requirement for efficiency of utilization must also be corrected. Once again, the best data have been published from studies of premature infants. If we accept the efficiency of utilization of 0.73 adopted by the IDECG group, the N needs of infants in this age range are approximately 171 mg N/kg per day. This estimate compares well with the mean protein N intakes reported by Butte et al. (16) for breastfed infants at 1 and 2 months of age. By 3 months of age the sum of the mean protein N intake and 30% of the mean NPN (assuming that this fraction consists of free amino acids) is 178 mg. By 4 months of age this sum is 161 mg N/kg, still reasonably close to the mean estimated requirement. This leaves us with the remainder of the NPN un- accounted for in terms of its potential utilization. Rates of NPN utilization vary greatly from approximately 10% to almost 50% (5). Given the very incomplete know- 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 20 ledge of factors that account for this five-fold range in utilization rates and the variability of this component in human milk, the presumption of its use and significance to infant nutrition appears tenuous. The decision was thus taken not to include it further in the above calculations. It is possible to estimate the prevalence of inadequacy from these data using the probability approach that was taken in the 1996 IDECG report. A requirement of approximately 170 mg N/kg, which is close to the report’s “Model C”, yielded a population inadequacy prevalence of approximately 8%. 3.2.5 Protein intake and growth Butte et al. examined the adequacy of protein intake from human milk by determining protein intakes and growth of exclusively breastfed infants from middle to upper economic groups in Houston, TX (16, 58). Protein intake was 1.6 ± 0.3 g/kg per day at 1 month and 0.9 ± 0.2 g/kg per day at 4 months of age. The mean Z-scores of these infants’ weights and lengths were consistently greater than zero (based on the WHO pooled breastfed data set) (Table 7) until the fourth month when the mean declined to slightly below zero. Later, Heinig et al. (45) evaluated a sample of breastfed infants from 0 to 12 months of age enrolled in the DARLING Study. Protein intakes of breastfed infants at 3 months were comparable to those reported by Butte et al. (1.1 ± 0.22 g/kg per day), and they remained at approximately 1.1 ± 0.3 g/kg per day through 6 months of exclusive breastfeeding. Weight-for-age Z-scores were between 0.5 and 0 for the first 6 months of life (59). Two other studies, also conducted in developed countries, reported that after the first 2 to 3 months breastfed infants gained weight less rapidly than formula-fed infants (60, 61). In both studies infants were not exclusively breastfed and there was a significant drop (17.5 to 45%) in sample size over time. The unstable anthropometric Z-scores in both studies are thus difficult to evaluate. Table 7. Protein intake of breastfed and formula-fed infants Type Protein intake (g/kg per day) of Reference N feeding 1 2 3 4 6 9 12 Growth Butte & Garza (58) 40 BF 1.6 ± 0.3 1.1 ± 0.2 1.0 ± 0.2 0.9 ± 0.2 60th percentile W/L Heinig et al. (45) 71 BF 1.09 ± 0.2 1.06 ± 0.3 1.67 ± 0.89 2.45 ± 1.1 Similar 46 FF 1.81 ± 0.3 1.76 ± 0.3 2.03 ± 0.4 2.48 ± 0.6 Motil et al. (231)a 10 BF 22 ± 3 14 ± 2 12 ± 3 Similar 10 FF 29 ± 5 25 ± 6 27 ± 10 Åkeson et al. (62) 27b BF 1.39 ± 0.2 1.67 ± 0.9 2.45 ± 1.1 Similar 10 FF-13 1.87 ± 0.2 2.01 ± 0.3 2.48 ± 0.4 9 FF-15 2.0 ± 0.2 2.18 ± 0.4 2.63 ± 0.5 8 FF-18 2.3 ± 0.2 2.32 ± 0.5 2.73 ± 0.3 Butte et al. (20) 15 BF 1.2 ± 0.3 Drop growth 15 1.1 ± 0.3 velocity Dewey et al. (63)c 50 BF 0.98 ± 0.2 Similar 91 Partial 1.18 ± 0.2 BF Abbreviations: BF: breastfed FF: Formula-fed W/L: weight-for-length percentile of the NCHS reference, 1977 a Proteins are in mmol/kg per day. b Sample size varies because breastfed infants were changed to formula. c Breastfeeding and solids after 6 months.
  • 21 Similarly, results from developing countries are incon- sistent. Although protein intakes of exclusively breastfed Mexican infants were comparable to those of American infants (1.2 ± 0.3 g protein per kg/day at 4 months and 1.1 ± 0.3 g/kg per day at 6 months), their weight and length velocities were significantly lower than those observed in American infants by 6 months of age (20). Weight velocity declined from 16.1 ± 3.2 g/day at 4 months (Z = approximately 0.2, using boys) to 8 ± 3.5 g/day (Z = approximately –1.25, using boys) at 6 months, and length velocities from 1.92 ± 0.22 cm/ month (Z = −0.25, using boys) to 1.02 ± 0.34 cm/month (Z = −0.75, using boys) (20). In contrast, a sample in Honduras of exclusively breastfed infants were assigned randomly at 4 months either to continue exclusive breastfeeding until 6 months or to receive a high-protein complementary food from 4 to 6 months. After 4 months of age, the mean protein intake (g/kg per day) in the group of infants who received solid food was 20% higher than that of the exclusively breastfed group. Despite these differences in protein intake, no differences from 4 to 6 months in weight or length gain were noted between feeding groups. Furthermore, 20 infants with the highest protein intakes were matched to 20 exclusively breastfed infants with similar energy intakes. Although protein intake was 33% higher in the non-exclusively breastfed group, growth rates were similar (5). These negative findings should be interpreted cautiously because of the precision of the balances used (accurate to 100 g) relative to the changes in weight observed between 4 and 6 months; and because earlier findings by the same group documented a positive correlation between weight gain and protein intake (39) when intakes and weight gain of both breast- and bottle-fed infants were examined but no such correlation when only breastfed infants were considered. In an experimental study (62), the growth of infants after 6 months receiving formulas with varying protein concentrations (13, 15 and 18 g/l) was compared to the growth of exclusively breastfed infants from 0 to 6 months. Breastfed infants from the DARLING Study were used as the comparison group (59). Although energy intakes were similar in all groups, protein intakes were significantly lower at 6 months of age in the breastfed group compared with those of the three formula-fed groups. Increments in weight and length between 4 and 8 months were similar in the formula- fed and breastfed groups (62). It thus appears that human milk meets the protein needs for growth of infants between 0 and 6 months. There are no data to evaluate the protein adequacy of exclusive breastfeeding at later ages (45, 62), and one may well ask whether any of the published studies have sufficient power to detect physiologically relevant differences in growth. However, the formula study described above suggests that protein should not be the limiting factor. Some concerns may be raised by the seemingly conflicting data of Butte et al. from Mexico (20) and Dewey et al. from Honduras (63). Each of the reports is based on infants from low socioeconomic status settings. Data from Butte et al. may reflect the insufficiency of exclusive or predominant breastfeeding for sustaining normal growth rates in harsh settings. On the other hand, data from Dewey et al. may reflect the reality that, under the circumstances, exclusive breastfeeding is “as good as” what is achievable in terms of growth. However, the period over which weight gain is calculated may influence this conclusion. Dewey et al. (63) reported a weight gain of 1017 g – or the equivalent of approximately 14.5 g/day – in the exclusively breastfed group, and 1004 g, or 14.3 g/day, in the supplemented breastfed group between 16 and 26 weeks of age. Although weight gains over the entire period were not discernibly different between groups, weekly weight gains cannot be calculated or assessed. In contrast Butte et al. evaluated specific weight gains (16.7, 12.3 and 7.8 g/day at 4, 5 and 6 months, respec- tively) and noted a downward trend in predominantly breastfed infants (20). 3.2.6 Plasma amino acids Postprandial concentrations of plasma amino acids also have been used as an index of the adequacy of protein intakes (64). We were unable to find any data evaluating changes in plasma amino-acid patterns in exclusively versus partially breastfed infants during the first year of life. 3.2.7 Immune function Protein undernutrition adversely affects immune function. Protein-deficient infants present impaired immune responses that, in turn, increase their risk of infectious episodes (65). Two papers have been published regarding the associa- tion between protein intake and immune function in breastfed infants. In one study infants were classified at birth as breastfed or formula-fed according to maternal choice (66). Formula-fed infants were assigned randomly to either a low- or high-soy protein formula, 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 22 or to a cow’s milk-based formula adapted to European Society of Paediatric Gastroenterology (ESPGAN) recommendations (i.e. a whey:casein ratio of 50:50). Infants received the polio immunization and the triple vaccine against diphtheria, pertussis and tetanus (DPT) at 2 and 4 months of age. Blood antibodies were ana- lysed at 5 and 8 months. Results were consistent with those reported in the previous study, i.e. infants fed on the low-protein cow’s milk- and soy-based formulas presented poorer antibody responses than did infants who received the high-protein cow’s milk-based formula. Infants consuming the adapted formula had a higher initial antibody response, which was not sustained. Five-month-old exclusively breastfed infants presented sustained antibody responses that were similar to those of the high-protein group (66). In another study, breastfed infants from Sweden presented significantly higher faecal titres of both IgA and IgM antibodies, as well as the secretory component to poliovirus and diphtheria and to tetanus toxoid than did infants receiving a formula with 1.1 or 1.5 g protein per 100 ml (67). The interpretation of the functional significance of these observations remains difficult without robust comparisons of morbidity in exclusively, predominantly and partially breastfed infants 4 to 12 months old in diverse settings. 3.2.8 Infant behaviour Several authors have reported better cognitive develop- ment and intelligence quotients in breastfed infants compared with those who are formula-fed (68, 69). A review by Pollitt et al. (70) amply demonstrates the complexities related to this issue and the difficulties presented by available studies because of their inability to distinguish among competing hypotheses. No studies were found that assess the behavioural outcomes of feeding healthy term infants diverse levels of protein during the first year of life. 3.2.9 Summary Based on factorial and balance studies, infants’ mean protein requirements are approximately 1.1 g/kg per day from 3 to 6 months of age. “True protein” provided by human milk is sufficient to meet the mean protein requirements of infants for the first 2 months of life, and “true protein” intake plus free amino acids and other forms of NPN are likely sufficient to meet the needs of most, though not all, infants after 4 months. A more precise estimate of the proportion of infants whose needs are met at all ages requires improved understanding of the efficiency of human milk nitrogen utilization (both protein and NPN), improved methods for estimating obligatory needs and better functional measures of nitrogen adequacy. 3.3 Vitamin A 3.3.1 Introduction Vitamin A is a generic term for a group of retinoids with similar biological activity. The term includes retinal, retinol, retinoic acid and substances considered to be pro-vitamin A because they can be transformed into retinol. Among the pro-vitamin A compounds, β-carotene has the highest potential vitamin A activity. Recent recommendations by the United States Food and Nutrition Board re-evaluated conversion equiva- lency and recommended use of 1/12 retinol equivalents (RE) from a mixed diet. Retinols are stored in the liver as esters, and storage increases in the fetal liver during late gestation. The placenta regulates the passage of a sufficient amount of vitamin A from mother to fetus to meet physiological requirements but not to build up a substantial body reserve. This tight regulation is believed to result in low hepatic reserves of vitamin A at birth, even in infants born to well-nourished mothers, compared to levels achieved in later life stages (71, 72). After birth, vitamin A is transferred to the infant through human milk. The vitamin A content of human milk depends on maternal vitamin A status. Infants of women with inadequate vitamin A status are born with low reserves of vitamin A, and thus their vitamin A status is likely to be protected for shorter periods than the status of infants born with higher reserves. Since most vitamin A for tissue reserves is transferred late in gestation, preterm infants have lower stores than full-term infants. In populations that are at risk of vitamin A deficiency, the age at which a deficiency occurs is related to the age of weaning, i.e. the shorter the duration of breast- feeding, the earlier the onset of deficiency (73). This is likely due to the combined effect of the consumption of complementary foods that are low in vitamin A and higher vitamin A utilization rates imposed by more frequent infections. 3.3.2 Vitamin A in human milk The mature milk of well-nourished mothers contains approximately 1.7 moles/l vitamin A (6). In addition,
  • 23 human milk contains carotene that may contribute to the vitamin A transferred to the infant (57) and bile salt-stimulated lipase, which facilitates the infant’s absorption of vitamin A and precursor carotenoids (74). Because the vitamin A content of human milk is strongly influenced by maternal nutritional status, it is not surprising to find lower amounts of vitamin A in human milk in regions were undernutrition is widespread and mothers consume vitamin A-containing foods less frequently than women in privileged environments. Consequently, the concentration of vitamin A in mature milk of women in underprivileged countries may be extremely low. For example, Muhilal et al. (75) reported baseline values of 0.60 ± 0.29 moles/ l in studies conducted in Indonesia. Vitamin A concentrations vary with the stage of lactation. In a cross-sectional study in Guatemala, vitamin A concentrations in milk of low-income women decreased from 1.40 µmoles/l at 6 months of lactation to 1.33 and 1.26 µmoles/l at 9 and 15 months, respectively (76). In the Philippines concentrations decreased from 1.26 µmoles/l at 3 months to 0.88 µmoles/ l at 9 months of lactation (76). Similarly, lactating Ethiopian mothers presented vitamin A concentrations of 1.16 ± 0.52 µmoles/l at 1.5–3.5 months of lactation, and 0.74 ± 0.25 µmoles/l at 11.5–23.5 months of lactation (77). According to Stoltzfus & Underwood (73), the best evi- dence that vitamin A levels in human milk correspond to maternal vitamin A status is the improved concen- trations in milk after maternal supplementation in areas where vitamin A deficiency is endemic (75, 78–80). 3.3.3 Estimates of vitamin A requirements The vitamin A requirements of infants are difficult to estimate accurately because of the lack of a sensitive index of vitamin A status. Plasma retinol levels are insensitive to the adequacy of intake until hepatic stores are severely depleted. Other methods that have been considered to assess vitamin A status include adaptation to darkness, the pupillary response test, total liver reserves by isotope dilution, relative dose response/ modified relative dose response, conjunctival impression cytology and immune function (6). However, none of these methods is completely suitable for assessing the vitamin A requirements of infants. Intestinal absorption is among the dietary factors that influence vitamin A requirements. In turn, dietary fat, infections, the food matrix and food processing all affect intestinal absorption (6). However, none of these factors is relevant for breastfed infants since the bioavailability of preformed vitamin A from human milk is likely to be greater than 90%, and breastfed infants are protected against infection, particularly gastrointestinal infections. The potential vitamin A activity of vitamin A precursors in human milk is not known. Thus, in children younger than 1 year, retinoid requirements have been based on the estimated intakes of this vitamin by breastfed infants (6). However, the dependence on maternal diets of human milk vitamin A levels makes accurate estimates of requirements difficult to calculate from milk composition data alone. The recommended vitamin A intake level for infants 0 to 6 months was set at 1.4 µmoles/day and 1.75 µmoles/ day for infants 6 to 12 months based on the intakes of breastfed infants of well-nourished women (6). A deficiency state has been defined as stores that are insufficient to maintain optimal vitamin A concen- trations in target tissues. This is generally observed when body stores fall below 0.07 moles/g liver (81). Serum retinol levels and the relative dose-response test have been used to assess hepatic vitamin A stores, but other functional measures of vitamin A status, e.g. ocular manifestations, are used more often in practice. Less specific measures of vitamin A status such as growth retardation, increased susceptibility to infections and greater mortality risk are also occasionally used (82, 83). 3.3.4 Plasma retinol Serum retinol levels in individuals are tightly regulated; for the reasons outlined above, however, they are indicative of vitamin A status in individuals only when body reserves are depleted or surpassed. Fortunately, serum vitamin A distribution curves and population dietary intake patterns can be used to assess and compare the vitamin A status of populations (83). However, interpretation of serum retinol levels can be confounded by stress, which reduces levels on an acute basis, resulting in abnormally high prevalence rates of poor vitamin A status. At birth, serum vitamin A concentrations in term infants of well-nourished mothers are approximately 0.70 µmoles/l or greater (84, 85). In contrast, serum vitamin A levels of infants born to mothers with marginal vitamin A status are reported at approximately 0.49 µmoles/l (86). In Indonesia more infants whose mothers had vitamin A concentrations below 1.4 µmol/l in their milk had evidence of depleted liver stores and had lower serum retinol concentrations than did infants whose mothers’ vitamin A milk concentrations were above this value (80). 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 24 WHO and UNICEF use a mean population value of 0.7 µmol/l to identify subclinical vitamin A deficiency in populations, but they caution that this value may not identify deficient individuals (87). None the less, this value is commonly used to describe the status of both populations and individuals and to characterize responses to interventions designed to improve vitamin A status. For example, the mean serum retinol levels of 6-month-old exclusively breastfed Bangladeshi infants was 0.77 ± 0.21 µmol/l. Thirty-four per cent presented levels below the 0.70 µmol/l cut-off (88). Serum levels were 0.84 ± 0.23 µmol/l (89) in a similar group of infants whose mothers were supplemented postnatally with vitamin A, but 25% of the infants in this group were reported to have serum values below 0.7 µmol/l. The vitamin A content of human milk in these populations was 0.87 ± 0.61 µmol/l in unsupplemented women and 0.85 ± 0.53 µmol/l in women supplemented with vitamin A. A mean serum retinol concentration of 0.67 µmol/l was reported in 1.5-month-old infants in a multicentre trial conducted in Ghana, India and Peru. Levels below 0.70 µmol/l were reported for 63% of those infants (90). The administration of 25 000 IU of vitamin A with each of the first three doses of DPT/poliomyelitis immunizations resulted in mean serum vitamin A levels of 0.84 µmol/ l in these groups at 6 months of age, and the percentage of infants with retinol levels below 0.70 µmol/l decreased to 30% by 6 months. However, the average retinol concentration 0.80 µmol/l and the percentage of infants with retinol levels below 0.7 µmol/l also dropped (37%) in the placebo group included in that trial (90). Of 339 infants 77% had abnormal relative dose response tests at 1.5 months of age. The percentages with abnormal tests declined to 43%, 38% and 28% at, respectively, 6, 9 and 12 months following the administration of vitamin A. Parallel declines were observed in the placebo group (90). The relative vitamin A concen- trations in milk were similar for both the treatment and placebo groups. 3.3.5 Functional end-points Growth and vitamin status Associations between linear growth retardation and vitamin A deficiency have been found in some, but not all, studies. In a community-based study conducted in Indonesia, 466 children were identified as vitamin A- deficient (presence of night blindness, Bitot’s spots or xerophthalmia). Age-specific paired comparisons showed a lower height-for-age, weight-for-height, mid- upper arm circumference and triceps skin-fold in children under 3 years of age with xerophthalmia than in controls. Vitamin A-deficient children consumed almost half the amount of vitamin A-containing foods (dark-green leafy vegetables and milk) than controls (91). In another study, also conducted in Indonesia by the same group, children who spontaneously recovered from xerophthalmia were compared to a group of children who did not recover spontaneously and to a group of healthy children. Weight and height were evaluated at 3-month intervals. Infants who recovered spontaneously gained weight at the same rate as healthy infants, but their height deficits persisted. Infants who did not recover, and those who became xerophthalmic during the follow-up period, presented the greatest weight and height deficits (92). Although such descriptive data are interesting, they are difficult to interpret because it is likely that all subjects suffered from multiple nutrient deficiencies. However, intervention trials that examined the effect of vitamin A intake on growth also present difficulties,. In a randomized, placebo-controlled study conducted in India, supplementing infants for 1 year with weekly doses of 2500 µg (8.8 moles) vitamin A and 20 mg vitamin E failed to improve growth (93). This occurred despite a higher mortality rate in the placebo group, suggesting a beneficial effect of vitamin A supplemen- tation. Failure to see a growth response suggests that either the level of vitamin A provided was insufficient to achieve normal growth or other nutrient levels were more limiting with respect to growth. In another randomized study conducted in Indonesia, children received 60 000 µg (210 moles) retinol or a placebo on two occasions within 1 year. Supplementation improved weight gain only in males 24 to 60 months of age and had no effect in males or females younger than 24 months (94). Similarly, in another Indonesian trial, commercial monosodium glutamate was fortified with vitamin A. Fortification resulted in improved linear growth, but this time only in children 12 to 24 months old (75). A more recent trial by the same group in Indonesia controlled for baseline vitamin A status. Children were supplemented randomly with vitamin A (103 000 to 206 000 IU, according to age) or a placebo. Results were adjusted by the children’s pre-treatment vitamin A status. An improvement in linear growth (0.16 cm), but not in weight, was observed after supplementation in children older than 24 months. After adjusting for pre-treatment vitamin A status, supplemented children with serum retinol < 0.35 µmol/l at baseline grew 0.39 cm and gained 152 g more weight in a period of
  • 25 16 weeks than children in the placebo group. Weight and height gains were not different between treatment groups in children with retinol concentrations above 0.35 µmol/l (95). Levels of vitamin A in human milk for the various groups were not reported. Thus, an effect of supplementation with vitamin A on growth may be observed in a group of children with a high likelihood of deficiency, but apparently not in infants, i.e. 0 to 12 months of age. The above-mentioned multicentre randomized and placebo-controlled study conducted in Ghana, India and Peru followed infants until 12 months of age. No difference in weight and length gain or Z-scores was observed between supple- mented and placebo groups despite the high percentage of infants with vitamin A deficiency as determined by serum retinol and relative dose response (90). Thus, it is possible that factors other than vitamin A status are more sensitive determinants of growth in infants in this age group. Indeed, in a study conducted in Egypt, the growth of sick and healthy infants was compared after supplementing their mothers with vitamin A. Milk retinol levels correlated significantly with the growth of healthy infants, but not with those who were ill (96). Ocular manifestations In Malawi 152 children with xerophthalmia were compared to 151 age-matched children without visual manifestations of vitamin A deficiency. Weaning was initiated and breastfeeding stopped significantly earlier for children with xerophthalmia than for healthy children (97). However, in another study conducted in Indonesia more than 90% of the children, with or without xerophthalmia, were breastfed for at least 12 months, and the duration of breastfeeding was similar between infants with xerophthalmia and controls. Although the age of introduction of solid foods was not investigated, infants with xerophthalmia received significantly less vitamin A-rich foods than did controls. This suggests that in some settings the quality of complementary foods plays as important a role as the duration of breastfeeding (91). Morbidity and mortality High morbidity and mortality rates due to infectious diseases are associated with clinical and subclinical vitamin A deficiency. Moreover, it has been reported that during infectious episodes vitamin A is excreted in urine at higher levels than usual (98). Thus, the risk of increased frequency and severity of infections is greater in vitamin A-deficient infants and their requirements for vitamin A are higher. Evidence for these associations comes from different types of studies. For example, in South Africa 10-month- old infants hospitalized with complicated measles and supplemented with a single dose of 400 000 IU vitamin A recovered more rapidly from pneumonia and diarrhoea than the placebo group (99). In Bangladesh, infants of vitamin A-supplemented mothers had significantly shorter episodes of respiratory tract infections and fewer febrile episodes in the first 9 months postpartum than infants of unsupplemented mothers (79). In contrast, after controlling for age and nutritional status, smaller but frequent doses of vitamin A supplements provided Indian infants 6 to 60 months of age (2500 µg weekly) had no effect on the incidence, severity or duration of diarrhoea or respiratory tract infections (93). Similarly, in the above-mentioned multicentre study conducted in Ghana, India and Peru no differences in the prevalence of diarrhoea and acute lower-respiratory infections were noted between placebo and supplemented groups (90). In Indonesia, a placebo- controlled trial was conducted in 2067 neonates who received either 50 000 IU vitamin A orally or a placebo on the first day of life. The vitamin A supplement reduced the infant mortality rate and the prevalence of severe respiratory infection (100). Vitamin A supplementation at birth reduced the risk of pneumococcal colonization in South Indian infants (101). The effect of vitamin A supplementation on mortality rates is also somewhat inconsistent. A recent review by Villamoor & Fawzi (102) summarized various issues related to vitamin A sufficiency. The authors reviewed the inconsistent results of community-based trials targeting infants older and younger than 6 months. Although supplementation of deficient populations generally appears to decrease mortality, this outcome has not always been observed. The inconsistency in results is ascribed to multiple factors that include interactions among multiple but variable nutrient deficiencies, other population-specific characteristics, and magnitude and frequency of supplementation (102). Mortality risks have been reported to be 30–60% higher in children with keratomalacia and xerophthalmia than in healthy populations (103). Most studies have reported reductions in mortality rates in preschool children after vitamin A supplementation (99, 75, 104, 103). However, other supplementation studies have failed to observe protective effects (105, 106). Two meta-analyses that included the above-cited studies 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 26 concluded that supplementation reduced mortality in preschool children (107, 108). However, more recent studies failed to observe similar protective effects. In Nepal, differences in mortality rates were not noted in infants, from 0–5 months of age, who received a single dose of 15 000 to 30 000 IU of vitamin A or a placebo (109). Cumulative morbidity and mortality rates were similar between supplemented and placebo groups from 1 to 12 months of age in the Ghanaian, Indian and Peruvian multicentre trial (90). Studies of this type suggest several possibilities. Either present cut-offs used to assess vitamin A adequacy should not be used as proxies for increased risk of morbidity and mortality in all infants; or inadequate vitamin A status of young infants in some study populations is not a major risk to increased morbidity or mortality; or inadequate vitamin A status acts in concert with other factors in a way that requires their simultaneous correction before expected benefits can be achieved. 3.3.6 Summary The absence of any evidence of vitamin A deficiency in well-nourished populations suggests that the vitamin A content of human milk is adequate to meet the vitamin A requirements for infants during the first 6 months of life when mothers are well nourished. However, it is important to recall that there are no population assessments of the vitamin A status of exclusively breastfed infants beyond this age. Human milk is the primary source of vitamin A in environments where vitamin A deficiency is prevalent, and in these settings the population of breastfed infants with deficient or marginal vitamin A stores appears to be significant from a public health perspective. None the less, the lower risk of xerophthalmia and mortality observed in breastfed infants compared to their non- breastfed counterparts argues strongly in favour of continued breastfeeding. This difference is likely to be the result of inappropriate complementary foods and heightened vitamin A requirements due to high rates of infection in prematurely weaned infants. Also, based on the available evidence, it is not possible to make a case for exclusive over predominant breastfeeding unless one argues that all supplementary feeding decreases milk intake and thus, in these settings, also diminishes vitamin A intakes. 3.4 Vitamin D 3.4.1 Introduction Vitamin D is a fat-soluble vitamin that is synthesized in the skin and may be obtained from the diet. There are two forms: vitamin D2 (ergocalciferol) and vitamin D3 (cholecalciferol). Vitamin D2 originates from ergosterol, a plant sterol, and is obtained through the diet; vitamin D3 originates from 7-dehydrocholesterol, a precursor of cholesterol. Both vitamins D2 and D3 require one hydroxylation in the liver to 25-hydoxy- vitamin D and another in the kidney to form the biologically active hormone, 1,25-dihydroxyvitamin D (1,25 (OH)2D). Receptors for 1,25 (OH)2 D are found in the small intestine and other tissues such as the brain, pancreas and heart. Anti-proliferation and pro-differentiation functions have been suggested for vitamin D (110). Receptors for 1,25 (OH)2 D have been detected in the small intestine and colon of the human fetus (110), which suggests that vitamin D has an important role in cell differentiation during gestation (111). In postnatal life, the most widely recognized functions of vitamin D are related to calcium and phosphate metabolism. 3.4.2 Factors influencing the vitamin D content of human milk It is widely accepted that human milk contains very low levels of vitamin D (Table 8). Vitamin D concen- trations in human milk depend on maternal vitamin D status (112). Factors affecting vitamin D status include skin pigmentation, season and latitude (113). Increased skin melanin concentration reduces the efficiency of vitamin D synthesis in the skin. Thus, individuals with dark skin and limited sun exposure are at greater risk of inadequate vitamin D synthesis than those with less skin pigment. Although the vitamin D2 and D3 content in the milk of dark-skinned women may be lower than that of light-skinned women, maternal serum 25(OH)D levels can nevertheless be similar in both groups (114). However, these findings are not consistent with an earlier report by Specker et al. (115) of lower 25(OH)D in the milk and maternal serum of dark-skinned than light-skinned women and a significant correlation between maternal 25(OH)D in serum and milk. The vitamin D in milk of mothers who deliver in the late autumn or winter at or above 40°N latitude or below 40°S latitude comes only from dietary sources or stores because there is hardly any synthesis in the skin at these times of the year (116). Thus, the vitamin D content of themilkofwomenlivingattheselatitudescanbereduced.
  • 27 Since it is not easy to obtain preformed vitamin D from the diet – it is found in only a few food sources such as egg yolk, liver and fatty fish – maternal vitamin D status is most often a function of sun exposure. The conse- quences of this relationship can be highly significant. For example, 70% of the women of upper socioeconomic class and their exclusively or predominantly breastfed infants studied in Pakistan were reported to be vitamin D deficient (117). These findings suggest that vitamin D activity in human milk can be increased by maternal supplementation with preformed vitamin D (118–121, 112). Ala-Houhala et al. (118) reported that the administration of 2000 IU of vitamin D to breastfeeding women normalized their infants’ 25(OH)D levels. A lower dose of 1000 IU was not effective in this regard. Yet, it is difficult to understand the rationale for supplementing women to correct their infants’ vitamin D status, unless maternal supplementation is also used as a strategy to increase maternal vitamin D stores in preparation for a subsequent pregnancy, or to correct or avoid other maternal vitamin D abnormalities. 3.4.3 Estimates of vitamin D requirements The United States Food and Nutrition Board (122) recommends 5 g of vitamin D for infants 0 to 6 months of age, although it also acknowledges that breastfed infants “with habitual small doses of sunshine” do not require supplemental vitamin D. Infants in far northern latitudes or those with minimal sunlight exposure require a minimum of 2.5 µg/day (100 IU) to prevent rickets. The physiological dependence on ultraviolet light for normal vitamin D status is most evident when one considers that approximately 6 litres of human milk daily would be necessary to obtain the minimal amount of vitamin D needed to prevent rickets where sun exposure is inadequate. Two hours is the required minimum weekly amount of sunlight for infants if only the face is exposed, or 30 minutes if the upper and lower extremities are exposed. Breastfed infants who are exposed to less sunlight present low 25(OH)D serum concentrations (115). Because of the normal depen- dence on sunshine for vitamin D adequacy, it is not currently possible to provide precise estimates of vitamin D requirements. Level of vitamin D intake and serum 25(OH)D Serum 25(OH)D is considered the best indicator of vitamin D status because it reflects the combined vitamin D obtained from diet, sunlight and liver stores (123, 124). The cut-off for defining vitamin D deficiency in adults is based on the level of serum 25(OH)D below which high serum parathyroid hormone (PTH) concentrations are observed (122). However, a cut-off based on PTH has not been determined for infants. The current cut-off of 27.5 nmol/ l for infants is based on serum 25(OH)D levels observed in cases of vitamin D deficiency rickets. It is also important to note that although there are significant correlations between milk and maternal serum 25(OH)D levels, no such associations are reported between milk vitamin D and infant serum 25(OH)D. This is likely a reflection of the infant’s endogenous synthesis of vitamin D (112). 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S Table 8. Vitamin D content of human milk Milk Vitamin D Stage Vitamin D concentration activity of Milk Reference N Country status (µg/l) (IU) lactation sample Hollis et al. (120) 5 Canada Normal (NS) 0.39 ± 9 25 1–21 days Whole milk Leerbeck & Sondergaard (233) 2 Europe 15 Pooled Lipid fraction Reeve et al. (234) 3 USA Normal (S) 0.16 53 Mid-lactation Bawnik et al. (119) 5 Israel Unknown (NS) 0.37 ± 0.03 15 3–21 days Whole milk 0.35 ± 0.07 15 pooled Zoeren-Grobben et al. (235) 8 Netherlands Healthy (NS) 1.5 ± 6 1–8 months Lipid fraction NA Abbreviations: NS = non-supplemented S = supplemented with vitamin D NA = not available.
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 28 Breastfed infants in regions where sunlight is plentiful have adequate serum concentrations of 25(OH)D before 6 months of age (125–129, 115). In contrast, infants less than 6 months of age living in regions where sunlight exposure is minimal have serum 25(OH)D concentrations within ranges typically observed in cases of rickets (130–133) (Table 9). Other biochemical and clinical parameters associated with vitamin D deficiency Decreases in the serum concentrations of phosphorus and increases in PTH are early signs of vitamin D deficiency. Decreases in serum calcium are observed only in very severe cases. Zeghoud et al. (134) evaluated responses to either 500 IU/day or 1000 IU/day of supplementary vitamin D in 42 infants born with subclinical vitamin D deficiency (low serum calcium and 25(OH)D and high PTH). Infants who received the higher dose achieved normal serum 25(OH)D and PTH concentrations in the first month with no further changes in either 25(OH)D or PTH. Infants who received the lower dose also had increased 25(OH)D concentrations and decreased PTH levels. Although PTH and 25(OH)D levels were within the normal range by the end of the first month in infants who received 500 IU/day of supplementary vitamin D, PTH and 25(OH)D levels continued to change through the third month, approaching levels in infants supplemented at the higher dose. In the control group with normal serum calcium, 25(OH)D and PTH concentrations presented only slight increases in 25(OH)D (15 nmol/l); PTH concentrations remained stable. All three groups were fed a formula containing 400 IU/l of vitamin D. Thus, the authors concluded that infants born with subclinical vitamin D deficiency can require higher vitamin D Table 9. Vitamin D status of breastfed infants Age and Serum duration of Vitamin D 25 (OH) D Reference N Country supplementation Supplement (ng/ml) BMC Growth Roberts et al. (129) 22 USA 14 days 0 17 ± 3 Normal in Normal 19 14 days–4 months 400 IU 22 ± 3 all groups Markestad et al. (130) 7 Norway 9–12 months 0 50% with Dropped at less than 6 months from 11 ng/ml 60th to 40th percentile Greer & Marshall (128) 24 USA 0–7 days 0 Dropped at 22 (Caucasian) 0–6 months 400 IU 1.5 months Normal Chan et al. (125) 22 USA Birth 0 19 ± 2 Normal in Normal in 29 (Caucasian) 0–6 months 400 IU 23 ± 3 all groups all groups Feliciano et al. (144) 255 China 3–5 days 100 IU Normal in 0–6 months 200 IU all groups 300 IU Fomon et al. (145) 26 USA 8 days 300 IU Normal in 11 (Caucasian) 0–6 months 400 IU all groups 13 1600 IU Atiq et al. (141) 38 Pakistan < 6 months 0 34 nmol/l 24 > 6 months Specker et al. (133) 52 China 3–5 days 100 IU 8 ± 13 Normal in 52 (North) 0–6 months 200 IU 6 ± 9 all groups 52 400 IU 11 ± 10 Abbreviations: BF = breastfed BMC = bone mineral content S = supplemented with vitamin D
  • 29 intakes in early life than those born with more adequate stores (134). Clinical manifestations of severe vitamin D deficiency include hypocalcaemic seizures. A study in the United Kingdom of Great Britain and Northern Ireland of 2- to 14-month-old infants born to parents of Pakistani origin presented with hypocalcaemic seizures and were found to be vitamin D deficient. The diagnosis was based on high concentrations of alkaline phosphatase and low concentrations of serum 25(OH)D, loss of metaphyseal definition and a positive response to vitamin D supplementation (117). Bone mineralization Severe vitamin D insufficiency results in inadequate mineralization of the skeleton. In growing infants deficient mineralization leads to rickets, a disease characterized by a widening of the ends of long bones, deformation of the rib cage (rachitic rosary), and limb deformations such as bowed legs and knocked knees. Studies of subclinical vitamin D deficiency and its effects on bone mineralization are inconsistent, and this likely reflects both the differential effects of PTH on cortical and trabecular bone and the ability of various measurements to distinguish such effects. Primary hyperthyroidism decreases cortical bone mineral density (BMD), and either it has no effect on, or it increases, trabecular BMD (135, 136). In a study of exclusively breastfed infants in the USA, 400 IU of supplemental vitamin D prevented a decline in bone mineralization at the distal radius that has been observed in infants administered a placebo (126). However, Specker et al. did not observe rickets at 6 months of age in any of 256 breastfed infants enrolled in a randomized, double-blind controlled study in China that provided either 100 IU, 200 IU or 400 IU of vitamin D per day (133). This study found supplementation with 100 IU to be sufficient to prevent rickets in breastfed infants with limited sun exposure and vitamin D stores. 3.4.4 Vitamin D status and rickets In 1925 Elliot reported a large number of breastfed infants with rickets in poor urban areas of the USA. Rickets in breastfed infants also has been reported more recently in Greece (137), Nigeria (138), Pakistan (119), and in the USA, mainly among African American infants (139, 140). In a study conducted in Chicago, Edidin et al. (140) described the social conditions that can lead to rickets in developed countries. Minimal sun exposure due to protective clothing, or unsafe neigh- bourhood conditions that prohibit outdoor activities, placed at risk infants of middle and lower socioeconomic groups. However, other studies have failed to identify breastfed infants with rickets despite low 25(OH)D serum concentrations. For rickets to develop, sustained low 25(OH)D concentrations for long periods are probably necessary. In a study conducted in northern China (40 to 47°N latitude) approximately 33% of the breast- fed infants presented 25(OH)D concentrations below 11 ng/ml, and this despite supplements of 2.5 to 5 µg (100 to 200 IU) of vitamin D (133). In the Republic of Korea 97% of breastfed infants born during winter and 47% born during summer were reported to be vitamin D-deficient (131). In Pakistan, 55% of breastfed infants presented with vitamin D serum concentrations below 10 ng/ml (141). In the USA Greer & Tsang (142) reported that exclusively breastfed 6-month-old infants presented with very low 25(OH)D serum concen- trations, but none in any of these populations presented with rickets. Thus, although there is abundant evidence suggesting that breastfed infants often receive less vitamin D than is required, most studies fail to find rickets in breastfed infants less than 6 months of age. However, this conclusion is tempered by studies of older infants. In 1979 Bacharach et al. reported rickets in breastfed infants older than 6 months whose mothers were vitamin D-deficient during pregnancy and lactation (139). In 1980, 9 cases of rickets were reported in Chicago in exclusively breastfed infants aged 7 to 24 months (140). None of the infants received any food from animal sources. Thirty children (median age 15.5 months) were diagnosed with rickets in North Carolina. All were African American and were breastfed for a median duration of 12.5 months with no vitamin D supplements (143). It thus seems that infants who are exclusively or predominantly breastfed for 6 months or longer can be at an increased risk of rickets if their mothers are at risk of vitamin D deficiency, and the infants receive limited sun exposure and no vitamin D supplements. 3.4.5 Vitamin D and growth in young infants The effects of vitamin D on growth in early infancy are best evaluated from results of a study conducted in China of breastfed infants assigned randomly to either 100, 200 or 400 IU of vitamin D per day. The different doses of vitamin D did not affect growth rates of infants who were born at the same latitude, but significant 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 30 differences were found in length gains over a 6-month period between infants living in northern or southern China. Length gains were greater in infants born in the north independent of supplement level. No seasonal differences were noted in either the south or the north. These data suggest that differences (e.g. genetic or environmental) other than vitamin D status may have influenced regional differences in length gain (144). 3.4.6 Vitamin D and growth in older infants The effect of marginal vitamin D status on growth in older infants remains somewhat controversial because of inconsistent findings. On the whole, however, there appear to be few data supporting adverse effects on growth. Fomon, Younoszai & Thomas (145) reported similar growth rates from birth to 140 days among infants receiving either a formula supplemented with 400 or 1600 IU of vitamin D and breastfed infants. Breastfed infants were allowed one formula feeding daily that provided 500 IU of vitamin D/l. Breastfed infants also received a multivitamin preparation containing 1500 IU vitamin A, 200 IU vitamin D, several of the B vitamins and ferrous sulphate. Also, infants were unlikely to be born with marginal vitamin D stores. In another study in the USA of infants less than 1 year of age, no differences in weight or length were detected between breastfed infants, breastfed infants supplemen- ted with 400 IU of vitamin D, and infants fed formula with added vitamin D. However, all mothers in the study were supplemented with vitamin D while infants were permitted one formula feeding per day during the first 4 months, after which solids were added to their diet (125). In a series of studies conducted by Brooke et al., slow statural growth was reported in the first year of life in infants who were born to vitamin D-deficient mothers supplemented with vitamin D in the postpartum period (146–148). Greer et al. (127) reported that Caucasian infants exclusively breastfed for 6 months in Wisconsin were 2 cm shorter at 1 year than infants who received 400 IU daily of supplemental vitamin D, although the difference did not attain statistical significance. It is unclear if there was no difference in attained stature or if failure to detect a difference reflected a lack of sufficient power in the experimental design. In another study of vitamin D-deficient infants who were exclusively breastfed for a mean of 7.5 months, length- for-age percentiles dropped from 60 to 40 between 6 to 12 months of age (130). Thus, breastfed infants of women with poor vitamin D status, or infants with biochemical evidence of vitamin D deficiency, appear to experience impaired growth unless supplemented with vitamin D. However, other nutrient deficiencies may account for growth retardation. 3.4.7 Summary The vitamin D content of human milk is low and dependent on maternal vitamin D status as reflected by maternal serum 25(OH)D. Breastfed infants can maintain normal vitamin D status in the early postnatal period only when their mothers’ vitamin D status is normal and/or the infants are exposed to adequate amounts of sunlight. Risk of vitamin D deficiency increases as infants’ sun exposure decreases, and the ability of infants of vitamin D-replete mothers to maintain normal vitamin D status in the absence of sun exposure remains unknown. Infants born at high latitudes, or in places where sun exposure is restricted for cultural or other reasons, are at special risk; they are likely to be born with low vitamin D stores due to low maternal vitamin D status. If sunlight exposure or exogenous intakes of vitamin D remain inadequate, the risk of vitamin D deficiency rises with age as stores are depleted. 3.5 Vitamin B6 3.5.1 Introduction Vitamin B6 functions as a coenzyme in the metabolism of protein, carbohydrate and fat. The term refers to several compounds, e.g. pyridoxal (PL), pyridoxine (PN), pyridoxamine (PM) and their respective phosphate forms – PLP, PNP and PMP. The major forms of vitamin B6 are PLP and PMP in animal tissues, and PN and PNP in plant tissues. Signs and symptoms of vitamin B6 deficiency include dermatitis, microcytic anaemia, seizures, depression and confusion. In infants vitamin B6 deficiency appears to adversely influence growth. 3.5.2 Vitamin B6 content in human milk The vitamin B6 content of human milk varies with maternal B6 status and intake. The mean B6 concen- tration in human milk of women with B6 intakes below 2.5 mg/day is 0.13 mg/l (778 nmol/l). Mean B6 levels in milk of women with B6 intakes between 2.5 and 5 mg/day are substantially higher – approximately 0.24 mg/l (149). Thus, the daily B6 intakes of infants 1 to 6 months of age who consume at least 780 ml/day of human milk with a B6 concentration of 0.13 mg/l
  • 31 should, as expected, meet the 0.1 mg/day estimated adequate intake (AI) for this age group (150) since the AI was based on B6 intake from human milk. The milk concentration of vitamin B6 in populations at risk of vitamin B6 deficiency may be sub-optimal. The concentration of B6 in the milk of 70 Egyptian women consuming 1.0 mg vitamin B6/day was 0.073 mg/l, substantially lower than that reported for women in Western societies (151). Lower concentrations of milk B6 were associated with lower birth weight and altered infant behaviour. Thus, human milk’s vitamin B6 content closely parallels the mother’s intake of this vitamin. Other factors, e.g. length of gestation, stage of lactation and the use of B6 supplements, influence the vitamin B6 concentration in human milk. The vitamin B6 concentrations in milk of women supplemented during lactation with 2 or 27 mg B6/day and who delivered prematurely were reported to be 0.05 mg/l and 0.22 mg/ l, respectively. These levels were sustained for 28 days postpartum. Levels in milk of women who delivered at term and were supplemented at the same levels were, respectively, 0.08 mg/l and 0.38 mg/l during the first week postpartum. Vitamin B6 levels in milk rose to 0.10 mg/l and 0.50 mg/l, respectively, by 28 days postpartum (152). Similarly, in a study conducted by Udipi et al., throughout the first month postpartum vitamin B6 levels in milk of women delivering prematurely were lower than the levels of women who delivered at term (153). Also analysed was the effect on vitamin B6 milk concentrations of different levels of supplementation. Women received 0, 2.5, 10 or 20 mg PN(HCL) for 3 consecutive days. Non-supplemented mothers had the lowest vitamin B6 levels in their milk (0.09 ± 0.01 mg/l) compared to the other groups (0.19 ± 0.02 mg/l, 0.25 ± 0.02 mg/l and 0.41 ± 0.04 mg/l, respectively) (154). 3.5.3 Approaches used to estimate vitamin B6 requirements Measurements of vitamin B6 concentrations in plasma, blood cells or urine have been used as indicators of B6 status. Functional indicators such as erythrocyte aminotransferase saturation by PLP or measurements of various tryptophan metabolites also have been considered as indicators of B6 status in depletion- repletion studies because of their responsiveness to changes in B6 intakes. Plasma PLP often has been used to assess vitamin B6 status because it reflects tissue stores, responds to changes in dietary B6 and correlates well with other B6 indices (155). However, erythrocyte PLP may be a more reliable indicator, particularly in infants (156). 3.5.4 Estimates of requirements The AI for vitamin B6 is 0.1 mg/day for infants 0 to 6 months and 0.3 mg/day for infants 6 to 12 months of age (160). The AI for the younger age group is based on intakes of exclusively breastfed infants. The AI for older infants is based on extrapolations from data obtained in both the younger age group and adults. 3.5.5 Vitamin B6 status of breastfed infants and lactating women Blood PLP concentrations are high in the fetus and newborn, and they decrease progressively throughout the first year of life (157). Reference ranges for erythro- cyte PLP (EPLP) concentrations and erythrocyte aspartate transaminase (EAST) activities in lactating Finnish women and their infants were established by Heiskanen et al. (156). To be included in the reference, infants had to be exclusively breastfed for 6 months by women with adequate B6 status who were supplemented with 1 mg PN/day, who fed appropriate complementary foods after 6 months, and who weaned to a cow’s milk- based formula at approximately 9 months. The 10th centile values for EPLP concentrations and EAST activity and activation coefficients were defined based on subsets (n=90 at 2, n=106 at 4, n=99 at 6, n=39 at 9, and n=100 at 12 months postpartum) of the original sample (n=198). In a follow-up analysis, Heiskanen et al. (158) evaluated the B6 status of 44 infants from the original sample of 198 who met WHO’s feeding recommendation (exclusive breastfeeding for 6 months and continued breastfeeding for 12 months with appropriate comple- mentary feeding). Low vitamin B6 status – diagnosed as at least two reference values below the 10th centile cut-offs – was observed in 7 of the 44 infants between 4 and 6 months of age. Weight velocities of these infants did not differ from infants with normal B6 status, but their length velocity was significantly lower at 6 to 9 months. The vitamin B6 status of exclusively breastfed infants was evaluated at 2 months (n=118), 4 months (n=118), 6 months (n=112), 7.5 months (n=70), 9 months (n=36), 10 months (n=14), 11 months (n=11) and 12 months (n=7) (159). During the first 4 months the vitamin B6 status of the infants was adequate and independent of maternal status. By 6 months 30% of the infants breastfed by mothers with low vitamin B6 status also had low status. By 6 months of exclusive breastfeeding, the low vitamin B6 status of mothers was reflected in the vitamin B6 status of their infants. At 6 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 32 and 7.5 months indicators of vitamin B6 status in mothers and infants were significantly correlated. Despite a daily PN supplement of 1 mg/day, maternal B6 status was inadequate in ~8% of mothers in the first 6 months and in 11% of mothers at 9 months post- partum. Prenatal vitamin B6 stores appear important for the maintenance of adequate vitamin B6 status of breastfed infants in the first 4 months of life. Human milk alone may not sustain vitamin B6 requirements beyond 6 months. 3.5.6 Growth of breastfed infants in relation to vitamin B6 status In the series of studies conducted by Heiskanen et al. (156, 158, 158) EPLP concentrations at 4 months of age correlated positively with length velocity from 0 to 6 months (r=0.46, p=0.006), and EAST activity in the entire sample correlated with length velocity and changes in length-for-age at 9 months. Weight velocity assessed during the entire first year did not differ statistically among infants with adequate or low B6 indices (n=7). Between 6 and 9 months of age, infants with low B6 indices experienced slower length velocities than infants with adequate B6 indices. Despite similar protein status at 4, 6 and 9 months determined by plasma total proteins, prealbumin and transferrin, all 7 infants with low B6 indices presented declines in length-for- age Z-scores. Kang-Yoon et al. (160) evaluated the growth of infants of well-nourished women supplemented with 2 or 27 mg PL-HCl/day during the first month postpartum. A subgroup was selected from infants born to women who received a 2 mg vitamin B6 supplement. This subgroup of infants was supplemented postnatally with 0.4 mg of vitamin B6. This subgroup, and infants whose mothers were supplemented at the higher level, achieved higher weight-for-age and length-for-age Z-scores than infants of women supplemented at the lowest level despite similar values at entry. 3.5.7 Summary Maternal B6 status and intake, length of gestation, stage of lactation and use of B6 supplements affect the B6 content of human milk. In well-nourished populations, human milk appears to maintain normal vitamin B6 status in most exclusively breastfed infants during the first 4 to 6 months of age; the risk of B6 inadequacy appears to increase beyond 6 months. After 6 months of exclusive breastfeeding, low vitamin B6 status in a mother was associated with low vitamin B6 status in her infant. Compromised linear growth associated with low vitamin B6 status in infants exclusively breastfed for 6 months was reversible through appropriate comple- mentary feeding. In populations with poor vitamin B6 nutriture, the concentration of B6 in human milk will be sub-optimal, with possible adverse effects on infant growth and neurological development. 3.6 Calcium 3.6.1 Human milk composition Human milk contains 250–300 mg/l of calcium with no pronounced changes during lactation (33). Generally, maternal diet does not appear to influence the concentration of calcium in milk. However, recent studies from the Gambia indicated that poorly nourished women on low-calcium diets produced milk with lower- than-normal calcium levels (161), which did not increase with calcium supplementation (162). 3.6.2 Estimates of calcium requirements Calcium requirements are affected substantially by genetic variability and other dietary factors (163). Pronounced calcium deficiency resulting in tetany rarely occurs in the healthy, breastfed infant and therefore is not helpful in determining requirements. Assessment of calcium status is difficult since serum levels are homeostatically regulated and therefore do not reflect body content. Inadequate calcium intake can result in lower-than-normal bone mineralization. Single-beam X-ray densitometry and, more recently, dual-energy X- ray absorptiometry (DXA) have been used to measure bone mineral content (BMC) and BMD. Using DXA, breastfed infants have been shown to have lower BMC and BMD than formula-fed infants at 6 months (164) and 12 months (37). However, the clinical relevance of this is uncertain since the differences in bone mineralization did not persist beyond weaning (37, 164). Since bone mineralization did not differ between breastfed and formula-fed infants after weaning, retention of more calcium than that achieved by breastfed infants does not seem to benefit bone mineralization later in life. Compared to British children, BMC at the radius in Gambian infants was slightly lower at birth, and it fell progressively during early childhood such that by 36 months it was 31% lower (165). The difference remained significant after correction for body weight, height and bone width. Although the BMC of Gambian and British women is remarkably similar, it could be
  • 33 argued that the BMC of Gambian women is less than their genetic potential, as African Americans are known to have significantly higher BMC than their fairer- skinned counterparts. Weaning breastfed infants onto low-calcium diets may compromise later bone mineralization. Balance studies in breastfed term infants indicate rates of absorption ranging from 40 to 70% (166, 167). In breastfed infants, a mean calcium intake was 327 mg/ day and the retention was 80 mg/day (166). Losses amounted to 247 mg/day. Stable-isotope studies using 44 calcium and 46 calcium have been used to determine calcium absorption and retention in term infants (168). Calcium absorption measured using stable isotopes averaged 61 ± 23% (range 27–89%) in a study of 14 human milk-fed infants, aged 5 to 7 months, with a mean weight of 7.8 kg (168). Based on an assumed milk concentration of 0.25 mg/ml and 766 ml/day, an endogenous faecal excretion of 3 mg/kg per day and a urinary excretion of 3 mg/kg per day, these authors estimated from their observations that 68 mg/day of calcium were retained from human milk (168). The accretion of body calcium during the first year of life has been estimated from changes in body weight (140 mg/day) (169) and metacarpal morphometry (80 mg/day) (170, 171). The calcium requirements of breastfed infants have been estimated from urinary calcium losses (3 mg/kg per day), faecal endogenous losses (3 mg/kg per day) (168), and rates of calcium accretion (Table 10). We estimated calcium accretion from BMC measurements by DXA taken at 15 days and 12 months of age (172) on the assumption that 32.2% of BMC was calcium (173). These estimated requirements were based on a small number of infants and several assumptions and thus should be confirmed by further study. Based on the estimated calcium intakes of exclusively breastfed infants, the efficiency of calcium absorption would have to be greater than 70% to cover these estimated requirements. 3.6.3 Summary Calcium requirements during infancy were derived from stable isotope studies of calcium absorption and retention, and calcium accretion rates. Calcium content of human milk is fairly constant throughout lactation and is not influenced by maternal diet. Based on the estimated calcium intakes of exclusively breastfed infants, human milk meets the calcium requirements 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S Table 10. Calcium requirements of breastfed infants Total Total Total Calcium Calcium requirement requirement requirement Calcium Calcium endogenous endogenous for net for net for net urinary urinary faecal faecal Calcium Calcium Calcium calcium calcium calcium losses losses losses losses gain gain gain absorption absorption absorption Age (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (months) BOYSA GIRLSA BOYSB GIRLSB BOYSC GIRLSC ALL BOYS GIRLS ALL 1 14 13 14 13 131 109 120 158 135 147 2 17 15 17 15 131 109 120 164 140 152 3 19 17 19 17 131 109 120 169 144 156 4 21 19 21 19 131 109 120 173 147 160 5 22 21 22 21 131 109 120 176 151 163 6 24 22 24 22 131 109 120 179 153 166 7 25 23 25 23 131 109 120 181 155 168 8 26 24 26 24 131 109 120 183 157 170 9 27 25 27 25 131 109 120 184 159 172 10 27 26 27 26 131 109 120 186 160 173 11 28 26 28 26 131 109 120 187 161 174 12 29 27 29 27 131 109 120 189 163 176 a Calcium urinary losses (3 mg/kg per day) (168). b Calcium endogenous faecal losses (3 mg/kg per day) (168). c Calcium gain (172).
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 34 of infants during the first 6 months of life if the efficiency of absorption is maintained at ~70%, which is within reported rates (166, 167). 3.7 Iron 3.7.1 Human milk composition The concentration of iron in human milk declines from ~0.4–0.8 mg/l in colostrum to ~0.2–0.4 mg/l in mature human milk (33). The iron content of human milk appears to be homeostatically controlled by up- and down-regulation of transferrin receptors in the mam- mary gland (174); consequently, it is unaffected by maternal iron status or diet. 3.7.2 Estimates of iron requirements Major factors determining iron requirements during infancy are iron endowment at birth, requirements for growth and a need to replace losses. The newborn infant is well endowed with iron stores and a high concen- tration of haemoglobin. In the first 6 to 8 weeks of life, there is a marked decline in haemoglobin from the highest to the lowest observed during development due to the abrupt decrease in erythropoiesis in response to increased postnatal delivery of oxygen to tissues (175). In the next stage, between 2 and 4 months of age, haemoglobin concentration gradually increases. Eryth- ropoiesis becomes more active, and there is an increase in erythroid precursors in the bone marrow and an elevation of the reticulocyte count. Between 4 and 6 months of age, there is an increased dependence on dietary iron. Dietary iron provides ~30% of the require- ment for haemoglobin iron turnover, compared to 5% in adults (175). Because of the considerable iron requirement for growth and the marginal supply of iron in infant diets, iron deficiency is prevalent among infants between 6 and 12 months of age. Iron-containing compounds in the body serve metabolic or enzymatic functions or are used for storage. Haemoglobin, myoglobin, the cytochromes and several other proteins function in transport, storage and utilization of oxygen. Iron is stored primarily as ferritin and haemosiderin. Iron is mobilized from these reserves to maintain haemoglobin and other iron-containing compounds. Body function is unlikely to be impaired as long as iron reserves are available. When iron reserves are depleted, iron deficiency will result in anaemia. Haemoglobin can be used to diagnose iron deficiency anaemia although the cut-off value for infants is debated. Serum ferritin, transferrin saturation, trans- ferrin receptor and mean corpuscular volume can be used to assess iron deficiency. Total body iron is relatively stable from birth to ~4 months of age, but the proportion of body iron in distinct compartments (e.g. red blood cells, myoglobin and stores) shifts dramatically as stores are depleted and demands for iron increase to meet needs imposed from 4 to 12 months of age by expanding red blood cell and myoglobin compartments. Iron requirements thus rise markedly around 4 to 6 months of age (176). These requirements are very high relative to infants’ energy requirements at this age. Factorial, balance and stable isotope methods have been used to estimate infants’ iron requirements. Iron needed to recover endogenous losses through the gastrointestinal tract (62 mg/year) and skin (29 mg/year) has been estimated to be approximately 91 mg/year. Iron at 1 year of life as haemoglobin (270 mg), myoglobin and enzymes (54 mg), and storage (53 mg) amounts to 109 mg above the amount present at birth (268 mg) (177). Using this factorial approach, the total iron requirement during infancy is ~200 mg/ year or 0.55 mg/day. Since there is a substantial increase in erythrocyte mass and myoglobin between 4 and 12 months (176, 178), the iron requirement is thought to be higher in later than early infancy. Iron requirements are thus estimated to be 0.5 mg/day for infants from 0 to 6 months of age and 0.9 mg/day for infants 6 to 12 months of age (Table 11). Table 11. Iron Requirements of breastfed infants Faecal Iron Total and skin gain iron Age losses (mg/day) requirement (months) (mg/day) All (mg/day) 1–6 0.24 0.25 0.49 7–12 0.37 0.53 0.90 Source: reference 177. Iron intakes from human milk are summarized in Table 4. At a fractional iron absorption rate of 0.20, it is clear that breastfed infants subsidize their requirements from iron reserves in the body. Stable isotope studies using 59 Fe have tended to overestimate the absorption of iron from human milk because of unequal distribution of the extrinsic label with intrinsic iron in human milk. Recent studies have indicated that the absorption of iron from human milk is more likely to be lower – ~19–20% (179, 180). A balance study in exclusively breastfed term infants resulted in positive iron balances up to 4 months
  • 35 of age (181). Recent results using 59 Fe and 58 Fe indicated a median absorption of iron from human milk of 14% at 6 months of age, 49% in non Fe-supplemented infants and 18% in Fe-supplemented infants at 9 months of age. Although iron absorption was enhanced, the iron in human milk would not be sufficient to meet estimated iron requirements (Abrams, personal communication). Iron status – assessed by the determination of haemo- globin, red blood cell counts, transferrin, transferrin saturation, serum iron and ferritin – of exclusively breastfed infants was satisfactory up to 6 months of age in studies by Duncan et al. (182), Lönnerdal & Hernell (183), Saarinen & Siimes (184) and Simes et al. (185). Iron status was adequate in one study up to 9 to 12 months of age in exclusively breastfed infants (186). However, other studies demonstrated that breastfed infants who do not receive iron supplements are at risk of becoming iron-deficient in the second half of infancy (187, 185). 3.7.3 Summary Human milk is a poor source of iron and cannot be altered by maternal iron supplementation. It is clear that the estimated iron requirements of infants cannot be met by human milk alone at any stage of infancy. The iron endowment at birth adequately provides for the iron needs of the breastfed infant in the first half of infancy. The iron available for growth and development should be adequate until iron stores are exhausted. Factorial and balance methods have been used to estimate the iron requirements of infants. Iron require- ments are estimated to be 0.5 mg/day for infants from 0 to 6 months of age and 0.9 mg/day for infants 7 to 12 months of age. Human milk’s iron content, which declines from ~0.4–0.8 mg/l in colostrum to ~0.2–0.4 mg/l in mature milk, is unaffected by maternal iron status or diet. The estimated iron intakes of exclusively breastfed infants are insufficient to meet their iron requirements. At a fractional iron absorption rate of 0.20, it is clear that breastfed infants subsidize their requirements from iron body reserves. It appears that breastfed infants who do not receive additional iron from supplements or complementary foods are at risk of becoming iron-deficient in the second half of infancy. 3.8 Zinc 3.8.1 Human milk composition The concentration of zinc in human milk declines precipitously from 4–5 mg/l in early milk, to 1–2 mg/l at 3 months postpartum, and to ~0.5 mg/l at 6 months (33). There is considerable inter-individual variation in milk zinc concentrations; in one study the coefficient of variation was 0.25 at 2 weeks postpartum and > 0.50 at 5 to 7 months (188). Interestingly, milk zinc concen- tration displays channelling or tracking in individuals throughout lactation. A significant correlation (r=0.60) was detected between the concentration of zinc in early milk at 2 weeks postpartum and mature milk at 5 to 7 months (188). Maternal dietary zinc has not been shown to affect the zinc content of human milk, while concentrations in human milk seem resistant to zinc supplementation. Studies of lactating women receiving daily zinc supple- ments did not show any effect on milk zinc concen- tration (188, 189), nor did daily doses of 50–150 mg zinc prevent a decline in milk zinc concentration (190). A slower rate of decline, however, was observed in lactating women supplemented with 15 mg/day zinc for 9 months of lactation (191). A randomized, controlled supplementation trial by the same group of investigators failed to confirm their earlier observations (188). A supplement of 20 mg/day for 9 months did not increase mean serum or milk zinc in Finnish women (191). However, a 40-mg supplement increased maternal serum levels at 2 months and the milk level after 6 months of supplementation. A recent study in lactating Spanish women provided evidence that both dietary zinc intake and serum zinc concentrations were positively correlated with milk zinc concentrations (193). Women with low zinc intake in their third trimester of pregnancy (< 10 mg/day zinc) had lower concentrations of zinc in their milk. A comparison of milk zinc concentrations from lactating women in developing and developed countries supports the hypothesis that chronically low dietary zinc is associated with lower milk zinc concentrations (194). 3.8.2 Estimates of zinc requirements Severe zinc deficiency results in acrodermatitis entero- pathica, impaired immune function, diarrhoea and growth retardation. Zinc status is commonly assessed by serum zinc; however, this indicator is affected by other factors, notably infection, stress and growth rate. Serum zinc is informative for groups of healthy infants but not for assessing individuals. There are several case reports of severe zinc deficiency in breastfed term infants receiving milk having lower- than-normal concentrations of zinc (195–200). Since maternal zinc supplementation failed to increase milk concentrations, zinc uptake or secretion by the mam- mary gland appeared defective in these cases. 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 36 Mean serum zinc was stable in breastfed infants from 2 to 9 months, but the number of infants in the low range (0.55mg/l) increased from 3% at birth to 30% at between 4 to 9 months (192). Serum zinc correlated with zinc intake and milk zinc concentrations. However, neither low zinc intakes nor low serum zinc levels were associated with poor growth. In contrast, a decline in serum zinc and erythrocyte metallothionein concentration from 6 to 9 months was observed in breastfed Danish infants (201). Serum zinc at 9 months was positively correlated with weight gain between 6 and 9 months. Mean serum zinc did not change significantly between 2 and 6 months, and then fell significantly between 6 and 9 months, reaching a low mean of 8.4 µmol/l. Median zinc balance in term predominantly breastfed infants studied at 17, 35, 57, 85 and 113 days of age has been shown to be positive (0.1 mg/kg per day); however, the range of zinc balances was high (202) and 33% of the infants were in negative balance. Stable-isotope studies using 67 Zn and 70 Zn demonstrated equilibration of the extrinsic label with intrinsic milk zinc (203). The mean fractional zinc absorption from human milk was 0.55 or 0.08 mg/kg per day in 2- to 5-month-old breast- fed infants with some variation with infant age (204). In the latter study, the infants all achieved positive zinc balance through relatively high fractional zinc absorp- tion and conservation of endogenous zinc losses. Since there is no pharmacological effect of zinc on growth, zinc supplementation trials of breastfed infants provide evidence as to whether zinc is limiting growth. A 3-month intervention trial was undertaken in 4- to 9-month-old breastfed infants who received either 5 mg/ day zinc or a placebo (205). A significant increase in weight gain and linear growth was observed in the supplemented infants. Complementary foods and formula use were not reported. Whether the amount of zinc provided by human milk during the complementary feeding period was insufficient or whether properties of food interfered with the absorption of zinc from human milk is uncertain (205). In another random double-blind study, exclusively breastfed infants were assigned to receive a 5 mg/day zinc-supplement or placebo from 2 to 6.5 months of age (206). Zinc supplementation did not enhance the growth of exclusively breastfed infants. This suggests either that zinc intakes and stores in these infants were sufficient to sustain growth or, alternatively, that zinc alone may not be limiting the growth of exclusively breastfed infants. Zinc, in combination with other trace Table 12. Zinc requirements of breastfed infants Total Urine Urine Urine Endogenous Endogenous Endogenous requirement and sweat and sweat and sweat faecal faecal faecal Zinc Zinc Zinc for net losses losses losses losses losses losses gain gain gain zinc Age (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) (mg/day) absorption (months) BOYSa GIRLSa ALL BOYSb GIRLSb ALL BOYSc GIRLSc ALL (mg/day) 1 0.092 0.087 0.089 0.229 0.218 0.223 0.704 0.566 0.635 0.947 2 0.110 0.103 0.106 0.275 0.257 0.266 0.599 0.507 0.553 0.925 3 0.126 0.116 0.121 0.314 0.291 0.303 0.461 0.421 0.441 0.864 4 0.139 0.128 0.134 0.347 0.321 0.334 0.375 0.362 0.368 0.836 5 0.150 0.138 0.144 0.374 0.346 0.360 0.322 0.309 0.316 0.820 6 0.159 0.147 0.153 0.397 0.368 0.382 0.257 0.257 0.257 0.791 7 0.166 0.154 0.160 0.415 0.386 0.400 0.230 0.217 0.224 0.784 8 0.172 0.161 0.167 0.431 0.402 0.416 0.211 0.184 0.197 0.780 9 0.178 0.166 0.172 0.444 0.416 0.430 0.178 0.171 0.174 0.776 10 0.183 0.171 0.177 0.456 0.428 0.442 0.158 0.158 0.158 0.777 11 0.187 0.175 0.181 0.469 0.437 0.453 0.158 0.145 0.151 0.785 12 0.192 0.180 0.186 0.481 0.450 0.466 0.158 0.145 0.151 0.803 a Urinary and sweat zinc losses (20 µg/kg per day) (209). b Endogenous faecal zinc losses (50 µg/kg per day) (204). c Zinc gain (20 µg/g weight gain) (210, 211).
  • 37 minerals present in very small amounts in human milk, might be limiting the growth of older exclusively breastfed infants. Using stable isotope studies, the estimated mean net zinc absorption, which does not include urinary or integumental losses, was 0.26 mg/day at 2 months and 0.29 mg/day at 4 to 5 months (207). Even with very efficient absorption and conservation of endogenous losses, net zinc absorption did not meet zinc require- ments at 2 months or 4 to 5 months. Mobilization of hepatic zinc bound to metallothionein may supplement the infant’s needs during the first months of life, but by 4.4 months hepatic metallothionein levels fall to those found in older children (208). Zinc requirements of infants may be estimated by the factorial method (209). Urinary and sweat zinc losses are estimated to be 20 µg/kg per day (209). Zinc required for new tissue accretion is estimated to be 20 µg/g weight gain or 30 µg/g lean tissue gain (210, 211). Endogenous faecal zinc losses are estimated to be 50 µg/kg per day (204). Total zinc requirements for net zinc absorption are summarized in Table 12. These estimated zinc requirements should be considered provisional since they were based on studies with small sample sizes and extrapolated data. Zinc requirements are higher in boys than in girls and are highest in early infancy, at the time of greatest weight gain. As growth velocity slows in later infancy, the losses in urine and sweat exceed the amount deposited in tissues. Mean zinc intakes from human milk are summarized in Table 4. At an estimated fractional zinc absorption of 0.55 (204), net zinc absorption will fall short of actual zinc needs. Zinc intakes from human milk are subject to inter-individual variation in milk zinc concentrations. Since milk zinc concentration displays significant tracking (r=0.60) in individuals throughout lactation (188), infants whose mothers produce low zinc concentrations will be at increased risk of zinc deficiency. Since milk intakes are driven by energy needs and not by zinc requirements, and since milk energy and zinc concentrations are not correlated, milk zinc intakes will not be determined by infant size or growth potential. 3.8.3 Summary The concentration of zinc in human milk declines precipitously between early and mature milk and is basically unaffected by maternal zinc supplementation. There is some evidence that chronically low dietary zinc is associated with lower milk zinc concentrations. Zinc requirements have been estimated by the factorial method. At an estimated fractional zinc absorption of 0.55, the net zinc absorption from human milk will fall short of zinc needs, which appear to be subsidized by prenatal stores. 3 . E N E R G Y A N D S P E C I F I C N U T R I E N T S
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  • 45 170. Garn SM. The course of bone gain and the phases of bone loss. The Orthopedic Clinics of North America, 1972, 3:503–520. 171. Weaver CM. Age-related calcium requirements due to changes in absorption and utilization. Journal of Nutrition, 1994, 124:1418S–1425S. 172. Butte NF et al. Body composition during the first two years of life: an updated reference. Pediatric Research, 2000, 47:578–585. 173. Ellis KJ et al. Total body calcium and bone mineral content: Comparison of dual-energy X-ray absorptiometry with neutron activation analysis. Journal of Bone and Mineral Research, 1996, 11:843– 848. 174. Sigman M & Lönnerdal B. Response of rat mammary gland transferrin receptors to maternal dietary iron during pregnancy and lactation. American Journal of Clinical Nutrition, 1990, 52:446–450. 175. Dallman PR, Siimes MA, Stekel A. Iron deficiency in infancy and childhood. American Journal of Clinical Nutrition, 1980, 33:86–118. 176. Dallman PR. Nutritional anemia of infancy: iron, folic acid, and vitamin B12. In: Tsang RC, Nichols BL, eds. Nutrition During Infancy. Philadelphia, Henley and Belfus, Inc., 1988:216-235. 177. Fomon SJ. Nutrition of Normal Infants. St. Louis, Mosby, 1993. 178. Stekel A. Iron requirements in infancy and childhood. In: Stekel A, ed. Iron Nutrition in Infancy and Childhood. New York, Raven, 1984:1– 10. 179. Davidsson L et. al. Influence of lactoferrin on iron absorption from human milk in infants. Pediatric Research, 1994, 35:117–124. 180. Fomon SJ, Ziegler EE, Nelson SE. Erythrocyte incorporation of ingested 58Fe by 56-day-old breast-fed and formula-fed infants. Pediatric Research, 1993, 33:573–576. 181. Schulz-Lell G et al. Iron balances in infant nutrition. Acta Paediatrica Scandinavica, 1987, 76:585-591. 182. Duncan B et al. Iron and the exclusively breast- fed infant from birth to 6 months. Journal of Pediatric Gastroenterology and Nutrition, 1985, 4:421–425. 183. Lönnerdal B & Hernell O. Iron, zinc, copper and selenium status of breast-fed infants and infants fed trace element fortified milk-based infant formula. Acta Paediatrica, 1994, 83:367-373. 184. Saarinen UM & Siimes MA. Iron absorption from infant milk formula and the optimal level of iron supplementation. Acta Paediatrica Scandinavica, 1977, 66:719–722. 185. Siimes MA, Salmenperä L, Perheentupa J. Exclusive breast-feeding for 9 months: risk of iron deficiency. Journal of Pediatrics, 1984, 104:196– 199. 186. Pisacone A et al. Iron status in breast-fed infants. Journal of Pediatrics, 1995, 127:429–431. 187. Pizarro F et al. Iron status with different infant feeding regimens: relevance to screening and prevention of iron deficiency. Journal of Pediatrics, 1991, 118:687–692. 188. Krebs NF et al. Zinc supplementation during lactation: effects on maternal status and milk zinc concentrations. American Journal of Clinical Nutrition, 1995, 61:1030–1036. 189. Moser-Veillon PB & Reynolds RD. A longitudinal study of pyridoxine and zinc supplementation of lactating women. American Journal of Clinical Nutrition, 1990, 52:135–141. 190. Moore MEC, Moran RJ, Green HL. Zinc supplementation in lactating women: evidence for mammary control of zinc secretion. Journal of Pediatrics, 1984, 105:600–602. 191. Krebs NF et al. The effects of a dietary zinc supplement during lactation on longitudinal changes in maternal zinc status and milk zinc concentrations. American Journal of Clinical Nutrition, 1985, 41:560–570. 192. Salmenperä L et al. Low zinc intake during exclusive breast-feeding does not impair growth. Journal of Pediatric Gastroenterology and Nutrition, 1994, 18:361–370. 193. Ortega RM et al. Zinc levels in maternal milk: the influence of nutritional status with respect to zinc during the third trimester of pregnancy. European Journal of Clinical Nutrition, 1997, 51:253–258. 194. Krebs NF. Zinc supplementation during lactation. American Journal of Clinical Nutrition, 1998, 68:509S–512S. R E F E R E N C E S
  • N U T R I E N T A D E Q U A C Y O F E X C L U S I V E B R E A S T F E E D I N G F O R T H E T E R M I N F A N T D U R I N G T H E F I R S T S I X M O N T H S O F L I F E 46 195. Bye AM, Goodfellow A, Atherton D J. Transient zinc deficiency in a full-term breast-fed infant of normal birth weight. Pediatric Dermatology, 1985, 2:308–311. 196. Glover MT & Atherton DJ. Transient zinc deficiency in two full-term breast-fed siblings associated with low maternal breast milk zinc concentrations. Pediatric Dermatology, 1988, 5:10– 13. 197. Khoshoo V et al. Zinc deficiency in a full-term breast-fed infant: Unusual presentation. Pediatrics, 1992, 89:1094–1095. 198. Kuramoto Y et al. Acquired zinc deficiency in two breast-fed mature infants. Acta Dermato- Venereologica, 1986, 66:359–361. 199. Lee MG, Hong KT, Kim JJ. Transient zinc deficiency in two full-term breast-fed siblings associated with low maternal breast milk zinc concentrations. Journal of the American Academy of Dermatology, 1990, 23:375–379. 200. Roberts LJ, Shadwick CF, Bergstresser PR. Zinc deficiency in two full-term breast-fed infants. Journal of the American Academy of Dermatology, 1987, 16:301–304. 201. Michaelsen KF et al. Zinc intake, zinc status and growth in a longitudinal study of healthy Danish infants. Acta Paediatrica, 1994, 83:1115–1121. 202. Sievers E et al. Longitudinal zinc balances in breast-fed and formula-fed infants. Acta Paediatrica, 1992, 81:1–6. 203. Serfass RE, Ziegler EE, Edwards BB. Intrinsic and extrinsic stable isotopic zinc absorption by infants from formulas. Journal of Nutrition, 1989, 119: 1661–1669. 204. Krebs NF et al. Zinc homeostasis in breast-fed infants. Pediatric Research, 1996, 39:661–665. 205. Walravens PA et al. Zinc supplements in breastfed infants. Lancet, 1992, 340:683–685. 206. Krebs NF, Westcott JE, Butler-Simon N. Effect of a zinc supplement on growth of normal breastfed infants. Journal of the Federation of American Societies for Experimental Biology, 1996, 10:A230 (abs.). 207. Krebs NF. Zinc transfer to the breastfed infant. Journal of Mammary Gland Biology and Neoplasia, 1999, 4:259–268. 208. Zlotkin SH & Cherian GM. Hepatic metallothi- onein as a source of zinc and cysteine during the first year of life. Pediatric Research, 1988, 24:326– 329. 209. Krebs NF & Hambidge KM. Zinc requirements and zinc intakes of breast-fed infants. American Journal of Clinical Nutrition, 1986, 43:288–292. 210. Widdowson EM, Southgate DAT, Hey E. Fetal growth and body composition. In: Lindblad BS., ed. Perinatal Nutrition. New York, Academic Press, 1988:3–14. 211. Trace elements in human nutrition. Report of a WHO Expert Committee. Geneva, World Health Organi- zation, 1973 (WHO Technical Report Series No. 532). 212. Goldberg GR et al. Longitudinal assessment of the components of energy balance in well-nourished lactating women. American Journal of Clinical Nutrition, 1991, 54:788–798. 213. Hofvander Y et al. The amount of milk consumed by 1–3 months old breast- or bottle-fed infants. Acta Paediatrica Scandinavica, 1982, 71:953–958. 214. Janas LM, Picciano MF, Hatch TF. Indices of protein metabolism in term infants fed human milk, whey-predominant formula, or cow’s milk formula. Pediatrics. 1985, 75:775–784. 215. Köhler L, Meeuwisse G, Mortensson W. Food intake and growth of infants between six and twenty-six weeks of age on breast milk, cow’s milk formula, or soy formula. Acta Paediatrica Scandinavica, 1984, 73:40–48. 216. Lönnerdal B, Forsum E, Hambraeus L. A longitu- dinal study of the protein, nitrogen, and lactose contents of human milk from Swedish well- nourished mothers. American Journal of Clinical Nutrition, 1976, 29:1127–1133. 217. Pao EM., Himes JM, Roche AF. Milk intakes and feeding patterns of breast-fed infants. Journal of the American Dietetic Association, 1980, 77:540–545. 218. Picciano MF et al. Milk and mineral intakes of breastfed infants. Acta Paediatrica Scandinavica, 1981, 70:189–194. 219. Rattigan S, Ghisalberti AV, Hartman PE. Breast- milk production in Australian women. British Journal of Nutrition, 1981, 45:243–249.
  • 47 220. Stuff JE et al. Sources of variation in milk and calorie intakes in breast-fed infants: implications for lactation study design and interpretation. American Journal of Clinical Nutrition, 1986, 43:361–366. 221. van Raaij JMA et al. Energy cost of lactation, and energy balances of well-nourished Dutch lactating women: reappraisal of the extra energy requirements of lactation. American Journal of Clinical Nutrition, 1991, 53:612–619. 222. Wood CS et al. Exclusively breast-fed infants: growth and caloric intake. Pediatric Nursing, 1988, 14:117–124. 223. Paul AA et al. Breast-milk intake and growth in infants from two to ten months. Journal of Human Nutrition and Dietetics, 1988, 1:437–450. 224. Prentice A et al. Cross-cultural differences in lactational performance. In: Hamosh M, Goldman AS, eds. Human Lactation 2: Maternal and Environmental Factors. New York, Plenum Press, 1986:13–44. 225. The quantity and quality of breast milk. Geneva, World Health Organization, 1985. 226. Gonzalez-Cossio T et al. Impact of food supplementation during lactation on infant breast- milk intake and on the proportion of infants exclusively breast-fed. Journal of Nutrition, 1998, 128:1692–1702. 227. van Steenbergen WM et al. Nutritional transition during infancy in East Java, Indonesia: 1. A longitudinal study of feeding pattern, breast milk intake and the consumption of additional foods. European Journal of Clinical Nutrition, 1991, 45: 67–75. 228. Frigerio C et al. A new procedure to assess the energy requirements of lactation in Gambian women. American Journal of Clinical Nutrition, 1991, 54:526–533. 229. Hennart P & Vis HL. Breast-feeding and post partum amenorrhoea in Central Africa. 1. Milk production in rural areas. Journal of Tropical Pediatrics, 1980, 26:177–183. 230. van Steenbergen WM, Kusin JA, van Rens MM. Lactation performance of Akamba mothers, Kenya. Breast feeding behaviour, breast milk yield and composition. Journal of Tropical Pediatrics, 1981, 27:161. 231. Motil KJ et al. Human milk protein does not limit growth of breast-fed infants. Journal of Pediatric Gastroenterology and Nutrition, 1997, 24:10–17. 232. Nielsen GA, Thomsen BL, Michaelsen KF. Influence of breastfeeding and complementary food on growth between 5 and 10 months. Acta Pædiatrica, 1998, 87:911–917. 233. Leerbeck E & Sondergaard H. The total content of vitamin D in human milk and cow’s milk. The British Journal of Nutrition, 1980, 44:7–12. 234. Reeve LL, Russell WC, DeLuca HF. Vitamin D of human milk: identification of biologically active forms. American Journal of Clinical Nutrition, 1982, 36:122–126. 235. Zoeren-Grobben DV et al. Human milk vitamin content after pasteurization, storage, or tube feeding. Archives of Disease in Childhood, 1987, 62:161–165. R E F E R E N C E S
  • SELECTED WHO PUBLICATIONS OF RELATED INTEREST Breastfeeding counselling – a training course, 1993 Document WHO/CHD/95.2 HIV and infant feeding • Guidelines for decision-makers Document WHO/FRH/NUT/CHD/98.1 http://www.unaids.org/unaids/document/mother-to-child/ infantpolicy.pdf • A guide for health care managers and supervisors Document WHO/FRH/NUT/CHD/98.2 http://www.unaids.org/unaids/document/mother-to-child/ infantguide.pdf • A review of HIV transmission through breastfeeding Document WHO/FRH/NUT/CHD/98.3 http://www.unaids.org./highband/document/mother-to-child/ hivmod3.pdf Complementary feeding: family foods for breastfed children 2000, iii + 52 pages WHO/NHD/00.1; WHO/FCH/CAH/00.6 In developing countries: Sw.fr. 7.70. Order no. 1930177 Complementary feeding of young children in developing countries A review of current scientific knowledge 1998, ix + 228 pages, WHO/NUT/98.1 Order no. 1930141 The optimal duration of exclusive breastfeeding. A systematic review http://www.who.int/child-adolescent-health/ New_Publications/NUTRITION/WHO_CAH_01_23.pdf The optimal duration of exclusive breastfeeding. Report of an expert consultation http://www.who.int/child-adolescent-health/ New_Publications/NUTRITION/WHO_CAH_01_24.pdf Global strategy for infant and young child feeding Fifty-fifth World Health Assembly, May 2002, document A55/15. http://www.who.int/gb/EB_WHA/PDF/WHA55/ea5515.pdf WHO Global Database on Growth and Malnutrition http://www.who.int/nutgrowthdb/ Infant feeding: the physiological basis 1990, 108 pages, ISBN 92 4 068670 3 Order no. 0036701 Protecting, promoting and supporting breast- feeding The special role of maternity services. A joint WHO/ UNICEF statement. 1989, iv + 32 pages, ISBN 92 4 156130 0 Order no. 1150326 Evidence for the ten steps to successful breastfeeding 1998, vi + 111 pages, WHO/CHD/98.9 Order no. 1930142 Hypoglycaemia of the newborn Review of the literature 1997, ii + 55 pages, WHO/CHD/97.1; WHO/MSM/97.1 Order no. 1930165 Promoting breast-feeding in health facilities 1996, 391 pages, 154 colour slides, eight training modules in loose-leaf binder, WHO/NUT/96.3 Order no. 1930100 The baby-friendly hospital initiative Monitoring and reassessment: tools to sustain progress 1999, four sections in a loose-leaf binder with computerized reporting system, WHO/NHD/99.2 Further information on these and other WHO publications can be obtained from Marketing and Dissemination World Health Organization 1211 Geneva 27, Switzerland e-mail: publications@who.int Direct fax: +41 22 791 4857 Phone: +41 22 791 2476 Links to related Web sites: http://www.who.int/nut/publications.htm http://www.who.int/child-adolescent-health
  • For further information please contact: Department of Nutrition for Health and Development (NHD) World Health Organization 20 Avenue Appia 1211 Geneva 27 Switzerland Tel: +41 22 791 3320 Fax: +41 22 791 4156 email: deonism@who.int website: www.who.int/nut This review, which was prepared as part of the background documentation for a WHO expert consultation, evaluates the nutrient adequacy of exclusive breastfeeding for term infants during the first 6 months of life. Nutrient intakes provided by human milk are compared with infant nutrient requirements. To avoid circular arguments, biochemical and physiological methods,independentofhumanmilk,areusedtodefinetheserequirements. The review focuses on human-milk nutrients, which may become growth limiting, and on nutrients for which there is a high prevalence of maternal dietary deficiency in some parts of the world; it assesses the adequacy of energy, protein, calcium, iron, zinc, and vitamins A, B6, and D. This task is confounded by the fact that the physiological needs for vitamins A and D, iron, zinc – and possibly other nutrients – are met by the combined availability of nutrients in human milk and endogenous nutrient stores. In evaluating the nutrient adequacy of exclusive breastfeeding, infant nutrientrequirementsareassessedintermsofrelevantfunctionaloutcomes. Nutrient adequacy is most commonly evaluated in terms of growth, but other functional outcomes, e.g. immune response and neurodevelopment, are also considered to the extent that available data permit. This review is limited to the nutrient needs of infants. It does not evaluate functional outcomes that depend on other bioactive factors in human milk, or behaviours and practices that are inseparable from breastfeeding, nor does it consider consequences for mothers. In determining the optimal duration of exclusive breastfeeding in specific contexts, it is important that functional outcomes, e.g. infant morbidity and mortality, also are taken into consideration. Department of Child and Adolescent Health and Development (CAH) World Health Organization 20 Avenue Appia 1211 Geneva 27 Switzerland Tel +41-22 791 3281 Fax +41-22 791 4853 email: cah@who.int website: http://www.who.int/child-adolescent-health
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 1/9 KellyMom Home Pregnancy Preparing to Breastfeed Breastfeeding when pregnant Breastfeeding Got Milk? What is Normal? Can I Breastfeed if…? Lifestyle choices Illness, Surgery & Medical Procedures Medications & Vaccines Herbs/natural treatments Chemical exposure Common Concerns Child Concerns Mother’s Concerns Finding Help Pumping & Employment Pumping & supply Feeding baby Milk handling/storage Employed moms Advocacy Ages & Stages Adoptive BF/ Relactation Newborn Breastfeeding Basics Common Newborn Concerns Older Infant After the First Year Tandem Breastfeeding BF FAQ: Tandem Tandem Articles Book: Tandem Nursing Weaning Considering weaning How to wean Parenting Parenting FAQ Nighttime parenting Reviews Health Baby’s Health Growth & Development Mom’s Health Can I Breastfeed if…? Nutrition
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 2/9 Solid Foods Mother’s Diet Vitamins/ Supplements Milk Fun Humor & Wisdom Trivia Store Handouts Free Handouts Professional Handouts Amazon Bookstore Logo Store How much expressed milk will my baby need? October 28, 2011. Posted in: Pumping issues By Kelly Bonyata, BS, IBCLC How much milk do babies need? Automatic milk calculator What if baby is eating solid foods? Is baby drinking too much or too little expressed milk? Other ways of estimating milk intake References Image credit: Jerry Bunkers on flickr How much milk do babies need? Like 5k More
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 3/9 Many mothers wonder how much expressed breastmilk they need to have available if they are away from baby. In exclusively breastfed babies, milk intake increases quickly during the first few weeks of life, then stays about the same between one and six months (though it likely increases short term during growth spurts). Current breastfeeding research does not indicate that breastmilk intake changes with baby’s age or weight between one and six months. After six months, breastmilk intake will continue at this same level until — sometime after six months, depending in baby’s intake from other foods — baby’s milk intake begins to decrease gradually (see below). The research tells us that exclusively breastfed babies take in an average of 25 oz (750 mL) per day between the ages of 1 month and 6 months. Different babies take in different amounts of milk; a typical range of milk intakes is 19-30 oz per day (570-900 mL per day). We can use this information to estimate the average amount of milk baby will need at a feeding: Estimate the number of times that baby nurses per day (24 hours). Then divide 25 oz by the number of nursings. This gives you a “ballpark” figure for the amount of expressed milk your exclusively breastfed baby will need at one feeding. Example: If baby usually nurses around 8 times per day, you can guess that baby might need around 3 ounces per feeding when mom is away. (25/8=3.1). Here’s a calculator so you don’t need to do the math… Milk Calculator (for the exclusively breastfed baby) Average number of feedings per day Calculate Reset Average per feeding, ounces Average per feeding, mL Low range, ounces Low range, mL High range, ounces High range, mL Notes: 1. Babies younger than one month old and babies who are more established on solid foods are expected to have a lower daily milk intake. 2. This calculator is based upon an average daily intake of 25 ounces, with a range of 19-30 ounces per day. Equivalent in mL is an average daily intake of 750 mL, with a range of 570-900 mL per day.
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 4/9 What if baby is eating solid foods? Sometime between six months and a year (as solids are introduced and slowly increased) baby’s milk intake may begin to decrease, but breastmilk should provide the majority of baby’s nutrition through the first year. Because of the great variability in the amount of solids that babies take during the second six months, the amount of milk will vary, too. One study found average breastmilk intake to be 30 oz per day (875 ml/day; 93% of total intake) at 7 months and 19 oz (550 ml/day; 50% of total energy intake) at 11-16 months. Several studies have measured breastmilk intake for babies between 12 and 24 months and found typical amounts to be 14-19 oz per day (400-550 mL per day). Studies looking at breastmilk intake between 24 and 36 months have found typical amounts to be 10-12 oz per day (300-360 mL per day). Is baby drinking too much or too little expressed milk? Keep in mind that the amount of milk that baby takes at a particular feeding will vary, just as the amount of food and drink that an adult takes throughout the day will vary. Baby will probably not drink the same amount of milk at each feeding. Watch baby’s cues instead of simply encouraging baby to finish the bottle. If your baby is taking substantially more than the average amounts, consider the possibility that baby is being given too much milk while you are away. Things that can contribute to overfeeding include: Fast flow bottles. Always use the lowest flow bottle nipple that baby will tolerate. Using bottle feeding as the primary way to comfort baby. Some well-meaning caregivers feed baby the bottle every time he makes a sound. Use the calculator above to estimate the amount of milk that baby needs, and start with that amount. If baby still seems to be hungry, have your caregiver first check to see whether baby will settle with walking, rocking, holding, etc. before offering another ounce or two. Baby’s need to suck. Babies have a very strong need to suck, and the need may be greater while mom is away (sucking is comforting to baby). A baby can control the flow of milk at the breast and will get minimal milk when he mainly needs to suck. When drinking from a bottle, baby gets a larger constant flow of milk as long as he is sucking. If baby is taking large amounts of expressed milk while you are away, you might consider encouraging baby to suck fingers or thumb, or consider using a pacifier for the times when mom is not available, to give baby something besides the bottle to satisfy his sucking needs. If, after trying these suggestions, you’re still having a hard time pumping enough milk, see I’m not pumping enough milk. What can I do? If baby is taking significantly less expressed milk than the average, it could be that baby is reverse-cycling, where baby takes just enough milk to “take the edge off” his hunger, then waits for mom to return to get the bulk of his calories. Baby will typically nurse more often and/or longer than usual once mom returns. Some
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 5/9 mothers encourage reverse cycling so they won’t need to pump as much milk. Reverse cycling is common for breastfed babies, especially those just starting out with the bottle. If your baby is reverse cycling, here are a few tips: Be patient. Try not to stress about it. Consider it a compliment – baby prefers you! Use small amounts of expressed milk per bottle so there is less waste. If you’re worrying that baby can’t go that long without more milk, keep in mind that some babies sleep through the night for 8 hours or so without mom needing to worry that baby is not eating during that time period. Keep an eye on wet diapers and weight gain to assure yourself that baby is getting enough milk. Ensure that baby has ample chance to nurse when you’re together. Other ways of estimating milk intake There are various ways of estimating the amount of milk intake related to the weight of the baby and the age of the baby, based upon formula intake – research has shown that after the early weeks these methods overestimate the amount of milk that baby actually needs. These are the estimates that we used for breastfed babies for years, with the caveat that most breastfed babies don’t take as much expressed milk as estimated by these methods. Current research tells us that breastmilk intake is quite constant after the first month and does not appreciably increase with age or weight, so the current findings are validating what moms and lactation counselors have observed all along. The Milk Calculator from the The Adoptive Breastfeeding Resource Website does this type of estimation. More: Breast Versus Bottle: How much milk should baby take? By Nancy Mohrbacher, IBCLC, FILCA Supplementation Guidelines from LowMilkSupply.org References Onyango, Adelheid W., Receveur, Olivier and Esrey, Steven A. The contribution of breast milk to toddler diets in western Kenya. Bull World Health Organ, 2002, vol.80 no.4. ISSN 0042-9686. Salazar G, Vio F, Garcia C, Aguirre E, Coward WA. Energy requirements in Chilean infants. Arch Dis Child Fetal Neonatal Ed. 2000 Sep;83(2):F120-3. Kent JC, Mitoulas L, Cox DB, Owens RA, Hartmann PE. Breast volume and milk production during extended lactation in women. Exp Physiol. 1999 Mar;84(2):435-47. Persson V, Greiner T, Islam S, and Gebre-Medhin M. The Helen Keller international food-frequency method underestimates vitamin A intake where sustained breastfeeding is common. Food and Nutrition Bulletin, vol.19 no.4. Tokyo, Japan: United Nations University Press, 1998. Cox DB, Owens RA, Hartmann PE. Blood and milk prolactin and the rate of milk synthesis in women. Exp Physiol. 1996 Nov;81(6):1007-20. Dewey KG, Heinig MJ, Nommsen LA, Lonnerdal B. Maternal versus infant factors related to breast milk intake and residual milk volume: the DARLING study. Pediatrics. 1991 Jun;87(6):829-37.
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 6/9 Neville MC, et al. Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactation. Am J Clin Nutr. 1988 Dec;48(6):1375-86. Dewey KG, Finley DA, Lonnerdal B. Breast milk volume and composition during late lactation (7-20 months). J Pediatr Gastroenterol Nutr. 1984 Nov;3(5):713-20. Butte NF, Garza C, Smith EO, Nichols BL. Human milk intake and growth in exclusively breast-fed infants. J Pediatr. 1984 Feb;104(2):187-95. Dewey KG, Lonnerdal B. Milk and nutrient intake of breast-fed infants from 1 to 6 months: relation to growth and fatness. J Pediatr Gastroenterol Nutr. 1983;2(3):497-506. Brown K, Black R, Robertson A, Akhtar N, Ahmed G, Becker S. Clinical and field studies of human lactation: methodological considerations. Am J Clin Nutr 1982;35:745-56. Jelliffe D, Jelliffe E. The volume and composition of human milk in poorly nourished communities: a review. Am J Clin Nutr 1978;31:492-515. Summary of Research Data Baby’s Age Average Milk Intake per 24 hours Reference g ml oz 5 days 498 +/- 129 g 483 ml 16 oz Neville 1988 1 mo 728 g 706 ml 24 oz Salazar 2000 1 mo – 673 ml 23 oz Dewey 1983 1 mo 708 +/- 54.7 g 687 ml 23 oz Cox 1996 1-6 mo 453.6+/-201 g per breast 440 ml x2 = 880 ml 30 oz Kent 1999 3 mo 818 g 793 ml 27 oz Dewey 1991 3-5 mo 753 +/- 89 g 730 ml 25 oz Neville 1988 6 mo – 896 ml 30 oz Dewey 1983 6 mo 742 +/- 79.4 g 720 ml 24 oz Cox 1996 7 mo – 875 ml (93% of total energy intake) 30 oz Dewey 1984 11-16 mo – 550 ml (50% of total energy intake) 19 oz Dewey 1984 11-16 mo 502 +/- 34 g 487 ml (32% of total energy intake) 16.5 oz Onyango 2002 12-17 mo 563 g 546 ml 18 oz Brown 1982 12-23 mo 548 g 532 ml 18 oz Persson 1998 15 mo 208.0+/-56.7 g per breast 202 ml x2 = 404 ml 14 oz Kent 1999 18-23 mo 501 g 486 ml 16 oz Brown 1982 >24 mo 368 g 357 ml 12 oz Brown 1982 24-36 mo 312 g 303 ml 10 oz Persson 1998 Specific Gravity of Mature Human Milk = 1.031, so Density of Mature Human Milk ~ 1.031 g/ml;1 oz = 29.6 ml;Numbers in gray were derived using the above conversion factors.
  • 8/15/13 How much expressed milkwill mybabyneed? : KellyMom kellymom.com/bf/pumpingmoms/pumping/milkcalc/ 7/9 Milk vs. formula… under the microscope Happy World Breastfeeding Week! Breastfeeding Helplines 29 You might also like: LinkWithin Enter Text & Click to Search Do you have a Breastfeeding or Parenting Question? Visit Our Mother-to-Mother Support Group on Facebook! Forum Archives about At KellyMom.com, our goal is to provide support & evidence-based information on breastfeeding, sleep and parenting. I am the mother of three lovely children, and I am an International Board Certified Lactation Consultant (IBCLC). I hope that my articles are helpful and encouraging. Thanks for visiting! Read more → Search LactMed Search National Library of Medicine Get this widget ShareShareShare ShareShareMore
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