Normal Growth, Growth Faltering, and Obesity in Breastfed Infants

General Considerations

The growth of exclusively breastfed infants has become the focus of much interest among pediatricians, researchers, and nutritionists. Historically, the Boyd-Orr cohort study in the 1920s and 1930s showed that breastfed children were taller in childhood and adulthood. ¹ Stature was associated with health and life expectancy. Adult leg length is very sensitive to environmental factors and diet in early childhood because this is the time of most rapid leg growth. Leg length has been used as the best measurement of growth progress. After infancy, chest growth is rapid before puberty and is sensitive to stress and illness.

A number of long-range follow-up studies were initiated to address the issues of growth during the critical first year of life, when brain growth is greater than it ever will be again in postnatal life. The issues of malnutrition and stunting continued to plague children worldwide. An interest in height and weight increments and ratios is only part of the concern about obesity and the long-range issues of adiposity. Does breastfeeding protect against adult obesity? Does human milk protect against hypercholesterolemia or dyslipidemia in adult life? The questions are clear, but the answers are not unless one assumes the teleologic approach: human milk is ideal for human infants, with its low protein, controlled calories, and persistent unchangeable cholesterol.

Other questions were raised regarding optimal growth: “Is it safe to overfeed an infant with formula?” “Is it safe to deprive an infant of cholesterol during a period of critical brain growth when brain growth depends on cholesterol?” and “When infants are deprived of cholesterol in early infancy, are they less able to tolerate it later?” This question is significant because infant formulas do not contain cholesterol deliberately.

Antiquated data and anthropometric standards based on that data have led to the belief that the growth curves and tables of normal height and weight do not reflect the growth of most healthy, well-fed breastfeeding infants. ² Reliability of weight gain as a measure of growth has developed because it is a measurement easily obtained. Measurement of length, however, is considered a better standard. ³ Weight gain and linear growth are not always correlated. Furthermore, during infancy and childhood, the lower leg grows at a higher rate than the rest of the body. Knee-heel length can be expressed as a percentage of total length and increases with age: 25% at birth, 27% at 12 months, and 31% in adult life. During several decades of formula feeding, “normal” growth curves were developed based only on formula-fed infants. These curves reflected how children grew “on average” of tall and short, fat and thin, and sick and well children. The curves did not reflect optimal growth of infants and children afforded optimal nutrition in a nurturing environment to achieve their growth potential.

The First 1000 Days: Nutrition and Growth

Along with recognizing the effects of malnutrition in infancy and early childhood leading to increased mortality in children younger than 5 years and morbidities associated with stunting and malnutrition, several other issues are clear. There is a crucial window for brain growth in the first several years of life and the effects early malnutrition might have on that growth. Early-life obesity leads to obesity in adolescents and adults with all the associated morbidities. Maternal prenatal nutrition also seems to influence growth in infancy and early childhood with a real potential for affecting longer term health. The first 1000 days of life (280 days+365 days+355 days= 1000), roughly the time from conception through an infant’s second birthday, coincides with the brain’s essential early growth and development and the establishment of physical growth, immune function, and other metabolic features consistent with long-term health or disease. In fact, the first 1000 days of life are susceptible to two major threats undernutrition/malnutrition (related to poverty, food insecurity, poor sanitation, etc.) and “overnutrition” and the risk for obesity (related to food excess, unbalanced diets, and inadequate nutritional understanding/education). ⁴ , ⁵ , ⁶ , ⁷ The United Nations International Children Education Fund (UNICEF), the World Health Organization (WHO), and World Bank Group track malnutrition worldwide in its various forms: stunting, wasting, and overweight. ⁸ Inroads have been made for “good nutrition” since 2000, with declines worldwide in malnutrition. ⁸ Current estimates for 2018 include 149 million children under 5 affected by stunting, 49 million children under 5 with wasting, and 40 million children under 5 years of age estimated to be overweight. These dire estimates exist despite the recommendations that exclusive breastfeeding should be provided for the first 6 months of life and continued through 12 to 24 months of age or longer, that whole cow milk be diminished or removed from an infant’s diet, and the introduction of appropriate complementary solid foods should occur at 6 months of age and older. Despite these recommendations by various health groups, including the WHO and UNICEF, the question remains concerning implementation, uptake, and support of these recommendations by governments, physicians, health care workers, and families.

Comparison of Formula-Fed Versus Breastfed Growth

Formula-fed infants gain more rapidly in weight and length during the first months of life than do breastfed infants. ⁹ Therefore evaluating an infant’s physical growth by standards set by bottle-fed infants predisposes one to the diagnosis of failure to thrive for breastfed infants.

Forman et al. ¹⁰ reported a longitudinal study of breastfed and bottle-fed infants during the first few months of life that demonstrated the 10th and 90th percentile values for weight and length of the two groups were similar at birth, and the 10th percentile values of the two groups were similar at age 112 days. The significant difference was in the values for the 90th percentile. Bottle-fed infants were above this percentile in substantially greater numbers. These differences were attributed to caloric intake rather than the difference in composition of the diet. Fomon et al. ¹¹ showed that the bottle-fed infant not only gains more in weight and length, but also gains more weight for a unit of length. Per the authors and others, this gain reflects the overfeeding of the bottle-fed infants.

Most studies of growth in breastfed infants have been plagued with the problem of variation in the definition of “breastfed” (exclusive, almost exclusive, partial breastfeeding, token), the amount of formula supplementation, and the occurrence of partial weaning.

The effects on growth of specific protein and energy intake in 4- to 6-month-old infants who were either breastfed or formula fed with high and low protein were measured by Axelsson et al. ¹² No significant differences were found in the growth rate of crown-heel length and head circumference or weight gain. The authors concluded that the differences in protein intake between breastfed and formula-fed infants without differences in growth indicate that the formulas may provide a protein intake in excess of the needs. When milk intake and growth in exclusively breastfed infants were carefully documented in the first 4 months by Butte et al., ¹³ energy and protein intakes were substantially less than current nutrient allowances. Infant growth progressed satisfactorily when compared with National Center for Health Statistics (NCHS) standards, despite that energy ingested by breastfed infants dropped from 110±24 kcal/kg per day at 1 month to 71±17 kcal/kg per day at 4 months. ¹³ Similarly, protein intake decreased from 1.6±0.3 g/kg per day at 1 month to 0.9±0.2 g/kg per day at 4 months. Reevaluation of protein and energy requirements is essential.

Weight-for-length and weight gain were significantly correlated with total energy intake but not with activity level during the first 6 months of life in breastfed infants studied by Dewey et al. ¹⁴ , ¹⁵ Energy intake was considerably lower than recommended—85 to 89 kcal/kg per day—when compared with the 115 kcal/kg per day recommended dietary allowances of the National Academy of Sciences in 1980. ¹⁶ Presently energy recommendations for infants 0–3 months of age suggested by the National Academy of Medicine (formerly the Institute of Medicine) are expressed as (89×weight[kg]−100)+175 kcal.

Infants who consumed the most breast milk became the fattest. A 4-kg infant would require 105 kcal/kg per day.

When patterns of growth are examined in the infants of marginally nourished mothers, weight gain is comparable to a reference population but does not permit recovery of weight differential at birth, which occurs in infants who are small for gestational age (SGA). ¹⁷ The intakes of energy and protein by individual infants were reflected in their weight gain but were below internationally recommended norms. ¹⁸ Maternal milk alone, when produced in sufficient amounts, can maintain normal growth up to the sixth month of life. Exclusive breastfeeding in Chilean infants of low-middle and low socioeconomic families produced the highest weight gain and practically no illness or hospitalization. ¹⁹

In the Copenhagen Cohort Study in 1994, exclusively breastfed term infants had a mean intake of 781 and 855 mL/24 hours at 2 and 4 months, respectively. ²⁰ The median fat concentration of human milk was 39.2 g/L and was positively associated with maternal weight gain during pregnancy. This supports the concept that maternal fat stores laid down during pregnancy are easier to mobilize during lactation than other fat stores. This may limit milk fat when pregnancy fat stores are exhausted.

In addition to recognizing the importance of genetic, metabolic, and environmental influences in producing significant differences in growth patterns, Barness suggests that recommendations for nutrition of healthy neonates may be too high for some and too low for others. ²¹ However, the benchmark for nutritional requirements of the full-term infant remains milk from the infant’s healthy, well-nourished mother.

Gain in physical growth is not as critical as gain in brain growth, but measurements of brain growth are only indirectly implied from growth of the head. In evaluating any infant’s progress, head circumference is an important consideration, especially in the first year of life. Deceleration in the rate of increase in head circumference occurs over the first year. The head circumference increases approximately 7.5 cm (3 inches) in the first year of life and another 7.5 cm in the next 16 years of life. When growth failure includes failure of head growth, the growth failure is severe. However, many other factors independent of body growth influence head growth.

Weight Loss in the First Week of Life (Formula-Fed Versus Breastfed Infants)

A weight loss of 3% to 5% is usually accepted as the norm for formula-fed infants in the first week of life, although supporting information in pediatric textbooks is meager. A loss of 5% to 7% is average for breastfed infants, with a nadir of weight loss at 2 to 4 days of life. When the weight loss continues to progress toward 10% or more or the weight loss continues to drop after day 3 or 4 of life, the clinician should be alerted to this and the breastfeeding process and milk ingestion carefully assessed, adjustments made, and intake followed to document a reversal of the weight loss. Macdonald et al. documented this difference in weight loss between formula-fed and breastfed infants ( n =937, 45% breastfed, 42% formula fed, and 13% mixed feeding), noting the median weight loss for formula-fed infants was 3.5% of birth weight and 6.6% for breastfed infants. ²² Weight loss for breastfed infants at the 95th centile (11.8% loss) and the 97.5th centile (12.8% loss) exceeded 10%, although it was rare for a formula-fed infant to lose 10% of birth weight. There were distinct differences in the time to recovery of birth weight: for breastfed infants median 8.3 days, 95th centile 18.7 days, 97.5th centile 21 days; formula-fed infants median 6.5 days, 95th centile 14.5 days and 97.5th centile 16.7 days. Additional studies confirmed these weight loss differences between formula-fed and breastfed infants and pointed to specific variables associated with “excess weight loss,” including cesarean birth, absence of labor before delivery, lower gestational age, higher birth weight, intrapartum fluid balance, and delayed lactogenesis. ²³ , ²⁴ , ²⁵ Systematic reviews reinforced the information, although there were concerns about methodologic flaws, such as gaps in data, poorly documented feeding groups, etc. ²⁶ For the breastfed infants, there was also evidence of supplementation with formula because of the concern for weight loss or concern for delayed lactogenesis. Along with this came concerns of interrupting exclusive breastfeeding and precipitation of stopping breastfeeding.

One group from the Northern Kaiser Permanente Hospitals studied early weight loss in both breastfed and formula-fed infants in an hour-by-hour analysis in hopes of facilitating detection of those infants at risk for an adverse outcome and in need of early intervention/assistance. Flaherman et al. published data for 108,907 exclusively breastfed newborns, with 83,433 by vaginal delivery and 25,474 delivered by cesarean. ²⁷ They reported that almost 5% of vaginally delivered infants and over 10% of infants from cesarean deliveries lost 10% or more of their birthweight 48 hours after delivery. Over 25% of infants from cesarean deliveries had lost more than 10% of their birth weight by 72 hours of age. They developed nomograms of early weight loss by hour over the first 72 hours, separately for vaginal and cesarean deliveries. (See Appendix F .) Subsequently Drs. Paul, Flaherman, and Schaefer in collaboration with a group of US academic centers created a tool for assessing and tracking breastfed infant weight loss in the first 72 to 96 hours of life. An online calculator (Newborn Weight Tool, NEWT, https://www.newbornweight.org ) is available for doing this. ²⁸ In subsequent work the same group developed similar nomograms for formula-fed newborns. ²⁹ They have gone on to validate the use of these nomograms and track early weight loss with breastfeeding outcomes through 1 month of age and health care usage relative to feeding mode and early weight loss. ³⁰ , ³¹ , ³²

It is impossible to predict which infants will be adversely affected by “excessive” early weight loss or the amount of weight loss or the timing of weight loss in an individual infant. It is possible to recognize risk factors for excessive weight loss, and it is possible to diagnose delayed lactogenesis and identify infants in need of supplementation. The Academy of Breastfeeding Medicine (ABM) has reviewed the issue of supplementary feedings for the healthy term infant, indications for supplementation, nonindications, ways to prevent the need for supplementation, and how to supplement and support continued breastfeeding if possible in their protocol on supplementation. ³³

They emphasize not blindly pushing on with breastfeeding, but rather pausing to truly assess the mother’s milk production, goals for breastfeeding, and evidence that the infant is or is not receiving adequate milk. Dr. B. Phillip and Dr. C. Rosen-Carole, faculty members of the ABM, offer their approach to this dilemma in an online discussion at Baby-Friendly USA ( https://www.babyfriendlyusa.org/news/what-should-happen-when-baby-does-not-get-enough-milk-from-mom/ ). ³⁴ Assess the infant by looking for signs that the infant is sleeping normally, easily takes to the breast, and appears satisfied with the feedings, demonstrating both early feeding cues and satiety without fussiness or hypersomnolence, good activity, and good urine output and stool frequency. There should be no signs or symptoms of dehydration, no excessive weight loss (use the nomograms or online NEWT weight tool [see Appendix F ]), and no evidence of hypoglycemia, abnormal electrolytes, or hyperbilirubinemia. Assess the mother’s milk production (breast fullness, let-down, milk leaking, and prefeeding and postfeeding breast changes), breast glandular sufficiency, history of breast pathologic condition or prior surgeries that might interfere with milk production/delivery. Check for temporary cessation of breastfeeding or separation of mother and baby without ongoing available breast milk for the infant, possible interference with milk production by maternal medications, or intolerable pain during feeding without relief from appropriate interventions. Always directly observe the mother and infant breastfeeding, checking positioning and latch and observing for success or difficulty. If the infant is not getting enough milk, the infant should be fed. Act to ensure the safe feeding of the infant at the same time as respecting the mother’s (and family’s) desires and plans for breastfeeding. If the mother is committed to breastfeeding, “bridge the gap,” “feed the baby,” “support the mother,” and “don’t undermine breastfeeding.” ³⁴ Supplementing, if necessary, then becomes part of appropriate medical care by (1) thinking about why the baby is being supplemented (indication[s] and expected outcome measures), (2) considering how much to supplement, (3) deciding what to supplement with (expressed breastmilk, donor breast milk, or formula), (4) deciding how to feed the infant (cup, syringe, bottle, or supplemental nursing system), (5) continuing or reinitiate breastfeeding (continue breast milk expression and use or storage), and (6) planning for follow-up and documentation of successful feeding and weight gain by the infant. ³⁴

Growth of Breastfed Infants

Dewey et al. suggested that new, separate growth charts are needed for breastfed infants. ¹⁵ , ³⁵ , ³⁶ The Davis Area Research on Lactation, Infant Nutrition, and Growth (DARLING) Study collected data prospectively on growth patterns, nutrient intake, morbidity, and activity levels of matched cohorts of infants who were either exclusively breastfed or bottle fed during the first 12 months of life. Measurements were followed beyond 12 months to 18, 21, 24, and 36 months as well. Growth in length and head circumference did not differ significantly between the two groups; however, weight gain was slower among breastfed infants after approximately 3 months of age. These weight gain differences continued even after solid foods were added at 6 months in both groups. Breastfed infants were leaner than their counterparts. The slower growth rates and lower energy intake of the breastfed infants were associated with normal or accelerated development and less morbidity from infectious illnesses. The authors concluded that it is normal for breastfed infants to gain at this pace, which is less rapid than that indicated by the scales developed for bottle-fed infants. ³⁵

When the growth patterns of a large sample of breastfed infants were pooled from the United States, Canada, and Europe, Dewey et al. reported that results were consistent across studies. ¹⁵ , ³⁵ , ³⁶ Breastfed infants grew more rapidly in weight during the first 2 months and less rapidly over 3 to 12 months. Head circumference was well above the WHO/Centers for Disease Control and Prevention (CDC) median throughout the first year. Length-for-age did not decline, nor did the weight-for-age and weight-for-length scores as breastfeeding increased in duration.

Garza et al. reviewed growth patterns of breastfed infants. Breastfed infants clearly consumed less energy than recommended by WHO in the second 3-month period by choice and not because the mother could not produce more milk. ³⁷ Dewey et al. first pointed this out when they had mothers pump to increase their production and found the infants self-regulated to the original intake measured before the pumping program in spite of the fact that the mother was producing more milk. ¹⁴ , ³⁸ Many researchers at that time recommended separate growth curves for exclusively breastfed infants.

International Growth Standards

It became clear that growth curves developed by the CDC were averages taken from bottle-fed infants, mostly overfed, fat and thin, tall and short, sick and well. They reflected how children grew on the average as predominately formula-fed infants. The WHO convened an international committee of experts to develop a model for how breastfed children should grow. Data were collected from six countries of widely divergent populations from stable families who breastfed exclusively for 6 months and continued breastmilk for a minimum of a year and longer. The infants had access to health care and good housing. This multicenter growth reference study involved 8440 children 0 to 5 years of age from Brazil, Ghana, India, Norway, Oman, and the United States (Sacramento, California). ³⁹ , ⁴⁰ The sample had ethnic or genetic variability in addition to cultural variation in how the children were nurtured, strengthening the standard’s universal applicability. One remarkable observation was that all the children grew at the same pace; curves could be superimposed, regardless of racial or ethnic background or geographic region. The observations confirmed the thought that children in a healthy environment can achieve their genetic growth potential regardless of poverty, ethnicity, or culture. The charts differ from the CDC growth charts, especially for the first 2 years of life, in which formula-fed infants show greater weight gain, which averages that the formula-fed infant is 600 to 650 g heavier at 12 months of age. Differences in length are minimal, and, therefore, breastfed infants are lower in weight-for-length measurements and other indices of fatness. Breastfed individuals are not shorter in adult life but are less likely to be obese. Assessment of sex differences and heterogeneity in motor milestone attainment among populations in the multicenter study supports the appropriateness of pooling data from all sites and both sexes for the purpose of an international standard. Six gross motor milestones were used: sitting without support, hands-and-knees crawling, standing with assistance, walking with assistance, standing alone, and walking alone. The WHO child growth standards depict normal growth under optimal environmental conditions for nutrition and growth and can be used to assess children everywhere, regardless of ethnicity, socioeconomic status, and type of feeding. They represent how children should grow globally. ⁴¹ , ⁴²

The recommendation for use of the WHO charts by the CDC states the following for infants under 24 months: use the WHO growth charts recognizing the values 2 standard deviations above and below the median, or the 2.3rd and 97.7th percentiles (labeled) as the 2nd and 98th percentile for possible recognition of children whose growth indicates an adverse health condition. The rationale for this use is recognition that breastfeeding is the recommended standard for infant feeding and, unlike the CDC charts, the WHO growth charts reflect patterns of breastfed infants for at least 4 months and still breastfeeding at 12 months, and all the data are based on a high-quality study (Multicentre Growth Reference Study [MGRS]). ⁴³

The continued use of CDC charts from 24 to 59 months is recommended because the charts extend out to 20 years, whereas WHO charts cover 0 to 59 months. Switching at 24 months is explained because of the transition at 24 months from measuring recumbent length to standing height. Nevertheless, the WHO charts reflect optimal growth whereas the CDC charts reflect population averages.

Impact of Weaning Foods on Growth

Weaning foods is a term used by breastfeeding practitioners, but the infant nutrition community uses the term complementary foods ; foods that complement breast milk. As an infant approaches 6 months of age, the stores of iron are diminishing and iron in human milk is not sufficient to meet needs; likewise, the once high levels of stored zinc are diminishing and the levels of zinc in human milk are decreasing. Thus complementary foods need to contain iron and zinc, as most meats and fortified cereals do. ⁴⁴ Krebs et al. found low measurements of iron and zinc levels in breastfeeding infants at 6 months; when meat was added as a weaning food, levels increased toward normal. ⁴⁵ Routine assessment of iron and zinc levels increased toward normal. Routine assessment of iron and zinc levels is not practical; therefore the Committee on Nutrition recommends fortified cereal or infant-style meats as weaning food. ⁴⁶

The transition from breast milk to a reliance on the calories and nutrients of complementary foods also depends on the infant’s developmental readiness to eat solid or semisolid foods. Some of the signs of developmental readiness include ability to sit without support, good head control, opening of the mouth when food is presented, and decreased extrusion reflex. Other signs of readiness are behaviors that demonstrate being unsatisfied after breast milk or formula feeding, demonstrated interest in what the caregiver is eating, and displaying cues that they are done eating by turning their head away or refusing additional food.

The timing of initiation of weaning foods before 6 months of age has shown that as energy intake increases from solid foods, energy intake from breast milk decreases. The downward trend of weight-to-age and weight-to-length ratios continues with the addition of solids, which would not be expected if growth faltering were the basis for the decline. ³⁷ Breastfed infants apparently self-regulate when offered solids in part by leaving some solids uneaten. When breastfed infants were given solids between 4 and 7 months, their weight-for-age and weight-for-length were consistently lower than those for infants introduced to solids at 8 months or older. Length-for-age was similar between the two groups.

Does the growth rate of exclusively breastfed infants reflect a need for increased protein? ⁴⁷ This question has challenged the wisdom of exclusive breastfeeding. A group of exclusively breastfed infants were matched with a second group who received prepared solid foods, including egg yolk, beginning at 4 months of age. ³⁸ Neither weight gain nor length gain from 4 to 6 months differed between the groups. The solid-food group received 20% higher protein intake as well as higher intakes of iron, zinc, calcium, vitamin A, and riboflavin. The authors concluded that protein intake is not a limiting factor in the growth of breastfed infants. ³⁸ , ⁴⁷

Similarly, Cohen et al. ⁴⁸ demonstrated that breastfed infants given solids at 4 months self-regulated so that the energy intake and protein intake were the same in both the supplemented group and the unsupplemented group. When Motil et al. calculated the gross efficiency of nutrient usage for each infant in a longitudinal study of breastfed and bottle-fed infants, length and weight gains and lean body mass and body fat accretion during the first 24 weeks of life were similar. ⁴⁹ The formula-fed infants had received significantly higher nitrogen and energy. The gross efficiency of dietary energy usage for lean body mass deposition was two times greater in breastfed than bottle-fed infants. No association was found between lean body mass deposition and dietary protein intake. This confirms previous studies that human milk protein does not limit growth. ⁴⁹ Breastfed infants self-regulate their energy intake at lower levels than formula-fed infants. Body temperature and metabolic rates are lower in breastfed infants. ⁵⁰

Recommendations for Optimal Duration of Exclusive Breastfeeding

Recommendations for optimal duration of exclusive breastfeeding have been controversial. ⁵⁰ The WHO has revised its recommendation for both developed and developing countries to promote exclusive breastfeeding for 6 months. ⁴⁰ Kramer and Kakuman provide a comprehensive review of the literature, including both controlled clinical trials and observational studies in any language comparing exclusive breastfeeding to exclusive breastfeeding for less time with mixed feeding for at least 6 months. ⁵¹ The health outcomes reported included growth, iron and zinc status, infectious morbidity, atopic disease, neuromotor development, rate of postpartum maternal weight loss, and duration of lactational amenorrhea. The conclusions were that exclusive breastfeeding for 6 months resulted in lower risk for gastrointestinal infection and no growth deficits. In concert with the WHO, the section on breastfeeding of the American Academy of Pediatrics (AAP) promotes exclusive breastfeeding for 6 months. The WHO recommends the need for animal source foods and fruits and vegetables in the initial period of 6 to 9 months of age, as demonstrated in the MGRS. ³⁹ , ⁴¹ , ⁴²

Prolonged Breastfeeding

Considerable controversy surrounds the question of prolonged breastfeeding. Although the value of prolonged breastfeeding has not been challenged in industrialized countries, it has in developing countries. When the fat and energy content were measured in 34 mothers of healthy term infants who had been lactating for more than a year (12 to 39 months) and compared with the milk of control mothers who had been lactating for 2 to 6 months, levels were significantly increased in fat and energy content. The elevated levels did not correlate with maternal age, diet, body mass index (BMI), or number of daily feedings. ⁵² Another analysis of breastmilk macronutrient content in prolonged lactation (women breastfeeding for ≥18 months) demonstrated that fat and protein increased and carbohydrates decreased compared with expressed milk of mothers breastfeeding for less than 12 months. ⁵³ Some studies showed that small, undergrown infants are breastfed longer. ⁵⁴ , ⁵⁵ Careful assessments reveal that larger infants are weaned earlier. A cautious review of available studies suggests that prolonged breastfeeding does not cause malnutrition; rather, the small and undergrown infants are kept at the breast longer. Child size appears to be related to the decision to wean so that, in general, large healthy infants are weaned completely from the breast earlier. ⁵⁴ Thus smaller infants being breastfed longer is not the cause of the undergrowth. The effect of prolonged breastfeeding on growth has been an issue of concern and been evaluated, especially in developing countries. ¹⁰ , ³⁵ In a review of 13 studies, Grummer-Strawn pointed out in 1993 that 8 reported a negative relationship, 2 had a positive relationship, and 3 had mixed results. ⁵⁶ Grummer-Strawn identified the flaws in study design and suggested that until better information is available, women should nurse as long as possible because the benefits to infant health (infection protection) exceed the risks in these geographic areas. ⁵⁶ Kramer et al. used three analytic approaches (intention-to-treat, observational [as fed], and instrumental variable [randomization as the instrument to create more than 12 months of breastfeeding]) to examine the relationship between prolonged lactation and infant growth. ⁵⁷ The observational approach of analysis of the data from the same children indicated an opposite causal inference compared with the other two approaches. The authors concluded that slower previous growth may have led to prolonged breastfeeding and is an example of apparent reverse causality. Hopefully, future study will accurately define the issue of causality related to prolonged breastfeeding and infant growth.

Catch-Up Growth in Small-for-Gestational-Age Infants

SGA infants have been identified as being at risk for continued growth failure in extrauterine life, learning difficulties, and behavioral problems. Lucas et al. ⁵⁸ explored the influence of early nutrition on growth in the first year of life in full-term SGA infants, comparing those receiving breast milk with those receiving formula. This was a subset of a study on early carnitine supplementation. An equal number of breastfed and formula-fed infants received carnitine. Additional demographic, social, clinical, and anthropometric data were collected. Breastfeeding was associated with a greater increase in weight at 2 weeks and 3 months of age, which persisted beyond the actual breastfeeding period. The authors reported greater catch-up growth in head measurement and a greater increase in body length in the breastfed infant. They suggest that breastfeeding promotes faster catch-up growth, and breastfed infants have the potential for improved catch-up growth in developmental parameters as well. ⁵⁸

In a study designed to examine the role of zinc supplementation in catch-up growth in SGA infants, Castillo-Duran et al. reported that infants who were exclusively breastfed had increased growth compared with those who were formula fed and supplemented with zinc. ⁵⁹ A recent study of premature SGA infants demonstrated the benefits of an exclusive human milk–based diet. The 18 SGA infants demonstrated good catch-up growth at 2 years of age without evidence of insulin resistance of increased adiposity compared with the 33 premature infants who were appropriate for gestational age. ⁶⁰ One systematic review by Santiago et al., reported from an analysis of seven articles of term infants, SGA, and breastfed (compared with high-calorie formula feeding) that the breastfed infants’ catch-up growth was without body composition alteration or increased insulin resistance. ⁶¹ They did report variability in type of evaluations completed and age of the infants at time of assessment. Campisi et al. reported in their systematic review that there was significant variability in the definitions of SGA, catch-up growth, and measured growth outcomes such that their conclusions were regarding the need for standardization of definitions, measurement, and follow-up. ⁶² They did recommend the use of international standards for fetal growth and infant size to facilitate agreed-on definitions and measurements. ⁶³ Other groups have recommended nutritional assessment in a practical approach applicable to preterm infants and SGA infants. They propose specific anthropometric measurements (weight gain velocity, body weight, body length, head circumference, mid-upper arm circumference, skinfolds, weight-to-length ratio, BMI, ponderal index) and biochemical markers (glucose, iron, ferritin, protein, BUN, serum prealbumin), serum transferrin, retinol-binding protein, serum calcium, phosphate, alkaline phosphatase, urinary calcium, and phosphate markers) to be tracked. ⁶⁴ They include references to the use of these measurements, techniques and instrumentation, and reference values. ⁶⁵ , ⁶⁶

Cognitive and Motor Development

Cognitive and motor development are intimately tied to growth in infants and children and essential to any definition of optimal growth and basic measurement of achieving human potential. Cognitive development in the first 7 years of life was related to breastfeeding practices of a birth cohort in New Zealand. ⁶⁷ The researchers took into account maternal intelligence, maternal education, maternal training in child rearing, childhood experiences, family socioeconomic status, birth weight, and gestational age. The breastfed children had slightly higher test scores on the Peabody Picture Vocabulary Test, the 5-year measure on the Stanford Binet Intelligence Scale, and the 7-year measure on the Wechsler Child Intelligence Scale. Measures of language development were equally influenced. This very small improvement in scores persisted when adjustments were made for all variables. The scores were also influenced by length of breastfeeding less than and longer than 4 months.

An additional study on the same birth cohort was done to assess breastfeeding and subsequent social adjustment in 6- to 8-year-old children. Fergusson et al. studied prospectively 1024 children who were part of the Christchurch Child Development Study. They used the maternal and teacher ratings of childhood conduct disorders. ⁶⁸ A statistically significant tendency for conduct disorder scores declined with increasing duration of breastfeeding; that is, breastfed children were less prone to conduct disorders than bottle-fed children. Breastfed children, however, tended to come from slightly more socially advantaged, economically privileged homes that were more stable. The analysis failed to examine early mother–infant interaction patterns.

This cohort of 1000 individuals now has been reported as an 18-year longitudinal study by Horwood and Fergusson. ⁶⁹ A small but detectable increase in child cognitive and educational achievement in the children who had been breastfed as infants was still seen. The results were confirmed in standardized tests, teacher ratings, and academic outcomes in high school and young adulthood.

De Andraca and Uauy ⁷⁰ reviewed the factors in human milk and the breastfeeding process that affect optimal mental and visual development. The complex relationships point to a clear advantage to breastfeeding.

The relationship of infant-feeding practices and dependent variables to the subsequent cognitive abilities were reported from the Yale Harvard Research Project in Tunisia. ⁷¹ Within the underprivileged group, they found that breastfeeding promoted not only physical growth but also sensor motor development as assessed by Bayley motor and mental scales. No great differences were found in the ability to sit alone or to take first steps, but especially among boys in the lower socioeconomic group, significant superiority of breastfed infants at 8, 14, and 16 months of age was observed in the Bayley mental scales. In this study, all infants were from the same social and intellectual strata.

The question of whether breastfeeding influences a child’s developmental outcome has appeared in modern literature since Hoefer and Hardy first reported in 1929 that breastfed infants were more active and achieved motor milestones earlier than bottle-fed infants. ⁷² These authors described enhanced learning ability and higher intelligence quotient (IQ) scores at 7 to 13 years of age in children exclusively breastfed for 4 to 9 months. Although socioeconomic status and mothers’ education were not reported, it is an interesting historic note that it was the well-educated, higher socioeconomic mothers who could afford to bottle feed in the 1920s and 1930s and into the 1940s. In an attempt to clarify the relationship to maternal status, Taylor and Wadsworth took the negative hypothesis but were unable to eliminate the possibility that breastfeeding had a positive effect on intellectual development at 5 years of age. ⁷³

In a national study of 13,135 children in England, Scotland, and Wales, a positive correlation between duration of breastfeeding and performance in tests of vocabulary and visuomotor coordination was found; these behavior scores remained steady when tested against intervening social and biologic variables. This British 1946 cohort study continued. They showed that breastfeeding was significantly and positively associated with educational attainment and cognition at age 15 years and with adult social class. Breastfeeding did not affect verbal memory independently at 53 years of age in this longitudinal cohort. Breastfeeding clearly has long-term potential impact across life’s course according to the authors. ⁷⁴

The advantage of human milk for at-risk infants has been investigated by Lucas et al., who raised public awareness when their results were reported in newspapers internationally in 1992. ⁷⁵ , ⁷⁶ The initial cohort of 771 infants whose birth weights were less than 1850 g were given their mothers’ milk; these infants had a mean 8-point advantage on the Bayley Mental Developmental Index compared with infants who did not receive their mothers’ milk. ⁷⁵ Both groups received nutrition by feeding tube for the first month of life. A 4.3-point advantage remained when outcome was adjusted for demographic and perinatal factors. The same advantage was found using an IQ equivalent test, which is a fundamentally different test. The same group of infants was tested regularly, and results at age 7½ to 8 years showed a 10-point advantage in IQ testing even when controlled for maternal social class and education.

This report precipitated a torrent of responses from other investigators, who provided support for and against the conclusion that breast milk is effective in improving the outcome of high-risk infants. ⁷⁷ , ⁷⁸ , ⁷⁹ A systematic review and meta-analysis of 17 studies demonstrated by a random effects model that breastfed infants achieved a higher IQ (mean difference 3.44 [95% confidence interval (CI), 2.30 to 4.58]) and controlling for maternal IQ demonstrated a smaller benefit (2.62 [95% CI, 1.25 to 3.98]). ⁸⁰ Evidence from a randomized trial demonstrated that children breastfed exclusively for up to 3 months had IQs that were on average 2.1 points higher compared with the others breastfed for a shorter period (95% CI, 0.24 to 3.9). Analysis on data of children breastfed for 4 to 6 months showed higher IQ by 2.6 points (95% CI, 0.87 to 4.27) and the benefit for children breastfed even longer (>6 months) was higher by 3.8 points (95% CI, 2.11 to 5.45). ⁸¹ This evidence showed that longer duration of exclusive breastfeeding has a dose effect on IQ and similarly, there is evidence of a dose effect of breastfeeding/use of human milk in preterm infant neurodevelopment. ⁸² These and other studies suggest a causal effect of breastmilk on intelligence. ⁸¹ , ⁸² , ⁸³

To determine the effect of breastfeeding on optimal visual development, Birch et al. ⁸⁴ studied term and preterm infants fed human milk or corn oil–based formula with no added omega-3 essential fatty acids. Visual testing using visual-evoked potential and forced-choice preferential looking activity was performed at 4 months’ adjusted age; infants given human milk scored better. This was confirmed at 36 months using random dot stereo acuity and letter-matching ability. Results correlated with a measure of dietary omega-3 sufficiency index from the infants’ red blood cells at 4 months.

Definition

Failure to thrive is an imprecise, archaic term. Failure to thrive is a symptom and not a diagnosis. The causes of failure to thrive in children have been associated with malfunctions of many organ systems and with nutritional, environmental, social, and psychologic factors. Failure to thrive while breastfeeding has often been inappropriately considered in the same terms as failure associated with other sources of nourishment and involving other age groups. ⁸⁵ Growth or weight faltering is another term proposed to diminish the strong negative connotations of failure. ⁸⁵ Growth faltering while breastfeeding is a phenomenon associated with the first year of life and more likely younger than 6 months. Exclusive breastfeeding is appropriate for the first 6 months, and then solids should be added. Therefore the symptom is no longer exclusively associated with lactation, except in rare cases in which the infant is breastfed beyond 9 months with no solids added.

The term failure to thrive has been loosely used to describe all infants who show some degree of growth faltering. ⁸⁶ (Here these two terms will be used interchangeably.) Severe malnutrition or insufficient caloric intake for energy expenditure impairs overall growth, which has an impact on weight first, length usually second, and head circumference third (relatively spared except in extreme malnutrition). It is a syndromic classification that has been used to describe infants whose gain in weight, length, or both fails to occur in a normal progressive fashion. For the breastfed infant, it may be a matter of using an inappropriate growth chart or comparing a slower gaining breastfed infant to the excessive weight-gain patterns of bottle-fed infants.

The current recommendations for diagnosis and treatment of failure to thrive emphasize the assessment of and therapy for malnutrition and its complications and the context in which they occur. ⁵⁰ The AAP suggests that the needs of each child who is not thriving should be evaluated according to four parameters: medical, nutritional, developmental, and social. The entire family should be included in the assessment as part of the infant’s environment for growth. The ecologic context in which such a situation occurs in countries where food is plentiful suggests the cause of deficiency is poverty and food insecurity. This approach is appropriate for children beyond infancy but not for the newborn and early months of life when the child is breastfed.

The disorder for an infant is defined as failure to thrive when the infant continues to lose weight after 10 days of life, does not regain birth weight by 3 weeks of age, or gains at a rate below the 10th percentile for weight gain beyond 1 month of age. Various growth standards are available depending on the situation and the age of the infant. ²⁸ , ⁴³ , ⁶³ Weight loss (5% to 7% of birth weight for a breastfed infant) in the first 10 to 14 days of life can be normal but may be an appropriate reason to assess the breastfeeding mother–infant dyad regarding milk production and intake. (See section on early weight loss earlier in this chapter and Appendix F .) Unlike a bottle-fed infant, who can be placed in a hospital where professionals can feed him or her, a breastfed infant needs to be evaluated in the home setting and observed nursing at the breast unless urgent intervention is indicated. If the infant requires hospitalization, the breastfeeding mother is included in the assessment of feeding, including examination of the breasts for signs of milk production and response to feeding, expressing, and/or pumping.

Human growth has been considered a continuous process, characterized by changing velocity of growth at different ages. Despite there being guides for median daily weight gain at different ages, the median daily weight gain often should be measured over slightly longer periods (e.g., 3, 5, 7, or 14 days depending on the situation) and not day to day. ( Table 10.1 presents median daily weight gain based on age of the child.) Lampl et al. made serial measurements of length in normal infants weekly, semiweekly, and daily during the infants’ first 21 months. ⁸⁷ They show clearly that growth in length occurs by discontinuous, periodic, saltatory spurts. Furthermore, these bursts were 0.5 to 2.5 cm (0.2 to 1 inch) of length or height during intervals separated by no measurable change (2 to 63 days’ duration). The authors suggest that 90% to 95% of normal development during infancy is growth free. ⁸⁷ Length accretion is distinctly a salutatory process of incremental bursts punctuating background stasis. Thus evaluation of length requires more than one measurement and the careful consideration of an experienced physician familiar with growth parameters. In standard textbooks, the term failure to thrive has been replaced with malnourished or suffering from protein energy malnutrition but is used for children older than a year and no longer depending solely on breast milk for their entire caloric needs.

As increasingly more women breastfeed, increasing numbers of cases of failure to thrive appear in the literature. No statistical data on incidence rates are available because no large prospective study has been done. ⁸⁸ Only in extreme cases are infants hospitalized, but the number of these cases is increasing as well, partly because of a failure to recognize poor weight gain or weight faltering earlier and to further evaluate the issues and make appropriate interventions for improved caloric intake.

With the introduction of the WHO growth standards based on normal healthy breastfed infants instead of on overfed formula-fed infants, the diagnosis of failure to thrive should be less frequent. An occasional child is clearly not gaining weight nor growing because of a lack of enough breast milk. That lack of weight gain may be related to a confluence of factors, including but not limited to breastfeeding difficulties related to latch, breast pain, and low milk production; contributing factors such as maternal fatigue, overtaxing family/household responsibilities, mother’s return to work or school; and the mother’s or family’s perception of insufficient milk supply. The question that arises is “Does early breastfeeding cessation represent actual failure to thrive by the infant, lactogenesis failure, or simply breastfeeding difficulty and lack of adequate support for the breastfeeding mother–infant dyad?” Steube et al. reported a prevalence of 12 per 100 women in the Infant Feeding Practices Study II in the United States who reported “lactation dysfunction,” which the authors defined as undesired, early weaning from breastfeeding and two of three common problems (breast pain, low milk supply, and difficulty with infant latch). ⁸⁹ They also reported three significant risk factors for early weaning being women who were overweight, obese, or manifested with depressive symptoms at 2 months postpartum. Feenstra et al. reported from Denmark on data from a postal survey from 1437 mothers with full-term singleton infants. ⁹⁰ Up to 40% of the women reported “early breastfeeding problems,” the most prominent of which were difficulty with latch and sore or cracked nipples. Pain was often reported with breastfeeding problems with no specific diagnosis for the pain. In another study from the United States of 7942 participants enrolled in a peer counseling breastfeeding support group the most common reasons for stopping breastfeeding were mother’s choice (39%) and low milk supply (21%). ⁹¹ The most common reasons for stopping in participants who stopped the earliest were “breastfeeding challenges,” low milk supply, and “mother’s preference.” ⁹¹ Neither failure to thrive by the infant nor lactogenesis failure were discussed in any of these studies.

L. Gatti did a literature review of original research papers on human milk, milk supply, and perceived milk supply. ⁹² She reported that a 35% of all women who wean early report “perceived insufficient milk supply,” although neither the mother nor clinicians and researchers reportedly assessed the actual milk production. Early breastfeeding behaviors of the mother–infant dyad and potential factors associated with perceived insufficient milk supply and socioeconomic or demographic factors were not carefully analyzed and reported in the selected research papers. A couple of other systematic reviews report mixed results of the influence of maternal confidence on exclusive breastfeeding duration and the various factors associated with breastfeeding cessation (maternal young age, low level of education, return to work within 12 weeks postpartum cesarean delivery, depression, and perceived inadequate milk supply. ⁹³ , ⁹⁴ It remains difficult to determine if failure to grow by a breastfeeding infant is a common occurrence or significant public health concern.

True failure to thrive with the resultant insufficient caloric and protein intake for an individual infant’s energy and growth needs can occur for reasons of medical illness in the infant. Undesired early weaning most likely represents a mixture of situations and contributing factors, only some of which are failure to thrive for the infant. Nevertheless, in any situation with poor infant growth, pain while breastfeeding, or perceived low milk supply, additional assessment and breastfeeding support and education are indicated.

Underlying metabolic disorders causing lack of metabolism of nutrients or lack of absorption are uncommon. Children with congenital anomalies of the first arch, such as cleft lip and/or cleft palate, are at risk but should be identified before hospital discharge and scheduled to receive close follow-up. Congenital illness or infection affecting major organs (lung, liver, heart, kidney, etc.) can affect both caloric and nutrient intake and need. Children with developmental delay may present after a month or so when they cannot maintain adequate suckling and the mothers’ milk supply dwindles with diminishing stimulation/milk removal. It is appropriate to evaluate an infant for lead intoxication when there is insufficient growth or developmental delay. Psychosocial risk factors include unusual health and nutrition beliefs of the family, including fear of obesity or other diseases that have been associated with rigid and restricted feeding patterns.

Diagnosis

The problem of slow or inadequate weight gain has confounded even the physicians most committed to breastfeeding. It should be approached with the same orderly diagnostic process used to address any medical problem. Thus a complete history, including the details of the breastfeeds, a physical examination of the infant, an examination of the maternal breast, observation of the feeding, and appropriate laboratory work are indicated. Organizing the data collected by this process will help identify the maternal and infant causes separately.

Slow Gaining Versus Failure to Thrive

Some helpful distinctions exist between a breastfed infant who is slow to gain weight and the infant who is failing to thrive while breastfeeding versus excess weight loss in the first 2 to 4 weeks of life. ⁹⁵ Assessing ongoing growth by serial weights, lengths, and head circumferences should be included in the routine “well baby” evaluation of all breastfed infants, beginning with the first visit. With serial measurements the infant’s demonstrated weight gain over a specific number of days can be compared with the median daily weight gain for age ( Table 10.1 ). ³¹ , ³⁴ With early discharge often occurring less than 48 hours after birth, the first outpatient visit may need to be within 48 hours of discharge from the hospital, depending on an infant’s gestational age, weight loss before discharge, and history of jaundice and in response to the mother’s experience or needs. The pediatric office or clinic should have a failsafe system of follow-up for all newborns that includes access by telephone. The pediatric office also should be alert to the close follow-up of primiparas, especially those mothers who are older and well educated. A study of delayed lactogenesis and excess neonatal weight loss by Dewey et al. ³⁸ revealed the high correlation not to ethnic groups, but to age and advanced education, noting increased problems with the early periods of breastfeeding. In the absence of reliable phone contact, visiting nurse involvement may be appropriate. Although many hospitals provide breastfeeding warm lines that mothers can call for information and help, the family must make the transition from the birthplace to the primary care provider promptly, especially for parents of a first baby who have no previous office contact. New parents often do not recognize when there is a problem.

The feeding pattern of an infant with slow weight gain is usually frequent feedings with evidence of a good suck (see Table 10.2 ). The mother’s breasts are full before feeding, and she can describe a let-down during the feeding. At least six diapers per day are wet, urine is pale and dilute, and stools are loose and seedy. Weight gain is slow but consistent. If the infant is gaining extremely slowly but is alert, bright, responsive, and developing along the appropriate level, the infant is a “slow gainer.” In contrast, the infant with true failure to thrive is usually apathetic or weakly crying with poor tone and poor turgor. Few diapers are wet (none is ever soaked) and urine is “strong.” Stools are infrequent and scanty. Feedings are often by schedule but always fewer than eight per day and brief. No signs of a good let-down reflex are found. True failure to thrive is potentially serious; early recognition is essential if the integrity of both brain growth and breastfeeding is to be safely preserved.

Table 10.2

Parameters for Evaluation of Breastfed Infants

Phillip B, Rosen-Carole C. What SHOULD happen when baby does not get enough milk from mom? https://www.babyfriendlyusa.org/news/what-should-happen-when-baby-does-not-get-enough-milk-from-mom/ . December 3, 2019. Accessed February 20, 2020.

Infant Who Is Slow to Gain Weight	Infant With Failure to Thrive
Alert healthy appearance	Apathetic or crying
Good muscle tone	Poor tone
Good skin turgor	Poor turgor
At least six wet diapers/day	Few wet diapers
Pale, dilute urine	“Strong” urine
Stools frequent, seedy (or if infrequent, large and soft)	Stools infrequent, scanty
Eight or more feedings/day, lasting 15–20 minutes	Fewer than eight feedings, often brief
Well-established let-down reflex	No signs of functioning let-down reflex
Weight gain consistent but slow	Weight erratic; may seem to lose weight at different points of assessment

Although slow gaining may be familial or genetic (small parents), it is always appropriate to be sure the process of breastfeeding is optimized. ⁴⁶ Attention to adequate fat in the milk is important, especially because mothers have often been encouraged to “switch nurse,” that is, switch back and forth between breasts in each feeding to build up an adequate milk supply. The switch-nursing process interrupts the release of fat and the production of fat-rich hindmilk. If the mother is interrupting the feeding to go to the other side, a period of feeding exclusively on one breast during each feeding may change the gaining pattern. If necessary, the level of fat in the milk can be checked by doing a “creamatocrit,” comparing milk before and after the switch from one breast to the other (see Chapter 22 ). By weighing the infant before and after a feeding with a digital readout scale, an accurate measurement of breast milk intake can be recorded. A slow gainer will have good intake during the individual feeding.

In a schema for classifying failure to thrive at the breast, the causes associated with infant behavior and problems are distinguished from those related to maternal problems ( Fig. 10.1 ). The causes in the infant can be further evaluated by looking at net intake, which may be associated with poor feeding, poor net intake from additional losses, or high energy needs. The maternal causes can be divided into poor production of milk and poor release of milk. When a poor let-down reflex continues long enough, it will eventually cause a decrease in milk production. Several factors may affect the outcome, and more than one management change may be indicated in supporting breastfeeding and suggesting changes to the mother.