Normal Growth, Failure to Thrive, and Obesity in Breastfed
Infants
Normal Growth
The focus on growth evaluations in childhood have relied on averages: averages of the fat, the thin, the tall, the short, the sick, and the well. The real sci- ence is looking at ideal growth in ideally fed chil- dren anywhere in the world.
The growth of exclusively breastfed infants has become the focus of much interest among pediatri- cians, researchers, and nutritionists.12Historically, the Boyd-Orr cohort study in the 1920s and 1930s showed that breastfed children were taller in child- hood and adulthood.80Stature was associated with health and life expectancy. Adult leg length is very sensitive to environment factors and diet in early childhood because this is the time of most rapid leg growth. After infancy, chest growth is rapid before puberty and is sensitive to stress and illness.
Cross-sectional association between cardiovascular risk factors and components of stature (total height, leg length, and trunk length) was demonstrated. The risk of coronary heart disease was inversely related to leg length but not trunk length in the Caerphilly study in South Wales.110
A number of long-range follow-up studies have been initiated to address the issues of growth dur- ing the critical first year of life, when brain growth is greater than it ever will be again in postnatal life.
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 breast- feeding protect against adult obesity? Does human
milk protect against cholesterol “intolerance” in adult life? The questions are clear, but the answers are not unless one assumes the teleological approach: human milk is ideal for human infants, with its low protein, controlled calories, and persis- tent unchangeable cholesterol.
The questions are actually, “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?”
Antiquated data and anthropometric standards 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.83Reliability of weight gain as a measure of growth has developed because it is a measurement easily obtained.83 Measurement of length, how- ever, is considered a better standard.93Weight gain and linear growth are not always correlated. Fur- thermore, 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. Furthermore, whole cow milk is fortunately almost totally abandoned, and the recommendations for introduction of solid food at 6 months and older have been universally 338
adopted by nutrition-conscious physicians and par- ents. World Health Organization (WHO) and United Nations International Children Education Fund (UNICEF) have reconfirmed that breastfeed- ing should be exclusive for the first 6 months.
Growth curves have been developed based on breastfed infants on delayed solids.
Bottle-fed infants gain more rapidly in weight and length during the first months of life than do breastfed infants.26Therefore, evaluating an infant’s physical growth by standards set by bottle-fed infants predis- poses one to the diagnosis of failure to thrive.
Forman et al.35reported 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 calo- ric intake rather than the difference in composition of the diet. Fomon et al. showed that the bottle-fed infant not only gains more in weight and length, but also gains more weight for a unit of length. This gain reflects the overfeeding of the bottle-fed infants.34
Most studies of growth in breastfed infants have been plagued with the problem of variation in sup- plementation 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.3No signif- icant differences were found in the growth rate of crown-heel length and head circumference or weight gain. The authors concluded that the differ- ences 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.,11 energy and protein intakes were substan- tially less than current nutrient allowances. Infant growth progressed satisfactorily when compared with National Center for Health Statistics (NCHS) standards, despite that energy dropped from 11024 kcal/kg/day at 1 month to 7117 kcal/
kg/day at 4 months.11 Similarly, protein intake decreased from 1.60.3 g/kg/day at 1 month to 0.90.2 g/kg/day at 4 months. Reevaluation of protein and energy requirements is essential.
Weight-for-length and weight gain were signifi- cantly 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.24,22
Energy intake was considerably lower than recom- mended—85 to 89 kcal/kg/day—when compared with the 115 kcal/kg/day recommended dietary allowances of the National Academy of Sciences in 1980.17 Presently energy recommendations suggested by the Institute of Medicine (IOM) are expressed as: (89wt[kg]100) + 175 kcal.
Those infants who consumed the most breast milk became the fattest. A 4-kg infant would require 105 kcal/kg/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 was significantly small for gestational age (SGA).7The intakes of energy and protein by individual infants were reflected in their weight gain but were below internationally recommended norms.30Maternal milk alone, when produced in sufficient amounts, can maintain normal growth up to the sixth month of life. Exclusive breastfeed- ing in Chilean infants of low-middle and low socio- economic families produced the highest weight gain and practically no illness or hospitalization.59 In the Copenhagen Cohort Study in 1994, exclu- sively breastfed term infants had a mean intake of 781 and 855 mL/24 hours at 2 and 4 months, respec- tively.82 The median fat concentration of human milk was 39.2 g/L and was positively associated with maternal weight gain during pregnancy. This sup- ports the concept that maternal fat stores laid down during pregnancy are easier to mobilize during lac- tation than other fat stores. This may limit milk fat when pregnancy fat stores are exhausted.
The effect of prolonged breastfeeding on growth has been an issue of concern, especially in develop- ing countries.35In a review of 13 studies, Grummer- Strawn42pointed out in 1993 that eight reported a negative relationship, two had a positive relation- ship, and three had mixed results. 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 exceed the risks in these geographic areas.
In addition to recognizing the importance of genetic, metabolic, and environmental influences in producing significant differences in growth pat- terns, Barness5suggests that recommendations for nutrition of healthy neonates may be too high for some and too low for others. However, the bench- mark 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 about 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 fail- ure includes failure of head growth, the failure is severe. However, many other factors independent of body growth influence head growth.
A weight loss of 5% is usually accepted as the norm for bottle-fed infants in the first week of life, although information in pediatric textbooks is mea- ger. A loss of 7% is average for breastfed infants, but when this occurs in the first 72 hours of life, a cli- nician should be alert to breastfeeding problems and should review the process. A loss of 10% is the maximum for breastfed infants. Clinicians should confirm that positioning and latch-on are correct and that the breasts have responded with some engorgement and milk production. The mother-infant dyad with this problem will need close observation and support. Referral to a licensed certified lactation consultant may be appropriate if the pediatric office does not have a trained staff member available (nurse practitioner with lactation training).
Initially after birth, a normal infant loses 5% of body weight before starting to gain, whether breastfed or bottle fed. Breastfed infants who are given added water or added formula to force fluids in the first few days of life lose more weight and are less likely to start gaining by the fourth day than infants who are exclusively breastfed or who were bottle fed.
The time at which an infant regains birth weight is equally unclear. In their extensive study of 1139 breastfed and formula-fed infants, Nelson et al.91 summarize weight at 8 days by stating, “Most formula-fed but not most breastfed infants have exceeded their birth weights by age 8 days.” They also report that gains in weight and length were greater for boys than for girls in the age intervals of 8 to 42 days, 42 to 112 days, and 8 to 112 days.
These authors provided weights and lengths for the critical first 112 days. Birth weight is doubled between the 50th and 75th percentiles at 4 months of age and tripled at 12 months. Obese infants with higher weight/length ratios tripled their weight sooner, suggesting that rapid tripling time may be an indicator of obesity. Black infants in general doubled and tripled their weights sooner, but more black infants were bottle fed.
GROWTH OF BREASTFED INFANTS
Dewey et al.24,25,21have suggested that new, sepa- rate growth charts are needed for breastfed infants.
The DARLING (Davis Area Research on Lactation, Infant Nutrition, and Growth) 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. Mea- surements 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 about 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 authors21concluded 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.
When the growth patterns of a large sample of breastfed infants were pooled from the United States, Canada, and Europe, Dewey et al.24,25,21 reported that results were consistent across studies.
Breastfed infants grew more rapidly in weight during the first 2 months and less rapidly during 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.37 reviewed growth patterns of breastfed infants. Breastfed infants clearly consumed less energy than recommended by WHO in the sec- ond 3-month period by choice and not because the mother could not produce more milk. Dewey et al.22,23 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.22
INTERNATIONAL GROWTH CHARTS 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. The WHO developed an inte- rnational committee of experts to develop a model for how children should grow. Data were collected from six countries of widely divergent populations from stable families who breastfed exclusively for
6 months and continued 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 zero to 5 years of age from Brazil, Ghana, India, Norway, Oman, and the United States (Sacramento, California).114,117 The sample had ethnic or genetic variability in addi- tion to cultural variation in how the children were nurtured, strengthening the standard’s universal applicability. The remarkable observation was that all the children grew at the same pace; curves could be superimposed, regardless of racial background.
The observations confirmed the thought that chil- dren in a healthy environment can achieve their genetic growth potential regardless of poverty, eth- nicity, 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 that averages 600 to 650 g heavier at 12 months of age. Differences in length are minimal and, there- fore, breastfed infants are lower in weight-for-length measurements and other indices of fatness. Breastfed individuals are not shorter in adult life but less likely to be obese. Assessment of sex differences and heterogeneity in motor milestone attainment among populations in the multicenter study support the appropriateness of pooling data from all sites and both sexes for the purpose of an international stan- dard. 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 and can be used to assess children everywhere, regardless of ethnicity, socio- economic status, and type of feeding. They represent how children should grow globally.113,116
The recommendation for use of the WHO charts by the CDC states the following for infants under 24 months: use the WHO growth charts recogniz- ing 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. The ratio- nale 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 4 months and still breastfeeding at 2 months, all based on a high-quality study.
The continued use of CDC charts from 24 to 59 months is recommended because they extend for 20 years, whereas WHO charts cover 0-59 months. Switching at 24 months is explained because of the transition at 24 months from measur- ing recumbent length to standing height. The WHO charts reflect optimal growth while the CDC charts reflect population averages.
IMPACT OF WEANING FOODS ON GROWTH
Weaning foodsis a term used by breastfeeding prac- titioners, but the infant nutrition community uses the termcomplementary 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; like- wise, the once high-levels of stored zinc are dimin- ishing, 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.103 Krebs et al.63 found low measure- ments of iron and zinc levels in breastfeeding infants at 6 months; when meat was added as a weaning food, levels increased toward normal. Rou- tine 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.9
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/age and weight/length ratios continues with the addi- tion 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 and also leave 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 higher protein?50 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.23Neither 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 limit- ing factor in the growth of breastfed infants.23,50
Similarly, Cohen et al.16 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.86calculated the gross efficiency of nutrient uti- lization for each infant in a longitudinal study of breastfed and bottle-fed infants, length and weight