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 science is looking at ideal growth in ideally fed children anywhere in the world.
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. Stature 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.
A number of long-range follow-up studies have been 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. 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 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 persistent 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. 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. 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. 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 adopted by nutrition-conscious physicians and parents. World Health Organization (WHO) and United Nations International Children Education Fund (UNICEF) have reconfirmed that breastfeeding 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. Therefore, evaluating an infant’s physical growth by standards set by bottle-fed infants predisposes one to the diagnosis of failure to thrive.
Forman et al. 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. 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.
Most studies of growth in breastfed infants have been plagued with the problem of variation in 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. 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., 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 dropped from 110 ± 24 kcal/kg/day at 1 month to 71 ± 17 kcal/kg/day at 4 months. Similarly, protein intake decreased from 1.6 ± 0.3 g/kg/day at 1 month to 0.9 ± 0.2 g/kg/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. , Energy intake was considerably lower than recommended—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. Presently energy recommendations suggested by the Institute of Medicine (IOM) are expressed as: (89 × wt[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). The intakes of energy and protein by individual infants were reflected in their weight gain but were below internationally recommended norms. 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.
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. 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.
The effect of prolonged breastfeeding on growth has been an issue of concern, especially in developing countries. In a review of 13 studies, Grummer-Strawn pointed out in 1993 that eight reported a negative relationship, two had a positive relationship, 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 patterns, Barness suggests that recommendations for nutrition of healthy neonates may be too high for some and too low for others. 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 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 failure 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 meager. A loss of 7% is average for breastfed infants, but when this occurs in the first 72 hours of life, a clinician 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. 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. , , have suggested that new, separate 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. 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 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 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.
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. 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. 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. 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.
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 international 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). , The sample had ethnic or genetic variability in addition 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 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 that averages 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 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 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 and can be used to assess children everywhere, regardless of ethnicity, socioeconomic status, and type of feeding. They represent how children should grow globally. ,
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. 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 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 measuring 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 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. 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. 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.
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 addition of solids, which would not be expected if growth faltering were the basis for the decline. 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? 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. 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. ,
Similarly, Cohen et al. 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 utilization 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. The formula-fed infants had received significantly higher nitrogen and energy. The gross efficiency of dietary energy utilization 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. Breastfed infants self-regulate their energy intake at lower levels than formulated. Body temperature and metabolic rates are lower in breastfed infants.
Recommendations for optimal duration of exclusive breastfeeding have been controversial. The WHO has revised its recommendation for both developed and developing countries to promote exclusive breastfeeding for 6 months. Kramer and Kakuman provided 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. 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 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 AAP promotes exclusive breastfeeding for 6 months. The WHO recommends the need for animal source foods as well as fruits and vegetables in the initial period of 6 to 9 months of age as demonstrated in the Multicenter Growth Reference Study. , ,
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. Some studies showed that small, undergrown infants are breastfed longer. , 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. Thus, smaller infants being breastfed longer is not the cause of the undergrowth.
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. 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.
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.
Cognitive and Motor Development
Cognitive development in the first 7 years of life was related to breastfeeding practices of a birth cohort in New Zealand. 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 all variables were taken into account. 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 Christ Church Child Development Study. They used the maternal and teacher ratings of childhood conduct disorders. 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 has now been reported as an 18-year longitudinal study by Horwood and Fergusson. 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 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 by the WHO Growth Reference Study Group from the Yale Harvard Research Project in Tunisia. 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. 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.
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 has continued. In 2002, Richards et al. used a meta-analysis to show that breastfeeding conferred a 3.2-point increment in cognitive function through adolescence. 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. Breastfeeding clearly has long-term potential impact across life’s course according to the authors.
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. The initial cohort of 771 infants whose birth weights were less than 1850 g were given their mothers’ milk; these infants had a mean eight-point advantage on the Bayley Mental Developmental Index compared with infants who did not receive their mothers’ milk. 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.
To determine the effect of breastfeeding on optimal visual development, Birch et al. 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.
Failure to Thrive
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 as well as with nutritional, environmental, social, and psychological 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. Failure to thrive 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 failure. It is a syndromic classification that has been used to describe infants whose gain in weight or length or both fails to occur in a normal progressive fashion. For the breastfed infant, it may be a matter of comparing a slower gainer to the excessive weight-gain patterns of the bottle-fed infant.
The current diagnosis and treatment of failure to thrive emphasizes the assessment of, and therapy for, malnutrition and its complications and the contexts in which they occur according to the AAP. 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. The ecologic context in which such a situation occurs in the land of plenty suggests the source 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. 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 nursing at the breast unless it is an emergency. If the infant requires hospitalization, then the breastfeeding mother is part of the work up, including examination of the breasts for signs of milk production and response to pumping.
A more serviceable measure of failure to thrive than percentiles is proposed by Frank et al., who suggest the use of a percentage of the median values for the age on the growth chart. Thus, normal is greater than 90% of median weight, mild malnutrition is 75% to 90% of median, moderate is 60% to 74% of median, and severe is less than 60% of median weight. Similar percentages are applied to height and weight-for-height. Thus a 1-month-old infant whose median weight-for-age would be 5000 g and who is only 3800 g is 75% of median, or mildly malnourished ( Table 11-1 ).
| Age (mo) | Median Daily Weight Gain (g) | Recommended Daily Allowance (kcal/kg/day) |
|---|---|---|
| 0-3 | 26-31 | 108 |
| 3-6 | 17-18 | 108 |
| 6-9 | 12-13 | 98 |
| 9-12 | 9 | 98 |
Human growth has been considered a continuous process, characterized by changing velocity with age. Lampl et al. made serial measurements of normal infants weekly, semiweekly, and daily during the infants’ first 21 months. 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) 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. 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 text books, 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 not breastfed.
As more and more women breastfeed, increasing numbers of cases of failure to thrive appear in the literature, although it is a rare phenomenon. No statistical data on incidence rates are available because no large prospective study has been done. Only in extreme cases are infants hospitalized, but the number of these cases is increasing as well, partly because of a failure to recognize the disorder and refer the infant to medical care promptly.
With the introduction of the WHO growth charts based on normal healthy breastfed infants instead of on overfed formula-fed infants, the diagnosis of failure to thrive is less frequent. An occasional child is clearly not gaining nor growing due to lack of sufficient breast milk or more likely because of an underlying metabolic disorder causing lack of metabolism of nutrients or lack of absorption. 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. Children with developmental delay may present after a month or so when they cannot maintain adequate suckling and the mothers’ milk supply dwindles. 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. Fear of obesity or other diseases have been associated with rigid and restricted feeding patterns. Allergic families may actually breastfeed to avoid the use of soy milk and other substitutes.
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 attack 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 to identify the facts that appear under 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. These parameters should be included in the routine “well baby” evaluation of all breastfed infants, beginning with the first visit ( Box 11-1 ). With early discharge often occurring less than 48 hours after birth, the first visit may need to be within 48 hours of discharge from the hospital, depending on an infant’s gestational age, weight loss before discharge, history of jaundice, and the mother’s experience. The pediatric office or clinic should have a failsafe system of follow-up for all newborns that includes access by telephone. The pediatric office should also 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. revealed the high correlation not to ethnic groups, but to age and advanced education, noting increased problems with early breastfeeding. In the absence of a telephone in the home, 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.
| 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 to 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 lose |
The feeding pattern of an infant with slow weight gain is usually frequent feedings with evidence of a good suck. 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, and 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.
Although slow gaining may be familial or genetic (small parents), it is always appropriate to be sure the process of breastfeeding is optimized. 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 hind milk. 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 timing change (see Chapter 21 ). 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 gainer will have good intake.
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 ( Figure 11-1 ). 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.
Evaluation of Infant
Examination of the infant should suggest any underlying physical problems, such as hypothyroidism, congenital heart disease, mechanical abnormalities of the mouth (e.g., cleft palate), or major neurologic disturbances. An infant’s ability to root, suck, and coordinate swallowing should be observed. Today, a greater risk for missing subtle structural problems exists because infants spend much of their hospital life out of the newborn nursery away from the eyes of experienced nurses and are discharged before problems become manifest.
The routine observation of a feeding by an infant’s physician should be part of the discharge examination from the hospital. If this is not practical, such an examination should be incorporated into the first office or clinic visit within the first week of life. The mother should be asked to let you see how the baby feeds. The focus, however, should be to watch the positioning of the mother and the infant, placement of the mother’s hands, and initiation of latch-on (see Chapter 8 ). A small number of infants will be identified with physical abnormalities that need medical attention ( Box 11-2 ).
| Absent or Diminished Suck | Mechanical Factors Interfering with Sucking | Disorders of Swallowing Mechanism (Not Including Esophageal Abnormalities) |
|---|---|---|
| Maternal anesthesia or analgesia | Macroglossia | Choanal atresia |
| Anoxia or hypoxia | Cleft lip | Cleft palate |
| Prematurity | Fusion of gums | Micrognathia |
| Trisomy 21 | Tumors of mouth or gums | Postintubation dysphagia |
| Trisomy 13-15 Hypothyroidism Neuromuscular abnormalities Kernicterus Werdnig-Hoffmann disease Neonatal myasthenia gravis Congenital muscular dystrophy Central nervous system infections Toxoplasmosis Cytomegalovirus infection Bacterial meningitis | Temporomandibular ankylosis or hypoplasia | Palatal paralysis Pharyngeal tumors Pharyngeal diverticula Familial dysautonomia |
Lukefahr identified 38 infants younger than 6 months of age in a suburban pediatric practice as having failure to thrive while breastfeeding. Only 2 of 28 infants (7.1%) who presented in the first 4 weeks had underlying illnesses (salt-losing adrenogenital syndrome and congenital hypotonia); 5 of the 10 presenting between 1 and 6 months had underlying disease (all of whom actually presented with a problem by 4 months). This report stresses the importance of ruling out underlying disease and the urgency of having a pediatrician evaluate a child when the symptom of poor weight gain is first suspected, thus avoiding the serious complications of dehydration and metabolic disorders that may result when “home remedies” for lactation problems are used.
Oral Motor Problems: Feeding Skills Disorder
Growth failure secondary to feeding skills disorder is the terminology proposed by Ramsay et al. to replace nonorganic failure to thrive. The authors describe a series of children who were referred for nonorganic failure to thrive who had displayed subtle problems since birth. The criteria include early abnormal feeding-related symptoms present shortly after birth, such as impaired oral function, suggesting the infants are minimally neurologically abnormal, sometimes associated with borderline low Apgar scores. Difficulties during earlier stages of feeding development not only may interfere with the development of more mature feeding skills, but also may contribute eventually to difficulties in mother-infant interaction. The common finding among all infants with failure to thrive was underlying feeding-related symptoms that were neurophysiologic but manifested in different degrees of oral sensorimotor (and pharyngeal) impairment. The neurologic impairment may vary from obvious cerebral palsy to symptoms that are not apparent on casual observation but lead to abnormal feeding-related symptoms in early life. When the mother copes and adapts, the disorder goes unnoticed until solid foods are added. Diagnosis requires oral sensorimotor assessments and a neurologic examination sensitive enough to measure minimal neurologic impairment in an apparently healthy child who is failing to gain. Early history is also critically important.
Small-for-Gestational-Age Infant
A SGA infant will be identified if gestational age and birth weight are scrutinized. This infant is small at birth despite full gestation time in utero. An SGA infant has a large nutritional deficit from intrauterine failure to grow. The cause of the intrauterine problem should be assessed: placental insufficiency, maternal disease, toxemia, heavy smoking, or intrauterine infection, such as toxoplasmosis.
SGA infants are difficult to feed initially by any method and often require tube feedings for a few days. Their caloric needs parallel the needs of an infant of appropriate weight for gestation rather than their actual low weight. SGA infants should be placed on frequent feedings, every 2 to 3 hours by day and every 4 hours at night. They should be awakened for feedings if they sleep long periods. If they have not been nursing well, the breast may not have been stimulated to produce to its full capability. The mother may need to express milk manually or mechanically pump milk to enhance her production. Her milk may then be given by a passive means such as a tube, a small cup, or the lactation supplementing device, which provides additional stimulus to the breast while providing the extra calories needed (see Chapter 19 ).
An infant who is sufficiently starved in utero may have a degree of inanition that prevents active suckling at first, predisposing to further starvation. The successful nursing of an SGA infant may require extended efforts by the mother to ensure adequate growth. Such efforts are well worth the trouble if one considers the impact of intrauterine growth failure on the central nervous system. It is to the infant’s advantage to have the critical amino acids, such as taurine and the lipids of human milk, with which to “catch up” brain growth. As noted earlier, SGA infants are more likely to close the growth gap more rapidly if breastfed.
Jaundice
An infant with an elevated bilirubin level from any cause may be neurologically depressed and lethargic and, therefore, may not nurse well. If the infant appears jaundiced, laboratory evaluation to determine the cause and its appropriate treatment should be undertaken. Visible jaundice under 24 hours of age requires a full evaluation and is not related to breastfeeding. When an infant is taken from the breast at 2 or 3 days of age because of jaundice, this interferes with the establishment of lactation at a critical time, especially for a primipara. Management of the jaundiced infant depends on adequate calories and the active passage of stools, which is the means by which the body excretes the bilirubin in meconium and stools.
“Breastfeeding jaundice,” which is related to underfeeding or starvation, does not develop until the infant is 3 or more days old, so other causes must be sought. In addition, care must be taken to help the mother continue to stimulate production with manual expression or pumping to avoid inducing iatrogenic lactation failure. (See Chapter 14 for discussion of hyperbilirubinemia.)
Metabolic Screen
Most hospitals provide, often because the law mandates it, screening for metabolic disorders, including galactosemia, phenylketonuria, maple syrup urine disease, and disorders of metabolism of other amino acids. If these simple screening tests were not performed or their validity is in doubt, they should be done again. Usually the service is available in the state or county laboratory. Thyroid screening for abnormal thyroxine (T 4 ) or thyroid-stimulating hormone should also be performed. Mass screening programs for neonatal thyroid disease have identified cases of deficiency that, even in retrospect, were not in evidence; the infant showed none of the characteristic findings of hypothyroidism, such as thick coarse features, hoarse cry, slow pulse, macroglossia, umbilical hernia, and jaundice. In the neonate, hypothyroidism is often associated with failure to thrive if undiagnosed and untreated.
Galactosemia
Galactosemia, which is a hereditary disorder of the metabolism of galactose-1-phosphate, is manifest by renal disease and liver dysfunction after ingestion of lactose. The lack of galactose-1-phosphate uridyltransferase activity may be relative or partial. The clinical symptoms may be fulminating, with severe jaundice, hepatosplenomegaly, weight loss, vomiting, and diarrhea, or may be more subtle. Cataracts are not invariably present. In mild cases, failure to thrive may be the presenting symptom. A urine screen for reducing substances (by Clinitest and not Dextrostix, which will only identify glucose) should be done on all infants who fail to thrive, especially if there is hepatomegaly or jaundice.
The definitive diagnosis is the identification of absence or near absence of galactose-1-phosphate uridyltransferase activity in red blood cell hemolysates. Even though a routine initial metabolic screen for galactosemia was done on the second or third day of life, a urine screen should be considered. The treatment is a lactose-free diet, which would mandate prompt weaning from breast milk to prevent further insult to the liver, kidneys, and brain. This is one of the few indications for prompt weaning from human milk. A formula free of lactose (e.g., Isomil, Nutramigen) is indicated. No medical indications exist, however, to use a lactose-free formula for a normal breastfeeding infant either to supplement or to wean from breast milk, which contains lactose. (Refer to pediatric texts on neonatal metabolic disorders for a full description of galactosemia; see also Chapter 14 .)
Vomiting and Diarrhea
Vomiting and diarrhea are unusual in a breastfed infant. Spitting up small amounts of milk after feedings is sometimes observed in otherwise normal infants and is of no consequence if it does not affect overall weight gain. Although pyloric stenosis is reportedly less common in breastfed infants, this phenomenon should be ruled out in any infant who vomits consistently after feeding, has diminished urine and stools, shows no weight gain or actually loses weight, and has reverse peristalsis. Usually these infants do well initially and then the vomiting becomes progressive.
Vomiting may be a presenting symptom for various metabolic disorders. Thus, metabolic disorders should be considered in the differential diagnosis. All possible metabolic disorders, such as congenital adrenal hyperplasia, are not routinely screened. These infants may present with vomiting and weight loss in the first week or two of life or with an acute episode of sepsis. The usual causes of vomiting, as well as the causes peculiar to breast milk, should be considered. Maternal diet should be checked for unusual foods. In families at high risk for allergy, intake by the mother of known family food allergens may cause symptoms in the infant. Diarrhea may be caused by foods in the mother’s diet or her use of cathartics, such as phenolphthalein.
Chronic Infections
Chronic fetal infection in utero, which predisposes a SGA infant to intrauterine growth failure, may continue to cause growth problems in the presence of adequate kilocalories. Chronic viral infections include cytomegalovirus, hepatitis, acquired immunodeficiency syndrome (AIDS), or other less common viruses (see Chapter 13 ).
Acute Infections
An infant who is not growing well may have an infection in the gastrointestinal tract; therefore, the nature of the stools is important. The urinary tract may be another site of infection not readily identified. If, however, the initial evaluation includes a urinalysis with microscopic evaluation and a white blood cell count and differential count, this can usually be ruled out (see Chapter 13 ).
High Energy Requirements
When the metabolic rate of an infant is increased, weight gain will be diminished or absent. When the infant is hyperactive with a strong startle reflex and sleeps poorly, consideration should be given to stimulants present in the milk as well as to neurologic disorders. When a mother drinks coffee, tea (including herbal teas), cola, or other carbonated beverages with added caffeine, the accumulated caffeine may be sufficient to make the infant irritable and hyperactive. The best treatment is to replace the caffeine-containing beverages (see Chapter 12 ). Some disorders of the central nervous system are associated with hyperactivity. Infants with severe congenital heart disease are constantly exercising to breathe and oxygenate and have greatly increased metabolic rates. For management of these special infants at the breast, see Chapter 14 .
Observation of Nursing Process
In addition to establishing that no obvious physical or metabolic reasons exist for the failure to gain weight, an infant should be observed suckling at the breast. Does the infant get a good grasp and suck vigorously? If not, what interferes? A receding chin, a weak suck, lack of coordination, the breast obstructing breathing, and mouthing of the nipple or other ineffectual sucking motions are some of the possibilities. If the problem is the suckling process, the infant may need assistance. This cause is more common with infants who have had some experience with bottles or rubber nipples or who use a pacifier. Small or slightly premature infants who were started on bottle feedings have trouble relearning the proper sucking motion with the tongue (see Chapter 8 ).
Bottle-feedings and pacifiers may have to be discontinued until the infant is more experienced at the breast. This will require a program of manually expressing milk to soften the areola, having milk at the nipple to entice the infant, and gently offering the nipple and areola well compressed between two fingers. If the infant has a receding chin or a relaxed jaw, it may help to have the mother hold the lower jaw forward by supporting the angle of the jaw with her thumb. The physician should examine the infant carefully to be sure the jaw is not dislocated, especially if a vertex delivery was done in the posterior position (sunny side up). The physician can easily move the jaw forward to relocate it.
Positioning the infant for the breast so the child directly faces the breast, straddling the mother’s leg in a semiupright position, may work best. This is the position twins may assume when nursing simultaneously when they are 3 to 4 months old. Although it is not recommended routinely, for an infant with a receding chin or a cleft, having the mother lean slightly forward for latch-on may help. She should then bring the infant upward as she sits back for the feeding.
It may be necessary to assist both mother and baby. If the infant by 2 weeks of age cannot maintain the breast in the mouth without the mother holding it, it is an indication of improper suckling. In that situation, the infant may need to be repositioned with the ventral surface squarely facing the mother’s chest wall—that is, tummy to tummy—and the breast presented by the mother with her hand positioned with thumb on top and fingers below the breast. (See discussion in Chapter 8 .) The mother may have to maintain support throughout the feeding. Failure to maintain the breast in the mouth has neurologic implications for long-term follow-up.
When infants have trouble maintaining the latch when the flow of milk is excessive and causes choking, the mother may try lying flat on her back holding the infant over the breast, which she supports with her hand. The flow becomes manageable and the infant’s mouth relaxes and draws the breast in.
A good check of adequate let-down is to observe the opposite breast as the baby nurses to see if milk flows. It can also be tested by seeing if milk is flowing when nursing is interrupted abruptly. If let-down was good, milk will continue to flow, at least drop by drop, for a few moments from the breast that had been suckled. A mother can be trained to listen for the infant’s swallowing. During proper suckling, the masseter muscle in the jaw is in full view and is contracting visibly and rhythmically. Swallowing can be seen and heard. The ratio of suck to swallow is 1:1 or 2:1. Occasionally, infants do not suck vigorously at the breast but occasionally use rapid shallow sucks called “flutter sucking” with little or no swallowing. These infants can be gradually taught to suck effectively. Correct positioning of the breast directly in the infant’s mouth and holding the breast firmly in position with all the fingers under the breast and only the thumb above allow the infant to grasp properly without sucking the tongue or lower lip. Nipple shields usually make the situation worse.
The most productive part of the diagnostic work up is often observation of the baby at the breast. For this reason, this critical responsibility should not be passed on to others but should be performed personally by the physician as well as an international board certified lactation consultant.
The five general types of nursing patterns described in Chapter 8 should be kept in mind. If the mother understands that it is acceptable for the infant to drop off to sleep and snack later, she may not hesitate to follow this lead, thus providing a more adequate feeding.
Some infants will not settle down and nurse well if there is too much activity or noise in the room. Some need to be tightly swaddled; others fall asleep and need to be unwrapped and stimulated to provide adequate suckling time. Frequent feedings, using both breasts, may be the answer in some cases. In others, there may be too many ineffective feedings, which are wearing the mother out; a change that lengthens the time between feedings but also lengthens the time at the breast may help, especially if it is quiet and the chair allows mother to nap while feeding. Concentrating on using one breast at a feeding to increase the fat content may be the most effective change.
Psychosocial Failure to Thrive
In the study of undernutrition in bottle-fed infants and infants beyond the suckling age, terminology has received more attention than the underlying issues. Thus, the emphasis has been on “organic” versus “nonorganic” failure to thrive. A disorder of maternal/infant bonding has become synonymous with maternal deprivation. Reactive attachment disorder has been the term substituted for psychosocial failure to thrive. When an infant does not have an organic disorder that explains the growth failure, the patient is diagnosed as having psychosocial failure to thrive. The typical psychosocial and nutritional pattern reported in psychosocial failure to thrive includes evidence of a chaotic family life, emotional deprivation, and inadequate nutrition.
Prolonged Exclusive Breastfeeding
Prolonged exclusive breastfeeding may occasionally result in a unique deficit in the developmental process of eating. Exclusive breastfeeding is not nutritionally adequate in the second half of the first year, especially beyond 12 months, although nursing can safely continue for several years when combined with adequate solids that provide protein, iron, and zinc.
The syndrome of the breastfed infant in the second 6 months of life with frequent breastfeedings, poor intake of complementary foods, and poor growth has been labeled a manifestation of “vulnerable child syndrome” by O’Connor and Szekely. These children are described to have good weight gain for 5 to 6 months, but by 8 months their weight/height score has decreased dramatically. The intake of solid foods is minimal. These infants refuse solids, aggressively spitting food out. The breastfeeding pattern is usually every 1 to 2 hours during the day and frequently at night. Further investigation revealed numerous household stressors and usually the mother’s need to maintain control by breastfeeding.
The growth of predominantly breastfed infants who live in underprivileged populations in developing countries falters between 4 and 6 months of age, but the reason has never been well understood. In developed countries, energy intake declines between 4 and 6 months but growth does not falter. To determine whether growth faltering in this age-group was due to inadequate intake of human milk, the nutrient intakes of 30 Otami Indian infants from farms in Capulhuac, Mexico, were studied from 4 to 6 months. Growth velocities were not correlated with nutrient intakes. The children’s growth faltered despite energy intakes comparable with those of children in more supportive and protected environments. The energy requirements of these children were significantly higher. Some infants in developed countries may live in equally challenging environments.
Parental misconception and health beliefs concerning what constitutes a normal diet for infants have been reported by Pugliese et al. as a cause for failure to thrive as well. They reported seven infants from 7 to 22 months of age with poor weight gain and linear growth who received only 60% to 90% of minimum caloric intake for their age and sex. The parents explained that they wanted to avoid obesity, atherosclerosis, or junk food habits. It has also been shown that parental health beliefs and expectations have led to short stature and delayed puberty in older children.
Fruit Juice Excess
The custom of excessive use of fruit juices in recent decades has replaced the use of water for additional fluids after 6 months of life when the infant is learning to drink from a cup or a straw. The attractive packaging has contributed to this trend. Excessive fruit juice diminishes appetite, resulting in decreased dietary intake of nutrient-dense foods and a decrease in weight gain and ultimately in linear growth. An excess of fruit juice may be a cause of failure to thrive in older infants. Decrease in total high-energy intake is combined with malabsorption of fructose and diarrhea from sorbitol, thus compounding the problem. Excessive fruit juice intake in infancy is a major nutrition problem because juice has low nutrient value but high calories. The AAP has developed a guideline with restrictions on the use of fruit juices. For older children, their high caloric content may be a contributor to obesity.
Maternal Causes
Questions about a mother’s health, dietary habits, sleep pattern, smoking habits, medication intake, the events that occur during nursing, and the psychosocial atmosphere in the home are an important part of the history ( Figure 11-2 ).
