Constitutional growth delay

The recognition of growth and developmental problems in infants and children is one of the major challenges facing primary care physicians. Failure to thrive (FTT) is a common condition of varying etiologies that has been associated with adverse effects on later growth and cognitive development. (1,2) Primary care physicians need to be able to diagnose and manage FTT promptly to reduce the risk of long-term sequelae.

Definition

FTT is best defined as inadequate physical growth diagnosed by observation of growth over time using a standard growth chart. The National Center for Health Statistics (NCHS) recently released improved growth charts that can be found at www.cdc.gov. While definitions of FTT have varied, most practitioners diagnose FTT when a child's weight for age falls below the fifth percentile of the standard NCHS growth chart or if it crosses two major percentile lines. (3) Recent research has validated that the weight-for-age approach is the simplest and most reasonable marker for FTT. (4) Other growth parameters that can assist in making the diagnosis of FTT are weight for height and height for age. FTT is diagnosed if a child falls below the 10th percentile for either of these measurements.

Etiology and Differential Diagnosis

Historically, FTT has been classified as organic or nonorganic. Usually, this distinction is not useful because most children have mixed etiologies. (5) For example, a child may have a medical disorder that causes feeding problems and family stress. The stress can compound the feeding problem and aggravate FTT. A more useful classification system is based on pathophysiology--inadequate caloric intake, inadequate absorption, excess metabolic demand, or defective utilization. This classification leads to a logical organization of the many conditions that cause or contribute to FTT (Table 1).

Stress and other psychosocial factors frequently contribute to FTT. For example, a depressed mother may not feed her infant adequately. The infant may become withdrawn, responding to the mother's depression, and feed less well. Another example is when parents are overly anxious about a child's feeding. Coercive practices can lead to feeding behavior problems and FTT.

Growth variation in normal infants can confound the diagnosis of FTT. Approximately 25 percent of children will shift down their weight or height by more than 25 percentile points in the first two years of life. (6) These children are falling to their genetic potential or demonstrating constitutional growth delay (slow growth with a bone age less than chronologic age). After shifting down, these infants grow at a normal rate along their new percentile and do not have FTT.

Specific infant populations with growth variations also need to be considered when making the diagnosis of FTT. Infants who have had intrauterine growth retardation or premature infants may appear to have FTT when they grow at less than the fifth percentile. As long as the child is growing along a curve with a normal interval growth rate, FTT should not be diagnosed. (7) In addition, using modified growth charts for specific populations, such as premature infants, (8) exclusively breastfed infants, specific ethnicities (e.g., Asian), and infants with genetic syndromes (e.g., Down syndrome), (9) can help reassure the physician that these children are growing appropriately.

Evaluation

RECOGNIZING FTT

The key to diagnosing FTT is finding the time in busy clinical practice to accurately measure and plot a child's weight, height, and head circumference, and then assess the trend. One study (10) from England demonstrated that 54 percent of general practitioners had not diagnosed FTT although a child's weight for age fell below two major percentile lines. In addition, a pilot study (11) performed at a family practice residency clinic found that of 29 children diagnosed with FTT, 100 percent of the charts contained measurements that were incorrectly plotted. The diagnosis was delayed in 41 percent of the patients.

HISTORY

After determining that FTT is a concern, the evaluation should focus on a careful history, including an assessment of diet and feeding or eating behaviors, and past and current medical, social, and family history. Table 2 details items that should be covered in each category.

It is important to ascertain the child's developmental status at the time of diagnosis because children with FTT have a higher incidence of developmental delays than the general population. (12) Physicians should still be concerned about a child without developmental delays who is failing to thrive. FTT is primarily a growth disorder, not a developmental problem.

PHYSICAL EXAMINATION

A complete physical examination is essential, with four main goals: (1) identification of dysmorphic features suggestive of a genetic disorder impeding growth; (2) detection of underlying disease that may impair growth; (3) assessment for signs of possible child abuse; and (4) assessment of the severity and possible effects of malnutrition. (12,13) The severity of a child's undernutrition can be determined most easily by using the Gomez criteria. By comparing the child's current weight for age with the expected weight (50th percentile) at that age, the degree of malnutrition can be assessed. If the weight is less than 60 percent of expected, the FTT is considered severe, 61 to 75 percent denotes moderate FTT, and 76 to 90 percent is mild. (14)

PARENT-CHILD INTERACTION

FTT often involves psychosocial problems compromising the relationship or fit between parent and child. Observing the interaction between a parent and child, especially during a feeding session in the office, may provide valuable information about the etiology of FTT. (3,12) Parents can be asked to feed an infant or bring in a snack for a toddler. The assessment should be done at a time when the child is hungry. It is important to pay attention to a caregiver's ability to recognize the child's cues, the child's responsiveness, and the parental warmth and appropriate behavior toward the child. (12) It is similarly important to observe the nature of the child's cues (clear or not), the child's temperament, and responses toward the parent. Developing a portrait of the relationship is key to guiding intervention.

LABORATORY EVALUATION

Laboratory evaluation should be guided by history and physical examination findings only. There are no routine laboratory tests that should be performed on every child, because the majority of children with FTT have no laboratory abnormalities. In a classic study of hospitalized children with FTT, only 1.4 percent (36 of 2,607 tests) were of diagnostic assistance. (15) [Evidence level B, historical, uncontrolled study] A practical approach to laboratory studies is to not order any at the time of diagnosis, unless suggested by the history or physical examination. For example, a history of steatorrhea (greasy, malodorous stools) should prompt the physician to send a stool sample for fecal fat and perhaps order a sweat test if there is suspicion of cystic fibrosis. If the child's growth has not improved, screening tests to consider at the next visit include a complete blood count and a urinalysis. If FTT persists despite an adequate diet, malabsorption can be further investigated by obtaining stool for fat and reducing substances, and possibly obtaining a celiac antibody profile.

Management Tools

The first rule for treating FTT is to identify the underlying cause and correct it. This requires a stepwise approach that is guided by history and response to therapy. Most cases can be managed by nutrition intervention or feeding behavior modification. Children who do not respond may require further evaluation. Two principles that hold true irrespective of the etiology are that all children with FTT need a high-calorie diet for catch-up growth, and all children with FTT need close follow-up. Usually, children should be followed at least monthly until catch-up growth is demonstrated and the positive trend is maintained.

THREE-DAY FOOD DIARY

It may seem surprising that undernutrition is a common factor in FTT, but with an energy need that is almost triple that of adults (in calories per kg) it becomes easier to understand how quickly infants can fall behind on growth. (16) Having parents write down the types of food and amounts a child eats over a three-day period is one way of quantifying caloric intake. In some instances, it can make parents aware of how much the child is or is not eating.

Limit fruit juice to 8 to 16 oz per day. Fruit juice is an important contributor to poor growth by providing relatively empty carbohydrate calories and diminishing a child's appetite for nutritious meals, leading to decreased caloric intake. (17)

HIGH-CALORIE DIET

Children with FTT will need 150 percent of their recommended daily caloric intake, based on their expected, not actual, weight (Table 3 (18)). (6,7) In infants, this increased calorie intake may be accomplished by concentrating formula or adding rice cereal to pureed foods. Toddlers can receive more calories by adding taste-pleasing fats such as cheese, sour cream, butter, and peanut butter to common toddler foods. The government's supplemental food program for women, infants, and children (WIC) also provides high-calorie milk drinks (e.g., PediaSure). One or two cans per day can be used instead of milk, providing 30 calories per oz instead of the 19 calories per oz in whole milk. Adding a multivitamin helps ensure that a child receives the minimum recommended vitamins and minerals. Some practitioners add zinc to reduce the energy cost of weight gain during catch-up growth, though the data about its benefit are mixed. (19,20)

FEEDING OR EATING BEHAVIORS

Parental anxiety about a child's FTT can be helped by reassurance. Parents should encourage, but not force, their child to eat. Meals should be pleasant, regularly scheduled, and not rushed. It often helps if the parents eat with the child. The child should be positioned so that the head is up and the child is comfortable (e.g., in high chair). Starting with small amounts of food and offering more is preferable to beginning with large quantities. Parents should consider foods that the child likes (e.g., it is not important for children to eat four different green vegetables, but it is important to encourage some variety and to cover the basic food groups). Snacks need to be timed in between meals so that the child's appetite will not be spoiled.

HOSPITALIZATION

Hospitalization is rarely required, and most children with FTT are managed as outpatients. The lack of benefit to hospitalization in most cases has been apparent for decades. (21) Hospitalization may be necessary when the safety of the child is a concern, outpatient management has failed, or the FTT is severe.

REFERRAL

For children who do not respond to initial management, it may be necessary to seek assistance from a subspecialist. Traditionally, a multidisciplinary approach to FTT--using physicians, nurses, dietitians, social workers, and psychologists--has produced better outcomes. (7) This approach may not be practical in all cases, but for children who are not improving because of an undiagnosed medical condition or a particularly challenging social situation, a multidisciplinary approach may be the best answer.

Outcomes

Children with FTT are at risk for adverse outcomes such as short stature, behavior problems, and developmental delay. (1,2,5,22-24) FTT is more likely a contributing or associated factor to these adverse outcomes, rather than the exclusive cause. There are a limited number of outcome studies on children with FTT, each with different definitions and designs, so it is difficult to comment with certainty on the long-term results of FTT. (25) In addition, it is often difficult to disentangle the effects of FTT from those of the high-risk environments in which FTT often occurs (e.g., poverty, high family stress, and poor parental coping skills). (5,26)

To decrease the risk of adverse effects, it is important to recognize and treat FTT promptly. Early childhood is a critical period for growth and development, and early intervention for any child with FTT will maximize the potential for better outcomes. (22) Given the evidence of long-term problems, all children who have been diagnosed with FTT need to be followed carefully for possible later sequelae.

Table 1

Selective Differential Diagnosis of Failure to Thrive

Inadequate caloric intake

Incorrect preparation of formula (too diluted, too concentrated)

Unsuitable feeding habits (food fads, excessive juice)

Behavior problems affecting eating

Poverty and food shortages

Neglect

Disturbed parent-child relationship

Mechanical feeding difficulties

(oromotor dysfunction, congenital anomalies, central nervous system damage, severe reflux)

Inadequate absorption

Celiac disease

Cystic fibrosis

Cow's milk protein allergy

Vitamin or mineral deficiencies (acrodermatitis enteropathica, scurvy)

Biliary atresia or liver disease

Necrotizing enterocolitis or short-gut syndrome

Increased metabolism

Hyperthyroidism

Chronic infection

(human immunodeficiency virus or other immunodeficiency, malignancy, renal disease)

Hypoxemia (congenital heart defects, chronic lung disease)

Defective utilization

Genetic abnormalities (trisomies 21, 18, and 13)

Congenital infections

Metabolic disorders (storage diseases, amino acid disorders)

The authors indicate that they do not have any conflicts of interest. Sources of funding: none reported.

REFERENCES

(1.) Kristiansson B, Fallstrom SP. Growth at the age of 4 years subsequent to early failure to thrive. Child Abuse Negl 1987;11:35-40.

(2.) Corbett SS, Drewett RF, Wright CM. Does a fall down a centile chart matter? The growth and developmental sequelae of mild failure to thrive. Acta Paediatr 1996;85:1278-83.

(3.) Bithoney WG, Dubowitz H, Egan H. Failure to thrive/ growth deficiency. Pediatr Rev 1992;13:453-60.

(4.) Raynor P, Rudolf MC. Anthropometric indices of failure to thrive. Arch Dis Child 2000;82:364-5.

(5.) Gahagan S, Holmes R. A stepwise approach to evaluation of undernutrition and failure to thrive. Pediatr Clin North Am 1998;45:169-87.

(6.) Schmitt BD, Mauro RD. Nonorganic failure to thrive: an outpatient approach. Child Abuse Negl 1989;13:23548.

(7.) Maggioni A, Lifshitz F. Nutritional management of failure to thrive. Pediatr Clin North Am 1995; 42:791810.

(8.) Babson SG. Growth of low-birth-weight infants. J Pediatr 1970;77:11-8.

(9.) Cronk C, Crocker AC, Pueschel SM, Shea AM, Zackai E, Pickens G, et al. Growth charts for children with Down syndrome: 1 month to 18 years of age. Pediatrics 1988;81:102-10.

(10.) Batchelor JA. Has recognition of failure to thrive changed? Child Care Health Dev 1996;22:235-40.

(11.) Krugman SD, Jablonski KA, Dubowitz H. Missed opportunities to diagnose failure to thrive in a family medicine resident practice. Pediatr Res 2000;47(2 pt 2):204A.

(12.) Rider EA, Bithoney WG. Medical assessment and management and the organization of medical services. In: Kessler DB, Dawson P, eds. Failure to thrive and pediatric undernutrition: a transdisciplinary approach. Baltimore: Brookes, 1999:173-94.

(13.) Wissow LS. Failure to thrive and psychosocial dwarfism. In: Wissow LS, ed. Child advocacy for the clinician: an approach to child abuse and neglect. Baltimore: Williams & Wilkins, 1990:133-57.

(14.) Powell GF. Nonorganic failure to thrive in infancy: an update on nutrition, behavior, and growth. J Am Coll Nutr 1988;7:345-53.

(15.) Sills RH. Failure to thrive. The role of clinical and laboratory evaluation. Am J Dis Child 1978; 132:967-9.

(16.) Wright CM. Identification and management of failure to thrive: a community perspective. Arch Dis Child 2000;82:59.

(17.) Smith MM, Lifshitz F. Excess fruit juice consumption as a contributing factor in nonorganic failure to thrive. Pediatrics 1994;93:438-43.

(18.) Hay WW. Current pediatric diagnosis and treatment. 15th ed. Norwalk, Conn.: Appleton & Lange, 2001:250.

(19.) Walravens PA, Hambidge KM, Koepfer DM. Zinc supplementation in infants with a nutritional pattern of failure to thrive: a double-blind, controlled study. Pediatrics 1989;83:532-8.

(20.) Hershkovitz E, Printzman L, Segev Y, Levy J, Phillip M. Zinc supplementation increases the level of serum insulin-like growth factor-I but does not promote growth in infants with nonorganic failure to thrive. Horm Res 1999;52:200-4.

(21.) Berwick DM, Levy JC, Kleinerman R. Failure to thrive: diagnostic yield of hospitalisation. Arch Dis Child 1982;57:347-51.

(22.) Metallinos-Katsaras E, Gorman KS. Effects of undernutrition on growth and development. In: Kessler DB, Dawson P, eds. Failure to thrive and pediatric undernutrition: a transdisciplinary approach. Baltimore: Brookes, 1999:37-64.

(23.) Oates RK, Peacock A, Forrest D. Long-term effects of nonorganic failure to thrive. Pediatrics 1985; 75:36-40.

(24.) Heffer RW, Kelley ML. Nonorganic failure to thrive: developmental outcomes and psychosocial assessment and intervention issues. Res Dev Disabil 1994;15:247-68.

(25.) Drotar D, Robinson J. Researching failure to thrive: progress, problems, and recommendations. In: Kessler DB, Dawson P, eds. Failure to thrive and pediatric undernutrition: a transdisciplinary approach. Baltimore: Brookes, 1999:77-95.

(26.) Sherry B. Epidemiology of inadequate growth. In: Kessler DB, Dawson P, eds. Failure to thrive and pediatric undernutrition: a transdisciplinary approach. Baltimore: Brookes, 1999:19-36.

SCOTT D. KRUGMAN, M.D., is chair of the pediatrics department at Franklin Square Hospital Center, Baltimore, and faculty for the family practice residency program. In addition, he is clinical assistant professor of pediatrics at the University of Maryland School of Medicine, Baltimore. After graduating from Dartmouth Medical School, Hanover, N.H., Dr. Krugman completed his pediatric residency at Johns Hopkins Hospital, Baltimore.

HOWARD DUBOWITZ, M.D., M.S., is professor of pediatrics and co-director of the Center for Families at the University of Maryland School of Medicine, Baltimore. He received his medical degree from the University of Cape Town, South Africa. After completing a pediatrics residency at Boston Medical Center, he completed a child maltreatment fellowship at Children's Hospital Boston.

Address correspondence to Scott D. Krugman, M.D., Dept. of Pediatrics, Franklin Square Hospital Center, 9000 Franklin Square Dr., Baltimore, MD 21237 (e-mail: scott.krugman@medstar.net). Reprints are not available from the authors.

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