Failure to thrive is usually considered a condition that develops after an infant is discharged from the hospital. However, suboptimal growth is very common in the NICU environment.
Definition
Failure to thrive is an outmoded, imprecise term that remains in use only because alternatives such as growth faltering have failed to catch on. Failure to thrive implies a growth rate less than that which should be achieved based on a child’s individual genetic potential during typical conditions of health and well-being. Although, there is no agreed definition of failure to thrive, most definitions involve poor rates of growth (typically slow rates of weight gain), combined with lower bodyweight (eg, a weight less than the 3rd centile).
Malnutrition as a diagnosis overlaps with failure to thrive. Several different methods of diagnosis have been used and many divide malnutrition into mild, moderate, and severe.
Incidence
Failure to thrive in the NICU may be better described as extrauterine growth restriction (EUGR) and it is very common in extremely preterm infants, as their nutritional intake during the first several weeks of life is much worse than it would be in utero. With the additional effect of their comorbidities impacting both nutritional intake and energy requirements, inhospital growth of the preterm infant is often poor, and discharge weights below the 10th centile for age are the rule, rather than the exception.
Pathophysiology
The simplest way to consider FTT is as an imbalance between energy intake and energy requirements. FTT can, therefore, result from
Inadequate nutritional intake
Increased nutritional requirements
Increased nutritional losses
Risk factors
Extremely low birthweight (ELBW)
Intrauterine growth restriction (IUGR)
Bronchopulmonary dysplasia (BPD)
Necrotizing enterocolitis (NEC, especially surgical)
Infection (both congenital and late onset)
Chromosomal anomaly
Inborn error of metabolism
Clinical presentation
Failure to achieve recommended weight gain from birthweight to discharge
Goal weight gain of ≥18 g/kg/d
Failure to achieve recommended increase in head circumference from birth to discharge
Goal increase in head circumference of ≥0.9 cm/wk
Diagnosis
Growth charts (Figures 15-1 to 15-5)
While daily weights are an important measure of fluid status and provide a single point in assessing nutritional status, plotting weight, length, and head circumference on a weekly basis is essential in understanding the overall health and nutrition in the NICU infant.
Fetal-infant growth chart
Should be used until gestational age of 50 weeks
CDC growth chart for boys/girls
Birth to 36 months
Weight, length, and head circumference for age percentiles
Plot according to corrected age
If recommended growth is not attained prior to discharge
Assess the infant’s diet and take the necessary steps to ensure adequate nutrition support such as increasing protein intake and dietary protein/energy ratio.
Consider further workup for FTT.
Management
Infants in the NICU who are unable to grow, despite adequate nutritional support, should undergo a complete diagnostic workup prior to discharge. Consider the following:
Chronic lung disease
Congenital heart disease
Feeding intolerance (fat malabsorption, milk protein allergy)
Chronic infection (CMV, UTI)
Endocrinopathies (hypothyroidism, growth hormone deficiency, hypercalcemia, adrenal insufficiency)
Inborn error of metabolism
Genetic syndromes (Noonan, Russell-Silver, Turner)
Chronic renal insufficiency
See below for guidelines for management.
Discharge
Prior to discharge from the NICU all preterm infants need a clear feeding plan established.
Infants should receive their planned home feeds (the same formula, the same density, the same feeding interval, etc) for at least 48 hours before discharge to ensure adequate growth on the planned regime.
For more complex infants (BPD, cardiac disease, etc) longer periods of weight monitoring on the home regime may be merited prior to discharge.
If facilities exist to allow families to room–in with the infant prior to discharge, these can be very helpful especially in more complex cases. This rooming-in allows the parents and infant to establish pattern of feeding that works for them, with the experience of nurses and physicians nearby if required.
Tube-fed infants must have a feeding plan that includes increasing volume every so often in order to establish catch-up growth and maintain steady-growth postdischarge.
For catch-up growth in a preterm infant receiving tube feedings at NICU discharge, instruct parents to increase feeds by 5 mL weekly until weight is 25th to 50th centile on the growth curve.
Once the tube-fed infant’s weight is >25th centile on the growth curve, instruct parents to increase feeds by 5 mL every other week in order to maintain steady growth for approximately the first 6 months.
Definitions
Underweight, shunting, wasting, failure to thrive
Underweight
This is an abnormally low bodyweight for age. It is a bodyweight below a critical age- and gender-specific cutoff, for example, the 3rd weight centile for age (although the 2nd, 5th, or 10th centiles are sometimes used).
This is also the basis of the Gomez classification of malnutrition (Table 15-1), where malnutrition is divided into mild (weight 75% to 89% of median for age [approximate z-score −1.0 to −2.2]), moderate (weight 60% to 74% of median for age [approximate z-score −2.2 to −4.0]), and severe (weight <60% of median for age [approximate z-score <−4.0]).
UNICEF defines moderate and severe underweight differently as a weight-for-age z-score of less than −2 and −3, respectively.
Shunting
This is an abnormally low body length (or height) for age, ie, shortness. This is the basis of the Waterlow criteria for chronic malnutrition (Table 15-1).
Wasting
Wasting is an abnormally low bodyweight for height. It implies body thinness, and is a marker for acute nutritional deprivation.
It is the basis of the Waterlow criteria for acute malnutrition and the McLaren-Read criteria (Table 15-1.
UNICEF defines moderate and severe malnutrition as being below a weight-for-height z-score of −2 and −3, respectively.
Failure to thrive
Multiple definitions exist.
For our purposes we will define failure to thrive as being both (i) having a weight-for-age z-score of less than −2 on two or more occasions, and (ii) having a growth velocity less than expected (ie, the infant is diverging away from the reference population, or the weight-for-age z-score is continuing to decrease).
Just because an infant fails to meet this definition of failure to thrive does not mean that their growth is normal, or that further attention/intervention is not required.
Catch-up growth
Preterm infants
As a group, preterm infants typically show some degree of catch-up growth in the first few years with AGA infants, those without significant comorbidities, and less preterm infants being most likely to catch-up.
In VLBW infants, the lowest weight and length z-scores (standard-deviation score) are seen near term corrected age.
By 8 months, length has largely caught-up, but catch-up in weight is slower and may continue for at least 20 months.
The proportion of AGA VLBW infants with a weight more than 2 standard deviations below the mean for age peaks at term corrected age when it reaches almost 50%.
The nadir in weight and height occurs later in more preterm infants, and in the most preterm infants (GA <25 weeks) it may not occur until 12 months of age.
Catch-up growth in preterm infants often follows a pattern: first head circumference, then weight, then length.
SGA infants
Most (>80%) SGA infants (term or preterm) show catch-up growth (ie, weight above the 10th centile for age).
Catch-up growth in SGA infants most commonly occur within the first 6 months of age (75%) or less often over several years (7%).
However, 11% show no catch-up growth.
8% initially catch-up within the first 6 months, but are unable to sustain this transient catch-up growth and subsequently fall below the 10th centile for age again. Similar patterns are seen for catch-up in length and head circumference.
Absent or transient catch-up growth appears to be most common in preterm infants, and in infants with other comorbidities such as a prolonged oxygen requirement.
Selection of growth standards
Two main growth charts have been used in the United States—the CDC/NCHS reference and the WHO reference dataset.
The WHO charts are now preferred for infants aged less than 2 years.
The centiles on the WHO charts tend to be lower than the earlier CDC/ NCHS charts, in part because the CDC/ NCHS charts include more formula-fed infants.
The use of the WHO charts is likely to reduce the number of infants identified as being below the 3rd centile.
Correction for prematurity (Table 15-2
Weight data should be corrected for the degree of prematurity until 24 months of age. For example, the weight of a former 28-week infant who is now 9.7-month old should be plotted at age 6.7 months.
Length data should be corrected for prematurity until 40 months. Recumbent length, rather than height, should be measured until age 2 years.
Head circumference should be corrected until 30 months.
Incidence
Although concerns about growth are a relatively frequent complaint in the NICU graduate, there is relatively little data on the incidence of FTT.
Up to 40% of those admitted to hospital for FTT are low birthweight infants, much higher than the 7% incidence of low birthweight in the general population.
In one study of LBW infants, almost 20% met the case definition of FTT (weight <5th centile for age and abnormally low growth velocity) at some point in the first 3 years of life.
The peak incidence of diagnosis of FTT in LBW infants is at 8 months of age, after which the incidence of the diagnosis rapidly declines.
Infants diagnosed with FTT continued to be smaller than their peers until at least 3 years of age.
Pathophysiology/etiology
The simplest way to consider FTT is as an imbalance between energy intake and energy requirements. FTT can, therefore, result from inadequate nutritional intake, increased nutritional requirements, or increased nutritional losses.
Inadequate intake
Inadequate nutritional intake is by far the most common cause of FTT in former preterm infants, and can be due to infant or maternal factors, or the interaction between the infant and mother.
Infant factors
Oral intake may be limited by a range of factors.
Developmental factors: Such as limited suck-swallow breath coordination, reduced arousal for feeds, oral aversion.
Anatomical factors: Such as cleft lip and palate, nasal obstruction, choanal atresia/stenosis, micrognathia, Pierre-Robin sequence, reduced size of nasopharynx.
Physiological factors: Including anemia that may limit exercise tolerance.
Functional factors: Such as cardiorespiratory problems that may limit enteral intake and slow the rate of feeding, gastroesophageal reflux.
Constitutional factors: Anorexia is a component of many chronic illnesses such as renal insufficiency, or chronic infections.
Maternal factors
These may include maternal lack of understanding of infant feeding or satiety cues, misunderstandings about the amount and composition of feeds to be given, poor supply of human milk (especially in exclusively breast-fed infants), effects of stress on maternal milk production, maternal fearfulness in caring for a preterm infant, care-giving fatigue, etc.
Maternal-infant interaction
Maternal separation from the infant may lead to nervousness with caring for a preterm infant that may be reflected in poor establishment of a robust maternal-infant pattern of feeding.
Effect of comorbidities
Many comorbidities may decrease feed intake.
Neurological problems, including cerebral palsy, may lead to hypo- or hypertonia and poor feeding. They may also lead to decreased arousal for feeds.
Respiratory diseases such as BPD may decrease exercise tolerance and limit feed intake. This may be worsened by desaturations that sometimes accompany feeds, and the increased respiratory rate that can be seen in BPD may make suck-swallow breath coordination more difficult.
Congenital heart disease limits exercise tolerance and such infants may have desaturations and dyspnea with feeds. These changes per se and care givers responses to them may limit feed intake.
Increased requirements
Energy requirements are high in preterm infants (120 kcal/kg/d) and may be much higher in the presence of comorbidities such as congenital heart disease (CHD) that may lead to increased energy requirements as high as 145 kcal/kg/d.
This appears to be especially true of conditions associated with pulmonary overcirculation.
Similarly, chronic lung disease or bronchopulmonary dysplasia can increase energy expenditure and lead to reduced growth.
Increased losses
Gastrointestinal malabsorption of fat, protein, or carbohydrate may cause FTT, as this may increase nutrient losses from the gut or the kidneys.
For example, some congenital heart diseases (eg, single ventricle physiology following Fontan) are associated with protein losing enteropathy, presumably due to elevated venous pressures.
NICU graduates with a history of NEC, short bowel syndrome, and cholestasis may also develop malabsorption.
Chronic conditions associated with FTT
A wide range of primary medical, genetic, or metabolic conditions may present as FTT in the NICU graduate just as they may in any other infant. However, they area relatively uncommon cause compared to inadequate intake.
Other causes
Medications: Some medications (eg, steroids) may limit growth.
Fluid restriction: The most common iatrogenic cause of FTT is probably fluid restriction. This is most commonly seen in infants with bronchopulmonary dysplasia or congestive heart failure where fluid restriction is a mainstay of therapy. However, extreme fluid restriction will limit the nutrient intake of the infant and reduce growth. This is problematic, as adequate nutrition and growth are the main curative therapy for BPD, and infants with cong-estive heart failure are already at elevated risk of growth failure.
Acidosis: Either metabolic or respiratory.
Electrolyte abnormalities (especially hyponatremia) are associated with growth failure. Once again, these may be iatrogenic in origin, for example, hyponatremia resulting from use of diuretics in an infant with congestive heart failure.
Anemia per se may cause growth failure, although the evidence for this is limited. However, severe anemia will reduce exercise tolerance and can lead to inadequate nutrient intake.
Risk factors
Risk factors for poor growth after hospital discharge and for the diagnosis of FTT include
Ethnicity (with African-Americans at increased risk)
The presence of chronic illnesses
Low birthweight z-score
Lower maternal education
Lower maternal height z-score
Comorbid conditions significantly increase the risk of failure to thrive in preterm infants, especially the presence of
Neurological abnormalities
Cerebral palsy
Bronchopulmonary dysplasia
Congenital heart disease
Diagnosis
Failure to thrive is underdiagnosed.
There are many causes for this including the variability in longitudinal weight measurements, as about 25% of children will have a change in weight centile of at least 25% within the first 2 years of life.
Underdiagnosis is probably more common in the NICU graduate because of a feeling that poor growth is inevitable or due to the difficulty accurately assessing rates of weight gain in subjects below the lowest centile line on the growth chart.
Severity
The most common grading of malnutrition is the Gomez criteria that utilize the ratio of the actual weight to the median weight for that age (Table 15-1.
A weight >60% of the median for age is considered severe malnutrition.
UNICEF defines moderate and severe malnutrition as having a weight-for-height z-score of less than −2 and −3, respectively, and moderate and severe underweight as a weight-for-age z-score of less than −2 and −3, respectively.
For comparison, the 5th centile line is equivalent to a z-score of −1.65, the 3rd centile to a z-score of −1.88, and the 2nd centile to a z-score = −2.05.
Workup
The most common cause of FTT in NICU graduates is inadequate nutritional intake. However, preterm infants are no less likely than term infants to present with failure to thrive due to renal insufficiency or fat malabsorption due to an underlying condition than is a term infant. The diagnostic workup should, therefore, concentrate on a thorough evaluation of nutritional and dietary factors, but seek to exclude underlying constitutional factors.
History
Growth history: Data should be collected on birthweight (and, if available, length and head circumference) and on subsequent weight, length, and head circumference measurements. These should be plotted on the gender-specific WHO growth charts after correcting for the degree of prematurity (Table 15-2. Failure to correct for prematurity is a possible cause of misdiagnosing a preterm infant with FTT. For example, a 6-month-old former 28-week infant’s growth will look very different if it is plotted at 6 months of age (actual age) rather than at 3 months of age (corrected age).
Important questions to answer are
Has the weight, length, and head circumference data been appropriately corrected for prematurity?
Was the baby SGA or AGA?
What is the baby’s current weight, length, and head circumference centile? A disproportionality low weight compared to length or head circumference suggests a nutritional cause for poor growth.
What is the baby’s current weight gain? Averaged over a month or more, the weight gain of term born infant is 26 to 31 g/d between 0 and 3 months, 17 to 18 g/d between 3 and 6 months, 12 to 13 g/d between 6 and 9 months, and 7 to 9 g/d between 9 and 12 months.
Is the baby’s growth parallel to centile lines or continuing to diverge away from them?
What is the pattern of growth? Weight deceleration preceding length deceleration suggests a nutritional cause.
Feeding history: A detailed history of the type and amount of feeds given is essential. A calculation of the approximate volume the baby is receiving in 24 hours should be made, and the calorie intake calculated. A reasonable target calorie intake immediately after hospital discharge should be about 120 kcal/kg/d. This could be provided by 180 mL/kg/d of human milk or a term formula, or 165 mL/kg/d of a postdischarge (22 kcal/oz) formula. Such a calculation cannot be made in the breast-fed infant without carrying out pre- and postweighing of the baby. This is difficult to do as an outpatient, and even as an inpatient requires an appropriate scale.
Important questions to answer are
What is the baby being fed? How much? And how often?
If the baby is being breast-fed, does the mother perceive breast fullness before feeds, and a sense on emptying after feeds?
Are nonnutritional fluids being given (eg, water, juices)?
How often is the baby stooling and voiding?
Does the baby awaken for feeds and seem hungry? Often when nutritional intake is inadequate, babies will stop awaking for feeds, and need to be woken to feed.
If formula is being given, how is it being prepared? Is the appropriate recipe being followed? Inadvertent feeding of overly dilute formulas is not an uncommon reason for poor growth.
Are any solid feeds being given?
Previous medical history: The baby’s previous medical history needs to be reviewed in detail. For example, a history of NEC with bowel resection would make malabsorption secondary to short bowel syndrome a possibility; if the baby had weaned off oxygen immediately prior to discharge then one would consider undertreated BPD and potential hypoxia and desaturations limiting feeds; an infant with hypotonia or Trisomy 21 would be at increased risk of poor feeding and inadequate intake.
Review of systems: A detailed review of systems is required to exclude rare constitutional causes of FTT. It may also provide a clue as to an underlying diagnosis. For example, if shortness of breath was noted during feeding one would need to consider choanal atresia, laryngomalacia, congestive heart failure, poorly controlled BPD, etc.
Medication history: Some medications (eg, steroids) may limit growth. Other medications may give a clue as to details of the medical history that have been overlooked. For example, a mother may not mention the history of mild BPD, or a VSD, unless prompted to say why the baby is receiving oral diuretics.
Social history: Questions should be gently directed to determining the mother’s comfort level with caring for the baby: Are there home circumstances complicating the care of the baby? Is the baby a difficult feeder who is being fed by several different people as the mother has returned to work, etc.
Physical examination
Infant examination: A thorough and complete physical examination looking for clues to underlying systemic diseases is needed.
Feeding evaluation: Whenever possible a feeding evaluation is needed. This may simply be watching the mother give a single feed and seeing how the baby is held, how the baby latches on, how the mother responds to the infant’s cues, etc. This is especially valuable in the human milk fed infant. Many physicians feel inadequate to this task, in which case an outpatient lactation consult or feeding evaluation by an experienced speech and/or occupational therapist may be helpful. Pre- and postweighing of the breast-fed baby before and after a fed will allow an approximate calculation of the milk intake.
Laboratory investigation
Laboratory investigations are rarely helpful unless there is a specific clinical suspicion based on details of the infant history or physical.
A baseline CBC, CRP, BUN, and electrolytes
A urinalysis
In infants with respiratory or cardiac disorders (BPD, VSD, congestive heart failure) a blood gas can be helpful even if the infant appears clinically stable. In both cases, growth failure may be the first sign of worsening respiratory or cardiac status and the identification of respiratory acidosis on the blood gas can be very informative.
In infants with severe brain injury, consider thyroid function tests (free thyroxine and thyroid stimulating hormone) or a screen for panhypopituitarism, including growth hormone studies (IGF-1, IGFBP-3).
Karyotype and DNA microarray.
A prealbumin level may better your understanding of nutritional intake.
Imaging
Brain MRI (with poor growth in HC or evidence of hypopituitarism)
Bone age determination (estimates skeletal maturation)
Management
In most cases of FTT, dietary intake is inadequate, either in absolute terms or relative to the increased needs of the infant (for example, secondary to BPD). Initial management should, therefore, focus on dietary measures. Should these interventions be unsuccessful, or if there are concerns about a constitutional disorder, further workup and possible referral to a specialist is reasonable.
For infants managed by the primary care physician, management should focus on excluding significant systemic disease by history and examination, with limited laboratory or diagnostic testing. The most common intervention is likely to be increasing the caloric intake.
Dietary intervention
There are limited options to increase the nutritional intake of ad libitum fed infants. As the volume of intake is determined by the infant, this is not modifiable by the care giver, and attempts to “get more milk into the baby” are almost always unsuccessful and lead to frustration for the care giver, baby, and physician!
Review current diet: If enriched postdischarge formulas were stopped before 6 months corrected age, they should be restarted and if solid foods were started before 6 months corrected age they should be discouraged.
Increasing caloric density
Increasing the caloric density of feeds can be very helpful in infants who are likely to tire out before taking their required volume. Such infants could include infants with the BPD, congestive heart failure, poor feeding coordination, hypotonia, or neurological disorders, or infants with syndromes such as Trisomy 21.
By reducing the volume of feed the infant needs to take, he or she may be able to achieve their required nutritional intake more easily. Furthermore, this may improve symptoms in infants with BPD or congestive cardiac failure.
Usually caloric density is increased stepwise from 20 or 22 kcal/oz to 24, 27, and finally 30 kcal/oz. Be sure the hydration status is adequate in infants on diuretics and feeds with a high caloric density.
In formula-fed infants and infants receiving expressed breast milk by bottle, the caloric density of the feeds can be increased.
In breast-fed infants, two to three breast-feeds daily can be replaced by a concentrated formula. If the formula acts to replace human milk, then the increased nutrient intake is small. However, if the mother’s milk supply is limited, the formula may be an addition to the total daily intake of human milk (rather than a replacement for some of it) and the increase in nutrient intake will be much greater. If infants are being bottle-fed human milk (either mother’s own milk or donor milk), this can be fortified by adding either modular fortifiers (protein, fat, carbohydrate, or a combination thereof) or powdered formula. The latter is most common and least expensive. Some state’s WIC programs will provide human milk fortifier; however, this can be very expensive if parents are paying out of pocket.
Changing feed composition
In ad libitum fed infants, changing the caloric density of the feed may have little effect on nutrient intake as the infant may downregulate their volume of intake to compensate for the increased density. However, changing the protein-energy ratio may have a bigger effect in cases such as protein losing enteropathies or nephrotic syndrome but otherwise it is rarely helpful.
Increasing volume of intake
This is often impractical in the ab libitum fed infant; however, there are exceptions.
Some infants with marginal cardiorespiratory status (eg, chronic lung disease or congestive cardiac failure) may be able to take larger volumes of feeds ad libitum following improved medical management of their underlying condition. For example, in infants with chronic lung disease provision of low flow oxygen (or increased flow compared to basal conditions) during feeds can increase intake in some infants.
Some infants sleep without waking to feed at night, sometimes up to 10- to 12-hour stretches. One strategy may be to add a nighttime feed (bottle or breast-feed) as one additional feed, which may go a long way in terms of growth.
In some infants with marginal feeding skills, relatively minor problems, such as nasal congestion from an upper respiratory illness or oral candidiasis, can have a significant effect on feeding volumes. Occasionally, treatment of these conditions can have unexpected large benefits to feeding intake.
In gavage fed infants (either nasogastric or gastrostomy tube fed) intake volumes can often be increased and tolerated well. In fact, not regularly increasing the volumes of feeds in tube-fed infants is often a cause for poor growth.
Feeding intervention
In babies with certain syndromes or anatomic defects, a feeding evaluation may identify methods to improve feeding. This is particularly true of infants with Pierre-Robin sequence or cleft palate. In infants who are unable to take sufficient feeds ad libitum, tube feeding (by either nasogastric or gastrostomy tubes) may need to be considered.
Need for referral
The primary care physician may be able to manage less severe degrees of malnutrition but referral for a specialist opinion should be considered in the following situations:
Malnutrition is severe (by Gomez stage, weight <60% of median for age, or weight-for-age z-score <−4), in which case referral to a gastroenterologist/nutritionist for closer observation is prudent.
If there are other related gastrointestinal symptoms, such as significant vomiting or diarrhea, refer to gastroenterologist.
There is severe chronic lung disease, or home oxygen use (refer to pulmonologist, and consider changes to pulmonary and nutritional care).
There is a clinically significant congenital heart disease (refer to cardiologist, and consider changes to cardiac and nutritional care).
There is a history of necrotizing enterocolitis with significant bowel resection (refer to gastroenterologist for possible malabsorption or short bowel syndrome).
There is a known endocrine abnormality that might impact growth (refer to endocrinologist).
In infants with poor oral feeding skills, including a difficulty in transitioning to solid foods, and no underlying medical condition, consider evaluation and feeding therapy with a lactation specialist, occupational therapist, or speech therapist skilled in infant feeding (see Chapter 47).
Follow-up
Whatever intervention is carried out, close follow-up is essential. Initially the family should be seen every week. Changes in weight velocity may not be apparent immediately, but evidence of improved nutritional intake can be seen week to week. If the infant does not show catch-up growth in response to the intervention within 4 weeks, referral to a specialist should be considered.
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