Nutritional well-being in early life is typically assessed by growth.1 Both overweight and underweight reflect an imbalance between a child's actual intake and the energy required to support ideal height and weight. Although obesity is an urgent focus worldwide, it is undernutrition that carries the greater morbidity and mortality in the immediate and long term.2 Globally, approximately 20 million children are severely undernourished, contributing to 45% of all child deaths.2 Being either overweight or underweight in early life increases the likelihood of future cardiometabolic disorders, but undernutrition also threatens neural development, cognition, and academic achievement.2,3 Undernutrition among children in the United States and other Western countries often goes unrecognized and untreated, even when malnutrition is moderate to severe (ie, below the third to fifth percentile, or a z score of −2 to −3 standard deviations [SD]).4–6 The malnourished population usually consists of children with acute or chronic illnesses; children with special health care needs involving physical, developmental, behavioral, or emotional disorders; and children who are hospitalized.
A recent expert panel on malnutrition cited three cause-based categories of diminished growth velocity: (1) acute illness resulting in a loss of energy and some nutrients, (2) chronic illness with severe deficits in both energy and nutrients, and (3) no apparent illness, which the consensus panel attributed primarily to energy deficit.5 The third category is the most common but also the least likely to be recognized by the primary care clinician early in its course. If “risk” is exclusively tied to a child's height and weight, then undernutrition in the absence of growth faltering will not merit intervention. But this implies that children in the “normal” range (5th to 85th percentile, or a z score of −1 to +1 SD) do not have the potential for adverse outcomes. Even in the absence of weight loss or overt nutrient deficiency, nutrient depletion alone may incur lasting problems.
Review and Discussion
Early Life Represents a Singularity
Although the velocity of linear growth and weight gain during the first years are unparalleled at any other time of life, the first years after birth are singularly unique for other reasons. Nutrition not only promotes increased bone length, muscle mass, and tissue growth, but also supports continued development of several highly metabolic organs, such as the gastrointestinal tract, the immune system, the cardiorespiratory system, the kidneys, and the central nervous system.7 From birth, sensory and motor experiences generate new synapses at a rate of nearly 700 per second.8 As a result, brain volume doubles by 12 months and triples by 36 months, which alone accounts for up to 60% of the infant's extremely high basal metabolic rate, which is 2.5 times that of an adult.7
The developmental outcomes associated with undernutrition may be subtle and difficult to diagnose if they fail to elicit the overt clinical manifestations associated with moderate-to-severe growth failure (malnutrition or stunting, delayed wound healing, weakened immunity, infectious disease) or with overt nutritional deficiency states (iron-deficiency anemia, vitamin D-deficient rickets, zinc-deficiency perioral rash or diarrhea).6 Choline-deficiency symptoms such as fatigue, memory impairment, learning disabilities, and mood shifts are difficult to appreciate in young children, as are insufficiencies of docosahexaenoic acid, iodine, lutein, or precursors to neurotransmitters such as B vitamins, phenylalanine, tyrosine, or taurine.
Researchers have begun to look at the potential consequences of poor diet quality in infant and toddlers. A recent study correlated low diet-quality scores in early life with poor cognitive skills, behavioral issues, and low academic achievement later in childhood or adolescence.9 Parents with an authoritarian feeding style, those with developmentally inappropriate expectations, or those engaged in food fads or highly restrictive dietary patterns may undermine their child's dietary pattern.10 Children who are particularly selective eaters, as well as those who are neglected or food insecure, also may face neurodevelopmental consequences despite adequate corporal growth.6,11
Identification of the Child with Nutritional Risk
Two populations of children often present to the primary care practitioner with a potential risk for undernutrition. The first group is comprised of infants and toddlers with medical histories that raise the likelihood of inadequate dietary intake (Table 1). Recurrent infections merit particular concern as well because the associated inflammatory cytokines can cause prolonged anorexia. Reestablishing growth with supplementation has been shown to restore appetite.12 Repeated antibiotic use can substantially alter the gut microbiome, which may affect satiety and metabolism.13 More than 20% of US children are food insecure and their poor nutritional status is often missed despite simple screening resources for clinical practice.14,15
Red Flags Indicating Potential Risk of Malnourishment or Growth Failure
The second group potentially at risk for undernutrition is comprised of highly selective eaters. Complaints about how and what their toddlers eat are reported by more than 50% of parents in some studies.16 The Avon Longitudinal Study of Parents and Children,17 using clear and specific questions, identified 10% to 15% of children as particularly selective eaters with a potential risk for inadequate nutrition. The terms “picky” or “fussy” eater may bias against clinical urgency, but the time between parental complaints about dietary intake and physician concerns about growth represents a prolonged period of poor diet quality (Figure 1).
Continuum from parental concern to physician concern over malnourishment in early childhood feeding.
Highly selective eaters tend to share similar traits. Their duration of being breast-fed is short and their exposure to solid food begins early. Children who are selective eaters are suspicious of new flavors and textures. They show a low enjoyment of food, eat slowly, and prefer liquids. Their limited food preferences often result in nutrient inadequacy at a crucial developmental stage, even if they consume sufficient energy to sustain growth.15 Rigid, authoritarian parenting commonly results in parent-child stress at meal times. Parent-child dietary struggles often further increase the child's resistance. Conversely, parental acquiescence to child preferences often erodes diet quality. These types of behavioral issues take time to correct, compounding nutritional risk.18,19
Clinicians usually recognize growth failure when a child is 2 SD below z score, but they may not acknowledge the potential risk when a child has fallen only 1 SD below the mean (Figure 2). A child who has fallen into the 5th to 25th percentile area of weight-for-height merits close scrutiny.20 A brief diet history can reveal parental attitudes, expectations, approaches, and frustrations that often affect infant-toddler feeding.10,18–20 Children at risk for undernutrition who have an extremely restricted energy and/or nutrient intake or parents who espouse nonconventional diets, fads, or ideation should be asked to provide a thorough 3-day dietary record.19
The z scores and corresponding percentiles indicating growth failure (−2 and −3 SD below the mean or below the third percentile) versus those at risk for growth failure (−1 SD below the mean, or the 2.3 to 15.9 percentile). From Wikimedia Commons (https://commons.wikimedia.org/wiki/File:PR_and_NCE.gif), in the public domain; permission is not required.
Early Intervention in Primary Care
If clinical assessment identifies a child at risk for undernutrition, then intervention is indicated. In the past, supplements such as oils, starches, and high-calorie foods or drinks were used to increase energy intake. More balanced energy and nutrient supplements were reserved for moderate-to-severe growth failure, and were delivered orally, parenterally, or via gastric drip.1 However, the need for dietary intervention to support brain development along with weight and height suggests that more balanced supplementation is indicated.
Alarcon et al.21 randomized a group of 3- to 5-year-old children (n = 92) who were between the 5th and 25th percentile for body mass index (BMI) to receive either dietary counseling alone or counseling plus a complete, balanced oral nutritional supplement (ONS; 40 kcal/kg/day) for 90 days. The study showed a significant improvement of weight-for-height in the ONS group at 60 days. At 90 days, there was no further increase, indicating that daily ONS did not cause obesity in this population.
A larger (n = 200) and longer (48 weeks) study was undertaken by Huynh et al.22 with 3- to 4-year-old Filipino children who were between the 5th and 25th percentile for BMI. As in the study by Alarcon et al.,21 the control group received three sessions of dietary counseling alone, whereas the treatment group received counseling plus ONS providing 450 kcal/day. The data showed significant improvement of energy intake and weight-for-height ratio by 8 weeks. Like the study by Alarcon et al.,21 the results showed no evidence of obesity in the treatment group, even over the course of 48 weeks. Comparing pre- and post-diet diversity scores, Huynh et al.23 showed no decrement in diet quality due to prolonged ONS.23 Surprisingly, their data also showed a gradual rise in mean height-for-age among the ONS group, which did not peak until after 40 weeks of ONS therapy.22,23 This finding suggests that study children had experienced a degree of height restriction due to energy and/or nutrient inadequacy, despite being above the third percentile cut-off for growth failure.
Although clinicians understand the role of hormones in growth plate physiology, nutrition also plays a critical role.24 Undernutrition, whether due to low energy, low vitamins and minerals, or poor-quality protein, affects both the endocrine (insulin-like growth factor 1, thyroid hormone, androgens and estrogens, and glucocorticoids) and the inflammatory (cytokines) system. The findings of Huynh et al.22,23 suggest that growth plate quiescence may occur in children at-risk for undernutrition but can be subclinical. The data further suggest that clinicians must be prepared to intervene long enough to restore not only weight, but also full linear growth. Even mild but persistent quiescence of the growth plate can result in permanent stunting.25,26
Early nutrition's influence on child development extends well beyond the first years.3 Between 1969 and 1977, researchers working on behalf of the Institute of Nutrition of Central America and Panama, studied the importance of an oral protein/nutrient supplement on children with a high potential for undernutrition in rural Guatemala.27 Matched villages (n = 2 villages per group) were recruited for a group randomized trial comparing a protein/nutrient drink (119 kcal/180 mL, 10.3 g of protein, 15.3 g of carbohydrates, and 0.2 g of fats, plus iron, vitamins A and C, calcium, phosphorus, thiamin, riboflavin, and niacin) with a carbohydrate drink (59 kcal/180 mL, 13.3 g of carbohydrates, no fat, no protein, and the same vitamin mineral supplementation). All pregnant women and children from birth to age 7 years were free to consume ad libitum the drink assigned to their village, which was available at multiple sites. Study results were surprising. In the ONS group, infant mortality fell by 66% and stunting by 45% compared to the group given only a carbohydrate drink. Maternal fat-free mass rose by 0.5 SD. In adolescence, children who were given the supplement showed greater height, weight, and fat-free mass, demonstrating a higher (0.7 SD) work capacity. More importantly, the study showed greatly improved cognitive performance and precortical executive function, which resulted in higher test scores and a concomitant increase in years of schooling completed.27
New research is changing the way pediatricians view the importance of nutrition's role in optimal infant and child development. More than simply fuel for growth, nutrition is vital for continued post-natal organ development, including the gastrointestinal tract, the immune system, and most importantly, the brain. Even before signs of growth faltering, undernutrition threatens optimal development. Using a simple approach (Table 2), the primary care clinician can assess the at-risk child, identify potential nutritional problems, and intervene effectively even before the child shows signs of overt growth failure. Primary care intervention is ideal when it uses balanced supplementation, supportive behavioral counseling, and close follow-up.
A Primary Care Approach to Parental Concerns about Child Nutrition
- Cole SZ, Lanham JS. Failure to thrive: an update. Am Fam Physician. 2011;83:829–834.
- Lenters L, Wazny K, Bhutta ZA. Management of severe and moderate acute malnutrition in children. In: Black RE, Laxminarayan R, Temmerman M, , eds. Reproductive, Maternal, Newborn, and Child Health: Disease Control Priorities. 3rd ed. Washington, DC: The World Bank; 2016.
- Hoddinott J, Behrman JR, Maluccio JA, et al. Adult consequences of growth failure in early childhood. Am J Clin Nutr. 2013;98:1170–1178. doi:. doi:10.3945/ajcn.113.064584 [CrossRef]
- Wright CM. Identification and management of failure to thrive: a community perspective. Arch Dis Child. 2000;82:5–9. doi:. doi:10.1136/adc.82.1.5 [CrossRef]
- Mehta NM, Corkins MR, Lyman B, et al. Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions. JPEN J Parenter Enteral Nutr. 2013;37(4):460–481. doi:. doi:10.1177/0148607113479972 [CrossRef]
- Becker P, Carney LN, Corkins MR, et al. Academy of Nutrition and DieteticsAmerican Society for Parenteral and Enteral Nutrition. Consensus statement of the Academy of Nutrition and Dietetics/American Society for Parenteral and Enteral Nutrition: indicators recommended for the identification and documentation of pediatric malnutrition (undernutrition). Nutr Clin Pract. 2015;30:147–161. doi:. doi:10.1177/0884533614557642 [CrossRef]
- Son'kin V, Tambovtseva R. Energy metabolism in children and adolescents. In: Clark K, ed. Bioenergetics. London, UK: Intech Press; 2012:121–142.
- Gould JF. Complementary feeding, micronutrients, and developmental outcomes of children. Nestle Nutr Inst Workshop Ser. 2017;87:13–28. doi:. doi:10.1159/000448934 [CrossRef]
- Nyaradi A, Oddy WH, Hickling S, Li J, Foster JK. The relationship between nutrition in infancy and cognitive performance during adolescence. Front Nutr. 2015;2:2. doi:. doi:10.3389/fnut.2015.00002 [CrossRef]
- Birch LL, Doub AE. Learning to eat: birth to age 2 years. Am J Clin Nutr. 2014;99(3):723s–728s. doi:. doi:10.3945/ajcn.113.069047 [CrossRef]
- Nyaradi A, Li J, Hickling S, Foster J, Oddy WH. The role of nutrition in children's neurocognitive development, from pregnancy through childhood. Front Hum Neruosci. 2013;7:97. doi:10.3389/fnhum.2013.00097 [CrossRef].
- Guerrant RL, DeBoer MD, Moore SR, Scharf RJ, Lima AAM. The impoverished gut—a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenerol Hepatol. 2013;10:220–229. doi:. doi:10.1038/nrgastro.2012.239 [CrossRef]
- Davis EC, Wang M, Donovan SM. The role of early life nutrition in the establishment of gastrointestinal microbial composition and function. Gut Microbes. 2017;8:143–171. doi:. doi:10.1080/19490976.2016.1278104 [CrossRef]
- Gitterman BA, Chilton LA, Cotton WH, et al. Council on Community Pediatrics; Committee On Nutrition. Promoting food security for all children. Pediatrics. 2015;136(5):1431–1438. doi:. doi:10.1542/peds.2015-3301 [CrossRef]
- Food Research and Action Center, American Academy of Pediatrics. Addressing food insecurity: a toolkit for pediatricians. http://frac.org/aaptoolkit. Accessed October 16, 2018.
- Taylor CM, Wernimont SM, Northstone K, Emmett PM. Picky/fussy eating in children: review of definitions, assessment, prevalence, and dietary intakes. Appetite. 2015;95:349–359. doi:. doi:10.1016/j.appet.2015.07.026 [CrossRef]
- Emmett PM, Jones LR. Diet, growth, and obesity development throughout childhood in the Avon Longitudinal Study of Parents and Children. Nutr Rev. 2015;73(suppl 3):175–206. doi:. doi:10.1093/nutrit/nuv054 [CrossRef]
- Ramos-Paul R, Marriage BJ, Debeza RR, et al. Impact of picky eating on level of family stress in healthy children between the ages of 3 and 6 years. The Open Nutr J. 2014;8:13–18. doi:. doi:10.2174/1874288201408010013 [CrossRef]
- Kerzner B, Milano K, MacLean WC, Berall G, Stuart S, Chatoor I. A practical approach to classifying and managing feeding difficulties. Pediatrics. 2015;135:344–353. doi:. doi:10.1542/peds.2014-1630 [CrossRef]
- Taylor CM, Northstone K, Wernimont SM, Emmett PM. Macro- and micronutrient intakes in picky eaters: a cause for concern?Am J Clin Nutr. 2016;104:1647–1656. doi:. doi:10.3945/ajcn.116.137356 [CrossRef]
- Alarcon PA, Lin LH, Noche M, et al. Effect of oral supplementation on catch-up growth in picky eaters. Clin Pediatr. 2003;42:209–217. doi:. doi:10.1177/000992280304200304 [CrossRef]
- Huynh DT, Estorninos E, Capeding RZ, Oliver JS, Low YL, Rosales FJ. Longitudinal growth and health outcomes in nutritionally at-risk children who received long-term nutritional intervention. J Hum Nutr Diet. 2015;28(6):623–635. doi:. doi:10.1111/jhn.12306 [CrossRef]
- Huynh DT, Estorninos E, Capeding MR, Oliver JS, Low YL, Rosales FJ. Impact of long-term use of oral nutritional supplement on nutritional adequacy, dietary diversity, food intake and growth of Filipino preschool children. Nutr Sci. 2016;5:e20. doi:. doi:10.1017/jns.2016.6 [CrossRef]
- Millward DJ. Nutrition, infection, and stunting: the roles of deficiencies of individual nutrients and foods, and of inflammation, as determinants of reduced linear growth of children. Nutr Res Rev. 2017;30:50–72. doi:. doi:10.1017/S0954422416000238 [CrossRef]
- Fazeli PK, Klibanski A. Determinants of growth hormone resistance in malnutrition. J Endocrinol. 2014;220(3):R57–R65. doi:. doi:10.1530/JOE-13-0477 [CrossRef]
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Red Flags Indicating Potential Risk of Malnourishment or Growth Failure
Infants born prematurely
Difficulty advancing foods
Children who are hospitalized
Chronic disease states
Children with special needs
First months of life
Single parent with inadequate social support
A Primary Care Approach to Parental Concerns about Child Nutrition
Plot growth: identify a fall of z score of greater than −1 SD for weight-for-height or BMI-for-age
Look for red flags in the medical history
Use the two-question screen for food insecurity
Do a verbal diet history and assess parent-child problems
Do a 3-day diet record of all foods and drinks (2 weekdays, 1 weekend day)
Consider referral to a dietitian for intensive dietary counseling
Intervene using a balanced oral energy and nutrient supplement
Ensure complete reestablishment of weight and height status
Observe the family closely