Growth Faltering: Underweight and Stunting

Author(s):
Andrew M. Prentice

The great majority of attention on growth faltering concentrates on the first “1,000 days” of life with a much lesser focus on toddlers and young preschoolers. The rationale for this is understandable since the first 1,000 days cover the period of most rapid growth and changes in body composition, the period of breastfeeding, and the complex transition from breastfeeding and weaning to complementary feeds, and then shifting
to the family/adult diet. There has also been a strong perception that once a child has become stunted or wasted in the first 2 years of life, there is little hope of recovery – an assumption we address below.

Global Distribution of Stunting, Wasting, and Underweight It is self-evident that, with the exception of certain rare clinical conditions or inappropriate parenting behaviors, stunting, wasting, and the consequent underweight are largely confined to the poorer populations of low-income countries. As countries emerge from poverty and pass
through the economic transition, malnutrition rates fall sharply and soon resemble those in first-world nations (Fig. 1); a corollary is that obesity rates rise rapidly as will be discussed elsewhere in this symposium.

Timing of the Development of Stunting and Wasting There are 3 critical periods in the development of stunting. The first relates to the generations before a child is even conceived. There is clear evidence for generational influences on population height. Intergenerational influences can be mediated through a mother’s small body size that
can impart effects through numerous possible mechanisms such as uterine constraints. Much less certain is whether there can be so-called transgenerational effects (i.e., effects not mediated by the direct influence of a mother’s diet or body size).
Transgenerational effects would require some



Fig. 1. Childhood stunting is predominantly a problem of low-income countries and resolves rapidly with economic advancement. Data compiled from Demographic Health Surveys since 2005. GDP, gross domestic product; PPP, purchasing power parity.

method (e.g., epigenetic programming marks that survive erasure in the very early embryo) that would convey a signal that would effect stunting; we have some evidence that this can occur [1], but much more research is needed. The second critical period is in utero, and it has been shown that a substantial proportion of childhood stunting and wasting has its origins during fetal life. The third critical window is in the early postnatal period.

Recent evidence from our own very detailed studies of growth trajectories suggests that the channels that will steer later growth are established surprisingly early in postnatal life. Can Toddlers and Young Preschoolers Recover from Stunting and Wasting? In most poor communities from low- and middle-income countries, there is a precipitous drop-off in average height-for-age Z-scores compared to the WHO growth reference. This seems to be caused, in large part, by exposure to infections and highly unhygienic living conditions.



Fig. 2. Toddlers and young preschoolers show slight height catchup following severe faltering in the first 2 years of life (modified from Prentice et al. [3] with permission).

Analysis of aggregate data from many such countries suggests that there is little evidence for a later recovery [2]. However, our own very detailed studies of poor rural Gambian children show that they achieve catchup of almost 1 Z-score between 2 and 5 years of age (Fig. 2). We interpret this as due to the fact that their immune systems have finally developed a resilience against all the prevalent infections. We have also emphasized that there can be a second period of catchup in adolescence [3]. Diets for Toddlers and Young Preschoolers in Low-Income Countries In developed countries, there are many foods designed to meet the energy and nutrient needs of growing and active toddlers; such foods are rarely available in very poor populations, and toddlers usually join the family food bowl and share the adult diet. The implications of this for
growth will be examined.

References
1. Eriksen KG, Radford EJ, Silver MJ, et al: Influence of intergenerational in utero parental energy and nutrient restriction on offspring growth in rural Gambia. FASEB
J 2017;31:4928–4934.
2. Victora CG, de Onis M, Hallal PC, et al: Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 2010;125:e473–e480.
3. Prentice AM, Ward KA, Goldberg GR, et al: Critical windows for nutritional interventions against stunting. Am J Clin Nutr 2013;97:911–918.

 

 

Abstract

The great majority of attention on growth faltering concentrates on the first “1,000 days”
with a much lesser focus on toddlers and young preschoolers. The rationale for this is understandable since the first 1,000 days cover the period of most rapid growth and changes in body composition, the period of breastfeeding, and the complex transition from breastfeeding and weaning to complementary feeds, and then moving to the family/adult diet. There has also been a strong perception that, once a child has become stunted or wasted in the first 2 years of life, there is little hope of recovery, an assumption we address below. This paper will describe the timing of the development of stunting and wasting, addressing 3 critical periods: intergenerational, in utero, and early postnatal life. The question of whether toddlers and young preschoolers can recover from stunting and wasting will also be addressed; our own studies suggest that a degree of recovery is certainly possible. The hormonal mechanisms regulating early growth will be examined. Finally, the issue of whether toddlers and young preschoolers should have special foods and diets will also be discussed.

Introduction

The great majority of attention on growth faltering concentrates on the first “1,000 days” with a much lesser focus on toddlers and young preschoolers. The rationale for this is understandable: the first 1,000 days cover the period of most 

 rapid growth and developmental changes in body composition (especially with respect to brain growth); it is the period of breastfeeding and of the complex transition from breastfeeding as the child is weaned onto complementary feeds; and in the second year of postnatal life, the child starts to adopt the family/adult diet. There has also been a strong perception that once a child has become stunted or wasted in the first 2 years of life, there is little hope of recovery [1] – an assumption we address below.
 

Global Distribution of Stunting, Wasting, and Underweight in Toddlers and Young Preschoolers

It is self-evident that, with the exception of certain rare clinical conditions or inappropriate parenting behaviors, stunting, wasting, and the consequent underweight are largely confined to the poorer populations of low-income countries. As some of these countries emerge from poverty and pass through the economic transition, malnutrition rates fall sharply and soon resemble those in first-world nations ( Fig. 1 ); a corollary is that obesity rates rise rapidly as will be discussed elsewhere in this symposium [2]. In 2012, the World Health Organization (WHO) estimated that there were 162 million stunted children worldwide and established a “Comprehensive Implementation Plan on Maternal, Infant, and Young Child Nutrition” that set one of the “Global Nutrition Targets” to reduce this number by 40% by the year 2025 [3]. Two-fifths of these children are in the toddler and preschooler age group (defined as 2–5 years for the purposes of this paper), and because there is only limited scope for recovering
growth deficits during this period, the greater emphasis on interventions must be placed on earlier periods, as discussed below.
 

Timing of the Development of Stunting and Wasting

There are 3 critical periods in the development of stunting. The first of these relates to the generations before a child is even conceived. There is clear evidence for intergenerational influences on population height, and it usually takes a number of generations for these influences to wash out as populations move to conditions of improved diets and living conditions [4]. In this field, there is a subtle but important terminological distinction between intergenerational influences and transgenerational influences [5]. The former can be mediated through a mother’s small body size which can impart effects through numerous possible mechanisms such as “uterine constraints.” The evidence for these effects is robust. To take a single example, Young et al. [6] described the relationship between the preconception maternal nutritional status and stunting at 2 years of age in the PRECONCEPT study in Vietnam. A height < 150 cm was associated with an incident risk ratio of 1.85 and a weight of < 43 kg with a risk of 1.35 for stunting at 2 years [6].

Much less certain is whether there can be transgenerational effects in humans. Such effects would not be mediated by the direct influence of a mother’s diet or body size. Transgenerational effects would therefore require some method (e.g., epigenetic programming marks that survive erasure in the very early embryo) that would convey a signal that would affect stunting; we have some evidence that this can occur [7], but much more research is needed. The second critical period is in utero, and it has been shown that a substantial proportion of childhood stunting and wasting has its origins in fetal life, especially in the last trimester of pregnancy when growth rates are proportionately faster than at any other period of life. A meta-analysis of data from 19 studies in low- and middle-income countries has shown that, relative to appropriate-for gestational- age and term babies, the risks of stunting in the age range from 12 to 60 months is 1.93 for appropriate-for-gestational-age but preterm babies, 2.43 for small-for-gestational-age and term babies, and 4.51 for small-for-gestational- age and preterm babies [8].

The third critical window is in the early postnatal period. Child growth is under hormonal control, and there are 3 recognized growth stages: fetal, infant, and child (and later adolescence) growth [9]. Fetal growth is largely driven by insulin (produced by the fetal pancreas). Infant growth is driven by insulin and IGF1 independently of growth hormone regulation. Then there is a transition, the so-called infant-to-child transition (ICT), as growth hormone starts to exert its control on the pace of growth; this is the period relevant to toddlers’ and young preschoolers’ growth, and delayed ICT is a recognized clinical syndrome [10]. Karlberg [9], the original proponent of ICT, hypothesized that poor growth of children in low-income settings may be due to a delayed ICT. In fact, our latest research suggests that, at least in the rural Gambian children whom we study,
there is evidence for advanced ICT which may be problematic in prematurely terminating the fetal-infant period of rapid growth [11]. Additional evidence from our own very detailed studies of growth trajectories suggests that the “channels” that will steer later growth are established surprisingly early in postnatal life [Bernstein et al., in preparation].
 

Can Toddlers and Young Preschoolers Recover from Stunting and Wasting?

In most poor communities from low- and middle-income countries, there is a precipitous drop-off in average height-for-age Z-scores compared to the WHO growth reference. This seems to be caused, in large part, by exposure to infections and highly unhygienic living conditions leading to high levels of morbidity that can impair growth through a number of pathways especially involving a persistently damaged gut mucosa [12]. Analysis of aggregate data from many such countries suggests that there is little evidence for a later recovery (see Victora et al. [1]). However, our own decades-long studies of poor rural Gambian children show that they achieve a catchup of almost 1 Z-score between 2 and 5 years of age (Fig. 2). There is a remarkable switch from a
negative growth trajectory of about –1 height-for-age Z-score per year in the first 2 years of life to a positive trajectory of about +0.2 Z-scores in the next 3 years. We interpret this as due to the fact that their immune systems have finally developed a resilience against the great majority of the most prevalent infections. We have also emphasized that there can be a second period of catchup in adolescence [13].

Nutrient Needs of Toddlers and Young Preschoolers

Human toddlers and preschoolers grow very slowly compared to the young of other species; this is an evolved mechanism assumed to have been designed primarily to allow plenty of time for the development, wiring, and training of a large and complex brain [14] . A consequence of this slow growth is that the nutrient requirements for deposition of new tissue are low. In early infancy (0–3 months), babies accrue about 2.5 g protein and 19 g fat per day with an energy cost of around 25 kJ/g [15] . The protein requirements required for this slow growth are low. In the first 6 months of life, a baby is estimated to deposit 0.46 g/kg/day of protein in new tissue growth and have a maintenance need of 0.66 g/kg/day giving a total requirement of 1.12 g/kg/day [16] . By 2 years of age, the estimated need for tissue deposition has fallen to 0.13 g/kg/day and by 4 years of age to just 0.03 g/kg/day giving total estimated protein needs of 0.79
and 0.69 g/kg/day.

In terms of energy, the overall estimated requirements are about 430 kJ/kg/ day in the first few months of life. By 2–3 years of age, the estimated energy needs have fallen to about 340 kJ/kg/day, and by 4–5 years they have declined further to about 315 kJ/kg/day. The requirements for basic metabolic needs would be lower but for 2 reasons: (a) due to the costs of ambulation and spontaneous physical activity in naturally active young children and (b) because the brain develops a high requirement for glucose [17] . The requirements for other nutrients are also relatively modest at this period of life as a consequence of the low growth rates; these are summarized else-
where in this volume [18].
 

Do Toddlers and Young Preschoolers Require Special Diets?

In developed countries, there are many foods designed to meet the energy and nutrient needs of growing and active toddlers, but such foods are not necessary in enabling this age group to meet their nutrient needs, and the health and nutrition agencies of most advanced countries provide ample advice to parents.

Such advice generally centers on the provision of a wide variety of nutrient dense
foods with plenty of whole grains, fresh fruits, and vegetables, and ensuring rich sources of iron and calcium. Such recommendations also counsel against giving in to children’s requests for “junk foods” – but frequently in vain. Surveys such as FITS (Feeding Infants and Toddlers Studies) [19] demonstrate that the great majority of young children are not receiving the ideal “healthy” diet in the USA for instance. In low- and middle-income countries, toddlers and young children usually join the “family food bowl” and share the adult diet. This means that they have low access to a nutrient-enriched diet best suited to the additional needs of growth and activity; however, on the other hand, they have lower exposure to “junk” foods unless and until they transition to more affluent urban settings.
 

Nutrition-Sensitive Actions and Interventions to Improve the Growth and Development of Toddlers and Young Preschoolers

It is crucial to understand that nutrition interventions alone cannot act as a panacea
to eliminate the many constraints on healthy growth and intellectual development
of young children, especially those in low- and middle-income countries. We have described elsewhere the profound effects of living in a poor and unhygienic environment [12], and have emphasized that there is a very high hygiene threshold that must be overcome before children will grow normally [20]. These effects are mediated by persistent infections and gut damage (so called environmental enteric disease) and low-grade inflammation leading to nutrient malabsorption and wastage. The importance of a healthy psychosocial environment also cannot be overemphasized and has close linkage with stunting and wasting. Numerous studies have demonstrated that the adverse effects of early childhood malnutrition on cognition, behavioral issues, and the development of human capital can, at least in part, be ameliorated by combining interventions to promote psychosocial stimulation alongside improved nutrition [21–24].

Conflict of Interest Statement
The author received an honorarium from the Nestlé Nutrition Institute (NNI) in respect
of attending this conference and preparing this paper. The author is a member of the
NNI Board.

References
1. Victora CG, de Onis M, Hallal PC, et al: Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 2010; 125:e473–e480.
2. Singhal A: Obesity in toddlers and young children: causes and consequences; in Black M, Singhal A, Hillman C (eds): Building Future Health and Well-Being of Thriving Toddlers and Young Children. Nestlé Nutr Inst Workshop Ser. Basel, Karger, vol 95, DOI: 10.1159/000511510.
3. World Health Organization: Global Nutrition Targets 2025: Stunting Policy Brief (WHO/NMH/ NHD/14.3). Geneva, WHO, 2014.
4. NCD Risk Factor Collaboration (NCD-RisC): A century of trends in adult human height. eLife 2016; 5:e13410.
5. Silver MJ: Intergenerational influences on child development: an epigenetic perspective; in Michaelsen KF, Neufeld LM, Prentice AM (eds): Global Landscape of Nutrition Challenges in Infants and Children. Nestlé Nutr Inst Workshop Ser. Basel, Karger, 2020, vol 93, pp 145–152.
6. Young MF, Nguyen PH, Gonzalez Casanova I, et al: Role of maternal preconception nutrition on offspring growth and risk of stunting across the first 1,000 days in Vietnam: a prospective cohort study. PLoS One 2018; 13:e0203201.
7. Eriksen KG, Radford EJ, Silver MJ, et al: Influence of intergenerational in utero parental energy and nutrient restriction on offspring growth in rural Gambia. FASEB J 2017; 31: 4928–4934.
8. Christian P, Lee SE, Donahue Angel M, et al: Risk of childhood undernutrition related to small-for gestational age and preterm birth in low- and middle-income countries. Int J Epidemiol 2013; 42: 1340–1355.
9. Karlberg J: On the modelling of human growth. Stat Med 1987; 6: 185–192.
10. Hochberg Z, Albertsson-Wikland K: Evo-devo of infantile and childhood growth. Pediatr Res 2008; 64: 2–7.
11. Bernstein RM, O’Connor GK, Vance EA, et al: Timing of the infancy-childhood transition in rural Gambia. Front Endocrinol (Lausanne) 2020; 11: 142.
12. Prentice AM: Environmental and physiological barriers to child growth and development; in Michaelsen KF, Neufeld LM, Prentice AM (eds): Global Landscape of Nutrition Challenges in Infants and Children. Nestlé Nutr Inst Workshop Ser. Basel, Karger, 2020, vol 93, pp 125–132.
13. Prentice AM, Ward KA, Goldberg GR, et al: Critical windows for nutritional interventions against stunting. Am J Clin Nutr 2013; 97: 911–918.
14. Gould SJ: Ontogeny and Phylogeny. Cambridge, Harvard University Press, 1977.
15. FAO/WHO/UNU: Protein and Amino Acid Requirements in Human Nutrition: Report of a Joint FAO/WHO/UNU Expert Consultation. WHO Technical Report Series, No. 935. Geneva, WHO, 2002.
16. FAO/WHO/UNU; Human Energy Requirements: Report of a Joint FAO/WHO/UNU Expert Consultation. FAO Food and Nutrition Technical Support Series 1. Geneva, WHO, 2001.
17. Kuzawa CW, Chugani HT, Grossman LI, et al: Metabolic costs and evolutionary implications of human brain development. Proc Natl Acad Sci USA 2014; 111: 13010–13015.
18. Abrams SA: Selected micronutrient needs of children 1–3 years of age; in Black M, Singhal A, Hillman C (eds): Building Future Health and Well- Being of Thriving Toddlers and Young Children. Nestlé Nutrition Institute Workshop. Basel, Karger, vol 95, DOI: 10.1159/000511507.
19. Duffy EW, Kay MC, Jacquier E, et al: Trends in food consumption patterns of US infants and toddlers from Feeding Infants and Toddlers Studies (FITS) in 2002, 2008, 2016. Nutrients 2019; 11: 2807.
20. Husseini M, Darboe MK, Moore SE, et al: Thresholds of socio-economic and environmental conditions necessary to escape from childhood malnutrition: a natural experiment in rural Gambia. BMC Med 2018; 16: 199.
21. Nahar B, Hossain MI, Hamadani JD, et al: Effects of psychosocial stimulation on improving home environment and child-rearing practices: results from a community-based trial among severely malnourished children in Bangladesh. BMC Public
Health 2012; 12: 622.
22. Perkins JM, Kim R, Krishna A, et al: Understanding the association between stunting and child development in low- and middle-income countries: next steps for research and intervention. Soc Sci Med 2017; 193: 101–109.
23. Walker SP, Wachs TD, Gardner JM, et al; International Child Development Steering Group: Child development: risk factors for adverse outcomes in developing countries. Lancet 2007; 369: 145–157.
24. Walker SP, Wachs TD, Grantham-McGregor S, et al: Inequality in early childhood: risk and protective factors for early child development. Lancet 2011; 378: 1325–1338