School age

Narrative Review
Nutrition in school-age children: a rationale for revisiting

priorities
Jose M. Saavedra and Andrew M. Prentice
.
Middle childhood and early adolescence have received disproportionately low levels
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of scientific attention relative to other life stages, especially as related to nutrition
and health. This is partly due to the justified emphasis on the first 1000 days of life,
and the idea that early deficits and consequences may not be fully reversible. In
addition, these stages of life may superficially appear less “eventful” than infancy or
late adolescence. Finally, there has been historical ambiguity and inconsistency in
terminology, depending on whether viewing “childhood” through physiologic,
social, legal, or other lenses. Nevertheless, this age bracket, which encompasses
most of the primary education and basic schooling years for most individuals, is
marked by significant changes, inflection points, and sexually driven divergence in
somatic and brain growth and development trajectories. These constitute transfor-
mative changes, and thus middle childhood and early adolescence represents a
major and last opportunity to influence long-term health and productivity. This
review highlights the specificities of growth and development in school age, with a
focus on middle childhood and early adolescence (5 years–15 years of age, for the
purposes of this review), the role of nutrition, the short- and long-term consequences
of inadequate nutrition, and the current global status of nutrition in this age group.
Adequate attention and emphasis on nutrition in the school-age years is critical: (a)
for maintaining an adequate course of somatic and cognitive development, (b) for
taking advantage of this last major opportunity to correct deficits of undernutrition
and “catch-up” to normal life course development, and (c) for addressing the nutri-
tional inadequacies and mitigating the longer-term consequences of overnutrition.
This review summarizes and provides a rationale for prioritizing nutrition in school-
age children, and for the need to revisit priorities and focus on this part of the life
cycle to maximize individuals’ potential and their contribution to society.
Affiliation: J.M. Saavedra is with the Division of Gastroenterology and Nutrition, Johns Hopkins University School of Medicine, Baltimore,
USA. A.M. Prentice is with the MRC Unit, The Gambia and MRC International Nutrition Group, London School of Hygiene & Tropical
Medicine, London, UK
Correspondence: J.M. Saavedra, Department of Pediatrics, Johns Hopkins University School of Medicine, 600 North Wolfe Street, Baltimore,
MD 21212, USA. E-mail: [email protected]
Key words: adolescence, children, growth, malnutrition, middle childhood, nutrition, obesity, school age, stunting
C The Author(s) 2022. Published by Oxford University Press on behalf of the International Life Sciences Institute.
V
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://
creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium,
provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please
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https://doi.org/10.1093/nutrit/nuac089
Nutrition ReviewsV Vol. 81(7):823–843
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INTRODUCTION To achieve this aim, a comprehensive review of the
literature was conducted, using PubMed to identify eli-
The last three decades of academic and public health gible and relevant publications through 2021. Papers
efforts have enthusiastically embraced the importance were identified by combining the following Medical
of early life nutrition as a foundational component of Subject Heading keywords: children, school age, middle
lifelong health. The gestational period through the first childhood, adolescence, nutrition, nutrients, growth,
2 years of age (the first 1000 d) and early childhood development (multiple aspects/organ systems), malnu-
through 5 years of age have received justified attention trition, stunting, overweight, and obesity. Literature was
over the last few decades. However, the ultimate realiza- selected and prioritized that included information and
tion of an individual’s potential requires a successful data for the 5–15-year age group, primarily based on
bridging from early childhood to adulthood. The subse- population, cohort, or epidemiologic studies and

quent periods in the life cycle—5 years to 9 years of age, reviews, as well as literature addressing biologic aspects
referred to as “middle childhood,” and 10 years– of specific areas of growth and development for this age
15 years, “early adolescence”—are commonly encom- group, with a focus on somatic growth, body composi-
passed in the “school years.” tion, and neurologic development. Nutrition- and diet-
Middle childhood and early adolescence bridge the related behavioral, psychologic, or social aspects were
period between the relatively steady growth occurring not included in the scope of this review.
from 2 years to 5 years of age and the final maturation
period of late adolescence to adulthood. This period is SCHOOL-AGE HEALTH AND NUTRITION TERMINOLOGY
characterized by multiple dramatic inflection points in AND KNOWLEDGE GAPS
the course of growth and development, as well as behav-
ioral and psychosocial events occurring around the Compared with the nutrition and health research litera-
arrival of puberty. These inflections represent transfor- ture for other life stages, there is a historical neglect of
mational changes in the brain and cognitive processing, middle childhood and adolescence. Estimates of the
linear bone growth and bone mineralization, body com- published literature describing child health (PubMed
sources 2005–2016) show 95.3% of this literature is
position, and other organ systems. It is also during this
dedicated to early childhood (<5 y), 3.5% to 5 years–
period that major sex-driven inflections and divergen-
9 years, 0.55% to 10 years–14 years, and 0.61% to
ces occur in growth and development. The nutrition of
15 years–19 years.6 The health and nutritional status of
children during this period is critical for supporting
school-age children, particularly that during middle
these changes. In addition, can help overcome early def-
childhood, remains the least studied of all life stages.
icits, and may help correct dietary excesses that have
Public databases of most agencies track rates of
been occurring since infancy. Thus, school age consti-
malnutrition, stunting, and other health markers for
tutes a final major window of opportunity to influence
children, but usually do so only until 5 years of age, and
growth and development, and the associated health only pick up again during adolescence or adulthood.7
consequences in mature life. Regional or international databases of nutritional data
Unfortunately, relative to other life stages, school- for middle childhood (5 y–10 y of age) are extremely
age nutrition has received a disproportionately low level scarce. Many reviews for this age group rely on extrapo-
of scientific attention, in part due to a misleading but lations, eg, using Demographic and Health Surveys
widespread perception that early deficits in growth and (DHS) data for children 4 years–5 years of age8 or
development cannot be rectified. In the last few years, including data of 10-year-olds to 14-year-olds within
scientific, public health, and other academic voices have child surveys.9 On the other end of school age, most
been calling attention to this life stage as a critical and research and data for children 10 years–15 years (early
potentially last major window of opportunity for inter- adolescence) is sometimes conflated with the data of
vention in maximizing the potential of individuals as adults, eg, Multiple Indicator Cluster Surveys (MICS)
productive members of society.1–5 and DHS data for females 15 years–19 years. As dis-
This aim of this review was to highlight the critical cussed below, research, particularly concerning child
growth, developmental, and nutritional aspects of these growth and cognition, led to the notion that the conse-
transformative school-age years, and the challenges and quences of nutritional and environmental insults in the
gaps in knowledge around these, and to provide argu- first 2 years of age were irreversible. This may have
ments for why nutrition during school age deserves resulted in reduced interest and research bias, due to
greater and more focused attention to maximize indi- underestimating the significant potential for growth
viduals’ growth, development, and ultimate and developmental catch-up possible during middle
productivity. childhood and adolescence.
824 Nutrition ReviewsV Vol. 81(7):823–843

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In part, inadequate research in this age group is between 5 years and 14 years of age, and there tends to
also due to ambiguity, inconsistency, and overlapping be late entry into school in low- and middle-income
terminology, resulting from viewing this age group countries. Many consider that “high school” and
through different lenses: physiologic, reproductive, “preparatory school” fall into this category; others do
social, legal, or school system, etc. Terms such as “early not. Schooling provides opportunities for promoting
childhood,” “middle childhood,” “late childhood,” nutrition and health. Research and interventions can
“school age”, “adolescence,” and “young adulthood” leverage society’s investment in education and take
often overlap. From the general physiologic point of advantage of the potential synergy between health and
view, “middle childhood” (ages 5 y–9 y) is a period of education investments.1 Figure 1 summarizes the termi-
growth and consolidation, followed by an adolescent nology most commonly used for childhood growth and
growth spurt (ages 10 y–14 y), each associated with spe- developmental stages. Acknowledging there is no per-

cific behavioral changes, before a final growth consoli- fect life-stage categorization, given the physiologic and
dation (ages 15 y to early 20s), and subsequent growth changes, most agree that data should be disag-
maturation into adulthood.1 More broadly speaking, gregated for 5 years–9 years (middle childhood),
the developmental stages in the life cycle have been clas- 10 years–14 years (early adolescence), 15 years–20 years
sified into 3 main categories: physical growth, cognitive (late adolescence), and 20 years–24 years (older adoles-
development, and socioemotional/psychosocial devel- cents or young adults).1,9 ”School age” defined as com-
opment.10 And while interdependent, the rate of prog- prising “middle childhood” (5 y–9 y) and “early
ress for each of these life-stage categories can vary adolescence” (10 y–15 y) will be the age group of focus
individually, making it hard to propose a purely chro- and the terminology used in this paper.
nological or age-based approach.
Many organizations and legal systems define SPECIFICITIES OF GROWTH AND DEVELOPMENT IN
“child” as an individual 0 years–18 years.8,11 WHO SCHOOL AGE
defines an “adolescent” as aged 10 years to 19 years,
“youth” in general as 15 years–24 years, and “young What makes school age of particular significance nutri-
people” covers 10 years–24 years.2,12 More recently, a tionally is that it encompasses numerous changes in tra-
broader definition for “adolescence” has been advocated jectory from the relatively steady growth of the
as including the entire 10-year-old to 24-year-old group preschool child, through sex differentiation, and into
within the term. As explained by the 2016 Lancet the final consolidation period of late adolescence. These
Commission on Adolescent Health and elsewhere,9,12 changes are driven by pubertal onset and course, with
this would support consideration of appropriate social population variations primarily dependent on genetic,
and economic policies, service systems, and legal frame- environmental, and nutritional factors. Pubertal sex
works for this broad age group. While useful for certain hormone secretion will also determine changes in
objectives, this approach fails to distinguish the signifi- growth rate and growth termination. However, much
cant differences between the transitional aspects of work still remains to be done in understanding the
development (and therefore the distinct difference in underlying genetics, the timing of puberty (including
needs) of early adolescence versus late adolescence. early-life determining factors), growth variability during
Others support the use of “young people” (not puberty, and adiposity and weight gain.14
“adolescents”) as a term for all 10–24-year-olds, distin- Two specific processes contribute to the sex-
guishing “adolescents” (10 y–19 y) from “young adults” differentiating physical developmental changes during
or “emerging adults” (20 y–24 y). And some suggest that this period: adrenarche and gonadarche. Adrenarche
considering people in their early 20s as adolescents occurs between 6 years and 8 years of age, earlier in girls
could lead to underestimating their competencies and and later in boys, and refers to the maturation of the
capabilities.13 Clearly, no definition should be rigid. adrenal cortex and increased secretion of adrenal
Approaches to defining “school age” and “adolescence” androgens, namely dehydroepiandrosterone. It is
can vary by setting and should consider the cultural and involved in the development of pubic hair (pubarche),
societal context. body odor, skin oiliness, and axillary hair. Gonadarche
Schools are a significant platform, not always is initiated by specialized neurons of the hypothalamus
adequately utilized, for delivering nutrition as well as that secrete gonadotropin-releasing hormone (GnRH)
education in nutrition. “Schooling” plays a role as a in a cyclical pattern that regulates the release of follicle-
defining factor in a person’s development, includes stimulating hormone (FSH) and luteinizing hormone
what is generally called “primary” and “secondary” (LH) by the anterior pituitary, leading to gonadarche,
schooling, and is quite variable from country to coun- starting at around 9 years–10 years of age in girls, and
try. Globally, most children in primary school are around 10 years–12 years in boys. In girls, FSH

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Figure 1 Major developmental life stages (in gray) and commonly used terminology for specific developmental stages as related to
age. Modified and adapted from Bundy et al 20171 and Sawyer et al 20189
stimulates estrogen production, follicle formation, and Increases in height and BMI are associated with an ear-
eventually ovulation and menarche. In boys, LH stimu- lier onset of puberty, and earlier puberty is associated
lates testosterone production and eventually maturation with an increased rate of later obesity.14 Obesity, which
of spermatozoa. has risen dramatically in children, is associated with a
Finally, these changes during middle childhood shift towards earlier onset of puberty, particularly in
and early adolescence are directly related to a differenti- girls; the situation is less clear in boys.16
ated phase of social learning and experimentation, her- The course of sex hormone secretion will deter-
alding shifts in cognition, motivation, and social mine the termination of growth during late adolescence
behavior, with significant implications for the ultimate into adulthood. The pubertal process is usually com-
development of each child’s personality. These shifts plete 2 years to 4 years after physical changes begin to
encompass major domains such as the development of occur. However, physical maturation will continue into
independence and decision-making, acquisition of cul- the third decade of life. For instance, bone and brain
tural norms, increase in complex moral reasoning, development continues into the 20 s. Hormonal differ-
increase in understanding of social hierarchies, increase ences during puberty will also affect the size and func-
in sense of gender identity, gender segregation, and tion of organ systems related to aerobic and anaerobic
romantic attraction, as well as changes in food preferen- physical fitness. Heart size and cardiac function, lung
ces and dietary habits, the expansion of which are size, bone development, muscle volume and strength,
beyond the scope of this paper.15 erythropoiesis, and substrate utilization will diverge and
These growth and change phenomena and influen- determine different ultimate fitness and strength
levels.18
tial factors are interrelated, and nutrition plays a funda-
Puberty happens in the middle of the school-age
mental role. Protein-energy malnutrition is associated
years and marks and determines the changes in trajec-
with delayed puberty, and subsequently poor growth
tory and the switch in somatic and brain growth and
and development. Secular trends have changed the tim-
development rates, which characterize this part of the
ing of these processes in different populations, likely
life cycle. Two significant phenomena arise in this
reflecting nutrition and health changes in the last cen-
period:
tury. In Europe and North America, from the early 19th
century to the mid 20th century, age at menarche • Several inflection points and trajectory changes occur
decreased from approximately 17 years to about in somatic and brain growth and development, at dif-
12 years–13 years.16 In China, in just the past 25 years, ferent time points, for various measures of develop-
the mean age of menarche has decreased by 4.5 months ment (eg, height, adiposity, lean mass accretion, bone
per decade.17 As discussed below, changes in growth mineralization, brain growth and reorganization, with
patterns, particularly in height and body–mass index subsequent cognitive development, and secondary sex-
(BMI), are interrelated with the onset of puberty. ual characteristics) and social and behavioral changes

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• Sex divergences appear or become significantly more their fat mass almost 5-fold, while boys will have
pronounced in these measures. increased theirs by around 3-fold. Ultimately, fat mass
will increase from 10%–12% of body weight at birth to
The dynamic somatic, cognitive, and behavioral
approximately 15% in young men and approximately
changes that occur during school age underscore the
25% in young women. In boys, after a prepubertal
importance of preparing children during middle child-
increase in percentage body fat, this percentage actually
hood and facilitating their transition into adolescence
declines with puberty and stabilizes with maturation.21
during this period. Figure 2 shows the changes in trajec-
The rate of accumulation of fat-free mass (including
tory for key anthropometric changes during the school
muscle mass) remains comparable by sex until the onset
years.
of puberty. With the onset of puberty, boys will accu-
mulate lean mass significantly faster and for a longer
Body composition

period than girls. Gains in adipose tissue are primarily
driven by an increase in the number and size of fat cells,
Although height velocity decreases during the preschool
while muscle development happens mainly by an
years, height gain remains relatively steady, and the
increase in muscle cell mass (hypertrophy). The
amount of body fat remains relatively constant; there-
increase in body weight gain during puberty is mainly
fore, most children in middle school will appear
attained through an increase in lean tissue in boys.
slimmer than when they were toddlers. In fact, median
Skeletal muscle mass, which represents about 25%
BMI will be at its lowest in life at about 5.2 years in girls of body weight at birth, will increase to 40%–45% body
and at about 5.75 years in boys, ie, just as they enter weight in late adolescence.18,20 Girls will reach adult sta-
school age.19 During this period, a child’s adiposity bilization by 15 years–16 years, while boys will do so by
(corresponding to an increase in number of adipocytes) 18 years–20 years.21 Skeletal muscle mass has been esti-
will rise, giving way to what is called the “adiposity mated for children of school age using appendicular
rebound” or second rise in BMI during life. BMI, a lean tissue mass extracted from dual photon absorpti-
reflection of adiposity, is the first anthropometric inflec- ometry measurements22 and bioelectrical impedance.23
tion point to appear in the school-age years.20 Both approaches show that muscle mass and rates of
The age at which this inflection happens is inver- gain are similar in both sexes until middle childhood.
sely proportional to their BMI percentile (children with At around 5 years of age, boys maintain a slightly higher
higher BMI will rebound earlier). Furthermore, an ear- muscle mass, and girls a higher fat mass, after which
lier adiposity rebound is associated with a higher risk of trajectories increasingly diverge. This results in an
later obesity. As mentioned above, secular trends show approximately 3.5–5-fold increase in muscle mass in
an interplay between nutritional status and puberty. In boys and a 3–4-fold increase in muscle mass in girls
addition, overweight and obesity in girls will lead to between 5 years and 15 years, in part depending on the
earlier puberty. Boys, however, show a less clear pattern: methodology used. Conversely, fat mass will increase
overweight boys seem to mature earlier, but obese boys more in girls than in boys during this period.
mature later. The mechanisms are not yet clear, and
there appears to be a bidirectional influence between Height and linear bone growth
puberty and weight gain.16
Body compositional changes during the school The increase in height gain is the most noticeable
years also mark significant changes in trajectory and sex change in trajectory in anthropometric measures of the
divergence. Large-scale normative data for body com- school years. About 40% of an individual’s linear
positional changes for middle childhood and early ado- growth will occur during this time. Based on the United
lescence are lacking, although some estimations and States CDC growth curve medians, by 5 years of age,
extrapolations have been done. Fat mass, fat-free mass, boys and girls will, on average, be at 61% and 65%,
and percentage body fat have been estimated by aggre- respectively, of their ultimate height. By 15 years, they
gating data from several cross-sectional analyses from will be at 96% and 99%, respectively of ultimate
European and American populations.21 During the pre- height.19 There are major differences between the first 5
school years, actual fat mass in kilograms is similar in and second 5 years of school age.
both sexes. Between 5 years and 10 years, girls will accu- During middle childhood, height velocity actually
mulate fat mass faster than boys, gaining approximately decreases, to the lowest levels of the entire life cycle,
6% (2 kg) more than boys. After this, with the onset of only to quickly increase in the middle of the school
puberty, girls will gain about 1.14 kg of fat, while boys years to the highest rate of linear gain of all post-
will maintain a relatively fixed fat mass. Throughout the infancy years. In North America, CDC growth velocity
school years, until 15 years, girls will have increased charts19 show median height velocity will be at its

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Figure 2 Growth trajectories in school-age years (gray-shaded area). Fat and fat mass: estimates. All others are medians. Compiled
and adapted from Tanner and Davies 198524 (height velocity), Weaver et al 201633 (BMC gain), Veldhuis et al 200521 (fat and fat mass), US
CDC19 (BMI). BMC: bone mineral content; BMI: body–mass index
lowest since birth just before 9 years of age in girls and With the onset of puberty, height velocity rapidly
at approximately 10.5 years in boys. At that point, increases. In early adolescence, median peak height
before the puberty-related acceleration, both girls and velocity in girls reaches its peak at around 11.5 years of
boys will have reached 80% of their final height. Thus, age, with growth rates similar to those at 2 years of age
height at that point will be a strong predictor of ulti- (8.3 cm/y). In boys, a peak growth rate of about
mate height in most individuals. This speaks to the 9.5 cm/year happens at around 13.5 years of age, sur-
importance of adequate nutrition and sustained growth passing the 2 years of age rate of height attainment.24 In
between 5 years and 10 years of age. girls, this growth spurt starts earlier (9 y in girls vs

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10.5 y in boys) and ends earlier (11.5 y vs 13.5 y), school age, more than 80% of total body BMC will have
lasting at least 0.5 years less than in boys. The ultimate been attained, and final total body BMC appears to pla-
median height in males will be greater due to greater teau at around 18 years of age in girls and 20 years in
height at the onset of puberty (boys 9 cm–10 cm taller boys.29,30
than girls), a more prolonged growth spurt period, and Similar to height gain, the BMC accretion will
a greater increase following pubertal onset (boys gain- increase rapidly with the onset of puberty, and the
ing 3 cm more than girls between the onset and end median peak rate of BMC accretion will occur at
of the growth spurt). The pubertal growth rate declines around 12.5 years in girls and 14 years in boys. Thus,
rapidly after their gender-specific peak in both sexes, to the peak BMC accretion rate will lag compared with the
1 cm/year or less after 14.5 years in girls and 17 years in peak height velocity, which occurs at around 11.5 years
boys.21,24 and around 13.5 years in girls and boys, respectively.

Height gains are dependent on longitudinal bone Therefore, there is a transient decrease in bone density
growth determined by epiphyseal growth plate function. relative to height and bone elongation, and conse-
Growth plate chondrocytes proliferate by mitosis, quently an increase in bone fragility lasting about
mature, become hypertrophic, lengthen the bone, and 12 months in girls and 6 months in boys (see Figure 2).
ultimately replace osteoblasts to form new calcified This may partially explain the higher rate of forearm
bone tissue. Growth hormone and insulin-like growth fractures reported in girls between 8 years and 10 years,
factor are the key hormonal drivers of this process. and in boys between 10 years and 12 years.30,31
Adequate nutrition is critical for providing substrates Ultimate bone mass, measured as bone mineral
for epiphysial growth, particularly energy, protein, and density (BMD) or mineral content divided by bone
zinc. Calcium and vitamin D may play lesser roles in area, will depend on genetic and environmental factors.
longitudinal bone growth. Very importantly, independ- Studies in twins suggest that genetics can explain 50%–
ent of nutrient provision, bone growth regulation can 85% of the variance in peak bone mass, with multiple
be blocked by corticosteroids and inflammatory cyto- genes being involved, some of which may interact with
kines. Chronic inflammation from infection, environ- environmental factors, including diet.32 Thus diet and
mental factors, autoimmune disease, and the use of “lifestyle” factors, including exercise, can still signifi-
corticosteroids can all curtail linear bone growth. In cantly influence BMC and BMD. As stated above, mid-
addition, inflammation can lead to insulin and growth dle childhood and early adolescence are the periods of
hormone resistance, which can further inhibit linear fastest mineral accrual, and more than 90% bone mass
bone growth, thus compounding the effect of undernu- is achieved by 18 years–20 years. By the late 20s, bone
trition, as often occurs in underserved populations.25–27 mass will begin a gradual process of decline, leading to
As discussed below, poor linear growth and stunting varying degrees of osteoporosis, which can only parti-
(two standard deviations beyond the normal curve ally be modified by diet and other environmental fac-
median) remain the most prevalent clinical manifesta- tors. It follows that school age becomes a critical age of
tion of undernutrition globally.28 intervention and “investment” in bone health by maxi-
mizing peak bone mass and decreasing the risk of frac-
Bone mineralization tures in later life. This includes optimizing nutrition,
particularly provision of protein, calcium, and
Linear bone growth is followed by increases in bone vitamin D, as well as activity and exercise during this
mass and bone mineralization. Bone matrix becomes life stage.31,33
mineralized with the deposition of calcium phosphate
nanocrystals (carbonated hydroxyapatite). The degree Brain and cognition
of deposition will determine bone mineral content
(BMC), measured in grams, for a specific skeletal loca- Brain size increases by 4-fold during the preschool
tion or for the total body. This sequence of events will years, reaching approximately 90% of adult volume by
be similar, with variations by sex. age 6.34 However, brain development will be a continu-
Total BMC will rapidly increase in early adoles- ous process with age-specific phases until adulthood.
cence. Data derived from North American individuals The growth rate of cortical gray matter peaks during
show that by the end of middle childhood, prior to the school age, by 10 years–12 years of age. Cerebral white
onset of the growth spurt (2.5 y to 3 y before peak matter volume increases through school age until mid-
height), children will have achieved 37%–40% of ulti- to-late adolescence, peaking by 18 years–20 years.35,36
mate total body BMC. In the short period between the Total brain size is about 9% greater in males than
2 years before and 2 years after peak height is attained, females, and the difference persists, even if controlling
another 39% of ultimate BMC is accrued. By the end of for height and weight. These differences should not be

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Figure 3 Neuromaturational and cognitive development trajectories in school-age years (gray-shaded area). Compiled and adapted
from Peterson et al 202138 (brain and gray matter growth), Tapert and Schweinsburg 2005114 (neuromaturation process rate), Lee et al
2014115 (brain region development), and Anderson 200246 (cognitive development executive domains)
understood as conferring advantage or disadvantage, as increase in synaptic refinement and pruning, both of
they do not represent neuronal or synaptic connectivity which are important for the efficiency of neuronal net-
or other components of brain architecture and function works. Dendritic synaptic pruning eliminates unused or
(see Figure 3).37,38 weak connections, and a reduction in myelination rates
During the school years, though at a slower rate than improves connectivity. This fine-tuning within and
during the preschool years, total brain size increases, as between brain regions strengthens a number of particular
does the sex-driven divergence, with boys being faster pathways, which increases brain efficiency, critical to the
and peaking by 14.5 years, and girls peaking earlier by development of cognitive abilities.39,40
11.5 years.37 During this period, brain development is School age will be marked by the highest rate of
also marked by a significant increase in 2 major neurodevelopment of specific areas of the brain, particularly
maturational processes: continued myelination and an the posterior sensorimotor cortex, temporal association

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complex, and prefrontal cortex, and this development pruning and myelination are driven or modified by an
peaks at between 5 years and 15 years of age, in the mid- individual’s experiences.47 Thus, behaviors toward the
dle of school age. All these areas are “associative environment are shaped by biologic changes in the brain,
cortices,” which process input from the sensory cortices which in turn may be shaped by environmental, social,
and ultimately generate behaviors (see Figure 3). These and cultural learning experiences. School age marks a
structures are the key determinants of higher-order major development of the associative brain regions and
functions, particularly cognitive development (includ- the resulting cognitive development and EFs, as well as
ing language, mathematics, and executive function the maturation of reward and emotional sensitivity areas,
[EF]) and socio-emotional regulation, which among which interact with higher function control areas to
other things, allows for organization of information to develop emotional regulation, identity development, and
serve goal-directed behaviors, decision-making, peer longer-term planning and purpose. Adequate provision
affiliation, and social behaviors.41,42 The parietal and

of nutrition, healthy social interactions, and cultural expe-
temporal association cortex, responsible for language riences, as well as adequate sleep, are all key to physical
skills, also develops at a fast rate and this development and psychosocial well-being.41
peaks during school age. For example, language acquisi- The onset of early adolescence will be marked by
tion and proficiency, especially the ability to master a an increase in social and cultural interactions, and
second language as a native speaker, decreases at the changes in the home, community, and school relation-
end of school age, by 15 years of age.43 ships, which influence behavior. The interaction
The development of the prefrontal cortex peaks in between behavior resulting from brain functions and
the middle of the school years and continues to mature external influences appears to be bidirectional. At the
into the third decade. The gray matter volume in the onset of puberty, the prefrontal associative brain areas
frontal cortex peaks at 11 years of age in girls and at just continue to develop, but at a slower pace than some
after 12 years in boys.44 This part of the brain supports subcortical brain areas. These limbic emotion- and
higher-level integration and processing, allowing for reward-related regions, such as the amygdala, appear to
abstract thinking, problem-solving, understanding mature earlier than the prefrontal areas, which are
others’ thoughts and intentions, and the relating of responsible for inhibitory control of impulses and regu-
thoughts temporally, allowing for goal setting. Thus, the lation of gratification and other emotions. This
prefrontal cortex is generally regarded as the “seat” of “mismatch” may in part explain the increase in risk-
EF. EF is a broad term that incorporates a collection of taking, emotion-driven behaviors seen in adolescence.48
mental processes that (a) enable individuals to hold and In summary, between the age of 5 years and
recall relevant information (working memory), (b) 15 years, children go through major accelerations and
focus their attention, inhibiting automatic responses to inflections in their somatic growth, from a prepubertal
stimuli (inhibitory control), and (c) shift the focus of state in the first 5 years to early adolescence changes in
attention to the managing of problems or multiple- the next 5 years. By the end of school age, and before
aspect tasks successfully (cognitive flexibility), to yield entering the final stages of “late adolescence,” healthy
purposeful, goal-directed behaviors. Ultimately, these boys and girls, respectively, will have attained approxi-
processes influence behavior, emotional control, and mately 96% and 95% of their adult height,19 92% and
social interaction. EF is associated with academic per- 77% of their total BMC,49 89% and 85% of their fat
formance as well as intelligence quotient (IQ).42,45,46 mass,21 and 84% and 95% of their muscle mass.22
One well-recognized model of EF conceptualizes and During this period, neuro-maturational processes will
maps chronologically 4 distinct and interrelated develop- have also undergone significant changes. These include
mental domains, each of which gathers and processes peaks in the development of specific areas of the brain
stimuli from multiple sources: attention control, informa- and particularly the prefrontal cortex (implicated in
tion processing, cognitive flexibility, and goal setting. complex cognitive behavior, planning, personality
Attentional control matures relatively early, by the end of expression, decision-making, and moderation of social
preschool age; information processing and cognitive flexi- behavior) in the middle of the school years. Processes
bility are mostly developed by the end of middle child- like synaptic pruning, which increase brain efficiency,
hood; and goal setting is well developed before the end of will also peak by the end of this period, allowing for
early adolescence (see Figure 3).46 plasticity and increased brain efficiency. Delaying, alter-
In addition, the increased synaptic pruning and mye- ing, or blunting these accelerations and inflection
lination that occurs during this period significantly points can significantly affect the ultimate attainment of
reshapes and modifies circuitry and allows malleability physical growth, and cognitive, and socioemotional/
and adaptation to environmental experiences, or brain psychosocial development. The necessity of preparing
plasticity. There is evidence, eg, that both synaptic the child for these changes and supporting them

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through these accelerations and inflections, leading to accumulation, increased body weight, and its related
the final maturational phase of late adolescence and consequences).
ultimately adulthood, cannot be overstated. The factors that affect child energy requirements
are growth and body composition (which are sex-
ROLE OF NUTRITION IN SCHOOL AGE dependent), as well as physical activity. Daily energy
requirements diverge by sex at the start of school age,
The number of changes and dynamics of development and will remain different throughout the life cycle. Sex
mentioned above make the school years a particularly differences in metabolic rate and energy expenditure
sensitive time, especially since most of the final growth are in part driven by differences in body fat and fat-free
and development is attained, which if not achieved will mass that emerge during school age.
limit physical, cognitive, and social potential. These Between 5 years and 15 years of age, physical activ-

changes happen against a genetic backdrop expressed ity is a particularly important factor in energy balance.
in, and dependent upon, multiple environmental and In adults, the estimated difference in energy require-
social scenarios that modulate physical and psychosocial ments between a sedentary individual and an active
development. individual is below 20%, while in 5-year-olds to 15-
All these changes are underpinned by adequate year-olds it is around 35%, indicating the need for
nutrition in this period, as is true for all life cycle adequate energy provision—in proportion to the rec-
phases. Inadequate nutrition will slow or blunt physical ommended “active” level of physical activity during this
and neurocognitive development trajectories during period of the life cycle.51 Energy provision throughout
this last period of growth and development, with long- the day is also critical for brain activity, where increased
term consequences, inhibiting an individual’s ultimate neuronal activity drives increased energy consumption.
potential. If environmental conditions, particularly In addition to all the neurodevelopmental changes
occurring during school age mentioned above, the cere-
nutrition, are favorable, the growth course and final
bral metabolic rate of glucose utilization is at its highest
height and overall body shape will be determined by an
in middle childhood and early adolescence (apart from
individual’s genes.27 The acceleration and change in
during the newborn period), then drops towards the
growth trajectories discussed above increase the chances
end of adolescence. The mature brain is only approxi-
for curtailing growth and development if increased
mately 2% of the body weight in adulthood, but is
nutritional demands are not met. Because of the growth
responsible for around 20% of energy consumption.
dynamics in this period, the school years become crit-
Estimations for 12-year-old children suggest that brain
ical for the necessary nutrition (a) to maintain adequate
energy consumption is as high as 30%.52–54 Lastly, this
growth trajectories until maturity, or (b) to correct increase in energy requirement and utilization is also
inadequacies and imbalances (deficits and excesses) for dependent on the presence of adequate quantities of
a healthy transition to a productive adulthood. several micronutrients. These include riboflavin (vita-
WHO, the US Institute of Medicine, the European min B2), niacin (nicotinamide; vitamin B3), pyridoxine
Food Safety Authority (EFSA), and other regional (vitamin B6), cobalamin (vitamin B12), vitamin C,
authoritative groups all distinguish and define specific vitamin D, calcium, iron, and phosphorus. They all act
energy, macro-, and micro-nutrient requirements for as co-factors for key enzymes in the metabolic pathways
the school-age years (early childhood and early adoles- that generate and use energy.
cence) distinct from those of other life stages. Protein is the major functional and structural com-
ponent of every cell in the body. The quality of a source
Energy and protein of dietary protein depends on its ability to provide the
nitrogen and amino acid requirements necessary for the
As the child grows, changes in metabolism are directly body’s growth, maintenance, and repair. Through to
related to total energy requirements and indirectly to the end of the growth years, enough protein is required
growth, and consist of basal metabolic rate, energy cost to maintain the nitrogen equilibrium plus protein depo-
of growth, and activity energy expenditure.50 As a frac- sition in tissues. Low consumption of protein, often
tion of the total energy requirements, the energy cost of associated with low protein quality, is strongly associ-
growth is highest in the newborn period, decreases to ated with stunting, and if marked, other signs of under-
about 3% at 1 year of age, and goes up again between nutrition. As opposed to requirements for energy and
middle childhood and early adolescence to about 4%.51 some micronutrients, protein requirements do not
Imbalances between energy intake and expenditure can change significantly by age or sex during the school
result in deficits (leading to a decrease in body fat and a years. The United States recommended dietary allow-
deceleration of growth) or excesses (in the form of fat ance is 0.95 g/kg/day, representing 10%–30% of total

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calories, from 4 years to 13 years of age. The recom- mineralization but appears to be of less consequence
mended dietary allowance decreases slightly after ado- regarding linear growth.27
lescence. In general, proteins from animal sources such Independent of nutrient provision, as mentioned
as meat, poultry, fish, eggs, milk, cheese, and yogurt above, bone growth regulation can be blocked by
provide all indispensable amino acids and are referred inflammation, such as recurrent childhood infections,
to as “complete proteins.” Proteins from plants, which, if bi-directionally compounded by undernutri-
legumes, grains, nuts, seeds, and vegetables tend to be tion, result in poor growth led to stunting. The term
deficient in one or more of the indispensable amino “environmental enteric dysfunction” has been used to
acids.Thus, attention needs to be paid to children whose refer to chronic and recurrent infections and infesta-
diets are low in animal protein sources to avoid essen- tions in areas with poor sanitation, where infection,
tial amino acid deficiencies.51 inflammation, and malabsorption coalesce and perpetu-

ate undernutrition. These conditions may explain why
Micronutrients nutrition or dietary interventions alone may not be suf-
ficient to address stunting in children. Current inter-
In the United States, the Estimated Adequate ventions to reduce stunting need to target sanitation
Requirements, and Dietary Reference Intakes for and environmental factors as well as nutrition in low-
micronutrients are the same for all children up to age and middle-income country settings.25,27
8 years. For the first time, they diverge for boys and girls Calcium is essential for adequate mineralization of
during the school years: there are small differences (eg, bones, and 99% of all calcium in humans is found in
for iron) for 9 years–13 years, and larger differences in bones and teeth. Dietary calcium can be absorbed pas-
requirements for late adolescence, at 14 years– sively, but the active transport of calcium in the gut is
18 years.51 EFSA has slightly different and more specific mediated by vitamin D. Both nutrients are inextricably
age cut-offs for Population Reference Intakes (PRIs) for linked in determining BMC. Low calcium intake in
most vitamins and minerals.55 Recommendations are young children is associated with low BMC, and sus-
made for 4 years–6 years, 7 years–10 years, 11 years– tained low intakes (below 200 mg daily) with radio-
14 years of age, and separately define PRIs for 4 years– graphic signs of rickets.56
10 years and 11 years–17 years for calcium, 1 year– There is clear evidence suggesting that peak bone
6 years, 7 years–11 years, and 12 years–17 years for iron, mass and risk of fractures in later life are influenced by
and 3 years–9 years and 10 years–17 years for copper, bone mineral accretion throughout childhood, includ-
with some differences for sex in these nutrients. EFSA ing school age. As discussed above, peak rates of bone
also differentiates requirements in energy and protein mineralization are reached 6 months–12 months after
for boys and girls starting at 4 years. While specific ben- the peak rate of bone elongation is reached. By the end
efits have been well established in relation to deficien- of school age, median peak height has been achieved in
cies for many micronutrients, consensus on optimal girls (achieved a year later in boys), and more than 80%
doses and combinations of these nutrients for promo- BMC has been accrued. The exact cessation of mineral
tion of specific health benefits in otherwise healthy accrual varies depending on the skeletal site, but
school-age children is not universal and would benefit appears to be complete by 18 years in the spine and
from further clinical research and substantiation. femoral neck. After peak BMC is reached, the rate of
Linear growth appears particularly sensitive to bone mass and mineral content accretion gradually and
restrictions in energy, protein (particularly essential continually decreases for the rest of an individual’s
amino acids), zinc, iodine, and phosphorus, as well as life.33,57 Therefore, the rate and amount of BMC
some electrolytes. Protein quantity and quality remain attained in the school years will greatly determine peak
fundamental components of adequate growth and func- bone mass and be a major contributor to the relative
tion at all ages. Yet, the minimum protein necessary for risk of low bone mass and eventual osteoporosis and
adequate linear growth remains to be ascertained. bone fractures for the rest of an individual’s life. Recent
Animal proteins, including dairy protein sources, have estimates from the United States in adults older than
a selective effect in promoting height gain in under- 50 years show a prevalence of low bone mass of 51.5%
nourished and well-nourished children. In populations in women and 33.5% in men, and frank osteoporosis of
with low consumption of foods from animal sources, 19.6% in women and 4.4% in men.58 Estimates from the
protein and zinc deficiencies will be more common. International Osteoporosis Foundation indicate that,
While iron and vitamin A are essential for multiple worldwide, after 50 years of age, 30% of women and
other reasons, intervention studies suggest that their 20% of men will have hip, vertebral, or wrist fractures
deficiency does not affect linear growth. As discussed from osteoporosis in the remainder of their lives.59
further below, calcium is critical for bone Thus, meeting dietary protein and calcium

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requirements, maintaining adequate vitamin D through Consequences of inadequate nutrition in school age
diet and sunlight exposure, and physical activity during on growth and development
school-age years constitute critical investments in
achieving long-term bone health.31,60 Inadequate nutrition in school age ultimately results
Iron, zinc, polyunsaturated fatty acids (especially from inadequate diets, which in turn are a consequence
docosahexaenoic acid), vitamin B12, and folate have all of multiple factors. On the one hand, food security,
been specifically identified as critical nutrients for availability, and provision are essential. On the other, a
adequate brain growth, cognition, and EF development. healthy diet requires appropriate food choices, which
However, as for other aspects of life-stage nutrition, depend on many environmental influences—from
most data have been accumulated for these nutrients home, the community, the school, and broader society.
and their longer-term effects in relation to consumption These influences will not only determine the delivery of
adequate foods but shape the behavior of children and

in the first 5 years of life. They have often not been the
primary focus of studies and are poorly investigated in thus their food choices for the long term. Influences at
healthy school-age populations.61 this age are critical, when cognitive, socioemotional,
Deficiency in iron deserves highlighting in relation to and psychosocial development are associated with
nutritional consequences for later life, due to its preva- increasing independence, decision-making, and self-
lence in and coexistence with all forms of malnutrition. image and awareness. Addressing all these factors
Iron deficiency is the most common nutritional deficit in remains critical for increasing an individual’s chances
people worldwide and the most common deficiency in for long-term health. Discussion of these is beyond the
children, whether suffering or not from acute or chronic scope of this review.
malnutrition. Anemia, half of which is due to iron defi- The immediate and most visible consequences of
ciency, affects around 33% of the global population. not meeting nutritional requirements are loss of body
Globally in 2019, iron deficiency was the leading cause of weight and adipose tissue (thinness/wasting/low BMI).
years lived with disability in children and young adults Prolonged marginal provision of macronutrients, most
(aged 10 y–24 y), with the highest prevalence in most often accompanied by micronutrient deficits, leads to
African and many Asian countries.62 While its prevalence slowing of linear growth (low height for age). In both
is higher in low- and middle-income countries, it persists cases, infection, or other inflammatory states, coupled
in varying degrees in all socio-economic levels. Iron is a with enteropathies related to poor sanitation, can fur-
crucial nutrient in maintaining levels of neurotransmitters, ther increase requirement for an effective immune
including dopamine and serotonin. And its deficiency can response, lead to a negative nitrogen balance, mobiliza-
decrease brain myelination, alter synaptogenesis, and tion of protein from muscle tissues, as well as inhibition
decrease the functioning of basal ganglia. The consequen- of linear bone growth.25,28 Wasting and stunting are
ces in childhood include deficits in motor function and often linked and can occur together in the same popula-
impaired cognitive development, leading to lower cognition, often in the same child.67 Longitudinal analyses
tive skills, lower school achievement, impaired psychomo- show that wasting is a precursor to stunting.68 In addi-
tor and behavioral development, and ultimately lower tion, low BMI and wasting are related to delayed puber-
work capacity and productivity in adulthood.63,64 tal onset, which in school-age children affects growth
The consequences of iron deficiency in childhood, trajectories. Globally, stunting (height-for-age greater
some of which may be irreversible, have been recog- than 2 standard deviations below the WHO reference)
nized for a long time and have led to global efforts in remains by far the most prevalent clinical manifestation
improving iron status through supplementation in of undernutrition, including micronutrient
infancy and childhood.64,65 Given the significant deficiencies.28
changes in brain structure and function that happen Stunting in early life is associated with poor cogni-
during the school years, and the potential long-term tive development, lower development of EF, lower rates
consequences of deficiency, iron remains a major of schooling and school achievement, and ultimately
nutrient of interest, highlighting the need for adequate decreased productivity and earning power. These asso-
preventive interventions as well as treatment of defi- ciations, however, do not necessarily infer causality.
ciencies during this life stage. There is increasing and Stunting is often accompanied by multiple nutrient
robust evidence that improving iron status, particularly deficiencies and their consequences, beyond iron defi-
in the presence of anemia, significantly affects cognitive ciency anemia. And the occurrence of stunting due to
performance in school-age children older than 5 years. poor nutrition, and its cognitive and other consequen-
Interestingly, the evidence for this effect of iron on ces, cannot be delinked from the effects of the physical
older children appears stronger than for interventions and social environments where stunting occurs69–71;
in children under 2 years of age.66 nonetheless, it is likely they are causally related. Beyond

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cognitive impact, not achieving an individual’s height GLOBAL STATUS OF NUTRITION IN SCHOOL AGE
potential can also be associated with higher psychologic
dysfunction all the way to late adolescence, with Compared with infant data, apart from some recent
increased chances of developing low self-esteem, anxi- increase in data on the adolescent years, there is a seri-
ety, depressive symptoms, and anti-social behaviors.72,73 ous lack of information on nutritional status and its
Stunting can occur at any age before adulthood, consequences for middle childhood through adoles-
but for most school-age children, it is a continuation of cence. One analysis showed that, a literature search for
poor growth in early infancy. WHO and World Bank 2004–2017 including the terms “health,” “mortality,” or
global estimates show that globally, stunting in children “cause of death in the first 20 years of life” found that
under 5 years of age has decreased from 33% (203.6 mil- about 99% of the publications in Google Scholar and
lion children) to 22% (149.2 million children) from 95% of the publications in PubMed focused on children
under age 5 years.8 Global School-based Student

2000 to 2020,7 with the highest prevalence in Africa and
parts of Asia and Latin America. Thus, a great number Surveys, a collaboration of WHO, CDC, UNICEF,
of children are stunted when entering school age. UNESCO, and UNAIDS, have primarily included only
Stunting prevalence in school age will result from stunt- 13-year-olds to 17-year-olds.78 In addition, data for this
ing occurring under 5 years, with some “new” cases age group is often embedded and difficult to disaggre-
gate from “childhood studies” that may include pre-
being added or a decrease in cases from “catch-up”
school and school-age children, or from studies on
growth.74 Although most stunting may start in infancy,
“adolescents” that include children of 10 years or
it can continue or worsen in the school years. As dis-
12 years and above. Overall, the ages 5 years–9 years and
cussed below, given school age is the last and second
10 years–14 years have the least number of research data
fastest period of height attainment after infancy, this life
sources for estimating morbidity and mortality risk fac-
stage may offer the last “window of opportunity” for
tors compared with 0 years–5 years and 15 years–
correcting deficits and potentially achieving catch-up
19 years. Another recent large population-based study
growth and catch-up cognitive development, ameliorat-
showed that, within the relatively small amount of avail-
ing its negative consequences for individuals and
able data for height, weight, and BMI in school-age chil-
society.
dren, 78.9% of studies had data for 15 years–19 years,
Lastly, children who remain stunted through school
but only 50.3% had data for 10 years–14 years, and
years may be at increased risk for obesity. There is
39.9% for 5 years–9 years of age.79 In another larger
growing evidence that stunted infants and children who
analysis, less than half of the studies included data for
gain weight rapidly in later childhood have an increased middle childhood (5 y–9 y), compared with nearly 90%
risk of overweight, obesity, and noncommunicable dis- with data for adolescents (10 y–19 y). Overall, the quan-
eases as adults.75,76 However, stunting at 1 year alone tity and quality of data vary significantly by country and
does not seem to raise obesity risk consistently.77 This region. Still, the relative lack of data for middle child-
is becoming increasingly important, as the secular tran- hood is notable across the board, limiting the capacity
sition from undernutrition to obesity is accelerating in to compare growth or nutrition outcomes of this age
many populations, as discussed below. The peak inci- group with earlier or later life stages.80
dence of obesity by age has been occurring earlier and A systematic review, one of the few studies focusing
earlier in life in many populations (see below). Its con- on school age (6 y–12 y) in low- and middle-income
sequences (related to metabolic disease, diabetes, cardi- countries (LMICs), showed underweight and thinness
ovascular disease, and other noncommunicable were most prevalent (21%–36%) in South-East Asian
conditions) constitute the greatest health challenges of and African countries, with lower prevalence in Latin
this century. America (8%–6%). The prevalence of overweight and
Specific nutrient deficiencies, individually or in obesity was highest in Latin America (26%), com-
combination, and their syndromes are both present and pared with 13% in Southeast Asia and 7% in Africa. The
prevalent in school age. The consequences of these in mean prevalence of iron deficiency ranged from 29% in
addition to those mentioned above are beyond this Africa to 20% in Southeast Asia, and 14% in Latin
review. Suffice it to say that persistent deficiencies such America. Iodine, vitamin A, and zinc deficiencies are
as of iron (and its effects on long-term cognitive func- the most common. The prevalence of vitamin A defi-
tion) as well as calcium and vitamin D (and their poten- ciency was 9% in Latin America (on the lower end), to
tial in preventing osteoporosis and fractures well into 54% zinc deficiency prevalence in Africa (on the highest
adult and mature life) are prime examples of the need end).81
for maintaining adequacy or correcting deficiencies Very recently, data from population-based studies
during school age. supported by the Non-Communicable Disease Risk

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Factor Collaboration79,80 and the B&M Gates in LMICs range from 52% in Guatemala and 44% in
Foundation82 are shedding light on this global picture. Bangladesh to 6% in Brazil.83
These are the most comprehensive reviews on growth The 2 most extensive global studies including chil-
and temporal trends available to date for this age group, dren 5 years–19 years of age79,80 did not report height
and the only available review addressing this age group based on a particular cut-off for stunting. Nevertheless,
at a global level. One analysis, NCD RisC 2017,79 in age-related trends, most countries showed that height
included 31.5 million children from 200 countries aged was at or above the WHO median for children at 5 years
5 years–19 years, and estimated trends from 1975 to of age, with girls doing better than boys. Still, in approx-
2016. The other, NCD RisC 2020,80 pooled data from imately 20% of countries for girls and 30% of countries
2181 population-based studies, with height and weight for boys, the mean height during the school years was
measurements for 65 million participants in 200 coun- significantly below the WHO median. Today, the esti-

tries, and estimated trends from 1985 to 2019 in height mated difference in height of 19-year-olds between
and BMI for children 5 years–19 years. In this study, countries with the tallest populations (eg, the
data were reported without specific cut-off points for Netherlands, Denmark) and the shortest populations
over- or under-nutrition. Data and trends from these (eg, Timor-Leste, Laos, Guatemala, Bangladesh) was
studies are summarized immediately below. 20 cm. More concerning is that, in some countries,
height adequacy in middle childhood may decrease as
children grow older. Children who have optimal height
Thinness and wasting
at 5 years of age fall under the WHO median at 19 years
From 1975 to 2016, the overall global prevalence of by 2 cm or more, particularly in some middle-income
moderate and severe underweight (thinness and wast- countries.
ing) in children 5 years–19 years decreased from 9.2% In terms of temporal trends, with rare exceptions,
the last 3 decades show significant gains in height in
to 8.4% in girls and from 14.8% to 12.4% in boys, with
most countries and all regions for boys and girls, except
the expected large variations regionally. The prevalence
for Sub-Saharan Africa (for both sexes) and Oceania
of moderate and severe underweight remained highest
(for boys). The greatest gains have been made in coun-
in south Asia, with 22.7% among girls and 30.7%
tries with emerging economies, including China and
among boys in India. Although the populations
South Korea, and parts of Southeast Asia, the Middle
increased in most regions, the number of moderately
East, and in some countries in North Africa, Latin
and severely underweight school-age children actually
America, and the Caribbean.80
decreased. And while prevalence declined, the relatively
small change at the global level was partly due to greater
Overnutrition
population growth in countries where the prevalence of
underweight is higher.79 Over the last 40 years, obesity has increased in every
Mean BMI trends showed increases in almost every country in the world. The NCD-RisC 2017 study79
country over the last 30 years, with the greatest showed that, from 1975 to 2016, the global prevalence
increases seen in Sub-Saharan Africa. Low BMI (com- of obesity in 5-year-olds to 29-year-olds increased from
pared with the WHO reference median in 5-year-old 0.7% to 5.6% in girls, and from 0.9% in 1975 to 7.8% in
children) persisted primarily in Southeast Asia and boys. The number of girls with obesity increased from
Sub-Saharan Africa. In most countries, it decreased as about 5 million to 50 million in 2016, and the number
they entered adolescence, and in some countries it dis- of boys from about 6 million to 74 million. Trends in
appeared by age 19 years.80 The trends showed that, mean BMI have continued accelerating, particularly in
globally, the absolute number of underweight children east and south Asia. Southern African countries had the
peaked around the year 2000 and has since been greatest rise in obesity (400% per decade), given the
decreasing, reaching levels in 2016 close to those in obesity prevalence was minimal 40 years ago.
1975.79 On the other hand, since about 2000, the increase
in prevalence has begun to plateau, and it recently flat-
Stunting tened in northwestern Europe, in “high-income
English-speaking” and Asia-Pacific regions for both
Data from surveys in 57 LMICs between 2003 and 2013, sexes, in southwestern Europe for boys, and in central
comprising children 12 years–15 years, showed a global and Andean Latin America for girls. While not exactly
prevalence of stunting of 10%.75 However, the limited comparable, these findings are consistent with another
data available on stunting in this age group shows very earlier large study82 that analyzed 1769 population-
wide variations. Stunting in adolescent girls (15 y–19 y) based surveys and studies in 19 244 children aged

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2 years–19 years (not reporting disaggregated data for closing of those gaps may signal a “too rapid” transition
school age). These investigators found that, from 1980 from a mostly underweight population to a mostly over-
to 2013, in developed countries, the prevalence of overweight and obese population, as has occurred in parts
weight and obesity for 2-year-old to 19-year-old chil- of Asia and Latin America, accelerating and increasing
dren (as a group) increased from 16.9% to 23.8% in the burden of nutrition-related conditions, particularly
boys and 16.2% to 22.6% in girls. In the same period, in for LMIC populations.
developing countries, the prevalence of overweight and While trajectories vary regionally, in many coun-
obesity increased from 8.1% to 12.9% in boys and 8.4% tries, based on height and BMI, nutritional status
to 13.4% in girls. All studies show that globally, the appears to be adequate at 5 years (which may reflect
peak prevalence of obesity is shifting to younger ages. efforts over the last decades in improving early child-
While the prevalence remains higher in developed hood health and nutrition) but deteriorates as children

countries, the great majority of overweight and obese move through the school years. This heightens the rela-
girls and boys (in absolute numbers) are from LIMCs,79 tive neglect in attention to school-age nutritional focus,
thus representing a double burden of poor nutrition for particularly for the 5–10 year-old population.
the most populous countries in the world. The global rise in obesity related to socio-economic
The NCD RisC 2020 study80 showed that the differ- and other environmental changes, including changes in
ence between the highest mean BMI (eg, Pacific Island nutrition, contributes to increases and exacerbations of
countries, the United States, Chile, South Africa) and type 2 diabetes, cardiovascular disease, and other non-
lowest mean BMI (eg, India, Bangladesh, Ethiopia, and communicable diseases, exacerbating the double burden
Chad) was 9 kg/m2–10 kg/m2 in girls. Thus, the mean of disease and of cost to society. Prevention, starting
BMI difference, between these countries, was greater prenatally, remains the most cost-effective and realistic
than 2 standard deviations in BMI for a 15-year-old approach.84 So far, however, no clear or strong regional
girl. Trends by age varied significantly, and they wors- or national success stories have been demonstrated in
ened with age in many countries. In some countries (eg, the last decades.82
Mexico, South Africa, New Zealand), 5-year-old chil-
dren with healthy BMI progressively gained more in Micronutrient deficiencies
BMI than in height through the school-age years. Over
time, some countries showed too little height gain, and/ Micronutrient deficiencies continue to be considered a
or too much weight gain for height (eg, Sub-Saharan major contributor to the global burden of disease.
Africa, New Zealand, the United States, Malaysia, some Despite this, a recent global report confirms a persistent
Pacific Island nations, and Mexico), with some differen- and wide gap in data and information around micronu-
ces by sex. trient intake and nutrient status for all ages.85
In summary, though the landscape has changed sig- Individual deficiencies rarely occur in isolation. As for
nificantly in the last few decades, undernutrition (wast- other indicators of nutrition and health, some school-
ing/thinness/low BMI) and poor linear growth (low age micronutrient data is available for some nutrients,
height for age/stunting), as well as overnutrition (ele- and some are available from studies in adolescents and
vated BMI with or without low height), remain major young adults. Still, data in 5-year-old to 15-year-old
nutritional challenges globally. Today, still, despite the children is the least available across the board.
increase in overweight and obesity, more school-age Based on the high prevalence of their deficiencies,
children worldwide are moderately or severely under- WHO considers iron, vitamin A, vitamin D, zinc,
weight than overweight or obese. That said, in most iodine, and folate the most critical micronutrients glob-
countries, the prevalence increases in overweight and ally. It is estimated that 25% of school-age children
obesity are greater than the declines in prevalence of (around 305 million children) have anemia and that
underweight. So, if current trends continue globally, the 50% of it is primarily associated with iron deficiency.86
prevalence of obesity in school age will be higher than A 2004 report estimated the prevalence of vitamin A
that of moderate and severe underweight before 2025.80 deficiency in school-age children in South Asia to be
The considerable global differences in these 23.4% or 83 million children, 9 million of whom had
markers of nutritional adequacy reflect the geographic xerophthalmia.87 In low-income countries, vitamin A
and socio-economic gaps that also persist globally. deficiency prevalence has been estimated at 20% among
While genetics and other factors play a role, a difference early adolescent (10–14-year-old) girls and 18% among
of 20 cm in height and 9 kg/m2–10 kg/m2 in BMI late adolescent (15–19-year-old) girls.83 Worldwide,
between extremes in populations is a partial reflection inadequate zinc intake is estimated at around 17%, with
of the persistence of undernutrition and the large global little data disaggregated for school children,88 90% of
nutritional and environmental gaps. Lastly, a rapid which is in Africa and Asia.89 The prevalence of

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inadequate iodine intake in 6-year-old to 12-year-old Early attention to the significant effect of nutrition
school-age children has been estimated at around 30% until 2 years of age and the assertions, even until
(241 million children), ranging from 13% in the recently, that stunting and cognitive delays were irre-
Americas to 39% in Africa.90 Limited data on folate versible97,98 may have contributed to the lower attention
deficiency in females 12 years–49 years (reproductive to middle childhood and adolescence as opportunities
age) indicate a prevalence of more than 20% in lower- for recovery, particularly as related to stunting and cog-
income and less than 5% in higher-income countries. nitive deficits. Evidence today suggests this is not the
There are no good global estimates of folate deficiency case.
for school-age children.88,91 Catch-up growth through the school-age years is
In one report, vitamin D deficiency in 6-year-old to possible with the right interventions. Historical reports
12-year-old children ranged from 16% in North and observational studies of immigrant populations and
America, to 28% in Mexico, to 88% in China.92 For cal-

adopted children document that in situations where
cium, as opposed to most other nutrients where environmental and nutritional conditions change posi-
adequacy can be measured using biomarkers, there is tively, meaningful linear catch-up is possible.99
no universally accepted definition for deficiency. So Longitudinal observational data from the COHORT
dietary intake is used as the best proxy for adequacy. In multicounty study and longitudinal data from rural
addition, recommended intakes vary significantly by Gambia have shown that significant catch-up in height
regional or expert groups. For school-age children, can be achieved between 2 years of age and the end of
EFSA has stated a PRI of 800 mg/day for 4-year-olds to middle childhood (10 y of age), and between middle
10-year-olds and 1150 mg/day for 11-year-olds to childhood and adulthood, even in the absence of any
17 year-olds. The Institute of Medicine in the United nutrition or health interventions.2 Catch-up growth is
States has stated a recommended dietary allowance of also possible in chronic conditions, including celiac dis-
1000 mg/day for 4-year-olds to 8-year-olds and 1300 mg ease and inflammatory bowel disease, with the right
for 9-year-olds to 13-year-olds.55 While good estimates medical and nutritional interventions.100,101
are lacking, average calcium intake in the United States Although results are not always consistent, some lon-
for children 1 year to 14 years has been estimated at gitudinal studies that include school-age populations
between 856 mg/day and 993 mg/day, depending on (6 y–11 y old) show linear catch-up is possible with multi-
methodology, suggesting that many children fall below ple micronutrient supplementation.102,103 A recent sys-
recommendations. There are no good global estima- tematic review and meta-analysis of the effectiveness of
tions, but from the little data available, it is evident that several nutrition-based interventions after 2 years of age
the great majority of children in developing countries (where more than half of the studies included children
fall far below any current recommendations.93 older than 5 years of age) showed including supplementa-
Micronutrient deficiencies further compound the total tion of protein, vitamin A, and/or multiple micronu-
burden of poor nutrition, as they coexist with wasting trients, and particularly zinc supplementation, can
and obesity. improve linear growth, especially in children that have
experienced early stunting. However, supplementation of
RECOVERY FROM NUTRIENT DEFICIENCIES, GROWTH other micronutrients, including iodine, iron, calcium, or
FALTERING, AND COGNITION IN SCHOOL-AGE food-based interventions, did not significantly affect
CHILDREN growth, even if resolving anemia or other deficiencies.96
Although populations and methodologies vary,
Studies and systematic reviews of micronutrient supple- some studies have not found a correlation between lin-
mentation and fortification that include school-age chil- ear growth recovery and cognitive measures in short-
dren clearly show that micronutrient status can be term studies over 6 months,104 while others have. Data
improved. The demonstration of clinical effects, includ- from a longitudinal observational cohort in several
ing growth and morbidity, varies significantly. The best LMICs found that children who had stunting by 1 year
documented is iron supplementation and fortification, of age with linear growth catch-up by age 8 years had
which has been shown to improve iron status and significantly better cognitive outcomes than those who
reduce anemia in school-age children 5 years–12 years remained stunted.105 Height catch-up in these children
old.94 A positive effect of iron supplementation on cog- was positively associated with improvements in mathe-
nitive development has been shown, and interestingly, matics achievement, reading comprehension, and
effectiveness appears greater for children older than receptive vocabulary. Children who remained stunted
7 years than for younger ages.95 Other effects of micro- performed less well, and children who were never
nutrient supplementation, including growth and mor- stunted remained ahead of the other groups. A subse-
bidity, are less clear.81,96 quent study of the same cohort74 analyzed catch-up

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growth between the ages of 8 years and 15 years and levels and by multiple stakeholders—a discussion that is
showed that more than one third of those stunted at age beyond the scope of this review.
8 years caught up to their peers by age 15 years, and also
improved their cognitive scores compared with those REVISITING PRIORITIES
who did not catch up in height. Notably, linear growth
faltering was also accompanied by a decrease in cogni- Very recently, the last 4 years to 5 years have brought
tive outcomes in those children who became stunted about an increasing level of attention and calls for
between 8 years and 15 years. Thus, associations action to address the health and nutrition of middle
between linear growth and cognitive development vary childhood and adolescence. In 2017, Bundy et al pub-
from country to country and do not always persist from lished a comprehensive volume as part of the World
middle childhood through adolescence.74,106 The extent Bank’s Disease Control Priorities series, with support

of linear catch-up effect in various studies will vary from the Bill and Melinda Gates Foundation, highlight-
obviously due to the timing of the initial insult, the timing child and adolescent health, with a focus on ages
ing of the intervention, the duration of the intervention, 5 years–19 years, as “neglected potential” that needs to
and other environmental conditions beyond nutrition. be realized.1 They noted an “asymmetry between the
Given the obvious genetic, epigenetic, and environmen- public investment in formal education versus health
tal carryover between young mothers and their off- during the age range of 5 years–19 years, and a lack of
spring, it seems likely also that reversing the cycle of recognition that the developmental returns from educa-
undernutrition will probably require cross-generational tion are themselves dependent on concurrent good
catch-up.107 health and diet.” This “historical neglect of invest-
Inadequate bone mass and mineral accretion in ments. . . [beyond the first 1000 d], including the next
7000 days of middle childhood and adolescence. . . is
school-age children can have long-term consequences.
also reflected in investment in research into the older
While no good markers (except assessment of calcium
age-groups.”1
intake and vitamin D) are available, adequate intakes
Around this time, collaborative efforts in
remain important for reducing long-term risks. During
population-based studies are finally presenting a more
the school-age years, a higher milk intake is associated
comprehensive and clearer global picture of the nutri-
with higher BMC, BMD, and reduced fracture risk in
tional status of children above 5 years of age.79,80 Several
adulthood. Consuming less than one serving of milk a
research groups have reported on the significant poten-
day in childhood was associated with a 2-fold increase
tial that nutrition and health interventions have on
in fracture risk as adults.108 Establishing healthy dietary
improving outcomes during school age, thus constitut-
behaviors with a well-balanced diet that includes
ing a true (and possibly last) major window of opportu-
adequate calcium and vitamin D, particularly with nity for supporting adequate nutrition, overcoming
inclusion of dairy products and regular physical activity, deficits from earlier life, shaping future dietary behav-
can bring about long-term bone health. iors, and improving long-term health and well-being.2–5
Despite the limited knowledge we have, the nutri- Even more recently, UNICEF’s Nutrition Strategy
tional objectives for school-age children appear quite for 2020–2030 Framework called for “strategic shifts” in
clear: providing energy and protein adequacy (includ- upholding children’s right to nutrition and ending child
ing avoiding excesses), decreasing deficiencies of iron, malnutrition in all its forms (as part of the global
iodine, vitamin A, vitamin D, calcium, zinc, and folate, Sustainable Development Goals). The Strategy includes
and avoiding excesses of simple sugars and sodium. a comprehensive life cycle approach to nutrition pro-
Long-term studies are still lacking, and there appears to gramming, and maternal and child nutrition during the
be no “magic bullet” for improving dietary intakes and first 1000 days as core to UNICEF programs, and also
avoiding excesses. However, there is increasing evi- explicitly states that “nutrition during middle childhood
dence to support school dietary and physical activity– and adolescence is both a right and a window of oppor-
based interventions in schoolchildren to prevent defi- tunity for growth, development and learning, particu-
ciencies and address overweight and obesity.109–111 The larly for girls, and for breaking the intergenerational
school setting has excellent potential for providing a sig- cycle of malnutrition.” The 2 first measurable Results
nificant part of daily intake to improve diet quality tail- areas for the Strategy are 1. Early Childhood Nutrition
ored to the local environment and educate children in and 2. Nutrition in Middle Childhood and
nutrition and diet. The potential remains to be tapped. Adolescence.112 UNICEF’s Programmatic Guidance for
This can only be accomplished with adequate indi- Nutrition in Middle Childhood and Adolescence
vidual, community, and population education, as well includes specific priorities of nutritious foods, healthy
as policies that support these endeavours at multiple food environments in schools and beyond,

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839
Figure 4 The figure depicts key events in somatic and brain growth and development trajectories occurring in middle childhood
and early adolescence. The timing is meant to show sequence, and the ages are best approximations. Divergence relates to differences
between sexes. See text for related references. BMC: bone mineral content.
micronutrient supplementation and deworming, nutri- After the first 1000 days, the school-age years repre-
tion education in school curricula, and healthy dietary sent the most dynamic period of change in somatic and
practices for school-age children and adolescents.113 cognitive development before an individual reaches
While not neglecting early-life nutrition, a life- maturity, with multiple changes and inflection points in
cycle approach to nutrition requires increased attention growth and development trajectories. Figure 4 summa-
and a re-prioritization of middle childhood and early rizes key milestones in somatic and brain growth and
adolescence. The school-age years provide unique development and shows how “eventful” this life-cycle
opportunities that will need to be embraced, even more period truly is. Deficits in growth, bone health, cogni-
so now, given the added challenges placed on the world tive development, and alterations in body composition
by the recent COVID pandemic and climate change. during this period have a life-long impact. It is possible
and critical that we intervene during school age (a) to
maintain an adequate course of somatic and cognitive
CONCLUSION development and a bridge to adult life, (b) to correct
deficits of undernutrition and “catch-up” to the normal
Nutrition during the formative years remains the founda-
course of growth and development, and (c) to modulate
tion for long-term health and productivity of the individ- or mitigate inadequacies of overnutrition and avoid
uals who make up society. Of these formative years, the longer-term consequences. Middle childhood and ado-
first 5, with good reason, have received great attention lescence are thus a last major opportunity for invest-
over the last few decades. Decreasing infant mortality, ment, to affect growth, nutrition, and ultimate health
including the vicious cycle of undernutrition and disease, and cognitive outcomes.
and a better understanding of health and disease’s devel- Childhood education, the basis for societal develop-
opmental origins, have improved our focus and under- ment, is not possible without adequate nutrition. In
standing of the critical first few years of life. This, addition, child education and school systems themselves
however, was coupled with the poorly documented provide significant tangible opportunities for influenc-
notion that somatic and cognitive harm or delay in the ing dietary intake as well as for educating future genera-
first 2 years of life were irreversible, and hindered in part tions on diet and nutrition. Therefore, it is imperative
the attention given to the rest of childhood, particularly to improve our understanding of the opportunities pre-
middle childhood and early adolescence. Middle child- senting themselves during this period of life, and to
hood and early adolescence remain the most underrepre- develop policies and strategies to improve the current
sented of all life stages in health and nutrition research level of response to those opportunities. Only very
and clinical, nutritional, and epidemiologic data. recently has this understanding led to a revisiting of

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priorities in combating poor nutrition and its long-term 13. McDonagh JE; European Training Effective Care and Health Faculty. The age of
adolescence. . .and young adulthood. Lancet Child Adolesc Health. 2018;2:e6.
consequences. The emphasis on intervention during the 14. Cousminer DL, Berry DJ, Timpson NJ, et al.; The ReproGen Consortium. Genome-
school-age years needs to be nurtured and reinforced. wide association and longitudinal analyses reveal genetic loci linking pubertal
height growth, pubertal timing and childhood adiposity. Hum Mol Genet.
2013;22:2735–2747.
Acknowledgments 15. DelGiudice M. Middle childhood: an evolutionary–developmental synthesis. In:
Halfon N, Forrest CB, Lerner RM, Faustman EM, eds. Handbook of Life Course
Health Development. Cham (CH): Springer; 2017:95–107.
The authors would like to thank Dr Francois-Pierre 16. Reinehr T, Roth CL. Is there a causal relationship between obesity and puberty?
Lancet Child Adolesc Health. 2019;3:44–54.
Martin, Dr Laurence Donato-Capel, and Dr Marie- 17. Song Y, Ma J, Wang HJ, et al. Trends of age at menarche and association with
Claire Fichot for reviewing and providing valuable sug- body mass index in Chinese school-aged girls, 1985–2010. J Pediatr.
gestions regarding the manuscript. 2014;165:1172–1177.e1.
18. Goswami B, Roy AS, Dalui R, et al. Impact of pubertal growth on physical fitness.
Am J Sports Med. 2014;2:34–39.

Author contributions. All authors participated in the 19. USA Centers for Disease Control and Prevention (CDC): National Center for
Health Statistics. CDC Growth Charts. Available at: https://www.cdc.gov/growth-
planning, review, and final approval of the manuscript. charts/cdc_charts.htm. Accessed May 11, 2022.
The content is solely and entirely the work of the 20. Cole TJ. Children grow and horses race: is the adiposity rebound a critical period
for later obesity? BMC Pediatr. 2004;4:6.
authors. 21. Veldhuis JD, Roemmich JN, Richmond EJ, et al. Endocrine control of body com-
position in infancy, childhood, and puberty. Endocr Rev. 2005;26:114–146.
22. Webber CE, Barr RD. Age- and gender-dependent values of skeletal muscle mass
Funding. The collection of material for this manuscript in healthy children and adolescents. J Cachexia Sarcopenia Muscle. 2012;3:25–29.
was partially supported by the Societe des Produits 23. McCarthy HD, Samani-Radia D, Jebb SA, et al. Skeletal muscle mass reference
curves for children and adolescents. Pediatr Obes. 2014;9:249–259.
Nestle. 24. Tanner JM, Davies PS. Clinical longitudinal standards for height and height veloc-
ity for North American children. J Pediatr. 1985;107:317–329.
25. Nijjar JK, Stafford D. Undernutrition and growth in the developing world. Curr
Declaration of interest. J.M.S. is a consultant for Societe Opin Endocrinol Diabetes Obes. 2019;26:32–38.
des Produits Nestle, and Scaled Microbiomics. A.P. is a 26. Owino V, Ahmed T, Freemark M, et al. Environmental enteric dysfunction and
board member of the Nestle Nutrition Institute. growth failure/stunting in global child health. Pediatrics. 2016;138:e20160641.
27. Millward DJ. Nutrition, infection and stunting: the roles of deficiencies of individ-
ual nutrients and foods, and of inflammation, as determinants of reduced linear
growth of children. Nutr Res Rev. 2017;30:50–72.
28. Prendergast AJ, Humphrey JH. The stunting syndrome in developing countries.
REFERENCES Paediatr Int Child Health. 2014;34:250–265.
29. Baxter-Jones AD, Faulkner RA, Forwood MR, et al. Bone mineral accrual from 8 to
1. Bundy DAP, Silva ND, Horton AP, et al. Child and adolescent health and develop- 30 years of age: an estimation of peak bone mass. J Bone Miner Res.
ment: realizing neglected potential. In: Bundy DAP, Silva ND, Horton S, Jamison 2011;26:1729–1739.
DT, Patton GC, eds. Child and Adolescent Health and Development. 3rd ed. 30. Maggioli C, Stagi S. Bone modeling, remodeling, and skeletal health in children
Washington, DC: The International Bank for Reconstruction and Development/ and adolescents: mineral accrual, assessment and treatment. Ann Pediatr
the World Bank; 2017:1–23. Endocrinol Metab. 2017;22:1–5.
2. Prentice AM, Ward KA, Goldberg GR, et al. Critical windows for nutritional inter- 31. Golden NH, Abrams SA; Committee on Nutrition. Optimizing bone health in chil-
ventions against stunting. Am J Clin Nutr. 2013;97:911–918. dren and adolescents. Pediatrics. 2014;134:e1229–e1243.
3. Best C, Neufingerl N, van Geel L, et al. The nutritional status of school-aged chil- 32. Ralston SH, de Crombrugghe B. Genetic regulation of bone mass and susceptibil-
dren: why should we care? Food Nutr Bull. 2010;31:400–417. ity to osteoporosis. Genes Dev. 2006;20:2492–2506.
4. Akseer N, Al-Gashm S, Mehta S, et al. Global and regional trends in the nutri- 33. Weaver CM, Gordon CM, Janz KF, et al. The National Osteoporosis Foundation’s
tional status of young people: a critical and neglected age group [published cor- position statement on peak bone mass development and lifestyle factors: a sys-
rection appears in Ann N Y Acad Sci. 2017;1396(1):236]. Ann NY Acad Sci. tematic review and implementation recommendations [published correction
2017;1393:3–20. appears in Osteoporos Int. 2016;27(4):1387]. Osteoporos Int. 2016;27:1281–1386.
5. Georgiadis A, Penny ME. Child undernutrition: opportunities beyond the first 34. Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev.
1000 days. Lancet Public Health. 2017;2:e399. 2010;20:327–348.
6. Bundy DAP, de Silva N, Horton S, et al. Annex 1A. Supplemental material. In: 35. Konrad K, Firk C, Uhlhaas PJ. Brain development during adolescence: neuroscien-
Bundy DAP, Silva ND, Horton S, Jamison DT, Patton GC, eds. Child and Adolescent tific insights into this developmental period. Dtsch Arztebl Int. 2013;110:425–431.
Health and Development. 3rd ed. Washington, DC: The International Bank for 36. Mills KL, Goddings AL, Herting MM, et al. Structural brain development between
Reconstruction and Development/the World Bank; 2017:1. Available at: http:// childhood and adulthood: convergence across four longitudinal samples.
www.dcp-3.org/chapter/2754/annexes. Accessed May 11, 2022. Neuroimage. 2016;141:273–281.
7. WHO. UNICEF, World Bank, and the Demographic and Health Surveys (DHS)/ 37. Lenroot RK, Giedd JN. Brain development in children and adolescents: insights
USAID database. 2021. Available at: https://dhsprogram.com/data/. Accessed from anatomical magnetic resonance imaging. Neurosci Biobehav Rev.
May 11, 2022. 2006;30:718–729.
8. Galloway R. Global nutrition outcomes at ages 5 to 19. In: Bundy DAP, Silva ND, 38. Peterson MR, Cherukuri V, Paulson JN, et al. Normal childhood brain growth and
Horton S, Jamison DT, Patton GC, eds. Child and Adolescent Health and a universal sex and anthropomorphic relationship to cerebrospinal fluid. J
Development. 3rd ed. Washington, DC: The International Bank for Reconstruction Neurosurg Pediatr. 2021;28:458–468.
and Development/the World Bank; 2017:37–45. 39. De Bellis MD, Keshavan MS, Beers SR, et al. Sex differences in brain maturation
9. Sawyer SM, Azzopardi PS, Wickremarathne D, et al. The age of adolescence. during childhood and adolescence. Cereb Cortex. 2001;11:552–557.
Lancet Child Adolesc Health. 2018;2:223–228. 40. Johnson SB, Blum RW, Giedd JN. Adolescent maturity and the brain: the promise
10. Alderman H, Behrman JR, Glewwe P, et al. Evidence of impact of interventions and pitfalls of neuroscience research in adolescent health policy. J Adolesc
on growth and development during early and middle childhood. In: Bundy DAP, Health. 2009;45:216–221.
Silva ND, Horton S, Jamison DT, Patton GC, eds. Child and Adolescent Health and 41. Immordino-Yang MH, Darling-Hammond L, Krone C. The Brain Basis for
Development. 3rd ed. Washington, DC: The International Bank for Reconstruction Integrated Social, Emotional, and Academic Development. How emotions and
and Development/the World Bank; 2017:79–98. social relationships drive learning. Washington, DC: The Aspen Institute National
11. United Nations Children’s Fund (UNICEF). Convention on the Rights of the Child. Commission on Social, Emotional, and Academic Development. 2018. Available
1990. Available at: https://www.unicef.org/child-rights-convention/convention- at: https://www.aspeninstitute.org/publications. Accessed May 11, 2022.
text. Accessed May 11, 2022. 42. Dumontheil I. Development of abstract thinking during childhood and adoles-
12. Patton GC, Sawyer SM, Santelli JS, et al. Our future: a Lancet commission on ado- cence: the role of rostrolateral prefrontal cortex. Dev Cogn Neurosci.
lescent health and wellbeing. Lancet. 2016;387:2423–2478. 2014;10:57–76.

R
841
43. Flege JE, Munro MJ, MacKay IR. Factors affecting strength of perceived foreign 75. Caleyachetty R, Thomas GN, Kengne AP, et al. The double burden of malnutrition
accent in a second language. J Acoust Soc Am. 1995;97:3125–3134. among adolescents: analysis of data from the Global School-Based Student
44. Giedd JN, Blumenthal J, Jeffries NO, et al. Brain development during childhood Health and Health Behavior in School-Aged Children surveys in 57 low- and
and adolescence: a longitudinal MRI study. Nat Neurosci. 1999;2:861–863. middle-income countries. Am J Clin Nutr. 2018;108:414–424.
45. Diamond A. Executive functions. Handb Clin Neurol. 2020;173:225–240. 76. Schott W, Aurino E, Penny ME, et al. The double burden of malnutrition among
46. Anderson P. Assessment and development of executive function (EF) during youth: trajectories and inequalities in four emerging economies. Econ Hum Biol.
childhood. Child Neuropsychol. 2002;8:71–82. 2019;34:80–91.
47. Spear LP. Adolescent neurodevelopment. J Adolesc Health. 2013;52:S7–S13. 77. Andersen CT, Stein AD, Reynolds SA, et al. Stunting in infancy is associated with
48. Mills KL, Goddings AL, Clasen LS, et al. The developmental mismatch in structural decreased risk of high body mass index for age at 8 and 12 years of age. J Nutr.
brain maturation during adolescence. Dev Neurosci. 2014;36:147–160. 2016;146:2296–2303.
49. Kelley JC, Crabtree N, Zemel BS. Bone density in the obese child: clinical consid- 78. World Health Organization. Noncommunicable Disease Surveillance, Monitoring
erations and diagnostic challenges. Calcif Tissue Int. 2017;100:514–527. and Reporting. Global School-based Student Health Survey. Available at: https://
50. Das JK, Salam RA, Thornburg KL, et al. Nutrition in adolescents: physiology, www.who.int/teams/noncommunicable-diseases/surveillance/systems-tools/
metabolism, and nutritional needs. Ann N Y Acad Sci. 2017;1393:21–33. global-school-based-student-health-survey. Accessed May 11, 2022.
51. Trumbo P, Schlicker S, Yates AA, et al.; Food and Nutrition Board of the Institute 79. NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in body–mass
of Medicine, The National Academies. Dietary reference intakes for energy, car- index, underweight, overweight, and obesity from 1975 to 2016: a pooled analy-

bohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids [published sis of 2416 population-based measurement studies in 1289 million children,
correction appears in J Am Diet Assoc. 2003;103(5):563]. J Am Diet Assoc. adolescents, and adults. Lancet. 2017;390:2627–2642.
2002;102:1621–1630. 80. NCD Risk Factor Collaboration (NCD-RisC). Height and body–mass index trajecto-
52. Chugani HT. Positron emission tomography scanning: applications in newborns. ries of school-aged children and adolescents from 1985 to 2019 in 200 countries
Clin Perinatol. 1993;20:395–409. and territories: a pooled analysis of 2181 population-based studies with 65 mil-
53. Grande Covian F. El metabolismo energetico del cerebro en la infancia [Energy lion participants. Lancet. 2020;396:1511–1524.
metabolism of the brain in children (author’s transl)]. An Esp Pediatr. 81. Best C, Neufingerl N, Del Rosso JM, et al. Can multi-micronutrient food fortifica-
1979;12:235–244. tion improve the micronutrient status, growth, health, and cognition of school-
54. Kalhan SC, Kiliç I. Carbohydrate as nutrient in the infant and child: range of
children? A systematic review. Nutr Rev. 2011;69:186–204.
acceptable intake. Eur J Clin Nutr. 1999;53(suppl 1):S94–S100.
82. Ng M, Fleming T, Robinson M, et al. Global, regional, and national prevalence of
55. European Food Safety Authority (EFSA). Overview on Dietary Reference Values
overweight and obesity in children and adults during 1980–2013: a systematic
for the EU population as derived by the EFSA Panel on Dietetic Products,
analysis for the Global Burden of Disease Study 2013 [published correction
Nutrition and Allergies (NDA). Summary of Dietary Reference Values – version 4.
appears in Lancet. 2014;384(9945):746]. Lancet. 2014;384:766–781.
September 2017. Available at: https://www.efsa.europa.eu/en/topics/topic/diet-
83. Christian P, Smith ER. Adolescent undernutrition: global burden, physiology, and
ary-reference-values. Accessed May 11, 2022.
nutritional risks. Ann Nutr Metab. 2018;72:316–328.
56. Branca F, Vatue~na S. Calcium, physical activity and bone health–building bones
84. Darnton-Hill I, Nishida C, James WP. A life course approach to diet, nutrition and
for a stronger future. Public Health Nutr. 2001;4:117–123.
the prevention of chronic diseases. Public Health Nutr. 2004;7:101–121.
57. Heaney RP, Abrams S, Dawson-Hughes B, et al. Peak bone mass. Osteoporos Int.
85. McLean E, Cogswell M, Egli I, et al. Global Nutrition Report. Chapter 3.
2000;11:985–1009.
Development Initiatives Poverty Research Ltd 2018. 2018. https://globalnutri-
58. Sarafrazi N, Wambogo EA, Shepherd JA. Osteoporosis or low bone mass in older
tionreport.org/reports/global-nutrition-report-2018/. Accessed May 11, 2022.
adults: United States, 2017–2018. NCHS Data Brief. 2021;(405):1–8.
86. McLean E, Cogswell M, Egli I, et al. Worldwide prevalence of anaemia, WHO
59. Fragility Fractures - Epidemiology. Nyon, Switzerland: International Osteoporosis
Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health
Foundation; 2021. Available at: https://www.osteoporosis.foundation/health-pro-
Nutr. 2009;12:444–454.
fessionals/fragility-fractures/epidemiology. Accessed May 11, 2022.
87. Singh V, West KP Jr. Vitamin A deficiency and xerophthalmia among school-
60. Prentice A, Schoenmakers I, Laskey MA, et al. Nutrition and bone growth and
aged children in Southeastern Asia. Eur J Clin Nutr. 2004;58:1342–1349.
development. Proc Nutr Soc. 2006;65:348–360.
88. Bailey RL, West KP Jr, Black RE. The epidemiology of global micronutrient defi-
61. Georgieff MK, Ramel SE, Cusick SE. Nutritional influences on brain development.
Acta Paediatr. 2018;107:1310–1321. ciencies. Ann Nutr Metab. 2015;66:22–33.
62. GBD 2019 Risk Factors Collaborators. Global burden of 87 risk factors in 204 89. Kumssa DB, Joy EJ, Ander EL, et al. Dietary calcium and zinc deficiency risks are
countries and territories, 1990–2019: a systematic analysis for the Global Burden decreasing but remain prevalent. Sci Rep. 2015;5:10974.
90. Andersson M, Takkouche B, Egli I, et al. Current global iodine status and progress
of Disease Study 2019. Lancet 2020;396:1223–1249.
63. Camaschella C. Iron deficiency. Blood 2019;133:30–39. over the last decade towards the elimination of iodine deficiency. Bull World
64. Pivina L, Semenova Y, Doşa MD, et al. Iron deficiency, cognitive functions, and Health Organ. 2005;83:518–525.
neurobehavioral disorders in children. J Mol Neurosci. 2019;68:1–10. 91. Rogers LM, Cordero AM, Pfeiffer CM, et al. Global folate status in women of
65. Lozoff B. Iron deficiency and child development. Food Nutr Bull. reproductive age: a systematic review with emphasis on methodological issues.
2007;28:S560–S571. Ann NY Acad Sci. 2018;1431:35–57.
66. Larson LM, Phiri KS, Pasricha SR. Iron and cognitive development: what is the evi- 92. Palacios C, Gonzalez L. Is vitamin D deficiency a major global public health prob-
dence? Ann Nutr Metab. 2017;71(suppl 3):25–38. lem? J Steroid Biochem Mol Biol. 2014;144(Pt A):138–145.
67. Briend A, Khara T, Dolan C. Wasting and stunting—similarities and differences: 93. Pettifor JM. Calcium and vitamin D metabolism in children in developing coun-
policy and programmatic implications. Food Nutr Bull. 2015;36:S15–S23. tries. Ann Nutr Metab. 2014;64(suppl 2):15–22.
68. Schoenbuchner SM, Dolan C, Mwangome M, et al. The relationship between 94. De-Regil LM, Jefferds ME, Sylvetsky AC, et al. Intermittent iron supplementation
wasting and stunting: a retrospective cohort analysis of longitudinal data in for improving nutrition and development in children under 12 years of age.
Gambian children from 1976 to 2016. Am J Clin Nutr. 2019;110:498–507. Cochrane Database Syst Rev 2011;2011:CD009085.
69. Fernald LCG, Prado E, Kariger P, et al. A Toolkit for Measuring Early Childhood 95. Sachdev H, Gera T, Nestel P. Effect of iron supplementation on mental and motor
Development in Low and Middle-Income Countries. 2017 International Bank for development in children: systematic review of randomised controlled trials.
Reconstruction and Development, The World Bank, Washington DC. License: CC Public Health Nutr. 2005;8:117–132.
BY 3.0 IGO. Available at: https://openknowledge.worldbank.org/handle/10986/ 96. Roberts JL, Stein AD. The impact of nutritional interventions beyond the first 2
29000. Accessed May 11, 2022. years of life on linear growth: a systematic review and meta-analysis. Adv Nutr.
70. Crookston BT, Penny ME, Alder SC, et al. Children who recover from early stunt- 2017;8:323–336.
ing and children who are not stunted demonstrate similar levels of cognition. J 97. Martorell R, Khan LK, Schroeder DG. Reversibility of stunting: epidemiological
Nutr. 2010;140:1996–2001. findings in children from developing countries. Eur J Clin Nutr. 1994;48(suppl
71. Sudfeld CR, McCoy DC, Danaei G, et al. Linear growth and child development in 1):S45–S57.
low- and middle-income countries: a meta-analysis. Pediatrics. 98. Victora CG, Adair L, Fall C, et al. Maternal and child undernutrition: consequences
2015;135:e1266–e1275. for adult health and human capital [published correction appears in Lancet.
72. Walker SP, Chang SM, Powell CA, et al. Early childhood stunting is associated 2008;371(9609):302]. Lancet. 2008;371:340–357.
with poor psychological functioning in late adolescence and effects are reduced 99. Watkins KL, Bundy DAP, Jamison DT, et al. Evidence of impact of interventions
by psychosocial stimulation. J Nutr. 2007;137:2464–2469. on health and development during middle childhood and school age. In: Bundy
73. Sanchez A. The structural relationship between early nutrition, cognitive skills DAP, Silva ND, Horton S, Jamison DT, Patton GC, eds. Child and Adolescent Health
and non-cognitive skills in four developing countries. Econ Hum Biol. and Development. 3rd ed. Washington, DC: The International Bank for
2017;27:33–54. Reconstruction and Development/the World Bank; 2017:99–105.
74. Fink G, Rockers PC. Childhood growth, schooling, and cognitive development: 100. Gasparetto M, Guariso G. Crohn’s disease and growth deficiency in children and
further evidence from the Young Lives study. Am J Clin Nutr. 2014;100:182–188. adolescents. World J Gastroenterol. 2014;20:13219–13233.

R
101. Boersma B, Houwen RH, Blum WF, et al. Catch-up growth and endocrine 109. Jacob CM, Hardy-Johnson PL, Inskip HM, et al. A systematic review and meta-
changes in childhood celiac disease. Endocrine changes during catch-up growth. analysis of school-based interventions with health education to reduce body
Horm Res. 2002;58(suppl 1):57–65. mass index in adolescents aged 10 to 19 years. Int J Behav Nutr Phys Act.
102. Abrams SA, Mushi A, Hilmers DC, et al. A multinutrient-fortified beverage enhan- 2021;18:1.
ces the nutritional status of children in Botswana. J Nutr. 2003;133:1834–1840. 110. Singhal J, Herd C, Adab P, et al. Effectiveness of school-based interventions to
103. Ash DM, Tatala SR, Frongillo EA Jr, et al. Randomized efficacy trial of a prevent obesity among children aged 4 to 12 years old in middle-income coun-
micronutrient-fortified beverage in primary school children in Tanzania. Am J tries: a systematic review and meta-analysis. Obes Rev. 2021;22:e13105.
Clin Nutr. 2003;77:891–898. 111. Kyere P, Veerman JL, Lee P, et al. Effectiveness of school-based nutrition inter-
104. Sokolovic N, Selvam S, Srinivasan K, et al. Catch-up growth does not associate ventions in sub-Saharan Africa: a systematic review. Public Health Nutr.
with cognitive development in Indian school-age children. Eur J Clin Nutr. 2020;23:2626–2636.
2014;68:14–18. 112. United Nations Children’s Fund (UNICEF). Nutrition, for Every Child: UNICEF
105. Crookston BT, Schott W, Cueto S, et al. Postinfancy growth, schooling, and cogni- Nutrition Strategy 2020–2030. New York: UNICEF. 2020. Available at: https://
tive achievement: young lives. Am J Clin Nutr. 2013;98:1555–1563. www.unicef.org/media/92031/file/UNICEF%20Nutrition%20Strategy%202020-
106. Georgiadis A, Benny L, Duc LT, et al. Growth recovery and faltering through early 2030.pdf. Accessed May 11, 2022.
adolescence in low- and middle-income countries: determinants and implica- 113. United Nations Children’s Fund (UNICEF). Programming Guidance: Nutrition in
tions for cognitive development. Soc Sci Med. 2017;179:81–90. Middle Childhood and Adolescence. New York, NY: UNICEF. 2021. Available at:
107. Golden MH. Is complete catch-up possible for stunted malnourished children? https://www.unicef.org/media/106406/file. Accessed May 11, 2022.

Eur J Clin Nutr. 1994;48(suppl 1):S58–S70; discussion S71. 114. Tapert SF, Schweinsburg AD. The human adolescent brain and alcohol use disor-
108. Kalkwarf HJ, Khoury JC, Lanphear BP. Milk intake during childhood and adoles- ders. Recent Dev Alcohol. 2005;17:177–197.
cence, adult bone density, and osteoporotic fractures in US women. Am J Clin 115. Lee FS, Heimer H, Giedd JN, et al. Mental health. Adolescent mental health—
Nutr. 2003;77:257–265. opportunity and obligation. Science. 2014;346:547–549.

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Narrative Review

Nutrition in school-age children: a rationale for revisiting

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