Systematic Review

Role of diet quality in bone health in children and adolescents:

a systematic review
Lara Gomes Suhett , Mariana De Santis Filgueiras , Juliana Farias de Novaes , and
Deeptha Sukumar

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Context: Poor diet quality and unhealthy dietary patterns have been linked to
poor bone health, yet few studies have investigated the role of diet quality in bone
health in pediatric populations. Objective: This systematic review aims to assess
the available evidence on the association between diet quality and bone health
markers in children and adolescents. Data Sources: The PubMed, Scopus, and
Virtual Health Library databases were searched electronically from October to
November 2022, without any restrictions on date or language. The STROBE
(Strengthening the Reporting of Observational Studies in Epidemiology) checklist
was used to assess the quality of the studies. Data Extraction: Published observa-
tional studies in children and adolescents (ages 2 to 19 years) that investigated the
association between diet quality and bone health were eligible for inclusion. Two
researchers independently analyzed and selected all articles using the Rayyan app.
Initially, 965 papers were identified. A total of 12 observational studies qualified,
including 8 cross-sectional and 4 longitudinal studies. The sample comprised
7130 individuals aged 3 to 17.9 years, representing both sexes. Bone health
was evaluated by measures of bone mineral density and bone mineral content.
Data Analysis: Seven studies (58.3%) showed significant associations between
diet quality and bone health markers, all of which evaluated diet quality by identi-
fying dietary patterns. Diet quality as evaluated by all dietary indexes was not asso-
ciated with bone health markers. Conclusions: Adherence to a healthy diet may
benefit bone health in children and adolescents. These findings emphasize the
importance of developing effective public health policies that encourage healthy
eating habits from childhood to preserve bone health. Longitudinal research
using a specific tool to assess diet quality in relation to bone health is warranted.
Future studies should also measure bone-regulating hormones and markers of
bone turnover.
Systematic Review Registration: PROSPERO registration no. CRD42022368610.

Affiliation: L.G. Suhett and D. Sukumar are with the Department of Nutrition Sciences, Drexel University, Philadelphia, Pennsylvania, USA.
M. De Santis Filgueiras and J.F. de Novaes are with the Department of Nutrition and Health, Universidade Federal de Vicosa, Vicosa, Minas
Gerais, Brazil.
Correspondence: D. Sukumar, Department of Nutrition Sciences, Drexel University, 11W33, HSB Building, 60 N 36 St, Philadelphia, PA,
19104, USA. E-mail: [email protected].
Key words: bones, childhood, dietary patterns, eating habits, nutritional epidemiology
C The Author(s) 2023. Published by Oxford University Press on behalf of the International Life Sciences Institute.
V
All rights reserved. For permissions, please e-mail: [email protected].

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 INTRODUCTION carbohydrates, has been related to worse bone health.8
However, the relationship between these dietary pat-
The skeleton is an active organ in constant remodeling, terns and bone health in children and adolescents is still
which is regulated by cytokines and circulating hor- not well established, and thus the effects of overall diet
mones such as parathyroid hormone and 1,25-dihy- quality in this population require further investigation.
droxyvitamin D [1,25(OH)2D].1 Osteoporosis, which The infant and juvenile phases of human life are
occurs frequently in older people, may have its roots in conducive to nutritional strategies that promote optimal
childhood, as bone mass gained early in life may be the diet quality, since eating habits are shaped during these
most important modifiable determinant of skeletal

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periods. For this reason, understanding the relationship
health throughout life.2 Childhood and adolescence are between diet and bone health at early ages can guide
critical phases for bone mineralization. It is estimated actions to prevent bone diseases and their comorbidities
that 40% to 60% of adult bone mass is accrued during later in life. Thus, the aim of this systematic review was
adolescence,1 with the peak bone accretion rate occur- to assess the available evidence on the association
ring at 12.5 years in girls and 14 years in boys.3 Thus, between diet quality and bone health markers in chil-
understanding the regulation of bone health in the dren and adolescents. The hypothesis is that a healthier
pediatric population can be crucial for preserving opti- diet is related to a better profile of bone health markers
mal bone health in later life cycles.4 in early ages.
Bone health is widely assessed by imaging scans,
such as dual-energy X-ray absorptiometry, which pro- METHODS
vides information on bone mineral content (BMC) and
bone mineral density (BMD), both markers of long- Study identification and selection
term bone status.5 On the other hand, circulating bone
turnover markers, such as osteocalcin, C- and N-termi- This systematic review aimed to answer the following
nal telopeptides of type I collagen, which are released by research question: “Does diet quality play an important
osteoblasts or osteoclasts, are current-phase biomarkers role in bone health in children and adolescents?” The
of bone turnover.6 Markers of bone turnover may be PICOS (Population, Intervention/exposure, Comparator,
useful in predicting bone loss and fracture risk and in Outcomes, and Study design) framework was used to
monitoring osteoporosis.6 determine the eligibility of studies (Table 1). The review
Modifiable determinants, such as nutrition and was performed in accordance with the PRISMA
physical activity, have synergistic effects to improve and (Preferred Reporting Items for Systematic Reviews and
maintain bone health in the pediatric population.7 The Meta-Analyses) guidelines updated in 20209 (see Tables S1
dietary intake of protein, calcium, and vitamin D, as and S2 in the Supporting Information online) and is regis-
well as their food sources, is paramount for bone tered in PROSPERO (registration no. CRD42022368610).
health.8 Protein intake contributes to the production of The literature search was conducted from October to
insulin-like growth factor-1, which regulates renal phos- November 2022 in the following electronic databases:
phate reabsorption and promotes the active uptake of PubMed, Scopus, and Virtual Health Library. No restric-
calcium and phosphate from the intestine and, conse- tions on date or language were imposed. The following
quently, the renal synthesis of 1,25-dihydroxyvitamin MeSH (Medical Subject Headings) descriptors and key-
D3.8 Calcium plays a role in bone rigidity, and its low words related to the topic were used: ([“bone mass” OR
intake is related to increased bone remodeling through “bone mineral density” OR “bone mineral content” OR
secondary hyperparathyroidism.8 Vitamin D deficiency “bone marker” OR “bone turnover” OR “bone regulating
is associated with rickets in children or osteomalacia in
adults. The active vitamin D metabolite, 1,25-dihydrox- Table 1 PICOS criteria for inclusion of studies
yvitamin D3, increases the intestinal absorption of cal- Parameter Criteria
cium and phosphate.8 Although the importance of these Population Children and adolescents
nutrients is well known, it is necessary to understand Intervention/exposure Unhealthy diet quality
the role of diet in bone health, as assessed through diet- Comparator Healthy diet quality
ary patterns, scores, or indexes, to gain insight about Outcomes Bone health markers (BMD, BMC, bone
mass, c-BUA, fracture risk, bone-reg-
the holistic effect of diet quality on bone health. ulating hormones, or bone turnover
Dietary patterns such as vegetarian and vegan diets, markers)
the Mediterranean diet, and the prudent diet, are Study design Observational and longitudinal studies
related to improved bone health profiles.8 In addition, (cross-sectional, cohort, and case-
control)
the increased consumption of energy-dense foods, par- Abbreviations: BMC, bone mineral content; BMD, bone mineral
ticularly saturated fats, sugars, and other refined density, c-BUA, calcaneal broadband ultrasound attenuation.

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Figure 1 Flow diagram of the literature search process.

hormones” OR “bone health” OR “osteoporosis” OR bone-regulating hormones, bone loss, bone diseases, or
“rickets” OR “osteopenia” OR “bone loss” OR “fracture”] fracture risk) were eligible for inclusion.Studies in
AND [“diet quality” OR “dietary quality” OR “dietary infants, adults, pregnant women, elderly persons, or
pattern” OR “food intake” OR “food consumption” OR animals were excluded, as were in vitro experiments
“food groups”] AND [“child” OR “adolescent”]). and papers that did not meet the inclusion criteria (did
The protocol for the identification and selection of not evaluate diet quality; evaluated only the intake of
original articles is shown in Figure 1. Two researchers nutrients, specific foods, or food groups; assessed cardi-
(L.G.S. and M.S.F.) independently analyzed and selected ometabolic health or other chronic diseases instead of
all articles using the free Rayyan app (http://rayyan.qcri. bone health). Reviews, book chapters, abstracts, ency-
org).10 Any conflicts about selection results were dis- clopedias, case reports, guidelines, editorials, gray litera-
cussed until consensus was reached. ture, theses and dissertations, and publications whose
full texts were not available were also excluded.
Eligibility criteria
Data extraction
Published observational studies in children and adoles-
cents (ages 2 to 19 years) that investigated the associa- The following information from the selected papers was
tion between diet quality and bone health (as assessed gathered and computed in an Excel spreadsheet:
by bone mass, BMD, BMC, bone turnover markers, authorship; year of publication; country; name of the

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study; study design; sample data (size, age, and sex); questionnaire21 to evaluate adherence to the
method used to assess diet quality; diet quality variables; Mediterranean diet. Seven studies evaluated diet quality
bone variables; main statistical analyses; adjustment through the identification of dietary patterns. The most
variables; main results; statistically significant result common methods of diet quality assessment used were
(yes/no). principal component factor analysis (n ¼ 2) and
reduced rank regression (n ¼ 2). In addition, 5 studies
Assessment of study quality also evaluated diet quality using dietary indexes, such as
the German Bone Healthy Eating Index, the

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The STROBE (Strengthening the Reporting of Mediterranean diet score, the Diet Quality Index for
Observational Studies in Epidemiology) checklist11 was Adolescents, the Dietary Approaches to Stop
used to assess the quality of all selected papers. Two Hypertension (DASH) diet index, and the Oslo Health
reviewers (L.G.S. and M.S.F.) analyzed the overall qual- Study dietary index.
ity of the papers individually by attributing 1 point for
each item on the checklist covered by the study. Each Bone health assessment
paper received a score that ranged between 0 and 22
points. The difference between the scores given by the Studies used dual-energy X-ray absorptiometry (n ¼ 9)
reviewers could not be greater than 1 point. The average or an ultrasound densitometer (n ¼ 3) to examine the
of the scores for all 22 items was calculated and pre- bones of children and adolescents. Almost all studies
sented as a percentage. used BMD and BMC (n ¼ 10) as markers of bone
health. Other bone markers were bone mass (n ¼ 2),
RESULTS calcaneal broadband ultrasound attenuation (n ¼ 1),
and risk of fracture using the speed of sound (m/s)
Study selection (n ¼ 1). None of the studies evaluated bone-regulating
hormones or markers of bone turnover.
Initially, 965 papers were identified, of which 304 were
duplicates. After removal of duplicates, 661 papers were Statistical analysis and adjustment variables
evaluated through title and abstract screening. After the
exclusion of 649 records, 12 papers that met the inclu- To examine the association between diet quality and
sion criteria were included in the present review markers of bone health, studies employed multiple lin-
(Figure 1). Studies were carried out in China (n ¼ 2), ear regression (n ¼ 8) or multiple logistic regression
Germany (n ¼ 1), Spain (n ¼ 2), Canada (n ¼ 1), (n ¼ 4), adjusted by potential confounding factors such
Colombia (n ¼ 1), Portugal (n ¼ 2), Korea (n ¼ 2), and as age, age of peak height velocity, sex, race, height,
the United States (n ¼ 1). All were observational studies weight, weight-loss attempts, body mass index, physical
carried out in children and adolescents of both sexes; 8 activity, accelerometer counts per minute, television-
were cross-sectional and 4 were cohorts. The sample viewing time, outdoor playtime, study location, house-
comprised 7130 individuals in total, with the sample hold income, parental education, passive smoking,
size of individual studies ranging from 125 to 1590. alcohol drinking, energy intake, protein intake, calcium
Participants ranged in age from 3 to 17.9 years, and intake, vitamin D intake, supplemental intake of cal-
4181 (58.64%) were girls (Table 212–23). Other charac- cium, supplemental intake of multivitamins, fat-free
teristics, such as authorship, publication year, methods mass, lean mass, Tanner stage, age at menarche, and
of assessing food intake and bone health markers, and pubertal status (Table 3).
exposure and outcome variables, are described in
Table 2. Table 312–23 shows the statistical analyses, Diet quality and markers of bone health
adjustment variables, main results, and STROBE scores.
Figure 2 shows the dietary patterns and diet quality Most of the studies showed significant associations
indexes associated with markers of bone health in chil- between diet quality and bone health in childhood
dren and adolescents identified in this review. (n ¼ 7), all of which evaluated diet quality by identifying
dietary patterns.12–18 A recent cross-sectional study
Diet quality assessment conducted in China in 465 children aged 6 to 9 years
observed that the “fruit–milk–eggs” dietary pattern was
The studies used food frequency questionnaires (n ¼ 5) positively associated with total body BMC (b ¼ 10.480;
or 24-hour dietary recalls (n ¼ 3) to identify dietary pat- 95%CI, 2.190–18.770) and total body less head BMC
terns and calculate dietary indexes for the evaluation of (b ¼ 5.577; 95%CI, 0.214–10.941), while the “animal
diet quality. Only two studies applied the KIDMED organs–refined cereals” pattern was associated with low

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Table 2 Characteristics of the studies included in the systematic review

Reference Country Study design Sample Method of assessing dietary Diet quality (exposure) Method of assessing Markers of bone health
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of study characteristics intake markers of bone (outcome)

(size, sex, age) health
Liao et al (2022)12 China Cross-sectional n ¼ 465 FFQ Vegetables-whole grains-red DXA Total body BMC and BMD,
200 girls Dietary patterns by principal meat and total body less head
265 boys component factor analysis Fruit-milk-eggs BMC and BMD
6–9 y Seafood-mushrooms-nuts
Beverages-fish-low-fat milk
Animal organs-refined cereals
Heydenreich et al Germany Cross-sectional n ¼ 486 Adapted FFQ German Bone Healthy Eating Quantitative ultra- Bone mass (stiffness index)
(2020)19 248 girls Index sound
13.4 6 1.9 y measurements
231 boys DXA
13.6 6 1.7 y
Mun~oz-Hernandez Spain Cross-sectional n ¼ 177 KIDMED questionnaire Mediterranean diet DXA Total body aBMC and BMD,
et al (2018)21 80 girls total body less head aBMC
97 boys and BMD, and upper limbs
8–12 y aBMC and BMD
Movassagh et al Canada Cross-sectional n ¼ 125 24-h recalls Vegetarian DXA Total body, femoral neck,
(2018)13 53 girls Dietary patterns by principal Western and lumbar spine BMC and
72 boys component factor analysis High-fat, high-protein aBMD measures
12.7 6 2 y Mixed
Snack
Julian et al (2018)20 Spain Cross-sectional n ¼ 179 24-h recalls and HELENA- Mediterranean Diet Score for DXA Total body less head, femoral
90 girls Dietary Intake Assessment Adolescents and the Diet neck, lumbar spine, and
89 boys Tool Quality Index for hip BMC measures
14.7 6 1.3 y Adolescents
Forero-Bogota et al Colombia Cross-sectional n ¼ 1118 KIDMED questionnaire Mediterranean diet Achilles ultrasound c-BUA
(2017)22 610 girls densitometer
508 boys
9–17.9 y
Yang et al (2016)14 China Cross-sectional n ¼ 1590 FFQ Western-type diet Ultrasound bone BMD and risk of fracture by
824 girls Dietary patterns by factor anal- Meat-based diet densitometer measuring speed of sound
766 boys ysis with varimax rotation Chinese and Western-type diet (m/s), an indicator of bone
11–17 y quality, on the right
calcaneus
(continued)
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Table 2 Continued
Reference Country Study design Sample Method of assessing dietary Diet quality (exposure) Method of assessing Markers of bone health
of study characteristics intake markers of bone (outcome)
(size, sex, age) health
Monjardino et al Portugal Cohort n ¼ 1007 FFQ Healthier DXA Forearm BMD
(2015)15 543 girls Dietary patterns by the K- Dairy products
464 boys means method enhanced by Fast food and sweets
13 and 17 y bootstrapping Lower intake
Shin et al (2012)16 Korea Cross-sectional n ¼ 196 6-d food records Traditional Korean DXA Lumbar spine and femur
101 girls Dietary patterns by exploratory Fast food BMD measures
95 boys factor analysis Milk and cereal
12–15 y Snacks
Monjardino et al Portugal Cohort n ¼ 1264 FFQ Mediterranean Diet Quality DXA Forearm BMD
(2014)23 673 girls KIDMED, DASH diet index, and Index, the Dietary
591 boys OHS dietary index scores Approaches to Stop
13 and 17 y Hypertension diet index, and
the Oslo Health Study diet-
ary index
Noh et al (2011)17 Korea Cohort n ¼ 198 24-h recall and 2-d dietary Eggs and rice DXA Left calcaneus BMC and BMD
673 girls record Fruit, nuts, milk beverage, measures
9–11 y Dietary patterns by reduced eggs, grains
rank regression
Wosje et al (2010)18 USA Cohort n ¼ 325 3-d dietary record DP1 DXA Bone mass
158 girls Dietary patterns by reduced DP2
167 boys rank regression
3.8–7.8 y
Abbreviations: aBMD, areal bone mineral density; aBMC, areal bone mineral content; BMC, bone mineral content; BMD, bone mineral density; c-BUA, calcaneal broadband ultrasound attenua-
tion; DASH, Dietary Approaches to Stop Hypertension; DP1, non-whole grains, cheese, processed meats, eggs, fried potatoes, discretionary fats, and artificially sweetened beverages; DP2, dark
green vegetables, deep yellow vegetables, and processed meats; DXA, dual-energy X-ray absorptiometry; FFQ, food frequency questionnaire; KIDMED, Mediterranean Diet Quality Index in chil-
dren and adolescents; OHS, Oslo Health Study.
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Table 3 Main statistical analyses, adjustment variables, findings, and quality assessment of studies that examined the association between diet quality and markers of
bone health in children and adolescents.
Reference Statistical analysis Adjustment variables Main findings Statistically STROBE score
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significant
result?
Liao et al (2022)12 Multiple linear Age, sex, energy intake, height, weight, Fruit-milk-eggs dietary pattern was positively asso- Yes 17.85 points
regression physical activity, household income, ciated with TB BMC (b ¼ 10.480; 95%CI, 2.190– 81.13%
parental education, passive smoking, 18.770) and TBLH BMC (b ¼ 5.577; 95%CI, 0.214–
protein intake, calcium intake, vitamin 10.941). Animal organs–refined cereals pattern
D intake, supplemental intake of cal- was associated with low TB BMC (b ¼ 10.305;
cium, and supplemental intake of 95%CI, 18.433 to 2.176), TBLH BMC
multivitamins (b ¼ 6.346; 95%CI, 11.596 to 1.096), TB
BMD (b ¼ 0.006; 95%CI, 0.011 to 0.001),
and TBLH BMD (b ¼ 0.004; 95%CI, 0.007 to
0.001).
Heydenreich et al Multiple linear Model was adjusted by independent vari- SI correlated with age, BMI, absolute fat-free mass, No 18.20 points
(2020)19 regression ables (age, fat-free mass, sex, and relative fat mass, PAL, and puberty category score 82.72%
physical activity level) in both girls and boys (r ¼ 0.18–0.56, P < 0.01),
but not with BoneHEI (P > 0.05). Age, absolute
fat-free mass, sex, and PAL explained 35% of the
variance of SI (P < 0.0001): SI ¼ 0.60 þ 2.97 age
(years) þ 0.65 fat-free mass (kg) þ 6.21 sex
(0 ¼ male, 1 ¼ female) þ 17.55 PAL.
Mu~noz-Hernandez et Multiple linear Age, sex, study location, height, lean There were no significant associations of adherence No 19.35 points
al (2018)21 regression mass, and energy intake to the MD with BMC or BMD (both adjusted, 87.95%
P > 0.1). However, in children with high adher-
ence to the MD, there were no significant associ-
ations of PAL, MPA, MVPA, VPA, or ST with BMD-
or BMC-related outcomes. In contrast, higher lev-
els of PA, MPA, MVPA, and VPA were associated
with higher BMC and BMD in the whole body (all
P < 0.01), while ST was negatively associated
with both BMC and BMD (P < 0.05) in children
with low adherence to the MD.
Movassagh et al Multiple linear Sex, age, age of peak height velocity, Vegetarian-style DP was a positive independent Yes 19.10 points
(2018)13 regression height, weight, physical activity, total predictor of adolescent TBBMC (b ¼ 35.2, 86.81%
energy intake P ¼ 0.025; R2 ¼ 0.84). Mean adolescent TBaBMD
was 5% higher in third quartile of vegetarian-
style DP compared with first quartile (P < 0.05).
(continued)
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Table 3 Continued
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Reference Statistical analysis Adjustment variables Main findings Statistically STROBE score
significant
result?
Julian et al (2018)20 Multivariable logistic Tanner stage, mother education, family An overall dietary score or index was not associated No 20.10 points
regression affluence index, lean mass, and physi- with BMC in a sample of Spanish adolescents. 91.36%
cal activity Only fruits, nuts, cereal, and root vegetables were
found to provide significant ORs regarding BMC.
The risk of having low BMC was reduced by 32%
(OR ¼0 .684; 95%CI, 0.473–0.988) for FN when
the ideal MDS-A was followed, but this associa-
tion lost significance when adjusting for lean
mass and physical activity. For every 1-point
increase in the cereal and root vegetables and in
the fruit and nut components, the risk of having
low FN BMC diminished by 56% (OR ¼ 0.442;
95%CI, 0.216–0.901) and by 67% (OR ¼ 0.332;
95%CI, 0.146–0.755), respectively.
Forero-Bogota et al Multivariable logistic Age and Tanner stage MD adherence was not associated with poor bone No 18.60 points
(2017)22 regression health (high adherence: reference; medium 84.54%
adherence: OR ¼ 0.91; 95%CI, 0.52–1.61; low
adherence: OR ¼ 0.98; 95%CI, 0.53–1.81). The
predisposing factors of having a c-BUA z score of
 1.5 SDs included being underweight or
obese, having an unhealthy lean mass, having an
unhealthy fat mass, SLJ performance, handgrip
performance, and unhealthy muscular index
score.
Yang et al (2016)14 Multivariable logistic Sex, passive smoking, alcohol drinking, The Chinese and Western dietary pattern was asso- Yes 19.10 points
regression calcium supplements, physical activity, ciated with a decreased risk of low bone quality 86.81%
BMI in model 3 (T3 vs T1: OR ¼ 0.421; 95%CI, 0.289–
0.559).
Monjardino et al Multiple linear Height, weight, energy intake, and, in No significant associations between dietary pattern Yes 20.50 points
(2015)15 regression girls, age at menarche and mean BMD at age 13 were found. However, 93.18%
among girls, adherence to a pattern characterized
by a low intake of energy was negatively associ-
ated with annual BMD variation between the
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ages of 13 and 17 years (b ¼ 0.451; 95%CI,

0.827 to 0.074).
Shin et al (2012)16 Multivariable logistic Sex, age, BMI percentiles, weight-loss Adolescents in the highest tertile of the milk and Yes 17.35 points
regression attempts, pubertal status, and regular cereal dietary pattern score had a significantly 78.86%
exercise reduced likelihood of having low BMD at the
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lumbar spine compared with those in the lowest

tertile (OR ¼ 0.36; 95%CI, 0.14–0.93; P ¼ 0.0461).
Other dietary patterns were not associated with
BMD in Korean adolescents.
(continued)
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Table 3 Continued
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Reference Statistical analysis Adjustment variables Main findings Statistically STROBE score
significant
result?
Monjardino et al Multiple linear Height and weight at 13 and 17 years of Both crude and adjusted linear regression coeffi- No 20.50 points
(2014)23 regression age, total energy intake, parental edu- cients confirm the lack of clear associations 93.18%
cation level, and, in girls, age at between the a priori dietary patterns studied and
menarche BMD at 13 years and longitudinal changes in
BMD at 17 years. Among males, higher adherence
to the MD pattern was significantly associated
with higher BMD at 13 years (b ¼ 0.248, 95%CI,
0.052–0.444; P ¼ 0.013) but not with its annual
variation.
Noh et al (2011)17 Multiple linear Age, BMI, percent body fat, BMC, BMD, Participants with a higher score on the egg and rice Yes 19.00 points
regression and Tanner stage dietary pattern had less of an increase in BMC (P 86.36%
for trend ¼ 0.04), whereas those with a higher
score on the FMBEG dietary pattern had a greater
increase in BMC (P for trend, < 0.01) over the
22 months.
Wosje et al (2010)18 Multiple linear Dietary pattern score, height, exact age, DP1 scores were significantly associated with higher Yes 17.60 points
regression race, sex, accelerometer counts per bone mass after adjusting for all covariables (all 80.00%
minute, television-viewing time, out- P < 0.05). DP2 scores were related to higher bone
door playtime, calcium intake, and mass in years 1, 3, and 4 (all P < 0.05) but not in
energy intake year 2 (P ¼ 0.2) in models adjusted for all covari-
ables. In year 4, high intakes of dark green and
deep yellow vegetables and processed meats and
low intakes of fried foods led to a lower DP2
score, which in turn was related to lower fat mass
and higher bone mass.
Abbreviations: aBMD, areal bone mineral density; BMC, bone mineral content; BMD, bone mineral density; BMI, body mass index; BoneHEI, German Bone Healthy Eating index; c-BUA, calcaneal
broadband ultrasound attenuation; DP, dietary pattern; FMBGE, fruit, nuts, milk beverage, eggs, grains; FN, femoral neck; MD, Mediterranean diet; MDS-A, Mediterranean Diet Score for
Adolescents; MPA, moderate physical activity; MVPA, moderate-vigorous physical activity; OR, odds ratio; PAL, physical activity level; SD, standard deviation; SI, stiffness index; SLJ, standing
long-jump; ST, sedentary time; T1, tertile 1; T3, tertile 3; TB, total body; TBLH, total body less head; TBBMC, total body bone mineral content; TBaBMD, total body areal bone mineral density;
VPA, vigorous physical activity.
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Figure 2 Role of diet quality in markers of bone health in children and adolescents. A vegetarian dietary pattern is rich in eggs, unre-
fined grains, 100% fruit juice, legumes, dark green vegetables, nuts and seeds, added fats, fruits, and low-fat milk (including nondairy milk). A
Chinese and Western dietary pattern is characterized by a high consumption of rice and rice products, flour and flour products, whole grains,
fresh vegetables, fresh fruit, poultry, eggs, freshwater fish, and shrimp, deep-sea fish, milk and dairy products, beans and bean products, nuts,
snacks, sugar, and barbecue. An animal organs or refined cereals dietary pattern is characterized by high consumption of refined cereals, pre-
served vegetables, red meat, and animal organs. A lower intake dietary pattern is defined by low intakes of energy and all food groups, par-
ticularly red meat, fish, fruits, pasta/potatoes/rice, dairy products, cereals, and added fats. Abbreviations: BMC, bone mineral content; BMD,
bone mineral density; DP, dietary pattern.

total body BMC (b ¼ 10.305; 95%CI, 18.433 to among girls, the “lower intake” dietary pattern, charac-
2.176), low total body less head BMC (b ¼ 6.346; terized by low intakes of energy and all food groups was
95%CI, 11.596 to 1.096), low total body BMD negatively associated with annual variation in BMD
(b ¼ 0.006; 95%CI, 0.011 to 0.001), and low total between ages 13 and 17 years (b ¼ 0.451; 95%CI,
body less head BMD (b ¼ 0.004; 95%CI, 0.007 to 0.827 to 0.074).15 Shin et al,16 in their cross-
0.001).12 Mossavagh et al,13 in their cross-sectional sectional study in 196 Korean adolescents aged 12 to
study in 125 Canadian adolescents aged 12.7 6 2 years, 15 years, demonstrated that a “milk and cereal” dietary
showed that a vegetarian dietary pattern rich in dark pattern was associated with a reduced likelihood of low
green vegetables, eggs, unrefined grains, 100% fruit BMD of the lumbar spine (OR ¼ 0.36; 95%CI, 0.14–
juice, legumes/nuts/seeds, added fats, fruits, and low-fat 0.93; P ¼ 0.0461). Corroborating these results, Noh
milk during adolescence may benefit bone health et al17 demonstrated in their cohort study that a well-
(b ¼ 35.2, P ¼ 0.025; R2 ¼ 0.84). Another study in chil- balanced diet, characterized by high intakes of fruits,
dren and adolescents aged 11 to 17 years from China nuts, milk beverages, and grains, increased the BMC of
concluded that the risk of low bone mineral quality Korean schoolchildren aged 9 to 11 years over
could be reduced by the Chinese and Western dietary 22 months (P for trend < 0.01). Another cohort study
pattern (tertile 3 vs tertile 1: OR ¼ 0.421; 95%CI, 0.289– carried out in the Unites States in 325 preschool chil-
0.559), which is also marked by the intake of natural, dren aged 3.8 to 7.8 years showed that diets rich in dark
fresh, and whole foods.14 In a cohort study with 1007 green and deep yellow vegetables and low in fried foods
adolescents aged 13 and 17 years old from Portugal, may lead to bone mass accrual (all P < 0.05).18

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 None of the studies that evaluated diet quality with included in the study, completing follow-up, and ana-
dietary indexes, such as the German Bone Healthy lyzed; (5) providing reasons for nonparticipation at
Eating Index, the Mediterranean diet score, the Diet each stage; (6) indicating the number of participants
Quality Index for Adolescents, the DASH score, and the with missing data for each variable of interest; (7) pro-
Oslo Health Study dietary index, reported significant viding unadjusted estimates and, if applicable,
associations between a higher diet quality and bone confounder-adjusted estimates and their precision (eg,
health in children and adolescents.19–23 A cross-sectional 95%CIs); and (8) making clear which confounders were
study performed in 486 adolescents from Germany adjusted for and why they were included.

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showed that the German Bone Healthy Eating Index was
not a significant predictor of bone mass (stiffness index) DISCUSSION
(P > 0.05).19 Julian et al,20 in their cross-sectional study
in 179 Spanish adolescents aged 14.7 6 1.3 years, also did As far as can be determined, this is the first systematic
not find significant associations of the Mediterranean review to gather the available evidence on the associa-
Diet Score for Adolescents and the Diet Quality Index tion between diet quality and bone health markers in
for Adolescents with BMC. However, the intake of some children and adolescents. Given that diet is an impor-
dietary components, such as cereal and root vegetables tant modifiable risk factor for chronic diseases24 and
(OR ¼ 0.442; 95%CI, 0.216–0.901) and fruits and nuts that childhood and adolescence are key stages for the
(OR ¼ 0.332; 95%CI, 0.146–0.755), may have contributed formation of healthy eating habits25 and the develop-
to a higher femoral neck BMC. In another cross- ment of adequate bone mineralization,1 it is crucial to
sectional study in 177 children and adolescents aged 8 to better understand the role of diet quality in bone health
12 years from Spain, Mu~ noz-Hernandez et al,21 similar at early ages.
20
to J ulian et al, found that adherence to a The evaluation of diet quality by dietary pattern
Mediterranean diet was not associated with BMC or showed significant associations with markers of bone
BMD measures (both adjusted, P > 0.1). Forero-Bogota health. Dietary patterns such as the vegetarian pattern
et al,22 in their cross-sectional study in 1118 Colombian and the Chinese and Western pattern, which are rich in
children and adolescents aged 9 to 17.9 years, did not fruits, milk, eggs, nuts, grains, cereals, yellow and dark
detect a significant effect of Mediterranean diet adher- green vegetables, and root vegetables, were positively
ence on bone health as assessed by calcaneal broadband associated with bone health in pediatric populations.12–18
ultrasound attenuation (high adherence: reference; Fruits and vegetables are rich in antioxidant compounds
medium adherence: OR ¼ 0.91; 95%CI, 0.52–1.61; low such as vitamin C, vitamin K, folate, and carotenoids,
adherence: OR ¼ 0.98; 95%CI, 0.53–1.81). In accordance which contribute to bone remodeling and repair.26 In
with these findings, a cohort study in 1007 adolescents addition, these foods contain minerals such as potassium
aged 13 and 17 years from Portugal did not find strong and magnesium, which may prevent bone loss by
associations between dietary indexes defined a priori, increasing urinary pH and, consequently, increasing
such as the Mediterranean diet score, the DASH score, renal calcium reabsorption.26 Eggs are important sources
or the Oslo Health Study dietary index, and forearm of protein, zinc, lutein, and zeaxanthin.27 Proteins pro-
BMD. However, in males, a significant linear trend vide amino acids that join in signaling pathways for bone
toward increased BMD at 13 years with increasing adher- maintenance and stimulate intestinal absorption of cal-
ence to the Mediterranean diet was observed (b ¼ 0.248; cium and phosphorus.28,29 Zinc can increase serum levels
95%CI, 0.052–0.444; P ¼ 0.013).23 of procollagen type 1 amino-terminal propeptide, which
plays a role in improving bone mass.30 Furthermore,
Study quality lutein and zeaxanthin have anti-inflammatory effects that
prevent bone loss and stimulate the maturation of osteo-
The STROBE score of the studies varied from 17.35 to blasts.31–33 Whole grains are a source of protein, fiber, B
20.50 points (78.86% to 93.18%) (Table 3). The vitamins, antioxidants, and minerals, while nuts are also
STROBE criteria on which the studies were less scored excellent sources of minerals and antioxidant com-
were as follows: (1) indicating the study design with a pounds.8 Given this evidence, it is possible that healthy
commonly used term in the title or the abstract; (2) pre- dietary patterns may exert synergistic positive effects on
senting key elements of the study design early in the markers of bone health.
paper; explaining how the study size was determined; Dietary patterns with high intakes of red meat, ani-
(3) explaining how missing data were addressed; (4) mal organs, refined cereals,12 and fried foods18 and low
reporting the numbers of individuals at each stage of intakes of energy15 negatively impacted the bone health
the study—eg, numbers of participants potentially eligi- of children and adolescents. One mechanism that may
ble, examined for eligibility, confirmed eligible, explain the associations between poor diet quality and a

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worse bone health profile is linked to the dietary-related This review has a number of strengths, such as the
inflammation triggered by an innate immune response inclusion of data from countries worldwide, the system-
that activates the nuclear factor jB pathway, leading to atic approach based on the PRISMA guidelines,9 and
unbalanced secretion of inflammatory cytokines.34,35 the evaluation of study quality using the STROBE
There is evidence that a proinflammatory diet rich in method.11 However, it was not possible to perform a
fat, processed meat, fast food, fried snacks, and added meta-analysis because of the heterogeneity of the stud-
sugar is associated with the higher release of inflamma- ies. Interestingly, the results indicate that dietary pat-
tory and the lower release of anti-inflammatory bio- tern analysis may be a more sensitive and precise

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markers into the circulation in pediatric method than assessment by dietary indexes to investi-
populations.36,37 Low-grade inflammation impairs bone gate the relationship between diet quality and bone
remodeling and promotes loss of bone mass by increas- health in children and adolescents, but more investiga-
ing osteoclast differentiation and suppressing osteoblast tions are needed to confirm this hypothesis. The limita-
function.38,39 Research in adults has shown significant tions of this review may help explain the lack of
associations between the dietary inflammatory potential significant results obtained with dietary indexes. First,
and adverse bone outcomes,40,41 although no studies in the number of included studies may be too low to con-
children and adolescents were identified in this review. firm the associations found between diet quality and
Another potential mechanism underlying the asso- markers of bone health. Second, most of the dietary
ciation between the “animal organs–refined cereals” indexes used in the studies were not created and vali-
dietary pattern and bone health may be related to
dated with the purpose of analyzing bone heath. Third,
intakes of potassium and sodium. The “animal organs–
bone health was evaluated only by measures of BMD
refined cereals” dietary pattern identified was rich in
and BMC, which are considered long-term bone
preserved vegetables,12 with high amounts of sodium
markers. Thus, although this review provides important
and low amounts of potassium.42 Low intake of potas-
insights, further longitudinal research using a tool
sium increases calcium resorption or bone mineral dis-
designed specifically to assess the effect of diet quality
solution, thereby enhancing calcium loss and disrupting
on bone health is required. Such research should
calcium balance.43 Sodium ions compete with calcium
include the analysis of bone-regulating hormones and
within renal tubules, and thus a higher sodium intake
markers of bone turnover in order to elucidate the
increases urinary calcium excretion, which requires
more calcium to compensate for the loss.44 Moreover, mechanisms involved and to formulate dietary recom-
metallic elements or contaminants (eg, cadmium) accu- mendations for children and adolescents to prevent the
mulated in animal organs may also negatively affect early occurrence of bone diseases.
bone health, since these compounds can contribute to
oxidative stress, affect osteoblast and osteoclast balance, CONCLUSION
and inhibit the synthesis of osteocalcin.45–47 Finally,
because the skeleton is mostly accrued before 20 years Current evidence indicates that healthy dietary patterns
of age,1,3 a lower consumption of energy, nutrients, and rich in fruits, nuts, milk, eggs, grains, cereals, yellow
important food groups, such as dairy products, fruits, and dark green vegetables, and root vegetables may
and vegetables, may compromise the growth of children benefit the bone health of children and adolescents,
and increase the risk of bone disease.15,48,49 while low-energy dietary patterns and high intakes of
Regarding the quality of the papers included in this red meat, animal organs, refined cereals, and fried foods
review, some did not show the study design in the title should be limited. These findings emphasize the impor-
or abstract but did report this information in the meth- tance of developing effective public health policies that
odology section. Most studies did not report the sample encourage healthy eating habits beginning in childhood
size calculation or the number of eligible, included, and to reduce the risk of adverse bone outcomes later in life.
excluded participants, and most did not explain how
missing data were addressed. In addition, a few studies Acknowledgments
did not show the results obtained from crude models,
instead reporting only results from adjusted models by Author contributions: L.G.S. contributed to study con-
potential confounders. Although some items in the ception, study design, data collection, data analysis, and
included studies were not fully described by the authors, the writing, revision, and final reading of the manu-
all studies were of good quality and provided additional script. M.S.F. contributed to data collection, data analy-
clarity about the relationship between diet quality and sis, and the writing, revision, and final reading of the
bone health, a topic that remains poorly explored, espe- manuscript. J.F.N. contributed to data analysis and final
cially in pediatric populations. reading of the manuscript. D.S. contributed to data

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analysis and final reading of the manuscript. All authors 21. Mu~ noz-Hernandez V, Arenaza L, Gracia-Marco L, et al. Influence of physical activity
on bone mineral content and density in overweight and obese children with low
read and approved the final manuscript. adherence to the Mediterranean dietary pattern. Nutrients. 2018;10:1075.
22. Forero-Bogota MA, Ojeda-Pardo ML, Garcıa-Hermoso A, et al. Body composition,
nutritional profile and muscular fitness affect bone health in a sample of school-
Funding. No external funds supported this work. children from Colombia: the Fuprecol study. Nutrients. 2017;9:106.
23. Monjardino T, Lucas R, Ramos E, et al. Associations between apriori-defined diet-
ary patterns and longitudinal changes in bone mineral density in adolescents.
Declaration of interest. The authors have no relevant Public Health Nutr. 2014;17:195–205.
24. World Health Organization. Diet, nutrition, and the prevention of chronic diseases:
interests to declare. report of a joint WHO/FAO expert consultation. WHO Technical Report Series 916.
World Health Organization; 2003. https://www.who.int/publications/i/item/

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through the online version of this article at the publish- systematic review and meta-analysis. PLoS One. 2019;14:e0217223.
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