Introduction
Bone accretion
Definition of peak bone mass
Importance of peak bone mass
Fracture
Tracking
Timing of peak bone mass
Methods for measuring peak bone mass
Dual-energy x-ray absorptiometry
Peripheral quantitative computed tomography
Mechanical loading
Body composition
Nonmodifiable factors
Genetics
Population ancestry
Sex
Maturation
Modifiable factors
Scientific statement aims
Methods
Level of evidencea
| Description |
---|---|
A: Strong | Clear evidence from at least one large, well-conducted, generalizable RCT that is adequately powered with a large effect size and is free of bias or other concerns |
OR | |
Clear evidence from multiple RCTs or many controlled trials that may have few limitations related to bias,measurement imprecision, inconsistent results, or other concerns | |
B: Moderate | Evidence obtained from multiple, well-designed, conducted, and controlled prospective cohort studies that have used adequate and relevant measurements and that gave similar results from different populations |
OR | |
Evidence obtained from a well-conducted meta-analysis of prospective cohort studies from different populations | |
C: Limited | Evidence obtained from multiple prospective cohort studies from diverse populations that have limitations related to bias, measurement imprecision, or inconsistent results or have other concerns |
OR | |
Evidence from only one well-designed prospective study with few limitations | |
OR | |
Evidence from multiple well-designed and conducted cross-sectional or case-controlled studies that have very few limitations that could invalidate the results from diverse populations | |
OR | |
Evidence from a meta-analysis that has design limitations | |
D: Inadequate | Evidence from studies that have one or more major methodological flaws or many minor methodological flaws that result in low confidence in the effect estimate |
OR | |
Insufficient data to support a hypothesis | |
OR | |
Evidence derived from clinical experience, historical studies (before and after), or uncontrolled descriptive studies or case reports |
Macronutrient | Reference | Study description | Population description | Number of subjects | End points | Results | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
Prospective studies | |||||||||||
Fat | Hogstrom et al. 2007 [141] | The objective of this study was to investigate the role of fatty acids in bone accumulation and the attainment of peak bone mass in young men | Sex: male Age: 16.7 years at baseline Race: white Location: Sweden Year(s): 1994 (baseline), first follow-up was at a mean of 6 years (age 22 years) | 78 | Data are shown for the overall group (N = 78) | Total body | Hip | Spine | |||
r
|
P
|
r
|
P
|
r
|
P
| ||||||
Palmitic acid | −0.04 | NS | 01 | NS | 0.01 | NS | |||||
Palmitoleic acid | 0.04 | NS | 0.03 | NS | 0.02 | NS | |||||
Stearic acid | 0.07 | NS | 0.02 | NS | 0.04 | NS | |||||
Oleic acid | −0.19 | NS | −0.10 | NS | −0.22 | NS | |||||
Linoleic acid | 0.00 | NS | −0.06 | NS | −0.15 | NS | |||||
Eicosatrienoic acid | −0.09 | NS | −0.04 | NS | −0.08 | NS | |||||
Arachidonic acid | 0.12 | NS | 0.15 | NS | 0.25 | <0.05 | |||||
Eicosapentaenoic acid | 0.04 | NS | 0.02 | NS | 0.16 | NS | |||||
Docosapentaenoic acid | 0.02 | NS | −0.07 | NS | 0.05 | NS | |||||
DHA | 0.10 | NS | 0.07 | NS | 0.26 | <0.05 | |||||
PUFA | 0.14 | NS | 0.07 | NS | 0.16 | NS | |||||
MUFA | −0.18 | NS | −0.09 | NS | −0.21 | NS | |||||
SFA | 0.04 | NS | 0.03 | NS | 0.05 | NS | |||||
n-6 | 0.04 | NS | 0.00 | NS | 0.07 | NS | |||||
n-3 | 0.10 | NS | 0.07 | NS | 0.26 | <0.05 | |||||
n-6:n-3 | −0.12 | NS | −0.13 | NS | −0.26 | <0.05 | |||||
Data presented above include Pearson’s correlations between fatty acids measured in the phospholipid fraction for changes in aBMD from 16 to 22 years | |||||||||||
Cross-sectional studies | |||||||||||
Fat | Eriksson et al. 2009 [142] | Serum phospholipid fatty acid pattern was studied in relation to bone parameters in healthy children | Sex: male and female Mean age: 8.2 years Race: Caucasian Location: Gothenburg, Sweden Year(s): not specified | 85 | Data are shown for the overall group (N = 85) | Total body BMC (g) | |||||
Correlation (r) |
P
| ||||||||||
Palmitic acid (16:0) | 0.17 | NS | |||||||||
Stearic acid (18:0) | −0.15 | NS | |||||||||
Arachidic acid (20:0) | 0.20 | NS | |||||||||
Nervonic acid (24:1n-9) | 0.27 | <0.05 | |||||||||
Linoleic acid (18:2n-6) | −0.17 | NS | |||||||||
Arachidonic acid (20:4n-6) | 0.23 | <0.05 | |||||||||
α-Linolenic acid (18:3n-3) | −0.22 | <0.05 | |||||||||
DHA (22:6n-3) | 0.03 | NS | |||||||||
∑ n-6 | −0.07 | NS | |||||||||
∑ n-3 | 0.03 | NS | |||||||||
n-6:n-3 | −0.06 | NS | |||||||||
Data presented above are from Pearson’s correlations |
Macronutrient | Reference | Study description | Population description | Number of subjects | End points | Results | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
RCTs | |||||||||||
Protein | Ballard et al. 2006 [143] | This study investigated whether 6 months of protein supplementation in conjunction with a strength and conditioning training program improves vBMD, bone geometry, and total body BMC. | Sex: male and female Age: 18–25 years Race: not specified Location: South Dakota, USA Year(s): not specified | 68 | Data are shown for the protein supplemented group (n = 36) | Mean change, protein group (n = 36) |
P
| ||||
4 % site | |||||||||||
Total vBMD (mg/cm3) | 0.20 | NS | |||||||||
Trabecular vBMD (mg/cm3) | −0.50 | NS | |||||||||
Total area (cm2) | 5.0 | NS | |||||||||
20 % site | |||||||||||
Cortical vBMD (mg/cm3) | 2.4 | NS | |||||||||
Cortical area (cm2) | 1.7 | NS | |||||||||
Cortical thickness (mm) | 0.05 | NS | |||||||||
Periosteal circumference (mm) | −0.20 | NS | |||||||||
Endosteal circumference (mm) | −0.50 | NS | |||||||||
Polar SSI (mm3) | 57 | NS | |||||||||
Total body | |||||||||||
BMC (g) | −3.5 | NS | |||||||||
Bone area (cm2) | −3.9 | NS | |||||||||
Leg | |||||||||||
BMC (g) | 1.3 | NS | |||||||||
Arm | |||||||||||
BMC (g) | 5.7 | NS | |||||||||
Data presented above are least-squares means determined by ANCOVA while controlling for initial height and weight and baseline bone value. | |||||||||||
Prospective studies | |||||||||||
Protein | Alexy et al. 2005 [144] | This study examined whether the long-term dietary protein intake and diet net acid load are associated with bone status in children. In a prospective study design, long-term dietary intakes were calculated from 3-day weighed dietary records that were collected yearly over the 4-year period before a one-time bone analysis using pQCT. | Sex: male and female Age: 6–18 years Race: white Location: Dortmund, Germany Year(s): 1998–1999 subcohort of the DONALD study | 229 | Data are shown for the overall group (N = 229) | Protein (g/day) | |||||
ß | ßstand
|
r
2
|
P
| ||||||||
Forearm | |||||||||||
Periosteal circumference (mm2) | 0.07 | 0.17 | 0.03 | <0.01 | |||||||
Cortical area (mm2) | 0.42 | 0.27 | 0.04 | <0.01 | |||||||
BMC (mg/mm) | 0.46 | 0.26 | 0.03 | <0.01 | |||||||
Polar SSI (mm3) | 1.83 | 0.29 | 0.06 | <0.01 | |||||||
• Data presented above are results from stepwise multiple regression and after adjustment for age, sex, and energy intake. • ßstand is the standardized parameter estimate. • Children with a higher dietary PRAL had significantly less cortical area (P < 0.05) and BMC (P < 0.01). • Long-term calcium intake had no significant effect on any bone variable. | |||||||||||
Protein | Bounds et al. 2005 [146] | This study aimed to identify factors related to children’s bone mineral indexes at age 8 years, and to assess bone mineral indexes in the same children at ages 6 and 8 years. Children’s dietary intake and BMC were assessed as part of a longitudinal study from ages 2 months to 8 years. | Sex: male and female Age: 6 years (baseline) and 8 years (follow-up) Race: white Location: Knoxville, TN Year(s): not specified | 52 | Data are shown for the overall group (N = 229) | Protein intake (g) over ages 2–8 years | |||||
r
|
P
| ||||||||||
Total body | |||||||||||
BMC at age 8 years | 0.37 | ≤0.05 | |||||||||
ß | Partial R
2
|
P
| |||||||||
BMC model 1 | (+) 2.40 | 0.08 | <0.01 | ||||||||
Data presented above show the Pearson’s correlation coefficient (r) relating protein intake over ages 2–8 years, representing 27 days of dietary data. BMC model 1 (R
2 = 0.69, F = 20.7, P < 0.01) | |||||||||||
Protein | Vatanparast et al. 2007 [147] | This mixed-longitudinal study investigated the influence of protein intake on bone mass measures in young adults, considering the influence of calcium intake through adolescence. Dietary intake was assessed via serial 24-h recalls carried out at least once yearly. | Sex: male and female Age: 8–21 years during phase I of the study; 17–29 years for phase II Race: majority Caucasian Location: Saskatoon, Saskatchewan, Canada Year(s): 1991–1997 (phase I); 2003–2006 (phase II); participating in the University of Saskatchewan Pediatric Bone Mineral Accrual Study | 133 | Data are shown for the overall group (N = 133) and a subgroup (n = 44) | Protein intake (g) | |||||
Regression coefficient | Partial R
2
|
P
| |||||||||
Total body (N = 133) | |||||||||||
BMC | NS | — | NS | ||||||||
BMC net gain | 0.11 | 0.21 | 0.02 | ||||||||
Total body (n = 44) | |||||||||||
BMC | 0.21 | 0.33 | 0.04 | ||||||||
BMC net gain | 0.21 | 0.37 | 0.02 | ||||||||
The net gain of total body BMC and the net gains of height and weight from age of peak height velocity to early adulthood were entered into the model. Variables in the multiple regression model (stepwise) were sex, current height, weight, physical activity level, protein intake, vegetable and fruit intake, and periadolescence intakes of vegetables and fruit, protein, and physical activity. Protein intake predicted total body BMC net gain in all subjects. In females at periadolescence or early adulthood with adequate calcium intake(>1000 mg/day) (n = 44), protein intake positively predicted total body BMC and BMC net gain. | |||||||||||
Protein | Zhang et al. 2010 [148] | This study assessed the association between protein intakes and bone mass accrual in girls who participated in a 5-year study including 2 years of milk supplementation (intervention groups only) and 3 years of follow-up study. | Sex: female Mean age: 10.1 years Race: Chinese Location: Beijing Year(s): 1999–2004 | 757 | Data are shown for the overall group (N = 757) | Average protein intake | |||||
ß |
P value | ||||||||||
Total body | |||||||||||
Bone area | – | NS | |||||||||
BMC | −1.92 | 0.02 | |||||||||
Proximal forearm | |||||||||||
Bone area | −9.11 | <0.01 | |||||||||
BMC | −10.2 | <0.01 | |||||||||
Distal forearm | |||||||||||
Bone area | – | NS | |||||||||
BMC | −4.82 | <0.01 | |||||||||
• Data presented above (ß) represent the percentage change in the dependent variable associated with intake of protein after controlling for baseline bone mass and pubertal development, age and physical activity, survey time, group, and clustering by schools. Protein, among other nutrients, was included in an initial model and flowed by backward elimination with P < 0.01 as the standard for retention, exclusion by the regression model. • When protein intake was considered according to animal or plant food sources, protein from animal foods, particularly meat, had significant negative effects on BMC accrual at the proximal and distal forearm (P < 0.05). | |||||||||||
Protein | Remer et al. 2011 [145] | The aim of the study was to examine whether the association of long-term dietary acid load and protein intake with children’s bone status can be confirmed using approved urinary biomarkers and whether these diet influences may be independent of potential bone-anabolic sex steroids. Data were collected in 197 healthy children during the 4 years preceding proximal forearm bone analyses by pQCT. | Sex: male and female Age: 6–18 years Race: white Location: Dortmund, Germany Year(s): 1998–1999 subcohort of the DONALD study | 197 | Data are shown for the overall group (N = 197) | Urinary uN | Urinary PRAL | ||||
ß |
P
| ß |
P
| ||||||||
Forearm | |||||||||||
BMC (mg/mm) [log 10] | 0.03 | <0.01 | −0.02 | 0.03 | |||||||
Cortical area (mm2) [log 10] | 0.02 | <0.01 | −0.02 | 0.03 | |||||||
Polar SSI (mm3) [log 10] | 0.02 | <0.01 | −0.01 | NS | |||||||
Periosteal circumference (mm) | 0.50 | 0.03 | 0.02 | NS | |||||||
BMD (mg/cm3) | 5.40 | NS | −8.70 | NS | |||||||
• Data presented above are from multivariate regression models showing independent associations of both long-term protein intake (as uN) and PRAL as explanatory variables with forearm bone variables. Data are adjusted for age, sex, pubertal stage, forearm muscle area, forearm length, and urinary calcium. • Data show that 1 Z-score variation in uN leads to an average 7.2 % increase in BMC and a 4.7 % increase in cortical area as well as SSI. A 1 Z-score uN corresponds to 0.28-g protein intake/kg body wt, implying that an additional 1-g protein intake/kg body wt may lead to an average increase of 26 % in BMC and 17 % in cortical area and SSI. A 1-g protein intake/kg body wt is associated with an average increase of 1.8-mm periosteal circumference. | |||||||||||
Cross-sectional studies | |||||||||||
Protein | Hoppe et al. 2000 [149] | The objective of the study was to identify associations between dietary factors and total body bone measurements in a random sample of healthy Danish children. | Sex: male and female Age: 10 years Race: Danish, otherwise unspecified Location: Hvidovre, Denmark Year(s): 1997–1998, from the Copenhagen Cohort Study on Infant Nutrition and Growth | 105 | Data are shown for the overall group (N = 105) | Protein (g/day) | |||||
Pearson’s r
|
P
| ||||||||||
Total body | |||||||||||
Bone area (cm2) | 0.31 | <0.01 | |||||||||
BMC (g) | 0.33 | <0.01 | |||||||||
• The data above are unadjusted. • In the multiple linear regression analysis including height, weight, sex, energy intake, and bone-related nutrients in the model, dietary protein was not significantly associated with bone area or BMC. After backward elimination, in which height, weight, and sex were forced to stay in the model, dietary protein was positively associated with bone area (P < 0.05). • Inclusion of pubertal stages in the analyses did not alter the bone area or BMC outcomes. | |||||||||||
Protein | Iuliano-Burns et al. 2005 [150] | This cross-sectional study assessed monozygotic and dizygotic male twin pairs to test the following hypotheses: (1) associations between bone mass and dimensions and exercise are greater than between bone mass and dimensions and protein or calcium intakes; and (2) exercise or nutrient intake are associated with appendicular bone mass before puberty and axial bone mass during and after puberty. | Sex: male Age: 7–20 years Race: not specified Location: Melbourne, Australia Year(s): 1997–2001 | 112 (56 twin pairs) | Data are shown for the overall group (N = 112) | Differences in protein | |||||
Univariate | Size adjusted | All lifestyle and size adjusted | |||||||||
ß |
P
| ß |
P
| ß |
P
| ||||||
Differences in BMC (g) | |||||||||||
Total body | 3.5 | NS | 1.3 | NS | 1.3 | NS | |||||
Arms | 0.8 | <0.05 | 0.7 | <0.05 | 0.8 | <0.05 | |||||
Legs | 1.6 | NS | 0.3 | NS | 0.3 | NS | |||||
Lumbar spine | 0.0 | NS | 0.0 | NS | 0.0 | NS | |||||
Differences in BMC (%) | |||||||||||
Total body | 0.3 | <0.05 | 0.2 | <0.05 | 0.1 | NS | |||||
Arms | 0.4 | <0.05 | 0.4 | <0.01 | 0.4 | <0.05 | |||||
Legs | 0.3 | NS | 0.1 | NS | 0.1 | NS | |||||
Lumbar spine | 0.1 | NS | 0.1 | NS | 0.2 | NS | |||||
Differences in bone dimensions (mm) | |||||||||||
Cortical thickness | 0.0 | NS | 0.0 | NS | 0.0 | NS | |||||
Periosteal diameter | 0.0 | NS | 0.0 | NS | 0.0 | NS | |||||
Endosteal diameter | 0.0 | NS | 0.0 | NS | −0.0 | NS | |||||
Differences in bone dimensions (%) | |||||||||||
Cortical thickness | 0.2 | NS | 0.1 | NS | 0.4 | NS | |||||
Periosteal diameter | 0.1 | NS | 0.0 | NS | 0.0 | NS | |||||
Endosteal diameter | −0.0 | NS | −0.1 | NS | −0.3 | NS | |||||
• Data presented above are ß coefficients for within-pair differences in protein versus (1) within-pair differences in BMC and bone dimensions, (2) within-pair differences in size-adjusted BMC and bone dimensions, and (3) when all within-pair differences in protein, calcium, exercise duration, and size are included in the regression equation. • A 1-g difference in protein intake was associated with a 0.8-g (0.4 %) difference in arm BMC (P < 0.05). These relationships were present in peripubertal and postpubertal pairs but not in prepubertal pairs. Exercise during growth appears to have greater skeletal benefits than variations in protein or calcium intakes, with the site-specific effects evident in more mature twins. | |||||||||||
Protein | Chevalley et al. 2008 [151] | This study analyzed the relationship between physical activity levels and protein compared with calcium intake on BMC in healthy prepubertal boys. | Sex: male Age: 6.5–8.5 years Race: white Location: Geneva, Switzerland Year(s): recruitment period 1999–2000, otherwise unspecified | 232 | Data are shown for the overall group (N = 232) | Correlation with protein intake (g/day) | |||||
r
|
P
| ßAdjusted
|
P
| ||||||||
BMC (g) | |||||||||||
Radial metaphysis | 0.26 | <0.01 | 0.20 | 0.01 | |||||||
Radial diaphysis | 0.21 | <0.01 | 0.12 | NS | |||||||
Total radius | 0.27 | <0.01 | 0.20 | 0.01 | |||||||
Femoral neck | 0.20 | <0.01 | 0.19 | 0.03 | |||||||
Total hip | 0.18 | <0.01 | 0.12 | NS | |||||||
Femoral diaphysis | 0.23 | <0.01 | 0.19 | 0.03 | |||||||
Lumbar spine | 0.24 | <0.01 | 0.22 | <0.01 | |||||||
Data presented above are from univariate (r) and multivariate (ßAdjusted) analyses; the latter takes into account the respective contribution of physical activity, protein, and calcium intakes. | |||||||||||
Protein | Esterle et al. 2009 [152] | This study explored dietary calcium sources and nutrients possibly associated with lumbar bone mineralization and calcium metabolism in adolescent girls and evaluated the possible influence of a genetic polymorphic trait associated with adult-type hypolactasia. | Sex: female Age: 12–22 years Race: Caucasian Location: France Year(s): not specified | 192 | Data are shown for the postmenarchal group only (n = 142) | Protein from milk | Protein from other foods | ||||
Adj R
2
| ßstand
|
P
| Adj R
2
| ßstand
|
P
| ||||||
Lumbar spine BMC (g) | |||||||||||
Absolute | 0.61 | 0.14 | <0.01 | 0.61 | <0.01 | NS | |||||
Adjusted | 0.60 | 0.13 | 0.02 | 0.60 | <0.01 | NS | |||||
• Data presented above are from multivariate linear analyses. • Absolute protein intake is expressed in g/days. • Adjusted protein intake for weight, years after menarche, and vertebral area is expressed in g/kg/days. • Girls with milk intakes <55 mL/day had significantly lower BMC compared to girls consuming >260 mL/day. • Neither BMC nor milk consumption was associated with −13,910 LCT polymorphism. | |||||||||||
Protein | Ekbote et al. 2011 [153] | The aim of this study was to examine lifestyle factors as determinants of total body BMC and bone area in Indian preschool children. | Sex: male and female Age: 2–3 years Race: Indian Location: Pune, India Year(s): 2009 | 71 | Data are shown for the overall group (N = 71) | Protein (g/days) | |||||
Normal | Malnourished | All | |||||||||
r
|
P
|
r
|
P
|
r
|
P
| ||||||
Total body | |||||||||||
Bone area | 0.65 | <0.01 | 0.57 | <0.01 | 0.58 | <0.05 | |||||
BMC | 0.62 | <0.01 | 0.44 | <0.05 | 0.55 | <0.01 | |||||
Data presented above are from Pearson’s correlation coefficients correlating protein intake and bone among normal children, malnourished children, and all (normal and malnourished children combined). | |||||||||||
Protein | Libuda et al. 2011 [154] | This study examined relevant nutrients that are supposed to have an impact on bone parameters and compared their effect sizes with those of known predictors of bone development. | Sex: male and female Median age: 8.1 years Race: white Location: Dortmund, Germany Year(s): 1998–1999 subcohort of the DONALD study | 107 | Data are shown for the overall group (N = 107) | Protein (g/MJ) | |||||
ß | ßstand
|
R
2
|
P
| ||||||||
Forearm | |||||||||||
Polar SSI (mm3) | – | – | – | NS | |||||||
Periosteal circumference (mm) | – | – | – | NS | |||||||
BMC (mg/mm) | 1.49 | 0.11 | 0.01 | NS | |||||||
Cortical area (mm2) | 1.37 | 0.11 | 0.01 | NS | |||||||
• Data presented above are from stepwise linear regression analyses, considering muscle area, BMI standard deviation scores, body fat %, age, sex, and rostenediol, as well as intakes of protein, calcium, vitamin D, and PRAL. • Of all nutrients considered, only protein showed a trend for an association with BMC (P = 0.073) and cortical area (P = 0.056) in stepwise linear regression models. • None of the other dietary variables were associated with bone parameters. • The protein effect did not differ between sexes. |
Nutrient | Reference | Study description | Population description | Number of subjects | End points | Results | ||
---|---|---|---|---|---|---|---|---|
RCTs | ||||||||
Supplements | ||||||||
Calcium carbonate, 1000 mg/day | Dibba et al. 2000 [160] | 12-month randomized, double-blind, placebo-controlled study Supplementation increased calcium intake from 342 to 1056 mg/day By young adulthood, there was no difference in the amount of bone accrued (mineral or size) or the rate of bone growth between supplemented and placebo. | Sex: 80 boys, 80 girls Age: 8.3–11.9 year Race: Gambian, otherwise unspecified Location: rural Gambia, West Africa | 160 | Difference in % gain between groups | |||
Midshaft arm BMC | 4.6 ± 0.9a
| |||||||
Distal radius BMC | 5.5 ± 2.7a
| |||||||
Adjusted for bone width, weight, and height | ||||||||
Calcium carbonate, 800 mg + 400 IU vitamin 3/day | Moyer-Mileur et al. 2003 [163] | 1-year double-blind RCT Baseline calcium: not reported Average intake during study: supplement, 1524 (353); placebo, 906 (345); 30 % dropout Trabecular vBMD values were significantly greater in the supplemented group at baseline. | Sex: female Age: 12 years; Tanner stage 2 Race: white Location: USA | 100 | Tibial pQCT measurements | Calcium and D | Placebo | |
Trabecular vBMD % increasea
| 1.0 | −2.0 | ||||||
Trabecular BMC % increasea
| 4.1 | 1.6 | ||||||
Adjusted for baseline values | ||||||||
Elemental calcium, 1000 mg/day | 12-month double-blind, placebo-controlled Habitual calcium intakes <800 mg/day Compliance dropped from 71 ± 26 % during the initial 6 months to 56 ± 34 % for the remaining study period (P = 0.0001) In follow-up study by Dodiuk-Gad et al., girls who have had compliance of ≥75 % on supplementation had significantly higher total body BMD after 3.5 years after supplementation than controls. | Sex: female; >1 year postmenarchal Age: 12–17 years Race: 85 Jewish girls and 27 Arab girls Location: Haifa, Israel | 112 | Calcium supplement | Placebo | |||
Lumbar spine BMC | 4.52 ± 0.48 | 3.95 ± 0.58 | ||||||
Total body BMC | 4.63 ± 0.42 | 4.65 ± 0.54 | ||||||
Femoral neck BMC | 4.30 ± 0.86 | 3.00 ± 0.81 | ||||||
Lumbar spine BMD | 3.66 ± 0.35a
| 3.00 ± 0.43 | ||||||
Total body BMD | 3.80 ± 0.30a
| 3.07 ± 0.29 | ||||||
Femoral neck BMD | 2.00 ± 0.51 | 1.39 ± 0.42 | ||||||
Not adjusted | ||||||||
Calcium carbonate (Caltrate) supplement, 1200 mg/day | Cameron et al. 2004 [161] | 24-month RCT of twins Baseline calcium intake: 786, trt; 772, control in those who completed 24 months All were premenarchal at baseline 24 (38 %) of pairs completed 24 months Compliance was 76 % for both groups | Sex: female Age: 8–13 years Race: not specified Location: Australia | 103 (50 twin pairs + 1 set of triplets) | End of 24-month intention to treat | Difference in % gain between groups | ||
Total body BMC | 3.69a
| |||||||
Hip BMD | −0.39a
| |||||||
Spine BMD | 1.40a
| |||||||
Femoral neck BMD | −0.57 | |||||||
End of 12 months | ||||||||
Total body BMC | 2.47a
| |||||||
Hip BMD | 1.64a
| |||||||
Spine BMD | 1.64a
| |||||||
Femoral neck BMD | 1.13 | |||||||
Adjusted for age, height, and weight | ||||||||
Calcium carbonate, 500 mg/day | Molgaard et al. 2004 [332] | 12-month randomized, double-blind, placebo-controlled intervention Subjects stratified at randomization according to baseline calcium intake Group A (n = 60) habitually consumed 1000–1307 mg/day (40th–60th percentile), and group B (n = 53) habitually consumed <713 mg/day (<20th percentile) | Sex: female Age: 12 years ± 6 months Race: white Location: Denmark | 113 | No significant interaction between habitual calcium intake (groups A and B) and the intervention (Calcium carbonate–Placebo) in the analyses of height, weight, BMC, size-adjusted BMC, bone area, or BMD (all P > 0.15). When groups A and B were analyzed together, there was a significant effect of the intervention on BMD (0.8 %; 95 % CI, 0.01 %, 1.54 %; P = 0.049). | |||
Calcium citrate malate, 1000 mg/day | Matkovic et al. 2005 [333] | 4-year randomized clinical trial and optionally extended for an additional 3 years Baseline calcium: 830 ± 236 mg/day 51 % of the subjects completed the 7-year trial. | Sex: female Age: 11 years; Tanner 2 Race: white Location: USA | 354 | Calcium supplement | Placebo | ||
End of 4-year gain | ||||||||
Total body BMD (g/cm2) | 0.215 ± 0.037a
| 0.204 ± 0.0353 | ||||||
Proximal radius BMD (g/cm2) | 0.167 ± 0.088 | 0.171 ± 0.079 | ||||||
Distal radius BMD (g/cm2) | 0.106 ± 0.047a
| 0.092 ± 0.046 | ||||||
Cortical area/total area | 0.079 ± 0.021 | 0.072 ± 0.0213 | ||||||
End of 7-year gain | ||||||||
Total body BMD (g/cm2) | 0.268 ± 0.049 | 0.263 ± 0.044 | ||||||
Proximal radius BMD (g/cm2) | 0.162 ± 0.038 | 0.156 ± 0.036 | ||||||
Distal radius BMD (g/cm2) | 0.171 ± 0.047 | 0.165 ± 0.040 | ||||||
Cortical area/total area | 0.095 ± 0.025a
| 0.085 ± 0.0242
| ||||||
By young adulthood, significant effects remained at metacarpals and at the forearm of tall persons. | ||||||||
Calcichew, 1000 mg/day | Prentice et al. 2005 [162] | 13-month randomized, double-blind, placebo-controlled study Subjects were stratified by high or low exercise at baseline. Those in the low group were randomized to exercise intervention or none. Compliance with exercise was poor and no statistically significant differences were found between groups. For final analysis, all exercise intervention groups were combined. Subjects were told to not take the supplement with meals. Baseline calcium: 1197, supplement; 1199, placebo Total calcium intake during study: supplement, 1858 ± 629; placebo, 1283 ± 586 Latter factored in compliance | Sex: male Age: 16–18 years Race: 90 % white; 10 % from various ethnic groups Location: Cambridge, UK | 143 | Difference in % gain between groups | |||
Total body BMC | 0.33 ± 0.34 | |||||||
Lumbar spine BMC | 0.18 ± 0.54 | |||||||
Total hip BMC | 1.09 ± 0.54a
| |||||||
Femoral neck BMC | 1.21 ± 0.65 | |||||||
Intertrochanter BMC | 0.99 ± 0.56 | |||||||
Trochanter BMC | 0.29 ± 0.80 | |||||||
Ultradistal radius BMC | 0.36 ± 0.86 | |||||||
Adjusted for bone area, weight, and height | ||||||||
Calcium carbonate, 800 mg/day and vitamin D3 400 IU/day | Greene and Naughton 2011 [164] | 6-month randomized placebo-controlled trial Baseline calcium: 763–786 mg/day | Sex: female; identical twins Age: 9–13 years Race: not indicated Location: Australia | 40 (20 pairs) | pQCT | Tibial difference in % gain between groups | ||
4 % location | ||||||||
Trabecular vBMD (mg/mm3) | 5.2 ± 1.96a
| |||||||
Trabecular area (mm2) | 5.4 ± 1.33a
| |||||||
Subcort density (mg/mm3) | 3.4 ± 0.82 | |||||||
Subcortical area (mm2) | 0.8 ± 0.07 | |||||||
SSI (mm3) | 6.6 ± 1.26a
| |||||||
14 % | ||||||||
Cortical BMD (mg/mm3) | 0.1 ± 0.04 | |||||||
Cortical area (mm2) | 1.3 ± 0.35 | |||||||
Total bone area (mm2) | 0.3 ± 0.02 | |||||||
Medullary CSA (mm2) | −0.4 ± 0.02 | |||||||
SSI (mm3) | 1.7 ± 0.22 | |||||||
38 % | ||||||||
Cortical BMD (mg/mm3) | 0.8 ± 0.03 | |||||||
Cortical area (mm2) | 5.8 ± 0.8a
| |||||||
Total bone area (mm2) | 0.5 ± 0.03 | |||||||
Medullary CSA (mm2) | −6.2 ± 1.6a
| |||||||
SSI (mm3) | 0.7 ± 0.06 | |||||||
66 % | ||||||||
Cortical BMD (mg/mm3) | 0.1 ± 0.02 | |||||||
Cortical area (mm2) | 5.7 ± 0.39a
| |||||||
Total bone area (mm2) | −0.7 ± 0.03 | |||||||
Medullary CSA (mm2) | −8.1 ± 1.82a
| |||||||
Muscle CSA (mm2) | 0.6 ± 0.02 | |||||||
Radial difference in % gain between groups | ||||||||
4 % location | ||||||||
Trabecular vBMD (mg/mm3) | 3.3 ± 0.28a
| |||||||
Trabecular area (mm2) | 2.8 ± 0.36a
| |||||||
Subcortical density (mg/mm3) | 0.1 ± 0.03 | |||||||
Subcortical area (mm2) | 0.3 ± 0.01 | |||||||
SSI (mm3) | 5.7 ± 0.51a
| |||||||
Calcium carbonate pills | Khadilkar et al. 2012 [334] | 1-year double-blind RCT of calcium, multivitamin with zinc, and vitamin D3
| Sex: female Age: 8–12 years Race: Indian Location: Pune, India | 214 | Total body BMC increase | Percent gain by group | ||
Calcium + multivitamin | Calcium | Control | ||||||
21.5 ± 5.7a
| 23.1 ± 6.1a
| 19.4 ± 4.2 | ||||||
Adjusted for Tanner stage and lean body mass | ||||||||
Calcium, 1000 mg/day by pill or cheese Vitamin D, 800 IU/day | Cheng et al. 2005 [159] | 2-year RCT; randomized to 1 of 4 groups: calcium 1000 mg/day + vitamin D 200 IU/day; calcium 1000 mg/day; cheese (1000 mg/day); placebo Baseline calcium 664–680 mg/day | Sex: female Age: 10–12 years Race: not indicated Location: Finland | 195 | Calcium + vitamin D | Calcium | Placebo | |
DXA | ||||||||
Total body BMC (%) | 34.7 | 35.0 | 35.0 | |||||
Femoral neck BMC (%) | 24.0 | 23.3 | 22.4 | |||||
Total femur BMC (%) | 33.6 | 36.4 | 33.6 | |||||
pQCT | ||||||||
Radius CSA | 23.0 | 26.0 | 21.3 | |||||
Radius BMC | 22.6 | 24.4 | 22.2 | |||||
Tibial CSA | 15.6 | 15.8 | 14.8 | |||||
Tibial BMC | 23.0 | 24.3 | 22.7 | |||||
No significant differences | ||||||||
Fortified foods | ||||||||
Calcium citrate-malate, 792 mg/day dissolved in a fruit drink | Lambert et al. 2008 [165] | 18-month randomized trial with follow-up 2 years after supplement withdrawal Low calcium intake at baseline (mean 636 mg/day) Differences in gain no longer apparent 2 years after supplement withdrawal | Sex: 96 girls Age: 11–12 years Race: white Location: Sheffield, UK | 96 | Calcium supplement | Placebo | ||
Total body BMC (g) | 1698 ± 14a
| 1667 ± 14 | ||||||
Lumbar spine BMC | 43.0 ± 0.6a
| 41.1 ± 0.6 | ||||||
Total hip BMC | 27.7 ± 0.3 | 27.2 ± 0.4 | ||||||
Adjusted for baseline values, age at menarche, and age at menarche × visit interaction | ||||||||
Calcium-enriched beverage, 1200 mg/day | Gibbons et al. 2004 [166] | 18-month placebo-controlled, double-blind RCT of a high-calcium beverage. Controls received 400 mg/day Baseline calcium intake: 934, supplement; 985, placebo 12-month additional follow-up after end of intervention | Sex: male and female Age: 8–10 years Race: NZ European or Pakeha Location: New Zealand | 154 | Treatment | Control | ||
Total body BMD | 4.4 % | 3.3 % (NS) | ||||||
Hip BMD | 4.8 % | 3.9 % (NS) | ||||||
Spine BMD | 5.9 % | 5.8 % (NS) | ||||||
Trochanter BMD | 6.2 % | 5.1 % (NS) | ||||||
Femoral neck BMD | 6.7 % | 7.0 % (NS) | ||||||
Calcium-fortified foods, 850 mg/day | Chevalley et al. 2005 [168] | 1-year double-blind RCT of calcium-fortified foods (850 mg/day) compared to an isocaloric control | Sex: male Age: 6.5–8.5 years Race: white Location: Switzerland | 235 | Spine BMD (L2–4) Femoral diaphysis BMD Femoral neck BMD Trochanter BMD Radius BMD | No difference in gain 19 % greater increase in trt (P < 0.006) 3 % lesser increase (NS) 22 % greater (NS) 15 % greater (NS) | ||
600 mg calcium in 375 mL soymilk | Ho et al. 2005 [167] | 1-year follow-up study between 104 adolescent girls receiving the fortified food and 95 girls in the control group | Sex: female Age: 14–16 years Race: Chinese Location: Hong Kong, China | 210 | Mean % change treatment ± SD | Mean % change, control | ||
Neck of the femur BMD | 2.7 ± 2.94 | 1.8 ± 3.49 | ||||||
Trochanter BMD | 3.3 ± 3.27a
| 1.6 ± 2.94 | ||||||
Intertrochanter BMD | 3.6 ± 3.05a
| 2.32 ± 2.95 | ||||||
Total hip BMD | 3.1 ± 2.39a
| 2.05 ± 2.22 | ||||||
Total hip BMC | 3.8 ± 3.05a
| 2.6 ± 2.96 | ||||||
Dairy foods | ||||||||
Dairy foods, 1000 mg/day | Merrilees et al. 2000 [169] | 2-year RCT of dairy foods Baseline calcium: 744, supplement; 765, control 1 year after end of supplementation, differences no longer seen | Sex: female Age: 15–17 years Race: unspecified NZ Location: New Zealand | 91 | Spine BMD Trochanter BMD Femoral neck BMD | 1.5 % greater increase in trt (P < 0.05) 4.6 % greater increase in trt 4.8 % greater increase in trt | ||
330 mL UHT milk (560 mg calcium), 330 mL UHT milk + 200 or 320 IU vitamin D3, or control | Du et al. 2004 [170] | 2-year school-based randomized trial | Sex: female Age: 10–12 years Race: Chinese Location: Beijing, China | 757 | Total body BMC Bone area | 35.9 % (P = 0.03) 31.3 % greater increase in trt (P = 0.2) |
Reference | Study description | Population description | Number of subjects | End points | Results | |
---|---|---|---|---|---|---|
Molgaard et al. 2001 [245] | 1-year prospective observational study to determine effects of dietary calcium and physical activity on bone changes. | Sex: 140 boys, 192 girls Age: 5–19 years at baseline Race: Caucasian Location: Copenhagen, Denmark | 332 | Correlation with calcium intake, r
| Correlation with physical activity, r
| |
Whole bone area gain adjusted for height and weight | 0.03, girls | 0.28 | ||||
−0.34, boys | 0.28 | |||||
Total body BMC gain adjusted for bone area, height, and weight | 0.21, girls | −0.06 | ||||
0.34, boys | −0.04 | |||||
Carter et al. 2001 [171] | Cross-sectional study to investigate the relationship between calcium intake and BMC. | Sex: 108 boys and 119 girls Mean age: 13 years Race: Primarily Caucasian Location: Saskatoon Canada | 227 | Total body BMC | No association | |
Lumbar spine BMC | No association | |||||
Lloyd et al. 2000 [174] | 6-year prospective study to determine effects of dietary calcium and physical activity on bone changes | Sex: girls Age: 12–18 years at baseline Race: Caucasian Location: Pennsylvania | 81 | Total body BMC gain | NS | |
Total body BMD gain | NS | |||||
Femoral neck BMDa
|
r = 0.42 with exercise | |||||
Lappe et al. 2014 [172] | 6-year prospective study of calcium intake and physical activity on bone accrual | Sex: boys and girls Age: 5–16 years at baseline Race: white, black, Asian, Hispanic, and non-Hispanic Location: 5 sites in the USA | 1743 | Mixed-model analyses | ||
Total body BMC gaina
| Associated with physical activity in nonblacks | |||||
Spine BMC gaina
| Associated with physical activity in blacks and nonblack males | |||||
Total hip BMC gaina
| Associated with calcium in nonblack females | |||||
Adjusted for changes in height, age, and baseline BMC | Associated with physical activity in nonblacks and black males |
Reference | Study description | Population description | Number of subjects | Primary end points | Results | ||||
---|---|---|---|---|---|---|---|---|---|
RCTs | |||||||||
Du et al. 2004 [170] | This study was a 2-year milk intervention trial in girls from nine primary schools in Beijing. Schools were randomized into three groups: (1) a carton of 330-mL milk fortified with calcium per school day, (2) a carton of 330-mL milk fortified with 200 or 320 IU 8 mg vitamin D3, and (3) control | Sex: female Age: 10–12 years Race: Asian (Chinese) Location: Beijing, China Year(s): 1999–2001 Baseline 25(OH)D as mean (SD) in nmol/L: Control: 19.1 (7.4) Calcium only: 17.7 (8.7) Calcium + vitamin D: 20.6 (8.8) | 757 | Data are shown for a subsample with bone measures (N = 346) | Percent change |
P
| |||
Milk with calcium (n = 111) | Milk with calcium + vitamin D (n = 113) | Control (n = 122) | |||||||
Total body | |||||||||
Bone area | 29.5 | 28.5 | 31.3 | NS | |||||
BMC | 38.4 | 39.7 | 35.9 | <0.01 | |||||
Percent change, calcium + vitamin D, minus calcium |
P
| Percent change, calcium + vitamin D, minus control |
P
| ||||||
Total body | |||||||||
Bone area | 0.8 | NS | −1.8 | 0.04 | |||||
BMC | −0.8 | NS | 2.6 | <0.01 | |||||
Size-adjusted BMC | 1.3 | <0.01 | 2.4 | <0.01 | |||||
• Mean percent change values in the calcium + vitamin D group were significantly different from controls. • Adjusted percentage difference in change values are adjusted for baseline. • Size-adjusted BMC is adjusted for baseline BMC, bone area, height, weight, and menstrual status. | |||||||||
Cheng et al. 2005 [159] | The purpose of this study was to examine the effects of both food-based and pill supplements of calcium and vitamin D3 on bone mass and body composition. Children were randomized into four groups: (1) 1000 mg calcium + 200 IU vitamin D3, (2) 1000 mg calcium + vitamin D3 placebo, (3) 1000 mg calcium from dairy products,and (4) calcium + vitamin D3 placebo for 2 years | Sex: female Age: 10–12 years Race: Finnish, otherwise unspecified Location: Jyvaskyla and surrounding cities in Central Finland Year(s): Unspecified Baseline 25(OH)D as mean (95 % CI): 45.9 (43.8, 48.0) nmol/L | 195 | Data are shown for the overall group who started the intervention (N = 181) | Percent change |
P
| |||
Calcium (n = 41) | Calcium + vitamin D3 (n = 46) | Cheese (n = 39) | Placebo (n = 39) | ||||||
Lumbar spine | |||||||||
Bone area | 28.4 | 23.0 | 25.3 | 23.4 | NS | ||||
BMC | 24.0 | 46.9 | 52.4 | 47.0 | NS | ||||
Total hip | |||||||||
Bone area | 24.1 | 17.0 | 18.1 | 17.3 | NS | ||||
BMC | 20.3 | 33.6 | 36.9 | 33.6 | NS | ||||
Femoral neck | |||||||||
Bone area | 3.8 | 12.6 | 13.1 | 15.0 | NS | ||||
BMC | 3.3 | 24.0 | 26.5 | 22.4 | NS | ||||
Radius | |||||||||
CSA | 26.0 | 23.0 | 26.2 | 21.3 | NS | ||||
BMC | 24.4 | 22.6 | 25.9 | 22.2 | NS | ||||
vBMD | 2.6 | 3.4 | 3.1 | 2.0 | NS | ||||
Polar moment of inertia | 62.0 | 53.3 | 61.8 | 51.8 | NS | ||||
Tibia | |||||||||
CSA | 15.8 | 15.6 | 15.9 | 14.8 | NS | ||||
BMC | 24.3 | 23.0 | 25.2 | 22.7 | NS | ||||
vBMD | 7.5 | 6.9 | 8.3 | 7.8 | NS | ||||
Cortical bone thickness | 29.8 | 31.7 | 37.1 | 31.1 | NS | ||||
Polar moment of inertia | 41.5 | 41.3 | 42.6 | 39.7 | NS | ||||
• Data presented above show no interaction between the groups with the intent-to-treat analysis. • There was a significant interaction with cortical thickness of the tibia between the groups (P < 0.05) where this measure increased more in the cheese group with a compliance >50 % versus placebo (P = 0.01), calcium + vitamin D (P < 0.01), or calcium (P = 0.04). • Bonferroni correction for multiple comparisons was applied to these analyses. | |||||||||
El-Hajj Fuleihan et al. 2006 [175] | Musculoskeletal responses were determined in response to weekly doses of vitamin D3 (1400 and 14,000 IU) over 1 year | Sex: female Age: 10–17 years Race: Lebanese, otherwise unspecified Location: greater Beirut, Lebanon area Year(s): 2001–2003 Baseline 25(OH)D as mean (SD): 14 (8) ng/ml | 179 | Data are shown for the overall group (N = 168) | Percent change |
P
| |||
High-dose treatment, 14,000 IU/week (n = 55) | Low-dose treatment, 1400 IU/week (n = 58) | Placebo (n = 55) | |||||||
Lumbar spine | |||||||||
Bone area | 4.3 | 5.0 | 4.0 | NS | |||||
BMC | 12.9 | 14.5 | 10.8 | NS | |||||
Total hip | |||||||||
Bone area | 5.7 | 4.0 | 2.4 | <0.01 | |||||
BMC | 12.8 | 11.2 | 7.8 | 0.02 | |||||
Femoral neck | |||||||||
Bone area | 0.8 | 0.0 | 0.7 | NS | |||||
BMC | 5.2 | 4.4 | 3.9 | NS | |||||
Trochanter | |||||||||
Bone area | 7.8 | 6.8 | 4.7 | NS | |||||
BMC | 14.2 | 13.6 | 9.4 | NS | |||||
Total body | |||||||||
Bone area | 6.2 | 6.1 | 5.0 | NS | |||||
BMC | 12.0 | 11.3 | 8.7 | NS | |||||
Lean mass | 9.0 | 8.7 | 5.7 | 0.05 | |||||
• In premenarchal girls, trochanter BMC and lean mass reached significance. • Postmenarchal girls did not exhibit significant changes in any parameters of interest. | |||||||||
Viljakainen et al. 2006 [177] | This study sought to determine the effect of vitamin D3 supplementation (200 or 400 IU/day) for 1 year on bone mineral augmentation in adolescent girls with adequate dietary calcium intake. | Sex: female Age: 11.4 ± 0.4 years Race: white Location: Helsinki, Finland Year(s): 2001–2003 Baseline 25(OH)D as mean (SD) in nM: Placebo: 47.8 (18.2) 5 μg/day: 46.3 (17.4) 10 μg/day: 46.7 (16.2) | 228 | Data are shown for the overall group (N = 212) | Mean change |
P
| |||
High-dose treatment, 400 IU/day (n = 74) | Low-dose treatment, 200 IU/day (n = 65) | Placebo (n = 73) | |||||||
Lumbar spine | |||||||||
Bone area (cm2) | 3.8 | 4.1 | 3.5 | NS | |||||
BMC (g) | 6.2 | 5.9 | 5.1 | NS | |||||
Femur | |||||||||
Bone area (cm2) | 2.0 | 2.2 | 2.4 | NS | |||||
BMC (g) | 3.3 | 3.4 | 3.2 | NS | |||||
• Data presented above are for the intent-to-treat analysis. • In the compliance-based analysis only in the entire sample, vitamin D supplementation vs placebo increased femoral BMC augmentation by 14.3 % with 200-IU doses and by 17.2 % with 400-IU doses (P = 0.012) • In the compliance-based analysis only in the entire sample, a dose–response effect was observed at the lumbar spine with the 400-IU (P = 0.039), but not the 200-IU dose. • In a subanalysis based on puberty (n = 111) and using a compliance-based analysis only, adjusted for Tanner stage, increase in bone area, and weight gain, there was a dose-dependent and significant difference in the lumbar spine BMC augmentation at midpuberty (P = 0.01), but not at early puberty. | |||||||||
Andersen et al. 2008 [180] | The aim of this study was to assess the effect of supplemental vitamin D on bone status in Pakistani immigrants. This 1-year intervention with vitamin D3 (10 and 20 μg /day) included girls (10.1–14.7 years), women (18.1–52.7 years), and men (17.9–63.5 years) of Pakistani origin living in Denmark | Sex: male and female Age: 10–63 years Race: of Pakistani origin Location: Copenhagen area, Denmark Year(s): 2002–2003 Baseline 25(OH)D as median (25th, 75th percentiles) in nmol/L: Placebo: 7.3 (5.3, 23.6) 10 μg/day: 16.9 (12.1, 21.1) 20 μg/day: 8.8 (5.2, 17.1) | 247 | Data are shown for the girls group only (n = 26) | Median value |
P
| |||
20 μg/day (n = 9) | 10 μg/day (n = 9) | Placebo (n = 8) | |||||||
Baseline | |||||||||
Total body | |||||||||
Bone area (cm2) | 1633 | 1497 | 1760 | NS | |||||
BMC (g) | 1473 | 1308 | 1666 | NS | |||||
Lumbar spine | |||||||||
Bone area (cm2) | 39.9 | 41.2 | 43.2 | NS | |||||
BMC (g) | 30.0 | 28.3 | 33.9 | NS | |||||
1 year | |||||||||
Total body | |||||||||
Bone area (cm2) | 1784 | 1669 | 1906 | NS | |||||
BMC (g) | 1625 | 1595 | 1923 | NS | |||||
Lumbar spine | |||||||||
Bone area (cm2) | 42.7 | 42.7 | 46.5 | NS | |||||
BMC (g) | 39.5 | 35.6 | 41.9 | NS | |||||
Data presented above indicate no significant differences between groups at baseline (nonparametric ANOVA) and no effect of the intervention on bone indices. | |||||||||
Khadilkar et al. 2010 [178] | This study investigated the effect of quarterly doses of vitamin D2 supplementation (300,000 IU or 7.5 mg) on BMC in underprivileged adolescent girls over 1 year | Sex: female Age: 14–15 years Race: Indian Location: Pune, India Year(s): 2006–2007 Baseline 25(OH)D as median (25th percentile–75th percentile): Vitamin D + calcium group: 24.5 (12.7–33.2) nmol/L Placebo + calcium group: 20.8 (12.7–30.4) nmol/L | 50 | Data are shown for the overall group (N = 50) | Percent change |
P
| |||
Vitamin D + calcium (n = 25) | Placebo + calcium (n = 25) | ||||||||
Total body | |||||||||
Bone area | 5.1 | 3.6 | NS | ||||||
BMC | 10.1 | 8.2 | NS | ||||||
Lumbar spine | |||||||||
Bone area | 3.3 | 3.9 | NS | ||||||
BMC | 10.5 | 11.3 | NS | ||||||
• Data presented above are unadjusted median percent change values. • After adjusting for age (current), height, weight, lean body mass, initial dietary calcium, and calcium compliance, there was a significant increase in the size and compliance adjusted total BMC and bone area change in subjects who were within 2 years of menarche versus those less than 2 years since menarche (both P ≤ 0.04). | |||||||||
Molgaard et al. 2010 [173] | This study investigated the effect of vitamin D3 supplementation (5 or 10 μg/day) for 1 year on bone mass and bone turnover, as well as the possible influence of VDR and ER genotype on the effect of the supplementation | Sex: female Age: 10–11 years Race: Danish-born citizens, otherwise unspecified Location: Copenhagen and Frederiksberg, Denmark Year(s): 2001–2003 Baseline 25(OH)D as mean (SD) in nmol/L: Placebo: 43.4 (17.1) 5 μg/day: 41.9 (17.6) 10 μg/day: 44.4 (16.6) | 225 | Data are shown for the overall group (N = 225) | Mean change |
P
| |||
High-dose treatment, 400 IU/day (n = 75) | Low-dose treatment, 200 IU/day (n = 75) | Placebo (n = 75) | |||||||
Total body | |||||||||
Bone area (cm2) | 195 | 189 | 188 | NS | |||||
BMC (g) | 249 | 245 | 241 | NS | |||||
Lumbar spine | |||||||||
Bone area (cm2) | 4.9 | 5.5 | 5.6 | 0.04 | |||||
BMC (g) | 7.4 | 8.1 | 8.2 | NS | |||||
• Lumbar spine bone area in the high-dose group differed significantly from placebo. • Vitamin D supplementation increased total body BMC (P = 0.048) in the FF VDR genotype but not in the Ff or ff VDR genotypes. | |||||||||
Ward et al. 2010 [179] | This study aimed to determine the effect of vitamin D2 supplementation (4 doses of 150,000 IU given over 1 year) on the adolescent musculoskeletal system determined by DXA and peripheral quantitative computed tomography. | Sex: female Age: 12–14 years Race: multiethnic, primarily South Asian Location: Manchester, UK Year(s): 2006–2007 Baseline 25(OH)D as mean (SD) in nmol/L: Placebo: 17.9 (7.4) Vitamin D: 18.1 (8.0) | 73 | Data are shown for the overall group (N = 72) | Mean change |
P
| |||
Vitamin D | Placebo | ||||||||
Lumbar spine | |||||||||
Bone area (cm2) | 0.20 | 0.15 | NS | ||||||
BMC (g) | 0.52 | 0.57 | NS | ||||||
Radius 4 % | |||||||||
Total BMD (mg/cm3) | 21.3 | 13.01 | NS | ||||||
Trab BMD (mg/cm3) | 3.07 | 3.23 | NS | ||||||
CSA_4 (mm2) | 6.19 | 9.27 | NS | ||||||
Radius 50 % | |||||||||
CSMA (mm2) | −29.4 | 47.1 | NS | ||||||
CSA_50 (mm2) | −0.67 | −1.91 | NS | ||||||
Ct BMC (mg/mm) | 2.73 | 3.12 | NS | ||||||
Ct BMD (mg/cm3) | 17.4 | 23.9 | NS | ||||||
Ct area (mm2) | 1.26 | 1.28 | NS | ||||||
Cort thk (mm) | 0.10 | 0.12 | NS | ||||||
SSI (mm3) | 3.02 | 6.91 | NS | ||||||
Tibia 4 % | |||||||||
Total BMD (mg/cm3) | 10.5 | 9.79 | NS | ||||||
Trab BMD (mg/cm3) | 9.31 | 7.00 | NS | ||||||
CSA_4 (mm2) | −1.19 | −3.28 | NS | ||||||
Tibia 66 % | |||||||||
CSMA (mm2) | 161.2 | 197.6 | NS | ||||||
CSA_66 (mm2) | 17.09 | 7.70 | NS | ||||||
Ct BMC (mg/mm) | 7.68 | 9.66 | NS | ||||||
Ct BMD (mg/cm3) | 14.26 | 13.98 | NS | ||||||
Ct area (mm2) | 3.98 | 5.85 | |||||||
Cort thk (mm) | −0.02 | 0.09 | |||||||
SSI (mm3) | 116.3 | 85.15 | |||||||
• P values presented above are adjusted for baseline and follow-up weight, follow-up height, and baseline bone measurement. • There were no effects of vitamin D supplementation on bone. | |||||||||
Al-Shaar et al. 2013 [176] | This study investigated the impact of weekly vitamin D3 (1400 and 14,000 IU) on hip geometric dimensions over 1 year. The images were acquired from DXA-derived hip structural analyses | Sex: male and female Age: 10–17 years Race: Lebanese, otherwise unspecified Location: greater Beirut, Lebanon area Year(s): 2001–2003 Baseline 25(OH)D as medians [interquartile range]: Overall, girls: 11.9 [9.1–16.6] ng/ml Overall, boys: 15.5 [6.0–44.9] ng/ml | 338 | Data are shown for females only (n = 167) | Percent change |
P
| |||
High-dose treatment, 14,000 IU/week (n = 54) | Low-dose treatment, 1400 IU/week (n = 58) | Placebo (n = 55) | |||||||
Narrow neck | |||||||||
CSA | 8.1 | 8.3 | 8.2 | NS | |||||
Outer diameter | 2.0 | 0.8 | 2.8 | 0.02 | |||||
Section modulus | 11.4 | 11.3 | 11.7 | NS | |||||
Buckling ratio | −4.2 | −6.5 | −2.0 | 0.05 | |||||
Shaft | |||||||||
CSA | 10.4 | 11.6 | 9.9 | NS | |||||
Outer diameter | 2.1 | 2.3 | 1.4 | NS | |||||
Section modulus | 12.5 | 13.5 | 11.0 | NS | |||||
Buckling ratio | −7.2 | −8.4 | −8.9 | NS | |||||
Intertrochanter | |||||||||
CSA | 8.5 | 9.5 | 7.1 | NS | |||||
Outer diameter | 2.5 | 1.3 | 1.9 | NS | |||||
Section modulus | 12.7 | 13.1 | 10.1 | NS | |||||
Buckling ratio | −3.0 | −5.6 | −3.6 | NS | |||||
• Data presented above were adjusted for baseline height, change in lean mass and height, sun exposure, physical activity, calcium intake, and menarchal status. • Boys did not exhibit significant changes in any parameters of interest. • A dose effect was not detected and no beneficial effect of vitamin D was observed by pubertal stage. | |||||||||
Prospective studies | |||||||||
Breen et al. 2011 [181] | This study sought to determine relationships among 25(OH)D, IGF-I, and bone in prepubertal females over a period of up to 9 years (median of 5 years) | Sex: female Age: 4–8 years Race: white and black Location: Georgia, USA Year(s): 1997–2008 | 76 | Data are shown for the overall group (N = 76) | Combined 25(OH)D + IGF-I | 25(OH)D | IGF-I | ||
BMC | |||||||||
Total body | 0.84 | 0.81 | 0.87 | ||||||
Lumbar spine | 0.72 | 0.70 | 0.76 | ||||||
Proximal femur | 0.81 | 0.77 | 0.85 | ||||||
Forearm | 0.78 | 0.76 | 0.81 | ||||||
• Data are presented above as R
2 and the linear mixed models regressed BMC on age, IGF-I, 25(OH)D, season, and race, and interactions among these variables and show that IGF-I was more strongly associated with BMC accrual than 25(OH)D at all sites • The rate of BMC accrual was negatively associated with 25(OH)D. When IGF-I and 25(OH)D were included in the same regression equation, 25(OH)D did not have a significant predictive effect on BMC accrual above and beyond that of IGF-I. | |||||||||
Cross-sectional studies | |||||||||
Cheng et al. 2003 [182] | Associations of serum 25(OH)D with BMC at different bone sites were measured by DXA and pQCT. | Sex: female Age: 10–12 years Race: Finnish, otherwise unspecified Location: Jyvaskyla, Finland Year(s): 1999–2000 | 193 | Data are shown for the overall group (N = 193) | Deficient, ≤25 nmol/L (n = 61) | Insufficient, 26–40 nmol/L (n = 89) | Sufficient, >40 nmol/L (n = 43) |
P
| |
Total body | |||||||||
Bone area (cm2) | 1468 | 1475 | 1436 | NS | |||||
BMC (g) | 1380 | 1414 | 1347 | NS | |||||
Femur | |||||||||
Bone area (cm2) | 23.9 | 23.7 | 23.1 | NS | |||||
BMC (g) | 19.7 | 20.4 | 18.9 | 0.05 | |||||
Femoral neck | |||||||||
Bone area (cm2) | 3.837 | 3.84 | 3.67 | NS | |||||
BMC (g) | 3.21 | 3.30 | 3.13 | NS | |||||
Lumbar spine | |||||||||
Bone area (cm2) | 27.5 | 28.1 | 27.3 | NS | |||||
BMC (g) | 22.6 | 23.9 | 21.9 | NS | |||||
Distal radius | |||||||||
Whole bone CSA (mm2) | 241 | 226 | 209 | <0.01 | |||||
Whole bone vBMD (mg/cm3) | 273 | 292 | 298 | <0.01 | |||||
Trabecular vBMD (mg/cm3) | 221 | 229 | 231 | NS | |||||
Tibia shaft | |||||||||
Whole bone CSA (mm2) | 368 | 372 | 363 | NS | |||||
Whole bone vBMD (mg/cm3) | 848 | 865 | 853 | 0.02 | |||||
Trabecular vBMD (mg/cm3) | 525 | 534 | 524 | NS | |||||
• Data are adjusted for Tanner stage and BMI. • P value is shown with Bonferroni adjustment in the ANOVA for multiple comparisons. • Sufficient is different from the insufficient group in BMC of the femur (P = 0.04). • Sufficient is different from the deficient group in whole bone CSA and vBMD of the radius (P < 0.01). • Insufficient is different from the deficient group in whole bone CSA (P = 0.05) and vBMD (P < 0.01) of the radius and whole bone vBMD (P < 0.02) of the tibia. | |||||||||
Foo et al. 2009 [183] | This cross-sectional study investigated the influence of low vitamin D status on bone mass, bone turnover, and muscle strength. | Sex: female Age: 15 years Race: Chinese, otherwise unspecified Location: Beijing, China Year(s): 2004 | 301 | Data are shown for the overall group (N = 301) | Severe deficiency, <25 nmol/L (n = 94) | Deficiency, ≤50 nmol/L (n = 174) | Sufficient, >50 nmol/L (n = 33) |
P trend | |
Size-adjusted BMC (g) | |||||||||
Total body | 2230 | 2291 | 2417 | <0.01 | |||||
Proximal forearm | 1.44 | 1.47 | 1.53 | <0.01 | |||||
Distal forearm | 1.10 | 1.52 | 1.86 | <0.01 | |||||
Data are presented as means adjusted for pubertal breast stage, handgrip muscle strength, organized sports participation, physical activity level, dietary vitamin D, and calcium. | |||||||||
Lee et al. 2013 [184] | Risk factors were evaluated for low 25(OH)D status and its relationships with bone health | Sex: male and female Age: 9.3 ± 1.9 years Race: Korean, otherwise unspecified Location: Seoul and Gyeonggi-do, South Korea Year(s): unspecified | 100 | Data are shown for the overall group (N = 100) | Total body BMC |
P
| |||
Unadjusted | 0.028 | 0.08 | |||||||
Adjusted model 1 | 0.02 | 0.07 | |||||||
Adjusted model 2 | 0.02 | 0.04 | |||||||
• Data presented above are β scores correlating 25(OH)D with BMC and corresponding P values using multiple linear regression analyses • Model 1 is adjusted for sex, puberty, fat mass, and lean mass • Model 2 is adjusted for model 1 variables + physical activity and calcium intake |
Micronutrient | Reference | Study description | Population description | Number of subjects | End points | Results | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
RCTs | |||||||||||
Magnesium | Carpenter et al. 2006 [185] | 1-year placebo-controlled, double-blind RCT of 300 mg/day supplementation of MgO | Sex: female Age: 8–14 years Race: white Location: New Haven, CT | 44 | BMC of total hip, femoral neck, Ward’s area, and lumbar spine | Combined overall hip | |||||
Treatment | Placebo | ||||||||||
1.05 % | 0.97 %, P = 0.0534 | ||||||||||
Prospective studies | |||||||||||
Fluoride | Levy et al. 2009 [187] | Lifetime associations of average daily fluoride intake and DXA bone outcomes at age 11 years | Sex: male and female Age: birth to 11 years for fluoride assessments; mean age 11.2 years for DXA assessment Race: 97 % white Location: Iowa Year(s): recruitment took place from 1992 to 1995 (fluoride study) and from 1998 to 2000 (bone development study) | 481 | BMC | Hip | Spine | Total body less head | |||
Girls | |||||||||||
0–11 years | 0.07, NS | 0.17, NS | 0.10, NS | ||||||||
0–8.5 years | 0.04, NS | 0.13, NS | 0.08, NS | ||||||||
0–3 years | 0.03, NS | 0.06, NS | 0.05, NS | ||||||||
3–6 years | −0.01, NS | 0.05, NS | 0.02, NS | ||||||||
6–8.5 years | 0.11, NS | 0.19, 0.01 | 0.16, NS | ||||||||
85.5–11 years | 0.18, 0.01 | 0.24, <0.01 | 0.19, NS | ||||||||
Boys | |||||||||||
0–11 years | 0.21, 0.01 | 0.23, 0.01 | 0.23, 0.01 | ||||||||
0–8.5 years | 0.21, 0.01 | 0.23, 0.01 | 0.24, 0.01 | ||||||||
0–3 years | 0.22, 0.01 | 0.22, 0.01 | 0.23, 0.01 | ||||||||
3–6 years | 0.14, NS | 0.18, NS | 0.19, 0.01 | ||||||||
6–8.5 years | 0.09, NS | 0.12, NS | 0.10, NS | ||||||||
85.5–11 years | 0.14, NS | 0.14, NS | 0.15, NS | ||||||||
• Data are from unadjusted bivariate associations (r) with fluoride intake and bone outcomes and corresponding P value. • No statistically significant relationships between daily fluoride intake and bone measures were found in adjusted models (for age, height, weight, and Tanner stage). | |||||||||||
Fluoride | Levy et al. 2014 [188] | Lifetime associations of average daily fluoride intake and DXA bone outcomes at age 15 years | Sex: male and female Age: birth to 15 years for fluoride assessments; mean age 15.3 years for DXA assessments Race: 98 % white Location: Iowa Year(s): recruitment took place from 1992 to 1995 (fluoride study) and from 1998 to 2000 (bone development study) | 358 | BMC | Females | Males | ||||
ß |
R
2
| Partial R
2
| ß |
R
2
| Partial R
2
| ||||||
Total body less head | 234, 0.02 | 0.03 | 0.03 | 182, NS | 0.02 | 0.02 | |||||
Spine | 7.32, 0.04 | 0.03 | 0.03 | 5.24, NS | 0.02 | 0.02 | |||||
Hip | 2.92, NS | 0.01 | 0.01 | 1.79, NS | <0.01 | <0.01 | |||||
• Data are from unadjusted bivariate associations (β) with fluoride intake and bone outcomes and corresponding P value. • With adjustment for height, weight, time since PHV, Tanner stage, calcium intake, and physical activity, none of the associations remained statistically significant. • No significant differences were observed between fluoride intake and bone measures across tertiles of fluoride intake from birth to 15 years. | |||||||||||
Observational studies | |||||||||||
Vitamin K | O’Connor et al. 2007 [191] | Cross-sectional associations of undercarboxylated osteocalcin (%ucOC) as an index of vitamin K status and BMC | Sex: female Age: 11–12 years Race: presumed white Location: Denmark | 223 | Serum %ucOC and total body BMC |
β = −0.045, P = 0.016 | |||||
Lumbar BMC |
β = −0.055, P = 0.037 | ||||||||||
Sodium | Hoppe et al. 2000 [149] | Cross-sectional analysis of nutrient intakes determined by 7-day diet records and bone | Sex: half were female, half were male Age: 10 years Race: presumed white Location: Denmark Year(s): 1997–1998 | 105 | Total body BMC |
r = −0.206, P < 0.05 | |||||
Anterior–posterior projected bone area (cm2) |
r = −0.215, P < 0.05 | ||||||||||
Phosphorous | Hoppe et al. 2000 [149] | Cross-sectional analysis of nutrient intakes determined by 7-day diet records and bone | Sex: half were female and half were male Age: 10 years Race: presumed white Location: Denmark Year(s): 1997–1998 | 105 | Total body BMC |
r = −0.297, P < 0.01 | |||||
Anterior–posterior projected bone area (cm2) |
r = −0.284, P < 0.01 | ||||||||||
Vitamin C | Prynne et al. 2006 [189] | Cross-sectional Cambridge Bone Studies to relate fruit and vegetable and nutrient intake from 7-day food diaries in 5 age and sex cohorts | Sex: female and male, nearly half of each Age: 16–19 years Race: presumed white Location: UK | 257 | Percent change with doubling in vitamin C intake from univariate analysis, in 4th-grade girls only | ||||||
Boys | Girls | ||||||||||
Total body BMC | 5.5, P < 0.01 | 1.4, NS | |||||||||
Spine BMC | 5.6, P < 0.05 | 2.1, NS | |||||||||
Total hip BMC | 5.7, P < 0.05 | −0.05, NS | |||||||||
Femoral neck BMC | 5.4, P < 0.01 | 5.2, NS | |||||||||
Trochanter BMC | 5.8, P < 0.05 | 2.5, NS | |||||||||
Vitamin C, zinc, and iron | Laudermilk et al. 2012 [190] | Cross-sectional analysis of nutrient intakes determined by the Harvard Youth/Adolescent Food frequency Questionnaire | Sex: female Age: 8–12 years, 4th- and 6th-grade students Race: ~87 % white, 7 % Asian, 3 % black, 2 % Latino and 1 % Native Hawaiian Location: Tucson, Arizona | 453 (n = 184 4th graders, n = 179 6th graders) | pQCT | Vitamin C | Zinc | ||||
Femur 20 % site | |||||||||||
Cortical density | NS | 0.16, P < 0.05 | |||||||||
Periosteal circumference | 0.17, P < 0.05 | NS | |||||||||
Endosteal circumference | 0.17, P < 0.05 | NS | |||||||||
SSI | 0.18, P < 0.05 | NS | |||||||||
Tibia 4 % site | |||||||||||
Trabecular area | 0.18, P < 0.05 | NS | |||||||||
Periosteal circumference | 0.19, P < 0.01 | NS | |||||||||
Tibia 66 % site | |||||||||||
Cortical density | NS | 0.15, P < 0.05 | |||||||||
Cortical area | 0.15, P < 0.05 | NS | |||||||||
SSI | 0.18, P < 0.05 | NS | |||||||||
In regression modeling, iron was negatively associated with femoral cortical area and tibia SSI. | |||||||||||
Fluoride | Grobler 2009 [186] | This field study included the whole population of children aged 10–15 years living in areas of high and low fluoride in the drinking water. | Sex: male and female Age: 10–15 years Race: not specified, but of mixed ethnicity (i.e., from Khoi, Caucasian, and Negroid roots that developed into a homogenous ethnic group over many years) Location: South Africa Year(s): not specified | 166 (n = 77 from a 0.19 mg/L F area; n = 89 from a 3.00 mg/L F area) | High fluoride | Low fluoride |
P
| ||||
Girls | Boys | Girls | Boys | ||||||||
Radius BMC (g) | |||||||||||
10–11 years | 1.29 | 1.29 | 1.26 | 1.32 | NS | ||||||
12–13 years | 1.56 | 1.41 | 1.33 | 1.29 | <0.05a
| ||||||
14–15 years | 1.80 | 1.80 | 1.18 | 1.52 | <0.05a
| ||||||
Radius bone width (cm) | |||||||||||
10–11 years | 0.97 | 0.98 | 0.98 | 1.01 | NS | ||||||
12–13 years | 1.09 | 1.08 | 1.04 | 1.15 | NS | ||||||
14–15 years | 1.10 | 1.14 | 1.18 | 1.21 | NS |
Food | Source | Study description | Population description | Number of subjects | End points | Results | |||
---|---|---|---|---|---|---|---|---|---|
RCTs | |||||||||
Dairy | Du et al. 2004 [170] | 2-year school-based randomized trial of 330 mL milk, 330 mL milk + 5 or 8 μg vitamin D3, or control | Sex: female Age: 10–12 years Race: Chinese Location: Beijing, China | 757 | Group mean increase |
P
| |||
Treatment | Placebo/control | ||||||||
Height | 0.95 % | 0.087 % | <0.0005 | ||||||
Total body BMC | 38.4 % | 35.9 % | 0.03 | ||||||
Bone area | 29.5 % | 31.3 % | 0.2 | ||||||
Dairy | Courteix et al. 2005 [158] | 12-month randomized, double-blind, placebo-controlled study Baseline calcium: supplement = 1008 (398); placebo = 988 (345) Was combined with an exercise intervention that found a combined effect not reported here. After randomization, fewer subjects were in the dairy group than in the placebo group (34 vs 79, respectively, at the baseline). It was expected that 240 subjects would be recruited, but because of the publicity surrounding Mad Cow disease, many parents were afraid of dairy products. | Sex: premenarchal female Age: 8–13 years Race: Caucasian Location: France | 113 | Calcium supplement | Placebo | |||
Total body | BMC | 155 ± 79 | 166 ± 66 | ||||||
Lumbar spine | BMC | 3.429 ± 2.388 | 3.228 ± 2.642 | ||||||
Femoral neck | BMC | 0.248 ± 0.187 | 0.185 ± 0.103 | ||||||
Trochanter | BMC | 0.941 ± 0.525 | 0.796 ± 0.582 | ||||||
Wards | BMC | 0.001 ± 0.054 | 0.047 ± 0.086 | ||||||
Ultradistal radius | BMC | 0.104 ± 0.091 | 0.111 ± 0.107 | ||||||
Mid radius | BMC | 0.305 ± 0.230 | 0.355 ± 0.322 | ||||||
1/3 distal | BMC | 0.072 ± 0.078 | 0.093 ± 0.077 | ||||||
Adjusted for lean tissue mass. All NS | |||||||||
Dairy | Cheng et al. 2005 [159] | 2 year double-blind, placebo-controlled RCT of calcium (1000 mg) + vitamin D3 (200 IU), calcium (1000 mg), cheese (1000 mg calcium), and placebo | Sex: female Age: 10–12 years Race: presumed white Location: Finland | 195 | Cheese |
P
| |||
Total body | BMD (%) | 10.4 | 8.9 (compliance >50) | 0.044 | |||||
Femoral neck | BMC (%) | 26.5 | 22.4 | NS | |||||
Total femur | BMC (%) | 36.9 | 33.6 | NS | |||||
Spine | BMC (%) | 52.4 | 47.0 | NS | |||||
Tibia cortical thickness | pQCT (%) | 37.1 | 31.1 (compliance 50) | 0.01 | |||||
Dairy | Merrilees et al. 2000 [169] | 2-year RCT of dairy food supplementation and 1-year follow-up after cessation of intervention | Sex: female Age: 15–17 years Race: presumed white Location: New Zealand Stratified by forearm BMD at baseline | 91 | Total body | BMC (g) | 168.9 | 167.4 | NS |
Lumbar spine | BMC (g) | 3.83 | 2.58 | NS | |||||
Femoral neck | BMC (g) | 0.12 | 0.06 | NS | |||||
Trochanter | BMC (g) | 0.75 | 0.25 | <0.05 | |||||
Difference disappeared 1 year after cessation | |||||||||
Fiber | Abrams et al. 2005 [193] | 1-year placebo-controlled RCT of 8 g/day mixed short and long inulin-type fructans | Sex: half were male and half were female Age: 9–13 years Tanner stage 2 or 3 Race: 53 % white, 14 % black, 22 % Hispanic, 10 % Asian Location: Houston, TX Between 5th and 95th percentile BMI | 100 | Total body | BMC, % | 18.3 | 16.7 | 0.03 |
Observational studies | |||||||||
Total diet | Wosje et al. 2010 [335] | Prospective study with cross-sectional analysis by age to relate 3-day diet records to fat and bone mass in children during the age period of 3.8–7.8 years, using reduced-rank regression | Sex: male and female (167/158) Age: 3.8–7.8 years Race: 75 % white, 25 % black Location: Cincinnati, OH Year(s): 2000–2004 | 325 | Fat mass (kg) Bone mass (g) | Diets high in dark-green and deep-yellow vegetables and processed meats and low in fried foods were associated with lower fat mass (P < 0.001) and higher bone mass (P = 0.03 for year 1, P = 0.2 for year 2, and P < 0.01 for years 3 and 4) | |||
Fruits and Vegetables | Prynne et al. 2006 [189] | Cross-sectional Cambridge Bone Studies to relate fruit and vegetable and nutrient intake from 7-day food diaries in 5 age and sex cohorts | Sex: female and male, nearly half of each Age: 16–19 years Race: presumed white Location: UK | 257 | Percent change with doubling in fruit and vegetable intake from univariate analysis | ||||
Boys |
P
| Girls |
P
| ||||||
Total body BMC | 9.2 | <0.001 | 5.2 | 0.02 | |||||
Spine BMC | 7.8 | 0.002 | 8.8 | 0.001 | |||||
Total hip BMC | 6.6 | 0.008 | 5.0 | 0.04 | |||||
Femoral neck BMC | 10.3 | <0.001 | 6.5 | 0.07 | |||||
Trochanter BMC | 7.9 | 0.01 | 5.2 | NS | |||||
Fruits and vegetables | McGartland et al. 2004 [195] | Cross-sectional study on effect of fruit and vegetable intake on BMD | Sex: male and female Age: 12 and 15 years Race: presumed white Location: Northern Ireland | 1345 | Forearm BMD Heel BMD | 12-year-old girls consuming high amounts of fruit had significantly higher heel BMD (β = 0.037; 95 % CI, 0.017, 0.056). No other associations were observed. | |||
Fruits and vegetables | Tylavsky et al. 2004 [196] | Cross-sectional study on the effect of low (<3 servings) versus high (≥3 servings) fruit and vegetable intake on urinary calcium excretion and bone mass | Sex: female Age: 8–13 years Race: white Location: Tennessee, USA | 56 | Total body bone area Wrist bone area | Compared with the low-consumption group, the high fruit and vegetable consumption group had 6 and 8.3 % larger total body (P < 0.03) and wrist bone area (P < 0.03). | |||
Total body BMC Wrist BMC | Whole body and wrist BMC was 7.4 (P = 0.07) and 7.0 % (P = 0.09) larger in the high-consumption group (P > 0.05). | ||||||||
Total body BMD Wrist BMD | Whole body and wrist BMD did not differ significantly between the low- and high-consumption groups (P > 0.05). | ||||||||
Urinary calcium | Those reporting high fruit and vegetable intake had lower concentrations of urinary calcium/kg body weight (P < 0.02). | ||||||||
Fruits and vegetables | Whiting et al. 2004 [197] | Cross-sectional study of bone growth in children | Sex: male and female Age: 8–14 years Race: presumed white Location: Saskatoon, Canada Year(s): 1991–1997 | 131 | BMC | Fruit and vegetable intake appears to influence BMC in adolescent girls but not boys. | |||
Fruits and vegetables | Vatanparast et al. 2005 [198] | Cross-sectional study on the effect of milk products, vegetables, and fruit on total body BMC | Sex: male and female Age: 8–20 years Race: presumed white Location: Saskatoon, Canada Year(s): 1991–1997 | 150 | Total body BMC | Fruit and vegetable intake was a significant independent predictor of total body BMC in boys but not girls. | |||
Caffeine | Conlisk and Galuska 2000 [204] | Cross-sectional study on effect of caffeine on BMD in healthy women | Sex: 177 women Age: 19–26 years Race: presumed white Location: Midwestern USA Year(s): 1991 | 177 | Caffeine consumption for past 12 weeks by self-report BMD at the lumbar spine and femoral neck by DXA | Caffeine was not significantly associated with BMD. | |||
Carbonated beverages | Wyshak 2000 [200] | Cross-sectional study of carbonated beverage consumption and bone fractures | Sex: girls Age: 9th and 10th graders (mean age 15.8 years) Race: unspecified, American high school students Location: “urban high school,” USA | 460 | Self-reported physical activity, carbonated beverage consumption, and bone fractures | Carbonated beverage consumption and bone fractures were associated (OR, 3.14; 95 % confidence limit, 1.45, 6.78; P = 0.004). | |||
Carbonated beverages | McGartland et al. 2003 [194] | Cross-sectional observational study of the association between CSDs and BMD in postprimary schools in Northern Ireland | Sex: 744 girls, 591 boys Age: 12 years (323 boys, 376 girls); 15 years (268 boys, 368 girls) Race: presumed white Location: Belfast, Northern Ireland Year(s): 2000 | 1335 | CSD consumption via RD-administered dietary history method BMD of the nondominant forearm (distal radius) and dominant heel (os calcis) by DXA | A significant inverse relationship between total CSD intake and BMD was observed in girls at the dominant heel (β, −0.099; 95 % CI, −0.173 to −0.025). Non-cola consumption was inversely associated with dominant heel BMD in girls (β, −0.121; 95 % CI, −0.194 to −0.048), and diet drinks were also inversely associated with heel BMD in girls (β, −0.087; 95 % CI, −0.158 to −0.016). No consistent relationships were observed between CSD intake and BMD in boys. | |||
Carbonated beverages | Ma and Jones 2004 [199] | Population-based case–control study to investigate the association between soft drink and milk consumption, physical activity, bone mass, and upper limb fractures in children aged 9–16 years | Sex: half male and half female Age: 9–16 years Race: presumed white Location: Tasmania, Australia Year(s): 1998–2002 | 206 fractures 206 controls | Bone mass using DXA at the total body, lumbar spine, right femoral neck: BMC aBMD BMAD Soft drink and dairy drink consumption (in-person interview) | None of the drink types (milk, cola, and carbonated drinks) was significantly different between cases and controls for total fracture. For wrist and forearm fractures, there was a positive association between cola drink consumption and fracture risk (OR, 1.39/unit; 95 % CI, 1.01, 1.91). | |||
Carbonated beverages | Manias et al. 2006 [201] | Cross-sectional study of recurrent fracture, diet, and physical activity | Sex: 78 girls, 72 boys Age: 4–16 years Race: presumed white Location: Sheffield, UK | 150 | Bone area, BMC, BMD of spine, lower body, and upper body by DXA Fracture history and trauma severity Diet (including beverage consumption), physical activity, and other lifestyle factors via questionnaires | Children with recurrent fractures had a significantly lower milk intake, lower levels of physical activity, a higher BMI, and a higher consumption of carbonated beverages than controls. | |||
Carbonated beverages | Libuda et al. 2008 [202] | Prospective (DONALD) study of diet from 3-day diet records for 4 years prior to a single forearm pQCT measure | Sex: 113 girls, 115 boys Age: 6–18 years Race: presumed white Location: Germany | 228 | Forearm pQCT | Carbonated beverage consumption was inversely associated with BMC (P < 0.05), cortical area (P < 0.05), and polar strength strain index (P < 0.05), polar strength strain index (P < 0.01), and periosteal circumference (P < 0.05) of the radius assessed by pQCT, after adjustment for age, sex, total energy intake, muscle area, BMI SD scores, and growth velocity. |
Source | Study description | Population description | Number of subjects | End points | Results | ||
---|---|---|---|---|---|---|---|
Koo et al. 2003 [211] | 6-month randomized, double-blind, parallel study assessing changes in bone mineral accretion by DXA in healthy infants fed a milk-based formula with or without palm olein | Sex: 57 males, 71 females Age: Infants >2 weeks at baseline Race:72 African American, 48 Caucasian, 8 Hispanic/Asian/other Location: USA and Canada | 128 | Total body BMC (%) | Group mean increase | ||
Breast-fed | Control formula (milk-based formula) | Treatment (milk-based formula with palm olein) | |||||
3 months | 62.1 | 76.2* | |||||
6 months | 134.3 | 149.6* | |||||
Observational studies | |||||||
Butte et al. 2000 [216] | Prospective cohort study of breast-fed and formula-fed infants over 24 months | Sex: 33 males, 43 females Age: >2 weeks at baseline Race: 55 Caucasian, 7 African American, 11 Hispanic, 3 Asian Location: USA | 76 | Total body BMC (g) | Breast-fed (<12 months) | Breast-fed (>12 months) | Formula-fed |
12 months | Data not reported | Lowera
| Highera,** | ||||
24 months | 310 (P = 0.05) | 289 (P = 0.05) | Data not reported | ||||
Jones et al. 2000 [217] | Prospective cohort study to determine whether breastfeeding in early life is associated with bone mass in prepubertal children | Sex: 215 males, 115 females Age: 8 years at follow-up Race: predominantly Caucasian Location: Tasmania | 330 | Breast-fed | Bottle fed | ||
Total body BMD at 8 years (g/cm2) | 0.642 ± 0.082 | 0.627 ± 0.073* | |||||
Femoral neck BMD at 8 years (g/cm2) | 0.608 ± 0.072 | 0.590 ± 0.068 | |||||
Lumbar spine BMD at 8 years, g/cm2
| 0.781 ± 0.047 | 0.766 ± 0.047** | |||||
Ma and Jones 2003 [219] | Population-based case-controlled study to examine the association between bone mass and upper limb fractures in children | Sex: 206 males, 124 females Age: 8 years at follow-up Race: predominantly Caucasian Location: Tasmania | 324 | Breast-fed | |||
Multivariate OR (95 % CI) | 0.43 (0.19–0.94)a
| ||||||
Young et al. 2005 [221] | BMD was assessed in healthy 4-year-old children after confirming the type of infant feeding by history. All children had exclusively consumed human milk, infant formula without palm olein oil, or an infant formula with palm olein oil. | Sex: 58 % male Mean age: 4.5 years Race: 85 % Caucasian Location: USA | 178 | Human milk | Formula without palm olein oil | Formula with palm olein oil | |
Total body BMC at 4 years (g) | 566 ± 12 | 583 ± 10c
| 570 ± 7 | ||||
Harvey et al. 2009 [213] | Prospective cohort study examining associations between duration of breastfeeding and compliance with infant dietary guidelines and later bone size and density at age 4 years | Sex: 158 males, 149 females Age: 6 months at baseline Race: not reported Location: UK | 599 | Breast milk (<1 month) | Breast milk (2–6 months) | ||
No differencea
| No differencea
| ||||||
Molgaard et al. 2011 [212] | Random sample of infants from the Copenhagen Cohort Study of Infant Growth and Nutrition were investigated to determine if early nutrition and early growth are associated with later bone mass in adolescence. | Sex: 44 males, 65 females Age: birth to 12 weeks. Examination at 17 years Race: Danish origin; otherwise not reported Location: Denmark Years: 1987–2005 | 109 | Lumbar spine BMC | The duration of exclusive breastfeeding was positively correlated with the sex-adjusted lumbar spine BMCa,**. | ||
Pirila et al. 2011 [214] | Prospective study of infants divided into three equal-sized groups according to the total duration of breastfeeding (short = 3 months, intermediate = >3 to <7 months, and prolonged = >7 months) followed-up after 32 years | Sex: 76 males, 82 females Age: 2 weeks to 12 months in original cohort; 31.7–34.0 years at follow-up Race: not reported Location: Finland Year(s): 2007–2009 | 158 | Total body BMC | In males, short breastfeeding was associated with higher bone area, BMC, and BMD compared to longer breastfeeding. Males in the short breastfeeding group had on average 4.7 % higher total body BMD than males in the prolonged breastfeeding groupa,**. | ||
Fewtrell et al. 2013 [220] | To compare total body and lumbar spine bone in children aged 10 years that as infants participated in a randomized trial and either were breast-fed or randomly received a control formula or an sn-2 palmitate-enriched formula using a double-blind permuted block allocation. The study was completed at 12 weeks and follow-up measurements were taken at 10 years. | Sex: 52 % male, 48 % female Age: birth to 12 weeks; follow-up at 10 years Race: not reported Location: Cambridge, UK | 91 | Breast-fed | Formula with standard fat blend | Formula with high sn-2 fat blend | |
Lumbar spine BMC (g) | 23.12 ± 4.46 | 22.54 ± 4.52 | 24.38 ± 5.15 | ||||
Total body BMC (g) | 1062 ± 213 | 1049 ± 264 | 1097 ± 231 | ||||
Jones et al. 2013 [218] | Birth cohort study to determine if early life factors (e.g., breastfeeding) were associated with bone mass and fractures in 16-year-old adolescents | Sex: 265 males, 150 females Age: 16 years at follow-up Race: predominantly Caucasian Location: Tasmania | 415 | OR (95 % CI) | Any fracture | Upper limb fracture | Lower limb fracture |
Intention to breastfeed | 0.71 (0.55–0.94)c
| 0.80 (0.55–1.66) | 0.63 (0.36–1.13) | ||||
Breastfeeding at 1 month | 0.65 (0.48–0.87)c
| 0.84 (0.54–1.73) | 0.49 (0.26–0.93)c
| ||||
Breastfeeding at 3 months | 0.80 (0.60–1.09) | 0.87 (0.58–1.31) | 0.82 (0.45–1.48) | ||||
Maternal recall of breastfeeding | 0.69 (0.54–0.89)c
| 0.73 (0.51–1.39) | 0.75 (0.42–1.34) | ||||
Kalkwarf et al. 2013 [215] | A cross-sectional study to describe age, sex, race, growth, and human milk feeding effects on bone | Sex: 158 males, 149 females Age: 1–36 months Race: 225 Caucasian, 63 African American, 15 mixed Caucasian and African American, and 4 Asian Location: USA | 307 | Human milk | No human milk | ||
Overall BMD Z-score | −0.05 | 0.21** |
Source | Study description | Population description | Number of subjects | End points | Results | ||
---|---|---|---|---|---|---|---|
Observational studies | |||||||
Lloyd et al. 2000 [223] | An 8-year longitudinal study of white females in the Penn State Young Women’s Health Study. OC users were those individuals who had used low-dose monophasic OCs for a minimum of 6 months at age ~12 and were still using them at age 20 years. | Sex: 62 females Age: 11.9 ± 0.5 years at baseline Race: Caucasian Location: USA | 62 | Total body BMC (g) at 12 years | OC users | Nonusers | |
1463.0 ± 64.0 | 1402.5 ± 45.5 | ||||||
Total body BMC (g) at 20 years | 2272.2 ± 55.9 | 2214.2 ± 45.1 | |||||
Total body BMD (g/cm2) at 12 years | 0.92 ± 0.01 | 0.91 ± 0.01 | |||||
Total body BMD (g/cm2) at 20 years | 1.13 ± 0.01 | 1.12 ± 0.01 | |||||
Hip BMD (g/cm2) at 20 years | 1.01 ± 0.02 | 0.99 ± 0.02 | |||||
The OC users did not differ in anthropometric, body, or total bone measurements at baseline or at age 20 years (no differences in age at menarche or exercise at age 20 years). OC pill use by healthy white teenage females did not affect acquisition of peak bone mass. | |||||||
Lara-Torre et al. 2004 [225] | Nonrandomized prospective study to examine BMD in control adolescent subjects vs those receiving DMPA injections or OCs over a 2-year period | Sex: 71 females Age: 11–19 years Race: Caucasian and black Location: USA | 148 | OC usersb
| DMPA injectionb
| Nonuserb
| |
% change in lumbar BMD at 6 months | 1.170 (−0.14, 2.48) | −0.249 (−1.25, −0.75)* | 2.768 (0.48, 5.05) | ||||
% change in lumbar BMD at 12 months | 2.35 (0.16, 3.78) | −1.59 (−2.53, 0.59)* | 2.45 (−2.01, 5.99) | ||||
% change in lumbar BMD at 18 months | 3.82 (−0.62, 6.41) | −2.91 (−3.64, −2.23)* | 0.73 (−1.01, 1.54) | ||||
% change in lumbar BMD at 24 months | −1.01 (−1.23, 5.33) | −1.85 (−4.15, −0.23)* | 5.89 (5.37, 6.85) | ||||
There was a statistically significant difference in BMD between DMPA users and the control at 6, 12, 18, and 24 months. There was no statistical difference between OC pill users and the control at any time point. | |||||||
Lloyd et al. 2004 [224] | A 10-year longitudinal study of white females in the Penn State Young Women’s Health Study. OC users were those individuals who had used low-dose monophasic OCs for a minimum of 6 months at age ~12 years and were still using them at age 22 years. | Sex: 80 females Age: 21.7 ± 0.1 years Race: Caucasian Location: USA | 80 | OC users | Nonusers | ||
Total body BMC (g) at 22 years | 2260 ± 55 | 2316 ± 66 | |||||
Total body BMD (g/cm2) at 22 years | 1.14 ± 0.01 | 1.15 ± 0.02 | |||||
Hip BMD (g/cm2) at 22 years | 1.0 ± 0.02 | 1.0 ± 0.02 | |||||
Femoral neck section modulus (cm3) at 22 years | 1.29 ± 0.05 | 1.32 ± 0.05 | |||||
Femoral neck section modulus (cm3) at 22 years | 1.70 ± 0.06 | 1.74 ± 0.07 | |||||
OC pill use among adolescents was not correlated with bone or body composition measurements. | |||||||
Rome et al. 2004 [227] | Prospective, observational design study to examine the effects of DMPA injections or OC (20 μg ethinyl estradiol/100 μg levonorgestrel) use on bone biochemical markers over 12 months | Sex: 165 females Age: 11–18 years Race: Caucasian and black Location: USA | 370 | Spine and femoral neck BMD | No significant differences reported between spine and femoral neck BMD for each group at each time point. Spine BMD was lower in the DMPA injection group vs the OC group. Exact values not reported | ||
Cromer et al. 2008 [226] | Observational prospective cohort study to examine the effects of DMPA injections or OC (20 μg ethinyl estradiol/100 μg levonorgestrel) use on BMD over 24 months | Sex: 375 females Age: 12–18 years Race: Caucasian and black Location: USA | 433 | OC users | DMPA injection | Nonuser | |
Spine BMD (g/cm2) | 1.03 ± 0.11 | 0.98 ± 0.09* | 0.98 ± 0.11 | ||||
Femoral neck BMD (g/cm3) | 0.97 ± 0.14 | 0.92 ± 0.14* | 0.92 ± 0.15 | ||||
Over 24 months, mean percent change in spine BMD was −1.5 % (DMPA injection), 4.2 % (OC use), and 6.3 % (control). Over 24 months, mean percent change in femoral neck BMD was −5.2 % (DMPA injection), 3.0 % (OC use), and 3.8 % (control). Adolescent girls receiving DMPA injections had significant loss of BMD. Clinical significance of this loss may be mitigated by the slowed loss after the first year of DMPA use. | |||||||
Pikkarainen et al. 2008 [228] | 4-year follow-up study examining the effects of estrogen-progestin OC use | Sex: 122 females Age: 12–19 years Race: Assumed predominantly Caucasian Location: Finland | 122 | OC user (1–2 years) | OC user (>2 years) | Nonuser | |
Lumbar spine area (cm2) at baseline | 56.1 ± 6.1 | 56.7 ± 5.9 | 55.1 ± 5.9 | ||||
Lumbar spine area (cm2) at 4 years | 58.6 ± 6.1 | 58.7 ± 0.7 | 59.5 ± 6.3 | ||||
Femoral neck area (cm2) at baseline | 4.79 ± 4.33 | 4.64 ± 0.37 | 4.66 ± 0.40 | ||||
Femoral neck area (cm2) at 4 years | 4.80 ± 0.3 | 4.7 ± 0.4 | 4.7 ± 0.40 | ||||
Lumbar spine BMC (g) at baseline | 54.3 ± 11.8 | 57.5 ± 11.9 | 51.2 ± 10.2 | ||||
Lumbar spine BMC (g) at 4 years | 59.10 ± 11.7 | 60.2 ± 12.3 | 59.2 ± 10.0 | ||||
Femoral neck BMC (g) at baseline | 4.3 ± 0.8 | 4.4 ± 0.8 | 4.1 ± 0.6 | ||||
Femoral neck BMC (g) at 4 years | 4.5 ± 0.8 | 4.4 ± 0.7 | 4.3 ± 0.6 | ||||
There was a significant trend of a lesser increase of BMC in lumbar spine in the OC users (>2 years) than in the other two groups (P < 0.0046). The development of the femoral neck was significantly different between the OC users (1–2 years) and OC users (>2 years). The longer duration of OC use seemed to suppress normal BMC development (P for linearity = 0.038) | |||||||
Walsh et al. 2008 [230] | A case-controlled matched study aiming to examine whether the effects of DMPA injections are age-specific and to determine the effects of DMPA on hormones and bone turnover | Sex: 100 females (50 pairs) Age: 12–18 years Race: Caucasian and black Location: USA | 100 | DMPA injectiona
| Nonusersa
| ||
Lumbar spine BMD (g/cm2) | 1.003 (0.972–1.035)* | 0.947 (0.950–0.977) | |||||
Total hip BMD (g/cm2) | 0.983 (0.950–1.016)* | 0.931 (0.897–0.966) | |||||
Distal forearm BMD (g/cm2) | 0.465 (0.446–0.483) | 0.474 (0.457–0.491) | |||||
DMPA injections are associated with a bone density deficit at the spine and hip when used before peak bone mass. | |||||||
Bonny et al. 2011 [222] | Prospective longitudinal study examining the relationship between weight and BMD and the correlation between weight change and BMD in premenarcheal girls reporting DMPA use or OC (20 μg ethinyl estradiol/100 μg levonorgestrel) use | Sex: 433 females Age: 12–18 years Race: Caucasian and black Location: USA | 433 | User | DMPA injection | Nonuser | |
Correlation between absolute change in weight (kg) and absolute change in femoral neck BMD at 12 months | 1.000 | 1.000 | 1.000 | ||||
Correlation between absolute change in weight (kg) and absolute change in femoral neck BMD at 24 months | 1.000 | 1.000 | 1.000 | ||||
Correlation between absolute change in weight (kg) and absolute change in spine BMD at 12 months | −0.82 | −0.101 | 0.10 | ||||
Correlation between absolute change in weight (kg) and absolute change in spine BMD at 24 months | −0.12 | 0.098 | 0.48 | ||||
Body weight was significantly positively associated with femoral neck BMD and spine BMD regardless of the contraceptive method (P < 0.05). Change in body weight at 12 and 24 months was highly correlated with change in femoral neck BMD (P < 0.0001) for all treatment groups. No statistically significant correlation between change in weight and change in spine BMD was seen in the DMPA, OC, or control subjects at 12 or 24 months. | |||||||
Biason et al. 2015 [229] | Nonrandomized parallel-control study with 1-year follow-up assessing the effect of OC (20 μg ethinyl estradiol/150 μg desogestrel) users on bone density | Sex: 67 females Age: 12–19 years Race: Assumed Brazilian Location: Brazil | 67 | OC user | Nonuser | ||
% variation lumbar BMD (g/cm2) | 2.07 | 12.16 | |||||
% variation lumbar BMC (g) | 1.57* | 16.84 | |||||
% variation subtotal BMD (g/cm2) | 0.56* | 5.28 | |||||
% variation subtotal BMC (g) | 1.18* | 16.04 | |||||
% variation whole body BMD (g/cm2) | 0.84 | 5.28 | |||||
% variation whole body BMC (g) | 1.22* | 11.34 | |||||
Use of low-dose OCs was associated with lower bone mass acquisition in adolescents over a 1-year period. OC users showed low bone mass acquisition in the lumbar spine and had BMD and BMC median variations of 2.07 and 1.57 %, respectively, between the measurements at baseline and 12 months. Nonusers showed median variations of 12.16 and 16.84 % for BMD and BMC, respectively, over the same period. |
Reference | Study description | Population description | Number of subjects | End points | Results | |||
---|---|---|---|---|---|---|---|---|
Prospective studies | ||||||||
Korkor et al. 2009 [231] | This 4-year prospective study assessed the relationship between smoking and alcohol intake and bone mass. Students in 9th grade were recruited. Number of alcoholic beverages in the last week was reported in the 9th through 12th grades. Subjects classified as any alcohol over 4 years vs not | Sex: 37 males, 72 females Age: 14–19 years at enrollment Race: white 83 %, Asian 1 %, Hispanic 4 %, unknown 12 % Location: Wisconsin, USA Year(s): 2000–2003 | 109 | Peripheral DXA | Simple model, any alcohol intake | Adjusted model, any alcohol, or smoking | ||
Heel aBMD in 12th grade (g/cm2) | −0.042, P = 0.047 (−7.2 %)
| −0.028, P = 0.05 (−4.8 %)
| ||||||
The simple model includes any alcohol over the 4-year study (yes, n = 13; no, n = 96). The adjusted model was adjusted for sex baseline aBMD dairy intake. Large overlap in smoking and alcohol use. Any smoking or alcohol combined (N = 14) was associated with a −0.028-g/cm2 lower aBMD. | ||||||||
Lucas et al. 2012 [235] | This prospective study quantified the association between early initiation of smoking and alcohol intake and forearm BMD in early and late adolescence. Alcohol intake reported at age 13 and 17 years and classified as never, tried but not currently drinking, <1 drink/week, or ≥1 drink/week | Sex: female Age: 13 and 17 years Race: not specified Location: Portugal Year(s): 2003–2007 | 716 | Peripheral DXA | Drinking at age 13 years vs never (n = 298) | |||
Distal radius aBMD | Tried, not currently drinking (n = 380) | Drinks < 1/week (n = 26) | Drinks ≥ 1/week (n = 8) |
P value | ||||
At age 13 years | 0.3 % | −2.0 % | −1.1 % | 0.826 | ||||
At age 17 years | −1.1 % | 2.3 % | −4.8 % | 0.282 | ||||
Drinking at age 17 years vs never (n = 120) | ||||||||
Tried, not currently(n = 273) | Drinks, not daily (n = 266) | Drinks, daily (n = 54) |
P value | |||||
At age 17 years | 1.1 % | 0.0 % | −2.3 % | 0.471 | ||||
Ever drank in adolescence vs never (n = 84) | ||||||||
Tried 13 years but before 17 years (n = 213) | Tried before 13 years (n = 419) |
P value | ||||||
−0.9 % | −2.0 % | 0.216 | ||||||
Means are adjusted for menarche age, alcohol intake, sports, and BMI. | ||||||||
Dorn et al. 2013 [233] | This 3-year prospective study of girls examined bone accrual according to smoking, alcohol intake, depression, and anxiety. Alcohol use was coded as 0–5 drinks or ≥6 drinks in lifetime. | Sex: female Age: 11–17 years Race: 62 % white, 33 % black, 5 % other Location: Ohio, USA Year(s): 2003–2010 | 262 | DXA Total body BMC (g) Spine aBMD (g/cm2) Hip aBMD (g/cm2) | There was no significant association between alcohol use and any bone outcome measure. Regression models were adjusted for race, puberty stage, weight, height, age at menarche, contraceptive use, calcium intake, vitamin D status, and physical activity. | |||
Cross-sectional studies | ||||||||
Elgan et al. 2002 [237] | This cross-sectional study conducted in nursing students measured lifestyle and physiologic factors. Alcohol intake was measured by questionnaire. | Sex: female Age: 16–24 years Race: not reported Location: Lund, Sweden Year(s): 1999 | 218 | Peripheral DXA Heel aBMD (g/cm2) | Correlation with alcohol intake, r = −0.05 (P = NS) Alcohol intake not significant (P = 0.84) in regression models adjusting for age, weight, physical activity, and hormonal age Average alcohol intake 16.6 g/month; 79 % reported some alcohol intake | |||
Kyriazopoulos et al. 2006 [236] | This cross-sectional study evaluated the influence of current dietary factors (calcium, proteins, alcohol, coffee, and tea intake), exercise, smoking, and sunlight on forearm bone mass in young Greek men. Alcohol intake reported as consumption per week | Sex: male Age: 18–30 years, mean 22 years Race: not reported
Location: Greece Year(s): not reported
| 300 | Peripheral DXA Distal radius BMC (g) Distal radius aBMD (g/cm2) Ultradistal radius aBMD (g/cm2) | Mean alcohol intake 3.78 ± 1.35 times/week. No association between alcohol intake (times/week) and bone measures with and without adjustment for height, weight, calcium intake, sunlight exposure, exercise, and work | |||
Dorn et al. 2011 [232] | This cross-sectional analysis of baseline data examined how bone mass and density varied according to smoking, alcohol intake, depression, and anxiety. Alcohol intake reported as no drinks (n = 135), 1–5 drinks (n = 59), ≥6 drinks (n = 67) in the past year | Sex: female Age: 11–17 years Race: 62 % white, 33 % black, 5 % other Location: Ohio, USA Year(s): 2003–2007 | 261 | DXA Total body BMC (g) Spine aBMD (g/cm2) Total hip aBMD (g/cm2) Femoral neck aBMD (g/cm2) | No significant main effect of alcohol group and any outcome measure (P > 0.10). Analyses were adjusted for age, weight, height, race, and maturational stage. | |||
Significant interactions between alcohol, smoking, and depression symptoms on bone outcomes. Stronger negative association between depressive symptoms and total body BMC among individuals who smoked and used alcohol | ||||||||
Eleftheriou et al. 2013 [238] | A cross-sectional study evaluating the association of smoking, alcohol consumption, and prior exercise with lower limb bone volume, composition, and structure by MRI and DXA in a large cohort of healthy Caucasian males. Alcohol intake was coded as none, low (1–9 U/week), moderate (12–21 U/week), or high (>21 U/week) | Sex: male Age: mean 19.9 years Race: Caucasian Location: UK Year(s): not reported | 651 | DXA | Difference between Alcohol intake group vs none | |||
Low 1–9 U/week | Moderate 12–24 U/week | High > 24 U/week |
P value | |||||
Total hip aBMD | 1.5 % | 2.3 % | −0.6 % | 0.017 | ||||
Femoral neck aBMD | −1.1 % | 2.8 % | −0.7 % | 0.015 | ||||
Proximal femur geometry by MRI | ||||||||
Periosteal volume | NS, data not shown | |||||||
Endosteal volume | NS, data not shown | |||||||
Cortical volume | NS, data not shown | |||||||
Adjusted for height, weight, smoking, and weight-bearing activity | ||||||||
Winther et al. 2014 [234] | This cross-sectional, population-based study compared BMD levels of Norwegian adolescents with lifestyle factors. Alcohol intake reported as never, ≤1 per month, or ≥2 per month. Alcohol use recoded for analysis as yes vs no | Sex: male and female Age: 15–17 years Race: not reported Location: Norway Year(s): 2010–2011 | 835 | Difference between alcohol users vs not | ||||
Age adjusted | Multivariable adjusted | |||||||
DXA | β |
P value | β |
P value | ||||
Males (n = 492) | ||||||||
Total hip aBMD (g/cm2) | 0.027 | 0.057 | 0.035 | 0.006 | ||||
Femoral neck aBMD (g/cm2) | 0.030 | 0.037 | 0.028 | 0.021 | ||||
Females (n = 469) | ||||||||
Total hip aBMD (g/cm2) | −0.014 | 0.297 | – | – | ||||
Femoral neck aBMD (g/cm2) | −0.013 | 0.330 | – | – | ||||
Alcohol uses include intakes of up to 1/month (44.7 % of girls, 36.4 % of boys) and ≥2 times/month (30.3 % of girls, 30.9 % of boys) vs never (23.4 % of girls, 30.4 % of boys). Multivariable analyses were adjusted for age, BMI, height, sexual maturation, physical activity, smoking, diseases, and medications known to affect bone hormonal contraceptives. |
Reference | Study description | Population description | Number of subjects | End points | Results | |||
---|---|---|---|---|---|---|---|---|
Prospective studies | ||||||||
Lappe et al. 2001 [42] | This prospective study of female army recruits examined risk factors for developing stress fractures during 8 weeks of basic training. | Sex: female Age: 21.1 ± 3.7 years Race: 31 % black, 53 % white, 16 % other Location: USA Years: 1995–1996 | 3758 | Stress fracture | Odds ratios (95 % CI) | |||
History of smoking 1.34 (1.05–1.71) Years smoked 1.05 (1.02–1.08) | ||||||||
•Adjusted for age, race and bone speed of sound | ||||||||
Elgan et al. 2003 [240] | This prospective study is a 2-year follow-up of the cohort reported in 2002 and investigated the joint effects of OC use and smoking. Smoking reported as monthly average. Twenty-eight subjects smoked as follows: n = 1, >25 cig/day; n = 6, 15–24 cig/day; n = 16, 5–14 cig/day;, n = 4, ≤4 cig/day. | Sex: female Age: 18–26 Race: not reported Location: Lund, Sweden Year(s): 2001 | 118 | Peripheral DXA | Difference from reference group, nonsmoker/no OC use (n = 35) | |||
Heel aBMD | Smoker/no OC use (n = 9) | Nonsmoker/OC use (n = 57) | Smoker/OC use (n = 17) | |||||
T2 aBMD (g/cm2) | ||||||||
Unadjusted | 0.0013 | 0.014 | −0.012 | |||||
Adjusteda
| −0.032* | −0.014 | −0.017* | |||||
2-year change in aBMD (g/cm2) | ||||||||
Unadjusted | −0.035* | −0.013 | −0.016 | |||||
Adjusteda
| −0.06 | −0.010 | −0.021 | |||||
aAdjusted for age, physical activity baseline BMD, body weight *P < 0.05 | ||||||||
Lappe et al. 2008 [241] | Secondary analyses of this randomized calcium and vitamin D supplementation trial examined other risk factors for developing stress fractures during basic training. | Sex: female Age: 19 years (17–35 years) Race: not specified Location: USA Years 2001–2006 | 5201 | Stress fracture | Risk of fracture was 41 % higher in women with history of smoking when adjusted for treatment group, P = 0.0075 Odds ratio for fracture was 1.32 (0.99–1.75) in women with history of smoking when adjusted for treatment, amenorrhea, high exercise, Depo Provera use, age, and running speed. | |||
Korkor et al. 2009 [231] | This 4-year prospective study assessed the relationship between smoking and alcohol intake and bone mass. Students in 9th grade were recruited. Number of cig smoked per day reported in the 9th, 10th, 11th, and 12th grades. Subjects classified as any smoking over 4 years vs not | Sex: 37 males, 72 females Age: 14–19 years at enrollment Race: white 83 %, Asian 1 %, Hispanic 4 %, unknown 12 % Location: Wisconsin, USA Year(s): 2000–2003 | 109 | Peripheral DXA | Simple model, any smokinga
| Adjusted model, any alcohol or smokingb
| ||
Heel aBMD in 12th grade (g/cm2) | −0.0249, P = 0.29 | −0.0281, P = 0.05 | ||||||
−4.3 % | −4.8 % | |||||||
aAny smoking over the 4-year study (yes, n = 8; no, n = 101)
bAdjusted for sex baseline aBMD dairy intake Large overlap in smoking and alcohol use. Any smoking or alcohol combined (N = 14) was associated with a −0.028-g/cm2 lower aBMD. | ||||||||
Lucas et al. 2012 [235] | This prospective study quantified the association between early initiation of smoking and alcohol intake and forearm BMD in early and late adolescence. Smoking reported at age 13 and 17 years and classified as: tried but not currently smoking, smokes but not daily or smokes daily | Sex: female Age: 13 years and 17 years Race: not specified
Location: Portugal Year(s): 2003–2007 | 713 | Peripheral DXA | Smoking at age 13 years vs never smoked (n = 523) | |||
Distal radius aBMD | Tried, not currently smoking (n = 165) | Smokes (n = 24) |
P value | |||||
At age 13 years | 1.1 % | −0.6 % | 0.410 | |||||
At age 17 years | −2.3 % | −0.7 % | 0.068 | |||||
Smoking at age 17 years vs never (n = 390) | ||||||||
Tried, not currently (n = 224) | Smokes, not daily (n = 33) | Smokes, daily (n = 72) |
P value | |||||
At age 17 years | −2.3 % | −3.2 % | −0.7 % | 0.438 | ||||
Ever smoked in adolescence vs never smoked (n = 353) | ||||||||
At age 17 years | Tried 13 years but before 17 years (n = 167) | Tried before 13 years (n = 192) |
P value | |||||
0.4 % | −1.8 % | 0.103 | ||||||
Adjusted for menarche age, alcohol intake, sports, and BMI | ||||||||
Dorn et al. 2013 [233] | This 3-year prospective study of girls examined bone accrual according to smoking, alcohol intake, depression, and anxiety. Smoking measured every 3 months and coded as cigarettes smoked in last 30 days: 0, 1–2 days, 3–5 days, 6–9, 10–19 days, 20–29 days, or 30 day | Sex: female Age: 11–17 years Race: 62 % white, 33 % black, 5 % other Location: Ohio, USA Year(s): 2003–2010 | 262 | DXA Total body BMC (g) Spine aBMD (g/cm2) Hip aBMD (g/cm2) | No significant main effect or age × smoking interaction on total body Significant age × smoking interaction for spine and hip aBMD. As smoking increased, the rate of bone accrual decreased as girls got older. Regression models adjusted for race, puberty stage, weight, height, and contraceptive use | |||
Cross-sectional studies | ||||||||
Elgan et al. 2002 [237] | This cross-sectional study conducted in nursing students measured lifestyle and physiologic factors. Smoking was measured by questionnaire and dichotomized as yes/no. 23 % smoked on a daily basis, 22 % were party smokers, and 55 % were nonsmokers. | Sex: female Age: 16–24 years Race: not reported Location: Lund, Sweden Year(s): 1999 | 218 | Peripheral DXA Heel aBMD (g/cm2) | Smoking status not significantly associated with aBMD in bivariate analyses. Data not shown Smoking not significant (P = 0.48) in regression models adjusting for age, weight, physical activity, and hormonal age | |||
Afghani et al. 2003 [336] | A cross-sectional analysis of baseline data from a smoking cessation trial. Analyses investigated the role of body composition, physical activity, menarche, smoking, and second-hand smoke on regional bone mass among Asian adolescents living in Wuhan, China. Smoking questions assessed if subjects “smoked at least 100 cigarettes in their life?” and “have smoked in last 30 day.” Smoking was reclassified for analyses as smoking yes/no. | Sex: male and female Age: 12–16 years, 14.5 ± 0.5 Race: Asian Location: Wuhan, China Year(s): not reported
| 466 | Peripheral DXA | Correlation with smoking (yes/no)a
|
P value | Multivariable modelsb
| |
Boys (n = 300) | ||||||||
Forearm BMC | 0.05 | NS | NS | |||||
Forearm aBMD | 0.04 | NS | – | |||||
Heel BMC | 0.05 | NS | NS | |||||
Heel aBMD | 0.00 | NS | – | |||||
Girls (n = 166) | ||||||||
Forearm BMC | 0.15 | <0.05 | NS | |||||
Forearm aBMD | 0.04 | NS | – | |||||
Heel BMC | 0.08 | NS | NS | |||||
Heel aBMD | 0.09 | NS | – | |||||
aUnclear how correlation derived given that smoking was a dichotomous variable
bAdjusting for age, height, lean mass, fat mass, team sports participation, menarche, and passive smoking Low level of smoking and inconsistent report of smoking in the sample limits conclusions. 38 % of girls and 14 % of boys inconsistently answered smoking questions. Among smokers, 58 % of girls and 51 % of boys smoked ≤1 cigarette in last 30 days. | ||||||||
Kyriazopoulos et al. 2006 [236] | This cross-sectional study evaluated the influence of current dietary factors (calcium, proteins, alcohol, coffee, and tea intake), exercise, smoking, and sunlight on forearm bone mass in young Greek men. Smoking coded as daily smoking (58.6 %) or no | Sex: male Age: 18–30 years, mean 22 years Race: not reported
Location: Greece Year(s): not reported
| 300 | Peripheral DXA Distal Radius BMC Distal radius aBMD Ultradistal radius aBMD | There was no association between daily smoking (58.6 % of sample) and bone measures with and without adjustment for height, weight, calcium intake, sunlight exposure, exercise, and work. Data not shown | |||
Lorentzon et al. 2007 [239] | The GOOD study is a cross-sectional study involving a random selection of males in Gothenburg. Bone mass, density, and geometry measured by DXA and pQCT. Smoking quantified as cigarettes/day and duration. For analyses, subjects were classified as smokers ≥1 cig/day vs not. | Sex: male Age: 18–20 years Race: not reported
Location: Gothenburg, Sweden Year(s): not reported
| 1063 | Difference between smoked ≥1 cigarette/daya vs not | ||||
Unadjusted |
P value | Adjustedb
|
P value | |||||
DXA | ||||||||
Total body aBMD | −2.1 % | <0.01 | −1.8 % | 0.01 | ||||
Spine aBMD | −4.3 % | <0.001 | −3.3 % | <0.01 | ||||
Femoral neck aBMD | −5.3 % | <0.001 | −3.9 % | <0.01 | ||||
Trochanter aBMD | −6.6 % | <0.001 | −5.0 % | <0.01 | ||||
pQCT | ||||||||
Tibia | ||||||||
Cortical vBMD | 0.0 % | 0.91 | – | NS | ||||
Cortical thickness | −4.5 % | <0.001 | −4.0 % | <0.001 | ||||
Periosteal circumference | 0.0 % | 0.97 | – | NS | ||||
Endosteal circumference | 2.5 % | <0.05 | 2.7 % | 0.01 | ||||
Trabecular vBMD | −4.2 % | <0.01 | −3.8 % | <0.01 | ||||
Radius | ||||||||
Cortical vBMD | −0.1 % | 0.55 | – | NS | ||||
Cortical thickness | −2.8 % | <0.01 | −2.9 % | <0.01 | ||||
Periosteal circumference | 0.7 % | 0.32 | – | NS | ||||
Endosteal circumference | 3.3 % | 0.02 | 4.5 % | <0.01 | ||||
Trabecular vBMD | −2.7 % | 0.16 | – | NS | ||||
aSmokers consumed 9.3 ± 6.3 cig/day. Mean duration of smoking 4.1 ± 2.1 years. Smokers less active than nonsmokers
bAdjusted for calcium intake, physical activity, age, height, and weight. Smokers had reduced BMD due to smaller cortical thickness greater endosteal circumference | ||||||||
Dorn et al. 2011 [232] | This cross-sectional analysis of data examined how bone mass and density varied according to smoking, alcohol intake, depression, and anxiety. Smoking ever in their life coded as never (n = 104), 1 puff to 2 cig (n = 54), and 3–99 cig (n = 51), >100 cig/day (n = 52) | Sex: female Age: 11–17 years Race: 62 % white 33 % black, 5 % other Location: Ohio, USA Year(s): 2003–2007 | 261 | DXA | ||||
Total body BMC (g) | No significant differences among smoking groups | |||||||
Spine aBMD (g/cm2) | No significant differences among smoking groups | |||||||
Total hip aBMD (g/cm2) | 1 puff to 2 cig group 6.5 % greater than >100 cig group, P < 0.05 | |||||||
Femoral neck aBMD (g/cm2) | 1 puff to 2 cig group 6.0 % greater than >100 cig group, P < 0.05 | |||||||
Analyses adjusted for age, weight, height, race, and maturational stage. Significant interactions between alcohol and tobacco use, and depression symptoms on bone outcomes. Stronger negative association between depressive symptoms and total body BMC among individuals who smoked and used alcohol. | ||||||||
Eleftheriou et al. 2013 [238] | A cross-sectional study evaluating the association of smoking, alcohol consumption, and prior exercise with lower limb bone volume, composition, and structure by MRI and DXA in a large cohort of healthy Caucasian males. Smoking status coded as nonsmoker, ex-smoker (>6 months), recent ex-smoker (≤6 months), or current smoker | Sex: male Age: mean 19.9 years Race: Caucasian Location: UK Year(s): not reported | 651 | Differencea between smoking status vs nonsmoker (n = 329) | ||||
Ex-smoker >6 months (n = 41) | Recent ex-smoker ≤ 6 months (n = 35) | Current smoker (n = 244) |
P value | |||||
DXA | ||||||||
Total hip aBMD | −5.0 % | −6.0 % | −4.7 % | 0.0001 | ||||
Femoral neck aBMD | −5.9 % | −5.3 % | −4.0 % | 0.001 | ||||
MRI | ||||||||
Periosteal volume | −5.0 % | −4.3 % | −0.4 % | 0.004 | ||||
Endosteal volume | NS, data not shown | |||||||
Cortical volume | NS, data not shown | |||||||
aAdjusted for height weight, alcohol intake, and weight-bearing activity | ||||||||
Winther et al. 2014 [234] | This cross-sectional population-based study compared BMD levels of Norwegian adolescents with lifestyle factors. Smoking was classified as daily smoking, sometimes smokes, or never smokes. | Sex: male and female Age: 15–17 years Race: Location: Norway Year(s): 2010–2011 | 835 | Difference between smokinga vs not | ||||
Age adjusted | Multivariable adjusteda
| |||||||
DXA | Beta |
P value | Beta |
P value | ||||
Males (n = 492) | ||||||||
Total hip aBMD (g/cm2) | −0.039 | 0.012 | 0.029 | 0.037 | ||||
Femoral neck aBMD (g/cm2) | −0.025 | 0.116 | – | – | ||||
Females: (n = 469) | ||||||||
Total hip aBMD (g/cm2) | −0.026 | 0.074 | – | – | ||||
Femoral neck aBMD (g/cm2) | −0.031 | 0.031 | – | – | ||||
aIncludes daily smoking (5.5 % of girls and 3.8 % of boys) and sometimes smokes (15.9 % girls, 20.2 % of boys) vs never smokes (76.6 % of girls and 74.2 % of boys)
bAdjusted for age, BMI, height, sexual maturation, physical activity, alcohol intake, diseases, and medications known to affect bone and hormonal contraceptives |
Reference | Study description | Population description | Number of subjects | Intervention | End points | Results | |||
---|---|---|---|---|---|---|---|---|---|
RCTs | |||||||||
Witzke and Snow 2000 [337] | 9-month jumping intervention Recruited for exercise group No randomization | Sex: female Age: 13–15 years Race: not listed Location: Corvallis, OR | 53 | Frequency: 3×/week Intensity: varied Time: 30–45 min/session Type: resistance training: squats, lunges, toe/heel raises, bench stepping, and jumping. Plyometric training: two-footed, in-place jumps to stair jumping, bounding, depth jumps Control: regular PE | DXA | Percent change, mean ± SD | |||
Significant
| EX | CON | |||||||
TR BMC | 3.13 ± 6.44* | 1.96 ± 6.69 | |||||||
NS
| Both groups experienced a significant increase in percent change in bone mass compared to zero for TB, FN, LS, and FS, but only EX improved BMC of the TR (3.1 vs 1.9 %). | ||||||||
TB, FN, LS, FS BMC | |||||||||
McKay et al. 2000 [338] | 8-month loading intervention Randomized by school | Sex: male and female Age: 6.9–10.2 years Race: 34 % Asian, 66 % white Location: Richmond, British Columbia | 144 | Frequency: 3×/week (2× PE, 1× classroom) Intensity: progressive Time: 10–30 min (minimum 10 min loading) Type: variety: games, circuit training, dances. Ten tuck jumps required at beginning of each session Control: regular PE | DXA | Percent change, mean ± SEM | |||
Significant
| EX | CON | |||||||
TR aBMD | 4.4 ± 0.5* | 3.2 ± 0.3 | |||||||
NS
| EX group showed significantly greater change in TR aBMD than CON group (4.4 vs 3.2 %). No group differences at other sites. | ||||||||
TB, LS, PF, FN aBMD | |||||||||
Heinonen et al. 2000 [244] | 9-month step aerobics/jumping intervention Randomized by school | Sex: female Age: 10–15 years Race: not specified Location: Tampere, Finland | 126 | Frequency: 2×/week Intensity: progressive Time: 50 min (10-min warm-up, 15-min nonimpact aerobic exercises, 20-min high-impact/jump training, 5-min cool down) Type: both-leg jumps at floor level, both-leg box jumps, one-leg box jumps Control: normal PA | DXA | Difference (g), mean (95 % CI) | |||
Significant
| Premenarchal EX vs CON | Postmenarchal EX vs CON |
P value Effect of EX (pre vs post) | ||||||
LS BMC | 1.01 (0.23, 1.78)* | ||||||||
FN BMC | 0.09 (0.02, 0.15)* | * | |||||||
TR BMC | * | ||||||||
In the premenarchal girls, BMC increased significantly more in the EX than in CON at LS (8.6 vs 5.3 %) and FN (9.3 vs 5.3 %). The postmenarchal girls showed no significant posttraining intergroup differences at any site. | |||||||||
Fuchs et al. 2001 [306] | 7-month jumping intervention Randomized by gender | Sex: male and female Age: 7.5 years ± 0.17 Race: 87 white, 1 Asian, 1 white-Hispanic Location: Corvallis, OR | 89 | Frequency: 3×/week, opposite PE Intensity: progressed from 50 to 80 jumps/day over 12 sessions; 100 jumps/day were performed for the remaining sessions Time: 20 min/session (5-min warm-up, 10-min jumping or stretching, 5-min cool down) Type: jumps off 61-cm box Control: nonimpact stretching | DXA | Postintervention values | |||
Significant
| EX | CON | |||||||
FN BMC | 2.00 ± 0.07*** | 1.89 ± 0.06 | |||||||
FN BA | 3.13 ± 0.08*** | 2.96 ± 0.07 | |||||||
LS BMC | 22.06 ± 0.57* | 21.64 ± 0.58 | |||||||
LS aBMD | 0.571 ± 0.008** | 0.553 ± 0.008 | |||||||
NS
| EX group had significantly greater changes in FN and LS BMC than CON group (4.5 and 3.1 %, respectively). EX group also had significantly greater changes in FN BA (2.9 %) and LS aBMD (2.0 %) than CON group. | ||||||||
FN aBMD, LS BA | |||||||||
Nichols et al. 2001 [243] | 15-month resistance training intervention Randomized | Sex: female Age: 14–17 years Race: not specified Location: Texas Woman’s University, TX | 16 | Frequency: 3×/week Intensity: progressive Time: not specified Type: 15 exercises all major muscle groups, combination free weights and machines Control: not specified | DXA | Percent change, mean | |||
Significant
| EX | CON | |||||||
FN aBMD | 3.67** | 1.35 | |||||||
NS
TB, LS, WA, TR aBMD TB, LS, FN, WA, TR BMC LS, FN BMAD | FN aBMD increased significantly in EX group (40 %), but not in CON group. No significant changes seen at other sites | ||||||||
Mackelvie et al. 2001 [26] | 9-month jumping intervention Randomized by school | Sex: female Age: 9–12 years Race: multiethnic population of city (45 % white, 34 % Asian, and 21 % mixed ethnicities) reflected in cohort Location: Richmond, British Columbia | 177 | Frequency: 3×/week (2x PE, 1 classroom) Intensity: progressed over school year by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm) Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: jumping exercises—jumping jacks, lunge jumps, hopping, jumping over various obstacles, drop jumps from platform Control: stretching | DXA | Change, mean (95 % CI) | |||
Significant
| Prepubertal EX | Prepubertal CON | Early Pubertal EX | Early Pubertal CON | |||||
LS BMC | 4.70 (4.38, 5.02)* | 4.18 (3.92, 4.44) | |||||||
LS aBMD | 0.057 (0.050, 0.064)** | 0.044 (0.038, 0.049) | |||||||
FN BMC | 0.31 (0.28, 0.34)* | 0.26 (0.24, 0.29) | |||||||
FN aBMD | 0.043 (0.036, 0.050)* | 0.034 (0.028, 0.039) | |||||||
FN vBMD | 0.010 (0.004, 0.015)* | 0.002(−0.003, 0.006) | |||||||
NS
| There were no significant differences between prepubertal EX and CON groups. Early pubertal girls in EX group gained 1.5 to 3.1 % more bone at FN and LS than CON girls; gain at other sites did not differ | ||||||||
TB, PF, TR BMC | |||||||||
TB, PF, TR aBMD | |||||||||
Mackelvie et al. 2002 [339] | 7-month jumping intervention Randomized by school | Sex: male Age: 8.8–11.7 years Race: multiethnic population of city (45 % white, 34 % Asian, and 21 % mixed ethnicities) reflected in cohort Location: Richmond, British Columbia | 121 | Frequency: 3×/week (2× PE, 1 classroom) Intensity: progressed over school year by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm) Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: jumping exercises—jumping jacks, lunge jumps, hopping, jumping over various obstacles, drop jumps from platform Control: stretching | DXA | Change, mean (95 % CI) | |||
Significant
| EX | CON | |||||||
TB BMC | 105.8 (97.7, 113.9)** | 90.0 (81.9, 98.2) | |||||||
PF aBMD | 0.025 (0.020, 0.030)* | 0.017 (0.013, 0.022) | |||||||
NS
| The EX group gained more TB BMC (1.6 %) and PF aBMD (1 %) than CON group did after adjusting for age, baseline weight, change in height, and loaded PA. | ||||||||
LS, PF, FN, TR BMC | |||||||||
LS, FN, TR aBMD | |||||||||
Kontulainen et al. 2005 [125] | 20-month follow-up to 9-month step aerobics/jumping intervention Randomized by school | Sex: female Age: 10–15 years Race: not specified Location: Tampere, Finland | 99 | Frequency: 2×/week Intensity: 100 both-leg jumps at floor level, increased to 200 box jumps (30 cm) using both legs and one leg Time: 50 min (10-min warm-up, 15-min nonimpact aerobic exercises, 20-min high-impact/jump training, 5-min cool down) Type: both-leg jumps at floor level, both-leg box jumps, one-leg box jumps Control: normal PA | DXA | Percent difference, mean (95 % CI) | |||
Significant
| |||||||||
LS BMC | 4.9 (0.9, 8.8)* | ||||||||
NS
| EX group had 4.9 % greater BMC accrual at the LS than the CON group during the 20-month follow-up. No other sites showed significant differences. | ||||||||
FN, TR BMC | |||||||||
Petit et al. 2002 [73] | 7-month jumping intervention Randomized by school | Sex: female Baseline age: 9–12 years Race: multiethnic population of city (~34 % Hong Kong Chinese and 57 % white) reflected in cohort Location: Richmond, British Columbia | 177 | Frequency: 3×/week (2× PE, 1 classroom) Intensity: progressed over school year by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm) Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: jumping exercises—jumping jacks, lung jumps, hopping, jumping over various obstacles, drop jumps from platform Control: stretching | DXA | No significant differences seen between EX and CON groups | |||
Significant
| |||||||||
None | |||||||||
NS
| |||||||||
NN, IT, FS aBMD | |||||||||
Laing et al. 2002 [340] | 36-month gymnastics participation Recruited due to enrollment in gymnastics | Sex: female Age: 8–13 years at baseline Race: all Caucasian (except one Hispanic control) Location: Athens, Georgia | 17 | Frequency: not specified Intensity: not specified Time: 9–24 h/week Type: regionally competitive gymnastics: vault, uneven bars, balance beam, floor routine Control: no gymnastics | DXA | At year 3, significant differences between EX and CON were noted at TB, LS, and PF for aBMD. Significant differences were noted for TB and LS for BMC. Both the EX group and CON groups had significant increases in BA at the TB, LS, FN, and PF. | |||
Significant
| |||||||||
TB aBMD | |||||||||
LS aBMD | |||||||||
PF aBMD | |||||||||
TB BMC | |||||||||
LS BMC | |||||||||
TB BA | |||||||||
LS BA | |||||||||
FN BA | |||||||||
PF BA | |||||||||
NS
| |||||||||
FN, TR, Rad aBMD | |||||||||
PF, FN, TR, Rad BMC | |||||||||
FN, Rad BA | |||||||||
MacKelvie et al. 2003 [341] | 20-month jumping intervention Randomized by school | Sex: female Age: 8.8–11.7 years at baseline Race: multiethnic population of city (57 % white, 34 % Hong Kong Chinese, 5 % East Indian, 4 % other ethnic origin or mixed ethnicity) reflected in the cohort Location: Richmond, British Columbia | 75 | Frequency: 3×/week (2× PE, 1 classroom) Intensity: year 1: progressed over school year by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm); year 2: higher proportion of high-impact jumps. Height increased every 8–10 weeks Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: year 1: jumping exercises such as jumping jacks, lung jumps, hopping, jumping over various obstacles, and drop jumps from platform; year 2: plyometric jumps, alternating-foot jumps, and 2-ft obstacle jumps Control: stretching | DXA | Change, mean (95 % CI) | |||
Significant
| EX | CON | |||||||
LS BMC | 10.9 (9.9, 11.9)* | 9.3 (8.4, 10.1) | |||||||
FN BMC | 0.66 (0.58, 0.73)* | 0.55 (0.48, 0.61) | |||||||
NS
| There were substantially greater gains in LS (41.7 vs 38.0 %) and FN (24.8 vs 20.2 %) BMC in EX group than in CON group. No significant differences between groups at other sites. | ||||||||
TB, PF, TR BMC | |||||||||
LS, PF, FN, TR BA | |||||||||
Van Langendonck et al. 2003 [342] | 9-month impact intervention on twins Twins randomized to exercise or control, keeping birth order equal between groups | Sex: female (21 twin pairs) Age: 8.7 years (SD = 0.7) Race: not specified Location: Belgium | 42 | Frequency: 3×/week Intensity: after the first trimester, participants went barefoot or wore very thin gym shoes to enhance mechanical loading Time: 10 min/session Type: 3 impact exercises- rope skipping 50 times; hopping 20 times as far as possible with the left and right leg; jumping from a wooden box of 40 cm high landing on both feet 30 times. 2 nonimpact exercises- moving 3.5 m sideways in a push-up position six times and six times moving 3.5 m backward on hands and feet like a crab Control: asked not to perform the exercises at school or home | DXA | None of the bone indices differed significantly between the EX and CON groups after the 9-month intervention. | |||
Significant
| |||||||||
None | |||||||||
NS
| |||||||||
LS, FN, PF, RA, TB BMC | |||||||||
LS, FN, PF, RA, TB aBMD | |||||||||
LS, FN, PF, RA, TB BA | |||||||||
Iuliano-Burns et al. 2003 [155] | 8.5-month randomized intervention trials with two factors (exercise and calcium) that each had two levels | Sex: female Age: 7–11 years Race: 15 % Asian descent Location: Melbourne, Australia | 66 | Frequency: 3×/week (PE) Intensity: moderate (2–4× body wt GRF) Time: 20 min/session Type: hopping-, jumping-, and skipping-based activities Control: stretching and low-impact dance routines (1× body wt) | DXA | Change, mean ± SEM | |||
EX | CON | ||||||||
Significant
| Calcium | Placebo | Calcium | Placebo | |||||
Leg BMC | 58.9 ± 7.1b
| 50.1 ± 3.3b
| |||||||
Femur BMC | 29.9 ± 4.1b
| 24.1 ± 2.0b
| |||||||
T-F BMC | 21.1 ± 1.8d,f
| 17.1 ± 1.3d
| 18.3 ± 2.2f
| ||||||
Arm BMC | 15.5 ± 1.9a,c
| 10.3 ± 1.3c,d
| 13.1 ± 0.91d
| 10.8 ± 1.3a
| |||||
Hum BMC | 7.3 ± 0.9c
| 5.2 ± 0.5c
| |||||||
U-R BMC | 4.4 ± 0.5a,c
| 3.1 ± 0.4c,d
| 4.7 ± 0.4d,e
| 3.3 ± 0.4a,c
| |||||
NS
| Like letters denote significant difference between groups (P < 0.05). An exercise-calcium interaction was detected at the femur (7.1 %). By contrast, there was no exercise–calcium interaction detected at the T-F; however, there was a main effect of exercise: BMC increased 2–4 % more in the calcium-supplemented groups than in the nonsupplemented groups at the humerus (12.0 vs 9.8 %) and R-U (12.6 vs 8.6 %). | ||||||||
TB, LS BMC | |||||||||
Specker and Binkley 2003 [81] | 1-year randomized, placebo-controlled, partially blinded trial of PA and calcium supplementation | Sex: male and female Age: 3–5 years Race: 94 % white, 6 % other Location: South Dakota | 178 | Frequency: 5×/wk Intensity: not specified Time: 30 min/day (5-min warm-up, 20-min activity, 5-min cool down) Type: hopping, jumping, skipping activities (17 different weekly programs) Control: 30 min/day of activities to keep them sitting quietly | DXA | Change, mean ± SEM | |||
Significant | EX | CON | |||||||
Calcium | Placebo | Calcium | Placebo | ||||||
Leg BMC | 40.9 ± 1.3 | 38.2 ± 1.2 | 37.3 ± 1.4 | 38.5 ± 1.3 | |||||
NS
| There was a significant interaction (P < 0.05) between the activity and supplement groups in leg BMC gain; the difference in BMC gain between EX and CON groups was more pronounced in children receiving calcium vs placebo. Among children receiving the placebo, leg BMC gain was similar in the EX and CON groups. However, among children receiving calcium, those in EX group has 9.7 % greater increase in leg BMC than those in CON group. | ||||||||
TB, arm BMC | |||||||||
TB, arm, leg BA | |||||||||
Stear et al. 2003 [156] | 15.5-month randomized, double-blind trial of PA and calcium supplementation | Sex: female Age: 17.3 ± 0.4 years Race: not listed Location: UK | 131 | Frequency: 3×/wk Intensity: moderate-to-vigorous intensity, moderate-to-high impact Time: 45 min/session (7- to 10-min warm-up, 30-min workout, 5- to 8-min warm-down and stretch) Type: exercise-to-music aerobics class Control: not invited to exercise sessions | DXA | No significant differences seen between EX and CON groups | |||
Significant
| |||||||||
None | |||||||||
NS
| |||||||||
TB, LS, Rad, R-Ul, R-Dis BMC | |||||||||
TB, LS, Rad, R-Ul, R-Dis SA-BMC | |||||||||
MacKelvie et al. 2004 [295] | 20-month jumping intervention Randomized by school | Sex: male Age: 8.8–12.1 years Race: multiethnic population of city (~34 % Hong Kong Chinese and 57 % North American/Western European Caucasian, 5 % Southeast Asian, and 4 % other or mixed ethnicity) reflected in cohort Location: Richmond, British Columbia | 64 | Frequency: 3×/wk (2× PE, 1 classroom) Intensity: progressed over 2 years by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: jumping exercises such as jumping jacks, lung jumps, hopping, jumping over various obstacles, drop jumps from platform Control: stretching | DXA | Change, mean (95 % CI) | |||
Significant
| EX | CON | |||||||
FN BMC | 0.50 (0.45, 0.55)** | 0.39 (0.34, 0.43) | |||||||
TB, LS, PF, FN, TR BA | |||||||||
NS
| FN BMC changes were significantly greater in EX boys (4.3 %); changes in bone area and BMC for other regions were not significantly different between groups. | ||||||||
TB, LS, PF, TR BMC | |||||||||
McKay et al. 2005 [297] | 8-month jumping intervention Control group used from previous study | Sex: male and female Age: 8.9 to 11.0 years Race: 38 % Caucasian, 48 % Asian, 15 % other (including mixed ethnic, black, and South Asian) Location: Richmond, British Columbia | 124 | Frequency: 3×/days Intensity: 5× body wt, maximum rate of force was >400 body wt/s (independent sample of 70 boys and girls) Time: 3 min/day Type: 10 counter movement jumps (two-foot take off, clutch knees, two-foot landing) Control: not specified, from previous study | DXA | Change, mean (95 % CI) | |||
Significant
| EX | CON | |||||||
TB BMC | 92.7 (83, 102)* | 106 (98, 114) | |||||||
TB BA | 76.7 (66.9, 86.5)* | 95.6 (87.6, 103.6) | |||||||
PF BMC | 2.3 (2.1, 2.6)* | 1.9 (1.7, 2.1) | |||||||
IT BMC | 1.5 (1.3, 1.7)* | 1.2 (1.0, 1.3) | |||||||
NS
| CON group had greater increase in adjusted TB BMC (1.4 %). EX group gained significantly more BMC at the PF (2 %) and at the IT region (27 %). | ||||||||
LS, PF, IT, GT, FN BA | |||||||||
LS, GT, FN BMC | |||||||||
Laing et al. 2005 [343] | 24-month quasi-experimental prospective gymnastics study Recruited due to enrollment in gymnastics | Sex: female Age: 4–8 years Race: 64 % white, 27 % black, 3 % Asian, 2 % Hispanic, 1 % Indian, and 3 % other Location: Athens, Georgia | 143 | Frequency: 1×/week Intensity: not specified Time: 1 h/session Type: recreational gymnastics class Control: participating in nongymnastic activities or no activities | DXA | Postintervention values, mean ± SD | |||
Significant
| EX | CON | |||||||
TB BA | 1392 ± 247* | 1545 ± 314 | |||||||
TB BMC | 997 ± 255* | 1151 ± 323 | |||||||
TB aBMD | 0.708 ± 0.06* | 0.736 ± 0.07 | |||||||
LS BA | 34.1 ± 50.5* | 36.6 ± 6.17 | |||||||
LS BMC | 20.5 ± 5.47* | 22.6 ± 6.24 | |||||||
PF BA | 18.8 ± 4.04* | 20.4 ± 4.53 | |||||||
PF BMC | 12.5 ± 4.07* | 14.1 ± 4.56 | |||||||
FA BA | 7.39 ± 1.58* | 8.05 ± 1.80 | |||||||
FA BMC | 2.85 ± 0.85* | 3.19 ± 0.97 | |||||||
NS
| Values suggest that EX remained lower in bone mineral measures after 2 years; however, after adjusting for initial differences, it was determined that EX had greater BA, BMC, and aBMD responses compared with CON at some skeletal sites. | ||||||||
LS, PF, FA aBMD | |||||||||
Yu et al. 2005 [242] | 36-week strength training intervention Randomized | Sex: male and female Age: 9–11 years Race: not specified Location: Hong Kong | 63 | Frequency: phase 1: 3×/week; phase 2: 1×/week Intensity: phase 1: 75 % 10 RM, increased to 100 % over time. 1 set, 20 reps; phase 2: weight adjusted according to ability. 2–3 sets of 10–20 reps Time: phase 1: 75 min/session (10-min warm-up, 30-min strength training, 10-min agility training, 5-min cool down); phase 2: 60 min/session (5-min warm-up, 10-min stretching, 40-min strength training, 5-min cool down) Type: phase 1: circuits (9 stations for strength training, 1 station for agility, 1 aerobic station); phase 2: similar to phase 1 Control: hypocaloric diet, no strength training | DXA | No significant differences in BMC were observed between the EX and CON groups at 36 weeks. | |||
Significant
| |||||||||
None | |||||||||
NS: | |||||||||
TB, TH, LS BMC | |||||||||
Valdimarsson et al. 2006 [344] | 1-year expanded PE intervention Randomized by school | Sex: female Age: 6.5–8.9 years Race: Caucasian Location: Malmö, Sweden | 103 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | Change, mean (SD) | |||
Significant
| EX | CON | |||||||
L2-L4 BMC | 2.4 (1.1)** | 1.8 (0.7) | |||||||
L3 BMC | 0.94 (0.63)*** | 0.53 (0.30) | |||||||
L2-L4 aBMD | 0.044 (0.03)*** | 0.026 (0.01) | |||||||
L3 aBMD | 0.047 (0.03)*** | 0.025 (0.02) | |||||||
L3 width | 0.17 (0.12)*** | 0.09 (0.06) | |||||||
NS
| The annual gain in BMC was 4.7 % higher in the LS and 9.5 % higher in L3 in the EX group than in the CON group. The annual gain in aBMD was 2.8 % higher in the LS and 3.1 % higher in L3 in the EX group than in the CON group. The annual gain in L3 width was 2.9 % higher in the EX group than in the CON group. | ||||||||
TB, FN, leg BMC | |||||||||
TB, FN, leg aBMD | |||||||||
L3, FN vBMD | |||||||||
FN width | |||||||||
Linden et al. 2006 [345] | 2-year expanded PE intervention Randomized by school | Sex: female Age: 6.5–8.9 years Race: white Location: Malmö, Sweden | 99 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | Change, mean | |||
Significant
| EX | CONZ | |||||||
L2-L4 BMC | 2.2* | 1.8 | |||||||
L3 BMC | 0.8*** | 0.6 | |||||||
L2-L4 aBMD | 0.034* | 0.026 | |||||||
FN vBMD | −0.004** | 0.006 | |||||||
L3 width | 0.136** | 0.092 | |||||||
NS
| The annual gain in BMC was greater in the EX group than in the CON group: L2-L4 3.8 %, L3 7.2 %. The EX group had greater annual gain in aBMD at L2-L4 (1.2 %). There was also a greater mean annual gain in bone size in the L3 vertebra (1.8 %). | ||||||||
TB, FN, leg BMC | |||||||||
TB, L3, FN, leg aBMD | |||||||||
L3 vBMD | |||||||||
FN width | |||||||||
Bass et al. 2007 [157] | 8.5-month randomized intervention trials with two factors (exercise and calcium) that each had two levels | Sex: male Age: 7–11 years Race: 22 % Asian descent Location: Melbourne, Australia | 88 | Frequency: 3×/week (PE) Intensity: moderate (2–8× body wt GRF) Time: 20 min/session Type: hopping-, jumping-, and skipping-based activities Control: stretching and low-impact dance routines (1× body wt) | DXA | Change, mean (SD) | |||
EX | CON | ||||||||
Significant
| Calcium | Placebo | Calcium | Placebo | |||||
Leg BMC | 64.4 (4.2)abc
| 54.0 (4.7)a
| 47.7 (4.2)b
| 43.3 (3.2)c
| |||||
Femur BMC | 30.1 (1.8)abc
| 24.9 (1.9)a
| 24.8 (1.4)b
| 23.1 (1.3)c
| |||||
T-F | 23.4 (2.1)a
| 16.8 (1.5)a
| |||||||
NS
| Like letters denote significant difference between groups (P < 0.05). The increase in femur BMC in the EX + calcium group was ~2 % greater than the increase in the EX + placebo, no-EX + calcium, or no-EX + placebo groups. At the T-F, the increase in BMC in the EX + calcium group was ~3 % greater than in the no-EX + placebo group | ||||||||
TB, LS, arm, Hum, U-R BMC | |||||||||
Linden et al. 2007 [298] | 1-year expanded PE intervention Randomized by school | Sex: male Age: 6.7–9.0 years Race: Caucasian (except 1 boy adopted from Colombia) Location: Malmö, Sweden | 138 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | Change, mean (SD) | |||
Significant
| EX | CON | |||||||
L3 BMC | 0.87 (0.55)*** | 0.58 (0.26) | |||||||
L3 aBMD | 0.041 (0.04)** | 0.027 (0.02) | |||||||
L3 width | 0.14 (0.14)*** | 0.07 (0.07) | |||||||
NS
| The mean annual gain in L3 BMC was 5.9 % higher, L3 aBMD a mean 2.1 % higher, and L3 width a mean 2.3 % higher in the EX group than in the CON group. | ||||||||
TB, FN BMC | |||||||||
TB FN aBMD | |||||||||
L3, FN vBMD | |||||||||
FN width | |||||||||
Barbeau et al. 2007 [346] | 10-month MVPA intervention Randomized | Sex: female Age: 8–12 years Race: black Location: Georgia | 201 | Frequency: every day school in session during school year; during summer Intensity: HR > 150 bpm during MVPA activity (HR monitor) Time: 110-min after-school program (80 min of PA) Type: 25-min skills development (dribbling basketball), 35-min MVPA, 20-min toning and stretching Control: no intervention | DXA | Difference, mean (95 % CI) | |||
Significant
| |||||||||
BMC | 0.044 (0.024, 0.064)*** | ||||||||
aBMD | 0.020 (0.012, 0.027)*** | ||||||||
Compared to the CON group, the EX group had a greater increase in BMC and aBMD. | |||||||||
Schneider et al. 2007 [347] | 1-year MVPA intervention Randomized by school | Sex: female Age: 15.04 years (SD = 0.79) Race: 57 % non-Hispanic white, 20 % Hispanic, 17 % Asian, 6 % other Location: 2 public high schools, location not specified | 122 | Frequency: 5 days/week Intensity: varied Time: 60 min/day Type: supervised activities included variety of aerobic (3×/week, including aerobic dance, kickboxing, and brisk walking) and strength-building (1×/week, including weightlifting and yoga) activities Control: no intervention | DXA | Percent change, mean | |||
Significant
| EX | CON | |||||||
TS BMC | 6.3** | 1.4 | |||||||
NS
| The effect of EX on BMC for the TS was significant and increased 6.3 % as opposed to 1.4 % in the CON group. None of the other sites for BMC or any aBMD measures were significant. | ||||||||
TB, LS, FN, TH, TR BMC | |||||||||
TB, LS, FN, TH, TS, TR aBMD | |||||||||
Gunter et al. 2008 [24] | 7-month jumping intervention Randomized by school | Sex: male and female Age: 7–10 years Race: not specified Location: Corvallis, OR | 56 | Frequency: 3×/week, during PE Intensity: Progressed to reach 90–100 jumps per session Time: 30 min/session (warm-up, fitness development (jumping), lesson focus, closing activity) Type: jumping Control: similar class structure, no jumping during fitness development | DXA | Postintervention values, mean (SD) | |||
Male | Female | ||||||||
Significant
| EX | CON | EX | CON | |||||
TH BMC | 28.5 (9.2)a
| 25.7 (7.56)a
| 24.6 (6.2)a
| 24.3 (6.1)a
| |||||
FN BMC | 3.8 (0.96)b
| 3.6 (0.77)b
| 3.3 (0.74)b
| 3.3 (0.71)b
| |||||
Other variables
|
aMales greater than females (P < 0.05); bmales greater than females (P < 0.01) Three years after the intervention had concluded, the EX group had 2.3, 3.2, 4.4, and 2.9 % greater BMC than controls at the LS, TH, FN, and TB, respectively. | ||||||||
TB, LS, TR BMC | |||||||||
Gunter et al. 2008 [24] | 7-month jumping intervention Randomized by school | Sex: male and female Age: 7–10 years Race: 47 white, 2 Asian Location: Corvallis, OR | 49 | Frequency: 3×/week, opposite PE Intensity: progressed to reach 100 jumps/session by the 5th wk of the program Time: 20 min/session (5-min warm-up, 10-min jumping or stretching, 5-min cool down) Type: jumps off 24 in box Control: nonimpact stretching | DXA | Postintervention values, mean (SD) | |||
Significant
| Males | Females | |||||||
EX | CON | EX | CON | ||||||
TH BMC | 39.93 (9.56)a
| 39.31 (9.93) | 31.26 (5.40)a
| 30.15 (3.38) | |||||
FN BMC | 4.92 (0.88)a
| 4.73 (0.93) | 4.18 (0.53)a
| 4.21 (0.69) | |||||
TR BMC | 11.11 (2.62)a
| 10.91 (2.54) | 8.31 (1.42)a
| 7.49 (1.05) | |||||
aMales significantly greater than females for all values (P < 0.01). Participants in the EX group had 1.4 % more TH BMC than those in the CON group after 8 years | |||||||||
Weeks et al. 2008 [296] | 8-month jumping intervention Randomized | Sex: male and female Age: boys 13.8 years (0.4); girls 13.7 years (0.5) Race: not specified Location: Gold Coast, Australia | 81 | Frequency: 2×/week Intensity: 1–3 Hz at a height of 0.2–0.4 m Time: 10 min (~300 jumps) Type: varied, but included jumps, hops, tuck jumps, jump squats, stride jumps, star jumps, lunges, side lunges, and skipping. Occasionally supplemented with upper body strengthening activities, including push-ups and exercises with resistive latex bands Control: usual PE warm-up and stretching | DXA | Girls in the EX group improved FN BMC (13.9 %) more than those in the CON group. Between-group comparisons of change showed EX group effects only for TB BMC (10.6 %) for boys. Boys in the EX group gained more TR BMC, LS BMC, and TB BMC than girls in the EX group. | |||
Significant
| |||||||||
FN BMC | |||||||||
TR BMC | |||||||||
TB BMC | |||||||||
NS
| |||||||||
FN, LS BA | |||||||||
LS BMC | |||||||||
Macdonald et al. 2008 [299] | 11-month PA and jumping intervention Randomized by school | Sex: male and female Age: 9–11 years Race: 53 % Asian (both parents or all four grandparents born in Hong Kong or China, India, Philippines, Vietnam, Korea, or Taiwan. 35 % Caucasian (parents born in North America or Europe). 12 % children mixed ethnicity or other ethnic origins Location: Vancouver and Richmond, British Columbia | 410 | Frequency: Classroom Action: 5 days/week; Bounce at the Bell: 5 days/week PA + 3×/day, 4 days/week jumping Intensity: not specified Time: Classroom Action: 15 min PA; Bounce at the Bell: 15 min PA + short bouts high-impact jumping Type: Classroom Action: skipping, dancing, playground circuits, simple resistance exercises with bands; Bounce at the Bell: Classroom Action + short bouts high-impact jumping. Phase I included 5 two-foot landing jumps (or 10 one-foot landing jumps) at each session. Phase II jumps were increased each month of the school year until a maximum of 36 jumps/day was reached. Control: usual PE | DXA | Percent difference, mean (95 % CI) | |||
Significant
| Males | Females | |||||||
FN BMC | 0.96 (−0.003, 1.93)* | 0.09 (0.005, 0.172)** | |||||||
LS BMC | 30.8 (7.2, 54.4)** | ||||||||
TB BMC | |||||||||
NS
| Boys in EX group had greater gains in BMC at the LS (2.7 %) and TB (1.7 %) than the controls did. Girls in the EX group had greater gains in FN BMC (3.5 %) than in controls. | ||||||||
PF BMC | |||||||||
Alwis et al. 2008 [300] | 1-year expanded PE intervention Randomized by school | Sex: female Age: 6.5–8.9 years Race: Caucasian Location: Malmö, Sweden | 103 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | No between-group differences were found during the 12-month study period for changes in FN variables. | |||
Significant
| |||||||||
None | |||||||||
NS
| |||||||||
FN BMC, aBMD, vBMD | |||||||||
Alwis et al. 2008 [300] | 2-year expanded PE intervention Randomized by school | Sex: male Age: 6.7–9.0 years Race: Caucasian Location: Malmö, Sweden | 137 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | Change, mean (SD) | |||
Significant
| EX | CON | |||||||
L3 BMC | 0.72 (0.30)** | 0.58 (0.26) | |||||||
L3 width | 0.11 (0.07)** | 0.07 (0.07) | |||||||
NS
| The mean annual gain in L3 BMC (3 %) and L3 width (1.3 %) were greater in the EX group than in the CON group . | ||||||||
TB, FN BMC | |||||||||
FN width | |||||||||
Alwis et al. 2008 [300] | 2-year expanded PE intervention Randomized by school | Sex: female Age: 6.8–8.9 years Race: Caucasian Location: Malmö, Sweden | 83 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | No between-group differences were observed for annual changes in the FN variables. | |||
Significant
| |||||||||
None | |||||||||
NS
| |||||||||
FN BMC, aBMD | |||||||||
Meyer et al. 2011 [348] | 9-month additional PE session intervention Randomized by class | Sex: male and female Age: prepubertal = 6–7 years; early pubertal = 11–12 years Race: not specified Location: Aargau and Baselland, Switzerland | 291 | Frequency: 2×/week (PE); 3×/day (activity breaks); 1×/day (home activity) Intensity: not specified Time: 45 min/session (PE); 2–5 min/session (activity breaks); 10 min/day (home activity) Type: Two PE lessons (plus 3 regular PE classes) taught mostly outdoors by PE teachers. All five sessions included jumping activities like hopping, jumping up and down stairs, rope skipping, etc. During academic lessons, 3–5 activity breaks comprised motor skill tasks such as jumping around on one leg, balancing on one leg, power games, or coordinative tasks were introduced every day. Daily home activity included aerobic, strength, or motor skill tasks like tooth brushing while standing on one leg, jumping up and down the stairs, and rope jumping. Control: participated in regular PE classes 3×/week | DXA | Difference, Z-score (95 % CI) | |||
Significant
| EX | ||||||||
TB BMC | 0.138 (0.06, 0.216)*** | ||||||||
FN BMC | 0.136 (0.008, 0.264)* | ||||||||
LS BMC | 0.118 (0.028, 0.2017)** | ||||||||
TB aBMD | 0.212 (0.088, 0.337)*** | ||||||||
LS aBMD | 0.184 (0.083, 0.285)*** | ||||||||
NS
| Compared to CON group, children in EX group showed statistically significant increases in BMC of TB (5.5 %), FN (5.4 %), and LS (4.7 %) and aBMD of TB (8.4 %) and LS (7.3 %) | ||||||||
FN aBMD | |||||||||
Silva et al. 2011 [349] | Sports study Recruited based on sport participation | Sex: male Age: 10–18 years Race: not specified Location: Brazil | 46 | Inclusion criteria: 3 year experience in sport, training at least 10 h/week in previous 6 months, only PA associated with sport, high competitive level Control: normal PE | DXA | aBMD, mean (SD) | |||
Significant
| Tennis | Soccer | Swimming | Controls | |||||
PF aBMD | 1.02 (0.18)* | 1.08 (0.16)* | |||||||
NS
| Results showed higher mean values in the PF region of tennis and soccer players than of swimmers and controls. In relation to the impact of sporting activities based on bone age determination, a significant difference in aBMD was observed at all evaluated sites at the end of puberty (16–18 years) compared with 10–12 years, with increases of 78 % at the LS, 37 % at the PF, and 38 % TB. | ||||||||
LS, TB aBMD | |||||||||
Lofgren et al. 2012 [28] | 4-year expanded PE intervention Randomized by school | Sex: male and female Age: 6.5–8.7 years Race: Caucasian Location: Malmö, Sweden | 221 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | Change, mean (95 % CI) | |||
Significant
| Male | Female | |||||||
EX | CON | EX | CON | ||||||
TB BMC | 179.6 (160.5, 198.7)* | 166.4 (149.4, 183.4) | |||||||
LS BMC | 7.0 (6.5, 7.6)* | 6.2 (5.8, 6.6) | 9.1 (7.9, 10.3)** | 7.1 (6.1, 8.0) | |||||
FN BMC | 0.29 (0.26, 0.31) | 0.27 (0.24, 0.31) | 0.39 (0.33, 0.45)** | 0.28 (0.23, 0.33) | |||||
TR BMC | 0.92 (0.82, 1.02)** | 0.72 (0.62, 0.83) | |||||||
L3 width | 0.13 (0.11, 0.14)** | 0.11 (0.09, 0.12) | |||||||
FN width | 0.12 (0.11, 0.13)* | 0.11 (0.09, 0.12) | 0.15 (0.12, 0.17)** | 0.10 (0.08, 0.13) | |||||
The mean annual gain in LS BMC was 7.0 % higher in girls and 3.3 % higher in boys, and in FN width 1.7 % higher in girls and 0.6 % higher in boys in the EX group than in the CON group. | |||||||||
Detter et al. 2014 [303] | 6-year expanded PE intervention Randomized by school | Sex: male and female Age: 6–8 years Race: Caucasian Location: Malmö, Sweden | 295 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added, Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | DXA | Difference, mean (95 % CI) | |||
Significant
| Male | Female | |||||||
LS aBMD | 0.006 (0.002, 0.01)** | 0.01 (0.003, 0.02)* | |||||||
FN BMC | 0.07 (0.01, 0.12)* | ||||||||
NS
| Girls in the EX group, compared with girls in the CON group, had 0.009 g/cm2 larger gain annually in LS aBMD and 0.07 g larger gain in FN BMC. Boys in the EX group has 0.006 g/cm2 larger gain annually in LS aBMD than CON boys, | ||||||||
TB, FN aBMD | |||||||||
TB, LS BMC | |||||||||
FN, LS BA | |||||||||
Observational studies | |||||||||
Reference | Study description | Population description |
N
| Exposure | End points | Results | |||
Lehtonen-Veromaa et al. 2000 [350] | 1-year prospective case comparison | Sex: 155 females Baseline age: 9–15 years Race: white Location: Turku, Finland | 51 gymnasts, 50 runners, 54 controls | Method: self-report questionnaire (2×) Variable: leisure-time PA met (h/week) | Follow-up TH (and subregions), LS aBMD, and BA | The 1-year increase in adjusted aBMD at the FN of the gymnasts was 115 % larger than that of the controls and 125 % larger than that of the runners. The 1-year increase in adjusted aBMD at the TR of the gymnasts was 49 % larger than that of controls. | |||
Molgaard et al. 2001 [245] | 1-year prospective follow-up | Sex: 140 males, 192 females Baseline age: 5–19 years Race: white Location: Copenhagen, Denmark | 332 | Method: 24-h recall questionnaire (3×) (I, supine; II, sitting; III, walking; IV, breathless PA) Variable: breathless PA (h/day) | Follow-up TB BMC, BA | Breathless PA not associated with BMC or BA | |||
Gustavsson et al. 2003 [351] | 2.5-year and 6-year prospective case comparison | Sex: 68 males Baseline age: 16 years Race: white Location: Umea, Sweden | 22 hockey, 21 retired hockey, 25 controls | Method: reported participation in ice hockey Variable: group membership: hockey, retired hockey, no hockey | Follow-up at 30 months (~2.5 years) and follow-up at 70 months (~6 years) TB, FN, LS aBMD | At 30 months, hockey players had greater gains in aBMD FN than controls (0.07 vs 0.03 g/cm2). Hockey players had significantly higher aBMD at FN and TB than controls. At 70 months, hockey players had greater aBMD at the FN, TB, and LS compared to nonplayers. Retired hockey players still had 4 % higher aBMD of FN than nonplayers after 70 months | |||
Nurmi-Lawton et al. 2004 [352] | 3-year prospective case comparison | Sex: 97 females Baseline age: 7.9–17.2 years Race: primarily white Location: England | 45 gymnasts, 52 controls | Method: reported participation in gymnastics Variable: group membership gymnastics, no gymnastics | Multilevel model comparing differences in TB, LS, arm, and leg BMC, as well as aBMD each year | Gymnasts had 24–51 % greater BMC and 13–28 % greater aBMD than controls. | |||
Laing et al. 2005 [343] | 2-year quasi-experimental | Sex: 143 females Baseline age: 4–8 years Race: 64 % white, 27 % Black, 3 % Asian, 2 % Hispanic, 4 % other Location: Athens, Georgia | 65 gymnasts, 78 controls | Method: reported participation in gymnastics Variables: group membership gymnastics, no gymnastics, and h gymnastics participation per week | Follow-up TB, LS, PF, forearm BMC, aBMD, and BA | LS aBMD and forearm BA increased at a greater rate in gymnasts than in controls. Forearm BA increased at a greater rate in high-hours-per-week gymnastics over low-hours-per-week gymnastics | |||
Janz et al. 2006 [353] | 3-year prospective follow-up | Sex: 171 males, 199 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 370 | Method: ActiGraph accelerometer Variables: total PA ct/min, active min/day (≥3000 ct/min) | Follow-up TB, TH, TR, and LS BMC | PA was significantly associated with TB, TH, TR, and LS BMC in males. In females, PA was associated with TB and TR BMC. PA explained 1–2 % of variance in BMC. | |||
Nordstrom et al. 2006 [354] | ~8-year prospective case comparison | Sex: 90 males Baseline age: 15–19 years Race: Caucasian Location: Umea, Sweden | 63 athletes, 27 controls | Method: reported participation in ice hockey or badminton Variables: weight-bearing PA (h/week) | Follow-up and sustained effects TB, FN, TH, and Hum BMD; FN BA, TH BA | Active athletes had significantly higher BMD at all measured sites vs controls (P < 0.05). Former athletes still had higher BMD of the FN, TH, and Hum than did controls (P < 0.05). | |||
Baxter-Jones et al. 2008 [22] | ~15-year prospective follow-up | Sex: 72 males, 82 females Baseline age: 8–15 years Race: not specified Location: Saskatoon, Saskatchewan, Canada | 154 | Method: self-report questionnaire (3×/year for 3 years, 2×/year after) Variable: general level of PA for year (1–5) | Follow-up (age 23–30 years) TB, LS, TH, and FN BMC | In young adulthood, males who were physically active as adolescents had 8–9 % greater BMC at TB, TH, and FN compared to inactive adolescent males. In young adulthood, females who were active adolescents had 9 % greater TH and 10 % greater FN compared to inactive adolescent females | |||
Cheng et al. 2009 [54] | 7-year prospective follow-up | Sex: 396 females Baseline age: 10–13 years Race: not specified Location: Jyvaskyla, Finland | 396 | Method: self-report leisure-time PA questionnaire with parent help Variables: leisure-time PA score | Follow-up TB BMC | PA did not contribute to variability in BMC. | |||
Janz et al. 2010 [355] | 3-year and 6-year prospective follow-up | Sex: 148 males, 185 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 333 | Method: ActiGraph accelerometer Variables: MVPA min/day (>3000 ct/min) | Follow-up at age 8 and age 11 TB, TH, and LS BMC | After adjustment for concurrent (age 8 or 11) age, height, weight, somatic maturity, and MVPA, age 5 MVPA was significant predictor of ages 8 and 11 BMC in boys and girls at TB, TH, and LS. | |||
Tervo et al. 2010 [356] | ~12-year case comparison | Sex: 85 males Baseline age: 15–19 years Race: not specified Location: Umea, Sweden | 18 badminton, 44 ice hockey, 23 controls | Method: reported participation in badminton or ice hockey Variables: weight-bearing PA (h/week) | Follow-up and sustained effects of TB, Hum, LS, FN, and leg aBMD | After adjusting for confounders, badminton players gained significantly more aBMD at all sites compared to both ice hockey players and controls. Ice hockey players gained significantly more aBMD at FN and Hum than at controls. After the end of the active career, ice hockey players and badminton players lost aBMD at a similar rate resulting in still significantly higher aBMD at all sites in badminton players compared to both ice hockey players and controls | |||
Erlandson et al. 2011 [357] | 4 year prospective case comparison | Sex: 163 males and females Baseline age: 4–7 years Race: 95 % white, 2 % Asian, 3 % other (biracial) Location: Saskatoon, Saskatchewan, Canada | 163 gymnasts, ex-gymnasts, nongymnasts | Method: parental-report questionnaire Variables: current PA score | Multilevel model comparing TB, FN, and LS BMC | By year 4, recreational and precompetitive gymnasts had 3 % more TB and 7 % more FN BMC than those in other sports when body size, PA, and diet were considered | |||
Scerpella et al. 2011 [358] | ~12-year prospective case comparison | Sex: 20 females Baseline age: 8–12 years Race: not specified Location: Syracuse, New York, USA | 6 ex-gymnasts, 14 nongymnasts | Method: self-report questionnaire Variables: activity (h/week) | Follow-up and sustained effect of skull aBMD and BMC; R-UD and 1/3 radius BA, BMC, and aBMD | All R-UD parameters were higher in ex-gymnasts than in nongymnasts (P < 0.02). In contrast, skull aBMD was not associated with gymnastic status. Gymnastic cessation was associated with an abrupt, temporary decrease in 1/3 aBMD, R-UD BMC, and R-UD aBMD. No significant gymnast cessation effects were observed for 1/3 BMC, 1/3 BA, R-UD BA, or skull aBMD | |||
Erlandson et al. 2012 [359] | 14-year prospective case comparison | Sex: 47 females Baseline age: 8–15 years Race: not specified Location: Saskatoon, Saskatchewan, Canada | 25 gymnasts, 22 controls | Method: self-report questionnaire Variables: past-week PA score | Follow-up TB, FN, LS BMC, and aBMD | Gymnasts had significantly greater size-adjusted BMC and aBMD compared to nongymnasts at all sites, with the exception of FN aBMD in adulthood. Retired gymnasts had greater size-adjusted TB (13 %), LS (19 %), and FN (13 %) BMC and TB (8 %) and LS (13 %) aBMD compared to nongymnasts. | |||
Farr et al. 2013 [360] | 2-year prospective follow-up | Sex: 248 females Baseline age: 9–12 years Race: 90 % white, 6 % Asian, 2 % black or African American, 1 % Native American or Alaska Native, 1 % Native Hawaiian or Pacific Islander, and 0.5 % other Location: Tucson, Arizona, USA | 248 | Method: self-report questionnaire Variables: past-year PA score | Follow-up tibia and femur cortical and trabecular vBMD | PA associated with increases in trabecular vBMD at metaphyseal femur | |||
Francis et al. 2014 [361] | 10-year prospective follow-up | Sex: 156 males, 170 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 326 | Method: ActiGraph accelerometer Variables: MVPA min/day (> 2296 ct/min) VPA min/day (> 4011 ct/min) | Follow-up at ages 13 and 15 LS and TH BMC | Ages 13 and 15 male LS BMC adjusted for baseline LS BMC predicted by age 5 MVPA and VPA | |||
Janz et al. 2014 [248] | 10-year prospective follow-up | Sex: 217 males, 235 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 452 | Method: ActiGraph accelerometer Variables: MVPA min/day (>2296 ct/min) VPA min/day (> 4011 ct/min) | TH and LS BMC at five measurement cycles (age 5, 8, 11, 13, and 15 years). Multilevel model included individual growth curves for each participant | MVPA and VPA added to prediction BMC at all assessed cycles except MVPA LS BMC in females age 5, and males in the 90th percentile for VPA had 8.5 % more hip BMC than males in the 10th percentile for VPA. At age 15, this difference was 2.0 %. Females at age 5 in the 90th percentile for VPA had 6.1 % more hip BMC than those in the 10th percentile for VPA. Age 15 difference was 1.8 %. | |||
Janz et al. 2014 [248] | 12-year prospective follow-up | Sex: 160 males, 189 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 349 | Method: ActiGraph accelerometer Variables: MVPA min/day (>2296 ct/min) | Follow-up (age 17) TB and TH BMC and aBMD | At age 17, girls in high trajectory for MVPA had greater TB BMC, TH BMC, and TH aBMD than in the other trajectories. Boys in the high trajectory for MVPA had greater TB BMC, TH BMC, and TH aBMD than in the other trajectories. | |||
Cardadeiro et al. 2014 [362] | 1-year prospective follow-up | Sex: 81 males, 96 females Baseline age: 10–12 years Race: primarily white Location: Lisbon area, Portugal | 177 | Method: bone-specific administered questionnaire ActiGraph accelerometer Variables: PA score Sedentary min/day (≤100 ct/min) Light min/day (101–2295 ct/min) Moderate min/day (2296–4011 ct/min) Vigorous min/day (>4012 ct/min) | Follow-up aBMD PF and subregions | PA measured with questionnaire and accelerometer measured MVPA significant in TR aBMD males. Questionnaire significant in superolateral FN aBMD, inferomedial FN aBMD, and FN aBMD in females | |||
Lappe et al. 2014 [172] | 6-year prospective follow-up | Sex: 910 males, 833 females Baseline age: 5–19 years Race: nonblack, black Location: Los Angeles, CA; Cincinnati, OH; Omaha, NE; Philadelphia, PA; New York, NY | 1743 | Method: self/parental-report questionnaire (1×/year) Variable: weight-bearing PA (h/week) | Follow-up and mixed-model analysis %chgBMC for TB, LS, and TH at each TS of maturity | The greatest BMC accrual at all skeletal sites occurred at TS4, with the exception that the greatest % accrual in hip BMC in females was at TS3. Significant PA × TS interactions were only observed in nonblack males and only for TB BMC. All other PA × TS interaction effects were nonsignificant. PA was a significant predictor of chgBMC at all skeletal sites after adjustment for calcium in nonblack males, LS and TH in black males, TB and TH in nonblack females, and at LS in black females. |
Results
Nutrition and peak bone mass
Macronutrients
-
Grade: Level of evidence D was assigned for evidence for the benefit of fat on bone.
-
Grade: Level of evidence C was assigned for the benefit of protein on bone.
Micronutrients
-
Grade: Level of evidence A was assigned for the benefit of calcium on bone.
-
Grade: Level of evidence B was assigned for the benefit of vitamin D on bone.
-
Grade: Level of evidence D was assigned for the benefit of micronutrients other than calcium and vitamin D on bone.
Food patterns (Table 8)
Dairy
Fiber
Fruits and vegetables
Detriment of cola and caffeinated beverages
Fruits and vegetables
-
Grade: Level of evidence B was assigned for the benefit of dairy consumption on bone. Level of evidence C was assigned for the benefit of certain types of fiber and fruit and vegetable intake on bone, as well as for a detrimental effect of cola and caffeinated beverages on bone.
Infant nutrition (Table 9)
-
Grade: Level of evidence D was assigned for the benefit of duration of breastfeeding on bone. Level of evidence D was assigned for the benefit of breastfeeding versus formula feeding on bone. Level of evidence D was assigned for the benefit of enriched formula feeding on bone.
Adolescent special issues
-
Grade: Level of evidence B was assigned for the detriment of DMPA injections on bone. Level of evidence D was assigned for the detriment of OCs on bone.
-
Grade: Level of evidence D was assigned for the detriment of alcohol on bone.
-
Grade: Level of evidence C was assigned for the detriment of smoking on bone.
Physical activity and exercise
-
Grade: Level of evidence A was assigned for the benefit of physical activity and exercise on bone mass and density.
Reference | Study description | Population description | Number of subjects | Intervention | End points | Results | ||
---|---|---|---|---|---|---|---|---|
RCTs | ||||||||
Heinonen et al. 2000 [244] | 9-month step aerobics/ jumping intervention Randomized by school | Sex: female Age: 10–15 years Race: not specified Location: Tampere, Finland | 126 | Frequency: 2×/week Intensity: progressive Time: 50 min (10-min warm-up, 15-min nonimpact aerobic exercises, 20-min high-impact/jump training, 5-min cool down) Type: both-leg jumps at floor level, both-leg box jumps, one-leg box jumps Control: normal PA | pQCT
Significant
None
NS
Tibia CoD, CoA, BSI | At the tibial midshaft, the intergroup differences (CoD, CoA, and BSI) were not significant | ||
Petit et al. 2002 [73] | 7-month jumping intervention Randomized by school | Sex: female Age: 9–12 years Race: multiethnic population of city (~34 % Hong Kong Chinese and 57 % white) reflected in cohort Location: Richmond, British Columbia | 177 | Frequency: 3×/week (2× PE, 1 classroom) Intensity: progressed over school year by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm) Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: jumping exercises—jumping jacks, lung jumps, hopping, jumping over various obstacles, drop jumps from platform Control: stretching | pQCT | Change in early pubertal girls, mean (95 % CI) | ||
Significant
| EX | CON | ||||||
NN CSA | 0.060 (0.043, 0.077)* | 0.035 (0.021, 0.049) | ||||||
NN Z | 0.145 (0.118, 0.0172)* | 0.106 (0.084, 0.129) | ||||||
NN CT | 0.012 (0.008, 0.016)* | 0.007 (0.004, 0.010) | ||||||
IT ED | 0.092 (0.064, 0.120)* | 0.138 (0.114, 0.161) | ||||||
NS
| There was no difference in change for bone structure in the PRE girls. The more mature girls (EARLY) in the EX group showed significantly greater gains in CSA and reduced endosteal expansion. Changes in SPW did not differ. Structural changes improved Z at the NN (4.0 %), but not at the IT region. There were no differences at the primarily cortical FS. | |||||||
NN length, SPW, ED | ||||||||
IT CSA, SPW, Z | ||||||||
FS CSA, SPW, Z, ED, CT | ||||||||
Specker and Binkley 2003 [81] | 1-year randomized, placebo-controlled, partially blinded trial of PA and calcium supplementation | Sex: male and female Age: 3–5 years Race: 94 % white, 6 % other Location: South Dakota | 178 | Frequency: 5 days/week Intensity: not specified Time: 30 min/day (5-min warm-up, 20-min activity, 5-min cool down) Type: hopping, jumping, skipping activities (17 different weekly programs) Control: 30 min/day of activities to keep them sitting quietly | pQCT | Exercise group had greater PCirc and ECirc than control group (P < 0.05). | ||
Significant
| ||||||||
PCirc | ||||||||
ECirc | ||||||||
NS
| ||||||||
CA, CT | ||||||||
MacKelvie et al. 2004 [295] | 20 month jumping intervention Randomized by school | Sex: male Age: 8.8–12.1 years Race: multiethnic population of city (~34 % Hong Kong Chinese and 57 % North American/Western European Caucasian, 5 % Southeast Asian, and 4 % other or mixed ethnicity) reflected in cohort Location: Richmond, British Columbia | 64 | Frequency: 3×/week (2× PE, 1 classroom) Intensity: progressed over school year by increasing number of jumps per station (from 10 to 20) and height (from 10 to 50 cm Time: 10–12 min (5 circuits, ~1.5–2 min each) Type: jumping exercises- jumping jacks, lung jumps, hopping, jumping over various obstacles, drop jumps from platform Control: stretching | HSA | Change, mean (95 % CI) | ||
Significant
| EX | CON | ||||||
NN CSMI | 0.23 (0.20, 0.27)* | 0.17 (0.14, 0.20) | ||||||
NN Z | 0.13 (0.11, 0.15)* | 0.09 (0.072, 0.11) | ||||||
NS
| At the NN region, EX boys had significantly greater changes in Z (7.5 %). Changes at the IT and FS regions were not significantly different between groups. | |||||||
NN length, CSA, PW, EW, CT | ||||||||
IT CSMI, CSA, PW, Z, ED, CT | ||||||||
FS CSA, PW, CSMI, Z, EW, CT | ||||||||
McKay et al. 2005 [297] | 8-month jumping intervention Control group used from previous study | Sex: male and female Age: 8.9 to 11.0 years Race: 38 % Caucasian, 48 % Asian, 15 % other (including mixed ethnic, black, and South Asian) Location: Richmond, British Columbia | 124 | Frequency: 3×/day Intensity: 5× body wt, maximum rate of force was > 400 body wt/s (independent sample of 70 boys and girls) Time: 3 min/day Type: 10 counter movement jumps (two-foot take off, clutch knees, two-foot landing) Control: not specified, from previous study | HSA | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
NN and FS BMD, CSA, SW, Z, ED, CT | ||||||||
Macdonald et al. 2007 [25] | 16-month PA and jumping intervention Randomized by school | Sex: male and female Age: 10.2 ± 0.6 years Race: 53 % Asian (Hong Kong or China, India Philippines, Vietnam, Korea, or Taiwan), 35 % Caucasian (North America or Europe), 12 % mixed or other ethnic origins Location: Richmond and Vancouver, British Columbia | 410 | Frequency: Classroom Action: 5 days/week; Bounce at the Bell: 5 days/week PA + 3×/day, 4 days/week jumping Intensity: not specified Time: Classroom Action: 15 min of PA; Bounce at the Bell: 15 min of PA + short bouts of high-impact jumping Type: Classroom Action: skipping, dancing, playground circuits and simple resistance exercises with bands; Bounce at the Bell: Classroom Action + short bouts high-impact jumping Control: regular PE | pQCT | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
Distal and midshaft BSI, ToA, ToD | ||||||||
Linden et al. 2007 [298] | 1 year expanded PE intervention Randomized by school | Sex: Male Age: 6.7–9.0 years Race: Caucasian (except 1 boy adopted from Colombia) Location: Malmö, Sweden | 138 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | HSA | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
FN CSMI, Z, CSA | ||||||||
Macdonald et al. 2008 [299] | 8-month PA and jumping intervention Randomized | Sex: male and female Age: 9–11 years Race: 53 % Asian (both parents or all four grandparents born in Hong Kong or China, India, Philippines, Vietnam, Korea, or Taiwan. 35 % Caucasian (parents born in North America or Europe). 12 % children mixed ethnicity or other ethnic origins Location: Vancouver and Richmond, British Columbia | 410 | Frequency: Classroom Action: 5 days/week; Bounce at the Bell: 5 days/week PA + 3×/day, 4 days/week jumping Intensity: not specified Time: Classroom Action: 15 min PA; Bounce at the Bell: 15 min PA + short bouts high-impact jumping Type: Classroom Action: skipping, dancing, playground circuits, simple resistance exercises with bands; Bounce at the Bell: Classroom Action + short bouts high-impact jumping. Phase I included 5 two-foot landing jumps (or 10 one-foot landing jumps) at each session. Phase II jumps were increased each month of the school year until a maximum of 36 jumps/day was reached. Control: Usual PE | HSA | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
NN Z, CSA, SPW | ||||||||
Alwis et al. 2008 [300] | 1-year expanded PE intervention Randomized by school | Sex: female Age: 6.5–8.9 years Race: Caucasian Location: Malmö, Sweden | 103 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | HSA | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
FN length, PW, CSA, Z, CSMI, EW, CT | ||||||||
Alwis et al. 2008 [300] | 2-year expanded PE intervention Randomized by school | Sex: male Age: 6.7–9.0 years Race: Caucasian Location: Malmö, Sweden | 137 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added. Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | HSA | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
FN CSA, Z, CSMI | ||||||||
Alwis et al. 2008 [300] | 2-year expanded PE intervention Randomized by school | Sex: female Age: 6.8–8.9 years Race: Caucasian Location: Malmö, Sweden | 291 | Frequency: 2×/week (PE); 3×/day (activity breaks); 1×/day (home activity) Intensity: not specified Time: 45 min/session (PE); 2–5 min/session (activity breaks); 10 min/day (home activity) Type: 2 PE lessons (plus 3 regular PE classes) taught mostly outdoors by PE teachers. All five sessions included jumping activities such as hopping, jumping up and down stairs, rope skipping, etc. During academic lessons, 3–5 activity breaks comprised motor skill tasks such as jumping around on one leg, balancing on one leg, power games, or coordinative tasks were introduced every day. Daily home activity included aerobic, strength, or motor skill tasks such as tooth brushing while standing on one leg, jumping up and down the stairs, and rope jumping. Control: participated in regular PE classes 3×/week | HSA | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
FN CSA, PW, Z, CSMI | ||||||||
Weeks et al. 2008 [296] | 8-month jumping intervention Randomized | Sex: male and female Age: boys 13.8 years (0.4); girls 13.7 years (0.5) Race: not specified Location: Gold Coast, Australia | 81 | Frequency: 2×/week Intensity: 1–3 Hz at a height of 0.2–0.4 m Time: 10 min (~300 jumps) Type: varied, but included- jumps, hops, tuck jumps, jump squats, stride jumps, star jumps, lunges, side lunges, and skipping. Occasionally supplemented with upper body strengthening activities, including push-ups and exercises with resistive latex bands Control: usual PE warm-up and stretching | DXA | Percent change, mean | ||
Significant
| EX | CON | ||||||
LS IBS | 17.9* | 14.4 | ||||||
NS
| LS IBS improved more for EX participants than for CON. No other differences in 8-month change in parameters of bone strength reached significance. | |||||||
FN, LS BMAD | ||||||||
FN CSMI | ||||||||
Greene et al. 2009 [301] | 28-week drop-landing intervention Randomized | Sex: female Age: 6–10 years Race: not listed Location: Sydney, Australia | 39 | Frequency: 3×/week Intensity: 14-cm height drop for low drop, 28-cm height drop for high drop (GRF 2–4× body wt); 10 sets of 5 steps per set; 50 steps per session Time: 15 min/day Type: single leg drop-landing exercises with nondominant leg serving as the training leg (dominant leg served as within-participant untrained control) Control: normal activity | pQCT | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
Cort, Medullary, and Total BA at Proximal, Mid, Distal | ||||||||
Macdonald et al. 2009 [250] | 16-month PA and jumping intervention Randomized | Sex: male Age: 10.2 ± 0.6 years Race: 52 % Asian (Hong Kong or China, India, Philippines, Vietnam, Korea, or Taiwan), 35 % Caucasian (North America or Europe), 12 % mixed or other ethnic origins Location: Richmond and Vancouver, British Columbia | 205 | Frequency: Classroom Action: 5 days/week; Bounce at the Bell: 5 days/week PA + 3×/day, 4 days/week jumping Intensity: not specified Time: Classroom Action: 15 min PA; Bounce at the Bell: 15 min PA + short bouts high-impact jumping Type: Classroom Action: skipping, dancing, playground circuits, simple resistance exercises with bands; Bounce at the Bell: Classroom Action + short bouts high-impact jumping. Phase I included 5 two-foot landing jumps (or 10 one-foot landing jumps) at each session. Phase II jumps were increased each month of the school year until a maximum of 36 jumps/day was reached. Control: Usual PE | pQCT | Difference, mean (95 % CI) | ||
Significant
| ||||||||
I
max
| 338.6 (16.4, 660.9)* | |||||||
NS
| The EX boys had a 3 % greater gain in I
max than CON boys. No other bone structural parameters differed between groups. | |||||||
I
min, I
max/I
min, CoA- Ant, CoA- Med, CoA- Post, CoA- Lat, CTh- Ant, CTh- Med, CTh- Post, CTh- Lat | ||||||||
Lofgren et al. 2012 [28] | 4-year expanded PE intervention Randomized by school | Sex: male and female Age: 6.5–8.7 years Race: Caucasian Location: Malmö, Sweden | 221 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | HSA | Change, mean (95 % CI) | ||
Male | Female | |||||||
EX | CON | |||||||
FN CSA | 0.11 (0.10, 0.13)* | 0.09 (0.07, 0.11) | ||||||
FN Z | 0.06 (0.05, 0.06)* | 0.05 (0.04, 0.06) | ||||||
FN CSMI | 0.10 (0.08, 0.11)* | 0.08 (0.07, 0.09) | ||||||
The EX girls had significantly greater gain in all HSA outcomes than CON girls. No differences were seen for boys. | ||||||||
Anliker et al. 2012 [302] | 9-month jumping intervention Randomized by school | Sex: male and female Age: 8–12 years Race: not listed Location: Lucerne, Switzerland | 45 | Frequency: 2×/week Intensity: intensity increased weekly. Number of jumps increased over time from ~60 to ~150 per session Time: 10 min Type: Jumping and sprinting exercises, including two- and one-legged hopping, drop jumps, side to side jumps, jumping jacks, jumps and landings from a podium, jumps over barriers and short multidirectional sprints Control: not specified | pQCT | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
Tibia 4 % vBMC, vBMDtr, vBMDtot, BAtb, BAtot | ||||||||
Detter et al. 2014 [303] | 6-year expanded PE intervention Randomized by school | Sex: male and female Age: 6–8 years Race: Caucasian Location: Malmö, Sweden | 133 | Frequency: 5 days/week Intensity: varied Time: 40 min/day Type: normal PE curriculum (running, jumping, climbing ropes, variety of ball games). Activities varied to reduce boredom. No specific osteogenic training program was added Control: normal PE curriculum, duration within normal limits (1–2 sessions/week, in total 60 min/week) | Cross-sectional pQCT | Change in bone structural parameters did not differ between groups. | ||
Significant
| ||||||||
None | ||||||||
NS
| ||||||||
Tibia 4 %, Radius 4 % | ||||||||
TR vBMD | ||||||||
Tibia 38 %, Radius 66 % | ||||||||
Cort vBMD | ||||||||
Cort BMC | ||||||||
Cort BA | ||||||||
Cort Th | ||||||||
CSA | ||||||||
Polar SSI | ||||||||
Observational studies | ||||||||
Reference | Study description | Population description |
N
| Exposure | End points | Results | ||
Forwood et al. 2006 [363] | 7-year prospective follow-up | Sex: 109 males, 121 females Baseline age: 8–15 years Race: white Location: Saskatoon, Saskatchewan, Canada | 230 | Method: self-report questionnaire (3×/year for 3 years, 2×/year after) Variable: general level of PA for year (1–7) | Multilevel models for FN Z, CSA, and SPW (HSA) | MVPA positively associated with FN Z and FN CSA males and females. A male with PA score of 1 had 0.0972 cm2 less CSA than a male with PA score of 5. Females with PA score of 1 had 0.0588 cm2 less CSA than females with score of 5. Males with PA score of 1 had 0.0615 cm2 less Z than males with PA score of 5. Females with PA score of 1 had 0.0355 cm2 less Z than females with score of 5. | ||
Janz et al. 2007 [364] | 6-year prospective follow-up | Sex: 212 males, 233 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 445 | Method: ActiGraph accelerometer Variable: MVPA min/day (>3000 ct/min) | Multilevel models for FN Z and CSA (HSA) | MVPA positively associated with Z and CSA males and females. When adjusted, LM only significant males | ||
40-min MVPA predicted 3–5 % greater CSA and Z compared to 10 min/day MVPA | ||||||||
When CSA and Z adjusted for LM, associations attenuated in males but remain significant. Associations become insignificant in females. | ||||||||
Farr et al. 2013 [360] | 2-year prospective follow-up | Sex: 248 females Baseline age: 9–12 years Race: 90 % white, 6 % Asian, 2 % black or African American, 0.5 % Native American or Alaska Native, 1 % Native Hawaiian or Pacific Islander, 0.5 % other Location: Tucson, Arizona, USA | 248 | Method: self-report questionnaire Variable: past-year PA score | Follow-up tibia and distal femur BSI | PA associated with increases in distal femur BSI | ||
Gruodyte-Raciene et al. 2013 [365] | 4-year prospective follow-up | Sex: 81 males, 84 females Baseline age: 4–10 years Race: 96 % white, 2 % Asian, 2 % other Locations: Saskatoon, Saskatchewan, Canada | 165 92 gymnasts, 73 nongymnasts | Method: parental-report questionnaire Variable: PA score 1–2 h/week gymnastics exposure | Yearly trajectories of PF CSA and Z (HSA) | When compared to nongymnasts, gymnasts 6 % greater NN CSA, 7 % greater NN Z, 5 % greater IT CSA, 6 % greater IT Z, and 3 % S CSA | ||
Janz et al. 2014 [248] | 12-year prospective follow-up | Sex: 160 males, 189 females Baseline age: 5 years Race: primarily white Location: Iowa, USA | 349 | Method: ActiGraph accelerometer Variable: MVPA min/day (≥2296 ct/min) | Follow-up (age 17) FN Z and CSA Tibia BSI Tibia polar moment of inertia | Participants in high trajectory for MVPA had greater geometric outcome measures (Z: females 21.0 %, males 9.4 %; CSA: females 11.8 %, males 10.0 %; BSI: females 19.0 %, males 12.8 %; polar moment of inertia: females 38 %, males 8.4 %) at age 17 compared to other trajectories. | ||
Jackowski et al. 2014 [251] | ~15-year prospective follow-up | Sex: 55 males, 49 females Baseline age: 8–15 years Race: primarily white Location: Saskatoon, Saskatchewan, Canada | 104 | Method: self-report questionnaires Variable: average activity score | Follow-up (age 23–30) PF CSA and Z (HSA) | Around time of PHV, active adolescents had 8–12 % greater CSA and 9–12 % greater Z than inactive peers at PF. When adult CSA and Z were adjusted for height, weight, adolescent bone geometry, and sex, those active during adolescence maintained 5–7 % benefit in CSA and 6–8 % benefit in Z in adulthood compared to inactive. In young adulthood, males and females who were physically active as adolescents had greater bone geometric measures. | ||
Duckham et al. 2014 [252] | ~18-year prospective follow-up | Sex: 49 males, 73 females Baseline age: 8–15 years Race: primarily white Location: Saskatoon, Saskatchewan, Canada | 122 | Method: self-report questionnaire Variable: general PA score | Follow-up (age 24–34) tibia and radius BA, BSI, SSIp, CoC, CoA, CoD, ToA, ToD, TrC, TrD, and BSIc (pQCT) | In young adulthood, males who were physically active as adolescents had 13 % greater SSIp and 10 % greater ToA at tibia. Females had 10 % larger CoA, 12 % larger CoC, and 3 % larger TrC at tibia. | ||
Cardadeiro et al. 2014 [362] | 1-year prospective follow-up | Sex: 81 males, 96 females Baseline age: 10–12 years Race: primarily white Location: Lisbon area, Portugal | 177 | Method: bone-specific administered questionnaire ActiGraph accelerometer Variables: PA score Sedentary min/day (≤100 ct/min) Light min/day (101–2295 ct/min) Moderate min/day (2296–4011 ct/min) Vigorous min/day (>4012 ct/min) | BMD distribution via three aBMD ratios: FN/PF, IM/SL, and TR/PF Geometric measures of the pelvis—IAD and PF ALA | Questionnaire significant in FN/PF ratio model in males |
-
Grade: Level of evidence B was assigned for the benefit of physical activity and exercise on bone structure.
Discussion
Grade A evidence
Macronutrients
Fat
Protein
Micronutrients
Calcium
Vitamin D
Micronutrients other than calcium and vitamin D
Food patterns
Infant nutrition
Adolescent special issues
Detriment of DMPA injections and oral contraceptives
Detriment of alcohol
Detriment of smoking
Physical activity and exercise
Research gaps
Topic area | What we need to know |
---|---|
Life stages of growth for interventions | Are interventions more effective during different stages of growth (e.g., rapid or slow)? Can deficiencies in one stage be overcome subsequently? |
Is there an influence of fetal programming? | |
What are the most effective diet and physical activity interventions at each stage? | |
What is the influence of diet and physical activity patterns, in the short-term and over long periods? | |
What are the determinants of bone acquisition and the impact of interventions in the understudied period of late adolescence to early adulthood? | |
Does response to intervention vary by factors such as sex and population ancestry? | |
Are there other understudied or unstudied lifestyle or environmental factors affect peak bone mass development (i.e., sleep, stress, etc.)? | |
Gene–environment interactions | Are there interactions that affect peak bone mass development? |
Biomarkers of exposure and effect | How do we generate better markers of nutritional status, physical activity and bone loading, and other environmental exposures? |
Among adolescents, exposures to consider include lifestyle habits such as smoking (both nicotine and marijuana) and alcohol, among others. | |
How do we generate better markers of stage of maturity, peak bone strength development, and associated intermediate mechanisms? | |
Attention to the multiple factors involved in bone and mineral metabolism is needed in interpreting responses to dietary interventions, including a focus on interactions between vitamin D, phosphorus, calcium, and fibroblast growth factor 23. | |
Organ and tissue interactions | What are bone interactions with other tissues (i.e., brain, fat, muscle, gut, etc.) on development of peak bone mass? |
Statistical guidelines
Element |
---|
Usual intake of nutrient or dietary component, nutritional status |
Duration of intervention (randomized trials) |
Age |
Sex |
Race |
Maturational stage |
Body size |
Physical activity |
Health status and medication use |
Baseline bone values (prospective studies) |
Implementation
Diet
Food source | Bone-related function | Recommended servingsa
| Percentage of population with usual intakes below recommendations | ||||
---|---|---|---|---|---|---|---|
Children | Males | Females | Children | Males | Females | ||
Dairy (cups)b
| Intakes correlated with linear growth, bone mass accrual, reduced fracture | 2–3 years: 2 | 9–13 years: 3 | 9–13 years: 3 | 2–3 years: 41 | 9–13 years: 8 | 9–13 years: 84 |
4–8 years: 2.5 | 14–18 years: 3 | 14–18 years: 3 | 4–8 years: 42 | 14–18 years: 68 | 14–18 years: 92 | ||
19–30 years: 3 | 19–30 years: 3 | 19–30 years: 80 | 19–30 years: 94 | ||||
Fruits (cups)c
| Provide micronutrients for optimal bone growth, preserve bone and calcium economy through acid–base balance | 2–3 years: 1 | 9–13 years: 1.5 | 9–13 years: 1.5 | 2–3 years: 32 | 9–13 years: 78 | 9–13 years: 81 |
4–8 years: 1–1.5 | 14–18 years: 2 | 14–18 years: 1.5 | 4–8 years: 63 | 14–18 years: 87 | 14–18 years: 85 | ||
19–30 years: 2 | 19–30 years: 2 | 19–30 years: 89 | 19–30 years: 93 | ||||
Vegetables (cups) | Provide micronutrients for optimal bone growth, preserve bone and calcium economy through acid–base balance | 2–3 years: 1 | 9–13 years: 2.5 | 9–13 years: 2 | 2–3 years: 80 | 9–13 years: 96 | 9–13 years: 95 |
4–8 years: 1.5 | 14–18 years: 3 | 14–18 years: 2.5 | 4–8 years: 92 | 14–18 years: 97 | 14–18 years: 99 | ||
19–30 years: 3 | 19–30 years: 2.5 | 19–30 years: 93 | 19–30 years: 94 |
Nutrients | Dietary sources | Bone-related function | RDA/AI | EARa,b
| Percentage of population with usual intakes < EARc,d (%) | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Children | Males | Females | Children | Males | Females | ≥2 years | 2–18 years | ≥19 years | |||
Macronutrients | |||||||||||
Protein (g/day) | Animal products, plants, legumes | Organic component of bone that also promotes bone mineral accrual | 1–3 years: 13 | 9–13 years: 34 | 9–13 years: 34 | 1–3 years: 0.87 | 9–13 years: 0.76 | 9–13 years: 0.76 | <3 | <3 | <3 |
4–8 years: 19 | 14–18 years: 52 | 14–18 years: 46 | 4–8 years: 0.76 | 14–18 years: 0.73 | 14–18 years: 0.71 | ||||||
19–30 years: 56 | 19–30 years: 46 | 19–30 years: 0.66 | 19–30 years: 0.66 | ||||||||
Micronutrients | |||||||||||
Calcium (mg/day) | Dairy, dark leafy greens | Inorganic component of bone essential for rigidity, strength, and elasticity of bone tissue | 1–3 years: 700 | 9–13 years: 1300 | 9–13 years: 1300 | 1–3 years: 500 | 9–13 years: 1100 | 9–13 years: 1100 | 38 | ~47 | ~36 |
4–8 years: 1000 | 14–18 years: 1300 | 14–18 years: 1300 | 4–8 years: 800 | 14–18 years: 1100 | 14–18 years: 1100 | ||||||
19–30 years: 1000 | 19–30 years: 1000 | 19–30 years: 800 | 19–30 years: 800 | ||||||||
Phosphorus (mg/day) | Dairy, meat, processed foods, colas | Inorganic component of bone that also functions as an acid–base buffer | 1–3 years: 460 | 9–13 years: 1250 | 9–13 years: 1250 | 1–3 years: 380 | 9–13 years: 1055 | 9–13 years: 1055 | 5 | ~16 | ~1 |
4–8 years: 500 | 14–18 years: 1250 | 14–18 years: 1250 | 4–8 years: 405 | 14–18 years: 1055 | 14–18 years: 1055 | ||||||
19–30 years: 700 | 19–30 years: 700 | 19–30 years: 580 | 19–30 years: 580 | ||||||||
Magnesium (mg/day) | Dairy, dark leafy greens, nuts, whole grains | Regulates structural development of bone (i.e., hydroxyapatite) | 1–3 years: 80 | 9–13 years: 240 | 9–13 years: 240 | 1–3 years: 65 | 9–13 years: 200 | 9–13 years: 200 | 45 | ~35 | ~48 |
4–8 years: 130 | 14–18 years: 410 | 14–18 years: 360 | 4–8 years: 110 | 14–18 years: 340 | 14–18 years: 300 | ||||||
19–30 years: 400 | 19–30 years: 310 | 19–30 years: 330 | 19–30 years: 255 | ||||||||
Potassium (g/day) | Dairy, fruit (e.g., oranges), vegetables (e.g., potatoes) | Regulation of acid–base balance affecting bone metabolism | 1–3 years: 3.0 | 9–13 years: 4.5 | 9–13 years: 4.5 | – | – | – | 3 (<AI) | – | – |
4–8 years: 3.8 | 14–18 years: 4.7 | 14–18 years: 4.7 | |||||||||
19–30 years: 4.7 | 19–30 years: 4.7 | ||||||||||
Zinc (mg/day) | Animal products, nuts, seeds | Required for collagen synthesis and bone formation | 1–3 years: 3 | 9–13 years: 8 | 9–13 years: 8 | 1–3 years: 2.5 | 9–13 years: 7.0 | 9–13 years: 7.0 | 8 | ~5 | ~8 |
4–8 years: 5 | 14–18 years: 11 | 14–18 years: 9 | 4–8 years: 4.0 | 14–18 years: 8.5 | 14–18 years: 7.3 | ||||||
19–30 years: 11 | 19–30 years: 8 | 19–30 years: 9.4 | 19–30 years: 6.8 | ||||||||
Iron (mg/day) | Animal products, fruits, vegetables, fortified grain products | Cofactor required for collagen synthesis and vitamin D activation | 1–3 years: 7 | 9–13 years: 8 | 9–13 years: 8 | 1–3 years: 3.0 | 9–13 years: 5.9 | 9–13 years: 5.7 | 5 | ~2 | ~6 |
4–8 years: 10 | 14–18 years: 11 | 14–18 years: 15 | 4–8 years: 4.1 | 14–18 years: 7.7 | 14–18 years: 7.9 | ||||||
19–30 years: 8 | 19–30 years: 18 | 19–30 years: 6.0 | 19–30 years: 8.1 | ||||||||
Manganese (mg/day) | Nuts, legumes, whole grains | Cofactor required for proteoglycan synthesis and bone formation | 1–3 years: 1.2 | 9–13 years: 1.9 | 9–13 years: 1.6 | — | — | — | — | — | — |
4–8 years: 1.5 | 14–18 years: 2.2 | 14–18 years: 1.6 | |||||||||
19–30 years: 2.3 | 19–30 years: 1.8 | ||||||||||
Vitamin K (μg/day) | Green vegetables, plant oils, margarine | Cofactor required for carboxylation of osteocalcin and bone formation | 1–3 years: 30 | 9–13 years: 60 | 9–13 years: 60 | – | – | – | 35 (<AI) | – | – |
4–8 years: 55 | 14–18 years: 75 | 14–18 years: 75 | |||||||||
19–30 years: 120 | 19–30 years: 90 | ||||||||||
Vitamin C (mg/day) | Citrus fruits, dark leafy greens | Cofactor required for cross-linking of collagen fibers | 1–3 years: 15 | 9–13 years: 45 | 9–13 years: 45 | 1–3 years: 13 | 9–13 years: 39 | 9–13 years: 39 | 25 | ~17 | ~28 |
4–8 years: 25 | 14–18 years: 75 | 14–18 years: 65 | 4–8 years: 22 | 14–18 years: 63 | 14–18 years: 56 | ||||||
19–30 years: 90 | 19–30 years: 75 | 19–30 years: 75 | 19–30 years: 60 | ||||||||
Vitamin A (μg/day) | Dairy, darkly colored fruits and leafy vegetables | Implicated in bone formation and resorption | 1–3 years: 300 | 9–13 years: 600 | 9–13 years: 600 | 1–3 years: 210 | 9–13 years: 445 | 9–13 years: 420 | 34 | ~28 | ~38 |
4–8 years: 400 | 14–18 years: 900 | 14–18 years: 700 | 4–8 years: 275 | 14–18 years: 630 | 14–18 years: 485 | ||||||
19–30 years: 900 | 19–30 years: 700 | 19–30 years: 625 | 19–30 years: 500 | ||||||||
Vitamin D (IU/day) | Fortified dairy, fatty fish | Regulates calcium homeostasis and bone metabolism | 1–3 years: 600 | 9–13 years: 600 | 9–13 years: 600 | 1–3 years: 400 | 9–13 years: 400 | 9–13 years: 400 | 70 | ~75 | ~69 |
4–8 years: 600 | 14–18 years: 600 | 14–18 years: 600 | 4–8 years: 400 | 14–18 years: 400 | 14–18 years: 400 | ||||||
19–30 years: 600 | 19–30 years: 600 | 19–30 years: 400 | 19–30 years: 400 |
Physical activity
Taking action
Families
Schools
Healthcare system
Federal, state, and local policy
Conclusions
Terminology | Acronym | Definition |
Areal bone mineral density | aBMD | DXA calculates BMD using area. This is not an accurate measurement of the true bone mineral density, which is mass divided by volume. It is a reasonable estimate of BMC. |
Bone mineral content | BMC | DXA measures the BMC of the spine, hip, wrist, femur, or any other selected part of the skeleton. It does this by focusing an x-ray on a body site and measuring the proportion of light rays that pass through the tissue as opposed to being blocked by minerals in the bone. Using computer software, it then divides that number by the surface area of the bone being measured to create BMD. |
Bone mineral density | BMD | BMD refers to the amount of mineral matter per square centimeter of bone. BMD is used as a predictor of osteoporosis and fracture risk. |
Computed tomography | CT | CT is an imaging procedure that uses special x-ray equipment to create a series of detailed pictures, or scans, of areas inside the body. It is also called computerized tomography and computerized axial tomography (CAT) scanning. |
Cross-sectional moment of inertia | CSMI | CSMI is a measure of the distribution of material around a given axis. It is used to calculate bending stress. |
Dual-energy x-ray absorptiometry | DXA | DXA is a means of measuring BMD. It is the most widely used and most thoroughly studied bone density measurement technology. Two x-ray beams with different energy levels are aimed at the patient’s bones. When soft tissue absorption is subtracted out, the BMD can be determined from the absorption of each beam by bone. |
Hip structural analysis | HSA | HSA measures not only the BMD of the hip bone but also structural geometry of cross-sections traversing the proximal femur at specific locations. The bone mass image is used directly from the DXA scan, where pixel values are expressed in areal mass (g/cm2). The method employs the principle that a line of pixel values across the bone axis corresponds to a cut plane traversing the bone at that location and contains some of the information about the cross-section. |
Percentage of undercarboxylated osteocalcin | %ucOC | %ucOC is a measure of vitamin K status. Osteocalcin is a vitamin K-dependent protein produced by the bone. The ratio of undercarboxylated to carboxylated or total osteocalcin has been regarded as a marker of inadequate vitamin K status. |
Peripheral quantitative computed tomography | pQCT | pQCT is a type of quantitative CT used for making measurements of the BMD in a peripheral part of the body, such as the forearms or legs, as opposed to CT that measures BMD at the hip and spine. pQCT is useful for measuring bone strength. |
Potential renal acid load | PRAL | PRAL is a measure of the acidic or basic effects that a food has on the body. |
Quantitative computed tomography | QCT | QCT measures BMD using a standard CT scanner with a calibration standard to convert Hounsfield units (HU) of the CT image to BMD values. QCT scans are primarily used to evaluate BMD at the lumbar spine and hip. |
Stress–strain index | SSI | The SSI of a bone is a surrogate measure of bone strength determined from a cross-sectional scan by QCT or pQCT. The SSI is used to compare the structural parameters determined by analysis of QCT/pQCT cross-sectional scans to the results of a three-point bending test. |
Volumetric bone mineral density | vBMD | In addition to aBMD using DXA, a projected posteroanterior lateral vertebral scan is added to measure vertebral width, height, and depth to estimate vBMD. This permits direct measurement of bone depth, rather than estimation of projected posteroanterior dimensions. |