CoChat
Sign Up
Cited by 1,378Bone health and osteoporosis researchVitamin D Research StudiesBone Metabolism and Diseases

The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: A systematic review and implementation recommendations

Open access
Weaver, C. M., Gordon, C. M., Janz, K. F., Kalkwarf, H. J., Lappe, J. M., Lewis, R., O’Karma, M., Wallace, T. C. +1 more·2016·Osteoporosis International
DOI 10.1007/s00198-015-3440-3PMC PMC4791473
Open this paper in CoChat — free accountOpen PDF

Abstract

Lifestyle choices influence 20–40 % of adult peak bone mass. Therefore, optimization of lifestyle factors known to influence peak bone mass and strength is an important strategy aimed at reducing risk of osteoporosis or low bone mass later in life. The National Osteoporosis Foundation has issued this scientific statement to provide evidence-based guidance and a national implementation strategy for the purpose of helping individuals achieve maximal peak bone mass early in life. In this scientific statement, we (1) report the results of an evidence-based review of the literature since 2000 on factors that influence achieving the full genetic potential for skeletal mass; (2) recommend lifestyle choices that promote maximal bone health throughout the lifespan; (3) outline a research agenda to address current gaps; and (4) identify implementation strategies. We conducted a systematic review of the role of individual nutrients, food patterns, special issues, contraceptives, and physical activity on bone mass and strength development in youth. An evidence grading system was applied to describe the strength of available evidence on these individual modifiable lifestyle factors that may (or may not) influence the development of peak bone mass (Table 1). A summary of the grades for each of these factors is given below. We describe the underpinning biology of these relationships as well as other factors for which a systematic review approach was not possible. Articles published since 2000, all of which followed the report by Heaney et al. [1] published in that year, were considered for this scientific statement. This current review is a systematic update of the previous review conducted by the National Osteoporosis Foundation [1]. Lifestyle Factor Grade Macronutrients Fat D Protein C Micronutrients Calcium A Vitamin D B Micronutrients other than calcium and vitamin D D Food Patterns Dairy B Fiber C Fruits and vegetables C Detriment of cola and caffeinated beverages C Infant Nutrition Duration of breastfeeding D Breastfeeding versus formula feeding D Enriched formula feeding D Adolescent Special Issues Detriment of oral contraceptives D Detriment of DMPA injections B Detriment of alcohol D Detriment of smoking C Physical Activity and Exercise Effect on bone mass and density A Effect on bone structural outcomes B Considering the evidence-based literature review, we recommend lifestyle choices that promote maximal bone health from childhood through young to late adolescence and outline a research agenda to address current gaps in knowledge. The best evidence (grade A) is available for positive effects of calcium intake and physical activity, especially during the late childhood and peripubertal years—a critical period for bone accretion. Good evidence is also available for a role of vitamin D and dairy consumption and a detriment of DMPA injections. However, more rigorous trial data on many other lifestyle choices are needed and this need is outlined in our research agenda. Implementation strategies for lifestyle modifications to promote development of peak bone mass and strength within one’s genetic potential require a multisectored (i.e., family, schools, healthcare systems) approach.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s00198-015-3440-3

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 354

  1. [1]Heaney RP Abrams S Dawson-Hughes B Looker A Marcus R Matkovic V Weaver C Peak bone mass Osteoporos Int 2000 11 985 1009 11256898
  2. [2]Parfitt AM The two faces of growth: benefits and risks to bone integrity Osteoporos Int 1994 4 382 398 7696836
  3. [3]Bailey DA McKay HA Mirwald RL Crocker PR Faulkner RA A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the University of Saskatchewan Bone Mineral Accrual Study J Bone Miner Res 1999 14 1672 1679 10491214
  4. [4]Baxter-Jones AD Faulkner RA Forwood MR Mirwald RL Bailey DA Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass J Bone Miner Res 2011 26 1729 1739 21520276
  5. [5]Gilsanz V Roe TF Mora S Costin G Goodman WG Changes in vertebral bone density in black girls and white girls during childhood and puberty N Engl J Med 1991 325 1597 1600 1944449
  6. [6]Gilsanz V Skaggs DL Kovanlikaya A Sayre J Loro ML Kaufman F Korenman SG Differential effect of race on the axial and appendicular skeletons of children J Clin Endocrinol Metab 1998 83 1420 1427 9589632
  7. [7]Kirmani S Christen D van Lenthe GH Fischer PR Bouxsein ML McCready LK Melton LJ 3rd Riggs BL Amin S Muller R Khosla S Bone structure at the distal radius during adolescent growth J Bone Miner Res 2009 24 1033 1042 19113916 PMC2683647
  8. [8]Wang Q Wang XF Iuliano-Burns S Ghasem-Zadeh A Zebaze R Seeman E Rapid growth produces transient cortical weakness: a risk factor for metaphyseal fractures during puberty J Bone Miner Res 2010 25 1521 1526 20200962
  9. [9]Riggs BL Melton LJ Robb RA Camp JJ Atkinson EJ McDaniel L Amin S Rouleau PA Khosla S A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men J Bone Miner Res 2008 23 205 214 17937534 PMC2665699
  10. [10]Berger C Goltzman D Langsetmo L Joseph L Jackson S Kreiger N Tenenhouse A Davison KS Josse RG Prior JC Hanley DA Peak bone mass from longitudinal data: implications for the prevalence, pathophysiology, and diagnosis of osteoporosis J Bone Miner Res 2010 25 1948 1957 20499378 PMC5101070
  11. [11]Kalkwarf HJ Laor T Bean JA Fracture risk in children with a forearm injury is associated with volumetric bone density and cortical area (by peripheral QCT) and areal bone density (by DXA) Osteoporos Int 2011 22 607 616 20571770 PMC3298088
  12. [12]World Health Organization Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report Series 843 1994 Geneva World Health Organization 7941614
  13. [13]Holloway KL Brennan SL Kotowicz MA Bucki-Smith G Timney EN Dobbins AG Williams LJ Pasco JA Prior fracture as a risk factor for future fracture in an Australian cohort Osteoporos Int 2015 26 629 635 25231678
  14. [14]Cooper C Dennison EM Leufkens HG Bishop N van Staa TP Epidemiology of childhood fractures in Britain: a study using the general practice research database J Bone Miner Res 2004 19 1976 1981 15537440
  15. [15]Landin LA Fracture patterns in children. Analysis of 8,682 fractures with special reference to incidence, etiology and secular changes in a Swedish urban population 1950–1979 Acta Orthop Scand Suppl 1983 202 1 109 6574687
  16. [16]Mayranpaa MK Makitie O Kallio PE Decreasing incidence and changing pattern of childhood fractures: a population-based study J Bone Miner Res 2010 25 2752 2759 20564246
  17. [17]Yeh FJ Grant AM Williams SM Goulding A Children who experience their first fracture at a young age have high rates of fracture Osteoporos Int 2006 17 267 272 16184318
  18. [18]de Putter CE van Beeck EF Looman CW Toet H Hovius SE Selles RW Trends in wrist fractures in children and adolescents, 1997–2009 J Hand Surg [Am] 2011 36 1810 1815.e1812 22036281
  19. [19]Jones G Boon P Which bone mass measures discriminate adolescents who have fractured from those who have not? Osteoporos Int 2008 19 251 255 17713714
  20. [20]Lyons RA Delahunty AM Kraus D Heaven M McCabe M Allen H Nash P Children’s fractures: a population based study Inj Prev 1999 5 129 132 10385833 PMC1730475
  21. [21]Clark EM Ness AR Tobias JH Vigorous physical activity increases fracture risk in children irrespective of bone mass: a prospective study of the independent risk factors for fractures in healthy children J Bone Miner Res 2008 23 1012 1022 18570539 PMC2742075
  22. [22]Baxter-Jones AD Kontulainen SA Faulkner RA Bailey DA A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood Bone 2008 43 1101 1107 18725335
  23. [23]Detter FT Rosengren BE Dencker M Nilsson JA Karlsson MK A 5-year exercise program in pre- and peripubertal children improves bone mass and bone size without affecting fracture risk Calcif Tissue Int 2013 92 385 393 23338815
  24. [24]Gunter K Baxter-Jones AD Mirwald RL Almstedt H Fuchs RK Durski S Snow C Impact exercise increases BMC during growth: an 8-year longitudinal study J Bone Miner Res 2008 23 986 993 18072874 PMC2679385
  25. [25]Macdonald HM Kontulainen SA Khan KM McKay HA Is a school-based physical activity intervention effective for increasing tibial bone strength in boys and girls? J Bone Miner Res 2007 22 434 446 17181400
  26. [26]Mackelvie KJ McKay HA Khan KM Crocker PR A school-based exercise intervention augments bone mineral accrual in early pubertal girls J Pediatr 2001 139 501 508 11598595
  27. [27]Slemenda CW Miller JZ Hui SL Reister TK Johnston CCJ Role of physical activity in the development of skeletal mass in children J Bone Miner Res 1991 6 1227 1233 1805545
  28. [28]Lofgren B Dencker M Nilsson JA Karlsson MK A 4-year exercise program in children increases bone mass without increasing fracture risk Pediatrics 2012 129 e1468 e1476 22641757
  29. [29]Khosla S Melton LJ 3rd Dekutoski MB Achenbach SJ Oberg AL Riggs BL Incidence of childhood distal forearm fractures over 30 years: a population-based study JAMA 2003 290 1479 1485 13129988
  30. [30]Kelsey JL Browner WS Seeley DG Nevitt MC Cummings SR Risk factors for fractures of the distal forearm and proximal humerus. The Study of Osteoporotic Fractures Research Group Am J Epidemiol 1992 135 477 489 1570814
  31. [31]Clark EM Ness AR Bishop NJ Tobias JH Association between bone mass and fractures in children: a prospective cohort study J Bone Miner Res 2006 21 1489 1495 16939408 PMC2742714
  32. [32]Kalkwarf HJ Gilsanz V Lappe JM Oberfield S Shepherd JA Hangartner TN Huang X Frederick MM Winer KK Zemel BS Tracking of bone mass and density during childhood and adolescence J Clin Endocrinol Metab 2010 95 1690 1698 20194709 PMC2853985
  33. [33]Bowden LS Jones CJ Ryan SW Bone mineralisation in ex-preterm infants aged 8 years Eur J Pediatr 1999 158 658 661 10445346
  34. [34]Dennison EM Syddall HE Sayer AA Gilbody HJ Cooper C Birth weight and weight at 1 year are independent determinants of bone mass in the seventh decade: the Hertfordshire cohort study Pediatr Res 2005 57 582 586 15695596
  35. [35]Farr JN Amin S Melton LJ 3rd Kirmani S McCready LK Atkinson EJ Muller R Khosla S Bone strength and structural deficits in children and adolescents with a distal forearm fracture resulting from mild trauma J Bone Miner Res 2014 29 590 599 23959563 PMC4074503
  36. [36]Thandrayen K Norris SA Pettifor JM Fracture rates in urban South African children of different ethnic origins: the Birth to Twenty cohort Osteoporos Int 2009 20 47 52 18465189 PMC2859163
  37. [37]Wren TA Shepherd JA Kalkwarf HJ Zemel BS Lappe JM Oberfield S Dorey FJ Winer KK Gilsanz V Racial disparity in fracture risk between white and nonwhite children in the United States J Pediatr 2012 161 1035 1040 22974572 PMC3504618
  38. [38]Cauley JA Lui LY Ensrud KE Zmuda JM Stone KL Hochberg MC Cummings SR Bone mineral density and the risk of incident nonspinal fractures in black and white women JAMA 2005 293 2102 2108 15870413
  39. [39]Shin MH Zmuda JM Barrett-Connor E Sheu Y Patrick AL Leung PC Kwok A Kweon SS Nam HS Cauley JA Race/ethnic differences in associations between bone mineral density and fracture history in older men Osteoporos Int 2014 25 837 845 24146094 PMC4058886
  40. [40]Loud KJ Gordon CM Micheli LJ Field AE Correlates of stress fractures among preadolescent and adolescent girls Pediatrics 2005 115 e399 e406 15805341
  41. [41]Hame SL LaFemina JM McAllister DR Schaadt GW Dorey FJ Fractures in the collegiate athlete Am J Sports Med 2004 32 446 451 14977672
  42. [42]Lappe JM Stegman MR Recker RR The impact of lifestyle factors on stress fractures in female army recruits Osteoporos Int 2001 12 35 42 11305081
  43. [43]Mattila VM Niva M Kiuru M Pihlajamaki H Risk factors for bone stress injuries: a follow-up study of 102,515 person-years Med Sci Sports Exerc 2007 39 1061 1066 17596772
  44. [44]Cosman F Ruffing J Zion M Uhorchak J Ralston S Tendy S McGuigan FE Lindsay R Nieves J Determinants of stress fracture risk in United States Military Academy cadets Bone 2013 55 359 366 23624291
  45. [45]Wentz L Liu PY Haymes E Ilich JZ Females have a greater incidence of stress fractures than males in both military and athletic populations: a systemic review Mil Med 2011 176 420 430 21539165
  46. [46]Knapik J Montain SJ McGraw S Grier T Ely M Jones BH Stress fracture risk factors in basic combat training Int J Sports Med 2012 33 940 946 22821178
  47. [47]Friedl KE Evans RK Moran DS Stress fracture and military medical readiness: bridging basic and applied research Med Sci Sports Exerc 2008 40 S609 S622 18849874
  48. [48]Gam A Goldstein L Karmon Y Mintser I Grotto I Guri A Goldberg A Ohana N Onn E Levi Y Bar-Dayan Y Comparison of stress fractures of male and female recruits during basic training in the Israeli anti-aircraft forces Mil Med 2005 170 710 712 16173215
  49. [49]Lappe J Davies K Recker R Heaney R Quantitative ultrasound: use in screening for susceptibility to stress fractures in female army recruits J Bone Miner Res 2005 20 571 578 15765175
  50. [50]Field AE Gordon CM Pierce LM Ramappa A Kocher MS Prospective study of physical activity and risk of developing a stress fracture among preadolescent and adolescent girls Arch Pediatr Adolesc Med 2011 165 723 728 21464375 PMC3132304
  51. [51]Loud KJ Micheli LJ Bristol S Austin SB Gordon CM Family history predicts stress fracture in active female adolescents Pediatrics 2007 120 e364 e372 17636110 PMC3200550
  52. [52]Friedl KE Nuovo JA Patience TH Dettori JR Factors associated with stress fracture in young army women: indications for further research Mil Med 1992 157 334 338 1528465
  53. [53]Budek AZ Mark T Michaelsen KF Molgaard C Tracking of size-adjusted bone mineral content and bone area in boys and girls from 10 to 17 years of age Osteoporos Int 2010 21 179 182 19387763
  54. [54]Cheng S Volgyi E Tylavsky FA Lyytikainen A Tormakangas T Xu L Cheng SM Kroger H Alen M Kujala UM Trait-specific tracking and determinants of body composition: a 7-year follow-up study of pubertal growth in girls BMC Med 2009 7 5 19171028 PMC2639618
  55. [55]Foley S Quinn S Jones G Tracking of bone mass from childhood to adolescence and factors that predict deviation from tracking Bone 2009 44 752 757 19103314
  56. [56]Fujita Y Iki M Ikeda Y Morita A Matsukura T Nishino H Yamagami T Kagamimori S Kagawa Y Yoneshima H Tracking of appendicular bone mineral density for 6 years including the pubertal growth spurt: Japanese population-based osteoporosis kids cohort study J Bone Miner Metab 2011 29 208 216 20711620
  57. [57]Wren TA Kalkwarf HJ Zemel BS Lappe JM Oberfield S Shepherd JA Winer KK Gilsanz V Longitudinal tracking of dual-energy X-ray absorptiometry bone measures over 6 years in children and adolescents: persistence of low bone mass to maturity J Pediatr 2014 164 1280 1285.e1282 24485819 PMC4035430
  58. [58]Lorentzon M Mellstrom D Ohlsson C Age of attainment of peak bone mass is site specific in Swedish men—the GOOD study J Bone Miner Res 2005 20 1223 1227 15940376
  59. [59]Thomas SR Kalkwarf HJ Buckley DD Heubi JE Effective dose of dual-energy X-ray absorptiometry scans in children as a function of age J Clin Densitom 2005 8 415 422 16311426
  60. [60]Crabtree NJ Arabi A Bachrach LK Fewtrell M El-Hajj Fuleihan G Kecskemethy HH Jaworski M Gordon CM Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions J Clin Densitom 2014 17 225 242 24690232
  61. [61]Zemel BS Leonard MB Kelly A Lappe JM Gilsanz V Oberfield S Mahboubi S Shepherd JA Hangartner TN Frederick MM Winer KK Kalkwarf HJ Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children J Clin Endocrinol Metab 2010 95 1265 1273 20103654 PMC2841534
  62. [62]Wren TA Liu X Pitukcheewanont P Gilsanz V Bone acquisition in healthy children and adolescents: comparisons of dual-energy x-ray absorptiometry and computed tomography measures J Clin Endocrinol Metab 2005 90 1925 1928 15634720
  63. [63]Prentice A Parsons TJ Cole TJ Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants Am J Clin Nutr 1994 60 837 842 7985621
  64. [64]Molgaard C Thomsen BL Prentice A Cole TJ Michaelsen KF Whole body bone mineral content in healthy children and adolescents Arch Dis Child 1997 76 9 15 9059153 PMC1717036
  65. [65]Hogler W Briody J Woodhead HJ Chan A Cowell CT Importance of lean mass in the interpretation of total body densitometry in children and adolescents J Pediatr 2003 143 81 88 12915829
  66. [66]Crabtree NJ Kibirige MS Fordham JN Banks LM Muntoni F Chinn D Boivin CM Shaw NJ The relationship between lean body mass and bone mineral content in paediatric health and disease Bone 2004 35 965 972 15454104
  67. [67]Short DF Zemel BS Gilsanz V Kalkwarf HJ Lappe JM Mahboubi S Oberfield SE Shepherd JA Winer KK Hangartner TN Fitting of bone mineral density with consideration of anthropometric parameters Osteoporos Int 2011 22 1047 1057 20495903 PMC2996478
  68. [68]Horlick M Wang J Pierson RNJ Thornton JC Prediction models for evaluation of total-body bone mass with dual-energy X-ray absorptiometry among children and adolescents Pediatrics 2004 114 e33 e45 15342895
  69. [69]Crabtree NJ Hogler W Cooper MS Shaw NJ Diagnostic evaluation of bone densitometric size adjustment techniques in children with and without low trauma fractures Osteoporos Int 2013 24 2015 2024 23361874
  70. [70]Beck TJ Ruff CB Warden KE Scott WWJ Rao GU Predicting femoral neck strength from bone mineral data. A structural approach Invest Radiol 1990 25 6 18 2298552
  71. [71]Beck TJ Stone KL Oreskovic TL Hochberg MC Nevitt MC Genant HK Cummings SR Effects of current and discontinued estrogen replacement therapy on hip structural geometry: the study of osteoporotic fractures J Bone Miner Res 2001 16 2103 2110 11697807
  72. [72]Burnham JM Shults J Petit MA Semeao E Beck TJ Zemel BS Leonard MB Alterations in proximal femur geometry in children treated with glucocorticoids for Crohn disease or nephrotic syndrome: impact of the underlying disease J Bone Miner Res 2007 22 551 559 17243860
  73. [73]Petit MA McKay HA MacKelvie KJ Heinonen A Khan KM Beck TJ A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study J Bone Miner Res 2002 17 363 372 11874228
  74. [74]Adams JE Engelke K Zemel BS Ward KA Quantitative computer tomography in children and adolescents: the 2013 ISCD Pediatric Official Positions J Clin Densitom 2014 17 258 274 24792821
  75. [75]Caspersen CJ Powell KE Christenson GM Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research Public Health Rep 1985 100 126 131 3920711 PMC1424733
  76. [77]Frost HM Schonau E The “muscle-bone unit” in children and adolescents: a 2000 overview J Pediatr Endocrinol Metab 2000 13 571 590 10905381
  77. [78]Frost HM Bone’s mechanostat: a 2003 update Anat Rec A: Discov Mol Cell Evol Biol 2003 275 1081 1101 14613308
  78. [79]Kannus P Haapasalo H Sankelo M Sievanen H Pasanen M Heinonen A Oja P Vuori I Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players Ann Intern Med 1995 123 27 31 7762910
  79. [80]Welten DC Kemper HC Post GB Van Mechelen W Twisk J Lips P Teule GJ Weight-bearing activity during youth is a more important factor for peak bone mass than calcium intake J Bone Miner Res 1994 9 1089 1096 7942156
  80. [81]Specker B Binkley T Randomized trial of physical activity and calcium supplementation on bone mineral content in 3- to 5-year-old children J Bone Miner Res 2003 18 885 892 12733728
  81. [82]Turner CH Forwood MR Rho JY Yoshikawa T Mechanical loading thresholds for lamellar and woven bone formation J Bone Miner Res 1994 9 87 97 8154314
  82. [83]Forwood MR Turner CH Skeletal adaptations to mechanical usage: results from tibial loading studies in rats Bone 1995 17 197S 205S 8579917
  83. [84]Turner CH Robling AG Designing exercise regimens to increase bone strength Exerc Sport Sci Rev 2003 31 45 50 12562170
  84. [85]Baptista F Janz K Preedy VR Physical activity, bone growth, and development in children and adolescents: a public health perspective Handbook of growth and growth monitoring in health and disease 2012 New York Springer 2395 2411
  85. [86]Khan K McKay HA Haapasalo H Bennell KL Forwood MR Kannus P Wark JD Does childhood and adolescence provide a unique opportunity for exercise to strengthen the skeleton? J Sci Med Sport 2000 3 150 164 11104307
  86. [87]Duncan RL Turner CH Mechanotransduction and the functional response of bone to mechanical strain Calcif Tissue Int 1995 57 344 358 8564797
  87. [88]Robling AG Hinant FM Burr DB Turner CH Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts J Bone Miner Res 2002 17 1545 1554 12162508
  88. [89]Ackerman A Thornton JC Wang J Pierson RNJ Horlick M Sex difference in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old Obesity (Silver Spring) 2006 14 819 825 16855191
  89. [90]Arabi A Tamim H Nabulsi M Maalouf J Khalife H Choucair M Vieth R El-Hajj Fuleihan G Sex differences in the effect of body-composition variables on bone mass in healthy children and adolescents Am J Clin Nutr 2004 80 1428 1435 15531697
  90. [91]Ausili E Rigante D Salvaggio E Focarelli B Rendeli C Ansuini V Paolucci V Triarico S Martini L Caradonna P Determinants of bone mineral density, bone mineral content, and body composition in a cohort of healthy children: influence of sex, age, puberty, and physical activity Rheumatol Int 2012 32 2737 2743 21809005
  91. [92]Pietrobelli A Faith MS Wang J Brambilla P Chiumello G Heymsfield SB Association of lean tissue and fat mass with bone mineral content in children and adolescents Obes Res 2002 10 56 60 11786602
  92. [93]Jackowski SA Faulkner RA Farthing JP Kontulainen SA Beck TJ Baxter-Jones AD Peak lean tissue mass accrual precedes changes in bone strength indices at the proximal femur during the pubertal growth spurt Bone 2009 44 1186 1190 19236963
  93. [94]Xu L Nicholson P Wang Q Alen M Cheng S Bone and muscle development during puberty in girls: a seven-year longitudinal study J Bone Miner Res 2009 24 1693 1698 19419294
  94. [95]Ashby RL Adams JE Roberts SA Mughal MZ Ward KA The muscle-bone unit of peripheral and central skeletal sites in children and young adults Osteoporos Int 2011 22 121 132 20333357 PMC3966020
  95. [96]Cardel M Higgins PB Willig AL Keita AD Casazza K Gower BA Fernandez JR African genetic admixture is associated with body composition and fat distribution in a cross-sectional study of children Int J Obes (Lond) 2011 35 60 65 20877287 PMC3804117
  96. [97]Seeman E Hopper JL Bach LA Cooper ME Parkinson E McKay J Jerums G Reduced bone mass in daughters of women with osteoporosis N Engl J Med 1989 320 554 558 2915666
  97. [98]Soroko SB Barrett-Connor E Edelstein SL Kritz-Silverstein D Family history of osteoporosis and bone mineral density at the axial skeleton: the Rancho Bernardo Study J Bone Miner Res 1994 9 761 769 8079652
  98. [99]Ferrari S Rizzoli R Slosman D Bonjour JP Familial resemblance for bone mineral mass is expressed before puberty J Clin Endocrinol Metab 1998 83 358 361 9467541
  99. [100]Duren DL Sherwood RJ Choh AC Czerwinski SA Chumlea WC Lee M Sun SS Demerath EW Siervogel RM Towne B Quantitative genetics of cortical bone mass in healthy 10-year-old children from the Fels Longitudinal Study Bone 2007 40 464 470 17056310 PMC1945206
  100. [101]Estrada K Styrkarsdottir U Evangelou E Hsu YH Duncan EL Ntzani EE Oei L Albagha OM Amin N Kemp JP Koller DL Li G Liu CT Minster RL Moayyeri A Vandenput L Willner D Xiao SM Yerges-Armstrong LM Zheng HF Alonso N Eriksson J Kammerer CM Kaptoge SK Leo PJ Thorleifsson G Wilson SG Wilson JF Aalto V Alen M Aragaki AK Aspelund T Center JR Dailiana Z Duggan DJ Garcia M Garcia-Giralt N Giroux S Hallmans G Hocking LJ Husted LB Jameson KA Khusainova R Kim GS Kooperberg C Koromila T Kruk M Laaksonen M Lacroix AZ Lee SH Leung PC Lewis JR Masi L Mencej-Bedrac S Nguyen TV Nogues X Patel MS Prezelj J Rose LM Scollen S Siggeirsdottir K Smith AV Svensson O Trompet S Trummer O van Schoor NM Woo J Zhu K Balcells S Brandi ML Buckley BM Cheng S Christiansen C Cooper C Dedoussis G Ford I Frost M Goltzman D Gonzalez-Macias J Kahonen M Karlsson M Khusnutdinova E Koh JM Kollia P Langdahl BL Leslie WD Lips P Ljunggren O Lorenc RS Marc J Mellstrom D Obermayer-Pietsch B Olmos JM Pettersson-Kymmer U Reid DM Riancho JA Ridker PM Rousseau F Slagboom PE Tang NL Urreizti R Van Hul W Viikari J Zarrabeitia MT Aulchenko YS Castano-Betancourt M Grundberg E Herrera L Ingvarsson T Johannsdottir H Kwan T Li R Luben R Medina-Gomez C Palsson ST Reppe S Rotter JI Sigurdsson G van Meurs JB Verlaan D Williams FM Wood AR Zhou Y Gautvik KM Pastinen T Raychaudhuri S Cauley JA Chasman DI Clark GR Cummings SR Danoy P Dennison EM Eastell R Eisman JA Gudnason V Hofman A Jackson RD Jones G Jukema JW Khaw KT Lehtimaki T Liu Y Lorentzon M McCloskey E Mitchell BD Nandakumar K Nicholson GC Oostra BA Peacock M Pols HA Prince RL Raitakari O Reid IR Robbins J Sambrook PN Sham PC Shuldiner AR Tylavsky FA van Duijn CM Wareham NJ Cupples LA Econs MJ Evans DM Harris TB Kung AW Psaty BM Reeve J Spector TD Streeten EA Zillikens MC Thorsteinsdottir U Ohlsson C Karasik D Richards JB Brown MA Stefansson K Uitterlinden AG Ralston SH Ioannidis JP Kiel DP Rivadeneira F Genome-wide meta-analysis identifies 56 bone mineral density loci and reveals 14 loci associated with risk of fracture Nat Genet 2012 44 491 501 22504420 PMC3338864
  101. [102]Zheng HF Tobias JH Duncan E Evans DM Eriksson J Paternoster L Yerges-Armstrong LM Lehtimaki T Bergstrom U Kahonen M Leo PJ Raitakari O Laaksonen M Nicholson GC Viikari J Ladouceur M Lyytikainen LP Medina-Gomez C Rivadeneira F Prince RL Sievanen H Leslie WD Mellstrom D Eisman JA Moverare-Skrtic S Goltzman D Hanley DA Jones G St Pourcain B Xiao Y Timpson NJ Smith GD Reid IR Ring SM Sambrook PN Karlsson M Dennison EM Kemp JP Danoy P Sayers A Wilson SG Nethander M McCloskey E Vandenput L Eastell R Liu J Spector T Mitchell BD Streeten EA Brommage R Pettersson-Kymmer U Brown MA Ohlsson C Richards JB Lorentzon M WNT16 influences bone mineral density, cortical bone thickness, bone strength, and osteoporotic fracture risk PLoS Genet 2012 8 e1002745 22792071 PMC3390364
  102. [103]Mora S Gilsanz V Establishment of peak bone mass Endocrinol Metab Clin North Am 2003 32 39 63 12699292
  103. [104]Krall EA Dawson-Hughes B Heritable and life-style determinants of bone mineral density J Bone Miner Res 1993 8 1 9 8427042
  104. [105]Chevalley T Rizzoli R Hans D Ferrari S Bonjour JP Interaction between calcium intake and menarcheal age on bone mass gain: an eight-year follow-up study from prepuberty to postmenarche J Clin Endocrinol Metab 2005 90 44 51 15507508
  105. [106]Timpson NJ Tobias JH Richards JB Soranzo N Duncan EL Sims AM Whittaker P Kumanduri V Zhai G Glaser B Eisman J Jones G Nicholson G Prince R Seeman E Spector TD Brown MA Peltonen L Smith GD Deloukas P Evans DM Common variants in the region around Osterix are associated with bone mineral density and growth in childhood Hum Mol Genet 2009 18 1510 1517 19181680 PMC2664147
  106. [107]Gueguen R Jouanny P Guillemin F Kuntz C Pourel J Siest G Segregation analysis and variance components analysis of bone mineral density in healthy families J Bone Miner Res 1995 10 2017 2022 8619384
  107. [108]McCormick DP Ponder SW Fawcett HD Palmer JL Spinal bone mineral density in 335 normal and obese children and adolescents: evidence for ethnic and sex differences J Bone Miner Res 1991 6 507 513 2068958
  108. [109]Bachrach LK Hastie T Wang MC Narasimhan B Marcus R Bone mineral acquisition in healthy Asian, Hispanic, black, and Caucasian youth: a longitudinal study J Clin Endocrinol Metab 1999 84 4702 4712 10599739
  109. [110]Bhudhikanok GS Wang MC Eckert K Matkin C Marcus R Bachrach LK Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size J Bone Miner Res 1996 11 1545 1556 8889856
  110. [111]Armstrong GT Chow EJ Sklar CA Alterations in pubertal timing following therapy for childhood malignancies Endocr Dev 2009 15 25 39 19293602
  111. [112]Weaver CM McCabe LD McCabe GP Novotny R Van Loan M Going S Matkovic V Boushey C Savaiano DA Bone mineral and predictors of bone mass in white, Hispanic, and Asian early pubertal girls Calcif Tissue Int 2007 81 352 363 17989943
  112. [113]Gilsanz V Kovanlikaya A Costin G Roe TF Sayre J Kaufman F Differential effect of gender on the sizes of the bones in the axial and appendicular skeletons J Clin Endocrinol Metab 1997 82 1603 1607 9141557
  113. [114]Gilsanz V Bone density in children: a review of the available techniques and indications Eur J Radiol 1998 26 177 182 9518226
  114. [115]Leonard MB Elmi A Mostoufi-Moab S Shults J Burnham JM Thayu M Kibe L Wetzsteon RJ Zemel BS Effects of sex, race, and puberty on cortical bone and the functional muscle bone unit in children, adolescents, and young adults J Clin Endocrinol Metab 2010 95 1681 1689 20157194 PMC2853999
  115. [116]Ellis KJ Body composition of a young, multiethnic, male population Am J Clin Nutr 1997 66 1323 1331 9394682
  116. [117]Ellis KJ Abrams SA Wong WW Body composition of a young, muiltiethnic female population Am J Clin Nutr 1997 65 724 731 9062521
  117. [118]Kalkwarf HJ Zemel BS Gilsanz V Lappe JM Horlick M Oberfield S Mahboubi S Fan B Frederick MM Winer K Shepherd JA The bone mineral density in childhood study: bone mineral content and density according to age, sex, and race J Clin Endocrinol Metab 2007 92 2087 2099 17311856
  118. [119]Hammami M Koo WW Hockman EM Body composition of neonates from fan beam dual energy X-ray absorptiometry measurement JPEN J Parenter Enteral Nutr 2003 27 423 426 14621124
  119. [120]Koo WW Bush AJ Walters J Carlson SE Postnatal development of bone mineral status during infancy J Am Coll Nutr 1998 17 65 70 9477392
  120. [121]Kurl S Heinonen K Jurvelin JS Lansimies E Lumbar bone mineral content and density measured using a Lunar DPX densitometer in healthy full-term infants during the first year of life Clin Physiol Func Imaging 2002 22 222 225 12076350
  121. [122]Unal A Gur E Arvas A Erginel A AlikasifoAglu M Ilter O Bone density values in healthy Turkish infants Indian Pediatr 2000 37 497 503 10820542
  122. [123]Rupich RC Specker BL Lieuw AFM Ho M Gender and race differences in bone mass during infancy Calcif Tissue Int 1996 58 395 397 8661478
  123. [124]Willing MC Torner JC Burns TL Janz KF Marshall TA Gilmore J Warren JJ Levy SM Percentile distributions of bone measurements in Iowa children: the Iowa Bone Development Study J Clin Densitom 2005 8 39 47 15722586
  124. [125]Kontulainen SA Macdonald HM Khan KM McKay HA Examining bone surfaces across puberty: a 20-month pQCT trial J Bone Miner Res 2005 20 1202 1207 15940373
  125. [126]Macdonald H Kontulainen S Petit M Janssen P McKay H Bone strength and its determinants in pre- and early pubertal boys and girls Bone 2006 39 598 608 16600704
  126. [127]Nishiyama KK Macdonald HM Moore SA Fung T Boyd SK McKay HA Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study J Bone Miner Res 2012 27 273 282 22028110
  127. [128]Gilsanz V Chalfant J Kalkwarf H Zemel B Lappe J Oberfield S Shepherd J Wren T Winer K Age at onset of puberty predicts bone mass in young adulthood J Pediatr 2011 158 100 105 20797727 PMC4767165
  128. [129]Chevalley T Bonjour JP Ferrari S Rizzoli R The influence of pubertal timing on bone mass acquisition: a predetermined trajectory detectable five years before menarche J Clin Endocrinol Metab 2009 94 3424 3431 19531591
  129. [130]Jackowski SA Erlandson MC Mirwald RL Faulkner RA Bailey DA Kontulainen SA Cooper DM Baxter-Jones AD Effect of maturational timing on bone mineral content accrual from childhood to adulthood: evidence from 15 years of longitudinal data Bone 2011 48 1178 1185 21338727
  130. [131]Darelid A Ohlsson C Nilsson M Kindblom JM Mellstrom D Lorentzon M Catch up in bone acquisition in young adult men with late normal puberty J Bone Miner Res 2012 27 2198 2207 22653693
  131. [132]Nikander R Sievanen H Heinonen A Daly RM Uusi-Rasi K Kannus P Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life BMC Med 2010 8 47 20663158 PMC2918523
  132. [133]Ishikawa S Kim Y Kang M Morgan DW Effects of weight-bearing exercise on bone health in girls: a meta-analysis Sports Med 2013 43 875 892 23754172
  133. [134]Burt LA Greene DA Ducher G Naughton GA Skeletal adaptations associated with pre-pubertal gymnastics participation as determined by DXA and pQCT: a systematic review and meta-analysis J Sci Med Sport 2013 16 231 239 22951266
  134. [135]Behringer M Gruetzner S McCourt M Mester J Effects of weight-bearing activities on bone mineral content and density in children and adolescents: a meta-analysis J Bone Miner Res 2014 29 467 478 23857721
  135. [136]Nogueira RC Weeks BK Beck BR Exercise to improve pediatric bone and fat: a systematic review and meta-analysis Med Sci Sports Exerc 2014 46 610 621 23899893
  136. [137]Tan VP Macdonald HM Kim S Nettlefold L Gabel L Ashe MC McKay HA Influence of physical activity on bone strength in children and adolescents: a systematic review and narrative synthesis J Bone Miner Res 2014 29 2161 2181 24737388
  137. [138]Cho SS Qi L Fahey GCJ Klurfeld DM Consumption of cereal fiber, mixtures of whole grains and bran, and whole grains and risk reduction in type 2 diabetes, obesity, and cardiovascular disease Am J Clin Nutr 2013 98 594 619 23803885
  138. [139]American Diabetes Association Introduction: the American Diabetes Association’s (ADA) evidence-based practice guidelines, standards, and related recommendations and documents for diabetes care Diabetes Care 2012 35 S1 S2 22187466 PMC3632170
  139. [140]Woolf SH Weighing the evidence to formulate dietary guidelines J Am Coll Nutr 2006 25 277S 284S 16772640
  140. [141]Hogstrom M Nordstrom P Nordstrom A n-3 Fatty acids are positively associated with peak bone mineral density and bone accrual in healthy men: the NO2 Study Am J Clin Nutr 2007 85 803 807 17344503
  141. [142]Eriksson S Mellstrom D Strandvik B Fatty acid pattern in serum is associated with bone mineralisation in healthy 8-year-old children Br J Nutr 2009 102 407 412 19175947
  142. [143]Ballard TL Specker BL Binkley TL Vukovich MD Effect of protein supplementation during a 6-month strength and conditioning program on areal and volumetric bone parameters Bone 2006 38 898 904 16364710
  143. [144]Alexy U Remer T Manz F Neu CM Schoenau E Long-term protein intake and dietary potential renal acid load are associated with bone modeling and remodeling at the proximal radius in healthy children Am J Clin Nutr 2005 82 1107 1114 16280446
  144. [145]Remer T Manz F Alexy U Schoenau E Wudy SA Shi L Long-term high urinary potential renal acid load and low nitrogen excretion predict reduced diaphyseal bone mass and bone size in children J Clin Endocrinol Metab 2011 96 2861 2868 21715531
  145. [146]Bounds W Skinner J Carruth BR Ziegler P The relationship of dietary and lifestyle factors to bone mineral indexes in children J Am Diet Assoc 2005 105 735 741 15883550
  146. [147]Vatanparast H Bailey DA Baxter-Jones AD Whiting SJ The effects of dietary protein on bone mineral mass in young adults may be modulated by adolescent calcium intake J Nutr 2007 137 2674 2679 18029482
  147. [148]Zhang Q Ma G Greenfield H Zhu K Du X Foo LH Hu X Fraser DR The association between dietary protein intake and bone mass accretion in pubertal girls with low calcium intakes Br J Nutr 2010 103 714 723 19814838
  148. [149]Hoppe C Molgaard C Michaelsen KF Bone size and bone mass in 10-year-old Danish children: effect of current diet Osteoporos Int 2000 11 1024 1030 11256893
  149. [150]Iuliano-Burns S Stone J Hopper JL Seeman E Diet and exercise during growth have site-specific skeletal effects: a co-twin control study Osteoporos Int 2005 16 1225 1232 15782284
  150. [151]Chevalley T Bonjour JP Ferrari S Rizzoli R High-protein intake enhances the positive impact of physical activity on BMC in prepubertal boys J Bone Miner Res 2008 23 131 142 17892378
  151. [152]Esterle L Sabatier JP Guillon-Metz F Walrant-Debray O Guaydier-Souquieres G Jehan F Garabedian M Milk, rather than other foods, is associated with vertebral bone mass and circulating IGF-1 in female adolescents Osteoporos Int 2009 20 567 575 18704544
  152. [153]Ekbote VH Khadilkar AV Chiplonkar SA Khadilkar VV Determinants of bone mineral content and bone area in Indian preschool children J Bone Miner Metab 2011 29 334 341 20941516
  153. [154]Libuda L Wudy SA Schoenau E Remer T Comparison of the effects of dietary protein, androstenediol and forearm muscle area on radial bone variables in healthy prepubertal children Br J Nutr 2011 105 428 435 20854701
  154. [155]Iuliano-Burns S Saxon L Naughton G Gibbons K Bass SL Regional specificity of exercise and calcium during skeletal growth in girls: a randomized controlled trial J Bone Miner Res 2003 18 156 162 12510818
  155. [156]Stear SJ Prentice A Jones SC Cole TJ Effect of a calcium and exercise intervention on the bone mineral status of 16–18-y-old adolescent girls Am J Clin Nutr 2003 77 985 992 12663301
  156. [157]Bass SL Naughton G Saxon L Iuliano-Burns S Daly R Briganti EM Hume C Nowson C Exercise and calcium combined results in a greater osteogenic effect than either factor alone: a blinded randomized placebo-controlled trial in boys J Bone Miner Res 2007 22 458 464 17181396
  157. [158]Courteix D Jaffre C Lespessailles E Benhamou L Cumulative effects of calcium supplementation and physical activity on bone accretion in premenarchal children: a double-blind randomised placebo-controlled trial Int J Sports Med 2005 26 332 338 15895314
  158. [159]Cheng S Lyytikainen A Kroger H Lamberg-Allardt C Alen M Koistinen A Wang QJ Suuriniemi M Suominen H Mahonen A Nicholson PH Ivaska KK Korpela R Ohlsson C Vaananen KH Tylavsky F Effects of calcium, dairy product, and vitamin D supplementation on bone mass accrual and body composition in 10–12-y-old girls: a 2-y randomized trial Am J Clin Nutr 2005 82 1115 1126 16280447
  159. [160]Dibba B Prentice A Ceesay M Stirling DM Cole TJ Poskitt EM Effect of calcium supplementation on bone mineral accretion in Gambian children accustomed to a low-calcium diet Am J Clin Nutr 2000 71 544 549 10648270
  160. [161]Cameron MA Paton LM Nowson CA Margerison C Frame M Wark JD The effect of calcium supplementation on bone density in premenarcheal females: a co-twin approach J Clin Endocrinol Metab 2004 89 4916 4922 15472185
  161. [162]Prentice A Ginty F Stear SJ Jones SC Laskey MA Cole TJ Calcium supplementation increases stature and bone mineral mass of 16- to 18-year-old boys J Clin Endocrinol Metab 2005 90 3153 3161 15755856
  162. [163]Moyer-Mileur LJ Xie B Ball SD Pratt T Bone mass and density response to a 12-month trial of calcium and vitamin D supplement in preadolescent girls J Musculoskelet Neuronal Interact 2003 3 63 70 15758367
  163. [164]Greene DA Naughton GA Calcium and vitamin-D supplementation on bone structural properties in peripubertal female identical twins: a randomised controlled trial Osteoporos Int 2011 22 489 498 20544178
  164. [165]Lambert HL Eastell R Karnik K Russell JM Barker ME Calcium supplementation and bone mineral accretion in adolescent girls: an 18-mo randomized controlled trial with 2-y follow-up Am J Clin Nutr 2008 87 455 462 18258639
  165. [166]Gibbons MJ Gilchrist NL Frampton C Maguire P Reilly PH March RL Wall CR The effects of a high calcium dairy food on bone health in pre-pubertal children in New Zealand Asia Pac J Clin Nutr 2004 13 341 347 15563438
  166. [167]Ho SC Guldan GS Woo J Yu R Tse MM Sham A Cheng J A prospective study of the effects of 1-year calcium-fortified soy milk supplementation on dietary calcium intake and bone health in Chinese adolescent girls aged 14 to 16 Osteoporos Int 2005 16 1907 1916 16133646
  167. [168]Chevalley T Bonjour JP Ferrari S Hans D Rizzoli R Skeletal site selectivity in the effects of calcium supplementation on areal bone mineral density gain: a randomized, double-blind, placebo-controlled trial in prepubertal boys J Clin Endocrinol Metab 2005 90 3342 3349 15755866
  168. [169]Merrilees MJ Smart EJ Gilchrist NL Frampton C Turner JG Hooke E March RL Maguire P Effects of dairy food supplements on bone mineral density in teenage girls Eur J Nutr 2000 39 256 262 11395985
  169. [170]Du X Zhu K Trube A Zhang Q Ma G Hu X Fraser DR Greenfield H School-milk intervention trial enhances growth and bone mineral accretion in Chinese girls aged 10–12 years in Beijing Br J Nutr 2004 92 159 168 15230999
  170. [171]Carter LM Whiting SJ Drinkwater DT Zello GA Faulkner RA Bailey DA Self-reported calcium intake and bone mineral content in children and adolescents J Am Coll Nutr 2001 20 502 509 11601565
  171. [172]Lappe JM Watson P Gilsanz V Hangartner T Kalkwarf HJ Oberfield S Shepherd J Winer KK Zemel B The longitudinal effects of physical activity and dietary calcium on bone mass accrual across stages of pubertal development J Bone Miner Res 2015 30 156 164 25130421 PMC4280289
  172. [173]Molgaard C Larnkjaer A Cashman KD Lamberg-Allardt C Jakobsen J Michaelsen KF Does vitamin D supplementation of healthy Danish Caucasian girls affect bone turnover and bone mineralization? Bone 2010 46 432 439 19735754
  173. [174]Lloyd T Chinchilli VM Johnson-Rollings N Kieselhorst K Eggli DF Marcus R Adult female hip bone density reflects teenage sports-exercise patterns but not teenage calcium intake Pediatrics 2000 106 40 44 10878147
  174. [175]El-Hajj Fuleihan G Nabulsi M Tamim H Maalouf J Salamoun M Khalife H Choucair M Arabi A Vieth R Effect of vitamin D replacement on musculoskeletal parameters in school children: a randomized controlled trial J Clin Endocrinol Metab 2006 91 405 412 16278262
  175. [176]Al-Shaar L Nabulsi M Maalouf J El-Rassi R Vieth R Beck TJ El-Hajj Fuleihan G Effect of vitamin D replacement on hip structural geometry in adolescents: a randomized controlled trial Bone 2013 56 296 303 23810841
  176. [177]Viljakainen HT Natri AM Karkkainen M Huttunen MM Palssa A Jakobsen J Cashman KD Molgaard C Lamberg-Allardt C A positive dose–response effect of vitamin D supplementation on site-specific bone mineral augmentation in adolescent girls: a double-blinded randomized placebo-controlled 1-year intervention J Bone Miner Res 2006 21 836 844 16753014
  177. [178]Khadilkar AV Sayyad MG Sanwalka NJ Bhandari DR Naik S Khadilkar VV Mughal MZ Vitamin D supplementation and bone mass accrual in underprivileged adolescent Indian girls Asia Pac J Clin Nutr 2010 19 465 472 21147706
  178. [179]Ward KA Das G Roberts SA Berry JL Adams JE Rawer R Mughal MZ A randomized, controlled trial of vitamin D supplementation upon musculoskeletal health in postmenarchal females J Clin Endocrinol Metab 2010 95 4643 4651 20631020
  179. [180]Andersen R Molgaard C Skovgaard LT Brot C Cashman KD Jakobsen J Lamberg-Allardt C Ovesen L Effect of vitamin D supplementation on bone and vitamin D status among Pakistani immigrants in Denmark: a randomised double-blinded placebo-controlled intervention study Br J Nutr 2008 100 197 207 18208636
  180. [181]Breen ME Laing EM Hall DB Hausman DB Taylor RG Isales CM Ding KH Pollock NK Hamrick MW Baile CA Lewis RD 25-hydroxyvitamin D, insulin-like growth factor-I, and bone mineral accrual during growth J Clin Endocrinol Metab 2011 96 E89 E98 20962027 PMC3038478
  181. [182]Cheng S Tylavsky F Kröger H Kärkkäinen M Lyytikäinen A Koistinen A Mahonen A Alen M Halleen J Väänänen K Lamberg-Allardt C Association of low 25-hydroxyvitamin D concentrations with elevated parathyroid hormone concentrations and low cortical bone density in early pubertal and prepubertal Finnish girls Am J Clin Nutr 2003 78 485 492 12936933
  182. [183]Foo LH Zhang Q Zhu K Ma G Hu X Greenfield H Fraser DR Low vitamin D status has an adverse influence on bone mass, bone turnover, and muscle strength in Chinese adolescent girls J Nutr 2009 139 1002 1007 19321588
  183. [184]Lee YA Kim JY Kang MJ Chung SJ Shin CH Yang SW Adequate vitamin D status and adiposity contribute to bone health in peripubertal nonobese children J Bone Miner Metab 2013 31 337 345 23371560
  184. [185]Carpenter TO DeLucia MC Zhang JH Bejnerowicz G Tartamella L Dziura J Petersen KF Befroy D Cohen D A randomized controlled study of effects of dietary magnesium oxide supplementation on bone mineral content in healthy girls J Clin Endocrinol Metab 2006 91 4866 4872 17018656 PMC2995550
  185. [186]Grobler SR Louw AJ Chikte UM Rossouw RJ van W Kotze TJ The relationships between two different drinking water fluoride levels, dental fluorosis and bone mineral density of children Open Dent J 2009 3 48 54 19444344 PMC2681167
  186. [187]Levy SM Eichenberger-Gilmore J Warren JJ Letuchy E Broffitt B Marshall TA Burns T Willing M Janz K Torner JC Associations of fluoride intake with children’s bone measures at age 11 Community Dent Oral Epidemiol 2009 37 416 426 19740248 PMC2765810
  187. [188]Levy SM Warren JJ Phipps K Letuchy E Broffitt B Eichenberger-Gilmore J Burns TL Kavand G Janz KF Torner JC Pauley CA Effects of life-long fluoride intake on bone measures of adolescents: a prospective cohort study J Dent Res 2014 93 353 359 24470542 PMC3957342
  188. [189]Prynne CJ Mishra GD O’Connell MA Muniz G Laskey MA Yan L Prentice A Ginty F Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts Am J Clin Nutr 2006 83 1420 1428 16789345
  189. [190]Laudermilk M Manore M Thomson C Houtkooper L Farr J Going S Vitamin C and zinc intakes are related to bone macroarchitectural structure and strength in prepubescent girls Calcif Tissue Int 2012 91 430 439 23076447 PMC3496253
  190. [191]O’Connor E Molgaard C Michaelsen KF Jakobsen J Lamberg-Allardt CJ Cashman KD Serum percentage undercarboxylated osteocalcin, a sensitive measure of vitamin K status, and its relationship to bone health indices in Danish girls Br J Nutr 2007 97 661 666 17349078
  191. [192]Kalkwarf HJ Khoury JC Bean J Elliot JG Vitamin K, bone turnover, and bone mass in girls Am J Clin Nutr 2004 80 1075 1080 15447922
  192. [193]Abrams SA Griffin IJ Hawthorne KM Liang L Gunn SK Darlington G Ellis KJ A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents Am J Clin Nutr 2005 82 471 476 16087995
  193. [194]McGartland C Robson PJ Murray L Cran G Savage MJ Watkins D Rooney M Boreham C Carbonated soft drink consumption and bone mineral density in adolescence: the Northern Ireland Young Hearts project J Bone Miner Res 2003 18 1563 1569 12968664
  194. [195]McGartland CP Robson PJ Murray LJ Cran GW Savage MJ Watkins DC Rooney MM Boreham CA Fruit and vegetable consumption and bone mineral density: the Northern Ireland Young Hearts Project Am J Clin Nutr 2004 80 1019 1023 15447914
  195. [196]Tylavsky FA Holliday K Danish R Womack C Norwood J Carbone L Fruit and vegetable intakes are an independent predictor of bone size in early pubertal children Am J Clin Nutr 2004 79 311 317 14749239
  196. [197]Whiting SJ Vatanparast H Baxter-Jones A Faulkner RA Mirwald R Bailey DA Factors that affect bone mineral accrual in the adolescent growth spurt J Nutr 2004 134 696S 700S 14988470
  197. [198]Vatanparast H Baxter-Jones A Faulkner RA Bailey DA Whiting SJ Positive effects of vegetable and fruit consumption and calcium intake on bone mineral accrual in boys during growth from childhood to adolescence: the University of Saskatchewan Pediatric Bone Mineral Accrual Study Am J Clin Nutr 2005 82 700 706 16155286
  198. [199]Ma D Jones G Soft drink and milk consumption, physical activity, bone mass, and upper limb fractures in children: a population-based case–control study Calcif Tissue Int 2004 75 286 291 15549642
  199. [200]Wyshak G Teenaged girls, carbonated beverage consumption, and bone fractures Arch Pediatr Adolesc Med 2000 154 610 613 10850510
  200. [201]Manias K McCabe D Bishop N Fractures and recurrent fractures in children; varying effects of environmental factors as well as bone size and mass Bone 2006 39 652 657 16765659

200 of 354 shown

Cited by

Sorted by citations

Authors
Weaver, C. M., Gordon, C. M., Janz, K. F., Kalkwarf, H. J., Lappe, J. M., Lewis, R., O’Karma, M., Wallace, T. C., & Zemel, B. S.
Affiliations
  • Purdue University West Lafayette (US)
  • Cincinnati Children's Hospital Medical Center (US)
  • University of Iowa (US)
  • Creighton University (US)
  • University of Georgia (US)
  • Children's Hospital of Philadelphia (US)
  • George Mason University (US)
Corresponding author
Wallace, T. C.
ORCID
Venue
Osteoporosis International
Publisher
Springer Science and Business Media LLC
Published
2016-02-08
Volume
27
Issue
4
Pages
1281-1386
ISSN
  • 0937-941X (ISSN-L)
  • 1433-2965
DOI
10.1007/s00198-015-3440-3
PMC
PMC4791473
OpenAlex
W2257516528
Cited by
1,378
References
5
Citations by year
2026: 124 · 2025: 133 · 2024: 145 · 2023: 145 · 2022: 156 · 2021: 179 · 2020: 146 · 2019: 116 · 2018: 124 · 2017: 81 · 2016: 26 · 2015: 2
FWCI
18.42
Type
journal article
Language
en
Update notices
erratum (2016-03-02)
Open access
Licence
Locations
  • Osteoporosis International (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Creighton Digital Repository (CDR) (submittedVersion)
Funders
National Center for Complementary and Integrative Health (R01AT008754)
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Vitamin D Research Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Keywords
peak bone mass, bone health, lifestyle factors, calcium intake, vitamin D, physical activity, bone accretion, adolescence, breastfeeding, infant nutrition, dairy consumption, oral contraceptives, alcohol, smoking, bone strength, osteoporosis prevention, research agenda
MeSH terms
Aging, Body Composition, Bone Development, Humans, Life Style, Nutritional Physiological Phenomena, Osteoporosis, Tomography, X-Ray Computed, Exercise, Absorptiometry, Photon, Bone Density, Weight-Bearing, Evidence-Based Medicine, Osteoporotic Fractures

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review