Human biology at the interface of paediatrics: Measuring bone mineral accretion during childhood

Annals of Human Biology

Volumn 39, Issue 5, 2012, Pages 402-411

  Zemel, Babette S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bone mineral content; Bone mineral density; Children; DXA; Growth charts

Indexed keywords

BIOLOGICAL DEVELOPMENT; BONE; CHILD HEALTH; GROWTH CURVE; LIFESTYLE; MINERAL; SKELETON; STANDARD (REFERENCE); TECHNOLOGICAL DEVELOPMENT;

BONE DENSITY; BONE DEVELOPMENT; BONE MINERALIZATION; CHILD; FRACTURE; GENETICS; GROWTH; HUMAN; METABOLIC BONE DISEASE; PHOTON ABSORPTIOMETRY; PHYSIOLOGY; PUBERTY; REFERENCE VALUE; REVIEW; RISK FACTOR;

ABSORPTIOMETRY, PHOTON; BONE DENSITY; BONE DEVELOPMENT; BONE DISEASES, METABOLIC; CALCIFICATION, PHYSIOLOGIC; CHILD; FRACTURES, BONE; GROWTH; HUMANS; PUBERTY; REFERENCE VALUES; RISK FACTORS;

EID: 84867509278     PISSN: 03014460     EISSN: 14645033     Source Type: Journal    
DOI: 10.3109/03014460.2012.704071     Document Type: Review

References (129)

1. Alexy U, Remer T, Manz F, Neu CM, Schoenau E. 2005. 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 82:1107-1114.
2. Bachrach LK. 2001. Acquisition of optimal bone mass in childhood and adolescence. Trends Endocrinol Metab 12:22-28.
3. Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus R. 1999. Bone mineral acquisition in healthy Asian, Hispanic, black, and Caucasian youth: a longitudinal study. J Clin Endocrinol Metab 84: 4702-4712.
4. Bailey DA, Martin AD, McKay HA, Whiting S, Mirwald R. 2000. Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 15:2245-2250.
5. Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA. 1999. 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 14: 1672-1679.
6. Barden EM, Kawchak DA, Ohene-Frempong K, Stallings VA, Zemel BS. 2002. Body composition in children with sickle cell disease. Am J Clin Nutr 76:218-225.
7. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E. 1999. The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest 104:795-804.
8. Bass SL, Saxon L, Daly RM, Turner CH, Robling AG, Seeman E, Stuckey S. 2002. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17:2274-2280.
9. Baxter-Jones AD, Burrows M, Bachrach LK, Lloyd T, Petit M, Macdonald H, Mirwald RL, Bailey D, McKay H. 2010. International longitudinal pediatric reference standards for bone mineral content. Bone 46:208-216.
10. Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. 2011. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 26:1729-1739.
11. Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA. 2008. A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone 43: 1101-1107.
12. Bhudhikanok GS, Wang MC, Eckert K, Matkin C, Marcus R, Bachrach LK. 1996. Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size. J Bone Miner Res 11:1545-1556.
13. Bonjour JP, Carrie AL, Ferrari S, Clavien H, Slosman D, Theintz G, Rizzoli R. 1997. Calcium-enriched foods and bone mass growth in prepubertal girls: a randomized, double-blind, placebo-controlled trial. J Clin Invest 99:1287-1294.
14. Bonjour JP, Chevalley T, Ferrari S, Rizzoli R. 2003. Peak bone mass and its regulation. In: Glorieux F, Pettifor J, Juppner H, editors. Pediatric bone biology and diseases. San Diego, CA: Academic Press. p 235-248.
15. Bonjour JP, Theintz G, Buchs B, Slosman D, Rizzoli R. 1991. Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab 73: 555-563.
16. Boot AM, de Ridder MA, Pols HA, Krenning EP, de Muinck Keizer-Schrama SM. 1997. Bone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity. J Clin Endocrinol Metab 82:57-62.
17. Boot AM, van der Sluis IM, de Muinck Keizer-Schrama SM, van Meurs JB, Krenning EP, Pols HA, Uitterlinden AG. 2004. Estrogen receptor alpha gene polymorphisms and bone mineral density in healthy children and young adults. Calcif Tiss Int 74: 495-500.
18. Bounds W, Skinner J, Carruth BR, Ziegler P. 2005. The relationship of dietary and lifestyle factors to bone mineral indexes in children. J Am Diet Assoc 105:735-741.
19. Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E. 2000. Heterogeneity in the growth of the axial and appendicular skeleton in boys: implications for the pathogenesis of bone fragility in men. J Bone Miner Res 15:1871-1878.
20. Breukhoven PE, Leunissen RW, de Kort SW, Willemsen RH, Hokken-Koelega AC. 2011. Preterm birth does not affect bone mineral density in young adults. Eur J Endocrinol 164:133-138.
21. Buison AM, Kawchak DA, Schall JI, Ohene-Frempong K, Stallings VA, Leonard MB, Zemel BS. 2005. Bone area and bone mineral content deficits in children with sickle cell disease. Pediatrics 116:943-949.
22. Burnham JM, Shults J, Semeao E, Foster B, Zemel BS, Stallings VA, Leonard MB. 2004. Whole body BMC in pediatric Crohn disease: independent effects of altered growth, maturation, and body composition. J Bone Miner Res 19:1961-1968.
23. Carter LM, Whiting SJ. 1997. Effect of calcium supplementation is greater in prepubertal girls with low calcium intake. Nutr Rev 55: 371-373.
24. Cassell C, Benedict M, Specker B. 1996. Bone mineral density in elite 7- to 9-yr-old female gymnasts and swimmers. Med Sci Sports Exerc 28:1243-1246.
25. 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. 2005. 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 82: 1115-1126, quiz 1147-1118.
26. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. 2008. High-protein intake enhances the positive impact of physical activity on BMC in prepubertal boys. J Bone Miner Res 23:131-142.
27. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. 2009. The influence of pubertal timing on bone mass acquisition: a predetermined trajectory detectable five years before menarche. J Clin Endocrinol Metab 94:3424-3431.
28. Clark EM, Tobias JH, Ness AR. 2006. Association between bone density and fractures in children: a systematic review and meta-analysis. Pediatrics 117:e291-e297.
29. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. 2000. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240-1243.
30. Cole TJ, Green PJ. 1992. Smoothing reference centile curves: the LMS method and penalized likelihood. Stat Med 11:1305-1319.
31. Cooper C, Dennison EM, Leufkens HG, Bishop N, van Staa TP. 2004. Epidemiology of childhood fractures in Britain: a study using the general practice research database. J Bone Miner Res 19:1976-1981.
32. Crabtree N, Leonard M, Zemel B. 2007. Dual-energy X-ray absorptiometry. In: Sawyer AJBL, Fung EB, editors. Bone densitometry in growing patients. Totowa, NJ: Humana Press. p 41-58.
33. Dawson-Hughes B. 2003. Interaction of dietary calcium and protein in bone health in humans. J Nutr 133:852S-854S.
34. de Onis M, Garza C, Onyango AW, Rolland-Cachera MF. 2009. [WHO growth standards for infants and young children]. Arch Pediatr 16: 47-53.
35. Dequeker J. 1976. Quantitative radiology: radiogrammetry of cortical bone. Br J Radiol 49:912-920.
36. Dubner SE, Shults J, Baldassano RN, Zemel BS, Thayu M, Burnham JM, Herskovitz RM, Howard KM, Leonard MB. 2009. Longitudinal assessment of bone density and structure in an incident cohort of children with Crohn's disease. Gastroenterology 136:123-130.
37. Ducher G, Tournaire N, Meddahi-Pelle A, Benhamou CL, Courteix D. 2006. Short-term and long-term site-specific effects of tennis playing on trabecular and cortical bone at the distal radius. J Bone Miner Metab 24:484-490.
38. Duren DL, Sherwood RJ, Choh AC, Czerwinski SA, Chumlea WC, Lee M, Sun SS, Demerath EW, Siervogel RM, Towne B. 2007. Quantitative genetics of cortical bone mass in healthy 10-year-old children from the Fels Longitudinal Study. Bone 40:464-470.
39. Ellis KJ, Shypailo RJ, Hergenroeder A, Perez M, Abrams S. 1996. Total body calcium and bone mineral content: comparison of dual-energy X-ray absorptiometry with neutron activation analysis. J Bone Miner Res 11:843-848.
40. Erlandson MC, Sherar LB, Baxter-Jones AD, Jackowski SA, Ludwig-Auser H, Arnold C, Sankaran K. 2011. Preterm birth and adolescent bone mineral content. Am J Perinatol 28:157-163.
41. Faulkner RA, Bailey DA, Drinkwater DT, McKay HA, Arnold C, Wilkinson AA. 1996. Bone densitometry in Canadian children 8-17 years of Age. Calcif Tissue Int 59:344-351.
42. Faulkner RA, Bailey DA, Drinkwater DT, Wilkinson AA, Houston CS, McKay HA. 1993. Regional and total body bone mineral content, bone mineral density, and total body tissue composition in children 8-16 years of age. Calcif Tissue Int 53:7-12.
43. Ferrari S, Rizzoli R, Slosman D, Bonjour JP. 1998. Familial resemblance for bone mineral mass is expressed before puberty. J Clin Endocrinol Metab 83:358-361.
44. Finkelstein JS, Neer RM, Biller BM, Crawford JD, Klibanski A. 1992. Osteopenia in men with a history of delayed puberty. N Engl J Med 326:600-604.
45. Freeman JV, Cole TJ, Chinn S, Jones PR, White EM, Preece MA. 1995. Cross sectional stature and weight reference curves for the UK, 1990. Arch Dis Child 73:17-24.
46. Gilsanz V, Chalfant J, Kalkwarf H, Zemel B, Lappe J, Oberfield S, Shepherd J, Wren T, Winer K. 2011. Age at onset of puberty predicts bone mass in young adulthood. J Pediatr 158:100-105.
47. Gilsanz V, Roe TF, Mora S, Costin G, Goodman WG. 1991. Changes in vertebral bone density in black girls and white girls during childhood and puberty. N Engl J Med 325:1597-1600.
48. Gilsanz V, Skaggs DL, Kovanlikaya A, Sayre J, Loro ML, Kaufman F, Korenman SG. 1998. Differential effect of race on the axial and appendicular skeletons of children. J Clin Endocrinol Metab 83: 1420-1427.
49. Glastre C, Braillon P, David L, Cochat P, Meunier PJ, Delmas PD. 1990. Measurement of bone mineral content of the lumbar spine by dual energy x-ray absorptiometry in normal children: correlations with growth parameters. J Clin Endocrinol Metab 70:1330-1333.
50. Gordon CM, Bachrach LK, Carpenter TO, Crabtree N, El-Hajj Fuleihan G, Kutilek S, Lorenc RS, Tosi LL, Ward KA, Ward LM, Kalkwarf HJ. 2008. Dual energy X-ray absorptiometry interpretation and reporting in children and adolescents: the 2007 ISCD Pediatric Official Positions. J Clin Densitom 11:43-58.
51. Goulding A, Jones IE, Taylor RW, Manning PJ, Williams SM. 2000. More broken bones: a 4-year double cohort study of young girls with and without distal forearm fractures. J Bone Miner Res 15: 2011-2018.
52. Goulding A, Rockell JE, Black RE, Grant AM, Jones IE, Williams SM. 2004. Children who avoid drinking cow's milk are at increased risk for prepubertal bone fractures. J Am Diet Assoc 104:250-253.
53. Grant SF, Reid DM, Blake G, Herd R, Fogelman I, Ralston SH. 1996. Reduced bone density and osteoporosis associated with a polymorphic Sp1 binding site in the collagen type I alpha 1 gene. Nat Genet 14:203-205.
54. Greulich W, Pyle S. 1950. Radiographic atlas of skeletal development of the hand and wrist. Stanford, CA: Stanford University Press.
55. Grimston SK, Willows ND, Hanley DA. 1993. Mechanical loading regime and its relationship to bone mineral density in children. Med Sci Sports Exerc 25:1203-1210.
56. Gunter K, Baxter-Jones AD, Mirwald RL, Almstedt H, Fuchs RK, Durski S, Snow C. 2008. Impact exercise increases BMC during growth: an 8-year longitudinal study. J Bone Miner Res 23:986-993.
57. Gustavsson A, Nordstrom P, Lorentzon R, Lerner UH, Lorentzon M. 2000. Osteocalcin gene polymorphism is related to bone density in healthy adolescent females. Osteoporos Int 11:847-851.
58. Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I. 2000. Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone 27:351-357.
59. Hasselstrom HA, Karlsson MK, Hansen SE, Gronfeldt V, Froberg K, Andersen LB. 2008. A 3-year physical activity intervention program increases the gain in bone mineral and bone width in prepubertal girls but not boys: the prospective copenhagen school child interventions study (CoSCIS). Calcif Tissue Int 83:243-250.
60. Heaney RP. 1988. Nutritional factors in causation of osteoporosis. Ann Chir Gynaecol 77:176-179.
61. Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C. 2000. Peak bone mass. Osteoporos Int 11: 985-1009.
62. Henderson RC, Berglund LM, May R, Zemel BS, Grossberg RI, Johnson J, Plotkin H, Stevenson RD, Szalay E, Wong B, Kecskemethy HH, Harcke HT. 2009. The relationship between fractures and DXA measures of BMD in the distal femur of children and adolescents with cerebral palsy or muscular dystrophy. J Bone Miner Res 25(3):520-526, 2010.
63. Henderson RC, Madsen CD. 1996. Bone density in children and adolescents with cystic fibrosis. J Pediatr 128:28-34.
64. Jackowski SA, Erlandson MC, Mirwald RL, Faulkner RA, Bailey DA, Kontulainen SA, Cooper DM, Baxter-Jones AD. 2011. Effect of maturational timing on bone mineral content accrual from childhood to adulthood: evidence from 15 years of longitudinal data. Bone 48:1178-1185.
65. Johnston CC, Jr, Miller JZ, Slemenda CW, Reister TK, Hui S, Christian JC, Peacock M. 1992. Calcium supplementation and increases in bone mineral density in children. N Engl J Med 327: 82-87.
66. Kalkwarf HJ, Laor T, Bean JA. 2011. 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 22:607-616.
67. Kelly T, Specker B, Binkley T, Zemel B, Leonard M, Kalkwarf H, Moyer-Mileur H, Pan H, Cole T, Shepherd J. 2005. Pediatric BMD reference database for U.S white children, International Conference on Children's Bone Health, Sorrento, Italy Kerstetter JE, O'Brien KO, Caseria DM, Wall DE, Insogna KL. 2005. The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab 90: 26-31.
68. Kerstetter JE, O'Brien KO, Insogna KL. 2003. Dietary protein, calcium metabolism, and skeletal homeostasis revisited. Am J Clin Nutr 78(Suppl 3):584S-592S.
69. Kindblom JM, Lorentzon M, Norjavaara E, Hellqvist A, Nilsson S, Mellstrom D, Ohlsson C. 2006. Pubertal timing predicts previous fractures and BMD in young adult men: the GOOD study. J Bone Miner Res 21:790-795.
70. Koay MA, Tobias JH, Leary SD, Steer CD, Vilarino-Guell C, Brown MA. 2007. The effect of LRP5 polymorphisms on bone mineral density is apparent in childhood. Calcif Tiss Int 81:1-9.
71. Krall EA, Dawson-Hughes B. 1993. Heritable and life-style determinants of bone mineral density. J Bone Miner Res 8:1-9.
72. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R,Mei Z, Curtin LR, Roche AF, Johnson CL. 2000. CDC growth charts: United States. Adv Data 8(314):1-27.
73. Lee WT, Leung SS, Leung DM, Cheng JC. 1996. A follow-up study on the effects of calcium-supplement withdrawal and puberty on bone acquisition of children. Am J Clin Nutr 64:71-77.
74. Lee WT, Leung SS, Leung DM, Tsang HS, Lau J, Cheng JC. 1995. A randomized double-blind controlled calcium supplementation trial, and bone and height acquisition in children. Br J Nutr 74:125-139.
75. Leib ES, Lewiecki EM, Binkley N, Hamdy RC. 2004. Official positions of the International Society for Clinical Densitometry. J Clin Densitom 7:1-6.
76. Leonard MB, Feldman HI, Zemel MB, Berlin JA, Riley EM, Stallings VA. 1998. Evaluation of low density spine software for the assessment of bone mineral density in children. J Bone Miner Res 13:1687-1690.
77. Leonard MB, Propert KJ, Zemel BS, Stallings VA, Feldman HI. 1999. Discrepancies in pediatric bone mineral density reference data: potential for misdiagnosis of osteopenia. J Pediatr 135:182-188.
78. Leonard MB, Shults J, Wilson BA, Tershakovec AM, Zemel BS. 2004. Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr 80:514-523.
79. Leonard MB, Zemel BS. 2002. Current concepts in pediatric bone disease. Pediatr Clin North Am 49:143-173.
80. Lohman T, Roche AF, Martorell R. 1988. Anthropometric standardization reference manual. Champaign, IL: Human Kinetics Books.
81. Looker AC, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP, Johnston CC, Jr, Lindsay R. 1998. Updated data on proximal femur bone mineral levels of US adults. Osteoporos Int 8:468-489.
82. Looker AC, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP, Johnston CC, Jr, Lindsay RL. 1995. Proximal femur bone mineral levels of US adults. Osteoporos Int 5:389-409.
83. Lorentzon M, Lorentzon R, Backstrom T, Nordstrom P. 1999. Estrogen receptor gene polymorphism, but not estradiol levels, is related to bone density in healthy adolescent boys: a cross-sectional and longitudinal study. Journal Clin Endocrinol Metab 84:4597-4601.
84. Lorentzon M, Lorentzon R, Nordstrom P. 2000. Interleukin-6 gene polymorphism is related to bone mineral density during and after puberty in healthy white males: a cross-sectional and longitudinal study. J Bone Miner Res 15:1944-1949.
85. Lorentzon M, Mellstrom D, Ohlsson C. 2005. Age of attainment of peak bone mass is site specific in Swedish men-The GOOD study. J Bone Miner Res 20:1223-1227.
86. Lorentzon M, Swanson C, Eriksson AL, Mellstrom D, Ohlsson C. 2006. Polymorphisms in the aromatase gene predict areal BMD as a result of affected cortical bone size: the GOOD study. J Bone Miner Res 21: 332-339.
87. Macdonald HM, Kontulainen SA, Khan KM, McKay HA
88. MacKelvie KJ, Khan KM, Petit MA, Janssen PA, McKay HA. 2003. A school-based exercise intervention elicits substantial bone health benefits: a 2-year randomized controlled trial in girls. Pediatrics 112:e447.
89. McCormick DP, Ponder SW, Fawcett HD, Palmer JL. 1991. Spinal bone mineral density in 335 normal and obese children and adolescents: evidence for ethnic and sex differences. J Bone Miner Res 6: 507-513.
90. McKay HA, Bailey DA, Mirwald RL, Davison KS, Faulkner RA. 1998. Peak bone mineral accrual and age at menarche in adolescent girls: a 6-year longitudinal study. J Pediatr 133:682-687.
91. McKay HA, Petit MA, Schutz RW, Prior JC, Barr SI, Khan KM. 2000. Augmented trochanteric bone mineral density after modified physical education classes: a randomized school-based exercise intervention study in prepubescent and early pubescent children. J Pediatr 136:156-162.
92. Moons P, Bovijn L, Budts W, Belmans A, Gewillig M. 2010. Temporal trends in survival to adulthood among patients born with congenital heart disease from 1970 to 1992 in Belgium. Circulation 122: 2264-2272.
93. Mora S, Gilsanz V. 2003. Establishment of peak bone mass. Endocrinol Metab Clin N Am 32:39-63.
94. Nelson DA, Simpson PM, Johnson CC, Barondess DA, Kleerekoper M. 1997. The accumulation of whole body skeletal mass in third- and fourth-grade children: effects of age, gender, ethnicity, and body composition. Bone 20:73-78.
95. Office of the Surgeon General. 2004. Bone health and osteoporosis: a report of the Surgeon General - Rockville, MD. Washington, D.C. U.S. Dept. of Health and Human Services, Public Health Service.
96. Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB. 2005. Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568-576.
97. Prentice A, Schoenmakers I, Laskey MA, de Bono S, Ginty F, Goldberg GR. 2006. Nutrition and bone growth and development. Proc Nutr 65:348-360.
98. Rauch F. 2007. Bone accrual in children: adding substance to surfaces. Pediatrics 119(Suppl 2):S137-S140.
99. Reid DW, Blizzard CL, Shugg DM, Flowers C, Cash C, Greville HM. 2011. Changes in cystic fibrosis mortality in Australia, 1979-2005. Med J Aust 195:392-395.
100. Richards JB, Rivadeneira F, Inouye M, Pastinen TM, Soranzo N, Wilson SG, Andrew T, Falchi M, Gwilliam R, Ahmadi KR, Valdes AM, Arp P,Whittaker P, Verlaan DJ, Jhamai M, Kumanduri V, Moorhouse M, van Meurs JB, Hofman A, Pols HA, Hart D, Zhai G, Kato BS, Mullin BH, Zhang F, Deloukas P, Uitterlinden AG, Spector TD. 2008. Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet 371:1505-1512.
101. Rivadeneira F, Styrkarsdottir U, Estrada K, Halldorsson BV, Hsu YH, Richards JB, Zillikens MC, Kavvoura FK, Amin N, Aulchenko YS, Cupples LA, Deloukas P, Demissie S, Grundberg E, Hofman A, Kong A, Karasik D, van Meurs JB, Oostra B, Pastinen T, Pols HA, Sigurdsson G, Soranzo N, Thorleifsson G, Thorsteinsdottir U, Williams FM, Wilson SG, Zhou Y, Ralston SH, van Duijn CM, Spector T, Kiel DP, Stefansson K, Ioannidis JP, Uitterlinden AG. 2009. Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies. Nat Genet 41: 1199-1206.
102. Saarinen A, Valimaki VV, Valimaki MJ, Loyttyniemi E, Auro K, Uusen P, Kuris M, Lehesjoki AE, Makitie O. 2007. The A1330V polymorphism of the low-density lipoprotein receptor-related protein 5 gene (LRP5) associates with low peak bone mass in young healthy men. Bone 40:1006-1012.
103. Sainz J, Van Tornout JM, Sayre J, Kaufman F, Gilsanz V. 1999. Association of collagen type 1 alpha1 gene polymorphism with bone density in early childhood. J Clin Endocrinol Metab 84:853-855.
104. Schonau E, Westermann F, Mokow E, Scheidhauer K, Werhahn E, Stabrey A, Muller-Berghaus J. 1998. The functional muscle-bone unit in health and disease. Paediatr Osteol 1154:191-202.
105. Shepherd JA, Wang L, Fan B, Gilsanz V, Kalkwarf HJ, Lappe J, Lu Y, Hangartner T, Zemel BS, Fredrick M, Oberfield S, Winer KK. 2011. Optimal monitoring time interval between DXA measures in children. J Bone Miner Res 26:2745-2752.
106. Shypailo RJ, Ellis KJ. 2005. Bone assessment in children: comparison of fan-beam DXA analysis. J Clin Densitom 8:445-453.
107. Slemenda CW, Reister TK, Hui SL, Miller JZ, Christian JC, Johnston CC. 1994. Influences on skeletal mineralization in children and adolescents: evidence for varying effects of sexual maturation and physical activity. J Pediatr 125:201-207.
108. Southard RN, Morris JD, Mahan JD, Hayes JR, Torch MA, Sommer A, Zipf WB. 1991. Bone mass in healthy children: measurement with quantitative DXA. Radiology 179:735-738.
109. Spencer RP, Garn SM, Coulombe MJ. 1966. Age-dependent changes in metacarpal cortical thickness in two populations. Invest Radiol 1: 394-397.
110. Stanojevic S, Wade A, Stocks J, Hankinson J, Coates AL, Pan H, Rosenthal M, Corey M, Lebecque P, Cole TJ. 2008. Reference ranges for spirometry across all ages: a new approach. Am J Respir Crit Care Med 177:253-260.
111. Stettler N, Berkowtiz RI, Cronquist JL, Shults J,Wadden TA, Zemel BS, Leonard MB. 2008. Observational study of bone accretion during successful weight loss in obese adolescents. Obesity (Silver Spring) 16:96-101.
112. Styrkarsdottir U, Halldorsson BV, Gretarsdottir S, Gudbjartsson DF, Walters GB, Ingvarsson T, Jonsdottir T, Saemundsdottir J, Center JR, Nguyen TV, Bagger Y, Gulcher JR, Eisman JA, Christiansen C, Sigurdsson G, Kong A, Thorsteinsdottir U, Stefansson K. 2008. Multiple genetic loci for bone mineral density and fractures. N Engl J Med 358:2355-2365.
113. Suuriniemi M, Kovanen V, Mahonen A, Alen M, Wang Q, Lyytikainen A, Cheng S. 2006. COL1A1 Sp1 polymorphism associates with bone density in early puberty. Bone 39:591-597.
114. Tanner J, Healy M, Goldstein H, Cameron N. 2001. Assessment of skeletal maturity and prediction of adult height (TW3) method. London: W.B. Saunders.
115. Tanner JM, Whitehouse RH. 1976. Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51:170-179.
116. Tanner JM, Whitehouse RH, Marubini E, Resele LF. 1976. The adolescent growth spurt of boys and girls of the Harpenden growth study. Ann Hum Biol 3:109-126.
117. Thayu M, Shults J, Burnham JM, Zemel BS, Baldassano RN, Leonard MB. 2007. Gender differences in body composition deficits at diagnosis in children and adolescents with Crohn's disease. Inflamm Bowel Dis 13(9):1121-1128.
118. 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. 2009. Common variants in the region around Osterix are associated with bone mineral density and growth in childhood. Hum Mol Genet 18: 1510-1517.
119. Tobias JH, Steer CD, Vilarino-Guell C, Brown MA. 2007. Estrogen receptor alpha regulates area-adjusted bone mineral content in late pubertal girls. J Clin Endocrinol Metab 92:641-647.
120. van Staa TP, Dennison EM, Leufkens HG, Cooper C. 2001. Epidemiology of fractures in England and Wales. Bone 29:517-522.
121. Vatanparast H, Bailey DA, Baxter-Jones AD, Whiting SJ. 2007. The effects of dietary protein on bone mineral mass in young adults may be modulated by adolescent calcium intake. J Nutr 137:2674-2679.
122. Ward KA, Roberts SA, Adams JE, Mughal MZ. 2005. Bone geometry and density in the skeleton of pre-pubertal gymnasts and school children. Bone 36:1012-1018.
123. Wells JC, Williams JE, Chomtho S, Darch T, Grijalva-Eternod C, Kennedy K, Haroun D, Wilson C, Cole TJ, Fewtrell MS. 2010. Pediatric reference data for lean tissue properties: density and hydration from age 5 to 20 y. Am J Clin Nutr 91:610-618.
124. Wetzsteon RJ, Zemel BS, Shults J, Howard KM, Kibe LW, Leonard MB. 2011. Mechanical loads and cortical bone geometry in healthy children and young adults. Bone 48:1103-1108.
125. Wey CL, Beare T, Biskeborn K, Binkley T, Arneson L, Specker B. 2009. High bone density in young Hutterite children. Bone 44:454-460.
126. Xu L, Nicholson P, Wang Q, Alen M, Cheng S. 2009. Bone and muscle development during puberty in girls: a seven-year longitudinal study. J Bone Miner Res 24:1693-1698.
127. Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, Frederick MM, Huang X, Lu M, Mahboubi S, Hangartner T, Winer KK. 2011. Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the bone mineral density in childhood study. J Clin Endocrinol Metab 96:3160-3169.
128. Zemel BS, Kawchak DA, Ohene-Frempong K, Schall JI, Stallings VA. 2007. Effects of delayed pubertal development, nutritional status, and disease severity on longitudinal patterns of growth failure in children with sickle cell disease. Pediatr Res 61:607-613.
129. Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, Mahboubi S, Shepherd JA, Hangartner TN, Frederick MM, Winer KK, Kalkwarf HJ. 2010. Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 95:1265-1273.