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Determinants of Peak Bone Mass Acquisition

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Osteoporosis

Part of the book series: Contemporary Endocrinology ((COE))

Abstract

Peak bone mass (PBM) is an important determinant of osteoporotic fracture risk later in life. Bone mineral mass accumulation from infancy to postpuberty is a complex process implicating interactions of genetic, endocrine, mechanical, and nutritional factors. PBM is attained in the axial skeleton and in the proximal femur by the end of the second decade of life. The increase in mass and strength is essentially due to an increment in bone size, with volumetric bone mineral density (BMD) changing very little during growth. In adult women, an increase of PBM by 10%, that is, by approximately 1 standard deviation (SD), could decrease the risk of fragility fracture by 50% or be equivalent to retarding menopause by 14 years. Bone mineral mass during growth follows a trajectory. The main influencing factor is genetics. Increasing calcium intake or mechanical loading can shift upward the age-bone mass trajectory, while chronic diseases and their treatment can shift it downward. Prepuberty appears to be an opportune time for obtaining a substantial benefit of increasing physical activity with appropriate intakes of calcium and proteins.

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References

  1. Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone. 2010;46:294–305.

    Article  PubMed  Google Scholar 

  2. Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O'Karma M, Wallace TC, Zemel BS. The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. 2016;27:1281–386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. 1996;312:1254–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hernandez CJ, Beaupre GS, Carter DR. A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int. 2003;14:843–7.

    Article  CAS  PubMed  Google Scholar 

  5. Binkovitz LA, Sparke P, Henwood MJ. Pediatric DXA: clinical applications. Pediatr Radiol. 2007;37(7):625–35.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bachrach LK. Assessing bone health in children: who to test and what does it mean? Pediatr Endocrinol Rev. 2005;2(Suppl 3):332–6.

    PubMed  Google Scholar 

  7. Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, Reginster JY. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int. 2013;24:23–57.

    Article  CAS  PubMed  Google Scholar 

  8. Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int. 2003;14(Suppl 3):S13–8.

    Article  PubMed  Google Scholar 

  9. Engelke K, Gluer CC. Quality and performance measures in bone densitometry: part 1: errors and diagnosis. Osteoporos Int. 2006;17:1283–92.

    Article  CAS  PubMed  Google Scholar 

  10. Kanis JA, Gluer CC. An update on the diagnosis and assessment of osteoporosis with densitometry. Committee of Scientific Advisors, international osteoporosis foundation. Osteoporos Int. 2000;11:192–202.

    Article  CAS  PubMed  Google Scholar 

  11. Slosman DO, Rizzoli R, Donath A, Bonjour JP. Vertebral bone mineral density measured laterally by dual-energy X-ray absorptiometry. Osteoporos Int. 1990;1:23–9.

    Article  CAS  PubMed  Google Scholar 

  12. Katzman DK, Bachrach LK, Carter DR, Marcus R. Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab. 1991;73:1332–9.

    Article  CAS  PubMed  Google Scholar 

  13. Biver E, Durosier-Izart C, Chevalley T, van Rietbergen B, Rizzoli R, Ferrari S. Evaluation of radius microstructure and areal bone mineral density improves fracture prediction in postmenopausal women. J Bone Miner Res. 2018;33:328–37.

    Article  PubMed  Google Scholar 

  14. Trotter M, Hixon BB. Sequential changes in weight, density, and percentage ash weight of human skeletons from an early fetal period through old age. Anat Rec. 1974;179:1–18.

    Article  CAS  PubMed  Google Scholar 

  15. Bonjour JP, Theintz G, Buchs B, Slosman D, Rizzoli R. Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab. 1991;73:555–63.

    Article  CAS  PubMed  Google Scholar 

  16. Gilsanz V, Boechat MI, Roe TF, Loro ML, Sayre JW, Goodman WG. Gender differences in vertebral body sizes in children and adolescents. Radiology. 1994;190:673–7.

    Article  CAS  PubMed  Google Scholar 

  17. Seeman E. Structural basis of growth-related gain and age-related loss of bone strength. Rheumatology (Oxford). 2008;47(Suppl 4):iv2–8.

    Google Scholar 

  18. Theintz G, Buchs B, Rizzoli R, Slosman D, Clavien H, Sizonenko PC, Bonjour JP. Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab. 1992;75:1060–5.

    CAS  PubMed  Google Scholar 

  19. Bonjour JP, Rizzoli R. Bone acquisition in adolescence. In: Marcus R, Feldman D, Kelsey J, editors. Osteoporosis. 2nd ed. San Diego: Academic Press; 2001. p. 621–38.

    Chapter  Google Scholar 

  20. Fournier PE, Rizzoli R, Slosman DO, Theintz G, Bonjour JP. Asynchrony between the rates of standing height gain and bone mass accumulation during puberty. Osteoporos Int. 1997;7:525–32.

    Article  CAS  PubMed  Google Scholar 

  21. Bailey DA, Wedge JH, McCulloch RG, Martin AD, Bernhardson SC. Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am. 1989;71:1225–31.

    Article  CAS  PubMed  Google Scholar 

  22. Ferrari SL, Chevalley T, Bonjour JP, Rizzoli R. Childhood fractures are associated with decreased bone mass gain during puberty: an early marker of persistent bone fragility? J Bone Miner Res. 2006;21:501–7.

    Article  PubMed  Google Scholar 

  23. Landin LA. Frcture 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.

    CAS  PubMed  Google Scholar 

  24. Kirmani S, Christen D, van Lenthe GH, et al. Bone structure at the distal radius during adolescent growth. J Bone Miner Res. 2009;24:1033–42.

    Article  PubMed  Google Scholar 

  25. 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;25:1521–6.

    Article  PubMed  Google Scholar 

  26. 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;27:273–82.

    Article  PubMed  Google Scholar 

  27. Gilsanz V, Gibbens DT, Carlson M, Boechat MI, Cann CE, Schulz EE. Peak trabecular vertebral density: a comparison of adolescent and adult females. Calcif Tissue Int. 1988;43:260–2.

    Article  CAS  PubMed  Google Scholar 

  28. Wren TA, Kim PS, Janicka A, Sanchez M, Gilsanz V. Timing of peak bone mass: discrepancies between CT and DXA. J Clin Endocrinol Metab. 2007;92:938–41.

    Article  CAS  PubMed  Google Scholar 

  29. Farr JN, Khosla S. Skeletal changes through the lifespan – from growth to senescence. Nat Rev Endocrinol. 2015;11:513–21.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Garn SM, Rohmann CG, Wagner B, Ascoli W. Continuing bone growth throughout life: a general phenomenon. Am J Phys Anthropol. 1967;26:313–7.

    Article  CAS  PubMed  Google Scholar 

  31. Garn SM, Wagner B, Rohmann CG, Ascoli W. Further evidence for continuing bone expansion. Am J Phys Anthropol. 1968;28:219–21.

    Article  CAS  PubMed  Google Scholar 

  32. Turner CH. Toward a cure for osteoporosis: reversal of excessive bone fragility. Osteoporos Int. 1991;2:12–9.

    Article  CAS  PubMed  Google Scholar 

  33. Caverzasio J, Montessuit C, Bonjour JP. Stimulatory effect of insulin-like growth factor-1 on renal Pi transport and plasma 1,25-dihydroxyvitamin D3. Endocrinology. 1990;127:453–9.

    Article  CAS  PubMed  Google Scholar 

  34. Rosen JF, Chesney RW. Circulating calcitriol concentrations in health and disease. J Pediatr. 1983;103:1–17.

    Article  CAS  PubMed  Google Scholar 

  35. Corvilain J, Abramow M. Growth and renal control of plasma phosphate. J Clin Endocrinol Metab. 1972;34:452–9.

    Article  CAS  PubMed  Google Scholar 

  36. Krabbe S, Transbol I, Christiansen C. Bone mineral homeostasis, bone growth, and mineralisation during years of pubertal growth: a unifying concept. Arch Dis Child. 1982;57:359–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Round JM, Butcher S, Steele R. Changes in plasma inorganic phosphorus and alkaline phosphatase activity during the adolescent growth spurt. Ann Hum Biol. 1979;6:129.

    Article  CAS  PubMed  Google Scholar 

  38. Caverzasio J, Bonjour JP. IGF-I, a key regulator of renal phosphate transport and 1,25-Dihydroxyvitamine D3 production during growth. News Physiol Sci. 1991;6:206–10.

    CAS  Google Scholar 

  39. Underwood LE, D’Ercole AJ, Van Wyk JJ. Somatomedin-C and the assessment of growth. Pediatr Clin N Am. 1980;27:771–82.

    Article  CAS  Google Scholar 

  40. Rizzoli R. Nutritional aspects of bone health. Best Pract Res Clin Endocrinol Metab. 2014;28:795–808.

    Article  CAS  PubMed  Google Scholar 

  41. Krabbe S, Christiansen C, Rodbro P, Transbol I. Pubertal growth as reflected by simultaneous changes in bone mineral content and serum alkaline phosphatase. Acta Paediatr Scand. 1980;69:49–52.

    Article  CAS  PubMed  Google Scholar 

  42. Szulc P, Seeman E, Delmas PD. Biochemical measurements of bone turnover in children and adolescents. Osteoporos Int. 2000;11:281–94.

    Article  CAS  PubMed  Google Scholar 

  43. Krabbe S, Christiansen C. Longitudinal study of calcium metabolism in male puberty. I. Bone mineral content, and serum levels of alkaline phosphatase, phosphate and calcium. Acta Paediatr Scand. 1984;73:745–9.

    Article  CAS  PubMed  Google Scholar 

  44. Fukumoto S, Yamashita T. FGF23 is a hormone-regulating phosphate metabolism-unique biological characteristics of FGF23. Bone. 2007;40:1190–5.

    Article  CAS  PubMed  Google Scholar 

  45. Ferrari SL, Bonjour JP, Rizzoli R. Fibroblast growth factor-23 relationship to dietary phosphate and renal phosphate handling in healthy young men. J Clin Endocrinol Metab. 2005;90:1519–24.

    Article  CAS  PubMed  Google Scholar 

  46. Cadogan J, Blumsohn A, Barker ME, Eastell R. A longitudinal study of bone gain in pubertal girls: anthropometric and biochemical correlates. J Bone Miner Res. 1998;13:1602–12.

    Article  CAS  PubMed  Google Scholar 

  47. Pocock NA, Eisman JA, Hopper JL, Yeates MG, Sambrook PN, Eberl S. Genetic determinants of bone mass in adults. A twin study J Clin Invest. 1987;80:706–10.

    Article  CAS  PubMed  Google Scholar 

  48. Rizzoli R, Bonjour JP, Ferrari SL. Osteoporosis, genetics and hormones. J Mol Endocrinol. 2001;26:79–94.

    Article  CAS  PubMed  Google Scholar 

  49. 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;320:554–8.

    Article  CAS  PubMed  Google Scholar 

  50. Nguyen TV, Howard GM, Kelly PJ, Eisman JA. Bone mass, lean mass, and fat mass: same genes or same environments? Am J Epidemiol. 1998;147:3–16.

    Article  CAS  PubMed  Google Scholar 

  51. Slemenda CW, Christian JC, Williams CJ, Norton JA, Johnston CC. Genetic determinants of bone mass in adult women: a reevaluation of the twin model and the potential importance of gene interaction on heritability estimates. J Bone Miner Res. 1991;6:561–7.

    Article  CAS  PubMed  Google Scholar 

  52. Ferrari S, Rizzoli R, Slosman D, Bonjour JP. Familial resemblance for bone mineral mass is expressed before puberty. J Clin Endocrinol Metab. 1998;83:358–61.

    CAS  PubMed  Google Scholar 

  53. Pepe J, Biver E, Bonnet N, Herrmann FR, Rizzoli R, Chevalley T, Ferrari SL. Within- and across-sex inheritance of bone microarchitecture. J Clin Endocrinol Metab. 2017;102:40–5.

    PubMed  Google Scholar 

  54. Garnero P, Arden NK, Griffiths G, Delmas PD, Spector TD. Genetic influence on bone turnover in postmenopausal twins. J Clin Endocrinol Metab. 1996;81:140–6.

    CAS  PubMed  Google Scholar 

  55. Ferrari SL, Rizzoli R. Gene variants for osteoporosis and their pleiotropic effects in aging. Mol Asp Med. 2005;26:145–67.

    Article  CAS  Google Scholar 

  56. Peacock M, Turner CH, Econs MJ, Foroud T. Genetics of osteoporosis. Endocr Rev. 2002;23:303–26.

    Article  CAS  PubMed  Google Scholar 

  57. Ferrari SL, Rizzoli R, Slosman DO, Bonjour JP. Do dietary calcium and age explain the controversy surrounding the relationship between bone mineral density and vitamin D receptor gene polymorphisms? J Bone Miner Res. 1998;13:363–70.

    Article  CAS  PubMed  Google Scholar 

  58. Sainz J, Van Tornout JM, Loro ML, Sayre J, Roe TF, Gilsanz V. Vitamin D-receptor gene polymorphisms and bone density in prepubertal American girls of Mexican descent. N Engl J Med. 1997;337:77–82.

    Article  CAS  PubMed  Google Scholar 

  59. Ferrari S, Bonjour JP, Rizzoli R. The vitamin D receptor gene and calcium metabolism. Trends Endocrinol Metab. 1998;9:259–65.

    Article  CAS  PubMed  Google Scholar 

  60. Ferrari SL, Deutsch S, Choudhury U, Chevalley T, Bonjour JP, Dermitzakis ET, Rizzoli R, Antonarakis SE. Polymorphisms in the low-density lipoprotein receptor-related protein 5 (LRP5) gene are associated with variation in vertebral bone mass, vertebral bone size, and stature in whites. Am J Hum Genet. 2004;74:866–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Rivadeneira F, Styrkarsdottir U, Estrada K, et al. Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies. Nat Genet. 2009;41:1199–206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ettinger B, Sidney S, Cummings SR, Libanati C, Bikle DD, Tekawa IS, Tolan K, Steiger P. Racial differences in bone density between young adult black and white subjects persist after adjustment for anthropometric, lifestyle, and biochemical differences. J Clin Endocrinol Metab. 1997;82:429–34.

    CAS  PubMed  Google Scholar 

  63. Rupich RC, Specker BL, Lieuw AFM, Ho M. Gender and race differences in bone mass during infancy. Calcif Tissue Int. 1996;58:395–7.

    Article  CAS  PubMed  Google Scholar 

  64. Bell NH, Gordon L, Stevens J, Shary JR. Demonstration that bone mineral density of the lumbar spine, trochanter, and femoral neck is higher in black than in white young men. Calcif Tissue Int. 1995;56:11–3.

    Article  CAS  PubMed  Google Scholar 

  65. Anderson SE, Dallal GE, Must A. Relative weight and race influence average age at menarche: results from two nationally representative surveys of US girls studied 25 years apart. Pediatrics. 2003;111:844–50.

    Article  PubMed  Google Scholar 

  66. 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;325:1597–600.

    Article  CAS  PubMed  Google Scholar 

  67. Bass S, Pearce G, Bradney M, Hendrich E, Delmas PD, Harding A, Seeman E. Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J Bone Miner Res. 1998;13:500–7.

    Article  CAS  PubMed  Google Scholar 

  68. 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.

    Article  CAS  PubMed  Google Scholar 

  69. Khan KM, Bennell KL, Hopper JL, Flicker L, Nowson CA, Sherwin AJ, Crichton KJ, Harcourt PR, Wark JD. Self-reported ballet classes undertaken at age 10–12 years and hip bone mineral density in later life. Osteoporos Int. 1998;8:165–73.

    Article  CAS  PubMed  Google Scholar 

  70. Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I. 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. 2000;27:351–7.

    Article  CAS  PubMed  Google Scholar 

  71. Morris FL, Naughton GA, Gibbs JL, Carlson JS, Wark JD. Prospective ten-month exercise intervention in premenarcheal girls: positive effects on bone and lean mass. J Bone Miner Res. 1997;12:1453–62.

    Article  CAS  PubMed  Google Scholar 

  72. Bradney M, Pearce G, Naughton G, Sullivan C, Bass S, Beck T, Carlson J, Seeman E. Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res. 1998;13:1814–21.

    Article  CAS  PubMed  Google Scholar 

  73. Meyer U, Romann M, Zahner L, Schindler C, Puder JJ, Kraenzlin M, Rizzoli R, Kriemler S. Effect of a general school-based physical activity intervention on bone mineral content and density: a cluster-randomized controlled trial. Bone. 2011;48:792–7.

    Article  PubMed  Google Scholar 

  74. Meyer U, Ernst D, Zahner L, Schindler C, Puder JJ, Kraenzlin M, Rizzoli R, Kriemler S. 3-year follow-up results of bone mineral content and density after a school-based physical activity randomized intervention trial. Bone. 2013;55:16–22.

    Article  PubMed  Google Scholar 

  75. Hind K, Burrows M. Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials. Bone. 2007;40:14–27.

    Article  CAS  PubMed  Google Scholar 

  76. Kriemler S, Zahner L, Puder J, Braun-Fahrlaender C, Schindler C, Kraenzlin M, Rizzoli R. Weight-bearing bones are more sensitive to physical exercise in boys than in girls during pre- and early puberty: a cross-sectional study. Osteoporos Int. 2008;19(12):1749–58.

    Article  CAS  PubMed  Google Scholar 

  77. Marcus R. Exercise: moving in the right direction. J Bone Miner Res. 1998;13:1793–6.

    Article  CAS  PubMed  Google Scholar 

  78. Karlsson MK, Johnell O, Obrant KJ. Is bone mineral density advantage maintained long-term in previous weight lifters? Calcif Tissue Int. 1995;57:325–8.

    Article  PubMed  Google Scholar 

  79. Kontulainen S, Kannus P, Haapasalo H, Heinonen A, Sievanen H, Oja P, Vuori I. Changes in bone mineral content with decreased training in competitive young adult tennis players and controls: a prospective 4-yr follow-up. Med Sci Sports Exerc. 1999;31:646–52.

    Article  CAS  PubMed  Google Scholar 

  80. Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, Fuchs RK. Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci U S A. 2014;111:5337–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Karlsson MK, Linden C, Karlsson C, Johnell O, Obrant K, Seeman E. Exercise during growth and bone mineral density and fractures in old age. Lancet. 2000;355:469–70.

    Article  CAS  PubMed  Google Scholar 

  82. Clavien H, Theintz G, Rizzoli R, Bonjour JP. Does puberty alter dietary habits in adolescents living in a western society? J Adolesc Health. 1996;19:68–75.

    Article  CAS  PubMed  Google Scholar 

  83. Bonjour JP, Rizzoli R. Bone acquisition in adolescence. In: Marcus R, Feldman D, Kelsey J, editors. Osteoporosis. San Diego: Academic Press; 1996. p. 465–76.

    Google Scholar 

  84. Weaver CM. Calcium requirements of physically active people. Am J Clin Nutr. 2000;72:579S–84S.

    Article  CAS  PubMed  Google Scholar 

  85. Chan GM. Dietary calcium and bone mineral status of children and adolescents. Am J Dis Child. 1991;145:631–4.

    CAS  PubMed  Google Scholar 

  86. Lloyd T, Rollings N, Andon MB, et al. Determinants of bone density in young women. I. Relationships among pubertal development, total body bone mass, and total body bone density in premenarchal females. J Clin Endocrinol Metab. 1992;75:383–7.

    CAS  PubMed  Google Scholar 

  87. Matkovic V, Landoll JD, Badenhop-Stevens NE, Ha EY, Crncevic-Orlic Z, Li B, Goel P. Nutrition influences skeletal development from childhood to adulthood: a study of hip, spine, and forearm in adolescent females. J Nutr. 2004;134:701S–5S.

    Article  PubMed  Google Scholar 

  88. Cheng JC, Maffulli N, Leung SS, Lee WT, Lau JT, Chan KM. Axial and peripheral bone mineral acquisition: a 3-year longitudinal study in Chinese adolescents. Eur J Pediatr. 1999;158:506–12.

    Article  CAS  PubMed  Google Scholar 

  89. Uusi-Rasi K, Haapasalo H, Kannus P, Pasanen M, Sievanen H, Oja P, Vuori I. Determinants of bone mineralization in 8 to 20 year old Finnish females. Eur J Clin Nutr. 1997;51:54–9.

    Article  CAS  PubMed  Google Scholar 

  90. Bonjour JP, Carrie AL, Ferrari S, Clavien H, Slosman D, Theintz G, Rizzoli R. Calcium-enriched foods and bone mass growth in prepubertal girls: a randomized, double-blind, placebo-controlled trial. J Clin Invest. 1997;99:1287–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. 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;90:3342–9.

    Article  CAS  PubMed  Google Scholar 

  92. 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.

    Article  CAS  PubMed  Google Scholar 

  93. Johnston CC, Miller JZ, Slemenda CW, Reister TK, Hui S, Christian JC, Peacock M. Calcium supplementation and increases in bone mineral density in children. N Engl J Med. 1992;327:82–7.

    Article  PubMed  Google Scholar 

  94. Matkovic V, Goel PK, Badenhop-Stevens NE, et al. Calcium supplementation and bone mineral density in females from childhood to young adulthood: a randomized controlled trial. Am J Clin Nutr. 2005;81:175–88.

    Article  CAS  PubMed  Google Scholar 

  95. Nowson CA, Green RM, Hopper JL, Sherwin AJ, Young D, Kaymakci B, Guest CS, Smid M, Larkins RG, Wark JD. A co-twin study of the effect of calcium supplementation on bone density during adolescence. Osteoporos Int. 1997;7:219–25.

    Article  CAS  PubMed  Google Scholar 

  96. Winzenberg T, Shaw K, Fryer J, Jones G. Effects of calcium supplementation on bone density in healthy children: meta-analysis of randomised controlled trials. BMJ. 2006;333:775.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Zamora SA, Rizzoli R, Belli DC, Slosman DO, Bonjour JP. Vitamin D supplementation during infancy is associated with higher bone mineral mass in prepubertal girls. J Clin Endocrinol Metab. 1999;84:4541–4.

    CAS  PubMed  Google Scholar 

  98. Barker DJ. Intrauterine programming of adult disease. Mol Med Today. 1995;1:418–23.

    Article  CAS  PubMed  Google Scholar 

  99. Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M. Review: developmental origins of osteoporotic fracture. Osteoporos Int. 2006;17:337–47.

    Article  PubMed  Google Scholar 

  100. Cadogan J, Eastell R, Jones N, Barker ME. Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. BMJ. 1997;315:1255–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Ferrari S, Rizzoli R, Manen D, Slosman D, Bonjour JP. Vitamin D receptor gene start codon polymorphisms (FokI) and bone mineral density: interaction with age, dietary calcium, and 3′-end region polymorphisms. J Bone Miner Res. 1998;13:925–30.

    Article  CAS  PubMed  Google Scholar 

  102. Gordon JI. Honor thy gut symbionts redux. Science. 2012;336:1251–3.

    Article  CAS  PubMed  Google Scholar 

  103. Lucas S, Omata Y, Hofmann J, et al. Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss. Nat Commun. 2018;9:55.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Smith MI, Yatsunenko T, Manary MJ, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339:548–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Whisner CM, Castillo LF. Prebiotics, bone and mineral metabolism. Calcif Tissue Int. 2018;102:443–79.

    Article  CAS  PubMed  Google Scholar 

  106. van den Heuvel EG, Muys T, van Dokkum W, Schaafsma G. Oligofructose stimulates calcium absorption in adolescents. Am J Clin Nutr. 1999;69:544–8.

    Article  PubMed  Google Scholar 

  107. Whisner CM, Martin BR, Schoterman MH, Nakatsu CH, McCabe LD, McCabe GP, Wastney ME, van den Heuvel EG, Weaver CM. Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br J Nutr. 2013;110:1292–303.

    Article  CAS  PubMed  Google Scholar 

  108. Whisner CM, Martin BR, Nakatsu CH, McCabe GP, McCabe LD, Peacock M, Weaver CM. Soluble maize fibre affects short-term calcium absorption in adolescent boys and girls: a randomised controlled trial using dual stable isotopic tracers. Br J Nutr. 2014;112:446–56.

    Article  CAS  PubMed  Google Scholar 

  109. 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;82:471–6.

    Article  CAS  PubMed  Google Scholar 

  110. Holscher HD, Faust KL, Czerkies LA, Litov R, Ziegler EE, Lessin H, Hatch T, Sun S, Tappenden KA. Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. JPEN J Parenter Enteral Nutr. 2012;36:95s–105s.

    Article  CAS  PubMed  Google Scholar 

  111. Van den Heuvel EG, Muijs T, Van Dokkum W, Schaafsma G. Lactulose stimulates calcium absorption in postmenopausal women. J Bone Miner Res. 1999;14:1211–6.

    Article  PubMed  Google Scholar 

  112. Griffin IJ, Davila PM, Abrams SA. Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. Br J Nutr. 2002;87(Suppl 2):S187–91.

    Article  CAS  PubMed  Google Scholar 

  113. Whisner CM, Martin BR, Nakatsu CH, Story JA, MacDonald-Clarke CJ, McCabe LD, McCabe GP, Weaver CM. Soluble corn Fiber increases calcium absorption associated with shifts in the gut microbiome: a randomized dose-response trial in free-living pubertal females. J Nutr. 2016;146:1298–306.

    Article  CAS  PubMed  Google Scholar 

  114. McCabe LR, Parameswaran N. Advances in probiotic regulation of bone and mineral metabolism. Calcif Tissue Int. 2018;102:480–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Rizzoli R, Biver E. Effects of fermented Milk products on bone. Calcif Tissue Int. 2018;102:489–500.

    Article  CAS  PubMed  Google Scholar 

  116. Alvaro E, Andrieux C, Rochet V, Rigottier-Gois L, Lepercq P, Sutren M, Galan P, Duval Y, Juste C, Dore J. Composition and metabolism of the intestinal microbiota in consumers and non-consumers of yogurt. Br J Nutr. 2007;97:126–33.

    Article  CAS  PubMed  Google Scholar 

  117. Tyagi AM, Yu M, Darby TM, Vaccaro C, Li JY, Owens JA, Hsu E, Adams J, Weitzmann MN, Jones RM, Pacifici R. The microbial metabolite butyrate stimulates bone formation via T regulatory cell-mediated regulation of WNT10B expression. Immunity. 2018;49:1116–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Rizzoli R, Bonjour JP. Dietary protein and bone health. J Bone Miner Res. 2004;19:527–31.

    Article  PubMed  Google Scholar 

  119. Rizzoli R, Biver E, Bonjour JP, et al. Benefits and safety of dietary protein for bone health-an expert consensus paper endorsed by the European Society for Clinical and Economical Aspects of Osteopororosis, osteoarthritis, and musculoskeletal diseases and by the international osteoporosis foundation. Osteoporos Int. 2018;29(9):1933–48.

    Article  CAS  PubMed  Google Scholar 

  120. Rizzoli R, Bonjour JP, Ferrari S, Chevalley T. Dietary protein intakes and bone growth. In: Burckhardt P, Heaney R, Dawson-Hughes B, editors. Elsevier international congress series. Amsterdam: Elsevier; 2007. p. 50–9.

    Google Scholar 

  121. Bonjour JP, Ammann P, Chevalley T, Rizzoli R. Protein intake and bone growth. Can J Appl Physiol. 2001;26(Suppl):S153–66.

    Article  CAS  PubMed  Google Scholar 

  122. Isley WL, Underwood LE, Clemmons DR. Dietary components that regulate serum somatomedin-C concentrations in humans. J Clin Invest. 1983;71:175–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Thissen JP, Ketelslegers JM, Underwood LE. Nutritional regulation of the insulin-like growth factors. Endocr Rev. 1994;15:80–101.

    CAS  PubMed  Google Scholar 

  124. Ammann P, Bourrin S, Bonjour JP, Meyer JM, Rizzoli R. Protein undernutrition-induced bone loss is associated with decreased IGF-I levels and estrogen deficiency. J Bone Miner Res. 2000;15:683–90.

    Article  CAS  PubMed  Google Scholar 

  125. Rosen CJ. Insulin-like growth factor I and bone mineral density: experience from animal models and human observational studies. Best Pract Res Clin Endocrinol Metab. 2004;18:423–35.

    Article  CAS  PubMed  Google Scholar 

  126. Yakar S, Rosen CJ. From mouse to man: redefining the role of insulin-like growth factor-I in the acquisition of bone mass. Exp Biol Med (Maywood). 2003;228:245–52.

    Article  CAS  Google Scholar 

  127. Ammann P, Rizzoli R, Muller K, Slosman D, Bonjour JP. IGF-I and pamidronate increase bone mineral density in ovariectomized adult rats. Am J Phys. 1993;265:E770–6.

    Article  CAS  Google Scholar 

  128. 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;82:1107–14.

    Article  CAS  PubMed  Google Scholar 

  129. Young VR, Borgonha S. Nitrogen and amino acid requirements: : the Massachusetts Institute of Technology amino acid requirement pattern. J Nutr. 2000;130:1841s–9s.

    Article  CAS  PubMed  Google Scholar 

  130. Roberts TJ, Azain MJ, White BD, Martin RJ. Rats treated with somatotropin select diets higher in protein. J Nutr. 1995;125:2669–78.

    CAS  PubMed  Google Scholar 

  131. Rizzoli R. Dairy products, yogurts, and bone health. Am J Clin Nutr. 2014;99:1256s–62s.

    Article  CAS  PubMed  Google Scholar 

  132. Black RE, Williams SM, Jones IE, Goulding A. Children who avoid drinking cow milk have low dietary calcium intakes and poor bone health. Am J Clin Nutr. 2002;76:675–80.

    Article  CAS  PubMed  Google Scholar 

  133. 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;105:735–41.

    Article  PubMed  Google Scholar 

  134. Chan GM, Hoffman K, McMurry M. Effects of dairy products on bone and body composition in pubertal girls. J Pediatr. 1995;126:551–6.

    Article  CAS  PubMed  Google Scholar 

  135. Henderson RC, Hayes PR. Bone mineralization in children and adolescents with a milk allergy. Bone Miner. 1994;27:1–12.

    Article  CAS  PubMed  Google Scholar 

  136. Hidvegi E, Arato A, Cserhati E, Horvath C, Szabo A. Slight decrease in bone mineralization in cow milk-sensitive children. J Pediatr Gastroenterol Nutr. 2003;36:44–9.

    Article  PubMed  Google Scholar 

  137. Infante D, Tormo R. Risk of inadequate bone mineralization in diseases involving long-term suppression of dairy products. J Pediatr Gastroenterol Nutr. 2000;30:310–3.

    Article  CAS  PubMed  Google Scholar 

  138. Jensen VB, Jorgensen IM, Rasmussen KB, Molgaard C, Prahl P. Bone mineral status in children with cow milk allergy. Pediatr Allergy Immunol. 2004;15:562–5.

    Article  PubMed  Google Scholar 

  139. Opotowsky AR, Bilezikian JP. Racial differences in the effect of early milk consumption on peak and postmenopausal bone mineral density. J Bone Miner Res. 2003;18:1978–88.

    Article  PubMed  Google Scholar 

  140. Rockell JE, Williams SM, Taylor RW, Grant AM, Jones IE, Goulding A. Two-year changes in bone and body composition in young children with a history of prolonged milk avoidance. Osteoporos Int. 2005;16:1016–23.

    Article  CAS  PubMed  Google Scholar 

  141. Goulding A, Rockell JE, Black RE, Grant AM, Jones IE, Williams SM. Children who avoid drinking cow's milk are at increased risk for prepubertal bone fractures. J Am Diet Assoc. 2004;104:250–3.

    Article  PubMed  Google Scholar 

  142. Teegarden D, Lyle RM, Proulx WR, Johnston CC, Weaver CM. Previous milk consumption is associated with greater bone density in young women. Am J Clin Nutr. 1999;69:1014–7.

    Article  CAS  PubMed  Google Scholar 

  143. Konstantynowicz J, Nguyen TV, Kaczmarski M, Jamiolkowski J, Piotrowska-Jastrzebska J, Seeman E. Fractures during growth: potential role of a milk-free diet. Osteoporos Int. 2007;18:1601–7.

    Article  CAS  PubMed  Google Scholar 

  144. Wiley AS. Does milk make children grow? Relationships between milk consumption and height in NHANES 1999-2002. Am J Hum Biol. 2005;17:425–41.

    Article  PubMed  Google Scholar 

  145. Baker IA, Elwood PC, Hughes J, Jones M, Moore F, Sweetnam PM. A randomised controlled trial of the effect of the provision of free school milk on the growth of children. J Epidemiol Community Health. 1980;34:31–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Cheng S, Lyytikainen A, Kroger H, et al. 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;82:1115–26; quiz 1147–1118.

    Article  CAS  PubMed  Google Scholar 

  147. 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;92:159–68.

    Article  CAS  PubMed  Google Scholar 

  148. Du X, Zhu K, Trube A, Fraser DR, Greenfield AH, Zhang Q, Ma G, Hu X. Effects of school-milk intervention on growth and bone mineral accretion in Chinese girls aged 10-12 years: accounting for cluster randomisation. Br J Nutr. 2005;94:1038–9.

    Article  PubMed  CAS  Google Scholar 

  149. Lau EM, Lynn H, Chan YH, Lau W, Woo J. Benefits of milk powder supplementation on bone accretion in Chinese children. Osteoporos Int. 2004;15:654–8.

    Article  CAS  PubMed  Google Scholar 

  150. Merrilees MJ, Smart EJ, Gilchrist NL, Frampton C, Turner JG, Hooke E, March RL, Maguire P. Effects of diary food supplements on bone mineral density in teenage girls. Eur J Nutr. 2000;39:256–62.

    Article  CAS  PubMed  Google Scholar 

  151. Volek JS, Gomez AL, Scheett TP, Sharman MJ, French DN, Rubin MR, Ratamess NA, McGuigan MM, Kraemer WJ. Increasing fluid milk favorably affects bone mineral density responses to resistance training in adolescent boys. J Am Diet Assoc. 2003;103:1353–6.

    Article  PubMed  Google Scholar 

  152. Zhu K, Du X, Cowell CT, Greenfield H, Blades B, Dobbins TA, Zhang Q, Fraser DR. Effects of school milk intervention on cortical bone accretion and indicators relevant to bone metabolism in Chinese girls aged 10-12 y in Beijing. Am J Clin Nutr. 2005;81:1168–75.

    Article  CAS  PubMed  Google Scholar 

  153. Zhu K, Greenfield H, Du X, Zhang Q, Fraser DR. Effects of milk supplementation on cortical bone gain in Chinese girls aged 10-12 years. Asia Pac J Clin Nutr. 2003;12(Suppl):S47.

    Google Scholar 

  154. Zhu K, Greenfield H, Zhang Q, Ma G, Zhang Z, Hu X, Fraser DR. Bone mineral accretion and growth in Chinese adolescent girls following the withdrawal of school milk intervention: preliminary results after two years. Asia Pac J Clin Nutr. 2004;13:S83.

    Google Scholar 

  155. Zhu K, Zhang Q, Foo LH, Trube A, Ma G, Hu X, Du X, Cowell CT, Fraser DR, Greenfield H. Growth, bone mass, and vitamin D status of Chinese adolescent girls 3 y after withdrawal of milk supplementation. Am J Clin Nutr. 2006;83:714–21.

    Article  CAS  PubMed  Google Scholar 

  156. Bachrach LK. Malnutrition, endocrinopathies, and deficits in bone mass acquisition. In: Bonjour JP, Tsang RC, editors. Nutrition and bone development. Philadelphia: Lippincott-Raven; 1999. p. 261–77.

    Google Scholar 

  157. Baroncelli GI, Bertelloni S, Sodini F, Saggese G. Osteoporosis in children and adolescents: etiology and management. Paediatr Drugs. 2005;7:295–323.

    Article  PubMed  Google Scholar 

  158. Pepe J, Zawadynski S, Herrmann FR, et al. Structural basis of bone fragility in young subjects with inflammatory bowel disease: a high-resolution pQCT study of the SWISS IBD cohort (SIBDC). Inflamm Bowel Dis. 2017;23:1410–7.

    Article  PubMed  Google Scholar 

  159. Bonjour JP, Chevalley T. Pubertal timing, bone acquisition, and risk of fracture throughout life. Endocr Rev. 2014;35:820–47.

    Article  CAS  PubMed  Google Scholar 

  160. Finkelstein JS, Neer RM, Biller BM, Crawford JD, Klibanski A. Osteopenia in men with a history of delayed puberty. N Engl J Med. 1992;326:600–4.

    Article  CAS  PubMed  Google Scholar 

  161. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. Influence of age at menarche on forearm bone microstructure in healthy young women. J Clin Endocrinol Metab. 2008;93:2594–601.

    Article  CAS  PubMed  Google Scholar 

  162. Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005;90:6508–15.

    Article  CAS  PubMed  Google Scholar 

  163. Kindblom JM, Lorentzon M, Norjavaara E, Hellqvist A, Nilsson S, Mellstrom D, Ohlsson C. Pubertal timing predicts previous fractures and BMD in young adult men: the GOOD study. J Bone Miner Res. 2006;21:790–5.

    Article  PubMed  Google Scholar 

  164. Bourguignon JP. Delayed puberty and hypogonadism. In: Bertrand J, Rappaport R, Sizonenko PC, editors. Pediatric endocrinology, physiology, pathophysiology, and clinical aspects. Baltimore: Williams & Wilkins; 1993. p. 404–29.

    Google Scholar 

  165. Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, Siervogel RM. Heritability of age at menarche in girls from the Fels longitudinal study. Am J Phys Anthropol. 2005;128:210–9.

    Article  PubMed  Google Scholar 

  166. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. Deleterious effect of late menarche on distal tibia microstructure in healthy 20-year-old and premenopausal middle-aged women. J Bone Miner Res. 2009;24:144–52.

    Article  PubMed  Google Scholar 

  167. Bonjour JP. Delayed puberty and peak bone mass. Eur J Endocrinol. 1998;139:257–9.

    Article  CAS  PubMed  Google Scholar 

  168. 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;94:3424–31.

    Article  CAS  PubMed  Google Scholar 

  169. Trombetti A, Richert L, Herrmann FR, Chevalley T, Graf JD, Rizzoli R. Selective determinants of low bone mineral mass in adult women with anorexia nervosa. Int J Endocrinol. 2013;2013:897193.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  170. Misra M, Golden NH, Katzman DK. State of the art systematic review of bone disease in anorexia nervosa. Int J Eat Disord. 2016;49:276–92.

    Article  PubMed  Google Scholar 

  171. Robinson L, Aldridge V, Clark EM, Misra M, Micali N. A systematic review and meta-analysis of the association between eating disorders and bone density. Osteoporos Int. 2016;27:1953–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Ackerman KE, Misra M. Bone health and the female athlete triad in adolescent athletes. Phys Sportsmed. 2011;39:131–41.

    Article  PubMed  PubMed Central  Google Scholar 

  173. Gordon CM, Ackerman KE, Berga SL, Kaplan JR, Mastorakos G, Misra M, Murad MH, Santoro NF, Warren MP. Functional hypothalamic amenorrhea: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2017;102:1413–39.

    Article  PubMed  Google Scholar 

  174. Gremion G, Rizzoli R, Slosman D, Theintz G, Bonjour JP. Oligo-amenorrheic long-distance runners may lose more bone in spine than in femur. Med Sci Sports Exerc. 2001;33:15–21.

    Article  CAS  PubMed  Google Scholar 

  175. 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;19:1976–81.

    Article  PubMed  Google Scholar 

  176. Cheuk KY, Wang XF, Wang J, et al. Sexual dimorphism in cortical and trabecular bone microstructure appears during puberty in Chinese children. J Bone Miner Res. 2018;33(11):1948–55.

    Article  CAS  PubMed  Google Scholar 

  177. Goulding A, Jones IE, Taylor RW, Manning PJ, Williams SM. More broken bones: a 4-year double cohort study of young girls with and without distal forearm fractures. J Bone Miner Res. 2000;15:2011–8.

    Article  CAS  PubMed  Google Scholar 

  178. Goulding A, Jones IE, Taylor RW, Williams SM, Manning PJ. Bone mineral density and body composition in boys with distal forearm fractures: a dual-energy x-ray absorptiometry study. J Pediatr. 2001;139:509–15.

    Article  CAS  PubMed  Google Scholar 

  179. Chevalley T, Bonjour JP, van Rietbergen B, Rizzoli R, Ferrari S. Fractures in healthy females followed from childhood to early adulthood are associated with later menarcheal age and with impaired bone microstructure at peak bone mass. J Clin Endocrinol Metab. 2012;97:4174–81.

    Article  CAS  PubMed  Google Scholar 

  180. Chevalley T, Bonjour JP, Audet MC, Merminod F, van Rietbergen B, Rizzoli R, Ferrari S. Fracture prospectively recorded from prepuberty to young adulthood: are they markers of peak bone mass and strength in males? J Bone Miner Res. 2017;32:1963–9.

    Article  CAS  PubMed  Google Scholar 

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Rizzoli, R., Bonjour, JP. (2020). Determinants of Peak Bone Mass Acquisition. In: Leder, B., Wein, M. (eds) Osteoporosis. Contemporary Endocrinology. Humana, Cham. https://doi.org/10.1007/978-3-319-69287-6_6

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