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The Developmental Origins of Osteoporosis

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Early Life Origins of Ageing and Longevity

Part of the book series: Healthy Ageing and Longevity ((HAL,volume 9))

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Abstract

Osteoporosis is a disease characterised by poor bone strength and microarchitecture, causing bone fragility, which leads to an increased risk of fractures. Although primarily seen as a disease of old age, evidence is accumulating that in utero and early life environment can set an individual on a trajectory for osteoporosis and fragility fracture in later life. The development of osteoporosis is dependent on peak bone mass, and the subsequent rate of loss. The peak bone mass achieved by the third decade of life has been shown to be a powerful predictor of osteoporosis; although peak bone mass is partly genetically determined, the remaining majority contribution is attributable to environmental exposures in early life and modifiable lifestyle factors through life. Current osteoporosis management focuses on bone loss later in life, but it is important to consider strategies earlier in the lifecourse. This review will focus on events operating in utero, or early in post-natal life that influence bone health of the individual.

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References

  • Abrahamsen B, Heitmann BL, Eiken PA (2012) Season of birth and the risk of hip fracture in danish men and women aged 65+. Front Endocrinol (Lausanne) 3:2

    Article  Google Scholar 

  • Alexander BT, Henry Dasinger J, Intapad S (2014) Effect of low birth weight on women’s health. Clin Ther 36(12):1913–1923

    Article  PubMed  PubMed Central  Google Scholar 

  • Amundson LA, Hernandez LL, Laporta J, Crenshaw TD (2016) Maternal dietary vitamin D carry-over alters offspring growth, skeletal mineralisation and tissue mRNA expressions of genes related to vitamin D, calcium and phosphorus homoeostasis in swine. Br J Nutr 116(5):774–787

    Article  CAS  PubMed  Google Scholar 

  • Andraos S, de Seymour JV, O’Sullivan JM, Kussmann M (2018) The impact of nutritional interventions in pregnant women on DNA methylation patterns of the offspring: a systematic review. Mol Nutr Food Res e1800034

    Google Scholar 

  • Antoniades L, MacGregor AJ, Andrew T, Spector TD (2003) Association of birth weight with osteoporosis and osteoarthritis in adult twins. Rheumatology (Oxford) 42(6):791–796

    Article  CAS  Google Scholar 

  • Baird J, Kurshid MA, Kim M, Harvey N, Dennison E, Cooper C (2011) Does birthweight predict bone mass in adulthood? A systematic review and meta-analysis. Osteoporos Int 22(5):1323–1334

    Article  CAS  PubMed  Google Scholar 

  • Barker DJ (1995) Fetal origins of coronary heart disease. BMJ 311(6998):171–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boghossian NS, Koo W, Liu A, Mumford SL, Tsai MY, Yeung EH (2018) Longitudinal measures of maternal vitamin D and neonatal body composition. Eur J Clin Nutr

    Google Scholar 

  • Bonjour JP, Carrie AL, Ferrari S, Clavien H, Slosman D, Theintz G et al (1997) Calcium-enriched foods and bone mass growth in prepubertal girls: a randomized, double-blind, placebo-controlled trial. J Clin Invest 99(6):1287–1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonjour JP, Chevalley T, Ammann P, Slosman D, Rizzoli R (2001) Gain in bone mineral mass in prepubertal girls 3.5 years after discontinuation of calcium supplementation: a follow-up study. Lancet 358(9289):1208–1212

    Article  CAS  Google Scholar 

  • Borg SA, Buckley H, Owen R, Marin AC, Lu Y, Eyles D et al (2018) Early life vitamin D depletion alters the postnatal response to skeletal loading in growing and mature bone. PLoS ONE 13(1):e0190675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA (2007) Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 97(3):435–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byberg L, Michaelsson K, Goodman A, Zethelius B, Koupil I (2014) Birth weight is not associated with risk of fracture: results from two Swedish cohort studies. J Bone Miner Res 29(10):2152–2160

    Article  PubMed  Google Scholar 

  • Callreus M, McGuigan F, Akesson K (2013) Birth weight is more important for peak bone mineral content than for bone density: the PEAK-25 study of 1,061 young adult women. Osteoporos Int 24(4):1347–1355

    Article  CAS  PubMed  Google Scholar 

  • Chen JR, Lazarenko OP, Zhao H, Alund AW, Shankar K (2018) Maternal obesity impairs skeletal development in adult offspring. J Endocrinol

    Google Scholar 

  • Chen JR, Zhang J, Lazarenko OP, Kang P, Blackburn ML, Ronis MJ et al (2012) Inhibition of fetal bone development through epigenetic down-regulation of HoxA10 in obese rats fed high-fat diet. Faseb J 26(3):1131–1141

    Article  CAS  PubMed  Google Scholar 

  • Chen JR, Lazarenko OP, Blackburn ML, Rose S, Frye RE, Badger TM et al (2016) Maternal obesity programs senescence signaling and glucose metabolism in osteo-progenitors from rat and human. Endocrinology 157(11):4172–4183

    Article  CAS  PubMed  Google Scholar 

  • Chevalley T, Bonjour JP, Ferrari S, Hans D, Rizzoli R (2005) 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 90(6):3342–3349

    Article  CAS  PubMed  Google Scholar 

  • Chmurzynska A (2010) Fetal programming: link between early nutrition, DNA methylation, and complex diseases. Nutr Rev 68(2):87–98

    Article  PubMed  Google Scholar 

  • Christoffersen T, Ahmed LA, Daltveit AK, Dennison EM, Evensen EK, Furberg AS et al (2017) The influence of birth weight and length on bone mineral density and content in adolescence: The Tromso Study, Fit Futures. Arch Osteoporos 12(1):54

    Article  PubMed  Google Scholar 

  • Cole ZA, Gale CR, Javaid MK, Robinson SM, Law C, Boucher BJ et al (2009) Maternal dietary patterns during pregnancy and childhood bone mass: a longitudinal study. J Bone Miner Res 24(4):663–668

    Article  PubMed  Google Scholar 

  • Cooper C, Cawley M, Bhalla A, Egger P, Ring F, Morton L et al (1995) Childhood growth, physical activity, and peak bone mass in women. J Bone Miner Res 10(6):940–947

    Article  CAS  PubMed  Google Scholar 

  • Cooper C, Fall C, Egger P, Hobbs R, Eastell R, Barker D (1997) Growth in infancy and bone mass in later life. Ann Rheum Dis 56(1):17–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper C, Eriksson JG, Forsen T, Osmond C, Tuomilehto J, Barker DJ (2001) Maternal height, childhood growth and risk of hip fracture in later life: a longitudinal study. Osteoporos Int 12(8):623–629

    Article  CAS  PubMed  Google Scholar 

  • Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M (2006) Review: developmental origins of osteoporotic fracture. Osteoporos Int 17(3):337–347

    Article  PubMed  Google Scholar 

  • Cooper C, Harvey NC, Bishop NJ, Kennedy S, Papageorghiou AT, Schoenmakers I et al (2016) Maternal gestational vitamin D supplementation and offspring bone health (MAVIDOS): a multicentre, double-blind, randomised placebo-controlled trial. Lancet Diabetes Endocrinol 4(5):393–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper C, Ferrari S, Mitchell P, Harvey N, Dennison E (2017) IOF compendium of osteoporosis. International Osteoporosis Foundation

    Google Scholar 

  • Curtis EM, Murray R, Titcombe P, Cook E, Clarke-Harris R, Costello P et al (2017) Perinatal DNA methylation at CDKN2A is associated with offspring bone mass: findings from the Southampton Women’s Survey. J Bone Miner Res 32(10):2030–2040

    Article  CAS  PubMed  Google Scholar 

  • de Bono S, Schoenmakers I, Ceesay M, Mendy M, Laskey MA, Cole TJ et al (2010) Birth weight predicts bone size in young adulthood at cortical sites in men and trabecular sites in women from The Gambia. Bone 46(5):1316–1321

    Article  PubMed  Google Scholar 

  • Dennison EM, Arden NK, Keen RW, Syddall H, Day IN, Spector TD et al (2001) Birthweight, vitamin D receptor genotype and the programming of osteoporosis. Paediatr Perinat Epidemiol 15(3):211–219

    Article  CAS  PubMed  Google Scholar 

  • Dennison EM, Hindmarsh PC, Kellingray S, Fall CH, Cooper C (2003) Growth hormone predicts bone density in elderly women. Bone 32(4):434–440

    Article  CAS  PubMed  Google Scholar 

  • Dennison EM, Syddall HE, Rodriguez S, Voropanov A, Day IN, Cooper C (2004) Polymorphism in the growth hormone gene, weight in infancy, and adult bone mass. J Clin Endocrinol Metab 89(10):4898–4903

    Article  CAS  PubMed  Google Scholar 

  • Dennison EM, Syddall HE, Sayer AA, Gilbody HJ, Cooper C (2005) Birth weight and weight at 1 year are independent determinants of bone mass in the seventh decade: the Hertfordshire cohort study. Pediatr Res 57(4):582–586

    Article  PubMed  Google Scholar 

  • Devlin MJ, Bouxsein ML (2012) Influence of pre- and peri-natal nutrition on skeletal acquisition and maintenance. Bone 50(2):444–451

    Article  CAS  PubMed  Google Scholar 

  • Dimitri P (2018) Fat and bone in children—where are we now? Ann Pediatr Endocrinol Metab 23(2):62–69

    Article  PubMed  PubMed Central  Google Scholar 

  • Diogenes ME, Bezerra FF, Rezende EP, Donangelo CM (2015) Calcium plus vitamin D supplementation during the third trimester of pregnancy in adolescents accustomed to low calcium diets does not affect infant bone mass at early lactation in a randomized controlled trial. J Nutr 145(7):1515–1523

    Article  CAS  PubMed  Google Scholar 

  • El Hage R, Moussa E, Hammoud A, Dandachi G, Jacob C (2010) Birth weight is an independent determinant of whole body bone mineral content and bone mineral density in a group of Lebanese adolescent girls. J Bone Miner Metab 28(3):360–363

    Article  PubMed  Google Scholar 

  • Elloumi M, Ben Ounis O, Courteix D, Makni E, Sellami S, Tabka Z et al (2009) Long-term rugby practice enhances bone mass and metabolism in relation with physical fitness and playing position. J Bone Miner Metab 27(6):713–720

    Article  PubMed  Google Scholar 

  • Fall C, Hindmarsh P, Dennison E, Kellingray S, Barker D, Cooper C (1998) Programming of growth hormone secretion and bone mineral density in elderly men: a hypothesis. J Clin Endocrinol Metab 83(1):135–139

    CAS  PubMed  Google Scholar 

  • Finch SL, Rauch F, Weiler HA (2010) Postnatal vitamin D supplementation following maternal dietary vitamin D deficiency does not affect bone mass in weanling guinea pigs. J Nutr 140(9):1574–1581

    Article  CAS  PubMed  Google Scholar 

  • Forestier F, Daffos F, Rainaut M, Bruneau M, Trivin F (1987) Blood chemistry of normal human fetuses at midtrimester of pregnancy. Pediatr Res 21(6):579–583

    Article  CAS  PubMed  Google Scholar 

  • Ganpule A, Yajnik CS, Fall CH, Rao S, Fisher DJ, Kanade A et al (2006) Bone mass in Indian children–relationships to maternal nutritional status and diet during pregnancy: the Pune Maternal Nutrition Study. J Clin Endocrinol Metab 91(8):2994–3001

    Article  CAS  PubMed  Google Scholar 

  • Glendenning P, Ratajczak T, Prince RL, Garamszegi N, Strehler EE (2000) The promoter region of the human PMCA1 gene mediates transcriptional downregulation by 1,25-dihydroxyvitamin D(3). Biochem Biophys Res Commun 277(3):722–728

    Article  CAS  PubMed  Google Scholar 

  • Godfrey K, Walker-Bone K, Robinson S, Taylor P, Shore S, Wheeler T et al (2001) Neonatal bone mass: influence of parental birthweight, maternal smoking, body composition, and activity during pregnancy. J Bone Miner Res 16(9):1694–1703

    Article  CAS  PubMed  Google Scholar 

  • Haentjens P, Magaziner J, Colon-Emeric CS, Vanderschueren D, Milisen K, Velkeniers B et al (2010) Meta-analysis: excess mortality after hip fracture among older women and men. Ann Intern Med 152(6):380–390

    Article  PubMed  PubMed Central  Google Scholar 

  • Hannam K, Lawlor DA, Tobias JH (2015) Maternal preeclampsia is associated with reduced adolescent offspring hip BMD in a UK population-based birth cohort. J Bone Miner Res 30(9):1684–1691

    Article  CAS  PubMed  Google Scholar 

  • Harvey NC, Javaid MK, Poole JR, Taylor P, Robinson SM, Inskip HM et al (2008) Paternal skeletal size predicts intrauterine bone mineral accrual. J Clin Endocrinol Metab 93(5):1676–1681

    Article  CAS  PubMed  Google Scholar 

  • Harvey NC, Mahon PA, Robinson SM, Nisbet CE, Javaid MK, Crozier SR et al (2010a) Different indices of fetal growth predict bone size and volumetric density at 4 years of age. J Bone Miner Res 25(4):920–927

    PubMed  Google Scholar 

  • Harvey NC, Javaid MK, Arden NK, Poole JR, Crozier SR, Robinson SM et al (2010b) Maternal predictors of neonatal bone size and geometry: the Southampton Women’s Survey. J Dev Orig Health Dis 1(1):35–41

    Article  PubMed  PubMed Central  Google Scholar 

  • Harvey NC, Mahon PA, Kim M, Cole ZA, Robinson SM, Javaid K et al (2012) Intrauterine growth and postnatal skeletal development: findings from the Southampton Women’s Survey. Paediatr Perinat Epidemiol 26(1):34–44

    Article  PubMed  PubMed Central  Google Scholar 

  • Harvey NC, Sheppard A, Godfrey KM, McLean C, Garratt E, Ntani G et al (2014) Childhood bone mineral content is associated with methylation status of the RXRA promoter at birth. J Bone Miner Res 29(3):600–607

    Article  CAS  PubMed  Google Scholar 

  • Heijmans BT, Tobi EW, Lumey LH, Slagboom PE (2009) The epigenome: archive of the prenatal environment. Epigenetics 4(8):526–531

    Article  CAS  PubMed  Google Scholar 

  • Heppe DH, Medina-Gomez C, Hofman A, Franco OH, Rivadeneira F, Jaddoe VW (2013) Maternal first-trimester diet and childhood bone mass: the Generation R Study. Am J Clin Nutr 98(1):224–232

    Article  CAS  PubMed  Google Scholar 

  • Heppe DH, Medina-Gomez C, de Jongste JC, Raat H, Steegers EA, Hofman A et al (2014) Fetal and childhood growth patterns associated with bone mass in school-age children: the Generation R Study. J Bone Miner Res 29(12):2584–2593

    Article  PubMed  Google Scholar 

  • Hernandez CJ, Beaupre GS, Carter DR (2003) A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int 14(10):843–847

    Article  CAS  PubMed  Google Scholar 

  • Hoffman DJ, Reynolds RM, Hardy DB (2017) Developmental origins of health and disease: current knowledge and potential mechanisms. Nutr Rev 75(12):951–970

    Article  PubMed  Google Scholar 

  • Holroyd CR, Harvey NC, Crozier SR, Winder NR, Mahon PA, Ntami G et al (2012) Placental size at 19 weeks predicts offspring bone mass at birth: findings from the Southampton Women’s Survey. Placenta 33(8):623–629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes PC, Tanner JM (1970) The assessment of skeletal maturity in the growing rat. J Anat 106(Pt 2):371–402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huncharek M, Muscat J, Kupelnick B (2008) Impact of dairy products and dietary calcium on bone-mineral content in children: results of a meta-analysis. Bone 43(2):312–321

    Article  CAS  PubMed  Google Scholar 

  • Ioannou C, Javaid MK, Mahon P, Yaqub MK, Harvey NC, Godfrey KM et al (2012) The effect of maternal vitamin D concentration on fetal bone. J Clin Endocrinol Metab 97(11):E2070–E2077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarjou LM, Prentice A, Sawo Y, Laskey MA, Bennett J, Goldberg GR et al (2006) Randomized, placebo-controlled, calcium supplementation study in pregnant Gambian women: effects on breast-milk calcium concentrations and infant birth weight, growth, and bone mineral accretion in the first year of life. Am J Clin Nutr 83(3):657–666

    Article  CAS  PubMed  Google Scholar 

  • Jarjou LM, Laskey MA, Sawo Y, Goldberg GR, Cole TJ, Prentice A (2010) Effect of calcium supplementation in pregnancy on maternal bone outcomes in women with a low calcium intake. Am J Clin Nutr 92(2):450–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarjou LM, Sawo Y, Goldberg GR, Laskey MA, Cole TJ, Prentice A (2013) Unexpected long-term effects of calcium supplementation in pregnancy on maternal bone outcomes in women with a low calcium intake: a follow-up study. Am J Clin Nutr 98(3):723–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Javaid MK, Godfrey KM, Taylor P, Shore SR, Breier B, Arden NK et al (2004) Umbilical venous IGF-1 concentration, neonatal bone mass, and body composition. J Bone Miner Res 19(1):56–63

    Article  CAS  PubMed  Google Scholar 

  • Javaid MK, Godfrey KM, Taylor P, Robinson SM, Crozier SR, Dennison EM et al (2005) Umbilical cord leptin predicts neonatal bone mass. Calcif Tissue Int 76(5):341–347

    Article  CAS  PubMed  Google Scholar 

  • Javaid MK, Lekamwasam S, Clark J, Dennison EM, Syddall HE, Loveridge N et al (2006) Infant growth influences proximal femoral geometry in adulthood. J Bone Miner Res 21(4):508–512

    Article  PubMed  Google Scholar 

  • Javaid MK, Eriksson JG, Kajantie E, Forsen T, Osmond C, Barker DJ et al (2011) Growth in childhood predicts hip fracture risk in later life. Osteoporos Int 22(1):69–73

    Article  CAS  PubMed  Google Scholar 

  • Jones G, Dwyer T (2000) Birth weight, birth length, and bone density in prepubertal children: evidence for an association that may be mediated by genetic factors. Calcif Tissue Int 67(4):304–308

    Article  CAS  PubMed  Google Scholar 

  • Jones G, Riley M, Dwyer T (1999) Maternal smoking during pregnancy, growth, and bone mass in prepubertal children. J Bone Miner Res 14(1):146–151

    Article  CAS  PubMed  Google Scholar 

  • Kalkwarf HJ, Khoury JC, Lanphear BP (2003) Milk intake during childhood and adolescence, adult bone density, and osteoporotic fractures in US women. Am J Clin Nutr 77(1):257–265

    Article  CAS  PubMed  Google Scholar 

  • Koo WW, Walters JC, Esterlitz J, Levine RJ, Bush AJ, Sibai B (1999) Maternal calcium supplementation and fetal bone mineralization. Obstet Gynecol 94(4):577–582

    CAS  PubMed  Google Scholar 

  • Kuh D, Wills AK, Shah I, Prentice A, Hardy R, Adams JE et al (2014) Growth from birth to adulthood and bone phenotype in early old age: a British birth cohort study. J Bone Miner Res 29(1):123–133

    Article  PubMed  Google Scholar 

  • Lanham SA, Roberts C, Cooper C, Oreffo RO (2008a) Intrauterine programming of bone. Part 1: Alteration of the osteogenic environment. Osteoporos Int 19(2):147–156

    Article  PubMed  Google Scholar 

  • Lanham SA, Roberts C, Perry MJ, Cooper C, Oreffo RO (2008b) Intrauterine programming of bone. Part 2: Alteration of skeletal structure. Osteoporos Int 19(2):157–167

    Article  PubMed  Google Scholar 

  • Lanham SA, Roberts C, Hollingworth T, Sreekumar R, Elahi MM, Cagampang FR et al (2010) Maternal high-fat diet: effects on offspring bone structure. Osteoporos Int 21(10):1703–1714

    Article  CAS  PubMed  Google Scholar 

  • Lanham SA, Roberts C, Habgood AK, Alexander S, Burne TH, Eyles DW et al (2013) Effect of vitamin D deficiency during pregnancy on offspring bone structure, composition and quality in later life. J Dev Orig Health Dis 4(1):49–55

    Article  CAS  PubMed  Google Scholar 

  • Lee WT, Leung SS, Leung DM, Wang SH, Xu YC, Zeng WP et al (1997) Bone mineral acquisition in low calcium intake children following the withdrawal of calcium supplement. Acta Paediatr 86(6):570–576

    Article  CAS  PubMed  Google Scholar 

  • Li J, Liu X, Zuo B, Zhang L (2016) The role of bone marrow microenvironment in governing the balance between osteoblastogenesis and adipogenesis. Aging Dis 7(4):514–525

    Article  PubMed  Google Scholar 

  • Liang C, Oest ME, Jones JC, Prater MR (2009) Gestational high saturated fat diet alters C57BL/6 mouse perinatal skeletal formation. Birth Defects Res B Dev Reprod Toxicol 86(5):362–369

    Article  CAS  PubMed  Google Scholar 

  • Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135(6):1382–1386

    Article  CAS  PubMed  Google Scholar 

  • Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97(6):1064–1073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC (2008) Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 100(2):278–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M (2008) Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40(1):46–62

    Article  CAS  PubMed  Google Scholar 

  • Mahon P, Harvey N, Crozier S, Inskip H, Robinson S, Arden N et al (2010) Low maternal vitamin D status and fetal bone development: cohort study. J Bone Miner Res 25(1):14–19

    Article  CAS  PubMed  Google Scholar 

  • Mantovani AM, de Lima MCS, Gobbo LA, Ronque ERV, Romanzini M, Turi-Lynch BC et al (2018) Adults engaged in sports in early life have higher bone mass than their inactive peers. J Phys Act Health. 15(7):516–522

    Article  PubMed  Google Scholar 

  • Martin R, Harvey NC, Crozier SR, Poole JR, Javaid MK, Dennison EM et al (2007) Placental calcium transporter (PMCA3) gene expression predicts intrauterine bone mineral accrual. Bone 40(5):1203–1208

    Article  CAS  PubMed  Google Scholar 

  • Matkovic V, Landoll JD, Badenhop-Stevens NE, Ha EY, Crncevic-Orlic Z, Li B et al (2004) Nutrition influences skeletal development from childhood to adulthood: a study of hip, spine, and forearm in adolescent females. J Nutr 134(3):701s–705s

    Article  PubMed  Google Scholar 

  • Mehta G, Roach HI, Langley-Evans S, Taylor P, Reading I, Oreffo RO et al (2002) Intrauterine exposure to a maternal low protein diet reduces adult bone mass and alters growth plate morphology in rats. Calcif Tissue Int 71(6):493–498

    Article  CAS  PubMed  Google Scholar 

  • Mikkola TM, von Bonsdorff MB, Osmond C, Salonen MK, Kajantie E, Eriksson JG (2017) Association of body size at birth and childhood growth with hip fractures in older age: an exploratory follow-up of the Helsinki Birth Cohort Study. J Bone Miner Res 32(6):1194–1200

    Article  PubMed  Google Scholar 

  • Monjardino T, Rodrigues T, Inskip H, Harvey N, Cooper C, Santos AC et al (2017) Weight trajectories from birth and bone mineralization at 7 years of age. J Pediatr 191(117–24):e2

    Google Scholar 

  • Mortada I, Mortada R (2018) Epigenetic changes in mesenchymal stem cells differentiation. Eur J Med Genet. 61(2):114–118

    Article  PubMed  Google Scholar 

  • Namgung R, Tsang RC, Lee C, Han DG, Ho ML, Sierra RI (1998) Low total body bone mineral content and high bone resorption in Korean winter-born versus summer-born newborn infants. J Pediatr 132(3 Pt 1):421–425

    Article  CAS  PubMed  Google Scholar 

  • Nieves JW, Golden AL, Siris E, Kelsey JL, Lindsay R (1995) Teenage and current calcium intake are related to bone mineral density of the hip and forearm in women aged 30–39 years. Am J Epidemiol 141(4):342–351

    Article  CAS  PubMed  Google Scholar 

  • Oreffo RO, Lashbrooke B, Roach HI, Clarke NM, Cooper C (2003) Maternal protein deficiency affects mesenchymal stem cell activity in the developing offspring. Bone 33(1):100–107

    Article  CAS  PubMed  Google Scholar 

  • Pillai SM, Sereda NH, Hoffman ML, Valley EV, Crenshaw TD, Park YK et al (2016) Effects of poor maternal nutrition during gestation on bone development and mesenchymal stem cell activity in offspring. PLoS ONE 11(12):e0168382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prentice A, Jarjou LM, Goldberg GR, Bennett J, Cole TJ, Schoenmakers I (2009) Maternal plasma 25-hydroxyvitamin D concentration and birthweight, growth and bone mineral accretion of Gambian infants. Acta Paediatr 98(8):1360–1362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raman L, Rajalakshmi K, Krishnamachari KA, Sastry JG (1978) Effect of calcium supplementation to undernourished mothers during pregnancy on the bone density of the bone density of the neonates. Am J Clin Nutr 31(3):466–469

    Article  CAS  PubMed  Google Scholar 

  • Romano T, Wark JD, Owens JA, Wlodek ME (2009) Prenatal growth restriction and postnatal growth restriction followed by accelerated growth independently program reduced bone growth and strength. Bone 45(1):132–141

    Article  PubMed  Google Scholar 

  • Sahoo SK, Katam KK, Das V, Agarwal A, Bhatia V (2017) Maternal vitamin D supplementation in pregnancy and offspring outcomes: a double-blind randomized placebo-controlled trial. J Bone Miner Metab 35(4):464–471

    Article  CAS  PubMed  Google Scholar 

  • Steer CD, Tobias JH (2011) Insights into the programming of bone development from the Avon Longitudinal Study of Parents and Children (ALSPAC). Am J Clin Nutr 94(6 Suppl):1861s–1864s

    Article  CAS  PubMed  Google Scholar 

  • Tobias JH, Steer CD, Emmett PM, Tonkin RJ, Cooper C, Ness AR (2005) Bone mass in childhood is related to maternal diet in pregnancy. Osteoporos Int 16(12):1731–1741

    Article  CAS  PubMed  Google Scholar 

  • Vaziri F, Dabbaghmanesh MH, Samsami A, Nasiri S, Shirazi PT (2016) Vitamin D supplementation during pregnancy on infant anthropometric measurements and bone mass of mother-infant pairs: a randomized placebo clinical trial. Early Hum Dev 103:61–68

    Article  CAS  PubMed  Google Scholar 

  • Viljakainen HT, Saarnio E, Hytinantti T, Miettinen M, Surcel H, Makitie O et al (2010) Maternal vitamin D status determines bone variables in the newborn. J Clin Endocrinol Metab 95(4):1749–1757

    Article  CAS  PubMed  Google Scholar 

  • Viljakainen HT, Korhonen T, Hytinantti T, Laitinen EK, Andersson S, Makitie O et al (2011) Maternal vitamin D status affects bone growth in early childhood—a prospective cohort study. Osteoporos Int 22(3):883–891

    Article  CAS  PubMed  Google Scholar 

  • Villa CR, Chen J, Wen B, Sacco SM, Taibi A, Ward WE et al (2016) Maternal vitamin D beneficially programs metabolic, gut and bone health of mouse male offspring in an obesogenic environment. Int J Obes (Lond). 40(12):1875–1883

    Article  CAS  Google Scholar 

  • Weiler H, Fitzpatrick-Wong S, Veitch R, Kovacs H, Schellenberg J, McCloy U et al (2005) Vitamin D deficiency and whole-body and femur bone mass relative to weight in healthy newborns. CMAJ 172(6):757–761

    Article  PubMed  PubMed Central  Google Scholar 

  • Yakar S, Isaksson O (2016) Regulation of skeletal growth and mineral acquisition by the GH/IGF-1 axis: lessons from mouse models. Growth Horm IGF Res 28:26–42

    Article  CAS  PubMed  Google Scholar 

  • Yarbrough DE, Barrett-Connor E, Morton DJ (2000) Birth weight as a predictor of adult bone mass in postmenopausal women: the Rancho Bernardo Study. Osteoporos Int 11(7):626–630

    Article  CAS  PubMed  Google Scholar 

  • Yin J, Dwyer T, Riley M, Cochrane J, Jones G (2010) The association between maternal diet during pregnancy and bone mass of the children at age 16. Eur J Clin Nutr 64(2):131–137

    Article  CAS  PubMed  Google Scholar 

  • Young BE, McNanley TJ, Cooper EM, McIntyre AW, Witter F, Harris ZL et al (2012) Maternal vitamin D status and calcium intake interact to affect fetal skeletal growth in utero in pregnant adolescents. Am J Clin Nutr 95(5):1103–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young BE, Cooper EM, McIntyre AW, Kent T, Witter F, Harris ZL et al (2014) Placental vitamin D receptor (VDR) expression is related to neonatal vitamin D status, placental calcium transfer, and fetal bone length in pregnant adolescents. Faseb J 28(5):2029–2037

    Article  CAS  PubMed  Google Scholar 

  • Zhu K, Whitehouse AJ, Hart PH, Kusel M, Mountain J, Lye S et al (2014) Maternal vitamin D status during pregnancy and bone mass in offspring at 20 years of age: a prospective cohort study. J Bone Miner Res 29(5):1088–1095

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Elaine M. Dennison .

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Shere, C., Cooper, C., Dennison, E.M. (2019). The Developmental Origins of Osteoporosis. In: Vaiserman, A. (eds) Early Life Origins of Ageing and Longevity. Healthy Ageing and Longevity, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-24958-8_8

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