Archives of Osteoporosis

, 12:19 | Cite as

Relationships among diet, physical activity, and dual plane dual-energy X-ray absorptiometry bone outcomes in pre-pubertalgirls

  • Jie Ren
  • Lynn S. Brann
  • Kay S. Bruening
  • Tamara A. Scerpella
  • Jodi N. Dowthwaite
Original Article



In pre-pubertal girls, nutrient intakes and non-aquatic organized activity were evaluated as factors in vertebral body bone mass, structure, and strength. Activity, vitamin B12, and dietary fiber predicted bone outcomes most consistently. Exercise and vitamin B12 appear beneficial, whereas high fiber intake appears to be adverse for vertebral body development.


Childhood development sets the baseline for adult fracture risk. Most studies evaluate development using postero-anterior (pa) dual-energy X-ray absorptiometry (DXA) areal bone mineral density, bone mineral content, and bone mineral apparent density. In a prior analysis, we demonstrated that pa DXA reflects posterior element properties, rather than vertebral body fracture sites, such that loading is associated with subtle differences in vertebral body geometry, not 3D density. The current analysis is restricted to pre-pubertal girls, for a focused exploration of key nutrient intakes and physical activity as factors in dual plane indices of vertebral body geometry, density, and strength.


This cross-sectional analysis used paired pa and supine lateral (lat) lumbar spine DXA scans to assess “3D” vertebral body bone mineral apparent density (palatBMAD), “3D” index of structural strength in axial compression (palatIBS), and fracture risk index (palatFRI). Diet data were collected using the Youth/Adolescent Questionnaire (YAQ, 1995); organized physical activity was recorded via calendar-based form. Pearson correlations and backward stepwise multiple linear regression analyzed associations among key nutrients, physical activity, and bone outcomes.


After accounting for activity and key covariates, fiber, unsupplemented vitamin B12, zinc, carbohydrate, vitamin C, unsupplemented magnesium, and unsupplemented calcium intake explained significant variance for one or more bone outcomes (p < 0.05). After adjustment for influential key nutrients and covariates, activity exposure was associated with postero-anterior (PA) areal bone mineral density, pa bone mineral content, PA width, lateral (LAT) BMC, “3D” bone cross-sectional area (coronal plane), “3D” palatIBS, and palatFRI benefits (p < 0.05).


Physical activity, fiber intake, and unsupplemented B12 intake appear to influence vertebral body bone mass, density, geometry, and strength in well-nourished pre-pubertal girls; high fiber intakes may adversely affect childhood vertebral body growth.


Children Nutrition Exercise Female Bone geometry Bone density 



Dual-energy X-ray absorptiometry




Supine lateral


Paired pa and lat scan calculated results


Postero-anterior areal bone mineral density


Postero-anterior bone mineral content


Lateral bone mineral content


Lateral vertebral depth (out of pa scan plane)


Lateral vertebral body height


Postero-anterior width


“3D” bone cross-sectional area (coronal plane)


“3D” index of structural strength in axial compression


“3D” vertebral body bone mineral apparent density


palat fracture risk index



We acknowledge the assistance of the following individuals with data collection: Cathy Riley, Eileen Burd, Amy Allen, Tina Craig, and Kristy Kmack. This research was supported by NIAMS (R01 AR54145) and bridge funding from the University of Wisconsin (Department of Orthopedics and Rehabilitation, School of Medicine and Public Health).

Compliance with ethical standards

The study was approved by the Institutional Review Board of SUNY Upstate Medical University and complies with US bioethical legislation and the ethical standards of the Declaration of Helsinki. Written parental consent and child assent were obtained.

Conflicts of interest



  1. 1.
    Lippuner K, Johansson H, Kanis JA, Rizzoli R (2009 Jul) Remaining lifetime and absolute 10-year probabilities of osteoporotic fracture in Swiss men and women. Osteoporos Int 20(7):1131–1140PubMedCrossRefGoogle Scholar
  2. 2.
    Huncharek M, Muscat J, Kupelnick B (2008 Aug) Impact of dairy products and dietary calcium on bone-mineral content in children: results of a meta-analysis. Bone 43(2):312–321PubMedCrossRefGoogle Scholar
  3. 3.
    Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA (2010 Feb) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46(2):294–305PubMedCrossRefGoogle Scholar
  4. 4.
    Greene DA, Naughton GA, Bradshaw E, Moresi M, Ducher G (2012 Sep) Mechanical loading with or without weight-bearing activity: influence on bone strength index in elite female adolescent athletes engaged in water polo, gymnastics, and track-and-field. J Bone Miner Metab 30(5):580–587PubMedCrossRefGoogle Scholar
  5. 5.
    Levis S, Lagari VS (2012 Dec) The role of diet in osteoporosis prevention and management. Curr Osteoporos Rep 10(4):296–302PubMedCrossRefGoogle Scholar
  6. 6.
    Handel MN, Heitmann BL, Abrahamsen B (2015 Nov) Nutrient and food intakes in early life and risk of childhood fractures: a systematic review and meta-analysis. Am J Clin Nutr 102(5):1182–1195PubMedCrossRefGoogle Scholar
  7. 7.
    Laudermilk MJ, Manore MM, Thomson CA, Houtkooper LB, Farr JN, Going SB (2012 Dec) Vitamin C and zinc intakes are related to bone macroarchitectural structure and strength in prepubescent girls. Calcif Tissue Int 91(6):430–439PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Bergman C, Gray-Scott D, Chen JJ, Meacham S (2009 Feb) What is next for the dietary reference intakes for bone metabolism related nutrients beyond calcium: phosphorus, magnesium, vitamin D, and fluoride? Crit Rev Food Sci Nutr 49(2):136–144PubMedCrossRefGoogle Scholar
  9. 9.
    van Wijngaarden JP, Doets EL, Szczecinska A, Souverein OW, Duffy ME, Dullemeijer C, Cavelaars AE, Pietruszka B, Van't Veer P, Brzozowska A, Dhonukshe-Rutten RA, de Groot CP (2013) Vitamin B12, folate, homocysteine, and bone health in adults and elderly people: a systematic review with meta-analyses. J Nutr Metab 2013:486186PubMedPubMedCentralGoogle Scholar
  10. 10.
    Fratoni V, Brandi ML (2015 Mar 30) B vitamins, homocysteine and bone health. Nutrients 7(4):2176–2192PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Dowthwaite JN, Scerpella TA (2009 Oct-Dec) Skeletal geometry and indices of bone strength in artistic gymnasts. J Musculoskelet Neuronal Interact 9(4):198–214PubMedPubMedCentralGoogle Scholar
  12. 12.
    Dowthwaite JN, Rosenbaum PF, Scerpella TA (2012 May) Site-specific advantages in skeletal geometry and strength at the proximal femur and forearm in young female gymnasts. Bone 50(5):1173–1183PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Dowthwaite JN, Scerpella TA (2011 Jan) Distal radius geometry and skeletal strength indices after peripubertal artistic gymnastics. Osteoporos Int 22(1):207–216PubMedCrossRefGoogle Scholar
  14. 14.
    Dowthwaite JN, Rosenbaum PF, Scerpella TA (2011 Nov) Mechanical loading during growth is associated with plane-specific differences in vertebral geometry: a cross-sectional analysis comparing artistic gymnasts vs. non-gymnasts. Bone 49(5):1046–1054PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Dowthwaite JN, Flowers PP, Scerpella TA (2011 Jun) Agreement between pQCT- and DXA-derived indices of bone geometry, density, and theoretical strength in females of varying age, maturity, and physical activity. J Bone Miner Res 26(6):1349–1357PubMedCrossRefGoogle Scholar
  16. 16.
    Mazess RB, Barden HS, Bisek JP, Hanson J (1990 Jun) Dual-energy x-ray absorptiometry for total-body and regional bone-mineral and soft-tissue composition. Am J Clin Nutr 51(6):1106–1112PubMedCrossRefGoogle Scholar
  17. 17.
    Leonard MB, Shults J, Zemel BS (2006 Jul-Sep) DXA estimates of vertebral volumetric bone mineral density in children: potential advantages of paired posteroanterior and lateral scans. J Clin Densitom 9(3):265–273PubMedCrossRefGoogle Scholar
  18. 18.
    Scerpella TA, Davenport M, Morganti CM, Kanaley JA, Johnson LM (2003 Jan) Dose related association of impact activity and bone mineral density in pre-pubertal girls. Calcif Tissue Int 72(1):24–31PubMedCrossRefGoogle Scholar
  19. 19.
    Centers for Disease Control and Prevention. Clinical Growth Charts. 2 to 20 years: Girls Body mass index-forage percentiles. [Internet]. Centers for Disease Control and Prevention Published May 2000. Revised October 16, 2000. [revised CDC Growth Charts; cited Accessed May 10, 2014.]. Available from: English.
  20. 20.
    Duke PM, Litt IF, Gross RT (1980 Dec) Adolescents’ self-assessment of sexual maturation. Pediatrics 66(6):918–920PubMedGoogle Scholar
  21. 21.
    Rockett HR, Breitenbach M, Frazier AL, Witschi J, Wolf AM, Field AE, Colditz GA (1997 Nov-Dec) Validation of a youth/adolescent food frequency questionnaire. Prev Med 26(6):808–816PubMedCrossRefGoogle Scholar
  22. 22.
    Dietary Reference Intakes (DRIs): Estimated Average Requirements Food and Nutrition Board, Institute of Medicine, National Academies. [Internet]. Institute of Medicine cited Accessed 7/5/16]. Available from:
  23. 23.
    Walther B, Karl JP, Booth SL, Boyaval P (2013 Jul 1) Menaquinones, bacteria, and the food supply: the relevance of dairy and fermented food products to vitamin K requirements. Adv Nutr 4(4):463–473PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Rupich RC, Griffin MG, Pacifici R, Avioli LV, Susman N (1992 Jan) Lateral dual-energy radiography: artifact error from rib and pelvic bone. J Bone Miner Res 7(1):97–101PubMedCrossRefGoogle Scholar
  25. 25.
    Valdimarsson O, Linden C, Johnell O, Gardsell P, Karlsson MK (2006 Feb) Daily physical education in the school curriculum in prepubertal girls during 1 year is followed by an increase in bone mineral accrual and bone width—data from the prospective controlled Malmo pediatric osteoporosis prevention study. Calcif Tissue Int 78(2):65–71PubMedCrossRefGoogle Scholar
  26. 26.
    Duan Y, Parfitt A, Seeman E (1999 Oct) Vertebral bone mass, size, and volumetric density in women with spinal fractures. J Bone Miner Res 14(10):1796–1802PubMedCrossRefGoogle Scholar
  27. 27.
    Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003 Jul 24) Bone loss and bone size after menopause. N Engl J Med 349(4):327–334PubMedCrossRefGoogle Scholar
  28. 28.
    Lofgren B, Detter F, Dencker M, Stenevi-Lundgren S, Nilsson JA, Karlsson MK (2011 Aug) Influence of a 3-year exercise intervention program on fracture risk, bone mass, and bone size in prepubertal children. J Bone Miner Res 26(8):1740–1747PubMedCrossRefGoogle Scholar
  29. 29.
    Barron E, Cano Sokoloff N, Maffazioli GD, Ackerman KE, Woolley R, Holmes TM, Anderson EJ, Misra M (2016 Mar) Diets high in fiber and vegetable protein are associated with low lumbar bone mineral density in young athletes with oligoamenorrhea. J Acad Nutr Diet 116(3):481–489PubMedCrossRefGoogle Scholar
  30. 30.
    Wolf RL, Cauley JA, Baker CE, Ferrell RE, Charron M, Caggiula AW, Salamone LM, Heaney RP, Kuller LH (2000 Aug) Factors associated with calcium absorption efficiency in pre- and perimenopausal women. Am J Clin Nutr 72(2):466–471PubMedGoogle Scholar
  31. 31.
    Baer DJ, Rumpler WV, Miles CW, Fahey GC Jr (1997 Apr) Dietary fiber decreases the metabolizable energy content and nutrient digestibility of mixed diets fed to humans. J Nutr 127(4):579–586PubMedGoogle Scholar
  32. 32.
    Adlercreutz H (1990) Diet, breast cancer, and sex hormone metabolism. Ann N Y Acad Sci 595:281–290PubMedCrossRefGoogle Scholar
  33. 33.
    Gaskins AJ, Mumford SL, Zhang C, Wactawski-Wende J, Hovey KM, Whitcomb BW, Howards PP, Perkins NJ, Yeung E, Schisterman EF, BioCycle Study Group (2009 Oct) Effect of daily fiber intake on reproductive function: the BioCycle study. Am J Clin Nutr 90(4):1061–1069PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Carmel R, Lau KH, Baylink DJ, Saxena S, Singer FR (1988 Jul 14) Cobalamin and osteoblast-specific proteins. N Engl J Med 319(2):70–75PubMedCrossRefGoogle Scholar
  35. 35.
    Dhonukshe-Rutten RA, van Dusseldorp M, Schneede J, de Groot LC, van Staveren WA (2005 Sep) Low bone mineral density and bone mineral content are associated with low cobalamin status in adolescents. Eur J Nutr 44(6):341–347PubMedCrossRefGoogle Scholar
  36. 36.
    Dhonukshe-Rutten RA, Lips M, de Jong N, Chin A, Paw MJ, Hiddink GJ, van Dusseldorp M, De Groot LC, van Staveren WA (2003 Mar) Vitamin B-12 status is associated with bone mineral content and bone mineral density in frail elderly women but not in men. J Nutr 133(3):801–807PubMedGoogle Scholar
  37. 37.
    McLean RR, Jacques PF, Selhub J, Tucker KL, Samelson EJ, Broe KE, Hannan MT, Cupples LA, Kiel DP (2004 May 13) Homocysteine as a predictive factor for hip fracture in older persons. N Engl J Med 350(20):2042–2049PubMedCrossRefGoogle Scholar
  38. 38.
    Dwyer J, Nahin RL, Rogers GT, Barnes PM, Jacques PM, Sempos CT, Bailey R (2013 Jun) Prevalence and predictors of children's dietary supplement use: the 2007 national health interview survey. Am J Clin Nutr 97(6):1331–1337PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    National Institutes of Health. Health Information. Vitamin D fact sheet for health professionals. [Internet]. National Institutes of Health. Reviewed November 10, 2014. [revised NIH website.; cited Accessed May 10, 2014]. Available from:
  40. 40.
    Bailey RL, Dodd KW, Goldman JA, Gahche JJ, Dwyer JT, Moshfegh AJ, Sempos CT, Picciano MF (2010 Apr) Estimation of total usual calcium and vitamin D intakes in the United States. J Nutr 140(4):817–822PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Cheng S, Tylavsky F, Kroger H, Karkkainen M, Lyytikainen A, Koistinen A, Mahonen A, Alen M, Halleen J, Vaananen K, Lamberg-Allardt C (2003 Sep) Association of low 25-hydroxyvitamin D concentrations with elevated parathyroid hormone concentrations and low cortical bone density in early pubertal and prepubertal Finnish girls. Am J Clin Nutr 78(3):485–492PubMedGoogle Scholar
  42. 42.
    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 Nov) 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(5) 1115,26; quiz 1147-8Google Scholar
  43. 43.
    Hind K, Burrows M (2007 Jan) Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials. Bone 40(1):14–27PubMedCrossRefGoogle Scholar
  44. 44.
    Merrilees MJ, Smart EJ, Gilchrist NL, Frampton C, Turner JG, Hooke E, March RL, Maguire P (2000 Dec) Effects of diary food supplements on bone mineral density in teenage girls. Eur J Nutr 39(6):256–262PubMedCrossRefGoogle Scholar
  45. 45.
    2008 Physical Activity Guidelines for Americans [Internet]. Office of Disease Prevention and Health Promotion October 18, 2016 [revised 45. Physical Activity Guidelines; cited Accessed October 18, 2016.]. Available from:

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2017

Authors and Affiliations

  • Jie Ren
    • 1
  • Lynn S. Brann
    • 2
  • Kay S. Bruening
    • 2
  • Tamara A. Scerpella
    • 3
  • Jodi N. Dowthwaite
    • 4
  1. 1.Nutrition Science and Dietetics ProgramSyracuse UniversitySunnyvaleUSA
  2. 2.Nutrition Science and Dietetics ProgramSyracuse UniversitySyracuseUSA
  3. 3.Department of Orthopedics and RehabilitationUniversity of Wisconsin-MadisonMadisonUSA
  4. 4.Department of Orthopedic SurgeryUpstate Medical UniversitySyracuseUSA

Personalised recommendations