Skip to main content

Advertisement

Log in

Prevalence of vitamin D insufficiency among adolescents and its correlation with bone parameters using high-resolution peripheral quantitative computed tomography

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

Vitamin D deficiency and insufficiency are highly prevalent among adolescents in Hong Kong, which is a sub-tropical city with ample sunshine. Vitamin D level is significantly correlated with key bone density and bone quality parameters. Further interventional studies are warranted to define the role of vitamin D supplementation for improvement of bone health among adolescents.

Introduction

The relationship between bone quality parameters and vitamin D (Vit-D) status remains undefined among adolescents. The aims of this study were to evaluate Vit-D status and its association with both bone density and bone quality parameters among adolescents.

Methods

Three hundred thirty-three girls and 230 boys (12–16 years old) with normal health were recruited in summer and winter separately from local schools. Serum 25(OH) Vit-D level, bone density and quality parameters by Dual Energy X-ray Absorptiometry (DXA) and High-Resolution peripheral Quantitative Computed Tomography (HR-pQCT), dietary calcium intake, and physical activity level were assessed.

Results

Sixty-four point seven percent and 11.4 % of subjects were insufficient [25 ≤ 25(OH)Vit-D ≤ 50 nmol/L] and deficient [25(OH)Vit-D < 25 nmol/L] in Vit-D, respectively. The mean level of serum 25(OH)Vit-D in summer was significantly higher than that in winter (44.7 ± 13.6 and 35.9 ± 12.6 nmol/L, respectively) without obvious gender difference. In girls, areal bone mineral density (aBMD) and bone mineral content (BMC) of bilateral femoral necks, cortical area, cortical thickness, total volumetric bone mineral density (vBMD), and trabecular thickness were significantly correlated with 25(OH)Vit-D levels. In boys, aBMD of bilateral femoral necks, BMC of the dominant femoral neck, cortical area, cortical thickness, total vBMD, trabecular vBMD, BV/TV, and trabecular separation were significantly correlated with 25(OH)Vit-D levels.

Conclusion

Vit-D insufficiency was highly prevalent among adolescents in Hong Kong with significant correlation between Vit-D levels and key bone density and bone quality parameters being detected in this study. Given that this is a cross-sectional study and causality relationship cannot be inferred, further interventional studies investigating the role of Vit-D supplementation on improving bone health among adolescents are warranted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

25(OH)Vit-D:

25-Hydroxy-vitamin D

aBMD:

Areal bone mineral density

BMC:

Bone mineral content

BMD:

Bone mineral density

BV/TV:

Bone volume-to-tissue volume ratio

Ca:

Calcium

CV:

Coefficient of variation

CtAr:

Cortical area

CtPm:

Cortical perimeter

CtTh:

Cortical thickness

Dcort:

Cortical volumetric bone mineral density

Dtrab:

Trabecular volumetric bone mineral density

Dtot:

Total volumetric bone mineral density

FFQ:

Food Frequency Questionnaire

HR-pQCT:

High-Resolution peripheral Quantitative Computed Tomography

pQCT:

Peripheral Quantitative Computed Tomography

PTH:

Parathyroid hormone

ROI:

Region of interest

SD:

Standard deviation

TbAr:

Trabecular area

TbN:

Trabeculae number

TbSp:

Trabecular separation

TbTh:

Trabecular thickness

vBMD:

Volumetric bone mineral density

Vit-D:

Vitamin D

References

  1. Holick MF (2007) Vitamin D deficiency. N Engl J Med 357(3):266–281. doi:10.1056/NEJMra070553

    Article  CAS  PubMed  Google Scholar 

  2. Lynn HS, Lau EM, Au B, Leung PC (2005) Bone mineral density reference norms for Hong Kong Chinese. Osteoporos Int 16(12):1663–1668. doi:10.1007/s00198-005-1899-z

    Article  CAS  PubMed  Google Scholar 

  3. Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46(2):294–305. doi:10.1016/j.bone.2009.10.005

    Article  PubMed  Google Scholar 

  4. Mithal A, Wahl DA, Bonjour JP, Burckhardt P, Dawson-Hughes B, Eisman JA, El-Hajj Fuleihan G, Josse RG, Lips P, Morales-Torres J (2009) Global vitamin D status and determinants of hypovitaminosis D. Osteoporos Int 20(11):1807–1820

    Article  CAS  PubMed  Google Scholar 

  5. Outila TA, Karkkainen MU, Lamberg-Allardt CJ (2001) Vitamin D status affects serum parathyroid hormone concentrations during winter in female adolescents: associations with forearm bone mineral density. Am J Clin Nutr 74(2):206–210

    CAS  PubMed  Google Scholar 

  6. Ganji V, Zhang X, Tangpricha V (2012) Serum 25-hydroxyvitamin D concentrations and prevalence estimates of hypovitaminosis D in the U.S. population based on assay-adjusted data. J Nutr 142(3):498–507. doi:10.3945/jn.111.151977

    Article  CAS  PubMed  Google Scholar 

  7. Zhu ZW, Zhan JY, Shao J, Chen WJ, Chen LQ, Li WH, Ji C, Zhao ZY (2012) High prevalence of vitamin D deficiency among children aged 1 month to 16 years in Hangzhou, China. BMC Public Health 12, 126. doi:10.1186/1471-2458-12-126

    Article  PubMed  PubMed Central  Google Scholar 

  8. Foo LH, Zhang Q, Zhu K, Ma G, Trube A, Greenfield H, Fraser DR (2009) Relationship between vitamin D status, body composition and physical exercise of adolescent girls in Beijing. Osteoporos Int 20(3):417–425. doi:10.1007/s00198-008-0667-2

    Article  CAS  PubMed  Google Scholar 

  9. Kim MS, Kong YH, Lee DY (2015) 25-Hydroxy vitamin D status in healthy Korean school children and adolescents: striking difference in prevalence of vitamin D deficiency with school grade and season. HK J Paediatr (new series) 20:3–9

    Google Scholar 

  10. Norman AW, Bouillon R (2010) Vitamin D nutritional policy needs a vision for the future. Exp Biol Med 235(9):1034–1045

    Article  CAS  Google Scholar 

  11. Hollis BW (2005) Circulating 25-hydroxyvitamin D levels indicative of vitamin D sufficiency: implications for establishing a new effective dietary intake recommendation for vitamin D. J Nutr 135(2):317–322

    CAS  PubMed  Google Scholar 

  12. Busse B, Bale HA, Zimmermann EA, Panganiban B, Barth HD, Carriero A, Vettorazzi E, Zustin J, Hahn M, Ager JW III, Puschel K, Amling M, Ritchie RO (2013) Vitamin D deficiency induces early signs of aging in human bone, increasing the risk of fracture. Sci Transl Med 5(193), 193ra188. doi:10.1126/scitranslmed.3006286

    Article  Google Scholar 

  13. Malabanan A, Veronikis IE, Holick MF (1998) Redefining vitamin D insufficiency. Lancet 351(9105):805–806

    Article  CAS  PubMed  Google Scholar 

  14. Paxton GA, Teale GR, Nowson CA, Mason RS, McGrath JJ, Thompson MJ, Siafarikas A, Rodda CP, Munns CF (2013) Vitamin D and health in pregnancy, infants, children and adolescents in Australia and New Zealand: a position statement. Med J Aust 198(3):142–143

    Article  PubMed  Google Scholar 

  15. Cheng S, Tylavsky F, Kroger H, Karkkainen M, Lyytikainen A, Koistinen A, Mahonen A, Alen M, Halleen J, Vaananen K, Lamberg-Allardt C (2003) 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):485–492

    CAS  PubMed  Google Scholar 

  16. Vinkhuyzen AA, Eyles DW, Burne TH, Blanken LM, Kruithof CJ, Verhulst F, Jaddoe VW, Tiemeier H, McGrath JJ (2015) Prevalence and predictors of vitamin D deficiency based on maternal mid-gestation and neonatal cord bloods: The Generation R Study. J Steroid Biochem Mol Biol. doi:10.1016/j.jsbmb.2015.09.018

    PubMed  Google Scholar 

  17. Lips P, van Schoor NM, de Jongh RT (2014) Diet, sun, and lifestyle as determinants of vitamin D status. Ann N Y Acad Sci 1317:92–98. doi:10.1111/nyas.12443

    Article  CAS  PubMed  Google Scholar 

  18. Institute of Medicine (2011) In: Ross AC, Taylor CL, Yaktine AL, Del Valle HB (eds) Dietary reference intakes for calcium and vitamin D. The National Academies Collection: Reports funded by National Institutes of Health, Washington (DC)

    Google Scholar 

  19. Food and Nutrition Board (1997) Dietary reference intakes for calcium, magnesium, phosphorus, vitamin D, and fluoride. National Academy Press, Institute of Medicine, Washington DC, pp 250–287

    Google Scholar 

  20. Mouratidou T, Vicente-Rodriguez G, Gracia-Marco L, Huybrechts I, Sioen I, Widhalm K, Valtuena J, Gonzalez-Gross M, Moreno LA (2013) Associations of dietary calcium, vitamin D, milk intakes, and 25-hydroxyvitamin D with bone mass in Spanish adolescents: the HELENA study. J Clin Densitom 16(1):110–117. doi:10.1016/j.jocd.2012.07.008

    Article  PubMed  Google Scholar 

  21. Lee EY, Kim D, Kim KM, Kim KJ, Choi HS, Rhee Y, Lim SK (2012) Age-related bone mineral density patterns in Koreans (KNHANES IV). J Clin Endocrinol Metab 97(9):3310–3318. doi:10.1210/jc.2012-1488

    Article  CAS  PubMed  Google Scholar 

  22. Pekkinen M, Viljakainen H, Saarnio E, Lamberg-Allardt C, Makitie O (2012) Vitamin D is a major determinant of bone mineral density at school age. PLoS One 7(7), e40090. doi:10.1371/journal.pone.0040090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Esterle L, Nguyen M, Walrant-Debray O, Sabatier JP, Garabedian M (2010) Adverse interaction of low-calcium diet and low 25(OH)D levels on lumbar spine mineralization in late-pubertal girls. J Bone Miner Res 25(11):2392–2398. doi:10.1002/jbmr.134

    Article  CAS  PubMed  Google Scholar 

  24. Bacchetta J, Boutroy S, Vilayphiou N, Ranchin B, Fouque-Aubert A, Basmaison O, Cochat P (2011) Bone assessment in children with chronic kidney disease: data from two new bone imaging techniques in a single-center pilot study. Pediatr Nephrol 26(4):587–595. doi:10.1007/s00467-010-1745-1

    Article  PubMed  Google Scholar 

  25. Weber LT, Mehls O (2010) Limitations of dual x-ray absorptiometry in children with chronic kidney disease. Pediatr Nephrol 25(1):3–5. doi:10.1007/s00467-009-1248-0

    Article  PubMed  Google Scholar 

  26. Geusens P, Chapurlat R, Schett G, Ghasem-Zadeh A, Seeman E, de Jong J, van den Bergh J (2014) High-resolution in vivo imaging of bone and joints: a window to microarchitecture. Nat Rev Rheumatol 10(5):304–313. doi:10.1038/nrrheum.2014.23

    Article  PubMed  Google Scholar 

  27. Marshell WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44(235):291–303

    Article  Google Scholar 

  28. Marshell WA, Tanner JM (1970) Variations in the pattern of pubertal changes in boys. Arch Dis Child 45(239):13–23

    Article  Google Scholar 

  29. Hung VW, Qin L, Cheung CS, Lam TP, Ng BK, Tse YK, Guo X, Lee KM, Cheng JC (2005) Osteopenia: a new prognostic factor of curve progression in adolescent idiopathic scoliosis. J Bone Joint Surg 87(12):2709–2716

    Article  CAS  PubMed  Google Scholar 

  30. Burrows M, Liu D, McKay H (2010) High-resolution peripheral QCT imaging of bone micro-structure in adolescents. Osteoporos Int 21(3):515–520. doi:10.1007/s00198-009-0913-2

    Article  CAS  PubMed  Google Scholar 

  31. Burrows M, Liu D, Perdios A, Moore S, Mulpuri K, McKay H (2010) Assessing bone microstructure at the distal radius in children and adolescents using HR-pQCT: a methodological pilot study. J Clin Densitom 13(4):451–455. doi:10.1016/j.jocd.2010.02.003

    Article  PubMed  Google Scholar 

  32. Yu WS, Chan KY, Yu FW, Yeung HY, Ng BK, Lee KM, Lam TP, Cheng JC (2013) Abnormal bone quality versus low bone mineral density in adolescent idiopathic scoliosis: a case-control study with in vivo high-resolution peripheral quantitative computed tomography. Spine J 13(11):1493–1499. doi:10.1016/j.spinee.2013.05.018

    Article  PubMed  Google Scholar 

  33. Paggiosi MA, Eastell R, Walsh JS (2014) Precision of high-resolution peripheral quantitative computed tomography measurement variables: influence of gender, examination site, and age. Calcif Tissue Int 94(2):191–201. doi:10.1007/s00223-013-9798-3

    Article  CAS  PubMed  Google Scholar 

  34. Farr JN, Amin S, Melton LJ 3rd, Kirmani S, McCready LK, Atkinson EJ, Muller R, Khosla S (2014) Bone strength and structural deficits in children and adolescents with a distal forearm fracture resulting from mild trauma. J Bone Miner Res 29(3):590–599. doi:10.1002/jbmr.2071

    Article  PubMed  PubMed Central  Google Scholar 

  35. Burt LA, Macdonald HM, Hanley DA, Boyd SK (2014) Bone microarchitecture and strength of the radius and tibia in a reference population of young adults: an HR-pQCT study. Arch Osteoporos 9:183. doi:10.1007/s11657-014-0183-2

    Article  PubMed  Google Scholar 

  36. Kim S, Macdonald HM, Nettlefold L, McKay HA (2013) A comparison of bone quality at the distal radius between Asian and white adolescents and young adults: an HR-pQCT study. J Bone Miner Res 28(9):2035–2042. doi:10.1002/jbmr.1939

    Article  PubMed  Google Scholar 

  37. Wang Q, Ghasem-Zadeh A, Wang XF, Iuliano-Burns S, Seeman E (2011) Trabecular bone of growth plate origin influences both trabecular and cortical morphology in adulthood. J Bone Miner Res 26(7):1577–1583. doi:10.1002/jbmr.360

    Article  PubMed  Google Scholar 

  38. Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, Klibanski A, Bouxsein M, Misra M (2012) Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone 51(4):680–687. doi:10.1016/j.bone.2012.07.019

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ 3rd, Riggs BL, Amin S, Muller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24(6):1033–1042

    Article  PubMed  Google Scholar 

  40. Yu WS, Chan KY, Yu FW, Ng BK, Lee KM, Qin L, Lam TP, Cheng JC (2014) Bone structural and mechanical indices in adolescent idiopathic scoliosis evaluated by high-resolution peripheral quantitative computed tomography (HR-pQCT). Bone 61:109–115. doi:10.1016/j.bone.2013.12.033

    Article  PubMed  Google Scholar 

  41. Laib A, Hauselmann HJ, Ruegsegger P (1998) In vivo high resolution 3D-QCT of the human forearm. Technol Health Care 6(5–6):329–337

    CAS  PubMed  Google Scholar 

  42. MacNeil JA, Boyd SK (2007) Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 29(10):1096–1105. doi:10.1016/j.medengphy.2006.11.002

    Article  PubMed  Google Scholar 

  43. Laib A, Ruegsegger P (1999) Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-micron-resolution microcomputed tomography. Bone 24(1):35–39

    Article  CAS  PubMed  Google Scholar 

  44. Ong L, Saw S, Sahabdeen NB, Tey KT, Ho CS, Sethi SK (2012) Current 25-hydroxyvitamin D assays: do they pass the test? Clin Chim Acta 413(13–14):1127–1134. doi:10.1016/j.cca.2012.03.009

    Article  CAS  PubMed  Google Scholar 

  45. Leung SSF, Ho SC, Woo J, Lam TH, Janus ED (1997) Hong Kong adult dietary survey 1995. Department of Paediatrics, The Chinese University of Hong Kong, Hong Kong

    Google Scholar 

  46. Woo J, Leung SSF, Ho SC, Lam TH, Janus ED (1997) A food frequency questionnaire for use in the Chinese population in Hong Kong: description and examination of validity. Nutr Res 17(11–12):1633–1641. doi:10.1016/S0271-5317(97)00170-X

    Article  CAS  Google Scholar 

  47. Institute of Nutrition and Food Safety (2002) China food composition. Peking University Medical Press, People's Republic of China

    Google Scholar 

  48. Pols MA, Peeters PH, Bueno-De-Mesquita HB, Ocke MC, Wentink CA, Kemper HC, Collette HJ (1995) Validity and repeatability of a modified Baecke questionnaire on physical activity. Int J Epidemiol 24(2):381–388

    Article  CAS  PubMed  Google Scholar 

  49. Xu C, Perera RA, Chan YH, Fang VJ, Ng S, Ip DK, Kam AM, Leung GM, Peiris JS, Cowling BJ (2015) Determinants of serum 25-hydroxyvitamin D in Hong Kong. The British journal of Nutrition:1–8. doi:10.1017/S0007114515001683

  50. Hong Kong Government (2015) Student Health Service: health information on “Facts about calcium”. http://www.studenthealth.gov.hk/english/health/health_dn/health_dn_ckhm.html. Accessed 29 November 2015.

  51. Jang H, Koo FK, Ke L, Clemson L, Cant R, Fraser DR, Seibel MJ, Tseng M, Mpofu E, Mason RS, Brock K (2013) Culture and sun exposure in immigrant East Asian women living in Australia. Women Health 53(5):504–518. doi:10.1080/03630242.2013.806386

    Article  PubMed  Google Scholar 

  52. Kung AW, Lee KK (2006) Knowledge of vitamin D and perceptions and attitudes toward sunlight among Chinese middle-aged and elderly women: a population survey in Hong Kong. BMC Public Health 6:226

    Article  PubMed  PubMed Central  Google Scholar 

  53. Voortman T, van den Hooven EH, Heijboer AC, Hofman A, Jaddoe VW, Franco OH (2015) Vitamin d deficiency in school-age children is associated with sociodemographic and lifestyle factors. J Nutr 145(4):791–798. doi:10.3945/jn.114.208280

    Article  CAS  PubMed  Google Scholar 

  54. Wong BY, Cerin E, Ho SY, Mak KK, Lo WS, Lam TH (2010) Adolescents’ physical activity: competition between perceived neighborhood sport facilities and home media resources. Int J Pediatr Obes 5(2):169–176. doi:10.3109/17477160903159432

    Article  PubMed  Google Scholar 

  55. Miller KK, Meenaghan E, Lawson EA, Misra M, Gleysteen S, Schoenfeld D, Herzog D, Klibanski A (2011) Effects of risedronate and low-dose transdermal testosterone on bone mineral density in women with anorexia nervosa: a randomized, placebo-controlled study. J Clin Endocrinol Metab 96(7):2081–2088. doi:10.1210/jc.2011-0380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lam TP, Ng BK, Cheung LW, Lee KM, Qin L, Cheng JC (2013) Effect of whole body vibration (WBV) therapy on bone density and bone quality in osteopenic girls with adolescent idiopathic scoliosis: a randomized, controlled trial. Osteoporos Int 24(5):1623–1636. doi:10.1007/s00198-012-2144-1

    Article  CAS  PubMed  Google Scholar 

  57. Cashman KD, Hill TR, Cotter AA, Boreham CA, Dubitzky W, Murray L, Strain J, Flynn A, Robson PJ, Wallace JM, Kiely M (2008) Low vitamin D status adversely affects bone health parameters in adolescents. Am J Clin Nutr 87(4):1039–1044

    CAS  PubMed  Google Scholar 

  58. Nakamura K, Nashimoto M, Matsuyama S, Yamamoto M (2001) Low serum concentrations of 25-hydroxyvitamin D in young adult Japanese women: a cross sectional study. Nutrition 17(11–12):921–925

    Article  CAS  PubMed  Google Scholar 

  59. Wang Q, Wang XF, Iuliano-Burns S, Ghasem-Zadeh A, Zebaze R, Seeman E (2010) Rapid growth produces transient cortical weakness: a risk factor for metaphyseal fractures during puberty. J Bone Miner Res 25(7):1521–1526. doi:10.1002/jbmr.46

    Article  PubMed  Google Scholar 

  60. Li CY, Jee WS, Chen JL, Mo A, Setterberg RB, Su M, Tian XY, Ling YF, Yao W (2003) Estrogen and “exercise” have a synergistic effect in preventing bone loss in the lumbar vertebra and femoral neck of the ovariectomized rat. Calcif Tissue Int 72(1):42–49. doi:10.1007/s00223-001-1086-y

    Article  CAS  PubMed  Google Scholar 

  61. Chaitou A, Boutroy S, Vilayphiou N, Varennes A, Richard M, Blaizot S, Munoz F, Delmas PD, Goudable J, Chapurlat R, Szulc P (2011) Association of bone microarchitecture with parathyroid hormone concentration and calcium intake in men: the STRAMBO study. Eur J Endocrinol 165(1):151–159. doi:10.1530/EJE-11-0184

    Article  CAS  PubMed  Google Scholar 

  62. Zebaze R, Seeman E (2015) Cortical bone: a challenging geography. J Bone Miner Res 30(1):24–29. doi:10.1002/jbmr.2419

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The project was supported by General Research Fund, Research Grants Council of Hong Kong Special Administrative Region (Project number: 468411, 468809). The funding body has no role in design of study, data collection and analysis, manuscript preparation, or decision to publish.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. P. Lam.

Ethics declarations

Ethical approval was obtained from the University and Hospital Clinical Research Ethics Committee. The study complied with the Declaration of Helsinki strictly. Detailed explanation of the study protocol was given in the presence of legal guardians. Written informed consents were obtained from all subjects and their legal guardians before examinations and measurements were conducted.

Conflicts of interest

Tsz Ping Lam received research funding from Pfizer. Jack Chun Yiu Cheng, Gary Wing Kin Wong, Suzanne Suet Ying Ho, Ling Qin, Kwong Man Lee, Bobby Kin Wah Ng, Tracy Yaner Zhu, Chung Shun Ho, Vivian Wing Yin Hung, Fiona Wai Ping Yu, Ka Yee Cheuk, and Tsz Fung Cheung declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheung, T.F., Cheuk, K.Y., Yu, F.W.P. et al. Prevalence of vitamin D insufficiency among adolescents and its correlation with bone parameters using high-resolution peripheral quantitative computed tomography. Osteoporos Int 27, 2477–2488 (2016). https://doi.org/10.1007/s00198-016-3552-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-016-3552-4

Keywords

Navigation