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.
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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
Holick MF (2007) Vitamin D deficiency. N Engl J Med 357(3):266–281. doi:10.1056/NEJMra070553
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
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
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
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
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
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
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
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
Norman AW, Bouillon R (2010) Vitamin D nutritional policy needs a vision for the future. Exp Biol Med 235(9):1034–1045
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
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
Malabanan A, Veronikis IE, Holick MF (1998) Redefining vitamin D insufficiency. Lancet 351(9105):805–806
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
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
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
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
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)
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
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
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
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
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
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
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
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
Marshell WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44(235):291–303
Marshell WA, Tanner JM (1970) Variations in the pattern of pubertal changes in boys. Arch Dis Child 45(239):13–23
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Institute of Nutrition and Food Safety (2002) China food composition. Peking University Medical Press, People's Republic of China
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
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
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.
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
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
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
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
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
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
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
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
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
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
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
Zebaze R, Seeman E (2015) Cortical bone: a challenging geography. J Bone Miner Res 30(1):24–29. doi:10.1002/jbmr.2419
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.
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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.
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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
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DOI: https://doi.org/10.1007/s00198-016-3552-4