Skip to main content
SpringerLink
Log in

Association between vitamin D status and serum parathyroid hormone concentration and calcaneal stiffness in Japanese adolescents: sex differences in susceptibility to vitamin D deficiency

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

There is currently insufficient information on serum 25-hydroxyvitamin D (25OHD) and parathyroid hormone (PTH) concentrations, and bone mineral status in healthy adolescents to allow reference values to be set. This study aimed to provide comparable data on vitamin D status in Japanese adolescents and to assess sex differences in susceptibility to vitamin D insufficiency. Serum 25OHD and PTH concentrations were measured in 1,380 healthy adolescents (aged 12–18 years). Subjects completed a questionnaire on exercise history, diet, and lifestyle factors. Calcaneal stiffness was evaluated by quantitative ultrasound. Serum 25OHD concentrations in boys and girls were 60.8 ± 18.3 and 52.8 ± 17.0 nmol/L, respectively. Approximately 30 % of boys and 47 % of girls had suboptimal 25OHD concentrations (<50 nmol/L). Serum PTH concentration was negatively correlated with serum 25OHD concentration in boys, but negatively correlated with calcium intake rather than serum 25OHD in girls. In contrast, the increment in calcaneal stiffness as a result of elevation of serum 25OHD was higher in girls than in boys. As vitamin D deficiency is common in Japanese adolescents, it was estimated that intakes of ≥12 and ≥14 μg/day vitamin D would be required to reach 25OHD concentrations of 50 nmol/L in boys and girls, respectively. Moreover, the results of the present study indicate that vitamin D deficiency has a greater association with calcaneal stiffness in girls than in boys.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Dawson-Hughes B, Dallal GE, Krall EA, Harris S, Sokoll LJ, Falconer G (1991) Effect of vitamin D supplementation on wintertime and overall bone loss in healthy postmenopausal women. Ann Intern Med 115:505–512

    Article  CAS  PubMed  Google Scholar 

  2. Oliveri MB, Ladizesky M, Mautalen CA, Alonso A, Martinez L (1993) Seasonal variations of 25 hydroxyvitamin D and parathyroid hormone in Ushuaia (Argentina), the southernmost city of the world. Bone Miner 20:99–108

    Article  CAS  PubMed  Google Scholar 

  3. Guillemant J, Taupin P, Le HT, Taright N, Allemandou A, Pérès G, Guillemant S (1999) Vitamin D status during puberty in French healthy male adolescents. Osteoporos Int 10:222–225

    Article  CAS  PubMed  Google Scholar 

  4. Outila TA, Kärkkäinen 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 74:206–210

    CAS  PubMed  Google Scholar 

  5. Harkness L, Cromer B (2005) Low levels of 25-hydroxy vitamin D are associated with elevated parathyroid hormone in healthy adolescent females. Osteoporos Int 16:109–113

    Article  CAS  PubMed  Google Scholar 

  6. Harinarayan CV, Ramalakshmi T, Prasad UV, Sudhakar D, Srinivasarao PV, Sarma KV, Kumar EG (2007) High prevalence of low dietary calcium, high phytate consumption, and vitamin D deficiency in healthy south Indians. Am J Clin Nutr 85:1062–1067

    CAS  PubMed  Google Scholar 

  7. Hill TR, Cotter AA, Mitchell S, Boreham CA, Dubitzky W, Murray L, Strain JJ, Flynn A, Robson PJ, Wallace JM, Kiely M, Cashman KD (2009) Vitamin D status and parathyroid hormone relationship in adolescents and its association with bone health parameters: analysis of the Northern Ireland Young Heart’s Project. Osteoporos Int 21:695–700

    Article  PubMed  Google Scholar 

  8. Lehtonen-Veromaa MK, Möttönen TT, Nuotio IO, Irjala KM, Leino AE, Viikari JS (2002) Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: a 3-y prospective study. Am J Clin Nutr 76:1446–1453

    CAS  PubMed  Google Scholar 

  9. Kärkkäinen MU, Wiersma JW, Lamberg-Allardt CJ (1997) Postprandial parathyroid hormone response to four calcium-rich foodstuffs. Am J Clin Nutr 65:1726–1730

    PubMed  Google Scholar 

  10. Hirota T, Kusu T, Hirota K (2005) Improvement of nutrition stimulates bone mineral gain in Japanese school children and adolescents. Osteoporos Int 16:1057–1064

    Article  PubMed  Google Scholar 

  11. The National Health and Nutrition Survey Japan (2007) http://www.mhlw.go.jp/bunya/kenkou/eiyou09/01.html. Accessed 15 Apr 2015

  12. The National Health and Nutrition Survey in Japan (2009) Ministry of Health, Labour and Welfare, Japan. Daiichishuppan, Japan

  13. Ersfeld DL, Rao DS, Body JJ, Sackrison JL Jr, Miller AB, Parikh N, Eskridge TL, Polinske A, Olson GT, MacFarlane GD (2004) Analytical and clinical validation of the 25 OH vitamin D assay for the LIAISON automated analyzer. Clin Biochem 37:867–874

    Article  CAS  PubMed  Google Scholar 

  14. Uenishi K, Ishida H, Nakamura K (2008) Development of a simple food frequency questionnaire to estimate intakes of calcium and other nutrients for the prevention and management of osteoporosis. J Nutr Sci Vitaminol 54:25–29

    Article  CAS  PubMed  Google Scholar 

  15. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH, Weaver CM (2011) Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 96:1911–1930

    Article  CAS  PubMed  Google Scholar 

  16. Rosen CJ (2011) Vitamin D insufficiency. N Engl J Med 364:248–254

    Article  CAS  PubMed  Google Scholar 

  17. Absoud M, Cummins C, Lim MJ, Wassmer E, Shaw N (2011) Prevalence and predictors of vitamin D insufficiency in children: a Great Britain population based study. PLoS One 6:e22179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ross AC, Manson JE, Abrams SA, Aloia JF, Brannon PM, Clinton SK, Durazo-Arvizu RA, Gallagher JC, Gallo RL, Jones G, Kovacs CS, Mayne ST, Rosen CJ, Shapses SA (2011) The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab 96:53–58

    Article  CAS  PubMed  Google Scholar 

  19. Uenishi K, Ishimi Y, Nakamura K, Kodama H, Esashi T (2013) Dietary reference intakes for Japanese 2010: macrominerals. J Nutr Sci Vitaminol 59:S83–S90

    Article  CAS  Google Scholar 

  20. Harkness LS, Cromer BA (2005) Vitamin D deficiency in adolescent females. J Adolesc Health 37:75

    Article  PubMed  Google Scholar 

  21. Lehtonen-Veromaa M, Möttönen T, Nuotio I, Irjala K, Viikari J (2002) The effect of conventional vitamin D2 supplementation on serum 25(OH)D concentration is weak among peripubertal Finnish girls: a 3-y prospective study. Eur J Clin Nutr 56:431–437

    Article  CAS  PubMed  Google Scholar 

  22. Weng FL, Shults J, Leonard MB, Stallings VA, Zemel BS (2007) Risk factors for low serum 25-hydroxyvitamin D concentrations in otherwise healthy children and adolescents. Am J Clin Nutr 86:150–158

    CAS  PubMed  Google Scholar 

  23. Ginty F, Cavadini C, Michaud PA, Burckhardt P, Baumgartner M, Mishra GD, Barclay DV (2004) Effects of usual nutrient intake and vitamin D status on markers of bone turnover in Swiss adolescents. Eur J Clin Nutr 58:1257–1265

    Article  CAS  PubMed  Google Scholar 

  24. Das G, Crocombe S, McGrath M, Berry JL, Mughal MZ (2006) Hypovitaminosis D among healthy adolescent girls attending an inner city school. Arch Dis Child 91:569–572

    Article  CAS  PubMed  Google Scholar 

  25. Gordon CM, DePeter KC, Feldman HA, Grace E, Emans SJ (2004) Prevalence of vitamin D deficiency among healthy adolescents. Arch Pediatr Adolesc Med 158:531–537

    Article  PubMed  Google Scholar 

  26. Looker AC, Dawson-Hughes B, Calvo MS, Gunter EW, Sahyoun NR (2002) Serum 25-hydroxyvitamin D status of adolescents and adults in two seasonal subpopulations from NHANES III. Bone 30:771–777

    Article  CAS  PubMed  Google Scholar 

  27. González-Gross M, Valtueña J, Breidenassel C, Moreno LA, Ferrari M, Kersting M, De Henauw S, Gottrand F, Azzini E, Widhalm K, Kafatos A, Manios Y, Stehle P (2012) Vitamin D status among adolescents in Europe: the Healthy Lifestyle in Europe by Nutrition in Adolescence study. Br J Nutr 107:755–764

    Article  PubMed  Google Scholar 

  28. Looker AC, Pfeiffer CM, Lacher DA, Schleicher RL, Picciano MF, Yetley EA (2008) Serum 25-hydroxyvitamin D status of the US population: 1988–1994 compared with 2000–2004. Am J Clin Nutr 88:1519–1527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Dong Y, Pollock N, Stallmann-Jorgensen IS, Gutin B, Lan L, Chen TC, Keeton D, Petty K, Holick MF, Zhu H (2010) Low 25-hydroxyvitamin D levels in adolescents: race, season, adiposity, physical activity, and fitness. Pediatrics 125:1104–1111

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rovner AJ, O’Brien KO (2008) Hypovitaminosis D among healthy children in the United States: a review of the current evidence. Arch Pediatr Adolesc Med 162:513–519

    Article  PubMed  Google Scholar 

  31. Zhu K, Zhang Q, Foo LH, Trube A, Ma G, Hu X, Du X, Cowell CT, Fraser DR, Greenfield H (2006) Growth, bone mass, and vitamin D status of Chinese adolescent girls 3 y after withdrawal of milk supplementation. Am J Clin Nutr 83:714–721

    CAS  PubMed  Google Scholar 

  32. Du X, Greenfield H, Fraser DR, Ge K, Trube A, Wang Y (2001) Vitamin D deficiency and associated factors in adolescent girls in Beijing. Am J Clin Nutr 74:494–500

    CAS  PubMed  Google Scholar 

  33. Marwaha RK, Tandon N, Reddy DR, Aggarwal R, Singh R, Sawhney RC, Saluja B, Ganie MA, Singh S (2005) Vitamin D and bone mineral density status of healthy schoolchildren in northern India. Am J Clin Nutr 82:477–482

    CAS  PubMed  Google Scholar 

  34. Tanaka K, Terao J, Shidoji Y, Tamai H, Imai E, Okano T (2013) Dietary reference intakes for Japanese 2010: fat-soluble vitamins. J Nutr Sci Vitaminol 59:S57–S66

    Article  CAS  Google Scholar 

  35. Institue of medicin of the National Academies (2011) Dietary reference intakes: calcium, vitamin D. The National Academies Press, pp 370–384. http://www.iom.edu/reports/2010/dietary-reference-intakes-for-calcium-and-vitamin-d.aspx

  36. Chapuy MC, Preziosi P, Maamer M, Arnaud S, Galan P, Hercberg S, Meunier PJ (1997) Prevalence of vitamin D insufficiency in an adult normal population. Osteoporos Int 7:439–443

    Article  CAS  PubMed  Google Scholar 

  37. Okazaki R, Sugimoto T, Kaji H, Fujii Y, Shiraki M, Inoue D, Endo I, Okano T, Hirota T, Kurahashi I, Matsumoto T (2011) Vitamin D insufficiency defined by serum 25-hydroxyvitamin D and parathyroid hormone before and after oral vitamin D load in Japanese subjects. J Bone Miner Metab 29:103–110

    Article  CAS  PubMed  Google Scholar 

  38. Krabbe S, Christiansen C, Rødbro P, Transbøl I (1979) Effect of puberty on rates of bone growth and mineralization: with observations in male delayed puberty. Arch Dis Child 54:950–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Neer RM, Arnaud CD, Zanchetta JR, Prince R, Gaich GA, Reginster JY, Hodsman AB, Eriksen EF, Ish-Shalom S, Genant HK, Wang O, Mitlak BH (2001) Effect of parathyroid hormone (1–34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 344:1434–1441

    Article  CAS  PubMed  Google Scholar 

  40. Krabbe S, Transbøl I, Christiansen C (1982) Bone mineral homeostasis, bone growth, and mineralisation during years of pubertal growth: a unifying concept. Arch Dis Child 57:359–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Cadogan J, Blumsohn A, Barker ME, Eastell R (1998) A longitudinal study of bone gain in pubertal girls: anthropometric and biochemical correlates. J Bone Miner Res 13:1602–1612

    Article  CAS  PubMed  Google Scholar 

  42. Bauer DC, Glüer CC, Cauley JA, Vogt TM, Ensrud KE, Genant HK, Black DM (1997) Broadband ultrasound attenuation predicts fractures strongly and independently of densitometry in older women. A prospective study. Study of Osteoporotic Fractures Research Group. Arch Intern Med 157:629–634

    Article  CAS  PubMed  Google Scholar 

  43. Schott AM, Hans D, Duboeuf F, Dargent-Molina P, Hajri T, Bréart G, Meunier PJ (2005) Quantitative ultrasound parameters as well as bone mineral density are better predictors of trochanteric than cervical hip fractures in elderly women. Results from the EPIDOS study. Bone 37:858–863

    Article  CAS  PubMed  Google Scholar 

  44. Yamamoto K, Nakatsuji T, Yaoi Y, Yamato Y, Yanagitani T, Matsukawa M, Yamazaki K, Matsuyama Y (2012) Relationships between the anisotropy of longitudinal wave velocity and hydroxyapatite crystallite orientation in bovine cortical bone. Ultrasonics 52:377–386

    Article  CAS  PubMed  Google Scholar 

  45. Frost ML, Blake GM, Fogelman I (2001) Quantitative ultrasound and bone mineral density are equally strongly associated with risk factors for osteoporosis. J Bone Miner Res 16:406–416

    Article  CAS  PubMed  Google Scholar 

  46. Nicholson PH, Müller R, Cheng XG, Rüegsegger P, Van Der Perre G, Dequeker J, Boonen S (2001) Quantitative ultrasound and trabecular architecture in the human calcaneus. J Bone Miner Res 16:1886–1892

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was partly supported by a Grant-in-Aid from the Japan Osteoporosis Foundation, a Grant-in-Aid (#20590078) from the Ministry of Education, Culture, Science, Sports and Technology of Japan, a Grant-in-Aid for Comprehensive Research on Cardiovascular Diseases and Research on Dietary Reference Intakes in the Japanese from the Ministry of Health Labor, and Welfare of Japan. We would like to thank Kyowa Medex Co., Ltd for the measurement of serum 25OHD concentrations.

Conflict of interest

Although Naoko Tsugawa and Toshio Okano were funded by Kyowa Medex Co., Ltd, it played no part in the design of the study, collection and analysis of data and decision to publish. The other authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Hygienic Sciences, Kobe Pharmaceutical University, Kobe, Japan

    Naoko Tsugawa, Reo Ozaki, Tomoki Takase, Takuya Minekami, Yuri Uchino, Maya Kamao & Toshio Okano

  2. Laboratory of Physiological Nutrition, Kagawa Nutrition University, Sakado, Japan

    Kazuhiro Uenishi

  3. Laboratory of Administrative Dietetics, Kagawa Nutrition University, Sakado, Japan

    Hiromi Ishida

  4. Laboratory of Public Health, Faculty of Health and Nutrition, Osaka Shoin Women’s University, 4-2-26, Hishiya-nishi, Higashiosaka, Osaka, 577-8550, Japan

    Naoko Tsugawa

Authors
  1. Naoko Tsugawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuhiro Uenishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiromi Ishida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reo Ozaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tomoki Takase
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takuya Minekami
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuri Uchino
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maya Kamao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Toshio Okano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naoko Tsugawa.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsugawa, N., Uenishi, K., Ishida, H. et al. Association between vitamin D status and serum parathyroid hormone concentration and calcaneal stiffness in Japanese adolescents: sex differences in susceptibility to vitamin D deficiency . J Bone Miner Metab 34, 464–474 (2016). https://doi.org/10.1007/s00774-015-0694-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-015-0694-y

Keywords

Search

Navigation