Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Bone turnover, calcium homeostasis, and vitamin D status in Danish vegans

European Journal of Clinical Nutrition volume 72, pages 1046–1054 (2018)Cite this article

Subjects

Abstract

Background/objectives

A vegan diet has been associated with increased bone fracture risk, but the physiology linking nutritional exposure to bone metabolism has only been partially elucidated. This study investigated whether a vegan diet is associated with increased bone turnover and altered calcium homeostasis due to insufficient intake of calcium and vitamin D.

Subjects/methods

Fractionated and total 25-hydroxyvitamin D (25(OH)-D), parathyroid hormone (PTH), calcium, and four bone turnover markers (osteocalcin, N-terminal propeptide of type I procollagen (PINP), bone-specific alkaline phosphatase (BAP), and C-terminal telopeptide of type I collagen (CTX)) were measured in serum from 78 vegans and 77 omnivores.

Results

When adjusting for seasonality and constitutional covariates (age, sex, and body fat percentage) vegans had higher concentrations of PINP (32 [95% CI: 7, 64]%, P = 0.01) and BAP (58 [95% CI: 27, 97]%, P < 0.001) compared to omnivores, whereas CTX (30 [95% CI: −1, 72]%, P = 0.06) and osteocalcin (21.8 [95% CI: −9.3, 63.7]%, P = 0.2) concentrations did not differ between the two groups. Vegans had higher serum PTH concentration (38 [95% CI: 19, 60]%; P < 0.001) and lower 25(OH)-D serum concentration (−33 [95% CI: −45, −19]%; P < 0.001), but similar serum calcium concentration (−1 [95% CI: −3, 1]%, P = 0.18 compared to omnivores.

Conclusions

Vegans have higher levels of circulating bone turnover markers compared to omnivores, which may in the long-term lead to poorer bone health. Differences in dietary habits including intake of vitamin D and calcium may, at least partly, explain the observed differences.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1

Similar content being viewed by others

References

  1. Davey GK, Spencer EA, Appleby PN, Allen NE, Knox KH, Key TJ. EPIC-Oxford: lifestyle characteristics and nutrient intakes in a cohort of 33 883 meat-eaters and 31 546 non meat-eaters in the UK. Public Health Nutr. 2003;6(3):259–69.

    Article  Google Scholar 

  2. Appleby P, Roddam A, Allen N, Key T. Comparative fracture risk in vegetarians and nonvegetarians in EPIC-Oxford. Eur J Clin Nutr. 2007;61(12):1400–6.

    Article  CAS  Google Scholar 

  3. Crowe FL, Steur M, Allen NE, Appleby PN, Travis RC, Key TJ. Plasma concentrations of 25-hydroxyvitamin D in meat eaters, fish eaters, vegetarians and vegans: results from the EPIC-Oxford study. Public Health Nutr. 2011;14(2):340–6.

    Article  Google Scholar 

  4. Ho-Pham LT, Nguyen ND, Nguyen TV. Effect of vegetarian diets on bone mineral density: a Bayesian meta-analysis. Am J Clin Nutr. 2009;90:943–50.

    Article  CAS  Google Scholar 

  5. Ho-Pham LT, Vu BQ, Lai TQ, Nguyen ND, Nguyen TV. Vegetarianism, bone loss, fracture and vitamin D: a longitudinal study in Asian vegans and non-vegans. Eur J Clin Nutr. 2012;66:75–82

    Article  CAS  Google Scholar 

  6. Kohlenberg-Mueller K, Raschka L. Calcium balance in young adults on a vegan and lactovegetarian diet. J Bone Miner Metab. 2003;21:28–33.

    Article  CAS  Google Scholar 

  7. Kristensen NB, Madsen ML, Hansen TH, Allin KH, Hoppe C, Fagt S, et al. Intake of macro- and micronutrients in Danish vegans. Nutr J. 2015;14:115.

    Article  Google Scholar 

  8. Aadahl M, Jorgensen T. Validation of a new self-report instrument for measuring physical activity. Med Sci Sports Exerc. 2003;35:1196–202.

    Article  Google Scholar 

  9. Thuesen B, Husemoen L, Fenger M, Jakobsen J, Schwarz P, Toft U, et al. Determinants of vitamin D status in a general population of Danish adults. Bone. 2012;50:605–10.

    Article  CAS  Google Scholar 

  10. Chan J, Jaceldo-Siegl K, Fraser GE. Serum 25-hydroxyvitamin D status of vegetarians, partial vegetarians, and nonvegetarians: the Adventist Health Study-2. Am J Clin Nutr. 2009;89(5):1686S–1692S.

    Article  CAS  Google Scholar 

  11. Woitge HW, Scheidt-Nave C, Kissling C, Leidig-Bruckner G, Meyer K, Grauer A, et al. Seasonal variation of biochemical indexes of bone turnover: results of a population-based study. J Clin Endocrinol Metab. 1998;83:68–75.

    CAS  PubMed  Google Scholar 

  12. Jorgensen NR, Mollehave LT, Hansen YBL, Quardon N, Lylloff L, Linneberg A. Comparison of two automated assays of BTM (CTX and P1NP) and reference intervals in a Danish population. Osteoporos Int. 2017;28:2103–13.

    Article  CAS  Google Scholar 

  13. Ross AC, Manson JE, Abrams SA, Aloia JF, Brannon PM, Clinton SK, et al. The2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab. 2011;96:53–58.

    Article  CAS  Google Scholar 

  14. Nussbaum SR, Zahradnik RJ, Lavigne JR, Brennan GL, Nozawa-Ung K, Kim LY, et al. Highly sensitive two-site immunoradiometric assay of parathyrin, and its clinical utility in evaluating patients with hypercalcemia. Clin Chem. 1987;33:1364–7.

    CAS  PubMed  Google Scholar 

  15. Brown JP, Albert C, Nassar BA, Adachi JD, Cole D, Davison KS, et al. Bone turnover markers in the management of postmenopausal osteoporosis. Clin Biochem. 2009;42:929–42.

    Article  CAS  Google Scholar 

  16. Holick MF. Vitamin D deficiency. N Eng J Med. 2007;357:266–81.

    Article  CAS  Google Scholar 

  17. Taylor CL, Patterson KY, Roseland JM, Wise SA, Merkel JM, Pehrsson PR, et al. Including food 25-hydroxyvitamin D in intake estimates may reduce the discrepancy between dietary and serum measures of vitamin D status. J Nutr. 2014;144:654–9.

    Article  CAS  Google Scholar 

  18. Brot C, Vestergaard P, Kolthoff N, Gram J, Hermann AP, Sorensen OH. Vitamin D status and its adequacy in healthy Danish perimenopausal women: relationships to dietary intake, sun exposure and serum parathyroid hormone. Br J Nutr. 2001;86:S97–103.

    Article  CAS  Google Scholar 

  19. Lamberg-Allardt C, Brustad M, Meyer HE, Steingrimsdottir L. Vitamin D—a systematic literature review for the 5th edition of the Nordic Nutrition Recommendations. Food Nutr Res. 2013;57. https://doi.org/10.3402/fnr.v57i0.22671

    Article  Google Scholar 

  20. Tripkovic L, Lambert H, Hart K, Smith CP, Bucca G, Penson S, et al. Comparison of vitamin D2 and vitamin D3 supplementation in raising serum 25-hydroxyvitamin D status: a systematic review and meta-analysis. Am J Clin Nutr. 2012;95:1357–64.

    Article  CAS  Google Scholar 

  21. Kemi VE, Karkkainen MU, Karp HJ, Laitinen KA, Lamberg-Allardt CJ. Increased calcium intake does not completely counteract the effects of increased phosphorus intake on bone: an acute dose-response study in healthy females. Br J Nutr. 2008;99:832–9.

    Article  CAS  Google Scholar 

  22. Lamberg-Allardt C, Karkkainen M, Seppanen R, Bistrom H. Low serum 25-hydroxyvitamin D concentrations and secondary hyperparathyroidism in middle-aged white strict vegetarians. Am J Clin Nutr. 1993;58:684–9.

    Article  CAS  Google Scholar 

  23. Nordic Council of Ministers NCoM. Nordic nutrition recommendations 2012. Nord Nutr Recomm 2012. 2014;5:1–3.

    Google Scholar 

  24. Christiansen P, Steiniche T, Brixen K, Hessov I, Melsen F, Charles P, et al. Primary hyperparathyroidism: Biochemical markers and bone mineral density at multiple skeletal sites in Danish patients. Bone. 1997;21(1):93–99.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank A Forman and T Lorentzen for technical assistance, and K Kaadtmann, T Toldsted, P Sandbeck and G Lademann for managerial assistance.

Funding

The Novo Nordisk Foundation Center for Basic Metabolic Research is an independent research centre at the University of Copenhagen partially funded by an unrestricted donation from the Novo Nordisk Foundation (www.metabol.ku.dk). Funders had no influence on study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author contributions

THH, TH, HV, OP, and KHA designed research; THH, NRJ, and AC conducted research; THH and MTBM analyzed data; THH, MTBM, and KHA wrote the paper; KHA had primary responsibility for final content. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

  1. The Novo Nordisk Foundation Center for Basic Metabolic Research, Section of Metabolic Genetics, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Tue H. Hansen, Marie T. B. Madsen, Torben Hansen, Henrik Vestergaard, Oluf Pedersen & Kristine H. Allin

  2. Department of Clinical Biochemistry, Research Center for Ageing and Osteoporosis, Rigshospitalet, Glostrup, Denmark

    Niklas R. Jørgensen

  3. OPEN, Odense Patient data Explorative Network, Odense University Hospital/Institute of Clinical Research, University of Southern Denmark, Odense, Denmark

    Niklas R. Jørgensen

  4. Danish Center for Neonatal Screening, Department Biobanks and Biomarkers, Statens Serum Institut, Copenhagen, Denmark

    Arieh S. Cohen

  5. Faculty of Health Sciences, University of Southern Denmark, Odense, Denmark

    Torben Hansen

  6. Steno Diabetes Center Copenhagen, Gentofte, Denmark

    Henrik Vestergaard

  7. Department of Clinical Epidemiology, Bispebjerg and Frederiksberg Hospital, Frederiksberg, Denmark

    Kristine H. Allin

Authors
  1. Tue H. Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie T. B. Madsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Niklas R. Jørgensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arieh S. Cohen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Torben Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Henrik Vestergaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Oluf Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kristine H. Allin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tue H. Hansen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hansen, T.H., Madsen, M.T.B., Jørgensen, N.R. et al. Bone turnover, calcium homeostasis, and vitamin D status in Danish vegans. Eur J Clin Nutr 72, 1046–1054 (2018). https://doi.org/10.1038/s41430-017-0081-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-017-0081-y

This article is cited by

Search

Advanced search

Quick links