Advertisement

European Journal of Nutrition

, Volume 49, Issue 3, pp 147–153 | Cite as

The association between high plasma homocysteine levels and lower bone mineral density in Slovak women: the impact of vegetarian diet

  • Zora KrivošíkováEmail author
  • Marica Krajčovičová-Kudláčková
  • Viera Spustová
  • Kornélia Štefíková
  • Martina Valachovičová
  • Pavel Blažíček
  • Tatiana Nĕmcová
Original Contribution

Abstract

Background

A long-term vegetarian diet is generally poor in vitamin B group. The lack of vitamin B12 together with vitamin B6 and folate deficiency is closely related to homocysteine metabolism. Hyperhomocysteinemia was found to be associated with increased bone turnover markers and increased fracture risk. Thus, hyperhomocysteinemia, vitamin B12 and folate deficiency may be regarded as novel risk factors for micronutrient deficiency-related osteoporosis.

Aim of the study

To assess the possible impact of a vegetarian diet on bone mineral density in cohort of Slovak vegetarian women.

Methods

Fasting serum glucose, albumin, calcium, phosphorous and creatinine as well as bone markers, serum vitamin B12, folate and plasma levels of total homocysteine were assessed in two nutritional groups (vegetarians vs. nonvegetarians) of apparently healthy women (age range 20–70 years). Bone mineral density of the femoral neck, trochanter, total femur and lumbar spine was measured in all subjects.

Results

Vegetarians had a significantly lower weight (p < 0.05), higher PTH (p < 0.01) and homocysteine (p < 0.001). Vitamin B12 was significantly higher in nonvegetarians (p < 0.001). No differences were observed in folate levels. Univariate analysis showed significant association between homocysteine and B12 (p < 0.01), folate (p < 0.001), creatinine (p < 0.001), total proteins (p < 0.049), age (p < 0.001) and vegetarian food intake (p < 0.001). Vegetarians had a significantly lower TrFBMD (p < 0.05) and ToFBMD (p < 0.05). Age and CTx were significant predictors in all sites of measured BMD and PTH. A strong correlation between homocysteine and FNBMD (r = −0.2009, p < 0.002), TrFBMD (r = −0.1810, p < 0.004) and ToFBMD (r = −0.2225, p < 0.001) was found in all subjects.

Conclusion

Homocysteine is one of the predictors of bone mineral density, and hyperhomocysteinemia is associated with lower bone mineral density. In healthy adults, homocysteine levels are dependent on age as well as on nutritional habits. Thus, elderly women on a vegetarian diet seem to be at higher risk of osteoporosis development than nonvegetarian women.

Keywords

Homocysteine Folate Vitamin B12 Bone mineral density Vegetarian diet 

Notes

Acknowledgments

We would like to thank Mr. Daniel Lichtenberger for careful reading of the manuscript and helpful comments. This work was supported by Research and Development Support Agency under the contract No: APVT-21-010104 and APVT-21-017704.

References

  1. 1.
    Blouin S, Thaler HW, Korninger C, Schmid R, Hofstaetter JG, Zoehrer R, Phipps R, Klaushofer K, Roschger P, Paschalis EP (2009) Bone matrix quality and plasma homocysteine levels. Bone 44(5):959–964CrossRefGoogle Scholar
  2. 2.
    Bozkurt N, Erdem M, Yilmaz E, Erdem A, Biri A, Kubatova A, Bozkurt M (2009) The relationship of homocysteine, B12 and folic acid with the bone mineral density of the femur and lumbar spine in Turkish postmenopausal women. Arch Gynecol Obstet 283(3):381–387CrossRefGoogle Scholar
  3. 3.
    Dhonukshe-Rutten RA, van Dusseldorp M, Schneede J, de Groot LC, van Staveren WA (2005) Low bone mineral density and bone mineral content are associated with low cobalamin status in adolescents. Eur J Nutr 44(6):341–347CrossRefGoogle Scholar
  4. 4.
    Elshorbagy AK, Gjesdal CG, Nurk E, Tell GS, Ueland PM, Nygard O, Tverdal A, Vollset SE, Smith AD, Refsum H (2009) Cysteine, homocysteine and bone mineral density: a role for body composition? Bone 44(5):954–958CrossRefGoogle Scholar
  5. 5.
    Gerdhem P, Ivaska KK, Isaksson A, Petterson K, Väänänen HK, Obrant KJ, Åkesson K (2007) Association between homocysteine, bone turnover, BMD, mortality and fracture risk in elderly women. J Bone Min Res 22(1):127–134CrossRefGoogle Scholar
  6. 6.
    Gjesdal CG, Vollset SE, Ueland PM, Refsum H, Meyer HE, Tell GS (2007) Plasma homocysteine, folate, and vitamin B12 and the risk of hip fracture: the Hordaland Homocysteine Study. J Bone Miner Res 22(5):747–756CrossRefGoogle Scholar
  7. 7.
    Golbahar J, Hamidi A, Aminzadeh MA, Omrani GR (2004) Association of plasma folate, plasma homocysteine, but not methylenetetrahydrofolate reductase C667T polymorphism, with bone mineral density in postmenopausal Iranian women: a cross-sectional study. Bone 35:760–765CrossRefGoogle Scholar
  8. 8.
    Grieco AJ (1977) Homocystinuria: pathogenic mechanisms. Am J Med Sci 273:120–132CrossRefGoogle Scholar
  9. 9.
    Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak bone mass. Osteoporos Int 11(12):985–1009CrossRefGoogle Scholar
  10. 10.
    Herrmann M, Kraenzlin M, Pape G, Sand-Hill M, Herrmann W (2005) Relationship between homocysteine and biochemical bone turnover markers and bone mineral density in peri- and post-menopausal women. Clin Chem Lab Med 43:1118–1123CrossRefGoogle Scholar
  11. 11.
    Herrmann M, Tami A, Wildemann B, Wolny M, Wagner A, Schorr H, Taban-Shomal O, Umanskaya N, Ross S, Garcia P, Hübner U, Herrmann W (2008) Hyperhomocysteinemia induces a tissue specific accumulation of homocysteine in bone by collagen binding and adversely affects bone. Bone 44(3):467–475CrossRefGoogle Scholar
  12. 12.
    Herrmann M, Widmann T, Colaianna G, Colucci S, Zallone A, Herrmann W (2005) Increased osteoclast activity in the presence of increased homocysteine concentrations. Clin Chem 51:2348–2353CrossRefGoogle Scholar
  13. 13.
    Herrmann M, Umanskaya N, Wildemann B, Colaianni G, Widmann T, Zallone A, Herrmann W (2008) Stimulation of osteoblast activity by homocysteine. J Cell Mol Med 12(4):1205–1210CrossRefGoogle Scholar
  14. 14.
    Herrmann M, Widmann T, Herrmann W (2005) Homocysteine—a newly recognised risk factor for osteoporosis. Clin Chem Lab Med 43(10):1111–1117CrossRefGoogle Scholar
  15. 15.
    Houze P, Gamra S, Madelaine I, Bousquet B, Gourmel B (2001) Simultaneous determination of total plasma glutathione, homocysteine, cysteinylglycine, and methionine by high performance liquid chromatography with electrochemical detection. J Clin Lab Anal 15:144–153CrossRefGoogle Scholar
  16. 16.
    Koebnick C, Garcia AL, Dagnelie PC, Strassner C, Lindemans J, Katz N, Leitzmann C, Hoffmann I (2005) Long-term consumption of a raw food diet is associated with favorable serum LDL cholesterol and triglycerides but also with elevated plasma homocysteine and low serum HDL cholesterol in humans. J Nutr 135(10):2372–2378Google Scholar
  17. 17.
    Leboff MS, Narweker R, Lacroix A, Wu L, Jackson R, Lee J, Bauer DC, Cauley J, Kooperberg C, Lewis C, Thomas AM, Cummings S (2009) Homocysteine levels and risk of hip fracture in postmenopausal women. J Clin Endocrinol Metab 94(4):1207–1213CrossRefGoogle Scholar
  18. 18.
    Majchrzak D, Singer I, Männer M, Rust P, Genser D, Wagner KH, Elmadfa I (2006) B-vitamin status and concentrations of homocysteine in Austrian omnivores, vegetarians and vegans. Ann Nutr Metab 50(6):485–491CrossRefGoogle Scholar
  19. 19.
    Maurer M, Burri S, de Marchi S, Hullin R, Martinelli M, Mohacsi P, Hess OM (2009) Plasma homocysteine and cardiovascular risk in heart failure with and without cardiorenal syndrome. Int J Cardiol (in press)Google Scholar
  20. 20.
    McLean RR, Jacques PF, Selhub J, Tucker KL, Samelson EJ, Broe KE, Hannan MT, Cupples LA, Kiel DP (2004) Homocysteine as a predictive factor for hip fracture in older persons. N Engl J Med 350:2042–2049CrossRefGoogle Scholar
  21. 21.
    Morris MS, Jacques PF, Selhub J (2005) Relation between homocysteine and B-vitamin status indicators and bone mineral density in older Americans. Bone 37:234–242CrossRefGoogle Scholar
  22. 22.
    Mudd SH, Skovby F, Levy HL, Pettigrew KD, Wilcken B, Pyeritz RE, Andria G, Boers GH, Bromberg IL, Cerone R (1985) The natural history of homocysteine due to the cystathionine beta synthase deficiency. Am J Hum Genet 37:1–31Google Scholar
  23. 23.
    Périer MA, Gineyts E, Munoz F, Sornay-Rendu E, Delmas PD (2007) Homocysteine and fracture risk in postmenopausal women: the OFELY study. Osteoporos Int 18:1329–1336CrossRefGoogle Scholar
  24. 24.
    Refsum H, Smith AD, Ueland PM, Nexo E, Clarke R, McPartlin J, Johnston C, Engbaek F, Schneede J, McPartlin C, Scott JM (2004) Facts and recommendations about total homocysteine determinations: an expert opinion. Clin Chem 50(1):3–32CrossRefGoogle Scholar
  25. 25.
    Saito M (2006) Elevated plasma concentration of homocysteine, low level of vitamin B6, pyridoxal, and vitamin D insufficiency in patients with hip fracture: a possible explanation for detrimental cross-link pattern in bone collagen. Clin Calcium 16(12):1974–1984Google Scholar
  26. 26.
    Saito M, Fujii K, Marumo K (2006) Degree of mineralization-related collagen crosslinks in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tissue Int 79:160–168CrossRefGoogle Scholar
  27. 27.
    Selhub J, Jacques PF, Wilson PW, Rush D, Rosenberg IH (1993) Vitamin status and intake as primary determinants of homocysteinemia in an elderly population. JAMA 270:2693–2698CrossRefGoogle Scholar
  28. 28.
    Slavícek J, Kittnar O, Fraser GE, Medová E, Konecná J, Zizka R, Dohnalová A, Novák V (2009) Lifestyle decreases risk factors for cardiovascular diseases. Cent Eur J Public Health 16(4):161–164Google Scholar
  29. 29.
    Stanger O, Herrmann W, Pietrzik K, Fowler B, Geisel J, Dierkes J, Weger M (2003) DACH-LIGA Homocystein eV (German, Austrian and Swiss homocysteine society): consensus paper on the rational clinical use of homocysteine, folic acid and B-vitamins in cardiovascular and thrombotic diseases: guidelines and recommendations. Clin Chem Lab Med 41:1392–1403CrossRefGoogle Scholar
  30. 30.
    Tucker KL, Qiao N, Scott T, Rosenberg I, Spiro A 3rd (2005) High homocysteine and low B vitamins predict cognitive decline in aging men: the Veterans Affairs Normative Aging Study. Am J Clin Nutr 82(3):627–635Google Scholar
  31. 31.
    Turner-McGrievy GM, Barnard ND, Scialli AR, Lanou AJ (2004) Effects of a low-fat vegan diet and a Step II diet on macro- and micronutrient intakes in overweight postmenopausal women. Nutrition 20(9):738–746CrossRefGoogle Scholar
  32. 32.
    van Meurs JB, Dhonukshe-Rutten RA, Pluijm SM, van der Klift M, de Jonge R, Lindemans J, de Groot LC, Hofman A, Witteman JC, van Leeuwen JP, Breteler MM, Lips P, Pols HA, Uitterlinden AG (2004) Homocysteine levels and the risk of osteoporotic fracture. N Engl J Med 350:2033–2041CrossRefGoogle Scholar
  33. 33.
    Wolters M, Herrmann S, Hahn A (2003) B vitamin status and concentrations of homocysteine and methylmalonic acid in elderly German women. Am J Clin Nutr 78:765–772Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Zora Krivošíková
    • 1
    Email author
  • Marica Krajčovičová-Kudláčková
    • 2
  • Viera Spustová
    • 1
  • Kornélia Štefíková
    • 1
  • Martina Valachovičová
    • 2
  • Pavel Blažíček
    • 3
  • Tatiana Nĕmcová
    • 4
  1. 1.Department of Clinical and Experimental PharmacotherapySlovak Medical UniversityBratislavaSlovakia
  2. 2.Department of Bioactive Compounds and Nutrition ScreeningSlovak Medical UniversityBratislavaSlovakia
  3. 3.Hospital of Ministry of DefenceBratislavaSlovakia
  4. 4.Faculty of Health and Social WorkTrnava’s UniversityTrnavaSlovakia

Personalised recommendations