Osteoporosis International

, Volume 19, Issue 2, pp 211–219 | Cite as

Bone mineral density in post-menopausal female subjects is associated with serum antioxidant carotenoids

  • M. Sugiura
  • M. Nakamura
  • K. Ogawa
  • Y. Ikoma
  • F. Ando
  • M. Yano
Original Article



High intake of fruit and vegetables may reduce the risk of osteoporosis. Carotenoids exist in abundance in these foods. This study showed the association of bone mineral density with serum carotenoids. The findings suggest that β-cryptoxanthin and β-carotene might provide benefits to bone health in post-menopausal female subjects.


Antioxidant carotenoids are abundant in fruit and vegetables. Recent epidemiological studies show that high intakes of fruit and vegetables may reduce the risk of osteoporosis, but little is known about the association of bone mineral density (BMD) with serum carotenoids.


A total of 699 subjects (222 males and 477 females) who had received health examinations in the town of Mikkabi, Shizuoka Prefecture, Japan, participated in the study. Radial BMD was measured using dual-energy X-ray absorptiometry (DXA). The associations of serum carotenoid concentrations with the radial BMD were evaluated cross-sectionally.


In male and pre-menopausal female subjects, the six serum carotenoids were not associated with the radial BMD. On the other hand, in post-menopausal female subjects, serum β-cryptoxanthin and β-carotene were weakly but positively correlated with the radial BMD. After adjustment for confounders, the odds ratio (OR) for the lowest quartile of BMD in the high groups (Q2–Q4) of serum β-cryptoxanthin against the lowest quartile (Q1) was 0.45 (95% confidence interval: 0.22–0.95) in post-menopausal female subjects. However, this association was not significant after further adjusting for intakes of minerals and vitamins.


Antioxidant carotenoids, especially β-cryptoxanthin, significantly but partly associate with the radial BMD in post-menopausal female subjects.


Bone mineral density Carotenoids Fruit and vegetables Post-menopausal female 


  1. 1.
    Ministry of Health, Labor and Welfare. Comprehensive survey of living conditions of the people on Health and Welfare. Section3 2004. Internet: http://www.mhlw.go.jp/toukei/saikin/hw/k-tyosa/k-tyosa04/4-2.html (accessed 16 March 2007)
  2. 2.
    Christodoulou C, Cooper C (2003) What is osteoporosis? Postgrad Med J 79:133–138PubMedCrossRefGoogle Scholar
  3. 3.
    Gennari C (2001) Calcium and vitamin D nutrition and bone disease of the elderly. Public Health Nutr 4:547–559PubMedGoogle Scholar
  4. 4.
    Prentice A (2004) Diet, nutrition and the prevention of osteoporosis. Public Health Nutr 7:227–243PubMedCrossRefGoogle Scholar
  5. 5.
    Macdonald HM, New SA, Golden MH et al (2004) Nutritional associations with bone loss during the menopausal transition: evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids. Am J Clin Nutr 79:155–165PubMedGoogle Scholar
  6. 6.
    New SA, Bolton-Smith C, Grubb DA et al (1997) Nutritional influences on bone mineral density: a cross-sectional study in premenopausal women. Am J Clin Nutr 65:1831–1839PubMedGoogle Scholar
  7. 7.
    Prynne CJ, Mishra GD, O’Connell MA et al (2006) Fruit and vegetable intakes and bone mineral status: a cross sectional study in 5 age and sex cohorts. Am J Clin Nutr 83:1420–1428PubMedGoogle Scholar
  8. 8.
    Okubo H, Sasaki S, Horiguchi H et al (2006) Dietary patterns associated with bone mineral density in premenopausal Japanese farmwomen. Am J Clin Nutr 83:1185–1192PubMedGoogle Scholar
  9. 9.
    McGartland CP, Robson PJ, Murray LJ et al (2004) Fruit and vegetable consumption and bone mineral density: the Northern Ireland Young Hearts Project. Am J Clin Nutr 80:1019–1023PubMedGoogle Scholar
  10. 10.
    Tucker KL, Chen H, Hannan MT et al (2002) Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 76:245–252PubMedGoogle Scholar
  11. 11.
    Andersen LF, Veierod MB, Johansson L et al (2005) Evaluation of three dietary assessment methods and serum biomarkers as measures of fruit and vegetable intake, using the method of triads. Br J Nutr 93:519–527PubMedCrossRefGoogle Scholar
  12. 12.
    Coyne T, Ibiebele TI, McNaughton S et al (2005) Evaluation of brief dietary questions to estimate vegetable and fruit consumption - using serum carotenoids and red-cell folate. Public Health Nutr 8:298–308PubMedCrossRefGoogle Scholar
  13. 13.
    Weinstein SJ, Vogt TM, Gerrior SA (2004) Healthy Eating Index scores are associated with blood nutrient concentrations in the third National Health and Nutrition Examination Survey. J Am Diet Assoc 104:576–584PubMedCrossRefGoogle Scholar
  14. 14.
    van Kappel AL, Steghens JP, Zeleniuch-Jacquotte A et al (2001) Serum carotenoids as biomarkers of fruit and vegetable consumption in the New York Women’s Health Study. Public Health Nutr 4:829–835PubMedGoogle Scholar
  15. 15.
    Gutteridge JM (1994) Biological origin of free radicals, and mechanisms of antioxidant protection. Chem Biol Interact 91:133–140PubMedCrossRefGoogle Scholar
  16. 16.
    Rock CL, Jacob RA, Bowen PE (1996) Update on the biological characteristics of the antioxidant micronutrients: vitamin C, vitamin E, and the carotenoids. J Am Diet Assoc 96:693–702PubMedCrossRefGoogle Scholar
  17. 17.
    Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84PubMedCrossRefGoogle Scholar
  18. 18.
    Melhus H, Michaelsson K, Holmberg L et al (1999) Smoking, antioxidant vitamins, and the risk of hip fracture. J Bone Miner Res 14:129–135PubMedCrossRefGoogle Scholar
  19. 19.
    Basu S, Michaelsson K, Olofsson H et al (2001) Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun 288:275–279PubMedCrossRefGoogle Scholar
  20. 20.
    Maggio D, Barabani M, Pierandrei M et al (2003) Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study. J Clin Endocrinol Metab 88:1523–1527PubMedCrossRefGoogle Scholar
  21. 21.
    Yalin S, Bagis S, Polat G et al (2005) Is there a role of free oxygen radicals in primary male osteoporosis? Clin Exp Rheumatol 23:689–692PubMedGoogle Scholar
  22. 22.
    Law MR, Hackshaw AK (1997) A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture: recognition of a major effect. BMJ 315:841–846PubMedGoogle Scholar
  23. 23.
    Maggio D, Polidori MC, Barabani M et al (2006) Low levels of carotenoids and retinol in involutional osteoporosis. Bone 38:244–248PubMedCrossRefGoogle Scholar
  24. 24.
    Sugiura M, Nakamura M, Ikoma Y et al (2005) High serum carotenoids are inversely associated with serum gamma-glutamyltransferase in alcohol drinkers within normal liver function. J Epidemiol 15:180–186PubMedCrossRefGoogle Scholar
  25. 25.
    Wakai K, Egami I, Kato K et al (1999) A simple food frequency questionnaire for Japanese diet-Part I. Development of the questionnaire, and reproducibility and validity for food groups. J Epidemiol 9:216–226PubMedGoogle Scholar
  26. 26.
    Egami I, Wakai K, Kato K et al (1999) A simple food frequency questionnaire for Japanese diet-Part II. Reproducibility and validity for nutrient intakes. J Epidemiol 9:227–234PubMedGoogle Scholar
  27. 27.
    Science and Technology Agency (1983) Standard tables of food composition in Japan, 4th edn. Printing Bureau, Ministry of Finance, Tokyo, Japan. (in Japanese)Google Scholar
  28. 28.
    Science and Technology Agency (1997) Standard tables of food composition in Japan, 5th edn. (for new foods). Printing Bureau, Ministry of Finance, Tokyo, Japan (in Japanese)Google Scholar
  29. 29.
    Hall SL, Greendale GA (1998) The relation of dietary vitamin C intake to bone mineral density: results from the PEPI study. Calcif Tissue Int 63:183–189PubMedCrossRefGoogle Scholar
  30. 30.
    Leveille SG, LaCroix AZ, Koepsell TD et al (1997) Dietary vitamin C and bone mineral density in postmenopausal women in Washington State, USA. J Epidemiol Community Health 51:479–485PubMedCrossRefGoogle Scholar
  31. 31.
    Wang MC, Luz Villa M, Marcus R et al (1997) Associations of vitamin C, calcium and protein with bone mass in postmenopausal Mexican American women. Osteoporos Int 7:533–538PubMedCrossRefGoogle Scholar
  32. 32.
    World Health Organization (2003) Diet, nutrition and the prevention of chronic diseases. World Health Organ Tech Rep Ser 916:i–viii, 1–149, 2003Google Scholar
  33. 33.
    Iotsova V, Caamano J, Loy J et al (1997) Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat Med 3:1285–1289PubMedCrossRefGoogle Scholar
  34. 34.
    Baeuerle PA, Rupec RA, Pahl HL (1996) Reactive oxygen intermediates as second messengers of a general pathogen response. Pathol Biol (Paris) 44:29–35Google Scholar
  35. 35.
    Garrett IR, Boyce BF, Oreffo RO et al (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639PubMedCrossRefGoogle Scholar
  36. 36.
    Bax BE, Alam AS, Banerji B et al (1992) Stimulation of osteoclastic bone resorption by hydrogen peroxide. Biochem Biophys Res Commun 183:1153–1158PubMedCrossRefGoogle Scholar
  37. 37.
    Goodner KL, Rouseff RL, Hofsommer HJ (2001) Orange, mandarin, and hybrid classification using multivariate statistics based on carotenoid profiles. J Agric Food Chem 49:1146–1150PubMedCrossRefGoogle Scholar
  38. 38.
    Holden JM, Eldridge AL, Beecher GR et al (1999) Carotenoid content of U. S. foods: an update of the database. J Food Comp Anal 12:169–196CrossRefGoogle Scholar
  39. 39.
    Hosseinimehr SJ, Nemati A (2006) Radioprotective effects of hesperidin against gamma irradiation in mouse bone marrow cells. Br J Radiol 79:415–418PubMedCrossRefGoogle Scholar
  40. 40.
    Chiba H, Uehara M, Wu J et al (2003) Hesperidin, a citrus flavonoid, inhibits bone loss and decreases serum and hepatic lipids in ovariectomized mice. J Nutr 133:1892–1897PubMedGoogle Scholar
  41. 41.
    Yamaguchi M, Uchiyama S (2003) Effect of carotenoid on calcium content and alkaline phosphatase activity in rat femoral tissues in vitro: the unique anabolic effect of beta-cryptoxanthin. Biol Pharm Bull 26:1188–1191PubMedCrossRefGoogle Scholar
  42. 42.
    Yamaguchi M, Uchiyama S (2004) Beta-Cryptoxanthin stimulates bone formation and inhibits bone resorption in tissue culture in vitro. Mol Cell Biochem 258:137–144PubMedCrossRefGoogle Scholar
  43. 43.
    Uchiyama S, Yamaguchi M (2004) Oral administration of beta-cryptoxanthin induces anabolic effects on bone components in the femoral tissues of rats in vivo. Biol Pharm Bull 27:232–235PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2007

Authors and Affiliations

  • M. Sugiura
    • 1
  • M. Nakamura
    • 2
  • K. Ogawa
    • 1
  • Y. Ikoma
    • 1
  • F. Ando
    • 2
  • M. Yano
    • 1
  1. 1.Research team for health benefit of fruitNational Institute of Fruit Tree ScienceShizuokaJapan
  2. 2.Department of EpidemiologyNational Institute for Longevity SciencesAichiJapan

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