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Dietary patterns of antioxidant vitamin and carotenoid intake associated with bone mineral density: findings from post-menopausal Japanese female subjects

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Abstract

Summary

Recent studies show that antioxidants may reduce the risk of osteoporosis. This study showed the associations of bone mineral density with dietary patterns of antioxidant vitamins and carotenoids. The findings suggest the combination of vitamin C and β-cryptoxanthin intakes might provide benefit to bone health in post-menopausal Japanese female subjects.

Introduction

Recent epidemiological studies show antioxidants may reduce the risk of osteoporosis, but little is known about the dietary patterns of antioxidant vitamin and carotenoid intakes and their relation with bone mineral density (BMD).

Methods

A total of 293 post-menopausal female subjects 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. Dietary intakes of antioxidant vitamins and carotenoids were assessed by using a validated food-frequency questionnaire. Dietary patterns were identified on a selected set of antioxidants through principal component factor analysis.

Results

Three dietary patterns were identified. The “retinol” pattern, characterized by notably high intakes of preformed retinol, zeaxanthin, and vitamin E, was positively associated with the risk for low BMD. In contrast, the “β-cryptoxanthin” pattern, characterized by notably high intakes of β-cryptoxanthin and vitamin C, was negatively associated with low BMD. The odds ratios for low BMD in the highest tertiles of dietary intakes of preformed retinol, vitamin C, and β-cryptoxanthin against the lowest tertiles were 3.22 [95% confidence interval (CI), 1.38–7.51], 0.25 (CI, 0.10–0.66), and 0.40 (CI, 0.17–0.92), respectively, after adjustments for confounders. However, negative associations of vitamin C and β-cryptoxanthin with low BMD were not significant after further adjustment for intake of β-cryptoxanthin or vitamin C, respectively. Higher intakes of both vitamin C and β-cryptoxanthin were significantly associated with low BMD (P < 0.05).

Conclusions

The combination of vitamin C and β-cryptoxanthin may be associated with radial BMD in post-menopausal Japanese female subjects.

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References

  1. Ministry of Health, Labor and Welfare. Comprehensive survey of living conditions of the people on Health and Welfare. Section3 2004. Available at: http://www.mhlw.go.jp/toukei/saikin/hw/k-tyosa/k-tyosa04/4-2.html (accessed 1 December 2009)

  2. Christodoulou C, Cooper C (2003) What is osteoporosis? Postgrad Med J 79:133–138

    Article  CAS  PubMed  Google Scholar 

  3. Gennari C (2001) Calcium and vitamin D nutrition and bone disease of the elderly. Public Health Nutr 4:547–559

    Article  CAS  PubMed  Google Scholar 

  4. Prentice A (2004) Diet, nutrition and the prevention of osteoporosis. Public Health Nutr 7:227–243

    Article  CAS  PubMed  Google Scholar 

  5. Macdonald HM, New SA, Golden MH, Campbell MK, Reid DM (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 79:155–165

    CAS  PubMed  Google Scholar 

  6. New SA, Bolton-Smith C, Grubb DA, Reid DM (1997) Nutritional influences on bone mineral density: a cross-sectional study in premenopausal women. Am J Clin Nutr 65:1831–1839

    CAS  PubMed  Google Scholar 

  7. Prynne CJ, Mishra GD, O’Connell MA, Muniz G, Laskey MA, Yan L, Prentice A, Ginty F (2006) Fruit and vegetable intakes and bone mineral status: a cross-sectional study in 5 age and sex cohorts. Am J Clin Nutr 83:1420–1428

    CAS  PubMed  Google Scholar 

  8. Okubo H, Sasaki S, Horiguchi H, Oguma E, Miyamoto K, Hosoi Y, Kim MK, Kayama F (2006) Dietary patterns associated with bone mineral density in premenopausal Japanese farmwomen. Am J Clin Nutr 83:1185–1192

    CAS  PubMed  Google Scholar 

  9. McGartland CP, Robson PJ, Murray LJ, Cran GW, Savage MJ, Watkins DC, Rooney MM, Boreham CA (2004) Fruit and vegetable consumption and bone mineral density: the Northern Ireland Young Hearts Project. Am J Clin Nutr 80:1019–1023

    CAS  PubMed  Google Scholar 

  10. Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, Felson D, Kiel DP (2002) Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 76:245–252

    CAS  PubMed  Google Scholar 

  11. Gutteridge JM (1994) Biological origin of free radicals, and mechanisms of antioxidant protection. Chem Biol Interact 91:133–140

    Article  CAS  PubMed  Google Scholar 

  12. 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 96:693–702

    Article  CAS  PubMed  Google Scholar 

  13. Almeida M, Han L, Martin-Millan M, O’Brien CA, Manolagas SC (2007) Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor- to forkhead box O-mediated transcription. J Biol Chem 282:27298–27305

    Article  CAS  PubMed  Google Scholar 

  14. Jilka RL, Weinstein RS, Parfitt AM, Manolagas SC (2007) Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J Bone Miner Res 22:1492–1501

    Article  PubMed  Google Scholar 

  15. Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639

    Article  CAS  PubMed  Google Scholar 

  16. Basu S, Michaelsson K, Olofsson H, Johansson S, Melhus H (2001) Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun 288:275–279

    Article  CAS  PubMed  Google Scholar 

  17. Yalin S, Bagis S, Polat G (2005) Is there a role of free oxygen radicals in primary male osteoporosis? Clin Exp Rheumatol 23:689–692

    CAS  PubMed  Google Scholar 

  18. 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 315:841–846

    CAS  PubMed  Google Scholar 

  19. Melhus H, Michaelsson K, Holmberg L, Wolk A, Ljunghall S (1999) Smoking, antioxidant vitamins, and the risk of hip fracture. J Bone Miner Res 14:129–135

    Article  CAS  PubMed  Google Scholar 

  20. Maggio D, Barabani M, Pierandrei M (2003) Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study. J Clin Endocrinol Metab 88:1523–1527

    Article  CAS  PubMed  Google Scholar 

  21. Maggio D, Polidori MC, Barabani M, Tufi A, Ruggiero C, Cecchetti R, Aisa MC, Stahl W, Cherubini A (2006) Low levels of carotenoids and retinol in involutional osteoporosis. Bone 38:244–248

    Article  CAS  PubMed  Google Scholar 

  22. Yang Z, Zhang Z, Penniston KL, Binkley N, Tanumihardjo SA (2008) Serum carotenoid concentrations in postmenopausal women from the United States with and without osteoporosis. Int J Vitam Nutr Res 78:105–111

    Article  CAS  PubMed  Google Scholar 

  23. Sahni S, Hannan MT, Blumberg J, Cupples LA, Kiel DP, Tucker KL (2009) Inverse association of carotenoid intakes with 4-y change in bone mineral density in elderly men and women: the Framingham Osteoporosis Study. Am J Clin Nutr 89:416–424

    Article  CAS  PubMed  Google Scholar 

  24. Sahni S, Hannan MT, Gagnon D, Blumberg J, Cupples LA, Kiel DP, Tucker KL (2009) Protective effect of total and supplemental vitamin C intake on the risk of hip fracture—a 17-year follow-up from the Framingham Osteoporosis Study. Osteoporos Int 20:1853–1861

    Article  CAS  PubMed  Google Scholar 

  25. Sugiura M, Nakamura M, Ogawa K, Ikoma Y, Ando F, Yano M (2008) Bone mineral density in post-menopausal female subjects is associated with serum antioxidant carotenoids. Osteoporos Int 19:211–219

    Article  CAS  PubMed  Google Scholar 

  26. Wakai K, Egami I, Kato K, Lin Y, Kawamura T, Tamakoshi A, Aoki R, Kojima M, Nakayama T, Wada M, Ohno Y (1999) A simple food frequency questionnaire for Japanese diet—Part I. Development of the questionnaire, and reproducibility and validity for food groups. J Epidemiol 9:216–226

    CAS  PubMed  Google Scholar 

  27. Egami I, Wakai K, Kato K, Lin Y, Kawamura T, Tamakoshi A, Aoki R, Kojima M, Nakayama T, Wada M, Ohno Y (1999) A simple food frequency questionnaire for Japanese diet—Part II. Reproducibility and validity for nutrient intakes. J Epidemiol 9:227–234

    CAS  PubMed  Google Scholar 

  28. Science and Technology Agency (1983) Standard tables of food composition in Japan, 4th edn. Printing Bureau, Ministry of Finance, Tokyo, in Japanese

    Google Scholar 

  29. Science and Technology Agency (1997) Standard tables of food composition in Japan. (for new foods], 5th edn. Printing Bureau, Ministry of Finance, Tokyo, in Japanese

    Google Scholar 

  30. Yano M, Kato M, Ikoma Y, Kawasaki A, Fukazawa Y, Sugiura M, Matsumoto H, Ohara Y, Nagao A, Ogawa K (2005) Quantitation of carotenoids in raw and processed fruits in Japan. Food Sci Technol Res 11:13–18

    Article  CAS  Google Scholar 

  31. Aizawa K, Inakuma T (2007) Quantitation of carotenoids in commonly consumed vegetables in Japan. Food Sci Technol Res 13:247–252

    Article  CAS  Google Scholar 

  32. Sugiura M, Nakamura M, Ogawa K, Ikoma Y, Matsumoto H, Ando F, Shimokata H, Yano M (2009) Synergistic interaction of cigarette smoking and alcohol drinking with serum carotenoid concentrations: findings from a middle-aged Japanese population. Br J Nutr 102:1211–1219

    Article  CAS  PubMed  Google Scholar 

  33. Orimo H, Hayashi Y, Fukunaga M et al (2001) Diagnostic criteria for primary osteoporosis. J Bone Miner Metab 19:331–337

    Article  CAS  PubMed  Google Scholar 

  34. Feskanich D, Singh V, Willett WC, Colditz GA (2002) Vitamin A intake and hip fractures among postmenopausal women. JAMA 287:47–54

    Article  CAS  PubMed  Google Scholar 

  35. Melhus H, Michaëlsson K, Kindmark A, Bergström R, Holmberg L, Mallmin H, Wolk A, Ljunghall S (1998) Excessive dietary intake of vitamin A is associated with reduced bone mineral density and increased risk for hip fracture. Ann Intern Med 129:770–778

    CAS  PubMed  Google Scholar 

  36. Promislow JH, Goodman-Gruen D, Slymen DJ, Barrett-Connor E (2002) Retinol intake and bone mineral density in the elderly: the Rancho Bernardo Study. J Bone Miner Res 17:1349–1358

    Article  CAS  PubMed  Google Scholar 

  37. Ministry of Health, Labor and Welfare. Recommended dietary allowance for Japanese: dietary reference intakes. Section 2 2009. Available at: http://www.mhlw.go.jp/shingi/2009/05/dl/s0529-4i.pdf (accessed 1 December 2009)

  38. Poal-Manresa J, Little K, Trueta J (1970) Some observations on the effects of vitamin C deficiency on bone. Br J Exp Pathol 51:372–378

    CAS  PubMed  Google Scholar 

  39. Kipp DE, McElvain M, Kimmel DB, Akhter MP, Robinson RG, Lukert BP (1996) Scurvy results in decreased collagen synthesis and bone density in the guinea pig animal model. Bone 18:281–288

    Article  CAS  PubMed  Google Scholar 

  40. Termine JD (1990) Cellular activity, matrix proteins, and aging bone. Exp Gerontol 25:217–221

    Article  CAS  PubMed  Google Scholar 

  41. Peterkofsky B (1991) Ascorbate requirement for hydroxylation and secretion of procollagen: relationship to inhibition of collagen synthesis in scurvy. Am J Clin Nutr 54:1135S–1140S

    CAS  PubMed  Google Scholar 

  42. Iotsova V, Caamano J, Loy J, Yang Y, Lewin A, Bravo R (1997) Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat Med 3:1285–1289

    Article  CAS  PubMed  Google Scholar 

  43. Baeuerle PA, Rupec RA, Pahl HL (1996) Reactive oxygen intermediates as second messengers of a general pathogen response. Pathol Biol (Paris) 44:29–35

    CAS  Google Scholar 

  44. Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR (1996) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639

    Article  Google Scholar 

  45. Bax BE, Alam AS, Banerji B, Bax CM, Bevis PJ, Stevens CR, Moonga BS, Blake DR, Zaidi M (1992) Stimulation of osteoclastic bone resorption by hydrogen peroxide. Biochem Biophys Res Commun 183:1153–1158

    Article  CAS  PubMed  Google Scholar 

  46. 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 26:1188–1191

    Article  CAS  PubMed  Google Scholar 

  47. Yamaguchi M, Uchiyama S (2004) Beta-cryptoxanthin stimulates bone formation and inhibits bone resorption in tissue culture in vitro. Mol Cell Biochem 258:137–144

    Article  CAS  PubMed  Google Scholar 

  48. 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 27:232–235

    Article  CAS  PubMed  Google Scholar 

  49. Hosseinimehr SJ, Nemati A (2006) Radioprotective effects of hesperidin against gamma irradiation in mouse bone marrow cells. Br J Radiol 79:415–418

    Article  CAS  PubMed  Google Scholar 

  50. Chiba H, Uehara M, Wu J, Wang X, Masuyama R, Suzuki K, Kanazawa K, Ishimi Y (2003) Hesperidin, a citrus flavonoid, inhibits bone loss and decreases serum and hepatic lipids in ovariectomized mice. J Nutr 133:1892–1897

    CAS  PubMed  Google Scholar 

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Acknowledgment

This work was supported by a grant from the Ministry of Agriculture, Forestry, and Fisheries (MAFF) for a food research project titled “Integrated Research on Safety and Physiological Function of Food” and a grant from the Council for Advancement of Fruit Tree Science. We are grateful to the participants in our survey and to the staff of the health examination program for residents of the town of Mikkabi, Shizuoka, Japan. We are also grateful to the staff of the Seirei Preventive Health Care Center (Shizuoka, Japan).

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Authors and Affiliations

  1. Research team for health benefit of fruit, National Institute of Fruit Tree Science, 485-6 Shimizu-Okitsu-nakachou, Shizuoka-shi, Shizuoka, 424-0292, Japan

    M. Sugiura, K. Ogawa, Y. Ikoma & M. Yano

  2. Department of Community Health and Preventive Medicine, Hamamatsu University School of Medicine, 1-20-1 Handayama, Hamamatsu-shi, Shizuoka, 431-3192, Japan

    M. Nakamura

  3. Department of Community Care Philanthropy, Aichi Shukutoku University, 23 Sakuragaoka, Nagoya-shi, Aichi, 464-8671, Japan

    F. Ando

  4. Department of Epidemiology, National Institute for Longevity Sciences, 36-3 Moriokachou, Obu-shi, Aichi, 474-8522, Japan

    H. Shimokata

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  1. M. Sugiura
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  2. M. Nakamura
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  3. K. Ogawa
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  4. Y. Ikoma
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  6. H. Shimokata
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  7. M. Yano
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Correspondence to M. Sugiura.

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Sugiura, M., Nakamura, M., Ogawa, K. et al. Dietary patterns of antioxidant vitamin and carotenoid intake associated with bone mineral density: findings from post-menopausal Japanese female subjects. Osteoporos Int 22, 143–152 (2011). https://doi.org/10.1007/s00198-010-1239-9

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  • DOI: https://doi.org/10.1007/s00198-010-1239-9

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