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Carotenoid dietary intakes and plasma concentrations are associated with heel bone ultrasound attenuation and osteoporotic fracture risk in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk cohort

  • Richard P. G. Hayhoe (a1), Marleen A. H. Lentjes (a2), Angela A. Mulligan (a2), Robert N. Luben (a2), Kay-Tee Khaw (a2) and Ailsa A. Welch (a1)...

Abstract

Carotenoids are found in abundance in fruit and vegetables, and may be involved in the positive association of these foods with bone health. This study aimed to explore the associations of dietary carotenoid intakes and plasma concentrations with bone density status and osteoporotic fracture risk in a European population. Cross-sectional analyses (n 14 803) of bone density status, using calcaneal broadband ultrasound attenuation (BUA) and longitudinal analyses (n 25 439) of fracture cases were conducted on data from the prospective European Prospective Investigation into Cancer and Nutrition-Norfolk cohort of middle-aged and older men and women. Health and lifestyle questionnaires were completed, and dietary nutrient intakes were derived from 7-d food diaries. Multiple regression demonstrated significant positive trends in BUA for women across quintiles of dietary α-carotene intake (P=0·029), β-carotene intake (P=0·003), β-cryptoxanthin intake (P=0·031), combined lutein and zeaxanthin intake (P=0·010) and lycopene intake (P=0·005). No significant trends across plasma carotenoid concentration quintiles were apparent (n 4570). The Prentice-weighted Cox regression showed no trends in fracture risk across dietary carotenoid intake quintiles (mean follow-up time 12·5 years), except for a lower risk for wrist fracture in women with higher lutein and zeaxanthin intake (P=0·022); nevertheless, inter-quintile differences in fracture risk were found for both sexes. Analysis of plasma carotenoid data (mean follow-up time 11·9 years) showed lower hip fracture risk in men across higher plasma α-carotene (P=0·026) and β-carotene (P=0·027) quintiles. This study provides novel evidence that dietary carotenoid intake is relevant to bone health in men and women, demonstrating that associations with bone density status and fracture risk exist for dietary intake of specific carotenoids and their plasma concentrations.

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Corresponding author

* Corresponding author: Dr R. P. G. Hayhoe, email r.hayhoe@uea.ac.uk

References

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1. Mitchell, PJ, Cooper, C, Dawson-Hughes, B, et al. (2015) Life-course approach to nutrition. Osteoporos Int 26, 27232742.
2. Gennari, C (2001) Calcium and vitamin D nutrition and bone disease of the elderly. Public Health Nutr 4, 547559.
3. Michaelsson, K (2015) Calcium supplements do not prevent fractures. BMJ 351, h4825.
4. Hayhoe, RP, Lentjes, MA, Luben, RN, et al. (2015) Dietary magnesium and potassium intakes and circulating magnesium are associated with heel bone ultrasound attenuation and osteoporotic fracture risk in the EPIC-Norfolk cohort study. Am J Clin Nutr 102, 376384.
5. Finck, H, Hart, AR, Jennings, A, et al. (2014) Is there a role for vitamin C in preventing osteoporosis and fractures? A review of the potential underlying mechanisms and current epidemiological evidence. Nutr Res Rev 27, 268283.
6. Arscott, SA (2013) Food sources of carotenoids. In Carotenoids and Human Health, pp. 319 [SA Tanumihardjo, editor]. New York: Springer.
7. Yamaguchi, M (2012) Role of carotenoid beta-cryptoxanthin in bone homeostasis. J Biomed Sci 19, 36.
8. Mody, N, Parhami, F, Sarafian, TA, et al. (2001) Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med 31, 509519.
9. 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, 632639.
10. Lee, NK, Choi, YG, Baik, JY, et al. (2005) A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 106, 852859.
11. Bai, XC, Lu, D, Liu, AL, et al. (2005) Reactive oxygen species stimulates receptor activator of NF-kappaB ligand expression in osteoblast. J Biol Chem 280, 1749717506.
12. Tanumihardjo, SA & Binkley, N (2013) Carotenoids and bone health. In Carotenoids and Human Health, pp. 237245 [SA Tanumihardjo, editor]. New York: Springer.
13. Kim, L, Rao, AV & Rao, LG (2003) Lycopene II – effect on osteoblasts: the carotenoid lycopene stimulates cell proliferation and alkaline phosphatase activity of SaOS-2 cells. J Med Food 6, 7986.
14. Park, CK, Ishimi, Y, Ohmura, M, et al. (1997) Vitamin A and carotenoids stimulate differentiation of mouse osteoblastic cells. J Nutr Sci Vitaminol (Tokyo) 43, 281296.
15. Uchiyama, S & Yamaguchi, M (2005) Beta-cryptoxanthin stimulates cell differentiation and mineralization in osteoblastic MC3T3-E1 cells. J Cell Biochem 95, 12241234.
16. Wattanapenpaiboon, N, Lukito, W, Wahlqvist, ML, et al. (2003) Dietary carotenoid intake as a predictor of bone mineral density. Asia Pac J Clin Nutr 12, 467473.
17. Sahni, S, Hannan, MT, Blumberg, J, et al. (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, 416424.
18. Sugiura, M, Nakamura, M, Ogawa, K, et al. (2011) Dietary patterns of antioxidant vitamin and carotenoid intake associated with bone mineral density: findings from post-menopausal Japanese female subjects. Osteoporos Int 22, 143152.
19. de Jonge, EA, Kiefte-de Jong, JC, Campos-Obando, N, et al. (2015) Dietary vitamin A intake and bone health in the elderly: the Rotterdam Study. Eur J Clin Nutr 69, 13601368.
20. Dai, Z, Wang, R, Ang, LW, et al. (2014) Protective effects of dietary carotenoids on risk of hip fracture in men: the Singapore Chinese Health Study. J Bone Miner Res 29, 408417.
21. Sahni, S, Hannan, MT, Blumberg, J, et al. (2009) Protective effect of total carotenoid and lycopene intake on the risk of hip fracture: a 17-year follow-up from the Framingham Osteoporosis Study. J Bone Miner Res 24, 10861094.
22. Sugiura, M, Nakamura, M, Ogawa, K, et al. (2008) Bone mineral density in post-menopausal female subjects is associated with serum antioxidant carotenoids. Osteoporos Int 19, 211219.
23. Sugiura, M, Nakamura, M, Ogawa, K, et al. (2012) High serum carotenoids associated with lower risk for bone loss and osteoporosis in post-menopausal Japanese female subjects: prospective cohort study. PLOS ONE 7, e52643.
24. Yang, Z, Zhang, Z, Penniston, KL, et al. (2008) Serum carotenoid concentrations in postmenopausal women from the United States with and without osteoporosis. Int J Vitam Nutr Res 78, 105111.
25. Day, N, Oakes, S, Luben, R, et al. (1999) EPIC-Norfolk: study design and characteristics of the cohort. European Prospective Investigation of Cancer. Br J Cancer 80, Suppl. 1, 95103.
26. Al-Delaimy, WK, van Kappel, AL, Ferrari, P, et al. (2004) Plasma levels of six carotenoids in nine European countries: report from the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr 7, 713722.
27. Wareham, NJ, Jakes, RW, Rennie, KL, et al. (2003) Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr 6, 407413.
28. Bingham, SA, Gill, C, Welch, A, et al. (1997) Validation of dietary assessment methods in the UK arm of EPIC using weighed records, and 24-hour urinary nitrogen and potassium and serum vitamin C and carotenoids as biomarkers. Int J Epidemiol 26, Suppl. 1, S137S151.
29. Riboli, E, Hunt, KJ, Slimani, N, et al. (2002) European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 5, 11131124.
30. Welch, AA, McTaggart, A, Mulligan, AA, et al. (2001) DINER (Data Into Nutrients for Epidemiological Research) – a new data-entry program for nutritional analysis in the EPIC-Norfolk cohort and the 7-day diary method. Public Health Nutr 4, 12531265.
31. Lentjes, MA, McTaggart, A, Mulligan, AA, et al. (2013) Dietary intake measurement using 7 d diet diaries in British men and women in the European Prospective Investigation into Cancer-Norfolk study: a focus on methodological issues. Br J Nutr, 111.
32. Lentjes, MA, Bhaniani, A, Mulligan, AA, et al. (2011) Developing a database of vitamin and mineral supplements (ViMiS) for the Norfolk arm of the European Prospective Investigation into Cancer (EPIC-Norfolk). Public Health Nutr 14, 459471.
33. Welch, A, Camus, J, Dalzell, N, et al. (2004) Broadband ultrasound attenuation (BUA) of the heel bone and its correlates in men and women in the EPIC-Norfolk cohort: a cross-sectional population-based study. Osteoporos Int 15, 217225.
34. Moayyeri, A, Kaptoge, S, Dalzell, N, et al. (2009) Is QUS or DXA better for predicting the 10-year absolute risk of fracture? J Bone Miner Res 24, 13191325.
35. Kanis, JA, Oden, A, Johnell, O, et al. (2001) The burden of osteoporotic fractures: a method for setting intervention thresholds. Osteoporos Int 12, 417427.
36. Chiuve, SE, Sampson, L & Willett, WC (2011) The association between a nutritional quality index and risk of chronic disease. Am J Prev Med 40, 505513.
37. Jakes, RW, Khaw, K, Day, NE, et al. (2001) Patterns of physical activity and ultrasound attenuation by heel bone among Norfolk cohort of European Prospective Investigation of Cancer (EPIC Norfolk): population based study. BMJ 322, 140.
38. Willett, WC, Howe, GR & Kushi, LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65, 1220S1228S; discussion 1229S–1231S.
39. Flynn, A (2003) The role of dietary calcium in bone health. Proc Nutr Soc 62, 851858.
40. Heaney, RP (2000) Calcium, dairy products and osteoporosis. J Am Coll Nutr 19, 83S99S.
41. Institute of Medicine of the National Academies (2002) Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: National Academies Press.
42. Willett, W editor (1998) Nutritional Epidemiology, 2nd ed. New York: Oxford University Press.
43. Goltz, SR & Ferruzzi, MG (2013) Carotenoid bioavailabiity: influence of dietary lipid and fiber. In Carotenoids and Human Health, pp. 111128 [SA Tanumihardjo, editor]. New York: Springer.
44. Lentjes, MA, Mulligan, AA, Welch, AA, et al. (2015) Contribution of cod liver oil-related nutrients (vitamins A, D, E and eicosapentaenoic acid and docosahexaenoic acid) to daily nutrient intake and their associations with plasma concentrations in the EPIC-Norfolk cohort. J Hum Nutr Diet 28, 568582.
45. Department of Health (1991) Dietary Reference Values for Food Energy and Nutrients for the United Kingdom. Report on Health and Social Subjects, no. 41. London: HSMO.
46. World Health Organization (2011) Serum retinol concentrations for determining the prevalence of vitamin A deficiency in populations. Vitamin and Mineral Nutrition Information System. http://www.who.int/vmnis/indicators/retinol.pdf (accessed December 2015).
47. Brady, WE, Mares-Perlman, JA, Bowen, P, et al. (1996) Human serum carotenoid concentrations are related to physiologic and lifestyle factors. J Nutr 126, 129137.
48. Talegawkar, SA, Johnson, EJ, Carithers, TC, et al. (2008) Carotenoid intakes, assessed by food-frequency questionnaires (FFQs), are associated with serum carotenoid concentrations in the Jackson Heart Study: validation of the Jackson Heart Study Delta NIRI Adult FFQs. Public Health Nutr 11, 989997.
49. Scott, KJ, Thurnham, DI, Hart, DJ, et al. (1996) The correlation between the intake of lutein, lycopene and beta-carotene from vegetables and fruits, and blood plasma concentrations in a group of women aged 50-65 years in the UK. Br J Nutr 75, 409418.
50. Tanumihardjo, SA (2011) Vitamin A: biomarkers of nutrition for development. Am J Clin Nutr 94, 658S665S.
51. Binkley, N & Krueger, D (2000) Hypervitaminosis A and bone. Nutr Rev 58, 138144.
52. Finck, H, Hart, AR, Lentjes, MA, et al. (2015) Cross-sectional and prospective associations between dietary and plasma vitamin C, heel bone ultrasound, and fracture risk in men and women in the European Prospective Investigation into Cancer in Norfolk cohort. Am J Clin Nutr 102, 14161424.
53. Myint, PK, Welch, AA, Bingham, SA, et al. (2007) Fruit and vegetable consumption and self-reported functional health in men and women in the European Prospective Investigation into Cancer-Norfolk (EPIC-Norfolk): a population-based cross-sectional study. Public Health Nutr 10, 3441.
54. Burri, BJ, Neidlinger, TR & Clifford, AJ (2001) Serum carotenoid depletion follows first-order kinetics in healthy adult women fed naturally low carotenoid diets. J Nutr 131, 20962100.
55. Wallstrom, P, Wirfalt, E, Lahmann, PH, et al. (2001) Serum concentrations of beta-carotene and alpha-tocopherol are associated with diet, smoking, and general and central adiposity. Am J Clin Nutr 73, 777785.
56. Kardinaal, AF, van ’t Veer, P, Brants, HA, et al. (1995) Relations between antioxidant vitamins in adipose tissue, plasma, and diet. Am J Epidemiol 141, 440450.
57. Wood, AD, Strachan, AA, Thies, F, et al. (2014) Patterns of dietary intake and serum carotenoid and tocopherol status are associated with biomarkers of chronic low-grade systemic inflammation and cardiovascular risk. Br J Nutr 112, 13411352.
58. Hosseini, B, Saedisomeolia, A & Skilton, MR (2017) Association between micronutrients intake/status and carotid intima media thickness: a systematic review. J Acad Nutr Diet 117, 6982.
59. Handelman, GJ, Packer, L & Cross, CE (1996) Destruction of tocopherols, carotenoids, and retinol in human plasma by cigarette smoke. Am J Clin Nutr 63, 559565.
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