Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-22T15:06:50.815Z Has data issue: false hasContentIssue false

Diet, nutrition and the prevention of osteoporosis

Published online by Cambridge University Press:  02 January 2007

A Prentice*
Affiliation:
MRC Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, UK
*
*Corresponding author: Email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Objective:

To review the evidence on diet and nutrition relating to osteoporosis and provide recommendations for preventing osteoporosis, in particular, osteopototic fracture.

Approach:

Firstly, to review the definition, diagnosis and epidemiology of osteoporosis, to discuss the difficulties in using bone mineral density to define osteoporosis risk in a world-wide context and to propose that fragility fracture should be considered as the disease endpoint. Secondly, to provide an overview of the scientific data, the strengths and weaknesses of the evidence and the conceptual difficulties in interpreting studies linking diet, nutrition and osteoporosis. The following were considered: calcium, vitamin D, phosphorus, magnesium, protein and fluorine. Other potential dietary influences on bone health were also discussed, including vitamins, trace elements, electrolytes, acid–base balance, phyto-oestrogens, vegetarianism and lactose intolerance.

Conclusions:

There is insufficient knowledge linking bone mineral status, growth rates or bone turnover in children and adolescents to long-term benefits in old age for these indices to be used as markers of osteoporotic disease risk. For adults, the evidence of a link between intakes of any dietary component and fracture risk is not sufficiently secure to make firm recommendations, with the exception of calcium and vitamin D. For other aspects of the diet, accumulating evidence suggests that current healthy-eating advice to decrease sodium intake, to increase potassium intake, and to consume more fresh fruits and vegetables is unlikely to be detrimental to bone health and may be beneficial.

Type
Research Article
Copyright
Copyright © CAB International 2004

References

1Consensus Development Conference. Diagnosis, prophylaxis and treatment of osteoporosis. American Journal of Medicine 1991; 90: 107–10.CrossRefGoogle Scholar
2Prentice, A. Is nutrition important in osteoporosis?. Proceedings of the Nutrition Society 1997; 56: 357–67.CrossRefGoogle ScholarPubMed
3Compston, J. Osteoporosis. In: Crisp, A, ed. The Management of Common Metabolic Bone Disorders. Cambridge: Cambridge University Press. 1993; 2962.CrossRefGoogle Scholar
4Johnell, O. The socioeconomic burden of fractures: today and in the 21st century. American Journal of Medicine 1997; 103: 20S–5S.CrossRefGoogle Scholar
5World Health Organization. Assessment of Fracture Risk and its Application to Screening for Postmenopausal Osteoporosis. WHO Technical Report Series 843. Geneva: World Health Organization, 1994;Google Scholar
6Aspray, TJ, Prentice, A, Cole, TJ, Sawo, Y, Reeve, J, Francis, RM. Low bone mineral content is common but osteoporotic fractures are rare in elderly rural Gambian women. Journal of Bone and Mineral Research 1996; 11: 1018–24.CrossRefGoogle ScholarPubMed
7Prentice, A, Parsons, TJ, Cole, TJ. Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants. American Journal of Clinical Nutrition 1994; 60: 837–42.CrossRefGoogle ScholarPubMed
8Russel-Aulet, M, Wang, J, Thornton, JC, Colt, EWD, Pierson, RN. Bone mineral density and mass in a cross-sectional study of White and Asian women. Journal of Bone and Mineral Research 1993; 8: 575–82.CrossRefGoogle Scholar
9Yan, L, Zhou, B, Prentice, A, Hou, J, Wang, X, Golden, MHN. Epidemiological study of hip fracture in Shenyang, P.R. China. Bone 1997; 24: 151–5.CrossRefGoogle Scholar
10Royal College of Physicians. Fractured Neck of Femur. London: Royal College of Physicians, 1989.Google Scholar
11Sanders, KM, Pasco, JA, Ugoni, AM. et al. The exclusion of high trauma fractures may underestimate the prevalence of bone fragility fractures in the community. The GEELONG osteoporosis study. Journal of Bone and Mineral Research 1998; 13: 1337–42.CrossRefGoogle ScholarPubMed
12Cooper, C, Campion, G, Melton, LJ. Hip fractures in the elderly: a world-wide projection. Osteoporosis International 1992; 2: 285–9.CrossRefGoogle ScholarPubMed
13Melton, LJ 3rd. Epidemiology of fractures. In: Melton, LJ, ed. Osteoporosis: Etiology, Diagnosis, and Management. 2nd ed. Philadelphia Lippincott-Raven 1995; 225–47.Google Scholar
14Ellfors, L, Allander, E, Kanis, JA, Gullberg, B, Johnell, O, Dequeker, J. The variable incidence of hip fracture in southern Europe. The MEDOS study. Osteoporosis International 1994; 4: 253–63.CrossRefGoogle Scholar
15Maggi, S, Kelsey, JL, Litvak, J, Heyse, SP. Incidence of hip fracture in the elderly: a cross-national analysis. Osteoporosis International 1991; 1: 232–41.CrossRefGoogle ScholarPubMed
16Eastell, R, Boyle, IT, Compston, J, et al. Management of male osteoporosis: report of the UK Consensus Group. Quarterly Journal of Medicine 1998; 91: 7192.CrossRefGoogle ScholarPubMed
17Royal College of Physicians. Osteoporosis. Clinical Guidelines for Prevention and Treatment. London: Royal College of Physicians of London, 1999.Google Scholar
18Kannus, P, Parkkari, J, Sievanen, H, Heinonen, A, Vuori, I, Jarvinen, M. Epidemiology of hip fractures. Bone 1996; 18(Suppl. 1): 57S63S.CrossRefGoogle ScholarPubMed
19Lau, EMC, Cooper, C. The epidemiology of osteoporosis. The oriental perspective in a world context. Clinical Orthopaedics and Related Research 1996; 323: 6574.CrossRefGoogle Scholar
20Kanis, J. The epidemiology of hip fracture in Europe. The MEDOS study. Revista Clinica Espanola 1991; 188(Suppl. 1) 12–4.Google Scholar
21O'Neill, TW, Felsenberg, D, Varlow, J, Cooper, C, Kanis, JA, Silman, AJ. The prevelance of vertebral deformity in European men and women: the European Vertebral Osteoporosis Study. Journal of Bone and Mineral Research 1996; 11: 1010–8.CrossRefGoogle Scholar
22Gardsell, P, Johnell, O, Nilsson, BE, Sernbo, I. Bone mass in an urban and a rural population: a comparative, population-based study in southern Sweden. Journal of Bone and Mineral Research 1991; 6: 6775.CrossRefGoogle Scholar
23Ross, PD, Davis, JW, Vogel, JM, Wasnich, RD. A critical review of bone mass and the risk of fractures in osteoporosis. Calcified Tissues International 1990; 46: 149–61.CrossRefGoogle ScholarPubMed
24Gardsell, P, Johnell, O, Nilsson, BE. The predictive value of bone loss for fagility fractures in women: a longitudinal study over 15 years. Calcified Tissues International 1991; 49: 90–4.CrossRefGoogle Scholar
25Cummings, S, Black, D, Nevitt, M, et al. Bone density at various sites for prediction of hip fractures. Lancet 1993; 341: 72–5.CrossRefGoogle ScholarPubMed
26Marshall, D, Johnell, O, Wedel, H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. British Medical Journal 1996; 312: 1254–9.CrossRefGoogle ScholarPubMed
27Faulkner, KG. Bone matters: are density increases necessary to reduce fracture risk?. Journal of Bone and Mineral Research 2000; 15: 183–7.CrossRefGoogle ScholarPubMed
28Prentice, A. Application of DXA and other techniques to the assessment of bone and body composition. In: Cole, TJ, ed. Body Composition Techniques and Assessment in Health and Disease. Society for the Study of Human Biology; vol Soc Study Human Biol Symp Series 36. Cambridge: Cambridge University Press, 1995, 113.Google Scholar
29Cole, TJ, Prentice, A. Bone mineral measurements. British Medical Journal 1992; 305: 1223–4.CrossRefGoogle ScholarPubMed
30Department of Health. Nutrition and Bone Health: With Particular Reference to Calcium and Vitamin D. Report of the Subgroup on Bone Health, Working Group on the Nutritional Status of the Population of the Committee on Medical Aspects of Food and Nutrition Policy. Report on Health and Social Subjects. Number 49 London: The Stationery Office, 1998.Google Scholar
31Parfitt, AM. Morphologic basis of bone mineral measurements: transient and steady state effects of treatment in osteoporosis. Mineral and Electrolyte Metabolism 1980; 4: 273–87.Google Scholar
32Frost, HM. Bone Remodelling and its Relationship to Metabolic Bone Disease. Springfield: Thomas, 1973.Google Scholar
33Kanis, JA. Calcium requirements for optimal skeletal health in women. Calcified Tissue International 1991; 49: S33–41.CrossRefGoogle ScholarPubMed
34Heaney, RP. The bone remodeling transient: Interpreting interventions involving bone-related nutrients. Nutrition Reviews 2001; 59: 327–34.CrossRefGoogle ScholarPubMed
35Garnero, P, Sornay-Rendu, E, Claustrat, B, Delmas, PD. Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study. Journal of Bone and Mineral Research 2000; 15: 1526–36.CrossRefGoogle ScholarPubMed
36Gunnes, M, Lehmann, EH, Mellstrom, D, Johnell, O. The relationship between anthropometric measurements and fractures in women. Bone 1996; 19: 407–13.CrossRefGoogle ScholarPubMed
37Bass, S, Delmas, PD, Pearce, G, Hendrich, E, Tabensky, A, Seeman, E. The differing tempo of growth in bone size, mass, and density in girls is region-specific. Journal of Clinical Investigation 1999; 104: 795804.CrossRefGoogle ScholarPubMed
38Cooper, C, Fall, C, Egger, P, Hobbs, R, Eastell, R, Barker, D. Growth in infancy and bone mass in later life. Annals of the Rheumatic Diseases 1997; 56: 1721.CrossRefGoogle ScholarPubMed
39Fewtrell, MS, Prentice, A, Jones, SC, et al. Bone mineralisation and turnover in preterm infants at 8–12 years of age: the effect of early diet. Journal of Bone and Mineral Research 1999; 14(5): 810–20.CrossRefGoogle ScholarPubMed
40Slemenda, CW, Peacock, M, Hui, S, Zhou, L, Johnston, CC. Reduced rates of skeletal remodeling are associated with increased bone mineral density during the development of peak bone mass. Journal of Bone and Mineral Research 1997; 12: 676–82.CrossRefGoogle Scholar
41Compston, JE. Pharmacological interventions for the prevention of vertebral and nonvertebral fractures in women with postmentopausal osteoporosis: does site-specificity exist?. Bone 2000; 27: 765–8.CrossRefGoogle ScholarPubMed
42Wilkin, TJ, Devendra, D. Bone densitometry is not a good predictor of hip fracture: for. British Medical Journal 2001; 323: 795–7.CrossRefGoogle ScholarPubMed
43Dequeker, J, Luyten, F. Bone densitometry is not a good predictor of hip fracture: against. British Medical Journal 2001; 323: 797–9.Google ScholarPubMed
44Chesnut, CH, 3rd Rosen, CJ. For the Bone Quality Discussion Group. Reconsidering the effects of antiresportive therapies in reducing osteoporotic fracture. Journal of Bone and Mineral Research 2001; 16: 2163–72.CrossRefGoogle Scholar
45Bjarnason, NH, Sarkar, S, Duong, T, Mitlak, B, Delmas, PD, Christiansen, C. Six and twelve month changes in bone turnover are related to reduction in vertebral fracture risk during 3 years of raloxifene treatment in postmenopausal osteoporosis. Osteoporosis International 2001; 12: 922–30.CrossRefGoogle ScholarPubMed
46Riggs, BL, Melton, LJ, 3rd. Bone turnover matters: the raloxifene treatment paradox of dramatic decreases in vertebral fractures without commensurate increases in bone density. Journal of Bone and Mineral Research 2002; 17: 11–4.CrossRefGoogle ScholarPubMed
47Pfeifer, M, Begerow, B, Minne, HW, Abrams, C, Nachtigall, D, Hansen, C. Effects of short-term vitamin D and calcium supplementation on body sway and secondary hyperparathyroidism. Journal of Bone and Mineral Research 2000; 15: 1113–8.CrossRefGoogle ScholarPubMed
48Sogaard, CH, Mosekilde, L, Richards, A, Mosekilde, L. Marked decrease in trabecular bone quality after five years on sodium fluoride therapy assessed by biomechanical testing of iliac crest bone biopsies in osteoporotic patients. Bone 1994; 15: 393400.CrossRefGoogle ScholarPubMed
49Dargent Molina, P, Favier, F, Grandjean, H, et al. Fall-related factors and risk of hip fracture: the EPIDOS prospective study. Lancet 1996; 348: 145–9.CrossRefGoogle ScholarPubMed
50Nguyen, T, Sambrook, P, Kelly, P, et al. Prediction of osteoporotic fractures by postural instability and bone density. British Medical Journal 1993; 307: 1111–5.CrossRefGoogle ScholarPubMed
51De Laet, CE, van Hout, BA, Burger, H, Hofman, A, Pols, HA. Bone density and risk of hip fracture in men and women: cross-sectional analysis. British Medical Journal 1997; 26: 221–5.CrossRefGoogle Scholar
52Prentice, A. The relative contribution of diet and genotype to bone development. Proceedings of the Nutrition Society 2001; 60: 18.CrossRefGoogle ScholarPubMed
53Cooper, C, Aihie, A. Osteoporosis: recent advances in pathogenesis and treatment. Quarterly Journal of Medicine 1994; 87: 203–9.Google ScholarPubMed
54Institute of Medicine Food and Nutrition Board. Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride. Washington, DC: National Academy Press, 1997.Google Scholar
55National Institutes of Health Consensus Development Panel. Optimal calcium intake. Journal of the American Medical Association 1994; 272: 1942–8.CrossRefGoogle Scholar
56Cumming, RG. Calcium intake and bone mass: a quantitative review of the evidence. Calcified Tissues International 1990; 47: 194201.CrossRefGoogle ScholarPubMed
57Welten, DC, Kemper, HCG, Post, GB, Van Staveren, WA. A meta-analysis of the effect of calcium intake on bone mass in young and middle aged females and males. Journal of Nutrition 1995; 125: 2802–13.Google Scholar
58Kreiger, N, Gross, A, Hunter, G. Dietary factors and fracture in postmenopausal women: a case-control study. International Journal of Epidemiology 1992; 21(5): 953–8.CrossRefGoogle ScholarPubMed
59Cummings, SR, Nevitt, MC, Browner, WS, et al. Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. New England Journal of Medicine 1995; 332(12): 767–73.CrossRefGoogle ScholarPubMed
60Wickham, CA, Walsh, K, Cooper, C, et al. Dietary calcium, physical activity, and risk of hip fracture: a prospective study. British Medical Journal 1989; 299(6704): 889–92.CrossRefGoogle ScholarPubMed
61Cooper, C, Barker, DJ, Wickham, C. Physical activity, muscle strength, and calcium intake in fracture of the proximal femur in Britain. British Medical Journal 1988; 297(6661): 1443–6.CrossRefGoogle ScholarPubMed
62Cumming, RG, Klineberg, RJ. Case-control study of risk factors for hip fractures in the elderly. American Journal of Epidemiology 1994; 139(5): 493503.CrossRefGoogle ScholarPubMed
63Hannan, MT, Felson, DT, Dawson-Hughes, B, et al. Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. Journal of Bone and Mineral Research 2000; 15(4): 710–20.CrossRefGoogle ScholarPubMed
64Lau, E, Donnan, S, Barker, DJ, Cooper, C. Physical activity and calcium intake in fracture of the proximal femur in Hong Kong. British Medical Journal 1988; 297(6661): 1441–3.CrossRefGoogle ScholarPubMed
65Holbrook, TL, Barrett-Connor, E, Wingard, DL. Dietary calcium and risk of hip fracture: 14-year prospective population study. Lancet 1988; 2(8619): 1046–9.CrossRefGoogle ScholarPubMed
66Johnell, O, Gullberg, B, Kanis, JA, et al. Risk factors for hip fracture in European women: the MEDOS Study. Mediterranean Osteoporosis Study. Journal of Bone and Mineral Research 1995; 10(11): 1802–15.CrossRefGoogle ScholarPubMed
67Kanis, J, Johnell, O, Gullberg, B, et al. Risk factors for hip fracture in men from southern Europe: the MEDOS study. Mediterranean Osteoporosis Study. Osteoporosis International 1999; 9(1): 4554.CrossRefGoogle ScholarPubMed
68Cumming, RG, Nevitt, MC. Calcium for prevention of osteoporotic fractures in postmenopausal women. Journal of Bone and Mineral Research 1997; 12: 1321–9.CrossRefGoogle ScholarPubMed
69Prentice, A. What are the dietary requirements for calcium and vitamin D?. Calcified Tissue International 2002; 70: 83–8.CrossRefGoogle ScholarPubMed
70Riis, B, Thomsen, K, Christiansen, C. Does calcium supplementation prevent postmenopausal bone loss?. New England Journal of Medicine 1987; 316: 173–7.CrossRefGoogle ScholarPubMed
71Elders, PJM, Lips, P, Netelenbos, JC, et al. Long-term effect of calcium supplementation on bone loss in perimenopausal women. Journal of Bone and Mineral Research 1994; 9: 963–70.CrossRefGoogle Scholar
72Dawson-Hughes, B, Dallal, GE, Krall, EA, Sadowski, L, Sahyoun, N, Tannenbaum, S. A controlled trial of the effect of calcium supplementation on bone density in postmenopausal women. New England Journal of Medicine 1990; 323: 878–83.CrossRefGoogle Scholar
73Riggs, BL, O'Fallon, WM, Muhs, J, O'Connor, MK, Kumar, R, Melton, LJ 3rd . Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women. Journal of Bone and Mineral Research 1998; 13: 168–74.CrossRefGoogle ScholarPubMed
74Reid, IR, Ames, RW, Evans, MC, Gamble, GD, Sharpe, SJ. Effect of calcium supplementation on bone loss in postmenopausal women. New England Journal of Medicine 1993; 328: 460–4.CrossRefGoogle Scholar
75Prince, RP, Devine, A, Dick, I, et al. The effects of calcium supplementation (milk powder or tablets) and exercise on bone density in postmenopausal women. Journal of Bone and Mineral Research 1995; 10: 1068–75.CrossRefGoogle Scholar
76Chevalley, T, Rizzoli, R, Nydegger, V, et al. Effects of calcium supplements on femoral bone mineral density and vertebral fracture rate in vitamin D replete elderly patients. Osteoporosis International 1994; 4: 245–52.CrossRefGoogle ScholarPubMed
77Peacock, M, Liu, G, Carey, M, et al. Effect of a calcium or 25OHD vitamin D3 dietary supplementation on bone loss at the hip in men and women over the age of 60. Journal of Clinical Endocrinology and Metabolism 2000; 85: 3011–9.Google ScholarPubMed
78Dibba, B, Prentice, A, Ceesay, M, Stirling, DM, Cole, TJ, Poskitt, EME. Effect of calcium supplementation on bone mineral accretion in Gambian children accustomed to a low calcium diet. American Journal of Clinical Nutrition 2000; 71: 544–9.CrossRefGoogle Scholar
79Cadogan, J, Eastell, R, Jones, N, Barker, ME. Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. British Medical Journal 1997; 315: 1255–60.CrossRefGoogle ScholarPubMed
80Recker, R, Hinders, S, Davies, KM, et al. Correcting calcium nutritional deficiency prevents spine fractures in elderly women. Journal of Bone and Mineral Research 1996; 11: 1961–6.CrossRefGoogle ScholarPubMed
81Reid, IR, Ames, RW, Evans, MC, Gamble, GD, Sharpe, SJ. Long-term effects of calcium supplementation on bone loss and fractures in postmenopausal women: a randomised controlled trial. American Journal of Medicine 1995; 98: 331–5.CrossRefGoogle Scholar
82Orimo, H, Shiraki, M, Hayashi, T, Nakamura, T. Reduced occurrence of verterbral crush fractures in senile osteoporosis treated with 1(OH)-vitamin D 3. Bone and Mineral 1987; 3: 4752.Google Scholar
83Commission of the European Communities. Nutrient and Energy Intakes for the European Community. Reports of the Scientific Committee for Food. Luxembourg: Office for Official Publications of the European Communities, 1993.Google Scholar
84Garn, SM, Rohmann, CG, Wagner, B. Bone loss is a general phenomenon in man. Federation Proceedings 1967; 26: 1729–36.Google ScholarPubMed
85Lee, WTK, Leung, SSF, Wang, S-H, et al. Double-blind, controlled calcium supplementation and bone mineral accretion in children accustomed to a low-calcium diet. American Journal of Clinical Nutrition 1994; 60: 744–50.CrossRefGoogle ScholarPubMed
86Lau, EMC, Woo, J, Leung, PC, Swaminathan, R, Leung, D. The effects of calcium supplementation and exercise on bone density in elderly Chinese women. Osteoporosis International 1992; 2: 168–73.CrossRefGoogle Scholar
87Prentice, A, Jarjou, LMA, Cole, TJ, Stirling, DM, Dibba, B, Fairweather-Tait, S. Calcium requirements of lactating Gambian mothers: effects of a calcium supplement on breastmilk calcium concentration, maternal bone mineral content, and urinary calcium excretion. American Journal of Clinical Nutrition 1995; 62: 5867.CrossRefGoogle ScholarPubMed
88Prentice, A. Calcium requirements of children. Nutrition Reviews 1995; 53(2): 3740.CrossRefGoogle Scholar
89Prentice, A. Calcium supplementation during breast-feeding. New England Journal of Medicine 1997; 337: 558–9.CrossRefGoogle ScholarPubMed
90Nordin, BEC, Marshall, DH. Dietary requirements for calcium. In: Nordon, BEC, ed. Calcium in Human Biology. London: Springer-Verlag, 1988.CrossRefGoogle Scholar
91Bates, CJ, Carter, GD, Mishra, GD, O'Shea, D, Jones, J, Prentice, A. In a population study, can parathyroid hormone aid the definition of adequate vitamin D status? A study of people aged 65 years and over from the British National Diet and Nutrition Survey. Osteoporosis International 2003; 14: 152–9.CrossRefGoogle Scholar
92Finch, S, Doyle, W, Lowe, C, et al. National Diet and Nutrition Survey: People Aged 65 years and Over. Volume 1: Report of the Diet and Nutrition Survey. London: The Stationery Office, 1998, 637.Google Scholar
93Chapuy, MC, Preziosi, P, Maamer, M, et al. Prevalence of vitamin D insufficiency in an adult normal population. Osteoporosis International 1997; 7(5): 439–43.CrossRefGoogle Scholar
94Khaw, KT, Sneyd, MJ, Compston, J. Bone density, parathyroid hormone and 25-hydroxyvitamin D. British Medical Journal 1992; 350: 263–7.Google Scholar
95Ooms, ME, Roos, JC, Bezemer, PD, Van Der Vijch, WJF, Bouter, LM, Lips, P. Prevention of bone loss by vitamin D supplementation in elderly women: a randomised double blind trial. Journal of Clinical Endocrinology and Metabolism 1995; 80: 1052–8.Google Scholar
96Lips, P, Graafman, WC, Ooms, ME, Bezemer, D, Bouter, LM. Vitamin D supplementation and fracture incidence in elderly persons. A randomized, placebo-controlled clinical trial. Annals of Internal Medicine 1996; 124: 400–6.CrossRefGoogle Scholar
97Heikinheimo, RJ, Inkovaara, JA, Harju, EJ, et al. Annual injection of vitamin D and fractures of aged bones. Calcified Tissues International 1992; 51: 105–10.CrossRefGoogle ScholarPubMed
98Dawson-Hughes, B, Harris, SS, Krall, EA, Dallal, GE. Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. New England Journal of Medicine 1997; 337: 670–6.CrossRefGoogle ScholarPubMed
99Chapuy, MC, Arlot, ME, Duboeuf, F, et al. Vitamin D3 and calcium to prevent hip fractures in elderly women. New England Journal of Medicine 1992; 327: 1637–42.CrossRefGoogle ScholarPubMed
100Chapuy, MC, Arlot, ME, Delmas, PD, Meunier, PJ. Effect of calcium and cholecalciferol treatment for three years on hip fractures in elderly women. British Medical Journal 1994; 308: 1081–2.CrossRefGoogle ScholarPubMed
101Lau, EM, Woo, J, Lam, V, Hong, A. Milk supplementation of the diet of postmenopausal Chinese women on a low calcium intake retards bone loss. Journal of Bone and Mineral Research 2001; 16(9): 1704–9.CrossRefGoogle ScholarPubMed
102Parfitt, AM. Osteoporosis: 50 years of change, mostly in the right direction. In: Ralston, SH, ed. Osteoporosis and Bone Biology: The State of the Art. London: International Medical Press, 2000, 113.Google Scholar
103American Society for Bone and Mineral Research. Primer of the Metabolic Bone Diseases and Disorders of Mineral Metabolism. In: Favus, M, ed. 4th ed. Philadelphia: Lippincott Williams & Wilkins, 1999.Google Scholar
104Department of Health. Dietary Reference Values for Food Energy and Nutrients for the United Kingdom. Report on Health and Social Subjects. vol. 41 London: Her Majesty's Stationery Office, 1991.Google Scholar
105Calvo, MS, Kumar, R, Heath, H 3rd. Persistently elevated parathyroid hormone secretion and action in young women after four weeks of ingesting high phosphorus, low calcium diets. Journal of Clinical Endocrinology and Metabolism 1990; 70: 1334–40.CrossRefGoogle ScholarPubMed
106Bizik, BK, Ding, W, Cerlewski, FL. Evidence that bone resorption of young men is not increased by high dietary phosphorus obtained from milk and cheese. Nutrition Research 1996; 16: 1143–6.CrossRefGoogle Scholar
107Heaney, RP, Rafferty, K. Carbonated beverages and urinary calcium excretion. American Journal of Clinical Nutrition 2001; 74: 343–7.CrossRefGoogle ScholarPubMed
108New, SA, Robins, SP, Campbell, MK, et al. Dietary influences on bone mass and bone metabolism: further evidence of a positive link between fruit and vegetable intake and bone health?. American Journal of Clinical Nutrition 2000; 71: 142–51.CrossRefGoogle Scholar
109Stendig-Lindberg, G, Tepper, R, Leichter, I. Trabecular bone density in a two year controlled trial of oeroral magnesium in osteoporosis. Magnesium Research 1993; 6: 155–63.Google Scholar
110Abelow, BJ, Holford, TR, Insogna, KL. Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calcified Tissue International 1992; 50: 14–8.CrossRefGoogle ScholarPubMed
111Hunt, JR, Gallagher, SK, Johnson, LK, Lykken, GI. High- versus low-meat diets: effects on zinc absorption, iron status, and calcium, copper, iron magnesium, manganese, nitrogen, phosphorus, and zinc balance in postmenopausal women. American Journal of Clinical Nutrition 1995; 62: 621–32.CrossRefGoogle ScholarPubMed
112Hannan, MT, Tucker, KL, Dawson-Hughes, B, Cupples, LA, Felson, DT, Kiel, DP. Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. Journal of Bone and Mineral Research 2000; 15(12): 2504–12.CrossRefGoogle Scholar
113Sellmeyer, DE, Stone, KL, Sebastian, A, Cummings, SR. For the Study of Osteoporotic Fractures Research Group. A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. American Journal of Clinical Nutrition 2001; 73(1): 118–22.CrossRefGoogle Scholar
114Heaney, RP. Protein intake and bone health: the influence of belief systems on the conduct of nutritional science. American Journal of Clinical Nutrition 2001; 73(1): 56.CrossRefGoogle ScholarPubMed
115Sebastian, A, Sellmeyer, DE, Stone, KL, Cummings, SR. Dietary ratio of animal to vegetable protein and rate of bone loss and risk of fracture in postmenopausal women (letter). American Journal of Clinical Nutrition 2001; 74: 411–2.CrossRefGoogle Scholar
116Heaney, RP. Reply to A Sebastian et al. (letter). American Journal of Clinical Nutrition 2001; 74: 412.CrossRefGoogle Scholar
117Mowe, M, Bohmer, T, Kindt, E. Reduced nutritional status in an elderly population (>70 year) is probable before disease and possibly contributes to the development of disease. American Journal of Clinical Nutrition 1994; 59: 317–24.CrossRefGoogle Scholar
118Larsson, J, Unosson, M, Ek, A-C, Nilsson, L, Thorslund, S, Bjurulf, P. Effect of dietary supplement on nutritional status and clinical outcome in 501 geriatric patients—a randomised study. Clinical Nutrition 1990; 9: 179–84.CrossRefGoogle ScholarPubMed
119Lipschitz, DA. Nutritonal assessment and interventions in the elderly. In: Burckhardt, P, Heaney, RP, ed. Nutritional Aspects of Osteoporosis /94. Rome: Ares-Serono Symposia Publications, Challenges of Modern Medicine vol. 7, 1995 177–91.Google Scholar
120Schurch, MA, Rizzoli, R, Slosman, D, Vadas, L, Vergnaud, P, Bonjour, JP. Protein supplements increase serum insulin-like growth factor-1 levels and attenuate proximal femur bone loss in patients with recent hip fracture. Annals of Internal Medicine 1998; 128: 801–9.CrossRefGoogle ScholarPubMed
121Rizzoli, R, Bonjour, JP. Determinants of peak bone mass and mechanisms of bone loss. Osteoporosis International 1999; 9(Suppl 2): S17–23.CrossRefGoogle ScholarPubMed
122World Health Organization. Diet, Nutrition, and the Prevention of Chronic Diseases. WHO Technical Report Series no. 797. Geneva: World Health Organization, 1990.Google Scholar
123Gordon, SL, Corbin, SB. Summary of workshop on drinking water fluoride influence on hip frature and on bone health. Osteoporosis International 1992; 2: 109–17.CrossRefGoogle Scholar
124Szulc, P, Arlot, M, Chapuy, MC, Duboeuf, F, Meunier, PJ, Delmas, PD. Serum undercarboxylated osteocalcin correlates with hip bone mineral density in elderly women. Journal of Bone and Mineral Research 1994; 9: 1591–5.CrossRefGoogle ScholarPubMed
125Shearer, MJ. Role of vitamin K and Gla proteins in the pathophysiology of osteoporosis and vascular calcification. Current Opinion in Clinical Nutrition and Metabolic Care 2000 3: 433–8.CrossRefGoogle ScholarPubMed
126Melhus, H, Michaelsson, K, Kindmark, A, et al. Excessive dietary intake of vitamin A is associated with reduced bone mineral density and increased risk for hip fracture. Annals of Internal Medicine 1998; 129: 770–8.CrossRefGoogle ScholarPubMed
127Prentice, A, Bates, CJ. Adequacy of dietary mineral supply for human bone growth and mineralisation. European Journal of Clinical Nutrition 1994; 48S: 161–77.Google Scholar
128Eaton-Evans, J, McIlrath, EM, Jackson, WE, McCartney, H, Strain, JJ. Copper supplementation, and the maintenance of bone mineral density in middle-aged women. Journal of Trace Element Experimental Medicine 1996; 9: 8794.3.0.CO;2-E>CrossRefGoogle Scholar
129Strause, L, Saltman, P, Smith, KT, Bracker, M, Andon, MB. Spinal bone loss in postmenopausal women supplemented with calcium and trace minerals. Journal of Nutrition 1994; 124: 1060–4.CrossRefGoogle ScholarPubMed
130Meacham, SL, Taper, LJ, Volpe, SL. Effects of boron supplementation on bone mineral density and dietary, blood and urinary calcium, phosphorus, magnesium and boron in female athletes. Environment and Health Perspectives 1994; 102: 7982.Google Scholar
131Dawson-Hughes, B, Fowler, SE, Dalsky, G, Gallagher, C. Sodium excretion influences calcium homeostasis in elderly men and women. Journal of Nutrition 1996; 126: 2107–12.CrossRefGoogle ScholarPubMed
132Evans, CE, Chugtai, AY, Blumsohn, A, Giles, M, Eastell, R. The effects of dietary sodium on calcium metabolism in premenopausal and postmenopausal women. European Journal of Clinical Nutrition 1997; 51: 394–9.CrossRefGoogle ScholarPubMed
133Devine, A, Criddle, RA, Dick, IM, Kerr, RA, Prince, RL. A longitudinal study of the effect of sodium and calcium intakes on regional bone density in postmenopausal women. American Journal of Clinical Nutrition 1995; 62: 740–5.CrossRefGoogle ScholarPubMed
134Ginty, F, Flynn, A, Cashman, KD. The effect of sodium intake on biochemical markers of bone metabolism in young women. British Journal of Nutrition 1998; 79: 343–50.CrossRefGoogle ScholarPubMed
135Tucker, KL, Hannan, MT, Chen, H, Cupples, LA, Wilson, PW, Kiel, DP. Potassium, magnesium, and fruit and vegetable intakes are associated with greater bone mineral density in elderly men and women. American Journal of Clinical Nutrition 1999; 69: 727–36.CrossRefGoogle ScholarPubMed
136Remer, T, Manz, F. Potential renal acid load of foods and its influence on urine pH. Journal of the American Dietetic Association 1995; 95: 791–2.CrossRefGoogle ScholarPubMed
137Reid, DM, New, SA. Nutritional influences on bone mass. British Journal of Nutrition 1997; 56: 977–87.Google ScholarPubMed
138Wood, RJ. Potassium bicarbonate supplementation and calcium metabolism in postmenopausal women: are we barking up the wrong tree?. Nutrition Reviews 1994; 52: 278–80.Google ScholarPubMed
139Sebastian, A, Harris, ST, Ottaway, JH, Todd, KM, Morris, RC. Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate. New England Journal of Medicine 1994; 330: 1776–81.CrossRefGoogle ScholarPubMed
140Bingham, SA, Atkinson, C, Liggins, J, Bluck, L, Coward, A. Phyto-oestrogens: where are we now?. British Journal of Nutrition 1998; 79: 393406.CrossRefGoogle ScholarPubMed
141Kardinaal, AF, Morton, MS, Bruggemann-Rotgans, IE, van-Beresteijn, EC. Phyto-oestrogen excretion and rate of bone loss in postmenopausal women. European Journal of Clinical Nutrition 1998; 52: 850–5.CrossRefGoogle ScholarPubMed
142Ho, SC, Chan, SG, Yi, Q, Wong, E, Leung, PC. Soy intake and the maintenance of peak bone mass in Hong Kong Chinese women. Journal of Bone and Mineral Research 2001; 16: 1363–9.CrossRefGoogle ScholarPubMed
143Grainge, MJ, Coupland, CA, Cliffe, SJ, Chilvers, CE, Hosking, DJ. Cigarette smoking, alcohol and caffeine consumtpion and bone mineral density in postmenopausal women. The Nottingham EPIC Study Group. Osteoporosis International 1998; 8: 355–63.CrossRefGoogle Scholar
144Lloyd, T, Johnson-Rollongs, N, Eggli, DF, Kieselhorst, K, Mauger, EA, Cusatis, DC. Bone status among postmenopausal women with different habitual caffeine intakes: a longitudinal investigation. Journal of the American College of Nutrition 2000; 19: 256–61.CrossRefGoogle ScholarPubMed
145Conlisk, AJ, Galuska, DA. Is caffeine associated with bone mineral density in young adult women?. Preventative Medicine 2000; 31: 562–8.CrossRefGoogle ScholarPubMed
146Rapuri, PB, Gallagher, JC, Kinyamu, HK, Ryschon, KL. Caffeine intake increases the rate of bone loss in elderly women and interacts with vitamin D receptor genotypes. American Journal of Clinical Nutrition 2001; 74: 694700.CrossRefGoogle ScholarPubMed
147Parsons, TJ, Prentice, A, Smith, EA, Cole, TJ, Compston, JE. Bone mineral mass consolidation in young British adults. Journal of Bone and Mineral Research 1996; 11: 264–74.CrossRefGoogle ScholarPubMed
148Baumgartner, RN, Stauber, PM, Koehler, KM, Romero, L, Garry, PJ. Associations of fat and muscle masses with bone mineral in elderly men and women. American Journal of Clinical Nutrition 1996; 63: 365–72.CrossRefGoogle ScholarPubMed
149Honkanen, R, Kroger, H, Alhava, E, Turpeinen, P, Tuppurainen, M, Saarikoski, S. Lactose intolerance associated with fractures of weight-bearing bones in Finnish women aged 38–57 years. Bone 1997; 21: 473–7.CrossRefGoogle ScholarPubMed
150Harma, M, Alhava, E. Is lactose malabsorption a risk factor for fractures of the elderly?. Annales Chirurgiae et Gynaecologiae 1988; 77: 180–3.Google ScholarPubMed
151Goulding, A, Taylor, RW, Keil, D, Gold, E, Lewis-Barned, NJ, Williams, SM. Lactose malabsorption and rate of bone loss in older women. Age and Ageing 1999; 28: 175–80.CrossRefGoogle ScholarPubMed