Dairy and bone health

Journal of the American College of Nutrition

Volumn 28, Issue , 2009, Pages 82S-90S

  Heaney, Robert P ^a  

^a CREIGHTON UNIVERSITY   (United States)

Author keywords

Bone; Bone mass; Calcium; Dairy foods; Milk; Osteoporosis; Potassium; Vitamin D

Indexed keywords

CALCIUM; CYANOCOBALAMIN; MAGNESIUM; PHOSPHORUS; POTASSIUM; SODIUM; TRACE ELEMENT; VITAMIN D; VITAMIN K GROUP; ZINC;

BONE MASS; BONE REMODELING; BONE STRUCTURE; CALCIUM INTAKE; DAIRY PRODUCT; DIET SUPPLEMENTATION; DIETARY INTAKE; HEALTH CARE COST; HUMAN; MUSCULOSKELETAL FUNCTION; NUTRITIONAL SUPPORT; NUTRITIONAL VALUE; OSTEOPOROSIS; POTASSIUM INTAKE; PROTEIN INTAKE; REVIEW; VITAMIN INTAKE; BONE; NUTRITION; NUTRITIONAL REQUIREMENT; PHYSIOLOGY;

BONE AND BONES; CALCIUM, DIETARY; DAIRY PRODUCTS; DIETARY PROTEINS; HUMANS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; NUTRITIONAL REQUIREMENTS; OSTEOPOROSIS; POTASSIUM, DIETARY;

EID: 70349247916     PISSN: 07315724     EISSN: 15411087     Source Type: Journal    
DOI: 10.1080/07315724.2009.10719808     Document Type: Article

References (94)

1. Ilich JZ, Kerstetter JE: Nutrition in bone health revisited: a story beyond calcium. J Am Coll Nutr 19:715–37, 2000.
2. Teegarden D, Lyle RM, McCabe GP, McCabe LD, Proulx WR, Michon K, Knight AP, Johnston CC, Weaver CM: Dietary calcium, protein, and phosphorus are related to bone mineral density and content in young women. Am J Clin Nutr 68:749–754, 1998.
3. National Osteoporosis Foundation: www.nof.org/osteoporosis/diseasefacts.htm 2008.
4. Dawson-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. N Engl J Med 337:670–676, 1997.
5. Chapuy MC, Arlot ME, Duboeuf F, Brun J, Crouzet B, Arnaud S, Delmas PD, Meunier PJ: Vitamin D3 and calcium to prevent hip fractures in the elderly women. N Engl J Med 327:1637–1642, 1992.
6. Power ML, Heaney RP, Kalkwarf HJ, Pitkin RM, Repke JT, Tsang RC, Schulkin J: The role of calcium in health and disease. Am J Obstet Gynecol 181:1560–1569, 1999.
7. Wosje KS, Specker BL: Role of calcium in bone health during childhood. Nutr Rev 58:253–268, 2000.
8. Heaney RP: Calcium in the prevention and treatment of osteoporosis. J Intern Med 231:169–180, 1992.
9. Nieves JW, Barrett-Connor E, Siris ES, Zion M, Barlas S, Chen YT: Calcium and vitamin D intake influence bone mass, but not short-term fracture risk, in Caucasian postmenopausal women from the National Osteoporosis Risk Assessment (NORA) study. Osteoporos Int 19:673–679, 2008.
10. Nieves JW, Golden AL, Siris E, Kelsey JL, Lindsay R: Teenage and current calcium intake are related to bone mineral density of the hip and forearm in women aged 30–39 years. Am J Epidemiol 141:342–351, 1995.
11. Holbrook TL, Barrett-Connor E, Wingard DL: Dietary calcium and risk of hip fracture: 14-year prospective population study. Lancet 2:1046–1049, 1988.
12. Weaver CM: The growing years and prevention of osteoporosis in later life. Proc Nutr Soc 59:303–306, 2000.
13. Heaney RP: Calcium, dairy products and osteoporosis. J Am Coll Nutr 19(2 Suppl):83S–99S, 2000.
14. Heaney RP, Weaver CM: Newer perspectives on calcium nutrition and bone quality. J Am Coll Nutr 24(6 Suppl):574S–81S, 2005.
15. Heaney RP: Is the paradigm shifting? Bone 33:457–465, 2003.
16. Jackman LA, Millane SS, Martin BR, Wood OB, McCabe GP, Peacock M, Weaver CM: Calcium retention in relation to calcium intake and postmenarcheal age in adolescent females. Am J Clin Nutr 66:327–333, 1997.
17. Matkovic V, Heaney RP: Calcium balance during human growth: evidence for threshold behavior. Am J Clin Nutr 55:992–996, 1992.
18. Hunt CD, Johnson LK: Calcium requirements: new estimations for men and women by cross-sectional statistical analyses of calcium balance data from metabolic studies. Am J Clin Nutr 86:1054–1063, 2007.
19. Moore CE, Murphy MM, Holick MF: Vitamin D intakes by children and adults in the United States differ among ethnic groups. J Nutr 135:2478–2485, 2005.
20. Kimball S, Fuleihan Gel H, Vieth R: Vitamin D: a growing perspective. Crit Rev Clin Lab Sci 45:339–414, 2008.
21. Raiten DJ, Picciano MF: Vitamin D and health in the 21st century: bone and beyond. Executive summary. Am J Clin Nutr 80(Suppl6): 1673S–1677S, 2004.
22. Weaver CM: Vitamin D, calcium homeostasis, and skeleton accretion in children. J Bone Miner Res 22(Suppl 2):45–49, 2007.
23. Tylavsky FA, Ryder KA, Lyytikainen A, Cheng S: Vitamin D, parathyroid hormone, and bone mass in adolescents. J Nutr 135: 2735S–2738S, 2005.
24. Feskanich D, Willett WC, Colditz GA: Calcium, vitamin D, milk consumption, and hip fractures: a prospective study among postmenopausal women. Am J Clin Nutr 77:504–511, 2003.
25. Heaney RP: The Vitamin D requirement in health and disease. J Steroid Biochem Mol Biol 97:13–19, 2005.
26. Heikinheimo RJ, Inkovaara JA, Harju EJ, Haavisto MV, Kaarela RH, Kataja JM, Kokko AM, Kolho LA, Rajala SA: Annual injection of vitamin D and fractures of aged bones. Calcif Tissue Int 51:105–110, 1992.
27. Ooms ME, Roos JC, Bezemer PD, van der Vijgh WJ, Bouter LM, Lips P: Prevention of bone loss by vitamin D supplementation in elderly women: a randomized double-blind trial. J Clin Endocrinol Metab 80:1052–1058, 1995.
28. Trivedi DP, Doll R, Khaw KT: Effect of four monthly oral vitamin D3 (cholecalciferol) supplementation on fractures and mortality in men and women living in the community: randomised double blind controlled trial. BMJ 326:469, 2003.
29. Bischoff-Ferrari HA, Willett WC, Wong JB, Giovannucci E, Dietrich T, Dawson-Hughes B: Fracture prevention with vitamin D supplementation: a meta-analysis of randomized controlled trials. JAMA 293:2257–2264, 2005.
30. Dawson-Hughes B, Harris SS: Calcium intake influences the association of protein intake with rates of bone loss in elderly men and women. Am J Clin Nutr 75:773–779, 2002.
31. Cooper C, Atkinson EJ, Hensrud DD, Wahner HW, O’Fallon WM, Riggs BL, Melton LJ, 3rd: Dietary protein intake and bone mass in women. Calcif Tissue Int 58:320–325, 1996.
32. Heaney RP: Effects of protein on the calcium economy. In Burckhardt P, Heaney RP, Dawson-Hughes B, eds: “Nutritional Aspects of Osteoporosis 2006.” Amsterdam: Elsevier Inc., pp 191–197, 2007.
33. Conigrave AD, Brown EM, Rizzoli R: Dietary protein and bone health: roles of amino acid-sensing receptors in the control of calcium metabolism and bone homeostasis. Annu Rev Nutr 28: 131–155, 2008.
34. Feskanich D, Willett WC, Stampfer MJ, Colditz GA: Protein consumption and bone fractures in women. Am J Epidemiol 143: 472–479, 1996.
35. Meyer HE, Pedersen JI, Loken EB, Tverdal A: Dietary factors and the incidence of hip fracture in middle-aged Norwegians. A prospective study. Am J Epidemiol 145:117–123, 1997.
36. Munger RG, Cerhan JR, Chiu BC: Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am J Clin Nutr 69:147–152, 1999.
37. Hannan 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. J Bone Miner Res 15:2504–2512, 2000.
38. Price JS, Oyajobi BO, Russell RG: The cell biology of bone growth. Eur J Clin Nutr 48(Suppl 1):S131–S149, 1994.
39. Bonjour JP: Dietary protein: an essential nutrient for bone health. J Am Coll Nutr 24(Suppl 6):526S–536S, 2005.
40. Bonjour JP, Schurch MA, Rizzoli R: Nutritional aspects of hip fractures. Bone 18(Suppl 3):139S–144S, 1996.
41. Delmi M, Rapin CH, Bengoa JM, Delmas PD, Vasey H, Bonjour JP: Dietary supplementation in elderly patients with fractured neck of the femur. Lancet 335:1013–1016, 1990.
42. Heaney RP: Effects of protein on the calcium economy. In Burckhardt P, Dawson-Hughes B, Heaney RP, eds: “Nutritional Aspects of Osteoporosis.” Amsterdam: Elsevier Inc., pp 773–779, 2007.
43. Bugel S: Vitamin K and bone health in adult humans. Vitam Horm 78:393–416, 2008.
44. Cashman KD, O’Connor E: Does high vitamin K1 intake protect against bone loss in later life? Nutr Rev 66:532–538, 2008.
45. Cockayne S, Adamson J, Lanham-New S, Shearer MJ, Gilbody S, Torgerson DJ: Vitamin K and the prevention of fractures: systematic review and meta-analysis of randomized controlled trials. Arch Intern Med 166:1256–1261, 2006.
46. Heiss C, Hoesel LM, Wehr U, Wenisch S, Drosse I, Alt V, Meyer C, Horas U, Schieker M, Schnettler R: Diagnosis of osteoporosis with vitamin k as a new biochemical marker. Vitam Horm 78:417–434, 2008.
47. Lanham-New SA: Importance of calcium, vitamin D and vitamin K for osteoporosis prevention and treatment. Proc Nutr Soc 67: 163–176, 2008.
48. Harrington M, Cashman KD: High salt intake appears to increase bone resorption in postmenopausal women but high potassium intake ameliorates this adverse effect. Nutr Rev 61(5 Pt 1):179–183, 2003.
49. Jones G, Beard T, Parameswaran V, Greenaway T, von Witt R: A population-based study of the relationship between salt intake, bone resorption and bone mass. Eur J Clin Nutr 51:561–565, 1997.
50. Lin PH, Ginty F, Appel LJ, Aickin M, Bohannon A, Garnero P, Barclay D, Svetkey LP: The DASH diet and sodium reduction improve markers of bone turnover and calcium metabolism in adults. J Nutr 133:3130–3136, 2003.
51. Mizushima S, Tsuchida K, Yamori Y: Preventive nutritional factors in epidemiology: interaction between sodium and calcium. Clin Exp Pharmacol Physiol 26:573–575, 1999.
52. Heaney RP: Phosphorus nutrition and the treatment of osteoporosis. Mayo Clin Proc 79:91–97, 2004.
53. Tucker 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. Am J Clin Nutr 69:727–736, 1999.
54. Kitchin B, Morgan SL: Not just calcium and vitamin D: other nutritional considerations in osteoporosis. Curr Rheumatol Rep 9:85–92, 2007.
55. Lanham-New SA: The balance of bone health: tipping the scales in favor of potassium-rich, bicarbonate-rich foods. J Nutr 138:172S–177S, 2008.
56. Macdonald HM, New SA, Fraser WD, Campbell MK, Reid DM: Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women. Am J Clin Nutr 81:923–933, 2005.
57. Dhonukshe-Rutten RA, Pluijm SM, de Groot LC, Lips P, Smit JH, van Staveren WA: Homocysteine and vitamin B12 status relate to bone turnover markers, broadband ultrasound attenuation, and fractures in healthy elderly people. J Bone Miner Res 20:921–929, 2005.
58. Nielsen FH, Milne DB: A moderately high intake compared to a low intake of zinc depresses magnesium balance and alters indices of bone turnover in postmenopausal women. Eur J Clin Nutr 58:703–710, 2004.
59. van Summeren MJ, van Coeverden SC, Schurgers LJ: VitaminK status is associated with childhood bone mineral content. Br J Nutr 100:852–858, 2008.
60. Knapen MH, Schurgers LJ, Vermeer C: Vitamin K2 supplementation improves hip bone geometry and bone strength indices in postmenopausal women. Osteoporos Int 18:963–972, 2007.
61. Teucher B, Dainty JR, Spinks CA, Majsak-Newman G, Berry DJ, Hoogewerff JA, Foxall RJ, Jakobsen J, Cashman KD, Flynn A, Fairweather-Tait SJ: Sodium and bone health: impact of moderately high and low salt intakes on calcium metabolism in postmenopausal women. J Bone Miner Res 23:1477–1485, 2008.
62. Calvo MS, Kumar R, Heath H: Persistently elevated parathyroid hormone secretion and action in young women after four weeks of ingesting high phosphorus, low calcium diets. J Clin Endocrinol Metab 70:1334–1340, 1990.
63. Brot C, Jorgensen N, Madsen OR, Jensen LB, Sorensen OH: Relationships between bone mineral density, serum vitamin D metabolites and calcium:phosphorus intake in healthy perimenopausal women. J Intern Med 245:509–516, 1999.
64. Barger-Lux MJ, Heaney RP: Effects of calcium restriction on metabolic characteristics of premenopausal women. J Clin Endocrinol Metab 76:103–197, 1993.
65. Ryder KM, Shorr RI, Bush AJ, Kritchevsky SB, Harris T, Stone K, Cauley J, Tylavsky FA: Magnesium intake from food and supplements is associated with bone mineral density in healthy older white subjects. J Am Geriatr Soc 53:1875–1880, 2005.
66. Frassetto LA, Morris RC, Jr, Sellmeyer DE, Sebastian A: Adverse effects of sodium chloride on bone in the aging human population resulting from habitual consumption of typical American diets. J Nutr 138:419S–422S, 2008.
67. Sellmeyer DE, Schloetter M, Sebastian A: Potassium citrate prevents increased urine calcium excretion and bone resorption induced by a high sodium chloride diet. J Clin Endocrinol Metab 87:2008–2012, 2002.
68. Gjesdal CG, Vollset SE, Ueland PM, Refsum H, Drevon CA, Gjessing HK, Tell GS: Plasma total homocysteine level and bone mineral density: the Hordaland Homocysteine Study. Arch Intern Med 166:88–94, 2006.
69. Dhonukshe-Rutten RA, Lips M, de Jong N, Chin APMJ, Hiddink GJ, van Dusseldorp M, De Groot LC, van Staveren WA: Vitamin B-12 status is associated with bone mineral content and bone mineral density in frail elderly women but not in men. J Nutr 133:801–807, 2003.
70. Morris MS, Jacques PF, Selhub J: Relation between homocysteine and B-vitamin status indicators and bone mineral density in older Americans. Bone 37:234–242, 2005.
71. Dietary Guidelines Advisory Committee Report. In http://www.health.gov/dietaryguidelines, 2005.
72. Lau EM, Lynn H, Chan YH, Lau W, Woo J: Benefits of milk powder supplementation on bone accretion in Chinese children. Osteoporos Int 15:654–658, 2004.
73. Du X, Zhu K, Trube A, Zhang Q, Ma G, Hu X, Fraser DR, Greenfield H: School-milk intervention trial enhances growth and bone mineral accretion in Chinese girls aged 10–12 years in Beijing. Br J Nutr 92:159–168, 2004.
74. Cheng S, Lyytikainen A, Kroger H, Lamberg-Allardt C, Alen M, Koistinen A, Wang QJ, Suuriniemi M, Suominen H, Mahonen A, Nicholson PH, Ivaska KK, Korpela R, Ohlsson C, Vaananen KH, Tylavsky F: Effects of calcium, dairy product, and vitamin D supplementation on bone mass accrual and body composition in 10–12-y-old girls: a 2-y randomized trial. Am J Clin Nutr 82: 1115–1126, Quiz 1147–1148, 2005.
75. Moschonis G, Manios Y: Skeletal site-dependent response of bone mineral density and quantitative ultrasound parameters following a 12-month dietary intervention using dairy products fortified with calcium and vitamin D: the Postmenopausal Health Study. Br J Nutr 96:1140–1148, 2006.
76. Manios Y, Moschonis G, Trovas G, Lyritis GP: Changes in biochemical indexes of bone metabolism and bone mineral density after a 12-mo dietary intervention program: the Postmenopausal Health Study. Am J Clin Nutr 86:781–789, 2007.
77. Huncharek M, Muscat J, Kupelnick B: Impact of dairy products and dietary calcium on bone-mineral content in children: results of a meta-analysis. Bone 43:312–321, 2008.
78. Chevalley T, Rizzoli R, Nydegger V, Slosman D, Rapin CH, Michel JP, Vasey H, Bonjour JP: Effects of calcium supplements on femoral bone mineral density and vertebral fracture rate in vitamin-D-replete elderly patients. Osteoporos Int 4:245–252, 1994.
79. Recker RR, Hinders S, Davies KM, Heaney RP, Stegman MR, Lappe JM, Kimmel DB: Correcting calcium nutritional deficiency prevents spine fractures in elderly women. J Bone Miner Res 11:1961–1966, 1996.
80. Chapuy MC, Arlot ME, Delmas PD, Meunier PJ: Effect of calcium and cholecalciferol treatment for three years on hip fractures in elderly women. BMJ 308:1081–1082, 1994.
81. Diez-Perez A, Gonzalez-Macias J, Marin F, Abizanda M, Alvarez R, Gimeno A, Pegenaute E, Vila J: Prediction of absolute risk of non-spinal fractures using clinical risk factors and heel quantitative ultrasound. Osteoporos Int 18:629–639, 2007.
82. Britten P, Lyon J, Weaver CM, Kris-Etherton PM, Nicklas TA, Weber JA, Davis CA: MyPyramid food intake pattern modeling for the Dietary Guidelines Advisory Committee. J Nutr Educ Behav 38(Suppl 6):S143–S152, 2006.
83. Gao X, Wilde PE, Lichtenstein AH, Tucker KL: Meeting adequate intake for dietary calcium without dairy foods in adolescents aged 9 to 18 years (National Health and Nutrition Examination Survey 2001–2002). J Am Diet Assoc 106:1759–1765, 2006.
84. Heaney RP, Dowell MS, Rafferty K, Bierman J: Bioavailability of the calcium in fortified soy imitation milk, with some observations on method. Am J Clin Nutr 71:1166–1169, 2000.
85. Heaney RP, Rafferty K, Bierman J: Not all calcium-fortified beverages are equal. Nutr today 40:39–44, 2005.
86. Heaney RP, Dowell MS, Barger-Lux MJ: Absorption of calcium as the carbonate and citrate salts, with some observations on method. Osteoporos Int 9:19–23, 1999.
87. Heaney RP, Dowell MS, Bierman J, Hale CA, Bendich A: Absorbability and cost effectiveness in calcium supplementation. J Am Coll Nutr 20:239–246, 2001.
88. Bonjour JP, Chevalley T, Ammann P, Slosman D, Rizzoli R: Gain in bone mineral mass in prepubertal girls 3.5 years after discontinuation of calcium supplementation: a follow-up study. Lancet 358:1208–1212, 2001.
89. Lee WT, Leung SS, Leung DM, Wang SH, Xu YC, Zeng WP, Cheng JC: Bone mineral acquisition in low calcium intake children following the withdrawal of calcium supplement. Acta Paediatr 86:570–576, 1997.
90. Slemenda 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 skeletal mass. J Bone Miner Res 12:676–682, 1997.
91. Lappe JM, Davies KM, Travers-Gustafson D, Heaney RP: Vitamin D status in a rural postmenopausal female population. J Am Coll Nutr 25:395–402, 2006.
92. McCarron DA, Heaney RP: Estimated healthcare savings associated with adequate dairy food intake. Am J Hypertens 17:88–97, 2004.
93. U.S. Department of Health and Human Services: “Bone Health and Osteoporosis: A Report of the Surgeon General.” Rockville, MD: U.S. Department of Health and Human Services, Office of the Surgeon General, p 57, 2004.
94. Barger-Lux MJ, Heaney RP, Packard PT, Lappe JM, Recker RR: Nutritional correlates of low calcium intake. Clin Appl Nutr 2:39–44, 1992.