Dietary Protein Intake above the Current RDA and Bone Health: A Systematic Review and Meta-Analysis

Journal of the American College of Nutrition

Volumn 36, Issue 6, 2017, Pages 481-496

  Wallace, Taylor C ^a,b   Frankenfeld, Cara L ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b Think Healthy Group Inc LLC   (United States)

Author keywords

bone; bone density; calcium; fractures; Protein

Indexed keywords

ALKALINE PHOSPHATASE; AMINO TERMINAL TELOPEPTIDE; BIOLOGICAL MARKER; CALCIUM; CARBOXY TERMINAL TELOPEPTIDE; COLLAGEN TYPE 1; DEOXYPYRIDINOLINE; OSTEOCALCIN; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 3;

ACIDURIA; BONE DENSITY; BONE DISEASE; BONE FRAGILITY; BONE TURNOVER; CALCIUM ABSORPTION; CALCIUM BALANCE; CLINICAL OUTCOME; CORTICAL BONE; DIETARY REFERENCE INTAKE; DISTAL RADIUS; FEMORAL NECK; FOREARM FRACTURE; FRACTURE; FRAGILITY FRACTURE; HIP FRACTURE; HUMAN; LUMBAR SPINE; META ANALYSIS; POSTMENOPAUSE; PROTEIN INTAKE; REVIEW; SPINE FRACTURE; SYSTEMATIC REVIEW; TIBIA; TRABECULAR BONE; ULNA; ADMINISTRATION AND DOSAGE; DRUG EFFECTS; METABOLISM; URINE;

BONE DENSITY; CALCIUM; DIETARY PROTEINS; HUMANS; RECOMMENDED DIETARY ALLOWANCES;

EID: 85028414964     PISSN: 07315724     EISSN: 15411087     Source Type: Journal    
DOI: 10.1080/07315724.2017.1322924     Document Type: Review

References (139)

1. Heaney RP, Layman DK, :Amount and type of protein influences bone health. Am J Clin Nutr 87:1567S–1570S, 2008.
2. EFSA Panel on Dietetic Products, Nutrition and Allergies:Scientific opinion on dietary reference values for protein. EFSA J 10:2557–2566, 2012.
3. National Academy of Medicine, Panel on Micronutrients:“Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein and Amino Acids.” Washington, DC:National Academies Press, 2005.
4. Sherman H, :Calcium requirement of maintenance in man. J Biol Chem 44:21–27, 1920.
5. Kerstetter JE, Allen LH, :Protein intake and calcium homeostasis. Adv Nutr Res 9:167–181, 1994.
6. Hegsted M, Linkswiler HM, :Long-term effects of level of protein intake on calcium metabolism in young adult women. J Nutr 111:244–251, 1981.
7. Schuette SA, Hegsted M, Zemel MB, Linkswiler HM, :Renal acid, urinary cyclic AMP, and hydroxyproline excretion as affected by level of protein, sulfur amino acid, and phosphorus intake. J Nutr 111:2106–2116, 1981.
8. Schuette SA, Zemel MB, Linkswiler HM, :Studies on the mechanism of protein-induced hypercalciuria in older men and women. J Nutr 110:305–315, 1980.
9. Anand CR, Linkswiler HM, :Effect of protein intake on calcium balance of young men given 500 mg calcium daily. J Nutr 104:695–700, 1974.
10. Hegsted M, Schuette SA, Zemel MB, Linkswiler HM, :Urinary calcium and calcium balance in young men as affected by level of protein and phosphorus intake. J Nutr 111:553–562, 1981.
11. Kim Y, Linkswiler HM, :Effect of level of protein intake on calcium metabolism and on parathyroid and renal function in the adult human male. J Nutr 109:1399–1404, 1979.
12. Spencer H, Kramer L, DeBartolo M, Norris C, Osis D, :Further studies of the effect of a high protein diet as meat on calcium metabolism. Am J Clin Nutr 37:924–929, 1983.
13. Allen LH, Oddoye EA, Margen S, :Protein-induced hypercalciuria:a longer term study. Am J Clin Nutr 32:741–749, 1979.
14. Kerstetter JE, O'Brien KO, Caseria DM, Wall DE, Insogna KL, :The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab 90:26–31, 2005.
15. Hunt JR, Johnson LK, Fariba Roughead ZK, :Dietary protein and calcium interact to influence calcium retention:a controlled feeding study. Am J Clin Nutr 89:1357–1365, 2009.
16. Roughead ZK, :Controlled high meat diets do not affect calcium retention or indices of bone status in healthy postmenopausal women. J Nutr 133:1020–1026, 2003.
17. Darling AL, Millward DJ, Torgerson DJ, Hewitt CE, Lanham-New SA, :Dietary protein and bone health:a systematic review and meta-analysis. Am J Clin Nutr 90:1674–1692, 2009.
18. Wu AM, Sun XL, Lv QB, Zhou Y, Xia DD, Xu HZ, Huang QS, Chi YL, :The relationship between dietary protein consumption and risk of fracture:a subgroup and dose–response meta-analysis of prospective cohort studies. Sci Rep 5:9151, 2015.
19. Shams-White MM, Chung M, Du M, Fu Z, Insogna KL, Karlsen MC, LeBoff MS, Shapses SA, Sackey J, Wallace TC, Weaver CM, :Dietary protein and bone health:a systematic review and meta-analysis. Am J Clin Nutr 105:1528–1543, 2017.
20. Moher D, Liberati A, Tetzlaff J, Altman DG, and the PRISMA Group:Preferred reporting items for systematic reviews and meta-analyses:the PRISMA statement. PLoS Med 6:e1000097, 2009.
21. Adolphi B, Scholz-Ahrens KE, de Vrese M, Acil Y, Laue C, Schrezenmeir J, :Short-term effect of bedtime consumption of fermented milk supplemented with calcium, inulin-type fructans and caseinphosphopeptides on bone metabolism in healthy, postmenopausal women. Eur J Nutr 48:45–53, 2009.
22. Allen LH, Oddoye EA, Margen S, :Protein-induced hypercalciuria:a longer term study. Am J Clin Nutr 32:741–749, 1979.
23. Aoe S, Koyama T, Toba Y, Itabashi A, Takada Y, :A controlled trial of the effect of milk basic protein (MBP) supplementation on bone metabolism in healthy menopausal women. Osteoporos Int 16:2123–128, 2005.
24. Appleby P, Roddam A, Allen N, Key T, :Comparative fracture risk in vegetarians and nonvegetarians in EPIC–Oxford. Eur J Clin Nutr 61:1400–1406, 2007.
25. Arjmandi BH, Khalil DA, Smith BJ, Lucas EA, Juma S, Payton ME, Wild RA, :Soy protein has a greater effect on bone in postmenopausal women not on hormone replacement therapy, as evidenced by reducing bone resorption and urinary calcium excretion. J Clin Endocrinol Metab 88:1048–1054, 2003.
26. Arjmandi BH, Lucas EA, Khalil DA, Devareddy L, Smith BJ, McDonald J, Arquitt AB, Payton ME, Mason C, :One year soy protein supplementation has positive effects on bone formation markers but not bone density in postmenopausal women. Nutr J 4:8, 2005.
27. Bachrach-Lindstrom M, Unosson M, Ek AC, Arnqvist HJ, :Assessment of nutritional status using biochemical and anthropometric variables in a nutritional intervention study of women with hip fracture. Clin Nutr 20:217–223, 2001.
28. Ballard TLP, Specker BL, Binkley TL, Vukovich MD, :Effect of protein supplementation during a 6-month strength and conditioning program on areal and volumetric bone parameters. Bone 38:898–904, 2006.
29. Ballard TL, Clapper JA, Specker BL, Binkley TL, Vukovich MD, :Effect of protein supplementation during a 6-mo strength and conditioning program on insulin-like growth factor I and markers of bone turnover in young adults. Am J Clin Nutr 81:1442–1448, 2005.
30. Beasley JM, LaCroix AZ, Larson JC, Huang Y, Neuhouser ML, Tinker LF, Jackson R, Snetselaar L, Johnson KC, Eaton CB, et al.:Biomarker-calibrated protein intake and bone health in the Women's Health Initiative clinical trials and observational study. Am J Clin Nutr 99:934–940, 2014.
31. Benetou V, Orfanos P, Pettersson-Kymmer U, Bergström U, Svensson O, Johansson I, Berrino F, Tumino R, Borch KB, Lund E, et al.:Mediterranean diet and incidence of hip fractures in a European cohort. Osteoporos Int 24:1587–1598, 2013.
32. Bihuniak JD, Simpson CA, Sullivan RR, Caseria DM, Kerstetter JE, Insogna KL, :Dietary protein-induced increases in urinary calcium are accompanied by similar increases in urinary nitrogen and urinary urea:a controlled clinical trial. J Acad Nutr Diet 113:447–451, 2013.
33. Bihuniak JD, Sullivan RR, Simpson CA, Caseria DM, Huedo-Medina TB, O'Brien KO, Kerstetter JE, Insogna KL, :Supplementing a low-protein diet with dibasic amino acids increases urinary calcium excretion in young women. J Nutr 144:282–288, 2014.
34. Block GD, Wood RJ, Allen LH, :A comparison of the effects of feeding sulfur amino acids and protein on urine calcium in man. Am J Clin Nutr 33:2128–2136, 1980.
35. Botella-Carretero JI, Iglesias B, Balsa JA, Arrieta F, Zamarron I, Vazquez C, :Perioperative oral nutritional supplements in normally or mildly undernourished geriatric patients submitted to surgery for hip fracture:a randomized clinical trial. Clin Nutr 29:574–579, 2010.
36. Botella-Carretero JI, Iglesias B, Balsa JA, Zamarron I, Arrieta F, Vazquez C, :Effects of oral nutritional supplements in normally nourished or mildly undernourished geriatric patients after surgery for hip fracture:a randomized clinical trial. JPEN J Parenter Enteral Nutr 32:120–128, 2008.
37. Brockis JG, Levitt AJ, Cruthers SM, :The effects of vegetable and animal protein diets on calcium, urate and oxalate excretion. Br J Urol 54:590–593, 1982.
38. Brownbill RA, Petrosian M, Ilich JZ, :Association between dietary conjugated linoleic acid and bone mineral density in postmenopausal women. J Am Coll Nutr 4:177–181, 2005.
39. Cameron ID, Kurrle SE, Uy C, Lockwood KA, Au L, Schaafsma FG, :Effectiveness of oral nutritional supplementation for older women after a fracture:rationale, design and study of the feasibility of a randomized controlled study. BMC Geriatr 11:32, 2011.
40. Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA, :Protein supplementation before and after resistance training in older men. Eur J Appl Physiol 97:548–556, 2006.
41. Cao JJ, Johnson LK, Hunt JR, :A diet high in meat protein and potential renal acid load increases fractional calcium absorption and urinary calcium excretion without affecting markers of bone resorption or formation in postmenopausal women. J Nutr 141:391–397, 2011.
42. Cao JJ, Pasiakos SM, Margolis LM, Sauter ER, Whigham LD, McClung JP, Young AJ, Combs GFJ, :Calcium homeostasis and bone metabolic responses to high-protein diets during energy deficit in healthy young adults:a randomized controlled trial. Am J Clin Nutr 99:400–407, 2014.
43. Carlsson P, Tidermark J, Ponzer S, Soderqvist A, Cederholm T, :Food habits and appetite of elderly women at the time of a femoral neck fracture and after nutritional and anabolic support. J Hum Nutr Diet 18:117–120, 2005.
44. Ceglia L, Harris SS, Abrams SA, Rasmussen HM, Dallal GE, Dawson-Hughes B, :Potassium bicarbonate attenuates the urinary nitrogen excretion that accompanies an increase in dietary protein and may promote calcium absorption. J Clin Endocrinol Metab 94:645–653, 2009.
45. Chevalley T, Hoffmeyer P, Bonjour J-P, Rizzoli R, :Early serum IGF-I response to oral protein supplements in elderly women with a recent hip fracture. Clin Nutr 29:78–83, 2010.
46. Chu JY, Margen S, Calloway DH, Costa FM, :Integumentary loss of calcium. Am J Clin Nutr 32:1699–1702, 1979.
47. Cornish SM, Candow DG, Jantz NT, Chilibeck PD, Little JP, Forbes S, Abeysekara S, Zello GA, :Conjugated linoleic acid combined with creatine monohydrate and whey protein supplementation during strength training. Int J Sport Nutr Exerc Metab 19:79–96, 2009.
48. Dargent-Molina P, Sabia S, Touvier M, Kesse E, Breart G, Clavel-Chapelon F, Boutron-Ruault M-C, :Proteins, dietary acid load, and calcium and risk of postmenopausal fractures in the E3N French women prospective study. J Bone Miner Res 23:1915–1922, 2008.
49. 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.
50. Dawson-Hughes B, Harris SS, Rasmussen H, Song L, Dallal GE, :Effect of dietary protein supplements on calcium excretion in healthy older men and women. J Clin Endocrinol Metab 89:1169–1173, 2004.
51. de Azevedo MNL, Nunes JV, Pasqualette HA, Tuma M, de FF, Nunes LCF, :Bone mineral density at 45 years of age, before menopause. J Natl Med Assoc 101:788–792, 2009.
52. 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.
53. Devine A, Dick IM, Islam AFM, Dhaliwal SS, Prince RL, :Protein consumption is an important predictor of lower limb bone mass in elderly women. Am J Clin Nutr 81:1423–1428, 2005.
54. Duff WRD, Chilibeck PD, Rooke JJ, Kaviani M, Krentz JR, Haines DM, :The effect of bovine colostrum supplementation in older adults during resistance training. Int J Sport Nutr Exerc Metab 24:276–285, 2014.
55. Espaulella J, Guyer H, Diaz-Escriu F, Mellado-Navas JA, Castells M, Pladevall M, :Nutritional supplementation of elderly hip fracture patients. A randomized, double-blind, placebo-controlled trial. Age Ageing 29:425–431, 2000.
56. Feskanich D, Willett WC, Stampfer MJ, Colditz GA, :Protein consumption and bone fractures in women. Am J Epidemiol 143:472–479, 1996.
57. Geinoz G, Rapin CH, Rizzoli R, Kraemer R, Buchs B, Slosman D, Michel JP, Bonjour JP, :Relationship between bone mineral density and dietary intakes in the elderly. Osteoporos Int 3:242–248, 1993.
58. Gregg EW, Kriska AM, Salamone LM, Wolf RL, Roberts MM, Ferrell RE, Anderson SJ, Kuller LH, Cauley JA, :Correlates of quantitative ultrasound in the Women's Healthy Lifestyle Project. Osteoporos Int 10:416–424, 1999.
59. 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.
60. Harrington M, Bennett T, Jakobsen J, Ovesen L, Brot C, Flynn A, Cashman KD, :Effect of a high-protein, high-salt diet on calcium and bone metabolism in postmenopausal women stratified by hormone replacement therapy use. Eur J Clin Nutr 58:1436–1439, 2004.
61. Harrington M, Bennett T, Jakobsen J, Ovesen L, Brot C, Flynn A, Cashman KD, :The effect of a high-protein, high-sodium diet on calcium and bone metabolism in postmenopausal women and its interaction with vitamin D receptor genotype. Br J Nutr 91:41–51, 2004.
62. Heaney RP, :Dietary protein and phosphorus do not affect calcium absorption. Am J Clin Nutr 72:758–761, 2000.
63. Hegsted M, Linkswiler HM, :Long-term effects of level of protein intake on calcium metabolism in young adult women. J Nutr 111:244–251, 1981.
64. Ho SC, Chan SG, Yip YB, Chan CSY, Woo JLF, Sham A, :Change in bone mineral density and its determinants in pre- and perimenopausal Chinese women:the Hong Kong Perimenopausal Women Osteoporosis Study. Osteoporos Int 19:1785–1796, 2008.
65. Holm L, Olesen JL, Matsumoto K, Doi T, Mizuno M, Alsted TJ, Mackey AL, Schwarz P, Kjaer M, :Protein-containing nutrient supplementation following strength training enhances the effect on muscle mass, strength, and bone formation in postmenopausal women. J Appl Physiol 105:274–281, 2008.
66. Hu T, Rianon NJ, Nettleton JA, Hyder JA, He J, Steffen LM, Jacobs DRJ, Criqui MH, Bazzano LA, :Protein intake and lumbar bone density:the Multi-Ethnic Study of Atherosclerosis (MESA). Br J Nutr 112:1384–1392, 2014.
67. Hunt 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. Am J Clin Nutr 62:621–632, 1995.
68. Hunt JR, Johnson LK, Fariba Roughead ZK, :Dietary protein and calcium interact to influence calcium retention:a controlled feeding study. Am J Clin Nutr 89:1357–1365, 2009.
69. Ince BA, Anderson EJ, Neer RM, :Lowering dietary protein to U.S. recommended dietary allowance levels reduces urinary calcium excretion and bone resorption in young women. J Clin Endocrinol Metab 89:3801–3807, 2004.
70. Jajoo R, Song L, Rasmussen H, Harris SS, Dawson-Hughes B, :Dietary acid–base balance, bone resorption, and calcium excretion. J Am Coll Nutr 25:224–230, 2006.
71. Jenkins DJA, Kendall CWC, Vidgen E, Augustin LSA, Parker T, Faulkner D, Vieth R, Vandenbroucke AC, Josse RG, :Effect of high vegetable protein diets on urinary calcium loss in middle-aged men and women. Eur J Clin Nutr 57:376–382, 2003.
72. Johnson NE, Alcantara EN, Linkswiler H, :Effect of level of protein intake on urinary and fecal calcium and calcium retention of young adult males. J Nutr 100:1425–1430, 1970.
73. Kerstetter JE, Mitnick ME, Gundberg CM, Caseria DM, Ellison AF, Carpenter TO, Insogna KL, :Changes in bone turnover in young women consuming different levels of dietary protein. J Clin Endocrinol Metab 84:1052–1055, 1999.
74. Kerstetter JE, O'Brien KO, Insogna KL, :Dietary protein affects intestinal calcium absorption. Am J Clin Nutr 68:859–865, 1998.
75. Kerstetter JE, Svastisalee CM, Caseria DM, Mitnick ME, Insogna KL, :A threshold for low-protein-diet-induced elevations in parathyroid hormone. Am J Clin Nutr 72:168–173, 2000.
76. Kerstetter JE, Bihuniak JD, Brindisi J, Sullivan RR, Mangano KM, Larocque S, Kotler BM, Simpson CA, Cusano AM, Gaffney-Stomberg E, et al.:The Effect of a whey protein supplement on bone mass in older caucasian adults. J Clin Endocrinol Metab 100:2214–2222, 2015.
77. Kerstetter JE, O'Brien KO, Caseria DM, Wall DE, Insogna KL, :The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab 90:26–31, 2005.
78. Kerstetter JE, O'Brien KO, Insogna KL, :Dietary protein, calcium metabolism, and skeletal homeostasis revisited. Am J Clin Nutr 78:584S–592S, 2003.
79. Kerstetter JE, Wall DE, O'Brien KO, Caseria DM, Insogna KL, :Meat and soy protein affect calcium homeostasis in healthy women. J Nutr 136:1890–1895, 2006.
80. Key TJ, Appleby PN, Spencer EA, Roddam AW, Neale RE, Allen NE, :Calcium, diet and fracture risk:a prospective study of 1898 incident fractures among 34,696 British women and men. Public Heal Nutr 10:1314–1320, 2007.
81. Khalil DA, Lucas EA, Juma S, Smith BJ, Payton ME, Arjmandi BH, :Soy protein supplementation increases serum insulin-like growth factor-I in young and old men but does not affect markers of bone metabolism. J Nutr 132:2605–2608, 2002.
82. Kitano T, Esashi T, Azami S, :Effect of protein intake on mineral (calcium, magnesium, and phosphorus) balance in Japanese males. J Nutr Sci Vitaminol 34:387–398, 1988.
83. Langsetmo L, Barr SI, Berger C, Kreiger N, Rahme E, Adachi JD, Papaioannou A, Kaiser SM, Prior JC, Hanley DA, et al.:Associations of protein intake and protein source with bone mineral density and fracture risk:a population-based cohort study. J Nutr Health Aging 19:861–868, 2015.
84. Larocque SC, Kerstetter JE, Cauley JA, Insogna KL, Ensrud K, Lui L-Y, Allore HG, :Dietary protein and vitamin D intake and risk of falls:a secondary analysis of postmenopausal women from the study of osteoporotic fractures. J Nutr Gerontol Geriatr 34:305–318, 2015.
85. Lavine JB, :Protein intake and the risk of hip fracture in postmenopausal women. Am J Clin Nutr 70:303, 1999.
86. Lousuebsakul-Matthews V, Thorpe DL, Knutsen R, Beeson WL, Fraser GE, Knutsen SF, :Legumes and meat analogues consumption are associated with hip fracture risk independently of meat intake among Caucasian men and women:the Adventist Health Study–2. Public Health Nutr 17:2333–2343, 2014.
87. Lutz J, :Calcium balance and acid–base status of women as affected by increased protein intake and by sodium bicarbonate ingestion. Am J Clin Nutr 39:281–288, 1984.
88. Mahalko JR, Sandstead HH, Johnson LK, Milne DB, :Effect of a moderate increase in dietary protein on the retention and excretion of Ca, Cu, Fe, Mg, P, and Zn by adult males. Am J Clin Nutr. 37:8–14, 1983.
89. Malafarina V, Uriz-Otano F, Gil-Guerrero L, Iniesta R, Zulet MA, Martinez JA, :Study protocol:high-protein nutritional intervention based on beta-hydroxy-beta-methylbutirate, vitamin D3 and calcium on obese and lean aged patients with hip fractures and sarcopenia. The HIPERPROT-GER Study. Maturitas. 76:123–128, 2013.
90. McCance RA, Widdowson EM, Lehmann H, :The effect of protein intake on the absorption of calcium and magnesium. Biochem J 36:686–691, 1942.
91. Meng X, Zhu K, Devine A, Kerr DA, Binns CW, Prince RL, :A 5-year cohort study of the effects of high protein intake on lean mass and BMC in elderly postmenopausal women. J Bone Miner Res 24:1827–1834, 2009.
92. Merrill RM, Aldana SG, :Consequences of a plant-based diet with low dairy consumption on intake of bone-relevant nutrients. J Womens Health 18:691–698, 2009.
93. 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.
94. Misra D, Berry SD, Broe KE, McLean RR, Cupples LA, Tucker KL, Kiel DP, Hannan MT, :Does dietary protein reduce hip fracture risk in elders? The Framingham Osteoporosis Study. Osteoporos Int 22:345–349, 2011.
95. Moriguti JC, Ferriolli E, Marchini JS, :Urinary calcium loss in elderly men on a vegetable:animal (1:1) high-protein diet. Gerontology 45:274–278, 1999.
96. Mullins NM, Sinning WE, :Effects of resistance training and protein supplementation on bone turnover in young adult women. Nutr Metab 2:19, 2005.
97. 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.
98. Mussolino ME, Looker AC, Madans JH, Langlois JA, Orwoll ES, :Risk factors for hip fracture in white men:the NHANES I Epidemiologic Follow-Up Study. J Bone Miner Res 13:918–924, 1998.
99. Neumann M, Friedmann J, Roy M-A, Jensen GL, :Provision of high-protein supplement for patients recovering from hip fracture. Nutrition 20:415–419, 2004.
100. Orwoll ES, Weigel RM, Oviatt SK, Meier DE, McClung MR, :Serum protein concentrations and bone mineral content in aging normal men. Am J Clin Nutr 46:614–621, 1987.
101. Page ME, Ringsdorf Jr WM, Cheraskin E, Hollis CF, :The effect of a low-refined-carbohydrate high-protein diet upon nonfasting blood calcium. Ann Biochem Exp Med 21:327–332, 1961.
102. Pannemans DL, Schaafsma G, Westerterp KR, :Calcium excretion, apparent calcium absorption and calcium balance in young and elderly subjects:influence of protein intake. Br J Nutr 77:721–729, 1997.
103. Poortmans JR, Dellalieux O, :Do regular high protein diets have potential health risks on kidney function in athletes? Int J Sport Nutr Exerc Metab 10:28–38, 2000.
104. Porter KH, Johnson MA, :Dietary protein supplementation and recovery from femoral fracture. Nutr Rev 56:337–340, 1998.
105. Promislow JHE, Goodman-Gruen D, Slymen DJ, Barrett-Connor E, :Protein consumption and bone mineral density in the elderly:the Rancho Bernardo Study. Am J Epidemiol 155:636–644, 2002.
106. Rapuri PB, Gallagher JC, Haynatzka V, :Protein intake:effects on bone mineral density and the rate of bone loss in elderly women. Am J Clin Nutr 77:1517–1525, 2003.
107. Roughead ZK, Johnson LK, Lykken GI, Hunt JR, :Controlled high meat diets do not affect calcium retention or indices of bone status in healthy postmenopausal women. J Nutr 133:1020–1026, 2003.
108. Sahni S, Broe KE, Tucker KL, McLean RR, Kiel DP, Cupples LA, Hannan MT, :Association of total protein intake with bone mineral density and bone loss in men and women from the Framingham Offspring Study. Public Health Nutr 17:2570–2576, 2014.
109. Sahni S, Cupples LA, McLean RR, Tucker KL, Broe KE, Kiel DP, Hannan MT, :Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham Offspring cohort. J Bone Miner Res 25:2770–2776, 2010.
110. Schuette SA, Zemel MB, Linkswiler HM, :Studies on the mechanism of protein-induced hypercalciuria in older men and women. J Nutr 110:305–315, 1980.
111. Schurch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P, Bonjour JP, :Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 128:801–809, 1998.
112. Sellmeyer DE, Stone KL, Sebastian A, Cummings SR, :A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Study of Osteoporotic Fractures Research Group. Am J Clin Nutr 73:118–122, 2001.
113. Shenoy S, Bedi R, Sandhu JS, :Effect of soy isolate protein and resistance exercises on muscle performance and bone health of osteopenic/osteoporotic post-menopausal women. J Women Aging 25:183–198, 2013.
114. Spencer H, Kramer L, DeBartolo M, Norris C, Osis D, :Further studies of the effect of a high protein diet as meat on calcium metabolism. Am J Clin Nutr 37:924–929, 1983.
115. Spencer H, Kramer L, Osis D, Norris C, :Effect of a high protein (meat) intake on calcium metabolism in man. Am J Clin Nutr 31:2167–2180, 1978.
116. Swanenburg J, de Bruin ED, Stauffacher M, Mulder T, Uebelhart D, :Effects of exercise and nutrition on postural balance and risk of falling in elderly people with decreased bone mineral density:randomized controlled trial pilot study. Clin Rehabil 21:523–534, 2007.
117. Thorpe DL, Knutsen SF, Beeson WL, Rajaram S, Fraser GE, :Effects of meat consumption and vegetarian diet on risk of wrist fracture over 25 years in a cohort of peri- and postmenopausal women. Public Health Nutr 11:564–572, 2008.
118. Tkatch L, Rapin CH, Rizzoli R, Slosman D, Nydegger V, Vasey H, Bonjour JP, :Benefits of oral protein supplementation in elderly patients with fracture of the proximal femur. J Am Coll Nutr 11:519–525, 1992.
119. Toba Y, Takada Y, Matsuoka Y, Morita Y, Motouri M, Hirai T, Suguri T, Aoe S, Kawakami H, Kumegawa M, et al.:Milk basic protein promotes bone formation and suppresses bone resorption in healthy adult men. Biosci Biotechnol Biochem 65:1353–1357, 2001.
120. Tucker KL, Hannan MT, Kiel DP, :The acid–base hypothesis:diet and bone in the Framingham Osteoporosis Study. Eur J Nutr 40:231–237, 2001.
121. Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PWF, Felson D, Kiel DP, :Bone mineral density and dietary patterns in older adults:the Framingham Osteoporosis Study. Am J Clin Nutr 76:245–252, 2002.
122. Uenishi K, Ishida H, Toba Y, Aoe S, Itabashi A, Takada Y, :Milk basic protein increases bone mineral density and improves bone metabolism in healthy young women. Osteoporos Int 18:385–390, 2007.
123. van Beresteijn EC, Brussaard JH, van Schaik M, :Relationship between the calcium-to-protein ratio in milk and the urinary calcium excretion in healthy adults—a controlled crossover study. Am J Clin Nutr 52:142–146, 1990.
124. Vupadhyayula PM, Gallagher JC, Templin T, Logsdon SM, Smith LM, :Effects of soy protein isolate on bone mineral density and physical performance indices in postmenopausal women—a 2-year randomized, double-blind, placebo-controlled trial. Menopause 16:320–328, 2009.
125. Weikert C, Walter D, Hoffmann K, Kroke A, Bergmann MM, Boeing H, :The relation between dietary protein, calcium and bone health in women:results from the EPIC–Potsdam cohort. Ann Nutr Metab 49:312–318, 2005.
126. Yamamura J-I, Aoe S, Toba Y, Motouri M, Kawakami H, Kumegawa M, Itabashi A, Takada Y, :Milk basic protein (MBP) increases radial bone mineral density in healthy adult women. Biosci Biotechnol Biochem 66:702–704, 2002.
127. Zemel MB, Schuette SA, Hegsted M, Linkswiler HM, :Role of the sulfur-containing amino acids in protein-induced hypercalciuria in men. J Nutr 111:545–552, 1981.
128. Zhang X, Shu X-O, Li H, Yang G, Li Q, Gao Y-T, Zheng W, :Prospective cohort study of soy food consumption and risk of bone fracture among postmenopausal women. Arch Intern Med 165:1890–1895, 2005.
129. Zhu K, Meng X, Kerr DA, Devine A, Solah V, Binns CW, Prince RL, :The effects of a two-year randomized, controlled trial of whey protein supplementation on bone structure, IGF-1, and urinary calcium excretion in older postmenopausal women. J Bone Miner Res 26:2298–2306, 2011.
130. Zou Z-Y, Lin X-M, Xu X-R, Xu R, Ma L, Li Y, Wang M-F, :Evaluation of milk basic protein supplementation on bone density and bone metabolism in Chinese young women. Eur J Nutr 48:301–306, 2009.
131. Ho-Pham LT, Vu BQ, Lai TQ, Nguyen ND, Nguyen TV, :Vegetarianism, bone loss, fracture and vitamin D:a longitudinal study in Asian vegans and non-vegans. Eur J Clin Nutr 66:75–82, 2012.
132. Pedone C, Napoli N, Pozzilli P, Lauretani F, Bandinelli S, Ferrucci L, Antonelli-Incalzi R, :Quality of diet and potential renal acid load as risk factors for reduced bone density in elderly women. Bone 46:1063–1067, 2010.
133. Kerstetter JE, Caseria DM, Mitnick ME, Ellison AF, Gay LF, Liskov TA, Carpenter TO, Insogna KL, :Increased circulating concentrations of parathyroid hormone in healthy, young women consuming a protein-restricted diet. Am J Clin Nutr 66:1188–1196, 1997.
134. Fung TT, Meyer HE, Willett WC, Feskanich D, :Protein intake and risk of hip fractures in postmenopausal women and men age 50 and older. Osteoporos Int 28:1401–1411, 2017.
135. Langsetmo L, Shikany JM, Cawthon PM, Cauley JA, Taylor BC, Vo TN, Bauer DC, Orwoll ES, Schousboe JT, Ensrud KE, :The association between protein intake by source and osteoporotic fractures in older men:a prospective cohort study. J Bone Min Res 32(3):592–600, 2017.
136. 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, 2004.
137. Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R, :Clinicians guide to prevention and treatment of osteoporosis. Osteoporos Int 25(10):2359–2381, 2014.
138. Bauer D, Krege J, Lane N, Leary E, Libanati C, Miller P, Myers G, Silverman S, Vesper HW, Lee D, Payette M, Randall S, :National Bone Health Alliance bone turnover marker standardization project:current practices and the need for U.S. harmonization, standardization, and common reference ranges. Osteoporos Int 23:2425–2433, 2012.
139. Qvist P, Christgau S, Pedersen BJ, Schlemmer A, Christiansen C, :Circadian variation in the serum concentraton of C-terminal telopeptide 1 collagen (serum s-CTX):effects of gender, age, menopausal status, posture, daylight, serum cortisol and fasting. Bone 31:57–61, 2002.