Osteoporosis International

, Volume 29, Issue 9, pp 1933–1948 | Cite as

Benefits and safety of dietary protein for bone health—an expert consensus paper endorsed by the European Society for Clinical and Economical Aspects of Osteopororosis, Osteoarthritis, and Musculoskeletal Diseases and by the International Osteoporosis Foundation

  • R. RizzoliEmail author
  • E. Biver
  • J.-P. Bonjour
  • V. Coxam
  • D. Goltzman
  • J. A. Kanis
  • J. Lappe
  • L. Rejnmark
  • S. Sahni
  • C. Weaver
  • H. Weiler
  • J.-Y. Reginster


A summary of systematic reviews and meta-analyses addressing the benefits and risks of dietary protein intakes for bone health in adults suggests that dietary protein levels even above the current RDA may be beneficial in reducing bone loss and hip fracture risk, provided calcium intakes are adequate. Several systematic reviews and meta-analyses have addressed the benefits and risks of dietary protein intakes for bone health in adults. This narrative review of the literature summarizes and synthesizes recent systematic reviews and meta-analyses and highlights key messages. Adequate supplies of dietary protein are required for optimal bone growth and maintenance of healthy bone. Variation in protein intakes within the “normal” range accounts for 2–4% of BMD variance in adults. In older people with osteoporosis, higher protein intake (≥ 0.8-g/kg body weight/day, i.e., above the current RDA) is associated with higher BMD, a slower rate of bone loss, and reduced risk of hip fracture, provided that dietary calcium intakes are adequate. Intervention with dietary protein supplements attenuate age-related BMD decrease and reduce bone turnover marker levels, together with an increase in IGF-I and a decrease in PTH. There is no evidence that diet-derived acid load is deleterious for bone health. Thus, insufficient dietary protein intakes may be a more severe problem than protein excess in the elderly. Long-term, well-controlled randomized trials are required to further assess the influence of dietary protein intakes on fracture risk.


Acid-base homeostasis Bone mineral density Bone turnover Dairy products Fracture Osteoporosis 


Funding information

The writing of this paper was supported by a grant from the Dairy Research Consortium (Dairy Farmers of Canada, Centre national interprofessionnel de l’économie laitière (CNIEL), National Dairy Council, Dairy Australia Ltd., Dutch Dairy Association, Danish Dairy Research Foundation), who did not intervene in data analysis, interpretation or conclusions.

Compliance with ethical standards

Conflicts of interest

RR received fees for lectures or advisory boards from Radius Health, Danone, Nestlé and Effrx/Labatec. EB received a research grant from Danone. JPB has nothing to disclose. VC received a grant from Rousselot and belongs to the advisory board of Triballat Institute. DG has nothing to disclose. JAK reports grants from Amgen, Eli Lilly, and Radius Health; non-financial support from Medimaps and Asahi; and other support from AgNovos. JL has nothing to disclose. LR has received institutional research grants from the Danish Dairy Research Foundation. SS has received institutional grants from Dairy Management, Inc. and is a member of the Nutrition Research Scientific Advisory Committee, National Dairy Council. CW received fees for lectures, advising, or grants from Pharmavite, Pfizer, ILSI, Alliance for Potato Research and Education, Tate & Lyle, Danone, and General Mills. HW received research grants from Dairy Farmers of Canada and the Dairy Research Cluster Initiative (Dairy Farmers of Canada, Agriculture and Agri-Food Canada, the Canadian Dairy Network and the Canadian Dairy Commission). JYR received fees for consulting from IBSA-Genevrier, Mylan, Radius Health, Pierre-Fabre and for lectures from IBSA-Genevrier, Mylan, CNIEL, Dairy Research Council.


  1. 1.
    Rizzoli R, Stevenson JC, Bauer JM, van Loon LJ, Walrand S, Kanis JA, Cooper C, Brandi ML, Diez-Perez A, Reginster JY (2014) The role of dietary protein and vitamin D in maintaining musculoskeletal health in postmenopausal women: a consensus statement from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Maturitas 79:122–132PubMedCrossRefGoogle Scholar
  2. 2.
    Institute of medicine (2002/2005) Dietary reference intakes for energy, carbohydrates, fiber, fat, protein and amino acids (macronutrients). The National Academies Press, Washington (DC)Google Scholar
  3. 3.
    Deutz NE, Bauer JM, Barazzoni R et al (2014) Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group. Clinical Nutrition (Edinburgh, Scotland) 33:929–936CrossRefGoogle Scholar
  4. 4.
    Darling AL, Millward DJ, Torgerson DJ, Hewitt CE, Lanham-New SA (2009) Dietary protein and bone health: a systematic review and meta-analysis. Am J Clin Nutr 90:1674–1692PubMedCrossRefGoogle Scholar
  5. 5.
    Wu AM, Sun XL, Lv QB, Zhou Y, Xia DD, Xu HZ, Huang QS, Chi YL (2015) The relationship between dietary protein consumption and risk of fracture: a subgroup and dose-response meta-analysis of prospective cohort studies. Sci Rep 5:9151PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Shams-White MM, Chung M, Du M et al (2017) Dietary protein and bone health: a systematic review and meta-analysis from the National Osteoporosis Foundation. Am J Clin Nutr 105:1528–1543PubMedGoogle Scholar
  7. 7.
    Wallace TC, Frankenfeld CL (2017) Dietary protein intake above the current RDA and bone health: a systematic review and meta-analysis. J Am Coll Nutr 36:481–496PubMedCrossRefGoogle Scholar
  8. 8.
    Bonjour JP (2013) Nutritional disturbance in acid-base balance and osteoporosis: a hypothesis that disregards the essential homeostatic role of the kidney. Br J Nutr 110:1168–1177PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Heaney RP (2001) Protein intake and bone health: the influence of belief systems on the conduct of nutritional science. Am J Clin Nutr 73:5–6PubMedCrossRefGoogle Scholar
  10. 10.
    Fenton TR, Eliasziw M, Lyon AW, Tough SC, Hanley DA (2008) Meta-analysis of the quantity of calcium excretion associated with the net acid excretion of the modern diet under the acid-ash diet hypothesis. Am J Clin Nutr 88:1159–1166PubMedCrossRefGoogle Scholar
  11. 11.
    Fenton TR, Lyon AW, Eliasziw M, Tough SC, Hanley DA (2009) Phosphate decreases urine calcium and increases calcium balance: a meta-analysis of the osteoporosis acid-ash diet hypothesis. Nutr J 8:41PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Fenton TR, Lyon AW, Eliasziw M, Tough SC, Hanley DA (2009) Meta-analysis of the effect of the acid-ash hypothesis of osteoporosis on calcium balance. J Bone Mineral Res: Official J Am Soc Bone Mineral Res 24:1835–1840CrossRefGoogle Scholar
  13. 13.
    Fenton TR, Tough SC, Lyon AW, Eliasziw M, Hanley DA (2011) Causal assessment of dietary acid load and bone disease: a systematic review & meta-analysis applying Hill’s epidemiologic criteria for causality. Nutr J 10:41PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Zhang X, Shu XO, Li H, Yang G, Li Q, Gao YT, Zheng W (2005) Prospective cohort study of soy food consumption and risk of bone fracture among postmenopausal women. Arch Intern Med 165:1890–1895PubMedCrossRefGoogle Scholar
  15. 15.
    Misra D, Berry SD, Broe KE, McLean RR, Cupples LA, Tucker KL, Kiel DP, Hannan MT (2011) Does dietary protein reduce hip fracture risk in elders? The Framingham Osteoporosis Study. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 22:345–349CrossRefGoogle Scholar
  16. 16.
    Feskanich D, Willett WC, Stampfer MJ, Colditz GA (1996) Protein consumption and bone fractures in women. Am J Epidemiol 143:472–479PubMedCrossRefGoogle Scholar
  17. 17.
    Sahni S, Cupples LA, McLean RR, Tucker KL, Broe KE, Kiel DP, Hannan MT (2010) Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham Offspring Cohort. J Bone Mineral Res: Official J Am Soc Bone Mineral Res 25:2770–2776CrossRefGoogle Scholar
  18. 18.
    Sellmeyer DE, Stone KL, Sebastian A, Cummings SR (2001) 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 73:118–122PubMedCrossRefGoogle Scholar
  19. 19.
    Beasley JM, LaCroix AZ, Larson JC et al (2014) Biomarker-calibrated protein intake and bone health in the Women’s Health Initiative Clinical Trials and Observational Study. Am J Clin Nutr 99:934–940PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Cauley JA, Cawthon PM, Peters KE, Cummings SR, Ensrud KE, Bauer DC, Taylor BC, Shikany JM, Hoffman AR, Lane NE, Kado DM, Stefanick ML, Orwoll ES, for the Osteoporotic Fractures in Men (MrOS) Study Research Group (2016) Risk factors for hip fracture in older men: the Osteoporotic Fractures in Men Study (MrOS). J Bone Miner Res Off J Am Soc Bone Miner Res 31:1810–1819CrossRefGoogle Scholar
  21. 21.
    Fung TT, Meyer HE, Willett WC, Feskanich D (2017) Protein intake and risk of hip fractures in postmenopausal women and men age 50 and older. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 28:1401–1411CrossRefGoogle Scholar
  22. 22.
    Huang Z, Himes JH, McGovern PG (1996) Nutrition and subsequent hip fracture risk among a national cohort of white women. Am J Epidemiol 144:124–134PubMedCrossRefGoogle Scholar
  23. 23.
    Koh WP, Wu AH, Wang R, Ang LW, Heng D, Yuan JM, Yu MC (2009) Gender-specific associations between soy and risk of hip fracture in the Singapore Chinese Health Study. Am J Epidemiol 170:901–909PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Langsetmo L, Barr SI, Berger C et al (2015) Associations of protein intake and protein source with bone mineral density and fracture risk: a population-based cohort study. J Nutr Health Aging 19:861–868PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Langsetmo L, Shikany JM, Cawthon PM, Cauley JA, Taylor BC, Vo TN, Bauer DC, Orwoll ES, Schousboe JT, Ensrud KE (2017) The association between protein intake by source and osteoporotic fracture in older men: a prospective cohort study. J Bone Miner Res Off J Am Soc Bone Miner Res 32:592–600CrossRefGoogle Scholar
  26. 26.
    Munger RG, Cerhan JR, Chiu BC (1999) Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am J Clin Nutr 69:147–152PubMedCrossRefGoogle Scholar
  27. 27.
    Mussolino ME, Looker AC, Madans JH, Langlois JA, Orwoll ES (1998) Risk factors for hip fracture in white men: the NHANES I Epidemiologic Follow-up Study. J Bone Miner Res Off J Am Soc Bone Miner Res 13:918–924CrossRefGoogle Scholar
  28. 28.
    Thorpe DL, Knutsen SF, Beeson WL, Rajaram S, Fraser GE (2008) 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 11:564–572PubMedCrossRefGoogle Scholar
  29. 29.
    Wengreen HJ, Munger RG, West NA, Cutler DR, Corcoran CD, Zhang J, Sassano NE (2004) Dietary protein intake and risk of osteoporotic hip fracture in elderly residents of Utah. J Bone Miner Res Off J Am Soc Bone Miner Res 19:537–545CrossRefGoogle Scholar
  30. 30.
    Dargent-Molina P, Sabia S, Touvier M, Kesse E, Breart G, Clavel-Chapelon F, Boutron-Ruault MC (2008) Proteins, dietary acid load, and calcium and risk of postmenopausal fractures in the E3N French women prospective study. J Bone Miner Res Off J Am Soc Bone Miner Res 23:1915–1922CrossRefGoogle Scholar
  31. 31.
    Key TJ, Appleby PN, Spencer EA, Roddam AW, Neale RE, Allen NE (2007) Calcium, diet and fracture risk: a prospective study of 1898 incident fractures among 34 696 British women and men. Public Health Nutr 10:1314–1320PubMedCrossRefGoogle Scholar
  32. 32.
    Meyer HE, Pedersen JI, Løken EB, Tverdal A (1997) Dietary factors and the incidence of hip fracture in middle-aged Norwegians. A prospective study. Am J Epidemiol 145:117–123PubMedCrossRefGoogle Scholar
  33. 33.
    Kanis JA, EV MC, Johansson H, Cooper C, Rizzoli R, Reginster JY, Scientific Advisory Board of the European Society for C, Economic Aspects of O, Osteoarthritis, the Committee of Scientific Advisors of the International Osteoporosis F (2013) European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 24:23–57CrossRefGoogle Scholar
  34. 34.
    Schurch MA, Rizzoli R, Slosman D, Vadas L, Vergnaud P, Bonjour JP (1998) 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 128:801–809PubMedCrossRefGoogle Scholar
  35. 35.
    Durosier-Izart C, Biver E, Merminod F, van Rietbergen B, Chevalley T, Herrmann FR, Ferrari SL, Rizzoli R (2017) Peripheral skeleton bone strength is positively correlated with total and dairy protein intakes in healthy postmenopausal women. Am J Clin Nutr 105:513–525PubMedCrossRefGoogle Scholar
  36. 36.
    Dawson-Hughes B, Harris SS (2002) Calcium intake influences the association of protein intake with rates of bone loss in elderly men and women. Am J Clin Nutr 75:773–779PubMedCrossRefGoogle Scholar
  37. 37.
    Rizzoli R (2014) Dairy products, yogurts, and bone health. Am J Clin Nutr 99:1256S–1262SPubMedCrossRefGoogle Scholar
  38. 38.
    Aoe S, Koyama T, Toba Y, Itabashi A, Takada Y (2005) A controlled trial of the effect of milk basic protein (MBP) supplementation on bone metabolism in healthy menopausal women. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 16:2123–2128CrossRefGoogle Scholar
  39. 39.
    Aoe S, Toba Y, Yamamura J, Kawakami H, Yahiro M, Kumegawa M, Itabashi A, Takada Y (2001) Controlled trial of the effects of milk basic protein (MBP) supplementation on bone metabolism in healthy adult women. Biosci Biotechnol Biochem 65:913–918PubMedCrossRefGoogle Scholar
  40. 40.
    Bonjour JP, Brandolini-Bunlon M, Boirie Y, Morel-Laporte F, Braesco V, Bertiere MC, Souberbielle JC (2008) Inhibition of bone turnover by milk intake in postmenopausal women. Br J Nutr 100:866–874PubMedCrossRefGoogle Scholar
  41. 41.
    Bonjour JP, Benoit V, Pourchaire O, Ferry M, Rousseau B, Souberbielle JC (2009) Inhibition of markers of bone resorption by consumption of vitamin D and calcium-fortified soft plain cheese by institutionalised elderly women. Br J Nutr 102:962–966PubMedCrossRefGoogle Scholar
  42. 42.
    Bonjour JP, Benoit V, Rousseau B, Souberbielle JC (2012) Consumption of vitamin D-and calcium-fortified soft white cheese lowers the biochemical marker of bone resorption TRAP 5b in postmenopausal women at moderate risk of osteoporosis fracture. J Nutr 142:698–703PubMedCrossRefGoogle Scholar
  43. 43.
    Chee WS, Suriah AR, Chan SP, Zaitun Y, Chan YM (2003) The effect of milk supplementation on bone mineral density in postmenopausal Chinese women in Malaysia. Osteoporosis Int: a J Established Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 14:828–834CrossRefGoogle Scholar
  44. 44.
    Daly RM, Brown M, Bass S, Kukuljan S, Nowson C (2006) Calcium- and vitamin D3-fortified milk reduces bone loss at clinically relevant skeletal sites in older men: a 2-year randomized controlled trial. J Bone Miner Res Off J Am Soc Bone Miner Res 21:397–405CrossRefGoogle Scholar
  45. 45.
    Daly RM, Bass S, Nowson C (2006) Long-term effects of calcium-vitamin-D3-fortified milk on bone geometry and strength in older men. Bone 39:946–953PubMedCrossRefGoogle Scholar
  46. 46.
    Gui JC, Brasic JR, Liu XD, Gong GY, Zhang GM, Liu CJ, Gao GQ (2012) Bone mineral density in postmenopausal Chinese women treated with calcium fortification in soymilk and cow’s milk. Osteoporosis Int: a J Established Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 23:1563–1570CrossRefGoogle Scholar
  47. 47.
    Heaney RP, Rafferty K, Dowell MS (2002) Effect of yogurt on a urinary marker of bone resorption in postmenopausal women. J Am Diet Assoc 102:1672–1674PubMedCrossRefGoogle Scholar
  48. 48.
    Josse AR, Tang JE, Tarnopolsky MA, Phillips SM (2010) Body composition and strength changes in women with milk and resistance exercise. Med Sci Sports Exerc 42:1122–1130PubMedGoogle Scholar
  49. 49.
    Kristensen M, Jensen M, Kudsk J, Henriksen M, Molgaard C (2005) Short-term effects on bone turnover of replacing milk with cola beverages: a 10-day interventional study in young men. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 16:1803–1808CrossRefGoogle Scholar
  50. 50.
    Kruger MC, Booth CL, Coad J, Schollum LM, Kuhn-Sherlock B, Shearer MJ (2006) Effect of calcium fortified milk supplementation with or without vitamin K on biochemical markers of bone turnover in premenopausal women. Nutrition (Burbank, Los Angeles County, Calif) 22:1120–1128CrossRefGoogle Scholar
  51. 51.
    Kruger MC, Ha PC, Todd JM, Kuhn-Sherlock B, Schollum LM, Ma J, Qin G, Lau E (2012) High-calcium, vitamin D fortified milk is effective in improving bone turnover markers and vitamin D status in healthy postmenopausal Chinese women. Eur J Clin Nutr 66:856–861PubMedCrossRefGoogle Scholar
  52. 52.
    Kruger MC, Schollum LM, Kuhn-Sherlock B, Hestiantoro A, Wijanto P, Li-Yu J, Agdeppa I, Todd JM, Eastell R (2010) The effect of a fortified milk drink on vitamin D status and bone turnover in post-menopausal women from South East Asia. Bone 46:759–767PubMedCrossRefGoogle Scholar
  53. 53.
    Kukuljan S, Nowson CA, Bass SL, Sanders K, Nicholson GC, Seibel MJ, Salmon J, Daly RM (2009) Effects of a multi-component exercise program and calcium-vitamin-D3-fortified milk on bone mineral density in older men: a randomised controlled trial. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 20:1241–1251CrossRefGoogle Scholar
  54. 54.
    Lau EM, Lynn H, Chan YH, Woo J (2002) Milk supplementation prevents bone loss in postmenopausal Chinese women over 3 years. Bone 31:536–540PubMedCrossRefGoogle Scholar
  55. 55.
    Lau EM, Woo J, Lam V, Hong A (2001) Milk supplementation of the diet of postmenopausal Chinese women on a low calcium intake retards bone loss. J Bone Miner Res Off J Am Soc Bone Miner Res 16:1704–1709CrossRefGoogle Scholar
  56. 56.
    Liu Z, Qiu L, Chen YM, Su YX (2011) Effect of milk and calcium supplementation on bone density and bone turnover in pregnant Chinese women: a randomized controlled trail. Arch Gynecol Obstet 283:205–211PubMedCrossRefGoogle Scholar
  57. 57.
    Manios Y, Moschonis G, Trovas G, Lyritis GP (2007) 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 86:781–789PubMedCrossRefGoogle Scholar
  58. 58.
    Moschonis G, Kanellakis S, Papaioannou N, Schaafsma A, Manios Y (2011) Possible site-specific effect of an intervention combining nutrition and lifestyle counselling with consumption of fortified dairy products on bone mass: the Postmenopausal Health Study II. J Bone Miner Metab 29:501–506PubMedCrossRefGoogle Scholar
  59. 59.
    Moschonis G, Katsaroli I, Lyritis GP, Manios Y (2010) The effects of a 30-month dietary intervention on bone mineral density: the Postmenopausal Health Study. Br J Nutr 104:100–107PubMedCrossRefGoogle Scholar
  60. 60.
    Tenta R, Moschonis G, Koutsilieris M, Manios Y (2011) Calcium and vitamin D supplementation through fortified dairy products counterbalances seasonal variations of bone metabolism indices: the Postmenopausal Health Study. Eur J Nutr 50:341–349PubMedCrossRefGoogle Scholar
  61. 61.
    Thorpe MP, Jacobson EH, Layman DK, He X, Kris-Etherton PM, Evans EM (2008) A diet high in protein, dairy, and calcium attenuates bone loss over twelve months of weight loss and maintenance relative to a conventional high-carbohydrate diet in adults. J Nutr 138:1096–1100PubMedCrossRefGoogle Scholar
  62. 62.
    Ting GP, Tan SY, Chan SP, Karuthan C, Zaitun Y, Suriah AR, Chee WS (2007) A follow-up study on the effects of a milk supplement on bone mineral density of postmenopausal Chinese women in Malaysia. J Nutrition, Health & Aging 11:69–73Google Scholar
  63. 63.
    Toxqui L, Perez-Granados AM, Blanco-Rojo R, Wright I, de la Piedra C, Vaquero MP (2014) Low iron status as a factor of increased bone resorption and effects of an iron and vitamin D-fortified skimmed milk on bone remodelling in young Spanish women. Eur J Nutr 53:441–448PubMedCrossRefGoogle Scholar
  64. 64.
    Trombetti A, Carrier E, Perroud A, Lang F, Herrmann FR, Rizzoli R (2016) Influence of a fermented protein-fortified dairy product on serum insulin-like growth factor-I in women with anorexia nervosa: a randomized controlled trial. Clinical Nutrition (Edinburgh, Scotland) 35:1032–1038CrossRefGoogle Scholar
  65. 65.
    Uenishi K, Ishida H, Toba Y, Aoe S, Itabashi A, Takada Y (2007) Milk basic protein increases bone mineral density and improves bone metabolism in healthy young women. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 18:385–390CrossRefGoogle Scholar
  66. 66.
    Woo J, Lau W, Xu L, Lam CWK, Zhao X, Yu W, Xing X, Lau E, Kuhn-Sherlock B, Pocock N, Eastell R (2007) Milk supplementation and bone health in young adult chinese women. J Women’s Health (2002) 16:692–702CrossRefGoogle Scholar
  67. 67.
    Zhu K, Meng X, Kerr DA, Devine A, Solah V, Binns CW, Prince RL (2011) 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 Off J Am Soc Bone Miner Res 26:2298–2306CrossRefGoogle Scholar
  68. 68.
    Zou ZY, Lin XM, Xu XR, Xu R, Ma L, Li Y, Wang MF (2009) Evaluation of milk basic protein supplementation on bone density and bone metabolism in Chinese young women. Eur J Nutr 48:301–306PubMedCrossRefGoogle Scholar
  69. 69.
    Rizzoli R, Biver E (2017) Effects of fermented milk products on bone. Calcif Tissue IntGoogle Scholar
  70. 70.
    Lemann J Jr, Litzow JR, Lennon EJ (1966) The effects of chronic acid loads in normal man: further evidence for the participation of bone mineral in the defense against chronic metabolic acidosis. J Clin Invest 45:1608–1614PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Sebastian A, Harris ST, Ottaway JH, Todd KM, Morris RC Jr (1994) Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate. N Engl J Med 330:1776–1781PubMedCrossRefGoogle Scholar
  72. 72.
    Litzow JR, Lemann J Jr, Lennon EJ (1967) The effect of treatment of acidosis on calcium balance in patients with chronic azotemic renal disease. J Clin Invest 46:280–286PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Macdonald HM, Black AJ, Aucott L, Duthie G, Duthie S, Sandison R, Hardcastle AC, Lanham New SA, Fraser WD, Reid DM (2008) Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: a randomized controlled trial. Am J Clin Nutr 88:465–474PubMedCrossRefGoogle Scholar
  74. 74.
    Jehle S, Hulter HN, Krapf R (2013) Effect of potassium citrate on bone density, microarchitecture, and fracture risk in healthy older adults without osteoporosis: a randomized controlled trial. J Clin Endocrinol Metab 98:207–217PubMedCrossRefGoogle Scholar
  75. 75.
    Moseley KF, Weaver CM, Appel L, Sebastian A, Sellmeyer DE (2013) Potassium citrate supplementation results in sustained improvement in calcium balance in older men and women. J Bone Miner Res Off J Am Soc Bone Miner Res 28:497–504CrossRefGoogle Scholar
  76. 76.
    Dawson-Hughes B, Harris SS, Palermo NJ, Gilhooly CH, Shea MK, Fielding RA, Ceglia L (2015) Potassium bicarbonate supplementation lowers bone turnover and calcium excretion in older men and women: a randomized dose-finding trial. J Bone Miner Res Off J Am Soc Bone Miner Res 30:2103–2111CrossRefGoogle Scholar
  77. 77.
    Lambert H, Frassetto L, Moore JB, Torgerson D, Gannon R, Burckhardt P, Lanham-New S (2015) The effect of supplementation with alkaline potassium salts on bone metabolism: a meta-analysis. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 26:1311–1318CrossRefGoogle Scholar
  78. 78.
    Ceglia L, Harris SS, Abrams SA, Rasmussen HM, Dallal GE, Dawson-Hughes B (2009) Potassium bicarbonate attenuates the urinary nitrogen excretion that accompanies an increase in dietary protein and may promote calcium absorption. J Clin Endocrinol Metab 94:645–653PubMedCrossRefGoogle Scholar
  79. 79.
    Buclin T, Cosma M, Appenzeller M, Jacquet AF, Decosterd LA, Biollaz J, Burckhardt P (2001) Diet acids and alkalis influence calcium retention in bone. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 12:493–499CrossRefGoogle Scholar
  80. 80.
    Maurer M, Riesen W, Muser J, Hulter HN, Krapf R (2003) Neutralization of western diet inhibits bone resorption independently of K intake and reduces cortisol secretion in humans. Am J Physiology Renal Physiology 284:F32–F40CrossRefGoogle Scholar
  81. 81.
    Ball D, Maughan RJ (1997) Blood and urine acid-base status of premenopausal omnivorous and vegetarian women. Br J Nutr 78:683–693PubMedCrossRefGoogle Scholar
  82. 82.
    Remer T, Manz F (1995) Potential renal acid load of foods and its influence on urine pH. J Am Diet Assoc 95:791–797PubMedCrossRefGoogle Scholar
  83. 83.
    Blekkenhorst LC, Hodgson JM, Lewis JR, Devine A, Woodman R, Lim W, Wong G, Zhu K, Bondonno C, Ward N, Prince R (2017) Vegetable and fruit intake and fracture-related hospitalisations: a prospective study of older women. Nutrients 9Google Scholar
  84. 84.
    Byberg L, Bellavia A, Orsini N, Wolk A, Michaelsson K (2015) Fruit and vegetable intake and risk of hip fracture: a cohort study of Swedish men and women. J Bone Miner Res Off J Am Soc Bone Miner Res 30:976–984CrossRefGoogle Scholar
  85. 85.
    Benetou V, Orfanos P, Feskanich D, Michaëlsson K, Pettersson-Kymmer U, Eriksson S, Grodstein F, Wolk A, Bellavia A, Ahmed LA, Boffeta P, Trichopoulou A (2016) Fruit and vegetable intake and hip fracture incidence in older men and women: the CHANCES Project. J Bone Miner Res Off J Am Soc Bone Miner Res 31:1743–1752CrossRefGoogle Scholar
  86. 86.
    Dai Z, Butler LM, van Dam RM, Ang LW, Yuan JM, Koh WP (2014) Adherence to a vegetable-fruit-soy dietary pattern or the Alternative Healthy Eating Index is associated with lower hip fracture risk among Singapore Chinese. J Nutr 144:511–518PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Luo S, Li Y, Luo H, Yin X, Lin d R, Zhao K, Huang G, Song J (2016) Increased intake of vegetables, but not fruits, may be associated with reduced risk of hip fracture: a meta-analysis. Sci Rep 6:19783PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Muhlbauer RC, Lozano A, Reinli A (2002) Onion and a mixture of vegetables, salads, and herbs affect bone resorption in the rat by a mechanism independent of their base excess. J Bone Miner Res Off J Am Soc Bone Miner Res 17:1230–1236CrossRefGoogle Scholar
  89. 89.
    Appleby P, Roddam A, Allen N, Key T (2007) Comparative fracture risk in vegetarians and nonvegetarians in EPIC-Oxford. Eur J Clin Nutr 61:1400–1406PubMedCrossRefGoogle Scholar
  90. 90.
    Frassetto LA, Todd KM, Morris RC Jr, Sebastian A (1998) Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents. Am J Clin Nutr 68:576–583PubMedCrossRefGoogle Scholar
  91. 91.
    Rizzoli R, Bonjour JP. (2006) Physiology of calcium and phosphate homeostasis. Dynamics of bone and cartilage metabolism: principles and clinical applications MJ Seibel, SP Robins, JP Bilezikian, editors: 345–360Google Scholar
  92. 92.
    Dawson-Hughes B, Harris SS, Rasmussen HM, Dallal GE (2007) Comparative effects of oral aromatic and branched-chain amino acids on urine calcium excretion in humans. Osteoporosis Int: a J Established Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 18:955–961CrossRefGoogle Scholar
  93. 93.
    Kerstetter JE, O'Brien KO, Insogna KL (2003) Dietary protein, calcium metabolism, and skeletal homeostasis revisited. Am J Clin Nutr 78:584s–592sPubMedCrossRefGoogle Scholar
  94. 94.
    Kerstetter JE, O'Brien KO, Caseria DM, Wall DE, Insogna KL (2005) The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab 90:26–31PubMedCrossRefGoogle Scholar
  95. 95.
    Remer T, Manz F (1994) Estimation of the renal net acid excretion by adults consuming diets containing variable amounts of protein. Am J Clin Nutr 59:1356–1361PubMedCrossRefGoogle Scholar
  96. 96.
    Heaney RP, Recker RR, Watson P, Lappe JM (2010) Phosphate and carbonate salts of calcium support robust bone building in osteoporosis. Am J Clin Nutr 92:101–105PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Itkonen ST, Rita HJ, Saarnio EM, Kemi VE, Karp HJ, Kärkkäinen MUM, Pekkinen MH, Laitinen EK, Risteli J, Koivula MK, Sievänen H, Lamberg-Allardt CJE (2017) Dietary phosphorus intake is negatively associated with bone formation among women and positively associated with some bone traits among men—a cross-sectional study in middle-aged Caucasians. Nutr Res 37:58–66PubMedCrossRefGoogle Scholar
  98. 98.
    Jia T, Byberg L, Lindholm B, Larsson TE, Lind L, Michaelsson K, Carrero JJ (2015) Dietary acid load, kidney function, osteoporosis, and risk of fractures in elderly men and women. Osteoporosis Int: a J Established Res Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 26:563–570CrossRefGoogle Scholar
  99. 99.
    Nieves JW, Grisso JA, Kelsey JL (1992) A case-control study of hip fracture: evaluation of selected dietary variables and teenage physical activity. Osteoporosis Int: a J Established as Result Cooperation Between European Foundation Osteoporosis National Osteoporosis Foundation USA 2:122–127CrossRefGoogle Scholar
  100. 100.
    Hinton PS, Rector RS, Donnelly JE, Smith BK, Bailey B (2010) Total body bone mineral content and density during weight loss and maintenance on a low- or recommended-dairy weight-maintenance diet in obese men and women. Eur J Clin Nutr 64:392–399PubMedCrossRefGoogle Scholar
  101. 101.
    Sukumar D, Ambia-Sobhan H, Zurfluh R, Schlussel Y, Stahl TJ, Gordon CL, Shapses SA (2011) Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: a randomized, controlled trial. J Bone Miner Res Off J Am Soc Bone Miner Res 26:1339–1348CrossRefGoogle Scholar
  102. 102.
    Ballard TL, Specker BL, Binkley TL, Vukovich MD (2006) Effect of protein supplementation during a 6-month strength and conditioning program on areal and volumetric bone parameters. Bone 38:898–904PubMedCrossRefGoogle Scholar
  103. 103.
    Kerstetter JE, Bihuniak JD, Brindisi J, Sullivan RR, Mangano KM, Larocque S, Kotler BM, Simpson CA, Cusano AM, Gaffney-Stomberg E, Kleppinger A, Reynolds J, Dziura J, Kenny AM, Insogna KL (2015) The effect of a whey protein supplement on bone mass in older Caucasian adults. J Clin Endocrinol Metab 100:2214–2222PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Wright CS, McMorrow AM, Weinheimer-Haus EM, Campbell WW (2017) Whey protein supplementation and higher total protein intake do not influence bone quantity in overweight and obese adults following a 36-week exercise and diet intervention. J Nutr 147:179–186PubMedCrossRefGoogle Scholar
  105. 105.
    Yamamura J, Aoe S, Toba Y, Motouri M, Kawakami H, Kumegawa M, Itabashi A, Takada Y (2002) Milk basic protein (MBP) increases radial bone mineral density in healthy adult women. Biosci Biotechnol Biochem 66:702–704PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • R. Rizzoli
    • 1
    Email author
  • E. Biver
    • 1
  • J.-P. Bonjour
    • 1
  • V. Coxam
    • 2
  • D. Goltzman
    • 3
  • J. A. Kanis
    • 4
    • 5
  • J. Lappe
    • 6
  • L. Rejnmark
    • 7
  • S. Sahni
    • 8
  • C. Weaver
    • 9
  • H. Weiler
    • 10
  • J.-Y. Reginster
    • 11
  1. 1.Division of Bone DiseasesGeneva University Hospitals and Faculty of MedicineGeneva 14Switzerland
  2. 2.INRA, Unité de Nutrition Humaine, CRNH AuvergneUniversité Clermont AuvergneClermont-FerrandFrance
  3. 3.McGill University Health CenterMontrealCanada
  4. 4.University of SheffieldSheffieldUK
  5. 5.Institute for Health and AgeingCatholic University of AustraliaMelbourneAustralia
  6. 6.College of NursingCreighton UniversityCreightonUSA
  7. 7.Aarhus University HospitalAarhusDenmark
  8. 8.Hebrew SeniorLife and Harvard Medical SchoolInstitute for Aging ResearchBostonUSA
  9. 9.Women’s Global Health Institute, Department of Nutrition SciencePurdue UniversityWest LafayetteUSA
  10. 10.School of Human NutritionMcGill UniversityQCCanada
  11. 11.Department of Public Health, Epidemiology and Health EconomicsUniversity of LiègeLiègeBelgium

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