Skip to main content
Log in

Association between total and animal proteins with risk of fracture: A systematic review and dose–response meta-analysis of cohort studies

  • Review
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Previous cohort studies have indicated that consumption of total and animal proteins are related to fracture risk; however, results were inconclusive. This dose-dependent review sought to summarize the earlier evidence regarding the relation between total and animal proteins and fracture risk. We searched Scopus, PubMed, and Web of Science until July 2023 for original research articles examining the association of certain types of proteins and the incidence of all fractures in general adults. Summary relative risks (RRs) were calculated using random effects analysis to examine the relation between each certain amount (g/day) increment of total and animal protein and fracture risk. Twenty cohort studies with serious to moderate risk of bias involving 780,322 individuals were included. There was a non-statistically significant relation between intake of animal proteins and dairy products and all fracture risk. However, 43% and 5% decreased incidence of fracture was obtained with total protein (RR, 0.57; 95%CI, 0.36 to 0.93; per 100 g/day) and fish (RR, 0.95; 95%CI, 0.91 to 0.99; per 15 g/day) intake. Every 100 g/day total and animal protein consumption and every 15 g/day fish consumption were linked to 48%, 50%, and 5% lower hip fracture risk. Greater dietary animal protein intake might reduce risk of hip but not fracture at any site. We obtained a lower risk of any or hip fracture with greater total protein (per 100 g/day) and fish (per 15 g/day) intake. No evidence was obtained that higher intake of dairy could decrease risk of fracture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All data indicated and analyzed for this study are available by request to the corresponding author.

Abbreviations

BMI:

Body mass index

BMD:

Bone mineral density

CI:

Confidence intervals

HR:

Hazard ratio

GRADE:

Grading of Recommendations, Assessment, Development, and Evaluations

IGF-1:

Insulin-like growth factor-1

OR:

Odds ratio

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

RR:

Relative risk

ROBINS-I:

Risk Of Bias In Non-randomized Studies-of Interventions

References

  1. Cieza A, Causey K, Kamenov K, Hanson SW, Chatterji S, Vos T (2020) Global estimates of the need for rehabilitation based on the Global Burden of Disease study 2019: a systematic analysis for the Global Burden of Disease Study 2019. The Lancet 396:2006–2017

    Article  CAS  Google Scholar 

  2. Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR (2009) Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA 301:513–521

    Article  CAS  PubMed  Google Scholar 

  3. Center JR (2017) Fracture burden: what two and a half decades of Dubbo Osteoporosis Epidemiology Study data reveal about clinical outcomes of osteoporosis. Curr Osteoporos Rep 15:88–95

    Article  PubMed  Google Scholar 

  4. Curry SJ, Krist AH, Owens DK, Barry MJ, Caughey AB, Davidson KW, Doubeni CA, Epling JW, Kemper AR, Kubik M (2018) Screening for osteoporosis to prevent fractures: US Preventive Services Task Force recommendation statement. JAMA 319:2521–2531

    Article  PubMed  Google Scholar 

  5. Johnston CB, Dagar M (2020) Osteoporosis in older adults. Medical. Clinics 104:873–884

    Google Scholar 

  6. Boonen S, Reginster J-Y, Kaufman J-M, Lippuner K, Zanchetta J, Langdahl B, Rizzoli R, Lipschitz S, Dimai HP, Witvrouw R (2012) Fracture risk and zoledronic acid therapy in men with osteoporosis. N Engl J Med 367:1714–1723

    Article  CAS  PubMed  Google Scholar 

  7. Donaldson L, Reckless I, Scholes S, Mindell JS, Shelton NJ (2008) The epidemiology of fractures in England. J Epidemiol Community Health 62:174–180

    Article  CAS  PubMed  Google Scholar 

  8. Hernlund E, Svedbom A, Ivergård M, Compston J, Cooper C, Stenmark J, McCloskey EV, Jönsson B, Kanis JA (2013) Osteoporosis in the European Union: medical management, epidemiology and economic burden: a report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 8:1–115

    Article  Google Scholar 

  9. Tatangelo G, Watts J, Lim K, Connaughton C, Abimanyi-Ochom J, Borgström F, Nicholson GC, Shore-Lorenti C, Stuart AL, Iuliano-Burns S (2019) The cost of osteoporosis, osteopenia, and associated fractures in Australia in 2017. J Bone Miner Res 34:616–625

    Article  PubMed  Google Scholar 

  10. Gullberg B, Johnell O, Kanis J (1997) World-wide projections for hip fracture. Osteoporosis Int 7:407–413

    Article  CAS  Google Scholar 

  11. Dong Y, Zhao R, Wang C, Guo T (2018) Tuina for osteoporosis: a systematic review protocol. Medicine 97:e9974

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lee DR, Lee J, Rota M, Lee J, Ahn HS, Park SM, Shin D (2014) Coffee consumption and risk of fractures: a systematic review and dose–response meta-analysis. Bone 63:20–28

    Article  CAS  PubMed  Google Scholar 

  13. Qu X, Zhang X, Zhai Z, Li H, Liu X, Li H, Liu G, Zhu Z, Hao Y, Dai K (2014) Association between physical activity and risk of fracture. J Bone Miner Res 29:202–211

    Article  PubMed  Google Scholar 

  14. Shen GS, Li Y, Zhao G, Zhou HB, Xie ZG, Xu W, Chen HN, Dong QR, Xu YJ (2015) Cigarette smoking and risk of hip fracture in women: a meta-analysis of prospective cohort studies. Injury 46:1333–1340

    Article  PubMed  Google Scholar 

  15. Wu A-M, Sun X-L, Lv Q-B, Zhou Y, Xia D-D, Xu H-Z, Huang Q-S, Chi Y-L (2015) The relationship between dietary protein consumption and risk of fracture: a subgroup and dose-response meta-analysis of prospective cohort studies. Sci Rep 5:9151

    Article  PubMed  PubMed Central  Google Scholar 

  16. Xu J, Song C, Song X, Zhang X, Li X (2017) Carotenoids and risk of fracture: a meta-analysis of observational studies. Oncotarget 8:2391

    Article  PubMed  Google Scholar 

  17. Beasley JM, LaCroix AZ, Larson JC, Huang Y, Neuhouser ML, Tinker LF, Jackson R, Snetselaar L, Johnson KC, Eaton CB (2014) Biomarker-calibrated protein intake and bone health in the Women’s Health Initiative clinical trials and observational study. Am J Clin Nutr 99:934–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Malmir H, Larijani B, Esmaillzadeh A (2020) Consumption of milk and dairy products and risk of osteoporosis and hip fracture: a systematic review and Meta-analysis. Crit Rev Food Sci Nutr 60:1722–1737

    Article  PubMed  Google Scholar 

  19. Sadeghi O, Djafarian K, Ghorabi S, Khodadost M, Nasiri M, Shab-Bidar S (2019) Dietary intake of fish, n-3 polyunsaturated fatty acids and risk of hip fracture: a systematic review and meta-analysis on observational studies. Crit Rev Food Sci Nutr 59:1320–1333

    Article  CAS  PubMed  Google Scholar 

  20. 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 36:481–496

    Article  CAS  PubMed  Google Scholar 

  21. Mangano KM, Sahni S, Kerstetter JE (2014) Dietary protein is beneficial to bone health under conditions of adequate calcium intake: an update on clinical research. Curr Opin Clin Nutr Metab Care 17:69–74

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Hidayat K, Du X, Shi B-M, Qin L-Q (2020) Systematic review and meta-analysis of the association between dairy consumption and the risk of hip fracture: critical interpretation of the currently available evidence. Osteoporosis Int 31:1411–1425

    Article  CAS  Google Scholar 

  23. Mann CJ (2003) Observational research methods. Research design II: cohort, cross sectional, and case-control studies. Emerg Med J 20:54–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Higgins JP, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA (2019) Cochrane handbook for systematic reviews of interventions. John Wiley & Sons

    Book  Google Scholar 

  25. Page MJ, Moher D, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE (2021) PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. Bmj 372:n160

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sterne JA, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M, Henry D, Altman DG, Ansari MT, Boutron I (2016) ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. Bmj 355:i4919

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sterne JA, Hernán MA, McAleenan A, Reeves BC, Higgins JP (2019) Chapter 25: assessing risk of bias in a non-randomized study. In: Cochrane Handbook for Systematic Reviews of Interventions. John Wiley & Sons, Chichester, UK, pp 621–641

  28. Symons M, Moore D (2002) Hazard rate ratio and prospective epidemiological studies. J Clin Epidemiol 55:893–899

    Article  CAS  PubMed  Google Scholar 

  29. Zhang J, Kai FY (1998) What’s the relative risk?: a method of correcting the odds ratio in cohort studies of common outcomes. JAMA 280:1690–1691

    Article  CAS  PubMed  Google Scholar 

  30. Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309

    Article  CAS  PubMed  Google Scholar 

  31. Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose–response data. Stand Genomic Sci 6:40–57

    Google Scholar 

  32. Talebi S, Zeraattalab-Motlagh S, Rahimlou M, Naeini F, Ranjbar M, Talebi A, Mohammadi H (2023) The association between total protein, animal protein, and animal protein sources with risk of inflammatory bowel diseases: a systematic review and meta-analysis of cohort studies. Adv Nutr 14:752–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zeraattalab-Motlagh S, Jayedi A, Shab-Bidar S (2022) Mediterranean dietary pattern and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis of prospective cohort studies. Eur J Nutr 61:1735–1748

    Article  CAS  PubMed  Google Scholar 

  34. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. Bmj 327:557–560

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hamling J, Lee P, Weitkunat R, Ambühl M (2008) Facilitating meta-analyses by deriving relative effect and precision estimates for alternative comparisons from a set of estimates presented by exposure level or disease category. Stat Med 27:954–970

    Article  PubMed  Google Scholar 

  36. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Harre FE Jr, Lee KL, Pollock BG (1988) Regression models in clinical studies: determining relationships between predictors and response. JNCI: J Nat Cancer Inst 80:1198–1202

    Article  Google Scholar 

  38. Crippa A, Discacciati A, Bottai M, Spiegelman D, Orsini N (2019) One-stage dose–response meta-analysis for aggregated data. Stat Methods Med Res 28:1579–1596

    Article  PubMed  Google Scholar 

  39. Neuenschwander M, Barbaresko J, Pischke CR, Iser N, Beckhaus J, Schwingshackl L, Schlesinger S (2020) Intake of dietary fats and fatty acids and the incidence of type 2 diabetes: a systematic review and dose-response meta-analysis of prospective observational studies. PLoS Med 17:e1003347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Schünemann HJ, Cuello C, Akl EA, Mustafa RA, Meerpohl JJ, Thayer K, Morgan RL, Gartlehner G, Kunz R, Katikireddi SV (2019) GRADE guidelines: 18. How ROBINS-I and other tools to assess risk of bias in nonrandomized studies should be used to rate the certainty of a body of evidence. J Clin Epidemiol 111:105–114

    Article  PubMed  Google Scholar 

  41. Benetou V, Orfanos P, Pettersson-Kymmer U et al (2013) Mediterranean diet and incidence of hip fractures in a European cohort. Osteoporosis Int 24:1587–1598

    Article  CAS  Google Scholar 

  42. Cumming RG, Cummings SR, Nevitt MC, Scott J, Ensrud KE, Vogt hM, Fox a, (1997) Calcium intake and fracture risk: results from the study of osteoporotic fractures. Am J Epidemiol 145:926–934

    Article  CAS  PubMed  Google Scholar 

  43. Dargent-Molina P, Sabia S, Touvier M, Kesse E, Bréart 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 23:1915–1922

    Article  CAS  PubMed  Google Scholar 

  44. 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 28:1401–1411

    Article  CAS  Google Scholar 

  45. Guo J, Givens DI, Heitmann BL (2022) Association between dairy consumption and cardiovascular disease events, bone fracture and all-cause mortality. PLoS ONE 17:e0271168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Holvik K, Meyer HE, Laake I, Feskanich D, Omsland TK, Søgaard A-J (2019) Milk drinking and risk of hip fracture: the Norwegian Epidemiologic Osteoporosis Studies (NOREPOS). Br J Nutr 121:709–718

    Article  CAS  PubMed  Google Scholar 

  47. Kojima A, Kamiya K, Kajita E, Tachiki T, Sato Y, Kouda K, Uenishi K, Tamaki J, Kagamimori S, Iki M (2023) Association between dairy product intake and risk of osteoporotic fractures in postmenopausal Japanese women: secondary analysis of 15-year follow-up data from the Japanese Population-based Osteoporosis (JPOS) cohort study. J Nutr Health Aging 27:228–237

    Article  CAS  PubMed  Google Scholar 

  48. Langsetmo L, Barr S, Berger C, Kreiger N, Rahme E, Adachi J, Papaioannou A, Kaiser S, Prior J, Hanley D (2015) Associations of protein intake and protein source with bone mineral density and fracture risk: a population-based cohort study. J Nutr Health Aging 19:861–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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 32:592–600

    Article  CAS  PubMed  Google Scholar 

  50. Lousuebsakul-Matthews V, Thorpe DL, Knutsen R, Beeson WL, Fraser GE, Knutsen SF (2014) 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

    Article  PubMed  Google Scholar 

  51. 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 145:117–123

    Article  CAS  PubMed  Google Scholar 

  52. Michaëlsson K, Wolk A, Langenskiöld S, Basu S, Lemming EW, Melhus H, Byberg L (2014) Milk intake and risk of mortality and fractures in women and men: cohort studies. Bmj 349:g6015

    Article  PubMed  PubMed Central  Google Scholar 

  53. 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 69:147–152

    Article  CAS  PubMed  Google Scholar 

  54. Na X, Xi Y, Qian S, Zhang J, Yang Y, Zhao A (2022) Association between dairy product intake and risk of fracture among adults: a cohort study from China health and nutrition survey. Nutrients 14:1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Sahni S, Mangano KM, Tucker KL, Kiel DP, Casey VA, Hannan MT (2014) Protective association of milk intake on the risk of hip fracture: results from the Framingham Original Cohort. J Bone Miner Res 29:1756–1762

    Article  CAS  PubMed  Google Scholar 

  56. 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 11:564–572

    Article  PubMed  Google Scholar 

  57. Virtanen JK, Mozaffarian D, Cauley JA, Mukamal KJ, Robbins J, Siscovick DS (2010) Fish consumption, bone mineral density, and risk of hip fracture among older adults: the cardiovascular health study. J Bone Miner Res 25:1972–1979

    Article  PubMed  PubMed Central  Google Scholar 

  58. Virtanen JK, Mozaffarian D, Willett WC, Feskanich D (2012) Dietary intake of polyunsaturated fatty acids and risk of hip fracture in men and women. Osteoporosis Int 23:2615–2624

    Article  CAS  Google Scholar 

  59. Weaver AA, Tooze JA, Cauley JA, Bauer DC, Tylavsky FA, Kritchevsky SB, Houston DK (2021) Effect of dietary protein intake on bone mineral density and fracture incidence in older adults in the health, aging, and body composition study. J Gerontol: Series A 76:2213–2222

    Article  CAS  Google Scholar 

  60. Webster J, Greenwood DC, Cade JE (2022) Foods, nutrients and hip fracture risk: a prospective study of middle-aged women. Clin Nutr 41:2825–2832

    Article  PubMed  Google Scholar 

  61. Darling AL, Manders RJF, Sahni S, Zhu K, Hewitt CE, Prince RL, Millward DJ, Lanham-New SA (2019) Dietary protein and bone health across the life-course: an updated systematic review and meta-analysis over 40 years. Osteoporos Int 30:741–761

    Article  CAS  PubMed  Google Scholar 

  62. Groenendijk I, den Boeft L, van Loon LJ, de Groot LC (2019) High versus low dietary protein intake and bone health in older adults: a systematic review and meta-analysis. Comput Struct Biotechnol J 17:1101–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Cao JJ, Johnson LK, Hunt JR (2011) 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

    Article  CAS  PubMed  Google Scholar 

  64. Hunt JR, Johnson LK, Fariba Roughead Z (2009) Dietary protein and calcium interact to influence calcium retention: a controlled feeding study. Am J Clin Nutr 89:1357–1365

    Article  CAS  PubMed  Google Scholar 

  65. 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 94:645–653

    Article  CAS  PubMed  Google Scholar 

  66. Børsheim E, Bui Q-UT, Tissier S, Kobayashi H, Ferrando AA, Wolfe RR (2008) Effect of amino acid supplementation on muscle mass, strength and physical function in elderly. Clin Nutr 27:189–195

    Article  PubMed  PubMed Central  Google Scholar 

  67. Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford AP, Casperson SL, Jiang J, Chinkes DL, Urban RJ (2009) Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women. J Clin Endocrinol Metab 94:1630–1637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wolfe RR (2006) The underappreciated role of muscle in health and disease. Am J Clin Nutr 84:475–482

    Article  CAS  PubMed  Google Scholar 

  69. Dawson-Hughes B (2003) Calcium and protein in bone health. Proc Nutr Soc 62:505–509

    Article  CAS  PubMed  Google Scholar 

  70. Corwin RL, Hartman TJ, Maczuga SA, Graubard BI (2006) Dietary saturated fat intake is inversely associated with bone density in humans: analysis of NHANES III. J Nutr 136:159–165

    Article  CAS  PubMed  Google Scholar 

  71. Deane CS, Bass JJ, Crossland H, Phillips BE, Atherton PJ (2020) Animal, plant, collagen and blended dietary proteins: effects on musculoskeletal outcomes. Nutrients 12:2670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Vijayan V, Khandelwal M, Manglani K, Gupta S, Surolia A (2014) Methionine down-regulates TLR 4/MyD 88/NF-κ B signalling in osteoclast precursors to reduce bone loss during osteoporosis. Br J Pharmacol 171:107–121

    Article  CAS  PubMed  Google Scholar 

  73. Sharan K, Lewis K, Furukawa T, Yadav VK (2017) Regulation of bone mass through pineal-derived melatonin-MT 2 receptor pathway. J Pineal Res 63:e12423

    Article  PubMed  PubMed Central  Google Scholar 

  74. Byberg L, Bellavia A, Larsson SC, Orsini N, Wolk A, Michaëlsson K (2016) Mediterranean diet and hip fracture in Swedish men and women. J Bone Miner Res 31:2098–2105

    Article  CAS  PubMed  Google Scholar 

  75. Erkkilä AT, Sadeghi H, Isanejad M, Mursu J, Tuppurainen M, Kröger H (2017) Associations of Baltic Sea and Mediterranean dietary patterns with bone mineral density in elderly women. Public Health Nutr 20:2735–2743

    Article  PubMed  PubMed Central  Google Scholar 

  76. Benetou V, Orfanos P, Zylis D, Sieri S, Contiero P, Tumino R, Giurdanella M, Peeters P, Linseisen J, Nieters A (2011) Diet and hip fractures among elderly Europeans in the EPIC cohort. Eur J Clin Nutr 65:132–139

    Article  CAS  PubMed  Google Scholar 

  77. Tucker KL, Hannan MT, Chen H, Cupples LA, Wilson PW, Kiel DP (1999) 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

    Article  CAS  PubMed  Google Scholar 

  78. Schulman RC, Weiss AJ, Mechanick JI (2011) Nutrition, bone, and aging: an integrative physiology approach. Curr Osteoporos Rep 9:184–195

    Article  PubMed  Google Scholar 

  79. Kerstetter JE, Kenny AM, Insogna KL (2011) Dietary protein and skeletal health: a review of recent human research. Curr Opin Lipidol 22:16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Díaz-Castro J, Kajarabille N, Pulido-Morán M, Moreno-Fernández J, López-Frías M, Ochoa JJ (2016) Influence of omega-3 fatty acids on bone turnover. In Hegde MV, Zanwar AA, Adekar SP (eds) Omega-3 Fatty Acids: Keys to Nutritional Health. Springer International Publishing, Cham, pp 285–291

  81. Bian S, Hu J, Zhang K, Wang Y, Yu M, Ma J (2018) Dairy product consumption and risk of hip fracture: a systematic review and meta-analysis. BMC Public Health 18:1–16

    Article  Google Scholar 

  82. Weaver CM, Gordon CM, Janz KF, Kalkwarf H, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel B (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporosis Int 27:1281–1386

    Article  CAS  Google Scholar 

  83. Zhu K, Prince RL (2015) Lifestyle and osteoporosis. Curr Osteoporos Rep 13:52–59

    Article  PubMed  Google Scholar 

  84. Burrow K, Young W, McConnell M, Carne A, Bekhit AED (2018) Do dairy minerals have a positive effect on bone health? Compr Rev Food Sci Food Safety 17:989–1005

    Article  Google Scholar 

  85. Rozenberg S, Body J-J, Bruyere O, Bergmann P, Brandi ML, Cooper C, Devogelaer J-P, Gielen E, Goemaere S, Kaufman J-M (2016) Effects of dairy products consumption on health: benefits and beliefs—a commentary from the Belgian Bone Club and the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases. Calcif Tissue Int 98:1–17

    Article  CAS  PubMed  Google Scholar 

  86. 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 1,2. Am J Clin Nutr 105:1528–1543

    Article  CAS  PubMed  Google Scholar 

  87. Ensrud KE, Palermo L, Black DM, Cauley J, Jergas M, Orwoll ES, Nevitt MC, Fox KM, Cummings SR (1995) Hip and calcaneal bone loss increase with advancing age: longitudinal results from the study of osteoporotic fractures. J Bone Miner Res 10:1778–1787

    Article  CAS  PubMed  Google Scholar 

  88. Xiao X, Xu Y, Wu Q (2018) Thiazide diuretic usage and risk of fracture: a meta-analysis of cohort studies. Osteoporosis Int 29:1515–1524

    Article  CAS  Google Scholar 

  89. Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res 25:513–519

    Article  PubMed  Google Scholar 

  90. Tagawa R, Watanabe D, Ito K, Ueda K, Nakayama K, Sanbongi C, Miyachi M (2021) Dose–response relationship between protein intake and muscle mass increase: a systematic review and meta-analysis of randomized controlled trials. Nutr Rev 79:66–75

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hamed Mohammadi.

Ethics declarations

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflicts of interest

None.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Protocol registration: PROSPERO (CRD42023411024).

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 98 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeraattalab-Motlagh, S., Mortazavi, A.S., Ghoreishy, S.M. et al. Association between total and animal proteins with risk of fracture: A systematic review and dose–response meta-analysis of cohort studies. Osteoporos Int 35, 11–23 (2024). https://doi.org/10.1007/s00198-023-06948-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-023-06948-8

Keywords

Navigation