Skip to main content

Advertisement

SpringerLink
Log in

The Impact of Diet on Bone and Fracture Risk in Diabetes

  • Bone and Diabetes (A Schwartz and P Vestergaard, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The purpose of this review is to summarize the recently published scientific evidence on the effects of diet on diabetes and skeletal health.

Recent Findings

The impact of diet on overall health has been a growing topic of interest among researchers. An inappropriate eating habit is a relatively modified risk factor for diabetes in adults. Parallel with the significant increase in the incidence of diabetes mellitus worldwide, many studies have shown the benefits of lifestyle modifications, including diet and exercise for people with, or at risk of developing, diabetes. In the last years, accumulating evidence suggests that diabetes is a risk factor for bone fragility. As lifestyle intervention represents an effective option for diabetes management and treatment, there is potential for an effect on bone health.

Summary

Healthy lifestyle is critical to prevent bone fragility. However, more studies are needed to fully understand the impact of diet and weight loss on fracture risk in diabetics.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data availability

Not applicable

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Kanis JA, Johnell O, Oden A, Sembo I, Redlund-Johnell I, Dawson A, et al. Long-term risk of osteoporotic fracture in Malmö. Osteoporos Int. 2000;11(8):669–74. https://doi.org/10.1007/s001980070064.

    Article  CAS  PubMed  Google Scholar 

  2. Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 2006;17(12):1726–33. https://doi.org/10.1007/s00198-006-0172-4.

    Article  CAS  PubMed  Google Scholar 

  3. Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. https://doi.org/10.1016/j.diabres.2019.107843.

    Article  Google Scholar 

  4. Cheng D. Prevalence, predisposition and prevention of type II diabetes. Nutr Metab (Lond). 2005;18(2):29. https://doi.org/10.1186/1743-7075-2-29.

    Article  CAS  Google Scholar 

  5. Unnikrishnan R, Pradeepa R, Joshi SR, Mohan V. Type 2 Diabetes: demystifying the global epidemic. Diabetes. 2017;66(6):1432–42. https://doi.org/10.2337/db16-0766.

    Article  CAS  PubMed  Google Scholar 

  6. Patterson CC, Dahlquist GG, Gyürüs E, Green A, Soltész G, EURODIAB Study Group. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet. 2009;373(9680):2027–33. https://doi.org/10.1016/S0140-6736(09)60568-7.

    Article  PubMed  Google Scholar 

  7. Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495–505. https://doi.org/10.1093/aje/kwm106.

    Article  PubMed  Google Scholar 

  8. Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, et al. Fracture risk in diabetic elderly men: the MrOS study. Diabetologia. 2014;57(10):2057–65. https://doi.org/10.1007/s00125-014-3289-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wang H, Ba Y, Xing Q, Du J-L. Diabetes mellitus and the risk of fractures at specific sites: a meta-analysis. BMJ Open. 2019;9(1):e024067. https://doi.org/10.1136/bmjopen-2018-024067.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Napoli N, Chandran M, Pierroz DD, Abrahamsen B, Schwartz AV, Ferrari SL, et al. Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol. 2017 Apr;13(4):208–19. https://doi.org/10.1038/nrendo.2016.153.

    Article  CAS  PubMed  Google Scholar 

  11. Krishan P, Bedi O, Rani M. Impact of diet restriction in the management of diabetes: evidences from preclinical studies. Naunyn Schmiedebergs Arch Pharmacol. 2018;391(3):235–45. https://doi.org/10.1007/s00210-017-1453-5.

    Article  CAS  PubMed  Google Scholar 

  12. Muñoz-Garach A, García-Fontana B, Muñoz-Torres M. Nutrients and dietary patterns related to osteoporosis. Nutrients. 2020 Jul 3;12(7):E1986. https://doi.org/10.3390/nu12071986.

    Article  CAS  PubMed  Google Scholar 

  13. Fujita Y. Impact of a high-fat diet on bone health during growth. Pediatric Dental Journal. 2018;28(1):1–6. https://doi.org/10.1016/j.pdj.2017.11.003.

    Article  Google Scholar 

  14. Wimalawansa SJ, Razzaque MS, Al-Daghri NM. Calcium and vitamin D in human health: hype or real? J Steroid Biochem Mol Biol. 2018;180:4–14. https://doi.org/10.1016/j.jsbmb.2017.12.009.

    Article  CAS  PubMed  Google Scholar 

  15. Barbarawi M, Zayed Y, Barbarawi O, Bala A, Alabdouh A, Gakhal I, et al. Effect of vitamin D supplementation on the incidence of diabetes mellitus. J Clin Endocrinol Metab. 2020;105(8):dgaa335. https://doi.org/10.1210/clinem/dgaa335.

    Article  PubMed  Google Scholar 

  16. Pittas AG, Dawson-Hughes B, Sheehan P, Ware JH, Knowler WC, Aroda VR, et al. Vitamin D supplementation and prevention of type 2 diabetes. N Engl J Med. 2019;381(6):520–30. https://doi.org/10.1056/NEJMoa1900906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Al Thani M, Sadoun E, Sofroniou A, Jayyousi A, Baagar KAM, Al Hammaq A, et al. The effect of vitamin D supplementation on the glycemic control of pre-diabetic Qatari patients in a randomized control trial. BMC Nutr. 2019;5:46. https://doi.org/10.1186/s40795-019-0311-x.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dong J-Y, Zhang W-G, Chen JJ, Zhang Z-L, Han S-F, Qin L-Q. Vitamin D intake and risk of type 1 diabetes: a meta-analysis of observational studies. Nutrients. 2013;5(9):3551–62. https://doi.org/10.3390/nu5093551.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Maddaloni E, Cavallari I, Napoli N, Conte C. Vitamin D and diabetes mellitus. In: Giustina A, Bilezikian JP, editors. Frontiers of Hormone Research [Internet]. S. Karger AG; 2018 [cited 2021 May 10]. p. 161–76. Available from: https://www.karger.com/Article/FullText/486083https://doi.org/10.1159/000486083

  20. Sacerdote A, Dave P, Lokshin V, Bahtiyar G. Type 2 diabetes mellitus, insulin resistance, and vitamin D. Curr Diab Rep. 2019;19(10):101. https://doi.org/10.1007/s11892-019-1201-y.

    Article  PubMed  Google Scholar 

  21. Kayaniyil S, Vieth R, Retnakaran R, Knight JA, Qi Y, Gerstein HC, et al. Association of vitamin D with insulin resistance and beta-cell dysfunction in subjects at risk for type 2 diabetes. Diabetes Care. 2010;33(6):1379–81. https://doi.org/10.2337/dc09-2321.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Maki KC, Fulgoni VL, Keast DR, Rains TM, Park KM, Rubin MR. Vitamin D intake and status are associated with lower prevalence of metabolic syndrome in U.S. adults: National Health and Nutrition Examination Surveys 2003-2006. Metab Syndr Relat Disord. 2012;10(5):363–72. https://doi.org/10.1089/met.2012.0020.

    Article  CAS  PubMed  Google Scholar 

  23. Cheng P, Fei P, Zhang Y, Hu Z, Gong H, Xu W, et al. Retracted: Serum 25-hydroxyvitamin D and risk of type 2 diabetes in older adults: a dose-response meta-analysis of prospective cohort studies. Medicine (Baltimore). 2018;97(1):e9517. https://doi.org/10.1097/MD.0000000000009517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Nikooyeh B, Neyestani TR, Farvid M, Alavi-Majd H, Houshiarrad A, Kalayi A, et al. Daily consumption of vitamin D- or vitamin D + calcium-fortified yogurt drink improved glycemic control in patients with type 2 diabetes: a randomized clinical trial. Am J Clin Nutr. 2011;93(4):764–71. https://doi.org/10.3945/ajcn.110.007336.

    Article  CAS  PubMed  Google Scholar 

  25. Lemieux P, Weisnagel SJ, Caron AZ, Julien A-S, Morisset A-S, Carreau A-M, et al. Effects of 6-month vitamin D supplementation on insulin sensitivity and secretion: a randomised, placebo-controlled trial. Eur J Endocrinol. 2019;181(3):287–99. https://doi.org/10.1530/EJE-19-0156.

    Article  CAS  PubMed  Google Scholar 

  26. Pittas AG, Dawson-Hughes B, Li T, Van Dam RM, Willett WC, Manson JE, et al. Vitamin D and calcium intake in relation to type 2 diabetes in women. Diabetes Care. 2006;29(3):650–6. https://doi.org/10.2337/diacare.29.03.06.dc05-1961.

    Article  CAS  PubMed  Google Scholar 

  27. van Dam RM, Hu FB, Rosenberg L, Krishnan S, Palmer JR. Dietary calcium and magnesium, major food sources, and risk of type 2 diabetes in U.S. black women. Diabetes Care. 2006;29(10):2238–43. https://doi.org/10.2337/dc06-1014.

    Article  CAS  PubMed  Google Scholar 

  28. Villegas R, Gao Y-T, Dai Q, Yang G, Cai H, Li H, et al. Dietary calcium and magnesium intakes and the risk of type 2 diabetes: the Shanghai Women’s Health Study. Am J Clin Nutr. 2009;89(4):1059–67. https://doi.org/10.3945/ajcn.2008.27182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kim K-N, Oh S-Y, Hong Y-C. Associations of serum calcium levels and dietary calcium intake with incident type 2 diabetes over 10 years: the Korean Genome and Epidemiology Study (KoGES). Diabetol Metab Syndr. 2018;10:50. https://doi.org/10.1186/s13098-018-0349-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Grantham NM, Magliano DJ, Hodge A, Jowett J, Meikle P, Shaw JE. The association between dairy food intake and the incidence of diabetes in Australia: the Australian Diabetes Obesity and Lifestyle Study (AusDiab). Public Health Nutr. 2013;16(2):339–45. https://doi.org/10.1017/S1368980012001310.

    Article  PubMed  Google Scholar 

  31. Muñoz-Garach A, García-Fontana B, Muñoz-Torres M. Vitamin D Status, Calcium Intake and Risk of Developing Type 2 Diabetes: An Unresolved Issue. Nutrients. 2019;16:11(3). https://doi.org/10.3390/nu11030642.

    Article  CAS  Google Scholar 

  32. Christakos S, Liu Y. Biological actions and mechanism of action of calbindin in the process of apoptosis. J Steroid Biochem Mol Biol. 2004;89–90(1–5):401–4. https://doi.org/10.1016/j.jsbmb.2004.03.007.

    Article  CAS  PubMed  Google Scholar 

  33. Pittas AG, Lau J, Hu FB, Dawson-Hughes B. The Role of Vitamin D and Calcium in Type 2 Diabetes. A Systematic Review and Meta-Analysis. The Journal of Clinical Endocrinology & Metabolism. 2007;92(6):2017–29. https://doi.org/10.1210/jc.2007-0298.

    Article  CAS  Google Scholar 

  34. Salum E, Kals J, Kampus P, Salum T, Zilmer K, Aunapuu M, et al. Vitamin D reduces deposition of advanced glycation end-products in the aortic wall and systemic oxidative stress in diabetic rats. Diabetes Res Clin Pract. 2013;100(2):243–9. https://doi.org/10.1016/j.diabres.2013.03.008.

    Article  CAS  PubMed  Google Scholar 

  35. Piccoli A, Cannata F, Strollo R, Pedone C, Leanza G, Russo F, et al. Sclerostin regulation, microarchitecture, and advanced glycation end-products in the bone of elderly women with type 2 diabetes. J Bone Miner Res. 2020;35(12):2415–22. https://doi.org/10.1002/jbmr.4153An Important study documenting that T2D affects the expression of genes involved in the regulation of bone formation (SOST and RUNX2). Moreover, it shows that AGEs accumulation is associated with impaired bone microarchitecture.

    Article  CAS  PubMed  Google Scholar 

  36. Furst JR, Bandeira LC, Fan W-W, Agarwal S, Nishiyama KK, McMahon DJ, et al. Advanced glycation endproducts and bone material strength in type 2 diabetes. The Journal of Clinical Endocrinology & Metabolism. 2016;101(6):2502–10. https://doi.org/10.1210/jc.2016-1437.

    Article  CAS  Google Scholar 

  37. Rubin MR. Skeletal fragility in diabetes. Ann N Y Acad Sci. 2017;1402(1):18–30. https://doi.org/10.1111/nyas.13463.

    Article  CAS  PubMed  Google Scholar 

  38. Cesareo R, Iozzino M, D’onofrio L, Terrinoni I, Maddaloni E, Casini A, et al. Effectiveness and safety of calcium and vitamin D treatment for postmenopausal osteoporosis. Minerva Endocrinol. 2015;40(3):231–7.

    CAS  PubMed  Google Scholar 

  39. Feng Y, Cheng G, Wang H, Chen B. The associations between serum 25-hydroxyvitamin D level and the risk of total fracture and hip fracture. Osteoporos Int. 2017;28(5):1641–52. https://doi.org/10.1007/s00198-017-3955-x.

    Article  CAS  PubMed  Google Scholar 

  40. Yao P, Bennett D, Mafham M, Lin X, Chen Z, Armitage J, et al. Vitamin D and calcium for the prevention of fracture: a systematic review and meta-analysis. JAMA Netw Open. 2019;2(12):e1917789. https://doi.org/10.1001/jamanetworkopen.2019.17789.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Ross AC, Manson JE, Abrams SA, Aloia JF, Brannon PM, Clinton SK, et al. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab. 2011;96(1):53–8. https://doi.org/10.1210/jc.2010-2704.

    Article  CAS  PubMed  Google Scholar 

  42. Tangestani H, Djafarian K, Emamat H, Arabzadegan N, Shab-Bidar S. Efficacy of vitamin D fortified foods on bone mineral density and serum bone biomarkers: a systematic review and meta-analysis of interventional studies. Crit Rev Food Sci Nutr. 2020;60(7):1094–103. https://doi.org/10.1080/10408398.2018.1558172.

    Article  CAS  PubMed  Google Scholar 

  43. Sahni S, Mangano KM, Tucker KL, Kiel DP, Casey VA, Hannan MT. Protective association of milk intake on the risk of hip fracture: results from the Framingham Original Cohort. J Bone Miner Res. 2014;29(8):1756–62. https://doi.org/10.1002/jbmr.2219.

    Article  CAS  PubMed  Google Scholar 

  44. van Dongen LH, Kiel DP, Soedamah-Muthu SS, Bouxsein ML, Hannan MT, Sahni S. Higher dairy food intake is associated with higher spine quantitative computed tomography (QCT) bone measures in the framingham study for men but not women. J Bone Miner Res. 2018;33(7):1283–90. https://doi.org/10.1002/jbmr.3414.

    Article  CAS  PubMed  Google Scholar 

  45. Radavelli-Bagatini S, Zhu K, Lewis JR, Prince RL. Dairy food intake, peripheral bone structure, and muscle mass in elderly ambulatory women. J Bone Miner Res. 2014;29(7):1691–700. https://doi.org/10.1002/jbmr.2181.

    Article  CAS  PubMed  Google Scholar 

  46. Sahni S, Mangano KM, Kiel DP, Tucker KL, Hannan MT. Dairy intake is protective against bone loss in older vitamin d supplement users: the Framingham study. J Nutr. 2017;147(4):645–52. https://doi.org/10.3945/jn.116.240390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Feskanich D, Meyer HE, Fung TT, Bischoff-Ferrari HA, Willett WC. Milk and other dairy foods and risk of hip fracture in men and women. Osteoporos Int. 2018;29(2):385–96. https://doi.org/10.1007/s00198-017-4285-8.

    Article  CAS  PubMed  Google Scholar 

  48. Bian S, Hu J, Zhang K, Wang Y, Yu M, Ma J. Dairy product consumption and risk of hip fracture: a systematic review and meta-analysis. BMC Public Health. 2018;18(1):165. https://doi.org/10.1186/s12889-018-5041-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Biver E, Durosier-Izart C, Merminod F, Chevalley T, van Rietbergen B, Ferrari SL, et al. Fermented dairy products consumption is associated with attenuated cortical bone loss independently of total calcium, protein, and energy intakes in healthy postmenopausal women. Osteoporos Int. 2018;29(8):1771–82. https://doi.org/10.1007/s00198-018-4535-4An interesting study evaluating the evolution of bone microarchitecture, strength, and structure in relation to dairy products consumption.

    Article  CAS  PubMed  Google Scholar 

  50. Rizzoli R, Biver E. Effects of fermented milk products on bone. Calcif Tissue Int. 2018;102(4):489–500. https://doi.org/10.1007/s00223-017-0317-9.

    Article  CAS  PubMed  Google Scholar 

  51. 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. 2003;326(7387):469. https://doi.org/10.1136/bmj.326.7387.469.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lyons RA, Johansen A, Brophy S, Newcombe RG, Phillips CJ, Lervy B, et al. Preventing fractures among older people living in institutional care: a pragmatic randomised double blind placebo controlled trial of vitamin D supplementation. Osteoporos Int. 2007;18(6):811–8. https://doi.org/10.1007/s00198-006-0309-5.

    Article  CAS  PubMed  Google Scholar 

  53. Bischoff-Ferrari HA, Willett WC, Wong JB, Stuck AE, Staehelin HB, Orav EJ, et al. Prevention of nonvertebral fractures with oral vitamin D and dose dependency: a meta-analysis of randomized controlled trials. Arch Intern Med. 2009;169(6):551–61. https://doi.org/10.1001/archinternmed.2008.600.

    Article  CAS  PubMed  Google Scholar 

  54. Sanders KM, Stuart AL, Williamson EJ, Simpson JA, Kotowicz MA, Young D, et al. Annual high-dose oral vitamin D and falls and fractures in older women: a randomized controlled trial. JAMA. 2010;303(18):1815–22. https://doi.org/10.1001/jama.2010.594.

    Article  CAS  PubMed  Google Scholar 

  55. Boonen S, Lips P, Bouillon R, Bischoff-Ferrari HA, Vanderschueren D, Haentjens P. Need for additional calcium to reduce the risk of hip fracture with vitamin d supplementation: evidence from a comparative metaanalysis of randomized controlled trials. J Clin Endocrinol Metab. 2007;92(4):1415–23. https://doi.org/10.1210/jc.2006-1404.

    Article  CAS  PubMed  Google Scholar 

  56. Hu Z-C, Tang Q, Sang C-M, Tang L, Li X, Zheng G, et al. Comparison of fracture risk using different supplemental doses of vitamin D, calcium or their combination: a network meta-analysis of randomised controlled trials. BMJ Open. 2019;9(10):e024595. https://doi.org/10.1136/bmjopen-2018-024595.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Trumbo P, Schlicker S, Yates AA, Poos M. Food and Nutrition Board of the Institute of Medicine, The National Academies. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J Am Diet Assoc. 2002;102(11):1621–30. https://doi.org/10.1016/s0002-8223(02)90346-9.

    Article  PubMed  Google Scholar 

  58. Russell WR, Baka A, Björck I, Delzenne N, Gao D, Griffiths HR, et al. Impact of diet composition on blood glucose regulation. Crit Rev Food Sci Nutr. 2016;56(4):541–90. https://doi.org/10.1080/10408398.2013.792772.

    Article  CAS  PubMed  Google Scholar 

  59. Evert AB, Boucher JL, Cypress M, Dunbar SA, Franz MJ, Mayer-Davis EJ, et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care. 2014;37(Suppl 1):S120–43. https://doi.org/10.2337/dc14-S120.

    Article  PubMed  Google Scholar 

  60. Weickert MO, Pfeiffer AFH. Impact of dietary fiber consumption on insulin resistance and the prevention of type 2 diabetes. J Nutr. 2018;148(1):7–12. https://doi.org/10.1093/jn/nxx008.

    Article  PubMed  Google Scholar 

  61. Silva FM, Kramer CK, de Almeida JC, Steemburgo T, Gross JL, Azevedo MJ. Fiber intake and glycemic control in patients with type 2 diabetes mellitus: a systematic review with meta-analysis of randomized controlled trials. Nutr Rev. 2013;71(12):790–801. https://doi.org/10.1111/nure.12076.

    Article  PubMed  Google Scholar 

  62. Soare A, Khazrai YM, Del Toro R, Roncella E, Fontana L, Fallucca S, et al. The effect of the macrobiotic Ma-Pi 2 diet vs. the recommended diet in the management of type 2 diabetes: the randomized controlled MADIAB trial. Nutr Metab (Lond). 2014;11:39. https://doi.org/10.1186/1743-7075-11-39.

    Article  CAS  Google Scholar 

  63. Weickert MO, Mohlig M, Koebnick C, Holst JJ, Namsolleck P, Ristow M, et al. Impact of cereal fibre on glucose-regulating factors. Diabetologia. 2005;48(11):2343–53. https://doi.org/10.1007/s00125-005-1941-x.

    Article  CAS  PubMed  Google Scholar 

  64. Samra RA, Anderson GH. Insoluble cereal fiber reduces appetite and short-term food intake and glycemic response to food consumed 75 min later by healthy men. Am J Clin Nutr. 2007;86(4):972–9. https://doi.org/10.1093/ajcn/86.4.972.

    Article  CAS  PubMed  Google Scholar 

  65. Brighenti F, Castellani G, Benini L, Casiraghi MC, Leopardi E, Crovetti R, et al. Effect of neutralized and native vinegar on blood glucose and acetate responses to a mixed meal in healthy subjects. Eur J Clin Nutr. 1995;49(4):242–7.

    CAS  PubMed  Google Scholar 

  66. Ostman EM, Liljeberg Elmståhl HGM, Björck IME. Barley bread containing lactic acid improves glucose tolerance at a subsequent meal in healthy men and women. J Nutr. 2002;132(6):1173–5. https://doi.org/10.1093/jn/132.6.1173.

    Article  CAS  PubMed  Google Scholar 

  67. Kelley DE, Mandarino LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes. 2000;49(5):677–83. https://doi.org/10.2337/diabetes.49.5.677.

    Article  CAS  PubMed  Google Scholar 

  68. Meyer KA, Kushi LH, Jacobs DR, Slavin J, Sellers TA, Folsom AR. Carbohydrates, dietary fiber, and incident type 2 diabetes in older women. Am J Clin Nutr. 2000;71(4):921–30. https://doi.org/10.1093/ajcn/71.4.921.

    Article  CAS  PubMed  Google Scholar 

  69. Slavin JL, Martini MC, Jacobs DR, Marquart L. Plausible mechanisms for the protectiveness of whole grains. Am J Clin Nutr. 1999;70(3 Suppl):459S–63S. https://doi.org/10.1093/ajcn/70.3.459s.

    Article  CAS  PubMed  Google Scholar 

  70. Paolisso G, Barbagallo M. Hypertension, diabetes mellitus, and insulin resistance: the role of intracellular magnesium. Am J Hypertens. 1997;10(3):346–55. https://doi.org/10.1016/s0895-7061(96)00342-1.

    Article  CAS  PubMed  Google Scholar 

  71. Jenkins DJ, Kendall CW, Axelsen M, Augustin LS, Vuksan V. Viscous and nonviscous fibres, nonabsorbable and low glycaemic index carbohydrates, blood lipids and coronary heart disease. Curr Opin Lipidol. 2000;11(1):49–56. https://doi.org/10.1097/00041433-200002000-00008.

    Article  CAS  PubMed  Google Scholar 

  72. Weickert MO, Pfeiffer AFH. Metabolic effects of dietary fiber consumption and prevention of diabetes. J Nutr. 2008;138(3):439–42. https://doi.org/10.1093/jn/138.3.439.

    Article  CAS  PubMed  Google Scholar 

  73. Ma Y, Griffith JA, Chasan-Taber L, Olendzki BC, Jackson E, Stanek EJ, et al. Association between dietary fiber and serum C-reactive protein. Am J Clin Nutr. 2006;83(4):760–6. https://doi.org/10.1093/ajcn/83.4.760.

    Article  CAS  PubMed  Google Scholar 

  74. Ajani UA, Ford ES, Mokdad AH. Dietary fiber and C-reactive protein: findings from national health and nutrition examination survey data. J Nutr. 2004;134(5):1181–5. https://doi.org/10.1093/jn/134.5.1181.

    Article  CAS  PubMed  Google Scholar 

  75. Langsetmo L, Hanley DA, Prior JC, Barr SI, Anastassiades T, Towheed T, et al. Dietary patterns and incident low-trauma fractures in postmenopausal women and men aged ≥ 50 y: a population-based cohort study. Am J Clin Nutr. 2011;93(1):192–9. https://doi.org/10.3945/ajcn.110.002956.

    Article  CAS  PubMed  Google Scholar 

  76. Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PWF, Felson D, et al. Bone mineral density and dietary patterns in older adults: the Framingham osteoporosis study. Am J Clin Nutr. 2002;76(1):245–52. https://doi.org/10.1093/ajcn/76.1.245.

    Article  CAS  PubMed  Google Scholar 

  77. Hardcastle AC, Aucott L, Fraser WD, Reid DM, Macdonald HM. Dietary patterns, bone resorption and bone mineral density in early post-menopausal Scottish women. Eur J Clin Nutr. 2011;65(3):378–85. https://doi.org/10.1038/ejcn.2010.264.

    Article  CAS  PubMed  Google Scholar 

  78. Dai Z, Zhang Y, Lu N, Felson DT, Kiel DP, Sahni S. Association between dietary fiber intake and bone loss in the Framingham offspring study: association between dietary fiber intake and bone loss. Journal of Bone and Mineral Research. 2018;33(2):241–9. https://doi.org/10.1002/jbmr.3308An interesting study investigating the association between dietary fiber intake and bone loss among 792 men and 1065 women followed up for 8 years.

    Article  CAS  PubMed  Google Scholar 

  79. McCabe L, Britton RA, Parameswaran N. Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr Osteoporos Rep. 2015;13(6):363–71. https://doi.org/10.1007/s11914-015-0292-x.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Lee T, Suh HS. Associations between dietary fiber intake and bone mineral density in adult korean population: analysis of national health and nutrition examination survey in 2011. Journal of Bone Metabolism. 2019;26(3):151. https://doi.org/10.11005/jbm.2019.26.3.151.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Zhou T, Wang M, Ma H, Li X, Heianza Y, Qi L. Dietary Fiber, Genetic variations of gut microbiota-derived short-chain fatty acids, and bone health in UK biobank. J Clin Endocrinol Metab. 2021;106(1):201–10. https://doi.org/10.1210/clinem/dgaa740.

    Article  PubMed  Google Scholar 

  82. Bryk G, Coronel MZ, Pellegrini G, Mandalunis P, Rio ME, de Portela MLPM, et al. Effect of a combination GOS/FOS® prebiotic mixture and interaction with calcium intake on mineral absorption and bone parameters in growing rats. Eur J Nutr. 2015;54(6):913–23. https://doi.org/10.1007/s00394-014-0768-y.

    Article  CAS  PubMed  Google Scholar 

  83. Legette LL, Lee W, Martin BR, Story JA, Campbell JK, Weaver CM. Prebiotics enhance magnesium absorption and inulin-based fibers exert chronic effects on calcium utilization in a postmenopausal rodent model. J Food Sci. 2012;77(4):H88–94. https://doi.org/10.1111/j.1750-3841.2011.02612.x.

    Article  CAS  PubMed  Google Scholar 

  84. Takahara S, Morohashi T, Sano T, Ohta A, Yamada S, Sasa R. Fructooligosaccharide consumption enhances femoral bone volume and mineral concentrations in rats. J Nutr. 2000;130(7):1792–5. https://doi.org/10.1093/jn/130.7.1792.

    Article  CAS  PubMed  Google Scholar 

  85. Jakeman SA, Henry CN, Martin BR, McCabe GP, McCabe LD, Jackson GS, et al. Soluble corn fiber increases bone calcium retention in postmenopausal women in a dose-dependent manner: a randomized crossover trial. The American Journal of Clinical Nutrition. 2016;104(3):837–43. https://doi.org/10.3945/ajcn.116.132761.

    Article  CAS  PubMed  Google Scholar 

  86. Abrams SA, Griffin IJ, Hawthorne KM, Liang L, Gunn SK, Darlington G, et al. A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr. 2005;82(2):471–6. https://doi.org/10.1093/ajcn.82.2.471.

    Article  CAS  PubMed  Google Scholar 

  87. Whisner CM, Martin BR, Nakatsu CH, Story JA, MacDonald-Clarke CJ, McCabe LD, et al. Soluble corn fiber increases calcium absorption associated with shifts in the gut microbiome: a randomized dose-response trial in free-living pubertal females. J Nutr. 2016;146(7):1298–306. https://doi.org/10.3945/jn.115.227256.

    Article  CAS  PubMed  Google Scholar 

  88. Weaver CM, Martin BR, Story JA, Hutchinson I, Sanders L. Novel fibers increase bone calcium content and strength beyond efficiency of large intestine fermentation. J Agric Food Chem. 2010;58(16):8952–7. https://doi.org/10.1021/jf904086d.

    Article  CAS  PubMed  Google Scholar 

  89. Scholz-Ahrens KE, Schrezenmeir J. Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J Nutr. 2007;137(11 Suppl):2513S–23S. https://doi.org/10.1093/jn/137.11.2513S.

    Article  CAS  PubMed  Google Scholar 

  90. Lucas S, Omata Y, Hofmann J, Böttcher M, Iljazovic A, Sarter K, et al. Short-chain fatty acids regulate systemic bone mass and protect from pathological bone loss. Nat Commun. 2018;9(1):55. https://doi.org/10.1038/s41467-017-02490-4This study shows the effect of SCFAs on osteoclast metabolism and bone homeostasis in vivo.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Shah M, Chandalia M, Adams-Huet B, Brinkley LJ, Sakhaee K, Grundy SM, et al. Effect of a high-fiber diet compared with a moderate-fiber diet on calcium and other mineral balances in subjects with type 2 diabetes. Diabetes Care. 2009;32(6):990–5. https://doi.org/10.2337/dc09-0126.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Martin BR, Braun MM, Wigertz K, Bryant R, Zhao Y, Lee W, et al. Fructo-oligosaccharides and calcium absorption and retention in adolescent girls. J Am Coll Nutr. 2010;29(4):382–6. https://doi.org/10.1080/07315724.2010.10719855.

    Article  CAS  PubMed  Google Scholar 

  93. Zupo R, Lampignano L, Lattanzio A, Mariano F, Osella AR, Bonfiglio C, et al. Association between adherence to the Mediterranean DIET AND CIRCULATING VITAMIN D LEVELS. International Journal of Food Sciences and Nutrition. 2020;71(7):884–90. https://doi.org/10.1080/09637486.2020.1744533.

    Article  CAS  PubMed  Google Scholar 

  94. Sofi F. The Mediterranean diet revisited: evidence of its effectiveness grows. Curr Opin Cardiol. 2009;24(5):442–6. https://doi.org/10.1097/HCO.0b013e32832f056e.

    Article  PubMed  Google Scholar 

  95. Bonaccio M, Pounis G, Cerletti C, Donati MB, Iacoviello L, de Gaetano G, et al. Mediterranean diet, dietary polyphenols and low grade inflammation: results from the MOLI-SANI study. Br J Clin Pharmacol. 2017;83(1):107–13. https://doi.org/10.1111/bcp.12924.

    Article  CAS  PubMed  Google Scholar 

  96. American Diabetes Association. 4. Lifestyle management: standards of medical care in diabetes-2018. Diabetes Care. 2018;41(Suppl 1):S38–50. https://doi.org/10.2337/dc18-S004.

    Article  Google Scholar 

  97. Chester B, Babu JR, Greene MW, Geetha T. The effects of popular diets on type 2 diabetes management. Diabetes Metab Res Rev. 2019;35(8):e3188. https://doi.org/10.1002/dmrr.3188.

    Article  PubMed  Google Scholar 

  98. Schwingshackl L, Missbach B, König J, Hoffmann G. Adherence to a Mediterranean diet and risk of diabetes: a systematic review and meta-analysis. Public Health Nutr. 2015;18(7):1292–9. https://doi.org/10.1017/S1368980014001542.

    Article  PubMed  Google Scholar 

  99. Koloverou E, Esposito K, Giugliano D, Panagiotakos D. The effect of Mediterranean diet on the development of type 2 diabetes mellitus: a meta-analysis of 10 prospective studies and 136,846 participants. Metabolism. 2014;63(7):903–11. https://doi.org/10.1016/j.metabol.2014.04.010.

    Article  CAS  PubMed  Google Scholar 

  100. Salas-Salvadó J, Bulló M, Estruch R, Ros E, Covas M-I, Ibarrola-Jurado N, et al. Prevention of diabetes with Mediterranean diets: a subgroup analysis of a randomized trial. Ann Intern Med. 2014;160(1):1–10. https://doi.org/10.7326/M13-1725.

    Article  PubMed  Google Scholar 

  101. Guasch-Ferré M, Hruby A, Salas-Salvadó J, Martínez-González MA, Sun Q, Willett WC, et al. Olive oil consumption and risk of type 2 diabetes in US women. Am J Clin Nutr. 2015;102(2):479–86. https://doi.org/10.3945/ajcn.115.112029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Zhong VW, Lamichhane AP, Crandell JL, Couch SC, Liese AD, The NS, et al. Association of adherence to a Mediterranean diet with glycemic control and cardiovascular risk factors in youth with type I diabetes: the SEARCH Nutrition Ancillary Study. Eur J Clin Nutr. 2016;70(7):802–7. https://doi.org/10.1038/ejcn.2016.8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Esposito K, Maiorino MI, Bellastella G, Chiodini P, Panagiotakos D, Giugliano D. A journey into a Mediterranean diet and type 2 diabetes: a systematic review with meta-analyses. BMJ Open. 2015;5(8):e008222. https://doi.org/10.1136/bmjopen-2015-008222.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Toobert DJ, Glasgow RE, Strycker LA, Barrera M, Radcliffe JL, Wander RC, et al. Biologic and quality-of-life outcomes from the Mediterranean Lifestyle Program: a randomized clinical trial. Diabetes Care. 2003;26(8):2288–93. https://doi.org/10.2337/diacare.26.8.2288.

    Article  PubMed  Google Scholar 

  105. Elhayany A, Lustman A, Abel R, Attal-Singer J, Vinker S. A low carbohydrate Mediterranean diet improves cardiovascular risk factors and diabetes control among overweight patients with type 2 diabetes mellitus: a 1-year prospective randomized intervention study. Diabetes Obes Metab. 2010;12(3):204–9. https://doi.org/10.1111/j.1463-1326.2009.01151.x.

    Article  CAS  PubMed  Google Scholar 

  106. Esposito K, Maiorino MI, Di Palo C, Giugliano D. Campanian Postprandial hyperglycemia study group. Adherence to a Mediterranean diet and glycaemic control in Type 2 diabetes mellitus. Diabet Med. 2009;26(9):900–7. https://doi.org/10.1111/j.1464-5491.2009.02798.x.

    Article  CAS  PubMed  Google Scholar 

  107. Santangelo C, Filesi C, Varì R, Scazzocchio B, Filardi T, Fogliano V, et al. Consumption of extra-virgin olive oil rich in phenolic compounds improves metabolic control in patients with type 2 diabetes mellitus: a possible involvement of reduced levels of circulating visfatin. J Endocrinol Invest. 2016;39(11):1295–301. https://doi.org/10.1007/s40618-016-0506-9.

    Article  CAS  PubMed  Google Scholar 

  108. Shai I, Schwarzfuchs D, Henkin Y, Shahar DR, Witkow S, Greenberg I, et al. Weight loss with a low-carbohydrate, Mediterranean, or low-fat diet. N Engl J Med. 2008;359(3):229–41. https://doi.org/10.1056/NEJMoa0708681.

    Article  CAS  PubMed  Google Scholar 

  109. Esposito K, Maiorino MI, Ciotola M, Di Palo C, Scognamiglio P, Gicchino M, et al. Effects of a Mediterranean-style diet on the need for antihyperglycemic drug therapy in patients with newly diagnosed type 2 diabetes: a randomized trial. Ann Intern Med. 2009;151(5):306–14. https://doi.org/10.7326/0003-4819-151-5-200909010-00004.

    Article  PubMed  Google Scholar 

  110. Panagiotakos DB, Tzima N, Pitsavos C, Chrysohoou C, Zampelas A, Toussoulis D, et al. The association between adherence to the Mediterranean diet and fasting indices of glucose homoeostasis: the ATTICA Study. J Am Coll Nutr. 2007;26(1):32–8. https://doi.org/10.1080/07315724.2007.10719583.

    Article  PubMed  Google Scholar 

  111. Soriguer F, Goday A, Bosch-Comas A, Bordiú E, Calle-Pascual A, Carmena R, et al. Prevalence of diabetes mellitus and impaired glucose regulation in Spain: the Di@bet.es Study. Diabetologia. 2012;55(1):88–93. https://doi.org/10.1007/s00125-011-2336-9.

    Article  CAS  PubMed  Google Scholar 

  112. Qian F, Korat AA, Malik V, Hu FB. Metabolic effects of monounsaturated fatty acid-enriched diets compared with carbohydrate or polyunsaturated fatty acid-enriched diets in patients with type 2 diabetes: a systematic review and meta-analysis of randomized controlled trials. Diabetes Care. 2016;39(8):1448–57. https://doi.org/10.2337/dc16-0513.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Jannasch F, Kröger J, Schulze MB. Dietary patterns and type 2 diabetes: a systematic literature review and meta-analysis of prospective studies. J Nutr. 2017;147(6):1174–82. https://doi.org/10.3945/jn.116.242552.

    Article  CAS  PubMed  Google Scholar 

  114. Schwingshackl L, Chaimani A, Hoffmann G, Schwedhelm C, Boeing H. A network meta-analysis on the comparative efficacy of different dietary approaches on glycaemic control in patients with type 2 diabetes mellitus. Eur J Epidemiol. 2018;33(2):157–70. https://doi.org/10.1007/s10654-017-0352-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Martinez-Lacoba R, Pardo-Garcia I, Amo-Saus E, Escribano-Sotos F. Mediterranean diet and health outcomes: a systematic meta-review. Eur J Public Health. 2018;28(5):955–61. https://doi.org/10.1093/eurpub/cky113.

    Article  PubMed  Google Scholar 

  116. Xu H, Luo J, Huang J, Wen Q. Flavonoids intake and risk of type 2 diabetes mellitus: a meta-analysis of prospective cohort studies. Medicine (Baltimore). 2018;97(19):e0686. https://doi.org/10.1097/MD.0000000000010686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Martín-Peláez S, Fito M, Castaner O. Mediterranean diet effects on type 2 diabetes prevention, disease progression, and related mechanisms. A Review. Nutrients. 2020;12(8):E2236. https://doi.org/10.3390/nu12082236.

    Article  CAS  PubMed  Google Scholar 

  118. Guasch-Ferré M, Merino J, Sun Q, Fitó M, Salas-Salvadó J. Dietary polyphenols, Mediterranean diet, prediabetes, and type 2 diabetes: a narrative review of the evidence. Oxid Med Cell Longev. 2017;2017:6723931. https://doi.org/10.1155/2017/6723931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Eid HM, Martineau LC, Saleem A, Muhammad A, Vallerand D, Benhaddou-Andaloussi A, et al. Stimulation of AMP-activated protein kinase and enhancement of basal glucose uptake in muscle cells by quercetin and quercetin glycosides, active principles of the antidiabetic medicinal plant Vaccinium vitis-idaea. Mol Nutr Food Res. 2010;54(7):991–1003. https://doi.org/10.1002/mnfr.200900218.

    Article  CAS  PubMed  Google Scholar 

  120. Dhanya R, Arya AD, Nisha P, Jayamurthy P. Quercetin, a Lead compound against type 2 diabetes ameliorates glucose uptake via AMPK pathway in skeletal muscle cell line. Front Pharmacol. 2017;8:336. https://doi.org/10.3389/fphar.2017.00336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Maiorino MI, Bellastella G, Petrizzo M, Scappaticcio L, Giugliano D, Esposito K. Mediterranean diet cools down the inflammatory milieu in type 2 diabetes: the MÉDITA randomized controlled trial. Endocrine. 2016;54(3):634–41. https://doi.org/10.1007/s12020-016-0881-1.

    Article  CAS  PubMed  Google Scholar 

  122. Tuck KL, Hayball PJ. Major phenolic compounds in olive oil: metabolism and health effects. J Nutr Biochem. 2002;13(11):636–44. https://doi.org/10.1016/s0955-2863(02)00229-2.

    Article  CAS  PubMed  Google Scholar 

  123. Torres-Peña JD, Garcia-Rios A, Delgado-Casado N, Gomez-Luna P, Alcala-Diaz JF, Yubero-Serrano EM, et al. Mediterranean diet improves endothelial function in patients with diabetes and prediabetes: A report from the CORDIOPREV study. Atherosclerosis. 2018;269:50–6. https://doi.org/10.1016/j.atherosclerosis.2017.12.012.

    Article  CAS  PubMed  Google Scholar 

  124. Estruch R, Martínez-González MA, Corella D, Salas-Salvadó J, Ruiz-Gutiérrez V, Covas MI, et al. Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med. 2006;145(1):1–11. https://doi.org/10.7326/0003-4819-145-1-200607040-00004.

    Article  PubMed  Google Scholar 

  125. Berger MM, Delodder F, Liaudet L, Tozzi P, Schlaepfer J, Chiolero RL, et al. Three short perioperative infusions of n-3 PUFAs reduce systemic inflammation induced by cardiopulmonary bypass surgery: a randomized controlled trial. Am J Clin Nutr. 2013;97(2):246–54. https://doi.org/10.3945/ajcn.112.046573.

    Article  CAS  PubMed  Google Scholar 

  126. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes. 2003;52(3):726–33. https://doi.org/10.2337/diabetes.52.3.726.

    Article  CAS  PubMed  Google Scholar 

  127. Ceriello A, Esposito K, La Sala L, Pujadas G, De Nigris V, Testa R, et al. The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: a preliminary report. Cardiovasc Diabetol. 2014;13:140. https://doi.org/10.1186/s12933-014-0140-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Sundström L, Myhre S, Sundqvist M, Ahnmark A, McCoull W, Raubo P, et al. The acute glucose lowering effect of specific GPR120 activation in mice is mainly driven by glucagon-like peptide 1. PLoS One. 2017;12(12):e0189060. https://doi.org/10.1371/journal.pone.0189060.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Palomeras-Vilches A, Viñals-Mayolas E, Bou-Mias C, Jordà-Castro M, Agüero-Martínez M, Busquets-Barceló M, et al. Adherence to the mediterranean diet and bone fracture risk in middle-aged women: a case control study. Nutrients. 2019;11(10):E2508. https://doi.org/10.3390/nu11102508.

    Article  CAS  PubMed  Google Scholar 

  130. da Silva TR, Martins CC, Ferreira LL, Spritzer PM. Mediterranean diet is associated with bone mineral density and muscle mass in postmenopausal women. Climacteric. 2019;22(2):162–8. https://doi.org/10.1080/13697137.2018.1529747.

    Article  PubMed  Google Scholar 

  131. Savanelli MC, Barrea L, Macchia PE, Savastano S, Falco A, Renzullo A, et al. Preliminary results demonstrating the impact of Mediterranean diet on bone health. J Transl Med. 2017;15(1):81. https://doi.org/10.1186/s12967-017-1184-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Malmir H, Saneei P, Larijani B, Esmaillzadeh A. Adherence to Mediterranean diet in relation to bone mineral density and risk of fracture: a systematic review and meta-analysis of observational studies. Eur J Nutr. 2018;57(6):2147–60. https://doi.org/10.1007/s00394-017-1490-3Meta-analysis across 358,746 individuals concluding that adherence to MD is associated with a decreased risk of fracture as well as with a higher BMD.

    Article  PubMed  Google Scholar 

  133. de Jonge EA, Kiefte-de Jong JC, Hofman A, Uitterlinden AG, Kieboom BC, Voortman T, et al. Dietary patterns explaining differences in bone mineral density and hip structure in the elderly: the Rotterdam Study. Am J Clin Nutr. 2017;105(1):203–11. https://doi.org/10.3945/ajcn.116.139196.

    Article  CAS  PubMed  Google Scholar 

  134. Chin K-Y, Ima-Nirwana S. Olives and bone: a green osteoporosis prevention option. Int J Environ Res Public Health. 2016;13(8):E755. https://doi.org/10.3390/ijerph13080755.

    Article  CAS  PubMed  Google Scholar 

  135. García-Martínez O, Rivas A, Ramos-Torrecillas J, De Luna-Bertos E, Ruiz C. The effect of olive oil on osteoporosis prevention. Int J Food Sci Nutr. 2014;65(7):834–40. https://doi.org/10.3109/09637486.2014.931361.

    Article  CAS  PubMed  Google Scholar 

  136. Fernández-Real JM, Bulló M, Moreno-Navarrete JM, Ricart W, Ros E, Estruch R, et al. A Mediterranean diet enriched with olive oil is associated with higher serum total osteocalcin levels in elderly men at high cardiovascular risk. J Clin Endocrinol Metab. 2012;97(10):3792–8. https://doi.org/10.1210/jc.2012-2221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Estruch R, Ros E, Salas-Salvadó J, Covas M-I, Corella D, Arós F, et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med. 2013;368(14):1279–90. https://doi.org/10.1056/NEJMoa1200303.

    Article  CAS  PubMed  Google Scholar 

  138. Nagao M, Asai A, Sugihara H, Oikawa S. Fat intake and the development of type 2 diabetes. Endocr J. 2015;62(7):561–72. https://doi.org/10.1507/endocrj.EJ15-0055.

    Article  CAS  PubMed  Google Scholar 

  139. Lovejoy JC. The influence of dietary fat on insulin resistance. Curr Diab Rep. 2002;2(5):435–40. https://doi.org/10.1007/s11892-002-0098-y.

    Article  PubMed  Google Scholar 

  140. Tencerova M, Figeac F, Ditzel N, Taipaleenmäki H, Nielsen TK, Kassem M. High-fat diet-induced obesity promotes expansion of bone marrow adipose tissue and impairs skeletal stem cell functions in mice. J Bone Miner Res. 2018;33(6):1154–65. https://doi.org/10.1002/jbmr.3408.

    Article  CAS  PubMed  Google Scholar 

  141. Compston J. Type 2 diabetes mellitus and bone. J Intern Med. 2018;283(2):140–53. https://doi.org/10.1111/joim.12725.

    Article  CAS  PubMed  Google Scholar 

  142. Movassagh EZ, Vatanparast H. Current evidence on the association of dietary patterns and bone health: a scoping review. Adv Nutr. 2017;8(1):1–16. https://doi.org/10.3945/an.116.013326.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Kwon Y-M, Kim GW, Yim HW, Paek YJ, Lee K-S. Association between dietary fat intake and bone mineral density in Korean adults: data from Korea National Health and Nutrition Examination Survey IV (2008 ∼ 2009). Osteoporos Int. 2015;26(3):969–76. https://doi.org/10.1007/s00198-014-2977-x.

    Article  PubMed  Google Scholar 

  144. Qiao J, Wu Y, Ren Y. The impact of a high fat diet on bones: potential mechanisms. Food Funct. 2021;12(3):963–75. https://doi.org/10.1039/d0fo02664fThis is a comprehensive review of the literature reporting the actual knowledge about the relationship between an HFD and bone health and summarizing the main underlying mechanisms by which an HFD may cause osteoporosis.

    Article  CAS  PubMed  Google Scholar 

  145. Ghanim H, Aljada A, Hofmeyer D, Syed T, Mohanty P, Dandona P. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation. 2004;110(12):1564–71. https://doi.org/10.1161/01.CIR.0000142055.53122.FA.

    Article  CAS  PubMed  Google Scholar 

  146. Bao M, Zhang K, Wei Y, Hua W, Gao Y, Li X, et al. Therapeutic potentials and modulatory mechanisms of fatty acids in bone. Cell Prolif. 2020;53(2):e12735. https://doi.org/10.1111/cpr.12735.

    Article  PubMed  Google Scholar 

  147. Karpouzos A, Diamantis E, Farmaki P, Savvanis S, Troupis T. Nutritional aspects of bone health and fracture healing. J Osteoporos. 2017;2017:4218472. https://doi.org/10.1155/2017/4218472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Wan Y, Wang F, Yuan J, Li J, Jiang D, Zhang J, et al. Effects of dietary fat on gut microbiota and faecal metabolites, and their relationship with cardiometabolic risk factors: a 6-month randomised controlled-feeding trial. Gut. 2019;68(8):1417–29. https://doi.org/10.1136/gutjnl-2018-317609.

    Article  CAS  PubMed  Google Scholar 

  149. Li Y, Lu Z, Ru JH, Lopes-Virella MF, Lyons TJ, Huang Y. Saturated fatty acid combined with lipopolysaccharide stimulates a strong inflammatory response in hepatocytes in vivo and in vitro. Am J Physiol Endocrinol Metab. 2018;315(5):E745–57. https://doi.org/10.1152/ajpendo.00015.2018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. McCabe LR, Irwin R, Tekalur A, Evans C, Schepper JD, Parameswaran N, et al. Exercise prevents high fat diet-induced bone loss, marrow adiposity and dysbiosis in male mice. Bone. 2019;118:20–31. https://doi.org/10.1016/j.bone.2018.03.024Interesting study showing that exercise can inhibit many of the negative effects of a high-fat diet on bone health.

    Article  CAS  PubMed  Google Scholar 

  151. Yang Y, Zhong Z, Wang B, Xia X, Yao W, Huang L, et al. Early-life high-fat diet-induced obesity programs hippocampal development and cognitive functions via regulation of gut commensal Akkermansia muciniphila. Neuropsychopharmacology. 2019;44(12):2054–64. https://doi.org/10.1038/s41386-019-0437-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Bibbò S, Ianiro G, Giorgio V, Scaldaferri F, Masucci L, Gasbarrini A, et al. The role of diet on gut microbiota composition. Eur Rev Med Pharmacol Sci. 2016;20(22):4742–9.

    PubMed  Google Scholar 

  153. Cortez M, Carmo LS, Rogero MM, Borelli P, Fock RA. A high-fat diet increases IL-1, IL-6, and TNF-α production by increasing NF-κB and attenuating PPAR-γ expression in bone marrow mesenchymal stem cells. Inflammation. 2013;36(2):379–86. https://doi.org/10.1007/s10753-012-9557-z.

    Article  CAS  PubMed  Google Scholar 

  154. Hafner H, Chang E, Carlson Z, Zhu A, Varghese M, Clemente J, et al. Lactational high-fat diet exposure programs metabolic inflammation and bone marrow adiposity in male offspring. Nutrients. 2019;11(6):E1393. https://doi.org/10.3390/nu11061393.

    Article  CAS  PubMed  Google Scholar 

  155. Zhou Z, Pan C, Wang N, Zhou L, Shan H, Gao Y, et al. A high-fat diet aggravates osteonecrosis through a macrophage-derived IL-6 pathway. Int Immunol. 2019;31(4):263–73. https://doi.org/10.1093/intimm/dxz002.

    Article  CAS  PubMed  Google Scholar 

  156. Feng W, Liu B, Liu D, Hasegawa T, Wang W, Han X, et al. Long-term administration of high-fat diet corrects abnormal bone remodeling in the tibiae of interleukin-6-deficient mice. J Histochem Cytochem. 2016;64(1):42–53. https://doi.org/10.1369/0022155415611931.

    Article  CAS  PubMed  Google Scholar 

  157. Zhang K, Wang C, Chen Y, Ji X, Chen X, Tian L, et al. Preservation of high-fat diet-induced femoral trabecular bone loss through genetic target of TNF-α. Endocrine. 2015;50(1):239–49. https://doi.org/10.1007/s12020-015-0554-5.

    Article  CAS  PubMed  Google Scholar 

  158. Zhang X, Li X, Sheng Z, Wang S, Li B, Tao S, et al. Effects of combined exposure to cadmium and high-fat diet on bone quality in male mice. Biol Trace Elem Res. 2020;193(2):434–44. https://doi.org/10.1007/s12011-019-01713-7.

    Article  CAS  PubMed  Google Scholar 

  159. Narayanan SA, Metzger CE, Bloomfield SA, Zawieja DC. Inflammation-induced lymphatic architecture and bone turnover changes are ameliorated by irisin treatment in chronic inflammatory bowel disease. FASEB J. 2018;32(9):4848–61. https://doi.org/10.1096/fj.201800178R.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Heiland GR, Zwerina K, Baum W, Kireva T, Distler JH, Grisanti M, et al. Neutralisation of Dkk-1 protects from systemic bone loss during inflammation and reduces sclerostin expression. Ann Rheum Dis. 2010;69(12):2152–9. https://doi.org/10.1136/ard.2010.132852.

    Article  CAS  PubMed  Google Scholar 

  161. Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev. 2010;31(3):266–300. https://doi.org/10.1210/er.2009-0024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Baek KH, Oh KW, Lee WY, Lee SS, Kim MK, Kwon HS, et al. Association of oxidative stress with postmenopausal osteoporosis and the effects of hydrogen peroxide on osteoclast formation in human bone marrow cell cultures. Calcif Tissue Int. 2010;87(3):226–35. https://doi.org/10.1007/s00223-010-9393-9.

    Article  CAS  PubMed  Google Scholar 

  163. Tencerova M, Figeac F, Ditzel N, Taipaleenmäki H, Nielsen TK, Kassem M. High-fat diet-induced obesity promotes expansion of bone marrow adipose tissue and impairs skeletal stem cell functions in mice. J Bone Miner Res. 2018;33(6):1154–65. https://doi.org/10.1002/jbmr.3408.

    Article  CAS  PubMed  Google Scholar 

  164. Kawao N, Ishida M, Kaji H. Roles of leptin in the recovery of muscle and bone by reloading after mechanical unloading in high fat diet-fed obese mice. PLoS One. 2019;14(10):e0224403. https://doi.org/10.1371/journal.pone.0224403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Yue R, Zhou BO, Shimada IS, Zhao Z, Morrison SJ. Leptin receptor promotes adipogenesis and reduces osteogenesis by regulating mesenchymal stromal cells in adult bone marrow. Cell Stem Cell. 2016;18(6):782–96. https://doi.org/10.1016/j.stem.2016.02.015.

    Article  CAS  PubMed  Google Scholar 

  166. Bi X, Loo YT, Henry CJ. Relationships between adiponectin and bone: sex difference. Nutrition. 2020;70:110489. https://doi.org/10.1016/j.nut.2019.04.004.

    Article  CAS  PubMed  Google Scholar 

  167. Cock T-A, Auwerx J. Leptin: cutting the fat off the bone. Lancet. 2003;362(9395):1572–4. https://doi.org/10.1016/S0140-6736(03)14747-2.

    Article  CAS  PubMed  Google Scholar 

  168. Naot D, Musson DS, Cornish J. The activity of adiponectin in bone. Calcif Tissue Int. 2017;100(5):486–99. https://doi.org/10.1007/s00223-016-0216-5.

    Article  CAS  PubMed  Google Scholar 

  169. Wahli W. PPAR gamma: ally and foe in bone metabolism. Cell Metab. 2008;7(3):188–90. https://doi.org/10.1016/j.cmet.2008.02.005.

    Article  CAS  PubMed  Google Scholar 

  170. Benetou V, Orfanos P, Pettersson-Kymmer U, Bergström U, Svensson O, Johansson I, et al. Mediterranean diet and incidence of hip fractures in a European cohort. Osteoporos Int. 2013;24(5):1587–98. https://doi.org/10.1007/s00198-012-2187-3.

    Article  CAS  PubMed  Google Scholar 

  171. García-Gavilán JF, Bulló M, Canudas S, Martínez-González MA, Estruch R, Giardina S, et al. Extra virgin olive oil consumption reduces the risk of osteoporotic fractures in the PREDIMED trial. Clin Nutr. 2018;37(1):329–35. https://doi.org/10.1016/j.clnu.2016.12.030.

    Article  CAS  PubMed  Google Scholar 

  172. Benetou V, Orfanos P, Feskanich D, Michaëlsson K, Pettersson-Kymmer U, Byberg L, et al. Mediterranean diet and hip fracture incidence among older adults: the CHANCES project. Osteoporos Int. 2018;29(7):1591–9. https://doi.org/10.1007/s00198-018-4517-6.

    Article  CAS  PubMed  Google Scholar 

  173. Sahni S, Mangano KM, McLean RR, Hannan MT, Kiel DP. Dietary approaches for bone health: lessons from the framingham osteoporosis study. Curr Osteoporos Rep. 2015;13(4):245–55. https://doi.org/10.1007/s11914-015-0272-1.

    Article  PubMed  PubMed Central  Google Scholar 

  174. Villareal DT, Apovian CM, Kushner RF, Klein S. American Society for Nutrition, NAASO, The Obesity Society. Obesity in older adults: technical review and position statement of the American Society for Nutrition and NAASO, The Obesity Society. Am J Clin Nutr. 2005;82(5):923–34. https://doi.org/10.1093/ajcn/82.5.923.

    Article  CAS  PubMed  Google Scholar 

  175. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med. 2011;364(13):1218–29. https://doi.org/10.1056/NEJMoa1008234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, et al. Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones. J Bone Miner Res. 2011;26(12):2851–9. https://doi.org/10.1002/jbmr.475.

    Article  CAS  PubMed  Google Scholar 

  177. Armamento-Villareal R, Sadler C, Napoli N, Shah K, Chode S, Sinacore DR, et al. Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. J Bone Miner Res. 2012;27(5):1215–21. https://doi.org/10.1002/jbmr.1560.

    Article  CAS  PubMed  Google Scholar 

  178. Johnson KC, Bray GA, Cheskin LJ, Clark JM, Egan CM, Foreyt JP, et al. The effect of intentional weight loss on fracture risk in persons with diabetes: results from the look AHEAD randomized clinical trial. J Bone Miner Res. 2017;32(11):2278–87. https://doi.org/10.1002/jbmr.3214.

    Article  PubMed  Google Scholar 

Download references

Code Availability

Not applicable

Funding

M.F. is supported by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 860898.

Author information

Authors and Affiliations

  1. Unit of Endocrinology and Diabetes, Department of Medicine, Campus Bio-Medico University of Rome, Via Alvaro del Portillo 21, 00128, Rome, Italy

    M. Faraj & N. Napoli

  2. Division of Bone and Mineral Diseases, Washington University in St. Louis, St. Louis, MO, USA

    N. Napoli

Authors
  1. M. Faraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Napoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Napoli.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Human and Animal Rights

All reported data coming from human studies performed by the authors have been previously published and complied with all applicable ethical standards including the Helsinki declaration and its amendments, institutional/national research committee standards and guidelines.

Additional information

Publisher’s Note

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

This article is part of the Topical Collection on Bone and Diabetes

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Faraj, M., Napoli, N. The Impact of Diet on Bone and Fracture Risk in Diabetes. Curr Osteoporos Rep 20, 26–42 (2022). https://doi.org/10.1007/s11914-022-00725-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11914-022-00725-y

Keywords

Search

Navigation