The effect of meals on bone turnover - a systematic review with focus on diabetic bone disease

References

• Khosla S, Riggs BL. Pathophysiology of age-related bone loss and osteoporosis. Endocrinol Metab Clin North Am. 2005;34(4):1015–1030.
   PubMed Web of Science ®Google Scholar
• IOF. IOF Epidemiology. 2015( 02/11).
   Google Scholar
• Starup-Linde J, Frost M, Vestergaard P, et al. Epidemiology of fractures in diabetes. Calcif Tissue Int. 2017;100(2):109-121.
   Web of Science ®Google Scholar
• Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int. 2007;18(4):427–444.
   PubMed Web of Science ®Google Scholar
• Starup-Linde J, Hygum K, Harslof T, et al. Indications of increased vertebral fracture risk in patients with type 2 diabetes. J Bone Miner Res. 2018;33(1):182.
   PubMed Web of Science ®Google Scholar
• Weber DR, Haynes K, Leonard MB, et al. Type 1 diabetes is associated with an increased risk of fracture across the life span: a population-based cohort study using the health improvement network (THIN). Diabetes Care. 2015;38:1913–1920.
   PubMed Web of Science ®Google Scholar
• Leslie WD, Morin SN, Lix LM, et al. Does diabetes modify the effect of FRAX risk factors for predicting major osteoporotic and hip fracture? Osteoporos Int. 2014;25(12):2817–2824.
   PubMed Web of Science ®Google Scholar
• Gonnelli S, Caffarelli C, Nuti R. Obesity and fracture risk. Clin Cases Miner Bone Metab. 2014;11(1):9–14.
   PubMedGoogle Scholar
• Yang L, Lv X, Wei D, et al. Metabolic syndrome and the risk of bone fractures: a Meta-analysis of prospective cohort studies. Bone. 2016;84:52–56.
   PubMed Web of Science ®Google Scholar
• Esposito K, Chiodini P, Capuano A, et al. Fracture risk and bone mineral density in metabolic syndrome: a meta-analysis. J Clin Endocrinol Metab. 2013;98(8):3306–3314.
   PubMed Web of Science ®Google Scholar
• Migliaccio S, Greco EA, Fornari R, et al. Skeletal alterations in women affected by obesity. Aging Clin Exp Res. 2013;25(Suppl 1):S35–7.
   PubMedGoogle Scholar
• Greco EA, Lenzi A, Migliaccio S. The obesity of bone. Ther Adv Endocrinol Metab. 2015;6(6):273–286.
   PubMed Web of Science ®Google Scholar
• Sogaard AJ, Holvik K, Omsland TK, et al. Abdominal obesity increases the risk of hip fracture. A population-based study of 43,000 women and men aged 60–79 years followed for 8 years. Cohort of Norway. J Intern Med. 2015;277(3):306–317.
   PubMed Web of Science ®Google Scholar
• Vestergaard P, Mosekilde L, Langdahl B. Fracture prevention in postmenopausal women. BMJ Clin Evid. 2011;1109.
   Google Scholar
• Hygum K, Langdahl BL, Starup-Linde J. Disentangling the association between diabetes and bone disease. Lancet Diabetes Endocrinol. 2017;5(10):769.
   PubMed Web of Science ®Google Scholar
• Starup-Linde J, Eriksen SA, Lykkeboe S, et al. Biochemical markers of bone turnover in diabetes patients - A meta-analysis, and a methodological study on the effects of glucose on bone markers. Osteoporosis Int. 2014;25(6):1697–1708.
   PubMed Web of Science ®Google Scholar
• Hernandez JL, Olmos JM, Pariente E, et al. Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause. 2010;17(5):955–961.
   PubMed Web of Science ®Google Scholar
• Rubin MR, Patsch JM. Assessment of bone turnover and bone quality in type 2 diabetic bone disease: current concepts and future directions. Bone Res. 2016;4:16001.
   PubMed Web of Science ®Google Scholar
• Clowes JA, Allen HC, Prentis DM, et al. Octreotide abolishes the acute decrease in bone turnover in response to oral glucose. J Clin Endocrinol Metab. 2003;88(10):4867–4873.
   PubMed Web of Science ®Google Scholar
• Lopes LS, Schwartz RP, Ferraz-de-Souza B, et al. The role of enteric hormone GLP-2 in the response of bone markers to a mixed meal in postmenopausal women with type 2 diabetes mellitus. Diabetol Metab Syndr. 2015;7:13–015–0006–7. eCollection 2015.
   PubMed Web of Science ®Google Scholar
• Yannakoulia M. Eating behavior among type 2 diabetic patients: a poorly recognized aspect in a poorly controlled disease. Rev Diabet Stud. 2006;3(1):11–16.
   PubMedGoogle Scholar
• Jannasch F, Kroger J, Schulze MB, et al. Type 2 diabetes: a systematic literature review and meta-analysis of prospective studies. J Nutr. 2017;147(6):1174–1182.
   PubMed Web of Science ®Google Scholar
• Starup-Linde J, Gregersen S, Frost M, et al. Use of glucose-lowering drugs and risk of fracture in patients with type 2 diabetes. Bone. 2017;95:136–142.
   PubMed Web of Science ®Google Scholar
• Bazelier MT, de Vries F, Vestergaard P, et al. Risk of fracture with thiazolidinediones: an individual patient data meta-analysis. Front Endocrinol (Lausanne). 2013;4:11.
   PubMedGoogle Scholar
• Starup-Linde J GS. Bone and Diabetes. In: Bonora EDR, editor. Diabetes complications, comorbidities and related disorders. endocrinology. Cham: Springer; 2018.
   Google Scholar
• Driessen JH, van Onzenoort HA, Starup-Linde J, et al. Use of glucagon-like-peptide 1 receptor agonists and risk of fracture as compared to use of other anti-hyperglycemic drugs. Calcif Tissue Int. 2015;97(5):506–515.
   Web of Science ®Google Scholar
• Driessen JH, van Onzenoort HA, Starup-Linde J, et al. Use of dipeptidyl peptidase 4 inhibitors and fracture risk compared to use of other anti-hyperglycemic drugs. Pharmacoepidemiol Drug Saf. 2015;24(10):1017–1025.
   PubMed Web of Science ®Google Scholar
• Mabilleau G, Mieczkowska A, Chappard D. Use of glucagon-like peptide-1 receptor agonists and bone fractures: a meta-analysis of randomized clinical trials. J Diabetes. 2014;6(3):260–266.
   PubMed Web of Science ®Google Scholar
• Tang HL, Li DD, Zhang JJ, et al. Lack of evidence for a harmful effect of sodium-glucose co-transporter 2 (SGLT2) inhibitors on fracture risk among type 2 diabetes patients: a network and cumulative meta-analysis of randomized controlled trials. Diabetes Obes Metab. 2016;18(12):1199–1206.
   PubMed Web of Science ®Google Scholar
• Keegan TH, Schwartz AV, Bauer DC, et al. fracture intervention trial. Effect of alendronate on bone mineral density and biochemical markers of bone turnover in type 2 diabetic women: the fracture intervention trial. Diabetes Care. 2004;27(7):1547–1553.
   PubMed Web of Science ®Google Scholar
• Vestergaard P, Rejnmark L, Mosekilde L. Are antiresorptive drugs effective against fractures in patients with diabetes? Calcif Tissue Int. 2011;88(3):209–214.
   PubMed Web of Science ®Google Scholar
• Ferrari S. Sequential/combined therapies in osteoporosis. Osteoporosis Int. 2015;26(1):S65.
   PubMedGoogle Scholar
• Schwartz AV, Pavo I, Alam J, et al. Teriparatide in patients with osteoporosis and type 2 diabetes. Bone. 2016;91:152–158.
   Google Scholar
• Krakauer JC, McKenna MJ, Buderer NF, et al. Bone loss and bone turnover in diabetes. Diabetes. 1995;44(7):775–782.
   PubMed Web of Science ®Google Scholar
• Manavalan JS, Cremers S, Dempster DW, et al. Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2012;97(9):3240–3250.
   PubMed Web of Science ®Google Scholar
• Hygum K, Starup-Linde J, Harslof T, et al. MECHANISMS IN ENDOCRINOLOGY: diabetes mellitus, a state of low bone turnover - a systematic review and meta-analysis. Eur J Endocrinol. 2017;176(3):R137–R157.
   PubMed Web of Science ®Google Scholar
• Farr JN, Drake MT, Amin S, et al. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014;29(4):787–795.
   PubMed Web of Science ®Google Scholar
• Nilsson AG, Sundh D, Johansson L, et al. Type 2 diabetes mellitus is associated with better bone microarchitecture but lower bone material strength and poorer physical function in elderly women: a population-based study. J Bone Miner Res. 2017;32(5):1062–1071.
   PubMed Web of Science ®Google Scholar
• Furst JR, Bandeira LC, Fan WW, et al. Advanced glycation endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab. 2016;101(6):2502–2510.
   PubMed Web of Science ®Google Scholar
• Rubin MR. Skeletal fragility in diabetes. Ann N Y Acad Sci. 2017;1402(1):18–30.
   PubMed Web of Science ®Google Scholar
• Shanbhogue VV, Hansen S, Hermann P, et al. Diabetic microvascular disease and bone structure in patients with type 2 diabetes mellitus. Diabetes. 2015;64:A174.
   Google Scholar
• Patsch JM, Burghardt AJ, Yap SP, et al. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res. 2013;28(2):313–324.
   PubMed Web of Science ®Google Scholar
• Heilmeier U, Cheng K, Pasco C, et al. Cortical bone laminar analysis reveals increased midcortical and periosteal porosity in type 2 diabetic postmenopausal women with history of fragility fractures compared to fracture-free diabetics. Osteoporos Int. 2016;27:2791–2802.
   PubMed Web of Science ®Google Scholar
• Samelson EJ, Demissie S, Cupples LA, et al. Diabetes and deficits in cortical bone density, microarchitecture, and bone size: framingham HR-pQCT study. J Bone Miner Res. 2018;33(1):54–62.
   PubMed Web of Science ®Google Scholar
• Saito M, Marumo K. Bone quality in diabetes. Front Endocrinol (Lausanne). 2013;4:72.
   PubMedGoogle Scholar
• Karim L, Moulton J, Van Vliet M, et al. Bone microarchitecture, biomechanical properties, and advanced glycation end-products in the proximal femur of adults with type 2 diabetes. Bone. 2018;114:32–39.
   PubMed Web of Science ®Google Scholar
• Yang X, Mostafa AJ, Appleford M, et al. Bone formation is affected by matrix advanced glycation end products (AGEs) in vivo. Calcif Tissue Int. 2016;99:373–383.
   PubMed Web of Science ®Google Scholar
• Conway BN, Long DM, Figaro MK, et al. Glycemic control and fracture risk in elderly patients with diabetes. Diabetes Res Clin Pract. 2016;115:47–53.
   PubMed Web of Science ®Google Scholar
• Li CI, Liu CS, Lin WY, et al. Glycated hemoglobin level and risk of hip fracture in older people with type 2 diabetes: a competing risk analysis of taiwan diabetes cohort study. J Bone Miner Res. 2015;30:1338–1346.
   PubMed Web of Science ®Google Scholar
• Oei L, Zillikens MC, Dehghan A, et al. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam Study. Diabetes Care. 2013;36(6):1619–1628.
   PubMed Web of Science ®Google Scholar
• Schwartz AV, Margolis KL, Sellmeyer DE, et al. Intensive glycemic control is not associated with fractures or falls in the ACCORD randomized trial. Diabetes Care. 2012;35(7):1525–1531.
   PubMed Web of Science ®Google Scholar
• Imai Y, Youn MY, Inoue K, et al. Nuclear receptors in bone physiology and diseases. Physiol Rev. 2013;93(2):481–523.
   PubMed Web of Science ®Google Scholar
• Neve A, Corrado A, Cantatore FP. Osteoblast physiology in normal and pathological conditions. Cell Tissue Res. 2011;343(2):289–302.
   PubMed Web of Science ®Google Scholar
• Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature. 2003;423(6937):337–342.
   PubMed Web of Science ®Google Scholar
• Pierce AM, Lindskog S, Hammarstrom L. Osteoclasts: structure and function. Electron Microsc Rev. 1991;4(1):1–45.
   PubMedGoogle Scholar
• Manolagas SC, Almeida M. Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol. 2007;21(11):2605–2614.
   PubMed Web of Science ®Google Scholar
• Hall JE, Guyton AC. Guyton and Hall textbook of medical physiology. 12th ed. Philadelphia: Saunders/Elsevier; 2011.
   Google Scholar
• Starup-Linde J, Vestergaard P. Biochemical bone turnover markers in diabetes mellitus - a systematic review. Bone. 2016;82:69–78.
   PubMed Web of Science ®Google Scholar
• Vasikaran S, Cooper C, Eastell R, et al. International osteoporosis foundation and international federation of clinical chemistry and laboratory medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med. 2011;49(8):1271–1274.
   PubMed Web of Science ®Google Scholar
• Yao CK, Gibson PR, Shepherd SJ. Design of clinical trials evaluating dietary interventions in patients with functional gastrointestinal disorders. Am J Gastroenterol. 2013;108(5):748–758.
   PubMed Web of Science ®Google Scholar
• Whiting SJ, Kohrt WM, Warren MP, Kraenzlin MI, Bonjour JP. Food fortification for bone health in adulthood: a scoping review. Eur J Clin Nutr. 2016;70(10):1099–1105.
   PubMed Web of Science ®Google Scholar
• Beasley JM, LaCroix AZ, Larson JC, et al. Biomarker-calibrated protein intake and bone health in the Women’s Health Initiative clinical trials and observational study. Am J Clin Nutr. 2014;99(4):934–940.
   PubMed Web of Science ®Google Scholar
• Sahni S, Cupples LA, McLean RR, et al. Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham offspring cohort. J Bone Miner Res. 2010;25(12):2770–2776.
   PubMed Web of Science ®Google Scholar
• Mangano KM, Sahni S, Kerstetter JE. Dietary protein is beneficial to bone health under conditions of adequate calcium intake: an update on clinical research. Curr Opin Clin Nutr Metab Care. 2014;17(1):69–74.
   PubMed Web of Science ®Google Scholar
• Henriksen DB, Alexandersen P, Bjarnason NH, et al. Role of gastrointestinal hormones in postprandial reduction of bone resorption. J Bone Miner Res. 2003;18(12):2180–2189.
   PubMed Web of Science ®Google Scholar
• Bonjour JP, Brandolini-Bunlon M, Boirie Y, et al. Inhibition of bone turnover by milk intake in postmenopausal women. Br J Nutr. 2008;100(4):866–874.
   PubMed Web of Science ®Google Scholar
• Kruger MC, Ha PC, Todd JM, et al. 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. 2012;66(7):856–861.
   PubMed Web of Science ®Google Scholar
• Aoe S, Toba Y, Yamamura J, et al. Controlled trial of the effects of milk basic protein (MBP) supplementation on bone metabolism in healthy adult women. Biosci Biotechnol Biochem. 2001;65(4):913–918.
   PubMed Web of Science ®Google Scholar
• Kerstetter JE, Bihuniak JD, Brindisi J, et al. The effect of a whey protein supplement on bone mass in older caucasian adults. J Clin Endocrinol Metab. 2015;100(6):2214–2222.
   PubMed Web of Science ®Google Scholar
• Bihuniak JD, Insogna KL. The effects of dietary protein and amino acids on skeletal metabolism. Mol Cell Endocrinol. 2015;410:78–86.
   PubMed Web of Science ®Google Scholar
• Slevin MM, Allsopp PJ, Magee PJ, et al. Supplementation with calcium and short-chain fructo-oligosaccharides affects markers of bone turnover but not bone mineral density in postmenopausal women. J Nutr. 2014;144(3):297–304.
   PubMed Web of Science ®Google Scholar
• Bjarnason NH, Henriksen EE, Alexandersen P, et al. Mechanism of circadian variation in bone resorption. Bone. 2002;30(1):307–313.
   PubMed Web of Science ®Google Scholar
• Elnenaei MO, Musto R, Alaghband-Zadeh J, et al. Postprandial bone turnover is independent of calories above 250 kcal. Ann Clin Biochem. 2010;47(Pt 4):318–320.
   PubMedGoogle Scholar
• Walsh JS, Henriksen DB. Feeding and bone. Arch Biochem Biophys. 2010;503(1):11–19.
   PubMed Web of Science ®Google Scholar
• Anson RM, Guo Z, de Cabo R, et al. Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci U S A. 2003;100(10):6216–6220.
   PubMed Web of Science ®Google Scholar
• Kahleova H, Belinova L, Malinska H, et al. Eating two larger meals a day (breakfast and lunch) is more effective than six smaller meals in a reduced-energy regimen for patients with type 2 diabetes: a randomised crossover study. Diabetologia. 2014;57(8):1552–1560.
   PubMed Web of Science ®Google Scholar
• Duval K, Strychar I, Cyr MJ, et al. Physical activity is a confounding factor of the relation between eating frequency and body composition. Am J Clin Nutr. 2008;88(5):1200–1205.
   PubMed Web of Science ®Google Scholar
• Yannakoulia M, Melistas L, Solomou E, et al. Association of eating frequency with body fatness in pre- and postmenopausal women. Obesity (Silver Spring). 2007;15(1):100–106.
   PubMed Web of Science ®Google Scholar
• Ewang-Emukowhate M, Alaghband-Zadeh J, Vincent RP, et al. An association between post-meal bile acid response and bone resorption in normal subjects. Ann Clin Biochem. 2013;50(Pt 6):558–563.
   PubMed Web of Science ®Google Scholar
• Clowes JA, Robinson RT, Heller SR, et al. Acute changes of bone turnover and PTH induced by insulin and glucose: euglycemic and hypoglycemic hyperinsulinemic clamp studies. J Clin Endocrinol Metab. 2002;87(7):3324–3329.
   PubMed Web of Science ®Google Scholar
• Madison D. Osteoporosis in Primary Hyperparathyroidism: considerations for Diagnosis and Treatment. In: Stack J, Bodenner D, editors. Medical and Surgical Treatment of Parathyroid Diseases: an Evidence-Based Approach. Springer International Publishing; Cham. 2017. p. 343–358.
   Google Scholar
• Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.
   PubMed Web of Science ®Google Scholar
• Mullins NM, Sinning WE. Effects of resistance training and protein supplementation on bone turnover in young adult women. Nutr Metab (Lond). 2005;2:19–7075–2–19.
   PubMedGoogle Scholar
• Svendsen OL, Hassager C, Christiansen C. Six months’ follow-up on exercise added to a short-term diet in overweight postmenopausal women–effects on body composition, resting metabolic rate, cardiovascular risk factors and bone. Int J Obes Relat Metab Disord. 1994;18(10):692–698.
   PubMed Web of Science ®Google Scholar
• Holst JJ, Hartmann B, Gottschalck IB, et al. Bone resorption is decreased postprandially by intestinal factors and glucagon-like peptide-2 is a possible candidate. Scand J Gastroenterol. 2007;42(7):814–820.
   PubMed Web of Science ®Google Scholar
• Rogers TS, Demmer E, Rivera N, et al. The role of a dairy fraction rich in milk fat globule membrane in the suppression of postprandial inflammatory markers and bone turnover in obese and overweight adults: an exploratory study. Nutr Metab (Lond). 2017;14: 36–017–0189-z. eCollection 2017.
   PubMed Web of Science ®Google Scholar
• Maagensen H, Junker AE, Jorgensen NR, et al. Bone turnover markers in patients with nonalcoholic fatty liver disease and/or type 2 diabetes during oral glucose and isoglycemic intravenous glucose. J Clin Endocrinol Metab. 2018;103(5):2042–2049.
   PubMed Web of Science ®Google Scholar
• Karatzoglou I, Yavropoulou MP, Pikilidou M, et al. Postprandial response of bone turnover markers in patients with Crohn’s disease. World J Gastroenterol. 2014;20(28):9534–9540.
   PubMed Web of Science ®Google Scholar
• Paldanius PM, Ivaska KK, Hovi P, et al. The effect of oral glucose tolerance test on serum osteocalcin and bone turnover markers in young adults. Calcif Tissue Int. 2012;90(2):90–95.
   PubMed Web of Science ®Google Scholar
• Viljakainen H, Ivaska KK, Paldanius P, et al. Suppressed bone turnover in obesity: a link to energy metabolism? A case-control study. J Clin Endocrinol Metab. 2014;99(6):2155–2163.
   PubMed Web of Science ®Google Scholar
• Westberg-Rasmussen S, Starup-Linde J, Hermansen K, et al. Differential impact of glucose administered intravenously or orally on bone turnover markers in healthy male subjects. Bone. 2017;97:261–266.
   PubMed Web of Science ®Google Scholar
• Yavropoulou MP, Tomos K, Tsekmekidou X, et al. Response of biochemical markers of bone turnover to oral glucose load in diseases that affect bone metabolism. Eur J Endocrinol. 2011;164(6):1035–1041.
   PubMed Web of Science ®Google Scholar
• Chailurkit LO, Chanprasertyothin S, Rajatanavin R, et al. Reduced attenuation of bone resorption after oral glucose in type 2 diabetes. Clin Endocrinol (Oxf). 2008;68(6):858–862.
   PubMed Web of Science ®Google Scholar
• Dawson-Hughes B, Harris SS, Rasmussen H, et al. Effect of dietary protein supplements on calcium excretion in healthy older men and women. J Clin Endocrinol Metab. 2004;89(3):1169–1173.
   PubMed Web of Science ®Google Scholar
• Heer M, Baecker N, Frings-Meuthen P, et al. Effects of high-protein intake on bone turnover in long-term bed rest in women. Appl Physiol Nutr Metab. 2017;42(5):537–546.
   PubMed Web of Science ®Google Scholar
• Kerstetter JE, Mitnick ME, Gundberg CM, et al. Changes in bone turnover in young women consuming different levels of dietary protein. J Clin Endocrinol Metab. 1999;84(3):1052–1055.
   PubMed Web of Science ®Google Scholar
• Kerstetter JE, O’Brien KO, Caseria DM, et al. The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab. 2005;90(1):26–31.
   PubMed Web of Science ®Google Scholar
• Nowson CA, Patchett A, Wattanapenpaiboon N. The effects of a low-sodium base-producing diet including red meat compared with a high-carbohydrate, low-fat diet on bone turnover markers in women aged 45–75 years. Br J Nutr. 2009;102(8):1161–1170.
   PubMed Web of Science ®Google Scholar
• Zittermann A, Scheld K, Danz A, et al. Wheat bran supplementation does not affect biochemical markers of bone turnover in young adult women with recommended calcium intake. Br J Nutr. 1999;82(6):431–435.
   PubMed Web of Science ®Google Scholar
• Hansen TH, Madsen MTB, Jorgensen NR, et al. Bone turnover, calcium homeostasis, and vitamin D status in Danish vegans. Eur J Clin Nutr. 2018.
   Web of Science ®Google Scholar
• Arjmandi BH, Khalil DA, Lucas EA, et al. Dried plums improve indices of bone formation in postmenopausal women. J Womens Health Gend Based Med. 2002;11(1):61–68.
   PubMedGoogle Scholar
• Strollo R, Soare A, Manon Khazrai Y, et al. Increased sclerostin and bone turnover after diet-induced weight loss in type 2 diabetes: a post hoc analysis of the MADIAB trial. Endocrine. 2017;56(3):667–674.
   PubMed Web of Science ®Google Scholar
• Carter JD, Vasey FB, Valeriano J. The effect of a low-carbohydrate diet on bone turnover. Osteoporos Int. 2006;17(9):1398–1403.
   PubMed Web of Science ®Google Scholar
• Bowen J, Noakes M, Clifton PM. A high dairy protein, high-calcium diet minimizes bone turnover in overweight adults during weight loss. J Nutr. 2004;134(3):568–573.
   PubMed Web of Science ®Google Scholar
• Brinkworth GD, Wycherley TP, Noakes M, et al. Long-term effects of a very-low-carbohydrate weight-loss diet and an isocaloric low-fat diet on bone health in obese adults. Nutrition. 2016;32(9):1033–1036.
   PubMed Web of Science ®Google Scholar
• Luscombe-Marsh ND, Noakes M, Wittert GA, et al. Carbohydrate-restricted diets high in either monounsaturated fat or protein are equally effective at promoting fat loss and improving blood lipids. Am J Clin Nutr. 2005;81(4):762–772.
   PubMed Web of Science ®Google Scholar
• Villareal DT, Fontana L, Das SK, et al. Effect of two-year caloric restriction on bone metabolism and bone mineral density in non-obese younger adults: a randomized clinical trial. J Bone Miner Res. 2016;31(1):40–51.
   PubMed Web of Science ®Google Scholar
• Noakes M, Keogh JB, Foster PR, et al. Effect of an energy-restricted, high-protein, low-fat diet relative to a conventional high-carbohydrate, low-fat diet on weight loss, body composition, nutritional status, and markers of cardiovascular health in obese women. Am J Clin Nutr. 2005;81(6):1298–1306.
   PubMed Web of Science ®Google Scholar
• Farnsworth E, Luscombe ND, Noakes M, et al. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. Am J Clin Nutr. 2003;78(1):31–39.
   PubMed Web of Science ®Google Scholar
• Haakonssen EC, Ross ML, Knight EJ, et al. The effects of a calcium-rich pre-exercise meal on biomarkers of calcium homeostasis in competitive female cyclists: a randomised crossover trial. PLoS One. 2015;10(5):e0123302.
   PubMed Web of Science ®Google Scholar
• Townsend R, Elliott-Sale KJ, Currell K, et al. The effect of postexercise carbohydrate and protein ingestion on bone metabolism. Med Sci Sports Exerc. 2017;49(6):1209–1218.
   PubMed Web of Science ®Google Scholar
• Sale C, Varley I, Jones TW, et al. Effect of carbohydrate feeding on the bone metabolic response to running. J Appl Physiol (1985). 2015;119(7):824–830.
   PubMed Web of Science ®Google Scholar
• Scott JP, Sale C, Greeves JP, et al. Effect of fasting versus feeding on the bone metabolic response to running. Bone. 2012;51(6):990–999.
   PubMed Web of Science ®Google Scholar
• Ballard TL, Clapper JA, Specker BL, et al. Effect of protein supplementation during a 6-mo strength and conditioning program on insulin-like growth factor I and markers of bone turnover in young adults. Am J Clin Nutr. 2005;81(6):1442–1448.
   PubMed Web of Science ®Google Scholar
• Josse AR, Atkinson SA, Tarnopolsky MA, et al. Diets higher in dairy foods and dietary protein support bone health during diet- and exercise-induced weight loss in overweight and obese premenopausal women. J Clin Endocrinol Metab. 2012;97(1):251–260.
   PubMed Web of Science ®Google Scholar
• Refaey ME, Zhong Q, Ding KH et al. Impact of dietary aromatic amino acids on osteoclastic activity. Calcif Tissue Int. 2014;95(2):174–182.
   PubMed Web of Science ®Google Scholar
• Seino Y, Fukushima M, Yabe DGIP. GLP-1, the two incretin hormones: similarities and differences. J Diabetes Investig. 2010;1(1–2):8–23.
   PubMed Web of Science ®Google Scholar
• Nauck MA, Heimesaat MM, Orskov C, et al. Preserved incretin activity of glucagon-like peptide 1 [7–36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest. 1993;91(1):301–307.
   PubMed Web of Science ®Google Scholar
• Vilsboll T, Krarup T, Madsbad S, et al. Defective amplification of the late phase insulin response to glucose by GIP in obese Type II diabetic patients. Diabetologia. 2002;45(8):1111–1119.
   PubMed Web of Science ®Google Scholar
• Nauck MA, Niedereichholz U, Ettler R, et al. Glucagon-like peptide 1 inhibition of gastric emptying outweighs its insulinotropic effects in healthy humans. Am J Physiol. 1997;273(5 Pt 1):E981–8.
   PubMed Web of Science ®Google Scholar
• Pacheco-Pantoja EL, Ranganath LR, Gallagher JA, et al. Receptors and effects of gut hormones in three osteoblastic cell lines. BMC Physiol. 2011;11:12–6793–11–12.
   PubMedGoogle Scholar
• Driessen JH, de Vries F, van Onzenoort H, et al. The use of incretins and fractures - a meta-analysis on population-based real life data. Br J Clin Pharmacol. 2017;83(4):923–926.
   PubMed Web of Science ®Google Scholar
• Bollag RJ, Zhong Q, Phillips P, et al. Osteoblast-derived cells express functional glucose-dependent insulinotropic peptide receptors. Endocrinology. 2000;141(3):1228–1235.
   PubMed Web of Science ®Google Scholar
• Zhong Q, Itokawa T, Sridhar S, et al. Effects of glucose-dependent insulinotropic peptide on osteoclast function. Am J Physiol Endocrinol Metab. 2007;292(2):E543–8.
   PubMed Web of Science ®Google Scholar
• Nissen A, Christensen M, Knop FK, et al. Glucose-dependent insulinotropic polypeptide inhibits bone resorption in humans. J Clin Endocrinol Metab. 2014;99(11):E2325–9.
   PubMed Web of Science ®Google Scholar
• Christensen MB, Lund A, Calanna S, et al. Glucose-Dependent insulinotropic polypeptide (GIP) inhibits bone resorption independently of insulin and glycemia. J Clin Endocrinol Metab. 2018;103(1):288–294.
   PubMed Web of Science ®Google Scholar
• Henriksen DB, Alexandersen P, Hartmann B, et al. Four-month treatment with GLP-2 significantly increases hip BMD: a randomized, placebo-controlled, dose-ranging study in postmenopausal women with low BMD. Bone. 2009;45(5):833–842.
   PubMed Web of Science ®Google Scholar
• Maccarinelli G, Sibilia V, Torsello A, et al. Ghrelin regulates proliferation and differentiation of osteoblastic cells. J Endocrinol. 2005;184(1):249–256.
   PubMed Web of Science ®Google Scholar
• Huda MS, Durham BH, Wong SP, et al. Lack of an acute effect of ghrelin on markers of bone turnover in healthy controls and post-gastrectomy subjects. Bone. 2007;41(3):406–413.
   PubMed Web of Science ®Google Scholar
• Holst JJ, Knop FK, Vilsboll T, et al. Loss of incretin effect is a specific, important, and early characteristic of type 2 diabetes. Diabetes Care. 2011;34(Suppl 2):S251–7.
   PubMed Web of Science ®Google Scholar
• Diez-Perez A, Naylor KE, Abrahamsen B, et al. International osteoporosis foundation and european calcified tissue society working group. recommendations for the screening of adherence to oral bisphosphonates. Osteoporos Int. 2017;28(3):767–774.
   PubMed Web of Science ®Google Scholar
• Langdahl BL, Teglbjaerg CS, Ho PR, et al. A 24-month study evaluating the efficacy and safety of denosumab for the treatment of men with low bone mineral density: results from the ADAMO trial. J Clin Endocrinol Metab. 2015;100(4):1335–1342.
   PubMed Web of Science ®Google Scholar
• Gu HF, Gu LJ, Wu Y, et al. Efficacy and safety of denosumab in postmenopausal women with osteoporosis: a meta-analysis. Medicine (Baltimore). 2015;94(44):e1674.
   PubMed Web of Science ®Google Scholar
• Torricelli P, Fini M, Giavaresi G, et al. Human osteopenic bone-derived osteoblasts: essential amino acids treatment effects. Artif Cells Blood Substit Immobil Biotechnol. 2003;31(1):35–46.
   PubMed Web of Science ®Google Scholar
• Hampson G, Martin FC, Moffat K, et al. Effects of dietary improvement on bone metabolism in elderly underweight women with osteoporosis: a randomised controlled trial. Osteoporos Int. 2003;14(9):750–756.
   PubMed Web of Science ®Google Scholar
• Wallace TC, Frankenfeld CL. Dietary protein intake above the current RDA and bone health: a systematic review and meta-analysis. J Am Coll Nutr. 2017;36(6):481–496.
   PubMed Web of Science ®Google Scholar
• Soeliman FA, Azadbakht L. Weight loss maintenance: a review on dietary related strategies. J Res Med Sci. 2014;19(3):268–275.
   PubMed Web of Science ®Google Scholar
• Iepsen EW, Lundgren JR, Hartmann B, et al. GLP-1 Receptor agonist treatment increases bone formation and prevents bone loss in weight-reduced obese women. J Clin Endocrinol Metab. 2015;100(8):2909–2917.
   PubMed Web of Science ®Google Scholar
• Thomas DM, Hards DK, Rogers SD, et al. Insulin receptor expression in bone. J Bone Miner Res. 1996;11(9):1312–1320.
   PubMed Web of Science ®Google Scholar
• Thomas DM, Udagawa N, Hards DK, et al. Insulin receptor expression in primary and cultured osteoclast-like cells. Bone. 1998;23(3):181–186.
   PubMed Web of Science ®Google Scholar
• Laurent MR, Cook MJ, Gielen E, et al. Lower bone turnover and relative bone deficits in men with metabolic syndrome: a matter of insulin sensitivity? The European male ageing study. Osteoporos Int. 2016;27(11):3227–3237.
   PubMed Web of Science ®Google Scholar
• Basu R, Peterson J, Rizza R, et al. Effects of physiological variations in circulating insulin levels on bone turnover in humans. J Clin Endocrinol Metab. 2011;96(5):1450–1455.
   PubMed Web of Science ®Google Scholar
• Samocha-Bonet D, Chisholm DJ, Tonks K, et al. Insulin-Sensitive obesity in humans - a ‘favorable fat’ phenotype? Trends Endocrinol Metab. 2012;23(3):116–124.
   PubMed Web of Science ®Google Scholar
• Kalimeri M, Leek F, Wang NX, et al. Association of insulin resistance with bone strength and bone turnover in menopausal chinese-singaporean women without diabetes. Int J Environ Res Public Health. 2018;15(6). DOI:10.3390/ijerph15061188
   PubMedGoogle Scholar
• Yang J, Hong N, Shim JS, et al. Association of insulin resistance with lower bone volume and strength index of the proximal femur in nondiabetic postmenopausal women. J Bone Metab. 2018;25(2):123–132.
   PubMedGoogle Scholar
• Wei J, Ferron M, Clarke CJ, et al. Bone-specific insulin resistance disrupts whole-body glucose homeostasis via decreased osteocalcin activation. J Clin Invest. 2014;124(4):1–13.
   PubMed Web of Science ®Google Scholar
• Tonks KT, White CP, Center JR, Samocha-Bonet D, Greenfield JR. Bone turnover is suppressed in insulin resistance, independent of adiposity. J Clin Endocrinol Metab. 2017;102(4):1112–1121.
   PubMed Web of Science ®Google Scholar