A Critical Analysis of Relationship and Management of Sweet Bones in Insulin-Dependent Diabetes Mellitus
DOI:
https://doi.org/10.37285/ijpsn.2022.15.6.7Abstract
Due to the increased risk of encountering several bone deformities as a result of insulin-dependent diabetes mellitus (Type 1 diabetes), it has become obligatory to study this relationship among them so that such conditions of skeletal complications might be detected and treated at a much earlier stage. Type 1 diabetic patients have ameliorated bone mineral density and bone turnover, thus increasing the risk of individuals suffering from fractures. The mechanism behind bone deformities is multifactorial and not completely understood yet. The major factors responsible are less amount of osteoclasts and decreased activity of osteoblasts due to deviated insulin signaling pathway. Other eminent factors involved are oxidative stress, elevated levels of calcium and magnesium in urine, and the build-up of advanced glycation end products. These eminent factors lead to the formation of sweet bones. Sweet bone is a name given collectively to the altered structure, strength, and metabolism of bones. This study will help the researchers to understand and maintain good lifestyle practices. Educating the patients about avoiding other diabetic complications, regular consumption of calcium and vitamin D, along with maintaining proper serum glucose levels are the major steps to be taken primarily in treating bone loss due to type 1 diabetes.
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Bone mineral density, Fractures, Insulin-dependent diabetes mellitus, Skeletal complications, Sweet bones, Type 1 diabetes
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Abdalrahaman N, McComb C, Foster JE, McLean J, Lindsay RS, McClure J, McMillan M, Drummond R, Gordon D, McKay GA, Shaikh MG, Perry CG, Ahmed SF. Deficits in trabecular bone microarchitecture in young women with type 1 diabetes mellitus. Journal of bone and mineral research. 2015 Aug 1;30(8):1386–1393.
Achemlal L, Tellal S, Rkiouak F, Nouijai A, Bezza A, Derouiche el M, Ghafir D, El Maghraoui A. Bone metabolism in male patients with type 2 diabetes. Clinical rheumatology. 2005 Mar 4;24(5): 493-496.
Ahmed LA, Joakimsen RM, Berntsen GK, Fønnebø V, Schirmer H. Diabetes mellitus and the risk of non-vertebral fractures: the Tromsø study. Osteoporosis international. 2006 Nov 10;17(4): 495-500.
Alexopoulou O, Jamart J, Devogelaer JP, Brichard S, de Nayer P, Buysschaert M. Bone density and markers of bone remodeling in type 1 male diabetic patients. Diabetes & metabolism. 2006 Apr 11;32(5): 453-458.
American Diabetes Association. Standards of medical care in diabetes—2009. Diabetes care. 2009 Jan;32(Suppl 1):S13.
Atkinson MA, Eisenbarth GS, Michels AW. Type 1 diabetes. The lancet. 2014 Jan 4;383(9911): 69-82.
Blake GM, Fogelman I. The role of DXA bone density scans in the diagnosis and treatment of osteoporosis. Postgraduate medical journal. 2007 Mar 30;83(982):509-517.
Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL, Johnson KC, Margolis KL. Risk of fracture in women with type 2 diabetes: the women’s health initiative observational study. The journal of clinical endocrinology and metabolism. 2006 Sep 1;91(9):3404–3410.
Bonewald LF. The amazing osteocyte. Journal of bone and mineral research. 2011 Feb;26(2):229–238.
Bouillon R. Diabetic bone disease. Calcified tissue international. 1991 May;49(3):155-160.
Bouillon R, Bex M, Van Herck E, Laureys J, Dooms L, Lesaffre E, Ravussin E. Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. The journal of clinical endocrinology and metabolism. 1995 Apr 1;80(4):1194-1202.
Boulton AJ, Gries FA, Jervell JA. Guidelines for the diagnosis and outpatient management of diabetic peripheral neuropathy. Diabetic medicine. 1998 Feb 4;15(6):508-514.
Botolin S, McCabe LR. Inhibition of PPARγ prevents type I diabetic bone marrow adiposity but not bone loss. Journal of cellular physiology. 2006 Dec;209(3):967-976.
Burch J, Rice S, Yang H, Neilson A, Stirk L, Francis R, Holloway P, Selby P, Craig D. Systematic review of the use of bone turnover markers for monitoring the response to osteoporosis treatment: the secondary prevention of fractures, and primary prevention of fractures in high-risk groups. Health technology assessment (Winchester, England). 2014 Feb 1;18(11):1-80.
Campos Pastor MM, Lopez-Ibarra PJ, Escobar-Jimenez F, Serrano Pardo MD, García-Cervigón AG. Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporosis international. 2000 May;11(5):455–459.
Carmo A, Cunha-Vaz JG, Carvalho AP, Lopes MC. L-arginine transport in retinas from streptozotocin diabetic rats: correlation with the level of IL-1 beta and NO synthase activity. Vision research. 1999 Nov 1;39(23):3817-3823.
Christodoulou S, Goula T, Ververidis A, Drosos G. Vitamin D and bone disease. Biomed research international. 2013 Jan 1;2013:396541.
Clark RG. Recombinant human insulin-like growth factor I (IGF-I): risks and benefits of normalizing blood IGF-I concentrations. Hormone research in pediatrics. 2004 Feb;62(Suppl 1):93-100.
Clausen P, Feldt-Rasmussen B, Jacobsen P, Rossing K, Parving HH, Nielsen PK, Feldt-Rasmussen U, Olgaard K. Microalbuminuria as an early indicator of osteopenia in male insulin-dependent diabetic patients. Diabetic medicine. 1997 Dec;14(12):1038-1043.
Clemens TL, Karsenty G. The osteoblast: an insulin target cell controlling glucose homeostasis. Journal of bone and mineral research. 2011 Apr;26(4):677-680.
Coe LM, Irwin R, Lippner D, McCabe LR. The bone marrow microenvironment contributes to type I diabetes induced osteoblast death. Journal of cellular physiology. 2011 Feb;226(2):477-483.
Compston J. Is fracture risk increased in patients with coeliac disease? Gut. 2003 Apr 1;52(4):459-460.
Crane JL, Zhao L, Frye JS, Xian L, Qiu T, Cao X. IGF-1 signaling is essential for differentiation of mesenchymal stem cells for peak bone mass. Bone Research. 2013 Dec;1(2):186–194.
Cunha JS, Ferreira VM, Maquigussa E, Naves MA, Boim MA. Effects of high glucose and high insulin concentrations on osteoblast function in vitro. Cell and tissue research. 2014 May 25;358(1):249-256.
Dallas SL, Prideaux M, Bonewald LF. The osteocyte: an endocrine cell … and more. Endocrine reviews. 2013 Oct 1;34(5):658-690.
Diabetes Control and Complications Trial Research Group, Nathan DM, Genuth S, Lachin J, Cleary P, Crofford O, Davis M, Rand L, Siebert C. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The New England journal of medicine.1993 Sep 30;329(14):977-986.
Danielson KK, Elliott ME, LeCaire T, Binkley N, Palta M. Poor glycemic control is associated with low BMD detected in premenopausal women with type 1 diabetes. Osteoporosis international. 2008 Oct 2;20(6):923–933.
Eller-Vainicher C, Zhukouskaya VV, Tolkachev YV, Koritko SS, Cairoli E, Grossi E, Beck-Peccoz P, Chiodini I, Shepelkevich AP. Low bone mineral density and its predictors in type 1 diabetic patients evaluated by the classic statistics and artificial neural network analysis. Diabetes care. 2011 Oct 1;34(10):2186–2191.
Fan Y, Wei F, Lang Y, Liu Y. Diabetes mellitus and risk of hip fractures: a meta-analysis. Osteoporosis international. 2016 Jan;27(1):219-228.
Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell. 2010 Jul 23;142(2):296-308.
Forst T, Pfutzner A, Kann P, Schehler B, Lobmann R, Schäfer H, Andreas J, Bockisch A, Beyer J. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabetic medicine. 1995 Oct;12(10):874–879.
Fowlkes JL, Bunn RC, Liu L, Wahl EC, Coleman HN, Cockrell GE, Perrien DS, Lumpkin CK Jr, Thrailkill KM. Runt-related transcription factor 2 (RUNX2) and RUNX2-related osteogenic genes are down-regulated throughout osteogenesis in type 1 diabetes mellitus. Endocrinology 2008 Apr 1;149(4):1697-1704.
Fraser JH, Helfrich MH, Wallace HM, Ralston SH. Hydrogen peroxide, but not superoxide, stimulates bone resorption in mouse calvariae. Bone 1996 Sep 1;19(3):223-226.
Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Brüning JC, Clemens TL. Insulin receptor signaling in osteoblasts regulates the postnatal bone acquisition and body composition. Cell. 2010 Jul 23;142(2):309-319.
Fuusager GB, Christesen HT, Milandt N, Schou AJ. Glycemic control and bone mineral density in children and adolescents with type 1 diabetes. Paediatric diabetes. 2019 Apr 24;20(5):629–636.
Gandhi A, Beam HA, O'Connor JP, Parsons JR, Lin SS. The effects of local insulin delivery on diabetic fracture healing. Bone. 2005 Oct 1;37(4):482-490.
Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circulation research. 2010 Oct 29;107(9):1058-1070.
Gil-Díaz MC, Raynor J, O'Brien KO, Schwartz GJ, Weber DR. Systematic review: associations of calcium intake, vitamin D intake, and physical activity with skeletal outcomes in people with Type 1 diabetes mellitus. Acta diabetologica. 2019 Oct;56(10):1091-1102.
Gopalakrishnan V, Vignesh RC, Arunakaran J, Aruldhas MM, Srinivasan N. Effects of glucose and its modulation by insulin and estradiol on BMSC differentiation into osteoblastic lineages. Biochemistry and cell biology. 2006 Feb 1;84(1):93-101.
Gordon CM, Leonard MB, Zemel BS. 2013 Pediatric position development conference: executive summary and reflections. Journal of clinical densitometry. 2014 Apr 1;17(2):219-224.
Gunczler P, Lanes R, Paoli M, Martinis R, Villaroel O, Weisinger JR. Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. Journal of paediatric endocrinology and metabolism. 2001 May 1;14(5):525–528.
Gundersen HJG. Peripheral blood flow and metabolic control in juvenile diabetes. Diabetologia. 1974 Jun;10(3):225–231.
Hage Hassan R, Bourron O, Hajduch E. Defect of insulin signal in peripheral tissues: important role of ceramide. World journal of diabetes. 2014 Jun 6;5(3):244.
Hamann C, Kirschner S, Günther KP, Hofbauer LC. Bone, sweet bone--osteoporotic fractures in diabetes mellitus. Nature reviews endocrinology. 2012 May;8(5):297-305.
Hamilton EJ, Rakic V, Davis WA, Chubb SA, Kamber N, Prince RL, Davis TM. Prevalence and predictors of osteopenia and osteoporosis in adults with Type 1 diabetes. Diabetic medicine. 2009 Jan;26(1):45–52.
Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Hartzell D, Baile CA. Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. Journal of bone and mineral research. 2005 Jun;20(6):994-1001.
Hanaki K, Becker DJ, Arslanian SA. Leptin before and after insulin therapy in children with new-onset type 1 diabetes. The journal of clinical endocrinology and metabolism. 1999 May 1;84(5):1524-1526.
He H, Liu R, Desta T, Leone C, Gerstenfeld LC, Graves DT. Diabetes causes decreased osteoclastogenesis, reduced bone formation, and enhanced apoptosis of osteoblastic cells in bacteria stimulated bone loss. Endocrinology. 2004 Jan 1;145(1):447-452.
Hofbauer LC, Brueck CC, Singh SK, Dobnig H. Osteoporosis in patients with diabetes mellitus. Journal of bone and mineral research. 2007 Sep;22(9):1317–1328.
Horcajada-Molteni MN, Chanteranne B, Lebecque P, Davicco MJ, Coxam V, Young A, Barlet JP. Amylin and bone metabolism in streptozotocin-induced diabetic rats. Journal of bone and mineral research. 2001 May;16(5):958-965.
Hothersall EJ, Livingstone SJ, Looker HC, Ahmed SF, Cleland S, Leese GP, Lindsay RS, McKnight J, Pearson D, Philip S, Wild SH, Colhoun HM. Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. Journal of bone and mineral research. 2014 May;29(5):1054-1060.
Hough FS, Pierroz DD, Cooper C, Ferrari SL. Mechanisms in endocrinology: Mechanisms and evaluation of bone fragility in type 1 diabetes mellitus. European journal of endocrinology. 2016 Apr 1;174(4):R127-138.
Hough S, Avioli LV, Bergfeld MA, Fallon MD, Slatopolsky E, Teitelbaum SL. Correction of abnormal bone and mineral metabolism in chronic streptozotocin-induced diabetes mellitus in the rat by insulin therapy. Endocrinology. 1981 Jun 1;108(6):2228-2234.
Hruska KA, Teitelbaum SL. Renal osteodystrophy. The New England journal of medicine. 1995 Jul 20;333(3):166-174.
Ishikawa K, Fukui T, Nagai T, Kuroda T, Hara N, Yamamoto T, Inagaki K, Hirano T. Type 1 diabetes patients have lower strength in femoral bone determined by quantitative computed tomography: a cross-sectional study. Journal of diabetes investigation. 2015 Nov;6(6):726–733.
Ivers RQ, Cumming RG, Mitchell P, Peduto AJ, Blue Mountains Eye Study. Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care. 2001 Jul 1;24(7):1198–1203.
Jackuliak P, Payer J. Osteoporosis, fractures, and diabetes. International journal of endocrinology. 2014 Jun 23;2014:820615.
Jehle PM, Jehle DR, Mohan S, Böhm BO. Serum levels of insulin-like growth factor system components and relationship to bone metabolism in Type 1 and Type 2 diabetes mellitus patients. Journal of endocrinology.1998 Nov 1;159(2):297-306.
Kaji H, Suzuki M, Yano S, Sugimoto T, Chihara K, Hattori S, Sekita K. Risk factors for hip fracture in hemodialysis patients. American journal of nephrology. 2002 Jul-Aug;22(4):325-331.
Kanazawa I. Osteocalcin is a hormone regulating glucose metabolism. World journal of diabetes. 2015 Dec 25;6(18):1345-1354.
Karagüzel G, Ozdem S, Boz A, Bircan I, Akçurin S. Leptin levels and body composition in children and adolescents with type 1 diabetes. Clinical biochemistry. 2006 Aug 1;39(8):788-793.
Kasahara T, Imai S, Kojima H, Katagi M, Kimura H, Chan L, Matsusue Y. Malfunction of bone marrow-derived osteoclasts and the delay of bone fracture healing in diabetic mice. Bone. 2010 Sep 1;47(3):617-625.
Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. Journal of endocrinological investigation. 2000 May;23(5):295-303.
Kim JH, Jung MH, Lee JM, Son HS, Cha BY, Chang SA. Diabetic peripheral neuropathy is highly associated with nontraumatic fractures in Korean patients with type 2 diabetes mellitus. Clinical endocrinology. 2012 Jul;77(1):51-55.
Kuroda T, Ishikawa K, Nagai T, Fukui T, Hirano T, Inagaki K. Quadrant analysis of quantitative computed tomography scans of the femoral neck reveals superior region-specific weakness in young and middle-aged men with type 1 diabetes mellitus. Journal of clinical densitometry. 2018 Apr 1;21(2):172–178.
Landis WJ. The strength of a calcified tissue depends in part on the molecular structure and organization of its constituent mineral crystals in their organic matrix. Bone. 1995 May 1;16(5):533–544.
Lechleitner M, Koch T, Herold M, Dzien A, Hoppichler F. Tumour necrosis factor-alpha plasma level in patients with type 1 diabetes mellitus and its association with glycaemic control and cardiovascular risk factors. Journal of internal medicine. 2000 Jul;248(1):67-76.
Lecka-Czernik B, Gubrij I, Moerman EJ, Kajkenova O, Lipschitz DA, Manolagas SC, Jilka RL. Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARgamma2. Journal of cellular biochemistry.1999 Sep 1;74(3):357-371.
Leib ES, Lewiecki EM, Binkley N, Hamdy RC. Official positions of the International Society for Clinical Densitometry. Journal of clinical densitometry. 2004 Mar 1;7(1):1-5.
Leslie WD, Morin SN, Lix LM, Majumdar SR. Does diabetes modify the effect of FRAX risk factors for predicting major osteoporotic and hip fracture? Osteoporosis international. 2014 Dec;25(12): 2817-2824.
Lips P, Hosking D, Lippuner K, Norquist JM, Wehren L, Maalouf G, Ragi-Eis S, Chandler J. The prevalence of vitamin D inadequacy amongst women with osteoporosis: an international epidemiological investigation. Journal of internal medicine. 2006 Sep;260(3): 245–254.
Liu EY, Wactawski-Wende J, Donahue RP, Dmochowski J, Hovey KM, Quattrin T. Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care. 2003 Aug 1;26(8):2365-2369.
Lombardi F, Franzese A, Iafusco D, del Puente A, Esposito A, Prisco F, Troncone R, Valerio G. Bone involvement in clusters of autoimmune diseases: just a complication? Bone. 2010 Feb 1;46(2):551–555.
Lopez-Ibarra PJ, Pastor MM, Escobar-Jimenez F, Pardo MD, González AG, Luna JD, Requena ME, Diosdado MA. Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocrine practice. 2001 Oct 1;7(5):346–351.
Lu H, Kraut D, Gerstenfeld LC, Graves DT. Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology. 2003 Jan 1;144(1):346-352.
Lumachi F, Camozzi V, Tombolan V, Luisetto G. Bone mineral density, osteocalcin, and bone-specific alkaline phosphatase in patients with insulin-dependent diabetes mellitus. Annals of the New York academy of sciences. 2009 Sep;1173:E64-67.
Luna R, Garcia-Mayor RV, Lage M, Andrade MA, Barreiro J, Pombo M, Dieguez C, Casanueva FF. High serum leptin levels in children with type 1 diabetes mellitus: contribution of age, BMI, pubertal development and metabolic status. Clinical endocrinology. 1999 Nov;51(5):603-610.
Lunt H, Florkowski CM, Cundy T, Kendall D, Brown LJ, Elliot JR, Wells JE, Turner JG. A population-based study of bone mineral density in women with longstanding type 1 (insulin dependent) diabetes. Diabetes research and clinical practice. 1998 Apr 1;40(1):31-38.
Ma L, Oei L, Jiang L, Estrada K, Chen H, Wang Z, Yu Q, Zillikens MC, Gao X, Rivadeneira F. Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. European journal of epidemiology. 2012 May;27(5):319-332.
Maddaloni E, D’Onofrio L, Lauria A, Maurizi AR, Strollo R, Palermo A, Napoli N, Angeletti S, Pozzilli P, Manfrini S. Osteocalcin levels are inversely associated with Hba1c and BMI in adult subjects with long-standing type 1 diabetes. Journal of endocrinological investigation. 2014 Jul;37(7):661-666.
Madsen JO, Jørgensen NR, Pociot F, Johannesen J. Bone turnover markers in children and adolescents with type 1 diabetes—a systematic review. Pediatric Diabetes. 2019 Aug;20(5):510-22.
Maggio AB, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ. Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. Journal of paediatric endocrinology and metabolism. 2010 Jul 1;23(7):697-707.
Martin A, de Vittoris R, David V, Moraes R, Bégeot M, Lafage-Proust MH, Alexandre C, Vico L, Thomas T. Leptin modulates both resorption and formation while preventing disuse-induced bone loss in tail-suspended female rats. Endocrinology. 2005 Aug 1;146(8):3652-3659.
Martin LM, McCabe LR. Type I diabetic bone phenotype is location but not gender dependent. Histochemistry and cell biology. 2007 Aug;128(2):125-133.
Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. 1996 May 18;312(7041):1254-1259.
Martos-Moreno GA, Barrios V, Soriano-Guillén L, Argente J. Relationship between adiponectin levels, acylated ghrelin levels, and short-term body mass index changes in children with diabetes mellitus type 1 at diagnosis and after insulin therapy. European journal of endocrinology. 2006 Nov 1;155(5):757-761.
Maser RE, Kolm P, Modlesky CM, Beck TJ, Lenhard MJ. Hip strength in adults with type 1 diabetes is associated with age at onset of diabetes. Journal of clinical densitometry. 2012 Jan 1;15(1):78-85.
Mathiassen B, Nielsen S, Johansen JS, Hartwell D, Ditzel J, Rødbro P, Christiansen C. Long-term bone loss in insulin-dependent diabetic patients with microvascular complications. Journal of diabetic complications. 1990 Oct 1;4(4):145-149.
Maurer MS, Burcham J, Cheng H. Diabetes mellitus is associated with an increased risk of falls in elderly residents of a long-term care facility. The journals of gerontology series A: biological sciences and medical sciences. 2005 Sep 1;60(9):1157-1162.
McCabe LR. Understanding the pathology and mechanisms of type I diabetic bone loss. Journal of cellular biochemistry. 2007 Dec 15;102(6):1343-1357.
Miao J, Brismar K, Nyrén O, Ugarph-Morawski A, Ye W. Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes care. 2005 Dec 1;28(12):2850-2855.
Miller SC, de Saint-Georges L, Bowman BM, Jee WS. Bone lining cells: structure and function. Scanning microscopy. 1989 Sep;3(3):27.
Moyer‐Mileur LJ, Slater H, Jordan KC, Murray MA. IGF‐1 and IGF‐binding proteins and bone mass, geometry, and strength: relation to metabolic control in adolescent girls with type 1 diabetes. Journal of bone and mineral research. 2008 Dec;23(12):1884-1891.
Munoz-Torres M, Jodar E, Escobar-Jimenez F, Lopez-Ibarra PJ, Luna JD. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcified tissue international. 1996 May;58(5):316-319.
Murray CE, Coleman CM. Impact of diabetes mellitus on bone health. International journal of molecular sciences. 2019 Sep 30;20(19):4873.
Neumann T, Lodes S, Kästner B, Franke S, Kiehntopf M, Lehmann T, Müller UA, Wolf G, Sämann A. High serum pentosidine but not esRAGE is associated with prevalent fractures in type 1 diabetes independent of bone mineral density and glycaemic control. Osteoporosis international. 2014 May;25(5):1527-1533.
Neumann T, Lodes S, Kästner B, Franke S, Kiehntopf M, Lehmann T, Müller UA, Wolf G, Sämann A. Osteocalcin, adipokines and their associations with glucose metabolism in type 1 diabetes. Bone. 2016a Jan 1;82:50-55.
Neumann T, Lodes S, Kästner B, Lehmann T, Hans D, Lamy O, Müller UA, Wolf G, Sämann A. Trabecular bone score in type 1 diabetes—a cross-sectional study. Osteoporosis International. 2016b Jan;27(1):127-133.
Nixon AJ, Lillich JT, Burton‐Wurster N, Lust G, Mohammed HO. Differentiated cellular function in fetal chondrocytes cultured with insulin‐like growth factor‐I and transforming growth factor‐β. Journal of orthopaedic research. 1998 Sep;16(5):531-541.
Nojiri H, Saita Y, Morikawa D, Kobayashi K, Tsuda C, Miyazaki T, Saito M, Marumo K, Yonezawa I, Kaneko K, Shirasawa T. Cytoplasmic superoxide causes bone fragility owing to low‐turnover osteoporosis and impaired collagen cross‐linking. Journal of bone and mineral research. 2011 Nov;26(11):2682-2694.
Papatheodorou K, Banach M, Edmonds M, Papanas N, Papazoglou D. Complications of diabetes. Journal of diabetes research. 2015 Jul 12;2015:189525.
Papatheodorou K, Papanas N, Banach M, Papazoglou D, Edmonds M. Complications of diabetes 2016. Journal of diabetes research. 2016 Oct 16;2016:6989453.
Pramojanee SN, Phimphilai M, Chattipakorn N, Chattipakorn SC. Possible roles of insulin signaling in osteoblasts. Endocrine research. 2014 Nov 1;39(4):144-151.
Pater A, Sypniewska G, Pilecki O. Biochemical markers of bone cell activity in children with type 1 diabetes mellitus. Journal of Pediatric Endocrinology and metabolism. 2010 Feb 1;23(1-2):81-86.
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. The lancet. 2009 Jun 13;373(9680):2027-2033.
Ramachandran A, Snehalatha C, Ma RC. Diabetes in south-east Asia: An update. Diabetes research and clinical practice. 2014 Feb 1;103(2):231-237.
Rigalleau V, Lasseur C, Raffaitin C, Perlemoine C, Barthe N, Chauveau P, Aparicio M, Combe C, Gin H. Bone loss in diabetic patients with chronic kidney disease. Diabetic medicine. 2007 Jan;24(1):91-93.
Rix M, Andreassen HE, Eskildsen P. Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes care. 1999 May 1;22(5):827-831.
Roggen I, Gies I, Vanbesien J, Louis O, De Schepper J. Trabecular bone mineral density and bone geometry of the distal radius at completion of pubertal growth in childhood type 1 diabetes. Hormone research in paediatrics. 2013;79(2):68-74.
Rosen CJ. Insulin-like growth factor I and bone mineral density: experience from animal models and human observational studies. Clinical endocrinology & metabolism. 2004 Sep 1;18(3):423-435.
Rozadilla A, Nolla JM, Montana E, Fiter J, Gomez-Vaquero C, Soler J, Roig-Escofet D. Bone mineral density in patients with type 1 diabetes mellitus. Joint bone spine. 2000 Jan 1;67(3):215-218.
Saito M, Marumo KM. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporosis international. 2010 Feb;21(2):195-214.
Santana RB, Xu L, Chase HB, Amar S, Graves DT, Trackman PC. A role for advanced glycation end products in diminished bone healing in type 1 diabetes. Diabetes. 2003 Jun 1;52(6):1502-1510.
Schacter GI, Leslie WD. Diabetes and bone disease. Endocrinology and metabolism clinics. 2017 Mar 1;46(1):63-85.
Schaffler MB, Cheung WY, Majeska R, Kennedy O. Osteocytes: master orchestrators of bone. Calcified tissue international. 2014 Jan;94(1):5-24.
Schwartz AV, Hillier TA, Sellmeyer DE, Resnick HE, Gregg E, Ensrud KE, Schreiner PJ, Margolis KL, Cauley JA, Nevitt MC, Black DM. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes care. 2002 Oct 1;25(10):1749-54.
Sealand R, Razavi C, Adler RA. Diabetes mellitus and osteoporosis. Current diabetes reports. 2013 Jun;13(3):411-418.
Seeman E, Delmas PD. Bone quality—the material and structural basis of bone strength and fragility. New England journal of medicine. 2006 May 25;354(21):2250-2261.
Seref‐Ferlengez Z, Suadicani SO, Thi MM. A new perspective on mechanisms governing skeletal complications in type 1 diabetes. Annals of the New York academy of sciences. 2016 Nov;1383(1):67-79.
Shah VN, Shah CS, Snell‐Bergeon JK. Type 1 diabetes and risk of fracture: meta‐analysis and review of the literature. Diabetic medicine. 2015 Sep;32(9):1134-1142.
Shah VN, Carpenter RD, Ferguson VL, Schwartz AV. Bone health in type 1 diabetes. Current opinion in endocrinology, diabetes, and obesity. 2018 Aug;25(4):231.
Shah VN, DiMeglio LA. Sweet bones: Diabetes effects on bone. InBasic and Applied Bone Biology 2019 Jan 1 (pp. 425-441). Academic Press.
Shah VN, Joshee P, Sippl R, Pyle L, Vigers T, Carpenter RD, Kohrt W, Snell-Bergeon JK. Type 1 diabetes onset at young age is associated with compromised bone quality. Bone. 2019b Jun 1;123:260-264.
Shanbhogue VV, Hansen S, Frost M, Jørgensen NR, Hermann AP, Henriksen JE, Brixen K. Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR‐pQCT in adult patients with type 1 diabetes mellitus. Journal of bone and mineral research. 2015 Dec;30(12):2188-2199.
Singer DE, Nathan DM, Fogel HA, Schachat AP. Screening for diabetic retinopathy. Annals of internal medicine. 1992 Apr 15;116(8):660-671.
Smets YF, De Fijter JW, Ringers JA, Lemkes HH, Hamdy NA. Long-term follow-up study on bone mineral density and fractures after simultaneous pancreas-kidney transplantation. Kidney international. 2004 Nov 1;66(5):2070-2076.
Starup-Linde J, Frost M, Vestergaard P, Abrahamsen B. Epidemiology of fractures in diabetes. Calcified tissue international. 2017 Feb;100(2):109-121.
Strotmeyer ES, Cauley JA, Orchard TJ, Steenkiste AR, Dorman JS. Middle-aged premenopausal women with type 1 diabetes have lower bone mineral density and calcaneal quantitative ultrasound than nondiabetic women. Diabetes care. 2006 Feb 1;29(2):306-311.
Thrailkill KM, Liu L, Wahl EC, Bunn RC, Perrien DS, Cockrell GE, Skinner RA, Hogue WR, Carver AA, Fowlkes JL, Aronson J. Bone formation is impaired in a model of type 1 diabetes. Diabetes. 2005 Oct 1;54(10):2875-2881.
Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA. Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporosis international. 2011 Feb;22(2):391-420.
Verhaeghe J, Suiker AM, Visser WJ, Van Herck E, Van Bree R, Bouillon R. The effects of systemic insulin, insulin-like growth factor-I and growth hormone on bone growth and turnover in spontaneously diabetic BB rats. Journal of endocrinology. 1992 Sep 1;134(3):485-492.
Verroken C, Pieters W, Beddeleem L, Goemaere S, Zmierczak HG, Shadid S, Kaufman JM, Lapauw B. Cortical bone size deficit in adult patients with type 1 diabetes mellitus. The journal of clinical endocrinology & metabolism. 2017 Aug 1;102(8):2887-2895.
Vestergaard P, Mosekilde L. Fractures in patients with hyperthyroidism and hypothyroidism: a nationwide follow-up study in 16,249 patients. Thyroid. 2002 May 1;12(5):411-419.
Vestergaard P, Rejnmark L, Mosekilde L. Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia. 2005 Jul;48(7):1292-1299.
Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporosis international. 2007 Apr;18(4):427-44.
Vestergaard P, Rejnmark L, Mosekilde L. Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcified tissue international. 2009 Jan;84(1):45-55.
Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F. Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. Journal of diabetes and its complications. 2011 Jul 1;25(4):216-221.
Wang L, Wang H, Xu X, Wang D, Liu H. Insulin facilitates osteoblast differentiation. Cell biology international. 2013 Nov;37(11):1157-1161.
Weber DR, Haynes K, Leonard MB, Willi SM, Denburg MR. 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 Oct 1;38(10):1913-1920.
Weber DR, Gordon RJ, Kelley JC, Leonard MB, Willi SM, Hatch-Stein J, Kelly A, Kosacci O, Kucheruk O, Kaafarani M, Zemel BS. Poor glycemic control is associated with impaired bone accrual in the year following a diagnosis of type 1 diabetes. The journal of clinical endocrinology & metabolism. 2019 Oct;104(10):4511-4520.
Witek PR, Witek J, Pańkowska E. Type 1 diabetes-associated autoimmune diseases: screening, diagnostic principles and management. Medycyna wieku rozwojowego. 2012 Jan 1;16(1):23-34.
Wittrant Y, Gorin Y, Woodruff K, Horn D, Abboud HE, Mohan S, Abboud-Werner SL. High d (+) glucose concentration inhibits RANKL-induced osteoclastogenesis. Bone. 2008 Jun 1;42(6):1122-1130.
Yamagishi S, Nakamura K, Inoue H. Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Medical hypotheses. 2005 Jan 1;65(6):1013-1015.
Yang J, Zhang X, Wang W, Liu J. Insulin stimulates osteoblast proliferation and differentiation through ERK and PI3K in MG‐63 cells. Cell Biochemistry and Function: Cellular biochemistry and its modulation by active agents or disease. 2010 Jun;28(4):334-341.
Yuuki T, Kanda T, Kimura Y, Kotajima N, Tamura JI, Kobayashi I, Kishi S. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. Journal of diabetes and its complications. 2001 Sep 1;15(5):257-259.
Zhang M, Xuan S, Bouxsein ML, Von Stechow D, Akeno N, Faugere MC, Malluche H, Zhao G, Rosen CJ, Efstratiadis A, Clemens TL. Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. Journal of biological chemistry. 2002 Nov 15;277(46):44005-44012.
Zhang W, Shen X, Wan C, Zhao Q, Zhang L, Zhou Q, Deng L. Effects of insulin and insulin‐like growth factor 1 on osteoblast proliferation and differentiation: differential signalling via Akt and ERK. Cell biochemistry and function. 2012 Jun;30(4):297-302.
Zhukouskaya VV, Eller-Vainicher C, Vadzianava VV, Shepelkevich AP, Zhurava IV, Korolenko GG, Salko OB, Cairoli E, Beck-Peccoz P, Chiodini I. Prevalence of morphometric vertebral fractures in patients with type 1 diabetes. Diabetes care. 2013 Jun 1;36(6):1635-40.
