Prevalence and determinants of osteoporosis in patients with type 1 and type 2 diabetes mellitus

BMC Endocrine Disorders

Volumn 14, Issue , 2014, Pages

  Leidig Bruckner, Gudrun ^a,b   Grobholz, Sonja ^b   Bruckner, Thomas ^b   Scheidt Nave, Christa ^c   Nawroth, Peter ^b   Schneider, Jochen G ^b,d  

^a Practice for Endocrinology and Nuclear Medicine Brückenstraße 21   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c ROBERT KOCH INSTITUTE   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

Author keywords

Bone mineral density; Diabetes mellitus; Fractures; Osteoporosis; Vascular complications

Indexed keywords

ANTACID AGENT; ANTIDIABETIC AGENT; GLUCOCORTICOID; HEMOGLOBIN A1C; INSULIN;

ADULT; ARTICLE; BONE DENSITY; CHRONIC LUNG DISEASE; COMPARATIVE STUDY; CONTROLLED STUDY; CORTICOSTEROID THERAPY; DIABETIC PATIENT; DIABETIC RETINOPATHY; DISEASE DURATION; FEMALE; FEMUR NECK; FRAGILITY FRACTURE; HEMOGLOBIN BLOOD LEVEL; HUMAN; HYPERTENSION; HYPERTHYROIDISM; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; ISCHEMIC HEART DISEASE; LUMBAR SPINE; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OSTEOPOROSIS; PERIPHERAL OCCLUSIVE ARTERY DISEASE; RHEUMATOID ARTHRITIS; RISK FACTOR; ADOLESCENT; AGED; CASE CONTROL STUDY; CLINICAL TRIAL; COMPLICATION; CROSS-SECTIONAL STUDY; FOLLOW UP; FRACTURES, BONE; LUMBAR VERTEBRA; MIDDLE AGED; MULTICENTER STUDY; PATHOLOGY; PATHOPHYSIOLOGY; PHOTON ABSORPTIOMETRY; PREVALENCE; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL; VERY ELDERLY; YOUNG ADULT;

ABSORPTIOMETRY, PHOTON; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BONE DENSITY; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FEMALE; FEMUR NECK; FOLLOW-UP STUDIES; FRACTURES, BONE; HUMANS; LUMBAR VERTEBRAE; MALE; MIDDLE AGED; OSTEOPOROSIS; PREVALENCE; PROGNOSIS; RISK FACTORS; YOUNG ADULT;

EID: 84899978763     PISSN: None     EISSN: 14726823     Source Type: Journal    
DOI: 10.1186/1472-6823-14-33     Document Type: Article

References (47)

1. Leidig-Bruckner G, Ziegler R. Diabetes mellitus a risk for osteoporosis?. Exp Clin Endocrinol Diabetes 2001, 109(Suppl 2):S493-S514. 10.1055/s-2001-18605, 11460594.
2. Hofbauer LC, Brueck CC, Singh SK, Dobnig H. Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 2007, 22(9):1317-1328. 10.1359/jbmr.070510, 17501667.
3. 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. 10.1093/aje/kwm106, 17575306.
4. 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 Res Clin Pract 1998, 40(1):31-38. 10.1016/S0168-8227(98)00012-6, 9699088.
5. Gunczler P, Lanes R, Paz-Martinez V, Martins R, Esaa S, Colmenares V, Weisinger JR. Decreased lumbar spine bone mass and low bone turnover in children and adolescents with insulin dependent diabetes mellitus followed longitudinally. J Pediatr Endocrinol Metab 1998, 11(3):413-419.
6. Forst T, Pfutzner A, Kann P, Schehler B, Lobmann R, Schafer H, Andreas J, Bockisch A, Beyer J. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med 1995, 12(10):874-879. 10.1111/j.1464-5491.1995.tb00389.x, 8846677.
7. Hui SL, Epstein S, Johnston CC. A prospective study of bone mass in patients with type I diabetes. J Clin Endocrinol Metab 1985, 60(1):74-80. 10.1210/jcem-60-1-74, 3964795.
8. Levin ME, Boisseau VC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med 1976, 294(5):241-245. 10.1056/NEJM197601292940502, 1244549.
9. Mastrandrea LD, Wactawski-Wende J, Donahue RP, Hovey KM, Clark A, Quattrin T. Young women with type 1 diabetes have lower bone mineral density that persists over time. Diabetes Care 2008, 31(9):1729-1735. 10.2337/dc07-2426, 2518333, 18591404.
10. Heath H, Melton LJ, Chu CP. Diabetes mellitus and risk of skeletal fracture. N Engl J Med 1980, 303(10):567-570. 10.1056/NEJM198009043031008, 7402221.
11. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 2001, 86(1):32-38. 10.1210/jcem.86.1.7139, 11231974.
12. Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 2001, 24(7):1192-1197. 10.2337/diacare.24.7.1192, 11423501.
13. Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Zmuda JM, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB. Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: The Health, Aging, and Body Composition Study. J Bone Miner Res 2004, 19(7):1084-1091. 10.1359/JBMR.040311, 15176990.
14. 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. J Clin Endocrinol Metab 2006, 91(9):3404-3410. 10.1210/jc.2006-0614, 16804043.
15. Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A. Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 2006, 91(9):3355-3363. 10.1210/jc.2006-0460, 16735485.
16. 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. 10.1007/s00198-006-0253-4, 17068657.
17. Lipscombe LL, Jamal SA, Booth GL, Hawker GA. The risk of hip fractures in older individuals with diabetes: a population-based study. Diabetes Care 2007, 30(4):835-841. 10.2337/dc06-1851, 17392544.
18. Melton LJ, Leibson CL, Achenbach SJ, Therneau TM, Khosla S. Fracture risk in type 2 diabetes: update of a population-based study. J Bone Miner Res 2008, 23(8):1334-1342. 10.1359/jbmr.080323, 2574704,2574704, 18348689.
19. Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T. Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Miner Res 2009, 24(4):702-709. 10.1359/jbmr.081207, 19049338.
20. de Liefde I, van der Klift M, de Laet CE, van Daele PL, Hofman A, Pols HA. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 2005, 16(12):1713-1720. 10.1007/s00198-005-1909-1, 15940395.
21. Kanis JA, Johnell O, Oden A, Johansson H, McCloskey E. FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int 2008, 19(4):385-397. 10.1007/s00198-007-0543-5, 2267485, 18292978.
22. Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, Donaldson MG, Cauley JA, Harris TB, Womack CR KA, Palermo L, Black DM, Study of Osteoporotic Fractures (SOF) Research Group; Osteoporotic Fractures in Men (MrOS) Research Group; Health, Aging, and Body Composition (Health ABC) Research Group Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 2011, 305(21):2184-2192. 10.1001/jama.2011.715, 3287389, 21632482, Study of Osteoporotic Fractures (SOF) Research Group; Osteoporotic Fractures in Men (MrOS) Research Group; Health, Aging, and Body Composition (Health ABC) Research Group.
23. Lunt M, Felsenberg D, Reeve J, Benevolenskaya L, Cannata J, Dequeker J, Dodenhof C, Falch JA, Masaryk P, Pols HA Poor G, Reid DM, Scheidt-Nave C, Weber K, Varlow J, Kanis JA, O'Neill TW, Silman AJ. Bone density variation and its effects on risk of vertebral deformity in men and women studied in thirteen European centers: the EVOS Study. J Bone Miner Res 1997, 12(11):1883-1894. 10.1359/jbmr.1997.12.11.1883, 9383693.
24. Scheidt-Nave C, Felsenberg D, Kragi G, Bruckner T, Leidig-Bruckner G, Wuster C, Ziegler R. Vertebral deformity as an index of osteoporosis-induced spinal fracture-an external validity construct based on bone density data. Med Klin (Munich) 1998, 93(Suppl 2):46-55.
25. Raspe A, Matthis C, Scheidt-Nave C, Raspe H. European Study of Vertebral Osteoporosis (EVOS): design and implementation in 8 German study centers. Med Klin (Munich) 1998, 93(Suppl 2):12-16,18.
26. O'Neill TW, Felsenberg D, Varlow J, Cooper C, Kanis JA, Silman AJ. The prevalence of vertebral deformity in european men and women: the European Vertebral Osteoporosis Study. J Bone Miner Res 1996, 11(7):1010-1018.
27. O'Neill TW, Cooper C, Cannata JB, Diaz Lopez JB, Hoszowski K, Johnell O, Lorenc RS, Nilsson B, Raspe H, Stewart O. Reproducibility of a questionnaire on risk factors for osteoporosis in a multicentre prevalence survey: the European Vertebral Osteoporosis Study. Int J Epidemiol 1994, 23(3):559-565. 10.1093/ije/23.3.559, 7960382.
28. Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet 2002, 359(9321):1929-1936. 10.1016/S0140-6736(02)08761-5, 12057569.
29. Isaia GC, Ardissone P, Di Stefano M, Ferrari D, Martina V, Porta M, Tagliabue M, Molinatti GM. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 1999, 36(1-2):35-38.
30. Compston JE, Smith EM, Matthews C, Schofield P. Whole body composition and regional bone mass in women with insulin-dependent diabetes mellitus. Clin Endocrinol (Oxf) 1994, 41(3):289-293. 10.1111/j.1365-2265.1994.tb02547.x, 7955434.
31. Tuominen JT, Impivaara O, Puukka P, Ronnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 1999, 22(7):1196-1200. 10.2337/diacare.22.7.1196, 10388989.
32. Majima T, Komatsu Y, Yamada T, Koike Y, Shigemoto M, Takagi C, Hatanaka I, Nakao K. Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int 2005, 16(8):907-913. 10.1007/s00198-004-1786-z, 15558237.
33. Forestier J, Lagier R. Ankylosing hyperostosis of the spine. Clin Orthop Relat Res 1971, 74:65-83.
34. Resnick D, Shapiro RF, Wiesner KB, Niwayama G, Utsinger PD, Shaul SR. Diffuse idiopathic skeletal hyperostosis (DISH) ankylosing hyperostosis of Forestier and Rotes-Querol]. Semin Arthritis Rheum 1978, 7(3):153-187. 10.1016/0049-0172(78)90036-7, 341323.
35. Spagnola AM, Bennett PH, Terasaki PI. Vertebral ankylosing hyperostosis (Forestier's disease) and HLA antigens in Pima Indians. Arthritis Rheum 1978, 21(4):467-472. 10.1002/art.1780210411, 656161.
36. Sencan D, Elden H, Nacitarhan V, Sencan M, Kaptanoglu E. The prevalence of diffuse idiopathic skeletal hyperostosis in patients with diabetes mellitus. Rheumatol Int 2005, 25(7):518-521. 10.1007/s00296-004-0474-9, 16167164.
37. Vestergaard P, Rejnmark L, Mosekilde L. Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 2009, 84(1):45-55. 10.1007/s00223-008-9195-5, 19067021.
38. Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 2000, 23(5):295-303.
39. 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. J Clin Endocrinol Metab 1995, 80(4):1194-1202.
40. Burkhardt R, Moser W, Bartl R, Mahl G. Is diabetic osteoporosis due to microangiopathy?. Lancet 1981, 1(8224):844.
41. Bandeira E, Neves AP, Costa C, Bandeira F. Association between vascular calcification and osteoporosis in men with type 2 diabetes. J Clin Densitom 2012, 15(1):55-60. 10.1016/j.jocd.2011.07.002, 22071025.
42. van der Klift M, Pols HA, Hak AE, Witteman JC, Hofman A, de Laet CE. Bone mineral density and the risk of peripheral arterial disease: the Rotterdam Study. Calcif Tissue Int 2002, 70(6):443-449. 10.1007/s00223-001-2076-9, 11976772.
43. Collins TC, Ewing SK, Diem SJ, Taylor BC, Orwoll ES, Cummings SR, Strotmeyer ES, Ensrud KE. Peripheral arterial disease is associated with higher rates of hip bone loss and increased fracture risk in older men. Circulation 2009, 119(17):2305-2312. 10.1161/CIRCULATIONAHA.108.820993, 2766264, 19380619.
44. Farhat GN, Cauley JA, Matthews KA, Newman AB, Johnston J, Mackey R, Edmundowicz D, Sutton-Tyrrell K. Volumetric BMD and vascular calcification in middle-aged women: the Study of Women's Health Across the Nation. J Bone Miner Res 2006, 21(12):1839-1846. 10.1359/jbmr.060903, 17002567.
45. Hyder JA, Allison MA, Wong N, Papa A, Lang TF, Sirlin C, Gapstur SM, Ouyang P, Carr JJ, Criqui MH. Association of coronary artery and aortic calcium with lumbar bone density: the MESA Abdominal Aortic Calcium Study. Am J Epidemiol 2009, 169(2):186-194. 2727254, 19064643.
46. Schwartz AV, Hillier TA, Sellmeyer DE, Resnick HE, Gregg E, Ensrud KE, Schreiner PJ, Margolis KL, Cauley JA, Nevitt MC Black DM, Cummings SR. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care 2002, 25(10):1749-1754. 10.2337/diacare.25.10.1749, 12351472.
47. Eisman JA, Bogoch ER, Dell R, Harrington JT, McKinney RE, McLellan A, Mitchell PJ, Silverman S, Singleton R, Siris E. Making the first fracture the last fracture: ASBMR task force report on secondary fracture prevention. J Bone Miner Res 2012, 27(10):2039-2046. 10.1002/jbmr.1698, 22836222.