Bone Geometry, Volumetric Density, Microarchitecture, and Estimated Bone Strength Assessed by HR-pQCT in Adult Patients With Type 1 Diabetes Mellitus
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The primary goal of this cross-sectional in vivo study was to assess peripheral bone microarchitecture, bone strength, and bone remodeling in adult type 1 diabetes (T1D) patients with and without diabetic microvascular disease (MVD+ and MVD–, respectively) and to compare them with age-, gender-, and height-matched healthy control subjects (CoMVD+ and CoMVD–, respectively). The secondary goal was to assess differences in MVD– and MVD+ patients. Fifty-five patients with T1DM (MVD+ group: n = 29) were recruited from the Funen Diabetes Database. Dual-energy X-ray absorptiometry (DXA), high-resolution peripheral quantitative computed tomography (HR-pQCT) of the ultradistal radius and tibia, and biochemical markers of bone turnover were performed in all participants. There were no significant differences in HR-pQCT parameters between MVD– and CoMVD– subjects. In contrast, MVD+ patients had larger total and trabecular bone areas (p = 0.04 and p = 0.02, respectively), lower total, trabecular, and cortical volumetric bone mineral density (vBMD) (p < 0.01, p < 0.04, and p < 0.02, respectively), and thinner cortex (p = 0.03) at the radius, and lower total and trabecular vBMD (p = 0.01 and p = 0.02, respectively) at the tibia in comparison to CoMVD+. MVD+ patients also exhibited lower total and trabecular vBMD (radius p = 0.01, tibia p < 0.01), trabecular thickness (radius p = 0.01), estimated bone strength, and greater trabecular separation (radius p = 0.01, tibia p < 0.01) and network inhomogeneity (radius p = 0.01, tibia p < 0.01) in comparison to MVD– patients. These differences remained significant after adjustment for age, body mass index, gender, disease duration, and glycemic control (average glycated hemoglobin over the previous 3 years). Although biochemical markers of bone turnover were significantly lower in MVD+ and MVD– groups in comparison to controls, they were similar between the MVD+ and MVD– groups. The results of our study suggest that the presence of MVD was associated with deficits in cortical and trabecular bone vBMD and microarchitecture that could partly explain the excess skeletal fragility observed in these patients. © 2015 American Society for Bone and Mineral Research.
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Cites
Bone Quality — The Material and Structural Basis of Bone Strength and Fragility
Seeman, E., & Delmas, P. D. (2006) · New England Journal of Medicine · doi:10.1056/nejmra053077 · Cited by 2,108 · see citing works
Vestergaard, P. F. (2006) · Osteoporosis International · doi:10.1007/s00198-006-0253-4 · Cited by 1,803 · see citing works
PARFITT, A. M., Mathews, C. H. E., Villanueva, A. R., Kleerekoper, M., Frame, B., & Rao, D. S. (1983) · Journal of Clinical Investigation · doi:10.1172/jci111096 · Cited by 1,542 · see citing works
Boutroy, S., Bouxsein, M., Munoz, F., & Delmas, P. D. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1258 · Cited by 1,190 · see citing works
The Role of Advanced Glycation End Products in Progression and Complications of Diabetes
Goh, S.-Y., & Cooper, M. E. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1817 · Cited by 987 · see citing works
Teriparatide or Alendronate in Glucocorticoid-Induced Osteoporosis
Saag, K. G., Shane, E., Boonen, S., Marín, F., Donley, D. W., Taylor, K. A., Dalsky, G. P., & Marcus, R. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa071408 · Cited by 914 · see citing works
Saito, M., & Marumo, K. (2009) · Osteoporosis International · doi:10.1007/s00198-009-1066-z · Cited by 914 · see citing works
Bone Loss and Bone Turnover in Diabetes
Krakauer, J. C., McKenna, M. J., Buderer, N. F., Rao, D. S., Whitehouse, F. W., & PARFITT, A. M. (1995) · Diabetes · doi:10.2337/diab.44.7.775 · Cited by 497 · see citing works
In vivo high resolution 3D-QCT of the human forearm
Laib, A., Häuselmann, H. J., & Ruegsegger, P. (1998) · Technology and Health Care · doi:10.3233/thc-1998-65-606 · Cited by 454 · see citing works
MacNeil, J. A., & Boyd, S. K. (2008) · Bone · doi:10.1016/j.bone.2008.01.017 · Cited by 440 · see citing works
Kurland, E. S., Cosman, F., McMahon, D. J., Rosen, C. J., Lindsay, R., & Bilezikian, J. P. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.9.6818 · Cited by 383 · see citing works
Burghardt, A. J., Kazakia, G. J., Ramachandran, S., Link, T. M., & Majumdar, S. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.091104 · Cited by 336 · see citing works
Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology
Kemink, S. A. G., Hermus, A. R. M. M., Swinkels, L. M. J. W., Lutterman, J. A., & SMALS, A. G. H. (2000) · Journal of Endocrinological Investigation · doi:10.1007/bf03343726 · Cited by 323 · see citing works
Nishiyama, K. K., MACDONALD, H. M., Buie, H. R., Hanley, D. A., & Boyd, S. K. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.091020 · Cited by 311 · see citing works
Pialat, J., Burghardt, A. J., Sode, M., Link, T. M., & Majumdar, S. (2011) · Bone · doi:10.1016/j.bone.2011.10.003 · Cited by 296 · see citing works
Kurland, E. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.9.3069 · Cited by 283 · see citing works
Vestergaard, P., Rejnmark, L., & Mosekilde, L. (2008) · Calcified Tissue International · doi:10.1007/s00223-008-9195-5 · Cited by 282 · see citing works
Laib, A., & Ruegsegger, P. (1999) · Bone · doi:10.1016/s8756-3282(98)00159-8 · Cited by 245 · see citing works
Intensive Insulin Therapy and Bone Mineral Density in Type 1 Diabetes Mellitus: A Prospective Study
Pastor, M. M. C., López-Ibarra, P. J., Escobar‐Jiménez, F., Pardo, M. D. S., & García‐Cervigón, A. (2000) · Osteoporosis International · doi:10.1007/s001980070114 · Cited by 223 · see citing works
Elevated Hip Fracture Risk in Type 1 Diabetic Patients
Miao, J., Brismar, K., Nyrén, O., Ugarph-Morawski, A., & Ye, W. (2005) · Diabetes Care · doi:10.2337/diacare.28.12.2850 · Cited by 198 · see citing works
Muñoz‐Torres, M., Jódar, E., Escobar‐Jiménez, F., López-Ibarra, P. J., & Luna, J. D. D. (1996) · Calcified Tissue International · doi:10.1007/bf02509378 · Cited by 174 · see citing works
Ridge number density: A new parameter for in vivo bone structure analysis
Laib, A., Hildebrand, T., Häuselmann, H. J., & Ruegsegger, P. (1997) · Bone · doi:10.1016/s8756-3282(97)00205-6 · Cited by 173 · see citing works
Heap, J., Murray, M. A., Miller, S. C., Jalili, T., & Moyer‐Mileur, L. J. (2004) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2003.10.066 · Cited by 171 · see citing works
Hansen, S. G., Hauge, E., Jensen, J. B., & Brixen, K. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1784 · Cited by 152 · see citing works
Self-citationValerio, G., PUENTE, A. D., Puente, A. E.-D., Buono, P., Mozzillo, E., & Franzese, A. (2002) · Hormone Research in Paediatrics · doi:10.1159/000066441 · Cited by 142 · see citing works
Impact of peripheral neuropathy on bone density in patients with type 1 diabetes.
Rix, M., Andreassen, H. F., & Eskildsen, P. C. (1999) · Diabetes Care · doi:10.2337/diacare.22.5.827 · Cited by 132 · see citing works
Trabecular bone histomorphometry in humans with Type 1 Diabetes Mellitus
Armas, L. A. G., Akhter, M. P., Drincic, A., & Recker, R. R. (2011) · Bone · doi:10.1016/j.bone.2011.09.055 · Cited by 116 · see citing works
Miazgowski, T., & Czekalski, S. (1998) · Osteoporosis International · doi:10.1007/s001980050082 · Cited by 115 · see citing works
Hansen, S. G., Shanbhogue, V. V., Folkestad, L., Nielsen, M. M. F., & Brixen, K. (2013) · Calcified Tissue International · doi:10.1007/s00223-013-9808-5 · Cited by 109 · see citing works
Self-citationImage-Based Micro-Finite-Element Modeling for Improved Distal Radius Strength Diagnosis
Pistoia, W., van Rietbergen, B., Lochmüller, E., Lill, C. A., Eckstein, F., & Ruegsegger, P. (2004) · Journal of Clinical Densitometry · doi:10.1385/jcd:7:2:153 · Cited by 100 · see citing works
Bone mineral acquisition in adolescents with type 1 diabetes
Moyer‐Mileur, L. J., Dixon, S. B., Quick, J. L., Askew, E. W., & Murray, M. A. (2004) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2004.06.070 · Cited by 96 · see citing works
Prevalence and predictors of osteopenia and osteoporosis in adults with Type 1 diabetes
Hamilton, E. J., Rakic, V., Davis, W. A., Chubb, S. A. P., Kamber, N., Prince, R. L., & Davis, T. M. E. (2009) · Diabetic Medicine · doi:10.1111/j.1464-5491.2008.02608.x · Cited by 93 · see citing works
McNair, P., Christiansen, C., Christensen, M. S., Madsbad, S., FABER, O. K., Binder, C., & Transbøl, I. (1981) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1981.tb01765.x · Cited by 93 · see citing works
Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus
Olmos, J. M., Pérez‐Castrillón, J. L., García, M. T. S., Garrido, J. C., Amado, J. A., & González-Macı́as, J. (1994) · Bone and Mineral · doi:10.1016/s0169-6009(08)80157-2 · Cited by 87 · see citing works
Influence of diabetes on peripheral bone mineral density in men: a controlled study
Bridges, M., Moochhala, S. H., Barbour, J., & Kelly, C. A. (2005) · Acta Diabetologica · doi:10.1007/s00592-005-0183-1 · Cited by 83 · see citing works
Bone Size Normalizes With Age in Children and Adolescents With Type 1 Diabetes
Bechtold, S. M., Putzker, S., Bonfig, W., Fuchs, O., Dirlenbach, I., & Schwarz, H. P. (2007) · Diabetes Care · doi:10.2337/dc07-0142 · Cited by 73 · see citing works
Bone density and markers of bone remodeling in type 1 male diabetic patients
Alexopoulou, O., Jamart, J., Devogelaer, J., Brichard, S. M., Nayer, P. D., & Buysschaert, M. (2006) · Diabetes & Metabolism · doi:10.1016/s1262-3636(07)70303-8 · Cited by 67 · see citing works
Lumachi, F., Camozzi, V., Tombolan, V., & Luisetto, G. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04955.x · Cited by 65 · see citing works
Body composition and bone mineral density in long‐standing type 1 diabetes
Ingberg, C. M., Palmér, M., Åman, J., Arvidsson, B., Schvarcz, E., & Berne, C. (2004) · Journal of Internal Medicine · doi:10.1046/j.1365-2796.2003.01283.x · Cited by 64 · see citing works
Shanbhogue, V. V., Hansen, S. G., Folkestad, L., Brixen, K., & Beck‐Nielsen, S. S. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2310 · Cited by 54 · see citing works
Self-citationLunt, H., Florkowski, C. M., Cundy, T., Kendall, D., Brown, L., Elliot, J. R., Wells, J. E., & Turner, J. G. (1998) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(98)00012-6 · Cited by 54 · see citing works
Osteoporosis and Diabetes: Lessons from the Diabetic BB Rat
Verhaeghe, J., Visser, W. J., Einhorn, T. A., & Bouillon, R. (2008) · Hormone Research · doi:10.1159/000181834 · Cited by 38 · see citing works
Faßbender, W. J., Gödde, M., Brandenburg, V. M., Usadel, K. H., & Stumpf, U. (2009) · Advances in Medical Sciences · doi:10.2478/v10039-009-0003-x · Cited by 19 · see citing works
Antiresorptive Therapy for the Prevention of Postmenopausal Osteoporosis
Vestergaard, P. (2005) · Treatments in Endocrinology · doi:10.2165/00024677-200504050-00001 · Cited by 13 · see citing works
Flagged first, then by citations
1 of the 45 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Bone fragility in diabetes: novel concepts and clinical implications
Hofbauer, L. C., Busse, B., Eastell, R., Ferrari, S., Frost, M., Müller, R., Burden, A. M., Rivadeneira, F., Napoli, N., & Rauner, M. (2022) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(21)00347-8 · Cited by 452 · see citing works
Self-citationBone Turnover Markers: Basic Biology to Clinical Applications
Schini, M., Vilaça, T., Gossiel, F., Salam, S., & Eastell, R. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnac031 · Cited by 415 · see citing works
Ebeling, P. R., Nguyen, H. H., Aleksova, J., Vincent, A. J., Wong, P., & Milat, F. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnab028 · Cited by 354 · see citing works
Hygum, K., Starup-Linde, J., Harsløf, T., Vestergaard, P., & Langdahl, B. (2017) · European Journal of Endocrinology · doi:10.1530/eje-16-0652 · Cited by 274 · see citing works
Vilaça, T., Schini, M., Harnan, S., Sutton, A., Poku, E. N., Allen, I. E., Cummings, S. R., & Eastell, R. (2020) · Bone · doi:10.1016/j.bone.2020.115457 · Cited by 237 · see citing works
Skeletal Metabolism, Fracture Risk, and Fracture Outcomes in Type 1 and Type 2 Diabetes
Sellmeyer, D. E., Civitelli, R., Hofbauer, L. C., Khosla, S., Lecka‐Czernik, B., & Schwartz, A. V. (2016) · Diabetes · doi:10.2337/db16-0063 · Cited by 207 · see citing works
Determinants of bone strength and quality in diabetes mellitus in humans
Farr, J. N., & Khosla, S. (2015) · Bone · doi:10.1016/j.bone.2015.07.027 · Cited by 192 · see citing works
MECHANISMS IN ENDOCRINOLOGY: Mechanisms and evaluation of bone fragility in type 1 diabetes mellitus
Hough, F. S., Pierroz, D. D., Cooper, C. C., Ferrari, S., & _, _. (2015) · European Journal of Endocrinology · doi:10.1530/eje-15-0820 · Cited by 160 · see citing works
Bone disease in diabetes: another manifestation of microvascular disease?
Shanbhogue, V. V., Hansen, S., Frost, M., Brixen, K., & Hermann, A. P. (2017) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(17)30134-1 · Cited by 158 · see citing works
Self-citationThe Bone Marrow-Derived Stromal Cells: Commitment and Regulation of Adipogenesis
Tencerova, M., & Kassem, M. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00127 · Cited by 149 · see citing works
Fracture Risk Assessment in Patients With Diabetes Mellitus
Poiană, C., & Capatina, C. A.-M. (2017) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2017.06.011 · Cited by 113 · see citing works
Valderrábano, R. J., & Linares, M. (2018) · Clinical Diabetes and Endocrinology · doi:10.1186/s40842-018-0060-9 · Cited by 115 · see citing works
Shah, V. N., Harrall, K. K., Shah, C. S., Gallo, T., Joshee, P., Snell‐Bergeon, J. K., & Kohrt, W. M. (2017) · Osteoporosis International · doi:10.1007/s00198-017-4097-x · Cited by 108 · see citing works
Cheng, K., Guo, Q., Yang, W., Wang, Y., Sun, Z., & Wu, H. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.918483 · Cited by 105 · see citing works
Bone Structure and Predictors of Fracture in Type 1 and Type 2 Diabetes
Starup‐Linde, J., Lykkeboe, S., Gregersen, S., Hauge, E. M., Langdahl, B. L., Handberg, A., & Vestergaard, P. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3882 · Cited by 97 · see citing works
Advanced Glycation Endproducts and Bone Material Properties in Type 1 Diabetic Mice
Rubin, M. R., Paschalis, E. P., Poundarik, A., Sroga, G. E., McMahon, D. J., Gamsjaeger, S., Klaushofer, K., & Vashishth, D. (2016) · PLOS ONE · doi:10.1371/journal.pone.0154700 · Cited by 90 · see citing works
Hygum, K., Starup‐Linde, J., & Langdahl, B. L. (2019) · Osteoporosis and Sarcopenia · doi:10.1016/j.afos.2019.05.001 · Cited by 86 · see citing works
Bone health in diabetes and prediabetes
Costantini, S., & Conte, C. (2019) · World Journal of Diabetes · doi:10.4239/wjd.v10.i8.421 · Cited by 84 · see citing works
Assessment of bone quality in patients with diabetes mellitus
Jiang, N., & Xia, W. (2018) · Osteoporosis International · doi:10.1007/s00198-018-4532-7 · Cited by 82 · see citing works
Risk factors for fragility fractures in type 1 diabetes
Leanza, G., Maddaloni, E., Pitocco, D., Conte, C., Palermo, A., Maurizi, A. R., Pantano, A. L., SURACI, C., Altomare, M., Strollo, R., et al. (2019) · Bone · doi:10.1016/j.bone.2019.04.017 · Cited by 82 · see citing works
Diabetes and Bone Marrow Adiposity
Kim, T. Y., & Schafer, A. L. (2016) · Current Osteoporosis Reports · doi:10.1007/s11914-016-0336-x · Cited by 80 · see citing works
Bone disorders associated with diabetes mellitus and its treatments
Cortet, B., Lucas, S., Legroux-Gérot, I., Penel, G., Chauveau, C., & Paccou, J. (2018) · Joint Bone Spine · doi:10.1016/j.jbspin.2018.08.002 · Cited by 78 · see citing works
Thong, E. P., Herath, M., Weber, D. R., Ranasinha, S., Ebeling, P. R., Milat, F., & Teede, H. J. (2018) · Clinical Endocrinology · doi:10.1111/cen.13761 · Cited by 75 · see citing works
Raisingani, M. G., Brar, P. C., Kohn, B., & Yakar, S. (2017) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2017.04.003 · Cited by 73 · see citing works
Walle, M., Whittier, D. E., Frost, M., Müller, R., & Collins, C. J. (2022) · Current Osteoporosis Reports · doi:10.1007/s11914-022-00755-6 · Cited by 72 · see citing works
Self-citationDIAGNOSIS OF ENDOCRINE DISEASE: Evaluation of bone fragility in endocrine disorders
Eller-Vainicher, C., Falchetti, A., Gennari, L., Cairoli, E., Bertoldo, F., Vescini, F., Scillitani, A., & Chiodini, I. (2019) · European Journal of Endocrinology · doi:10.1530/eje-18-0991 · Cited by 64 · see citing works
Bone health in type 1 diabetes
Shah, V. N., Carpenter, R. D., Ferguson, V. L., & Schwartz, A. V. (2018) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000421 · Cited by 64 · see citing works
Skeletal fragility in diabetes
Rubin, M. R. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13463 · Cited by 60 · see citing works
Epidemiology of Skeletal Health in Type 1 Diabetes
Weber, D. R., & Schwartz, G. J. (2016) · Current Osteoporosis Reports · doi:10.1007/s11914-016-0333-0 · Cited by 59 · see citing works
Schacter, G. I., & Leslie, W. D. (2021) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2021.03.005 · Cited by 58 · see citing works
Zhang, H., Gan, L., Zhu, X., Wang, J., Li-cun, H., Peng, C., Jing, D., Zhang, X., & Shan, Q. (2017) · Bone · doi:10.1016/j.bone.2017.10.024 · Cited by 57 · see citing works
Type 1 Diabetes and Bone Fragility: Links and Risks
Starup‐Linde, J., Hygum, K., Harsløf, T., & Langdahl, B. L. (2019) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s191091 · Cited by 54 · see citing works
Peripheral Neuropathy as a Component of Skeletal Disease in Diabetes
Beeve, A. T., Brazill, J. M., & Scheller, E. L. (2019) · Current Osteoporosis Reports · doi:10.1007/s11914-019-00528-8 · Cited by 54 · see citing works
Bone health in subjects with type 1 diabetes for more than 50 years
Maddaloni, E., D’Eon, S., Hastings, S. M., TINSLEY, L. J., Napoli, N., Khamaisi, M., Bouxsein, M., Fouda, S. M. R., & Keenan, H. A. (2017) · Acta Diabetologica · doi:10.1007/s00592-017-0973-2 · Cited by 55 · see citing works
Bone Microarchitecture and Strength in Long-Standing Type 1 Diabetes
Sewing, L., Potasso, L., Baumann, S., Schenk, D., Gazozcu, F., Lippuner, K., KRAENZLIN, M. E., Zysset, P. K., & Meier, C. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4517 · Cited by 53 · see citing works
A human mission to Mars: Predicting the bone mineral density loss of astronauts
Axpe, E., Chan, D., Abegaz, M. F., Schreurs, A.-S., Alwood, J. S., Globus, R. K., & Appel, E. A. (2020) · PLOS ONE · doi:10.1371/journal.pone.0226434 · Cited by 51 · see citing works
“There is evidence that trabecular microarchitecture and bone geometry affect the bone strength [34].”
BackgroundCai, J., Li, W., Sun, T., Li, X., Luo, E., & Jing, D. (2018) · Osteoporosis International · doi:10.1007/s00198-018-4392-1 · Cited by 47 · see citing works
Mitchell, D. M., Caksa, S., Joseph, T., Bouxsein, M., & Misra, M. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgz221 · Cited by 48 · see citing works
Stemmler, F., Simón, D., Liphardt, A., Englbrecht, M., Rech, J., Hueber, A. J., Engelke, K., Schett, G. A., & Kleyer, A. (2018) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2017-212404 · Cited by 47 · see citing works
Wierzbicka, E., Świercz, A., Płudowski, P., Jaworski, M., & Szalecki, M. (2018) · Journal of Diabetes Research · doi:10.1155/2018/8121634 · Cited by 46 · see citing works
Bone turnover markers in children and adolescents with type 1 diabetes—A systematic review
Madsen, J. O. B., Jørgensen, N. R., Pociot, F., & Johannesen, J. (2019) · Pediatric Diabetes · doi:10.1111/pedi.12853 · Cited by 49 · see citing works
Self-citationChallenges to Improve Bone Healing Under Diabetic Conditions
Chen, Y., Zhou, Y., Lin, J., & Zhang, S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.861878 · Cited by 45 · see citing works
Li, O., Wei, P., Li, M., & Gao, F. (2019) · Acta Cirúrgica Brasileira · doi:10.1590/s0102-865020190050000002 · Cited by 44 · see citing works
Fracture Patterns in Type 1 and Type 2 Diabetes Mellitus: A Narrative Review of Recent Literature
van Hulten, V., Rasmussen, N. H., Driessen, J. H. M., Burden, A. M., Kvist, A. V., & van den Bergh, J. P. (2021) · Current Osteoporosis Reports · doi:10.1007/s11914-021-00715-6 · Cited by 41 · see citing works
Type 1 diabetes onset at young age is associated with compromised bone quality
Shah, V. N., Joshee, P., Sippl, R., Pyle, L., Vigers, T., Carpenter, R. D., Kohrt, W. M., & Snell‐Bergeon, J. K. (2019) · Bone · doi:10.1016/j.bone.2019.03.039 · Cited by 40 · see citing works
Large cortical bone pores in the tibia are associated with proximal femur strength
Iori, G., Schneider, J., Reisinger, A., Heyer, F. L., Peralta, L. M., Wyers, C. E., Gräsel, M., Barkmann, R., Glüer, C., van den Bergh, J. P., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0215405 · Cited by 39 · see citing works
Vilaça, T., Paggiosi, M., Walsh, J., Selvarajah, D., & Eastell, R. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4271 · Cited by 39 · see citing works
Cortical Bone Size Deficit in Adult Patients With Type 1 Diabetes Mellitus
Verroken, C., Pieters, W., Beddeleem, L., Goemaere, S., Zmierczak, H., Shadid, S., Kaufman, J., & Lapauw, B. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-00620 · Cited by 37 · see citing works
Dhaliwal, R., Foster, N. C., Boyle, C., Mukaddam, M. A., Weinstock, R. S., Rickels, M. R., Shah, V. N., & DiMeglio, L. A. (2018) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2018.08.016 · Cited by 36 · see citing works
Growth in patients with type 1 diabetes
Mitchell, D. M. (2016) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000310 · Cited by 35 · see citing works
Bone Microarchitecture in Type 1 Diabetes: It Is Complicated
Keenan, H. A., & Maddaloni, E. (2016) · Current Osteoporosis Reports · doi:10.1007/s11914-016-0338-8 · Cited by 34 · see citing works
Comparison of fracture risk between type 1 and type 2 diabetes: a comprehensive real-world data
Ha, J., Jeong, C., Han, K., Lim, Y., Kim, M. K., Kwon, H., Song, K., Kang, M. I., & Baek, K. (2021) · Osteoporosis International · doi:10.1007/s00198-021-06032-z · Cited by 34 · see citing works
Devaraja, J., Jacques, R., Paggiosi, M., Clark, C. D., & Dimitri, P. (2020) · JBMR Plus · doi:10.1002/jbm4.10422 · Cited by 33 · see citing works
Critical review of bone health, fracture risk and management of bone fragility in diabetes mellitus
Palui, R., Pramanik, S., Mondal, S., & Ray, S. (2021) · World Journal of Diabetes · doi:10.4239/wjd.v12.i6.706 · Cited by 31 · see citing works
Rasmussen, N. H., Dal, J., Kvist, A. V., van den Bergh, J. P., Jensen, M. H., & Vestergaard, P. (2023) · Bone · doi:10.1016/j.bone.2023.116753 · Cited by 30 · see citing works
Chen, F., Kuo, S., Lin, Y., Fan, C.-M., & Chen, J. (2018) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0000000000001185 · Cited by 28 · see citing works
Diabetes and fractures: new evidence of atypical femoral fractures?
Rasmussen, N. H.-H., Dal, J., de Vries, F., van den Bergh, J. P., Jensen, M. H., & Vestergaard, P. (2019) · Osteoporosis International · doi:10.1007/s00198-019-05224-y · Cited by 28 · see citing works
Travis, C., Srivastava, P. S., Hawke, T. J., & Kalaitzoglou, E. (2022) · Journal of Diabetes Research · doi:10.1155/2022/2650342 · Cited by 27 · see citing works
Jing, D., Yan, Z., Cai, J., Tong, S., Li, X., Guo, Z., & Luo, E. (2017) · Bone · doi:10.1016/j.bone.2017.10.001 · Cited by 28 · see citing works
Chen, S., Liu, D., He, S., Yang, L., Bao, Q., Qin, H., Liu, H., Zhao, Y., & Zong, Z. (2018) · Experimental & Molecular Medicine · doi:10.1038/s12276-018-0186-y · Cited by 28 · see citing works
Peng, S., Shi, S., Tao, G., Li, Y., Xiao, D., Wang, L., He, Q., Cai, X., & Xiao, J. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02163-6 · Cited by 27 · see citing works
Biochemical Markers of Bone Turnover in Older Adults With Type 1 Diabetes
Rubin, M. R., de Boer, I. H., Backlund, J. C., Arends, V. L., Gubitosi‐Klug, R., Wallia, A., Gregory, N. S., Barnie, A., Burghardt, A. J., Lachin, J. M., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac099 · Cited by 26 · see citing works
Shen, Y., Guo, S., Chen, G., Ding, Y., Wu, Y., & Tian, W. (2018) · Calcified Tissue International · doi:10.1007/s00223-018-0499-9 · Cited by 25 · see citing works
de Araújo, I. M., Moreira, M. L. M., & de Paula, F. J. A. (2022) · Archives of Endocrinology and Metabolism · doi:10.20945/2359-3997000000552 · Cited by 25 · see citing works
Bone Fragility in Diabetes and its Management: A Narrative Review
Leungsuwan, D. S., & Chandran, M. (2024) · Drugs · doi:10.1007/s40265-024-02078-5 · Cited by 24 · see citing works
Role of nitric oxide in type 1 diabetes-induced osteoporosis
Jeddi, S., Yousefzadeh, N., Kashfi, K., & Ghasemi, A. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114888 · Cited by 24 · see citing works
Bone deficits in children and youth with type 1 diabetes: A systematic review and meta-analysis
Zheng, Y., Abadi, M. R. H., Ghafouri, Z., Góes, S. M., Johnston, J. D., Nour, M. A., & Kontulainen, S. A. (2022) · Bone · doi:10.1016/j.bone.2022.116509 · Cited by 25 · see citing works
Bone Geometry, Quality, and Bone Markers in Children with Type 1 Diabetes Mellitus
Franceschi, R., Longhi, S., Cauvin, V., Fassio, A., Gallo, G., Lupi, F., Reinstadler, P., Fanolla, A., Gatti, D., & Radetti, G. (2017) · Calcified Tissue International · doi:10.1007/s00223-017-0381-1 · Cited by 24 · see citing works
The effects of diabetes therapy on bone: A clinical perspective
Kheniser, K. G., Santos, C. M. P., & Kashyap, S. R. (2018) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2018.04.005 · Cited by 24 · see citing works
Vilaça, T., Walsh, J., & Eastell, R. (2018) · Osteoporosis International · doi:10.1007/s00198-018-4717-0 · Cited by 24 · see citing works
Hua, Y., Bi, R., Zhang, Y., Xu, L., Guo, J., & Li, Y. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205503 · Cited by 24 · see citing works
Jin, S., Li, M., Wang, Q., Zeng, X., Xia, W., Yu, W., Guan, W., & Hsieh, E. (2021) · Arthritis Research & Therapy · doi:10.1186/s13075-021-02503-0 · Cited by 23 · see citing works
Thangavelu, T., Silverman, E., Akhter, M. P., Lyden, E. R., Recker, R. R., & Graeff-Armas, L. A. (2020) · Bone · doi:10.1016/j.bone.2020.115451 · Cited by 21 · see citing works
The effects of type 1 and type 2 diabetes mellitus on bone health in chronic kidney disease
Aleksova, J., Ebeling, P., & Elder, G. (2025) · Nature Reviews Endocrinology · doi:10.1038/s41574-024-01083-8 · Cited by 20 · see citing works
Bone microstructure and TBS in diabetes: what have we learned? A narrative review
Ferrari, S., Åkesson, K., Al‐Daghri, N. M., Biver, E., Chandran, M., Chevalley, T., Josse, R. G., Kendler, D. L., Lane, N. E., Makras, P., et al. (2025) · Osteoporosis International · doi:10.1007/s00198-025-07495-0 · Cited by 20 · see citing works
Resveratrol treatment promotes titanium implant osseointegration in diabetes mellitus rats
Hua, Y., Bi, R., Li, Z., & Li, Y. (2020) · Journal of Orthopaedic Research® · doi:10.1002/jor.24651 · Cited by 20 · see citing works
Dou, J., Wang, J., & Zhang, Q. (2021) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-021-00687-8 · Cited by 20 · see citing works
Wölfel, E. M., Schmidt, F. N., Scheidt, A. V., Siebels, A. K., Wulff, B., Mushumba, H., Ondruschka, B., Püschel, K., Scheijen, J. L. J. M., Schalkwijk, C. G., et al. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4706 · Cited by 20 · see citing works
Langdahl, J. H., Frederiksen, A. L., Hansen, S. J., Andersen, P. H., Yderstræde, K. B., Dunø, M., Vissing, J., & Frost, M. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3193 · Cited by 20 · see citing works
Self-citationBone tissue material composition is compromised in premenopausal women with Type 2 diabetes
Rokidi, S. G., Andrade, V. F. C., Borba, V. Z. C., Shane, E. J., Cohen, A., Zwerina, J., Paschalis, E. P., & Moreira, C. A. (2020) · Bone · doi:10.1016/j.bone.2020.115634 · Cited by 19 · see citing works
Hamilton, E. J., Drinkwater, J. J., Chubb, S. A. P., Rakic, V., Kamber, N., Zhu, K., Prince, R. L., Davis, W. A., & Davis, T. M. E. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00850 · Cited by 20 · see citing works
Xu, L., Yu, J., Wang, O., Hou, Y., Li, W., Zhang, H., Ping, F., Xu, Q., Li, Y., & Xia, W. (2020) · Endocrine · doi:10.1007/s12020-020-02480-5 · Cited by 19 · see citing works
Trabecular bone score in adults with type 1 diabetes: a meta-analysis
Bhattacharya, S., Nagendra, L., Chandran, M., Kapoor, N., Patil, P., Dutta, D., & Kalra, S. (2023) · Osteoporosis International · doi:10.1007/s00198-023-06935-z · Cited by 18 · see citing works
Walle, M., Duseja, A., Whittier, D. E., Vilaça, T., Paggiosi, M., Eastell, R., Müller, R., & Collins, C. J. (2024) · Journal of Bone and Mineral Research · doi:10.1093/jbmr/zjad014 · Cited by 18 · see citing works
Abdalrahaman, N., McComb, C., Foster, J. E., Lindsay, R. S., Drummond, R. S., McKay, G. A., Perry, C. G., & Ahmed, S. F. (2017) · Clinical Endocrinology · doi:10.1111/cen.13410 · Cited by 18 · see citing works
Aleksova, J., Milat, F., Kotowicz, M. A., Pasco, J. A., Schultz, C., Wong, P., Ebeling, P. R., & Elder, G. J. (2019) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfz195 · Cited by 18 · see citing works
Unaffected bone mineral density in Danish children and adolescents with type 1 diabetes
Madsen, J. O. B., Herskin, C. W., Zerahn, B., Jensen, A. K., Jørgensen, N. R., Olsen, B. S., Pociot, F., & Johannesen, J. (2019) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-019-01058-0 · Cited by 18 · see citing works
Self-citationInsulin resistance and skeletal health
Lei, W. S., & Kindler, J. M. (2022) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000738 · Cited by 17 · see citing works
Thong, E. P., Wong, P., Dev, A. T., Ebeling, P. R., Teede, H. J., & Milat, F. (2017) · Clinical Endocrinology · doi:10.1111/cen.13488 · Cited by 17 · see citing works
Understanding Bone Disease in Patients with Diabetic Kidney Disease: a Narrative Review
Hauge, S. C., Frost, M., & Hansen, D. (2020) · Current Osteoporosis Reports · doi:10.1007/s11914-020-00630-2 · Cited by 16 · see citing works
Self-citationGregory, N. S., Burghardt, A. J., Backlund, J. C., Rubin, M. R., Bebu, I., Braffett, B. H., Kenny, D. J., Link, T. M., Kazakia, G. J., Barnie, A., et al. (2023) · Diabetes Care · doi:10.2337/dc23-0839 · Cited by 15 · see citing works
Weber, D. R., O'Brien, K. O., & Schwartz, G. J. (2017) · Bone · doi:10.1016/j.bone.2017.09.001 · Cited by 14 · see citing works
Emerzian, S. R., Johannesdottir, F., Yu, E. W., & Bouxsein, M. (2024) · JBMR Plus · doi:10.1093/jbmrpl/ziae003 · Cited by 13 · see citing works
Imaging techniques to study diabetic bone disease
Carballido‐Gamio, J. (2022) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000749 · Cited by 13 · see citing works
Kuroda, T., Ishikawa, K., Nagai, T., Fukui, T., Hirano, T., & Inagaki, K. (2017) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2017.01.005 · Cited by 13 · see citing works
Maurotti, S., Russo, C., Musolino, V., Nucera, S., Gliozzi, M., Scicchitano, M., Bosco, F., Morittu, V. M., Ragusa, M., Mazza, E., et al. (2020) · Calcified Tissue International · doi:10.1007/s00223-020-00716-0 · Cited by 13 · see citing works
Sclerostin as a new target of diabetes-induced osteoporosis
Lǐ, Y., Luo, Y., Huang, D., & Peng, L. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1491066 · Cited by 13 · see citing works
Shitole, P., Choubey, A., Mondal, P., & Ghosh, R. (2021) · Materials Science and Engineering C · doi:10.1016/j.msec.2021.112011 · Cited by 12 · see citing works
Childhood type 1 diabetes is associated with abnormal bone development
Vora, K., Munns, C. F., Donaghue, K. C., Craig, M. E., BRIODY, J. N., & Benitez‐Aguirre, P. (2022) · Pediatric Diabetes · doi:10.1111/pedi.13367 · Cited by 12 · see citing works
Aleksova, J., Ebeling, P. R., Milat, F., & Elder, G. J. (2022) · European Journal of Endocrinology · doi:10.1530/eje-22-0687 · Cited by 12 · see citing works
- Authors
- Shanbhogue, V. V., Hansen, S., Frost, M., Jørgensen, N. R., Hermann, A. P., Henriksen, J. E., & Brixen, K.
- Affiliations
- University of Southern Denmark (DK)
- Corresponding author
- Shanbhogue, Vikram V
- ORCID
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-06-10
- Volume
- 30
- Issue
- 12
- Pages
- 2188-2199
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- OpenAlex
- W2109729276
- Cited by
- 183
- References
- 45
- Citations by year
- 2026: 6 · 2025: 16 · 2024: 15 · 2023: 17 · 2022: 18 · 2021: 15 · 2020: 17 · 2019: 21 · 2018: 23 · 2017: 22 · 2016: 11 · 2015: 2
- FWCI
- 19.90
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Journal of Bone and Mineral Research (publishedVersion)
- PubMed (publishedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion, other-oa)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- This work was supported by grants from The Research Foundation, Odense University Hospital. MN was supported by a grant from the Danish Council for Independent Research.
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Health Sciences › Medicine › Emergency Medicine › HIV-related health complications and treatments
- Keywords
- type 1 diabetes, diabetic microangiopathy, bone microarchitecture, bone mineral density, bone strength, bone remodeling, bone turnover markers, trabecular bone, cortical bone, bone geometry, ultradistal radius, tibia, trabecular separation, trabecular thickness, network heterogeneity, glycemic control
- MeSH terms
- Adolescent, Adult, Anthropometry, Bone and Bones, Child, Cross-Sectional Studies, Diabetes Mellitus, Type 1, Female, Humans, Male, Microcirculation, Middle Aged, Radius, Tibia, Tomography, X-Ray Computed, Vascular Diseases, Absorptiometry, Photon, Bone Density, Body Mass Index, Case-Control Studies, Bone Remodeling, Young Adult
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