{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T05:35:34Z","timestamp":1790919334194,"version":"4.1.0"},"reference-count":41,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2020,11,19]],"date-time":"2020-11-19T00:00:00Z","timestamp":1605744000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Introduction<\/jats:title>\n<jats:p>Studies show trabecular bone score (TBS) may provide information regarding bone quality independent of bone mineral density (BMD) in type 2 diabetes (DM2) patients. We analyzed our Southeast Asian severe osteoporotic hip fracture patients to study these differences.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>We conducted a retrospective cross-sectional analysis of subjects admitted to Changi General Hospital, Singapore with severe osteoporotic hip fractures from 2014\u20132017 who had BMD performed. Electronic records were reviewed and subjects were classified as having diabetes according to the WHO 2019 criteria. DM2 patients were classified according to their HbA1c into well controlled (HbA1c &lt; 7%) and poorly controlled (HbA1c \u2265 7%) DM2.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>Elderly patients with hip fractures present with average femur neck T scores at the osteoporotic range, however those with DM2 had higher BMD and TBS values compared to non DM2 patients. These differences were statistically significant in elderly women\u2014poorly controlled elderly DM2 women with hip fracture had the highest total hip T-score (-2.57 \u00b1 0.86) vs (-2.76 \u00b1 0.96) in well controlled DM2 and (-3.09 \u00b1 1.01) in non DM2 women with hip fracture, p &lt; 0.001. In contrast, TBS scores were lower in poorly controlled DM2 women with hip fracture compared to well controlled DM2 women with hip fracture (1.22 \u00b1 0.11) vs (1.24 \u00b1 0.09), but these were still significantly higher compared to non DM2 women with hip fracture (1.19 \u00b1 0.10), p &lt; 0.001. In elderly men with hip fractures, univariate analysis showed no statistically significant differences in TBS or hip or LS BMD between those with poorly controlled DM2, well controlled DM2 and non DM2. The differences in TBS and BMD remained significant in all DM2 women with hip fractures even after adjustments for potential confounders. Differences in TBS and BMD in poorly controlled DM2 men with hip fractures only became significant after accounting for potential confounders. However, upon inclusion of LS BMD into the multivariate model these differences were attenuated and remained significant only between elderly women with well controlled DM2 and non DM2 women with hip fractures.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>Elderly patients with DM2 and severe osteoporosis present with hip fractures at a higher BMD and TBS values compared to non DM2 patients. These differences were significant after adjustment for confounders in all DM2 women and poorly controlled DM2 men with hip fractures, TBS differences were attenuated with the inclusion LS BMD. Further studies are needed to ascertain differences in BMD and TBS in older Southeast Asian DM2 patients with variable glycemic control and severe osteoporosis.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0241616","type":"journal-article","created":{"date-parts":[[2020,11,19]],"date-time":"2020-11-19T18:44:13Z","timestamp":1605811453000},"page":"e0241616","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":19,"title":["Bone mineral density and trabecular bone score in elderly type 2 diabetes Southeast Asian patients with severe osteoporotic hip fractures"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3699-2406","authenticated-orcid":true,"given":"Linsey U.","family":"Gani","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kundan R.","family":"Saripalli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karen","family":"Fernandes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suet F.","family":"Leong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Koh T.","family":"Tsai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pei T.","family":"Tan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Le R.","family":"Chong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas F. 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Silva","year":"2015","journal-title":"J Clin Densitom"},{"issue":"3","key":"pone.0241616.ref018","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.jocd.2018.02.004","article-title":"Trabecular Bone Score Is a Valuable Addition to Bone Mineral Density for Bone Quality Assessment in Older Mexican American Women With Type 2 Diabetes","volume":"21","author":"N Rianon","year":"2018","journal-title":"J Clin Densitom"},{"issue":"2","key":"pone.0241616.ref019","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1016\/j.jocd.2016.04.003","article-title":"Ethnic Differences in Trabecular Bone Score","volume":"20","author":"RK Jain","year":"2017","journal-title":"J Clin Densitom"},{"issue":"2","key":"pone.0241616.ref020","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1210\/jc.2014-2047","article-title":"Trabecular bone score as an indicator for skeletal deterioration in diabetes","volume":"100","author":"JH Kim","year":"2015","journal-title":"J Clin Endocrinol 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Martineau","year":"2018","journal-title":"Bone"},{"issue":"3","key":"pone.0241616.ref024","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.jocd.2013.01.006","article-title":"Clinical factors associated with trabecular bone score","volume":"16","author":"WD Leslie","year":"2013","journal-title":"Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry"},{"issue":"4","key":"pone.0241616.ref025","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1016\/j.jocd.2015.05.068","article-title":"Age-Adjusted Dual X-ray Absorptiometry-Derived Trabecular Bone Score Curve for the Lumbar Spine in Thai Females and Males","volume":"19","author":"C Sritara","year":"2016","journal-title":"J Clin Densitom"},{"issue":"5","key":"pone.0241616.ref026","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1002\/jbmr.2407","article-title":"Bone Density, Microstructure and Strength in Obese and Normal Weight Men and Women in Younger 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Classification of Diabetes Mellitus 2019 WHO. 2019."},{"issue":"4","key":"pone.0241616.ref029","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1002\/jbmr.3640","article-title":"The Cost of Osteoporosis, Osteopenia, and Associated Fractures in Australia in 2017","volume":"34","author":"G Tatangelo","year":"2019","journal-title":"J Bone Miner Res"},{"issue":"1","key":"pone.0241616.ref030","doi-asserted-by":"crossref","first-page":"e000012","DOI":"10.1136\/bmjdrc-2013-000012","article-title":"Forecasting the burden of type 2 diabetes in Singapore using a demographic epidemiological model of Singapore","volume":"2","author":"TP Phan","year":"2014","journal-title":"BMJ Open Diabetes Research & Care"},{"issue":"11","key":"pone.0241616.ref031","doi-asserted-by":"crossref","first-page":"2837","DOI":"10.1007\/s00198-013-2384-8","article-title":"Generation and validation of a normative, age-specific reference curve for lumbar spine trabecular bone score (TBS) in French women","volume":"24","author":"R Dufour","year":"2013","journal-title":"Osteoporosis International"},{"issue":"2","key":"pone.0241616.ref032","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1210\/jc.2012-3118","article-title":"TBS (trabecular bone score) and diabetes-related fracture risk","volume":"98","author":"WD Leslie","year":"2013","journal-title":"J Clin Endocrinol Metab"},{"issue":"5","key":"pone.0241616.ref033","doi-asserted-by":"crossref","first-page":"E735","DOI":"10.1152\/ajpendo.00159.2005","article-title":"Is insulin an anabolic agent in bone? 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