{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T21:45:50Z","timestamp":1792014350536,"version":"4.4.0"},"reference-count":46,"publisher":"Oxford University Press (OUP)","issue":"11","license":[{"start":{"date-parts":[[2018,6,28]],"date-time":"2018-06-28T00:00:00Z","timestamp":1530144000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"},{"start":{"date-parts":[[2018,7,16]],"date-time":"2018-07-16T00:00:00Z","timestamp":1531699200000},"content-version":"vor","delay-in-days":18,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":["asbmr.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2018,11,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n               <jats:sec>\n                  <jats:title>\u2003<\/jats:title>\n                  <jats:p>Type 2 diabetes is a risk factor for fracture independent of FRAX (fracture risk assessment) probability. We directly compared four proposed methods to improve the performance of FRAX for type 2 diabetes by: (1) including the rheumatoid arthritis (RA) input to FRAX; (2) making a trabecular bone score (TBS) adjustment to FRAX; (3) reducing the femoral neck T-score input to FRAX by 0.5 SD; and (4) increasing the age input to FRAX by 10 years. We examined major osteoporotic fractures (MOFs) and hip fractures (HFs) over a mean of 8.3 years observation among 44,543 women and men 40 years of age or older (4136 with diabetes) with baseline lumbar spine and hip DXA from 1999 through 2016. Controlled for unadjusted FRAX probability, diabetes was associated with an increased risk for MOFs and HFs. All four FRAX adjustments attenuated the effect of diabetes, but a residual effect of diabetes was seen on MOF risk after TBS adjustment, and on HF risk after the RA and TBS adjustments. Among those with diabetes, unadjusted FRAX risk underestimated MOF (observed\/predicted ratio 1.15; 95% CI, 1.03 to 1.28), but this was no longer significant after applying the diabetes adjustments. HF risk was more severely underestimated (observed\/predicted ratio 1.85; 95% CI, 1.51 to 2.20) and was only partially corrected with the diabetes adjustments (still significant for the RA and TBS adjustments). Among those with diabetes, there was moderate reclassification based upon a fixed MOF cut-off of 20% (4.1% to 7.1%) or fixed HF cut-off of 3% (5.7% to 16.5%). Net reclassification improvement increased for MOF with each of the diabetes adjustments (range 3.9% to 5.6% in the diabetes subgroup). In conclusion, each of the proposed methods for addressing limitations in the ability of FRAX to assess fracture risk in individuals with diabetes was found to improve performance, though no single method was optimal in all settings. \u00a9 2018 American Society for Bone and Mineral Research.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1002\/jbmr.3538","type":"journal-article","created":{"date-parts":[[2018,6,28]],"date-time":"2018-06-28T17:59:33Z","timestamp":1530208773000},"page":"1923-1930","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":165,"title":["Comparison of Methods for Improving Fracture Risk Assessment in Diabetes: The Manitoba BMD Registry"],"prefix":"10.1093","volume":"33","author":[{"given":"William D","family":"Leslie","sequence":"first","affiliation":[{"name":"Department of Internal MedicineUniversity of ManitobaWinnipegManitobaCanada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helena","family":"Johansson","sequence":"additional","affiliation":[{"name":"Centre for Metabolic Bone DiseasesUniversity of Sheffield Medical SchoolSheffieldUK"},{"name":"Institute for Health and AgingCatholic University of AustraliaMelbourneAustralia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eugene V","family":"McCloskey","sequence":"additional","affiliation":[{"name":"Centre for Metabolic Bone DiseasesUniversity of Sheffield Medical SchoolSheffieldUK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas C","family":"Harvey","sequence":"additional","affiliation":[{"name":"NIHR Southampton Biomedical Research CentreUniversity of Southampton and University Hospital Southampton NHS Foundation TrustSouthamptonUK"},{"name":"MRC Lifecourse Epidemiology UnitUniversity of SouthamptonSouthamptonUK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John A","family":"Kanis","sequence":"additional","affiliation":[{"name":"Centre for Metabolic Bone DiseasesUniversity of Sheffield Medical SchoolSheffieldUK"},{"name":"Institute for Health and AgingCatholic University of AustraliaMelbourneAustralia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Didier","family":"Hans","sequence":"additional","affiliation":[{"name":"Bone and Joint DepartmentLausanne University HospitalLausanneSwitzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2018,6,28]]},"reference":[{"issue":"6","key":"2024021014283272400_jbmr3538-bib-0001","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1016\/0002-9343(93)90218-E","article-title":"Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis","volume":"94","year":"1993","journal-title":"Am J Med"},{"issue":"3","key":"2024021014283272400_jbmr3538-bib-0002","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/0168-8510(95)00785-7","article-title":"Health policy on bone density measurement technology in Sweden and Australia","volume":"35","author":"Marshall","year":"1996","journal-title":"Health Policy"},{"issue":"6","key":"2024021014283272400_jbmr3538-bib-0003","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1503\/cmaj.070234","article-title":"Low bone mineral density and fracture burden in postmenopausal women","volume":"177","author":"Cranney","year":"2007","journal-title":"CMAJ"},{"issue":"11","key":"2024021014283272400_jbmr3538-bib-0004","doi-asserted-by":"crossref","first-page":"1947","DOI":"10.1359\/jbmr.2003.18.11.1947","article-title":"BMD at multiple sites and risk of fracture of multiple types: long-term results from the Study of Osteoporotic Fractures","volume":"18","author":"Stone","year":"2003","journal-title":"J Bone Miner Res"},{"key":"2024021014283272400_jbmr3538-bib-0005","author":"Kanis","year":"2007"},{"issue":"1","key":"2024021014283272400_jbmr3538-bib-0006","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s11657-016-0278-z","article-title":"A systematic review of intervention thresholds based on FRAX: a report prepared for the National Osteoporosis Guideline Group and the International Osteoporosis Foundation","volume":"11","author":"Kanis","year":"2016","journal-title":"Arch Osteoporos"},{"issue":"11","key":"2024021014283272400_jbmr3538-bib-0007","doi-asserted-by":"crossref","first-page":"2231","DOI":"10.1002\/jbmr.1759","article-title":"Type 2 diabetes and bone","volume":"27","author":"Leslie","year":"2012","journal-title":"J Bone Miner Res"},{"issue":"21","key":"2024021014283272400_jbmr3538-bib-0008","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.1001\/jama.2011.715","article-title":"Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes","volume":"305","author":"Schwartz","year":"2011","journal-title":"JAMA"},{"issue":"2","key":"2024021014283272400_jbmr3538-bib-0009","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1002\/jbmr.556","article-title":"FRAX underestimates fracture risk in patients with diabetes","volume":"27","author":"Giangregorio","year":"2012","journal-title":"J Bone Miner Res"},{"key":"2024021014283272400_jbmr3538-bib-0010","author":"Lecka-Czernik","year":"2015"},{"issue":"4","key":"2024021014283272400_jbmr3538-bib-0011","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1038\/nrendo.2016.153","article-title":"Mechanisms of diabetes mellitus-induced bone fragility","volume":"13","author":"Napoli","year":"2017","journal-title":"Nat Rev Endocrinol"},{"issue":"1","key":"2024021014283272400_jbmr3538-bib-0012","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.ecl.2016.09.010","article-title":"Diabetes and bone disease","volume":"46","author":"Schacter","year":"2017","journal-title":"Endocrinol Metab Clin North Am"},{"issue":"6 Suppl","key":"2024021014283272400_jbmr3538-bib-0013","first-page":"JS10","article-title":"Revisiting the Manitoba Centre for Health Policy and Evaluation and its population-based health information system","volume":"37","author":"Roos","year":"1999","journal-title":"Med Care"},{"key":"2024021014283272400_jbmr3538-bib-0014","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1186\/1471-2458-12-301","article-title":"Osteoporosis-related fracture case definitions for population-based administrative data","volume":"12","author":"Lix","year":"2012","journal-title":"BMC Public Health"},{"key":"2024021014283272400_jbmr3538-bib-0015","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1007\/s11657-013-0143-2","article-title":"Canadian Chronic Disease Surveillance System Osteoporosis Working Group. Use of administrative data for national surveillance of osteoporosis and related fractures in Canada: results from a feasibility study","volume":"8","author":"O'Donnell","year":"2013","journal-title":"Arch Osteoporos"},{"issue":"7","key":"2024021014283272400_jbmr3538-bib-0016","doi-asserted-by":"crossref","first-page":"2137","DOI":"10.1007\/s00198-010-1470-4","article-title":"Secular decreases in fracture rates 1986-2006 for Manitoba, Canada: a population-based analysis","volume":"22","author":"Leslie","year":"2011","journal-title":"Osteoporos Int"},{"issue":"11","key":"2024021014283272400_jbmr3538-bib-0017","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.1345\/aph.18117","article-title":"Validation of an electronic, population-based prescription database","volume":"32","author":"Kozyrskyj","year":"1998","journal-title":"Ann Pharmacother"},{"issue":"3","key":"2024021014283272400_jbmr3538-bib-0018","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1385\/JCD:6:3:275","article-title":"Establishing a regional bone density program: lessons from the Manitoba experience","volume":"6","author":"Leslie","year":"2003","journal-title":"J Clin Densitom"},{"issue":"1","key":"2024021014283272400_jbmr3538-bib-0019","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1385\/JCD:8:1:025","article-title":"Construction and validation of a population-based bone densitometry database","volume":"8","author":"Leslie","year":"2005","journal-title":"J Clin Densitom"},{"issue":"11","key":"2024021014283272400_jbmr3538-bib-0020","doi-asserted-by":"crossref","first-page":"1761","DOI":"10.1359\/jbmr.1997.12.11.1761","article-title":"Prevalence of low femoral bone density in older U.S. adults from NHANES III","volume":"12","author":"Looker","year":"1997","journal-title":"J Bone Miner Res"},{"key":"2024021014283272400_jbmr3538-bib-0021","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.bone.2015.05.016","article-title":"Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice","volume":"78","author":"Harvey","year":"2015","journal-title":"Bone"},{"issue":"3","key":"2024021014283272400_jbmr3538-bib-0022","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.jocd.2015.06.008","article-title":"Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions Part 2: trabecular bone score","volume":"18","author":"Silva","year":"2015","journal-title":"J Clin Densitom"},{"issue":"7","key":"2024021014283272400_jbmr3538-bib-0023","doi-asserted-by":"crossref","first-page":"1568","DOI":"10.1002\/jbmr.3124","article-title":"Clinical utility of using lumbar spine trabecular bone score to adjust fracture probability: the Manitoba BMD cohort","volume":"32","author":"Martineau","year":"2017","journal-title":"J Bone Miner Res"},{"issue":"11","key":"2024021014283272400_jbmr3538-bib-0024","doi-asserted-by":"crossref","first-page":"2350","DOI":"10.1002\/jbmr.123","article-title":"Independent clinical validation of a Canadian FRAX tool: fracture prediction and model calibration","volume":"25","author":"Leslie","year":"2010","journal-title":"J Bone Miner Res"},{"issue":"7","key":"2024021014283272400_jbmr3538-bib-0025","doi-asserted-by":"crossref","first-page":"1675","DOI":"10.1002\/jbmr.2204","article-title":"The importance of previous fracture site on osteoporosis diagnosis and incident fractures in women","volume":"29","author":"Morin","year":"2014","journal-title":"J Bone Miner Res"},{"key":"2024021014283272400_jbmr3538-bib-0026","first-page":"1","article-title":"Accuracy of offspring-reported parental hip fractures: a novel population-based parent\u2013offspring record linkage study","author":"Lix","year":"2017","journal-title":"Am J Epidemiol"},{"issue":"3","key":"2024021014283272400_jbmr3538-bib-0027","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1007\/s00198-010-1465-1","article-title":"Fracture prediction and calibration of a Canadian FRAX(R) tool: a population-based report from CaMos","volume":"22","author":"Fraser","year":"2011","journal-title":"Osteoporos Int"},{"issue":"8","key":"2024021014283272400_jbmr3538-bib-0028","doi-asserted-by":"crossref","first-page":"807","DOI":"10.2337\/diacare.19.8.807","article-title":"Incidence and prevalence of diabetes in Manitoba, 1986\u20131991","volume":"19","author":"Blanchard","year":"1996","journal-title":"Diabetes Care"},{"issue":"1","key":"2024021014283272400_jbmr3538-bib-0029","doi-asserted-by":"crossref","first-page":"31","DOI":"10.24095\/hpcdp.29.1.04","article-title":"Population-based data sources for chronic disease surveillance","volume":"29","author":"Lix","year":"2008","journal-title":"Chronic Dis Can"},{"issue":"11","key":"2024021014283272400_jbmr3538-bib-0030","doi-asserted-by":"crossref","first-page":"4489","DOI":"10.1210\/jc.2016-2569","article-title":"Longer duration of diabetes strongly impacts fracture risk assessment: the Manitoba BMD Cohort","volume":"101","author":"Majumdar","year":"2016","journal-title":"J Clin Endocrinol Metab"},{"key":"2024021014283272400_jbmr3538-bib-0031","doi-asserted-by":"crossref","first-page":"e3427","DOI":"10.1136\/bmj.e3427","article-title":"Derivation and validation of updated QFracture algorithm to predict risk of osteoporotic fracture in primary care in the United Kingdom: prospective open cohort study","volume":"344","author":"Hippisley-Cox","year":"2012","journal-title":"BMJ"},{"key":"2024021014283272400_jbmr3538-bib-0032","first-page":"45","author":"Leslie","year":"2015"},{"issue":"2","key":"2024021014283272400_jbmr3538-bib-0033","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1210\/jc.2012-3118","article-title":"Manitoba Bone Density P. TBS (trabecular bone score) and diabetes-related fracture risk","volume":"98","author":"Leslie","year":"2013","journal-title":"J Clin Endocrinol Metab"},{"issue":"7","key":"2024021014283272400_jbmr3538-bib-0034","doi-asserted-by":"crossref","first-page":"1969","DOI":"10.1007\/s00198-014-2704-7","article-title":"Bone quality assessment in type 2 diabetes mellitus","volume":"25","author":"Dhaliwal","year":"2014","journal-title":"Osteoporos Int"},{"issue":"2","key":"2024021014283272400_jbmr3538-bib-0035","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":"Kim","year":"2015","journal-title":"J Clin Endocrinol Metab"},{"issue":"4","key":"2024021014283272400_jbmr3538-bib-0036","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.jocd.2016.04.001","article-title":"Trabecular bone score (TBS) and TBS-adjusted fracture risk assessment tool are potential supplementary tools for the discrimination of morphometric vertebral fractures in postmenopausal women with type 2 diabetes","volume":"19","author":"Choi","year":"2016","journal-title":"J Clin Densitom"},{"issue":"1","key":"2024021014283272400_jbmr3538-bib-0037","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1007\/s00223-017-0330-z","article-title":"Trabecular bone score in men and women with impaired fasting glucose and diabetes","volume":"102","author":"Holloway","year":"2018","journal-title":"Calcif Tissue Int"},{"issue":"5","key":"2024021014283272400_jbmr3538-bib-0038","doi-asserted-by":"crossref","first-page":"940","DOI":"10.1002\/jbmr.2734","article-title":"A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX","volume":"31","author":"McCloskey","year":"2016","journal-title":"J Bone Miner Res"},{"issue":"6","key":"2024021014283272400_jbmr3538-bib-0039","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1007\/s00223-015-9980-x","article-title":"Adjusting fracture probability by trabecular bone score","volume":"96","author":"McCloskey","year":"2015","journal-title":"Calcif Tissue Int"},{"issue":"7","key":"2024021014283272400_jbmr3538-bib-0040","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1038\/sj.bjc.6602102","article-title":"A note on competing risks in survival data analysis","volume":"91","author":"Satagopan","year":"2004","journal-title":"Br J Cancer"},{"issue":"2","key":"2024021014283272400_jbmr3538-bib-0041","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1007\/s00198-012-2051-5","article-title":"Manitoba Bone Density P. Competing mortality and fracture risk assessment","volume":"24","author":"Leslie","year":"2013","journal-title":"Osteoporos Int"},{"issue":"10","key":"2024021014283272400_jbmr3538-bib-0042","doi-asserted-by":"crossref","first-page":"2359","DOI":"10.1007\/s00198-014-2794-2","article-title":"Clinician's guide to prevention and treatment of osteoporosis","volume":"25","author":"Cosman","year":"2014","journal-title":"Osteoporos Int"},{"issue":"2","key":"2024021014283272400_jbmr3538-bib-0043","doi-asserted-by":"crossref","first-page":"122","DOI":"10.7326\/M13-1522","article-title":"Net reclassification improvement: computation, interpretation, and controversies: a literature review and clinician's guide","volume":"160","author":"Leening","year":"2014","journal-title":"Ann Intern Med"},{"issue":"2","key":"2024021014283272400_jbmr3538-bib-0044","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1002\/sim.2929","article-title":"Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond","volume":"27","author":"Pencina","year":"2008","journal-title":"Stat Med"},{"issue":"4","key":"2024021014283272400_jbmr3538-bib-0045","doi-asserted-by":"crossref","first-page":"R127","DOI":"10.1530\/EJE-15-0820","article-title":"Diabetes Working Group. Mechanisms and evaluation of bone fragility in type 1 diabetes mellitus","volume":"174","author":"Hough","year":"2016","journal-title":"Eur J Endocrinol"},{"issue":"4","key":"2024021014283272400_jbmr3538-bib-0046","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1007\/s00198-006-0253-4","article-title":"Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes\u2014a meta-analysis","volume":"18","author":"Vestergaard","year":"2007","journal-title":"Osteoporos Int"}],"container-title":["Journal of Bone and Mineral Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fjbmr.3538","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/jbmr.3538","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/jbmr.3538","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/33\/11\/1923\/56649051\/jbmr3538.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/33\/11\/1923\/56649051\/jbmr3538.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,13]],"date-time":"2024-03-13T15:02:21Z","timestamp":1710342141000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jbmr\/article\/33\/11\/1923-1930\/7605127"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,6,28]]},"references-count":46,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2018,6,28]]},"published-print":{"date-parts":[[2018,11,1]]}},"URL":"https:\/\/doi.org\/10.1002\/jbmr.3538","relation":{},"ISSN":["0884-0431","1523-4681"],"issn-type":[{"value":"0884-0431","type":"print"},{"value":"1523-4681","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2018,11,1]]},"published":{"date-parts":[[2018,6,28]]},"assertion":[{"value":"2018-02-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-06-22","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-07-16","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}