{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T14:16:37Z","timestamp":1784556997980,"version":"3.55.0"},"reference-count":34,"publisher":"Bioscientifica","issue":"7","license":[{"start":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T00:00:00Z","timestamp":1682380800000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":["ec.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2023,4,25]]},"abstract":"<jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Radiotherapy-related insufficiency fractures (RRIFs) represent a common, burdensome consequence of pelvic radiotherapy. Their underlying mechanisms remain unclear, and data on the effect of osteoporosis are contradictory, with limited studies assessing bone mineral density (BMD) by dual-energy x-ray absorptiometry (DXA).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>BMD by DXA (Hologic) scan and fracture risk following pelvic RRIF were retrospectively assessed in 39 patients (median age 68 years) at a tertiary cancer centre. Patient characteristics and treatment history are presented narratively; correlations were explored using univariate regression analyses.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Additional cancer treatments included chemotherapy (\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u200931), surgery (\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u200920) and brachytherapy (\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u200919). Median interval between initiation of radiotherapy and RRIF was 11 (7.5\u201320.8) and that between RRIF and DXA 3 was (1\u20136) months. Three patients had normal BMD, 16 had osteopenia and 16 osteoporosis, following World Health Organization classification. Four patients were &lt;40 years at the time of DXA (all\n                      <jats:italic>Z<\/jats:italic>\n                      -scores &gt; \u20132). Median 10-year risk for hip and major osteoporotic fracture was 3.1% (1.5\u20135.7) and 11.5% (7.1\u201313.8), respectively. Only 33.3% of patients had high fracture risk (hip fracture &gt;4% and\/or major osteoporotic &gt;20%), and 31% fell above the intervention threshold per National Osteoporosis Guidelines Group (NOGG) guidance (2017). Higher BMD was predicted by lower pelvic radiotherapy dose (only in L3 and L4), concomitant chemotherapy and higher body mass index.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>At the time of RRIF, most patients did not have osteoporosis, some had normal BMD and overall had low fracture risk. Whilst low BMD is a probable risk factor, it is unlikely to be the main mechanism underlying RRIFs, and further studies are required to understand the predictive value of BMD.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1530\/ec-22-0328","type":"journal-article","created":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T10:01:54Z","timestamp":1682416914000},"update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-10","source":"Crossref","is-referenced-by-count":5,"title":["Radiotherapy-related insufficiency fractures and bone mineral density: what is the connection?"],"prefix":"10.1530","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9064-0532","authenticated-orcid":true,"given":"Victoria","family":"Chatzimavridou-Grigoriadou","sequence":"first","affiliation":[{"name":"Department of Endocrinology, Christie Hospital NHS Foundation Trust, Manchester, UK"},{"name":"Department of Endocrinology, University of Manchester, School of Medical Sciences, Manchester, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa H","family":"Barraclough","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, Christie Hospital NHS Foundation Trust, Manchester, UK"},{"name":"Department of Endocrinology, University of Manchester, School of Medical Sciences, Manchester, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rohit","family":"Kochhar","sequence":"additional","affiliation":[{"name":"Department of Clinical Oncology, Christie Hospital NHS Foundation Trust, Manchester, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucy","family":"Buckley","sequence":"additional","affiliation":[{"name":"Department of Radiology, Christie Hospital NHS Foundation Trust, Manchester, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nooreen","family":"Alam","sequence":"additional","affiliation":[{"name":"Department of Radiotherapy, Christie Hospital NHS Foundation Trust, Manchester, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0917-9743","authenticated-orcid":true,"given":"Claire E","family":"Higham","sequence":"additional","affiliation":[{"name":"Department of Endocrinology, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"416","reference":[{"key":"bib1","article-title":"CancerData on Radiotherapy delivery in England","unstructured":"NDRS & NHS Digital. CancerData on Radiotherapy delivery in England. (available at: https:\/\/www.cancerdata.nhs.uk\/radiotherapy)"},{"key":"bib2","article-title":"Cancer treatment & survivorship","unstructured":"American Cancer Society. Cancer treatment & survivorship. (available at: https:\/\/www.cancer.org\/content\/dam\/cancer-org\/research\/cancer-facts-and-statistics\/cancer-treatment-and-survivorship-facts-and-figures\/cancer-treatment-and-survivorship-facts-and-figures-2019-2021.pdf)"},{"key":"bib3","series-title":"Clinical Oncology","first-page":"668","article-title":"Bone health and pelvic radiotherapy","volume":"27","author":"Higham","year":"2015","unstructured":"Higham CE & Faithfull S. Bone health and pelvic radiotherapy. Clinical Oncology201527668\u2013678. (https:\/\/doi.org\/10.1016\/j.clon.2015.07.006)"},{"key":"bib4","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"1183","article-title":"Pelvic insufficiency fracture after pelvic radiotherapy for cervical cancer: analysis of risk factors","volume":"70","author":"Oh","year":"2008","unstructured":"Oh DHuh SJNam HPark WHan YLim DHAhn YCLee JWKim BGBae DS, Pelvic insufficiency fracture after pelvic radiotherapy for cervical cancer: analysis of risk factors. International Journal of Radiation Oncology, Biology, Physics2008701183\u20131188. (https:\/\/doi.org\/10.1016\/j.ijrobp.2007.08.005)"},{"key":"bib5","series-title":"Progress in Rehabilitation Medicine","article-title":"Walking disability in patients with pelvic insufficiency fracture after radiotherapy for uterine cervical cancer","volume":"1","author":"Kido","year":"2016","unstructured":"Kido AYoshida SShimoda EIshida YHasegawa MKobayashi HHonoki KHorikawa HTanaka Y. Walking disability in patients with pelvic insufficiency fracture after radiotherapy for uterine cervical cancer. Progress in Rehabilitation Medicine20161 20160009. (https:\/\/doi.org\/10.2490\/prm.20160009)"},{"key":"bib6","series-title":"JAMA","first-page":"1001","article-title":"Fatigue, insufficiency, and pathologic fractures","volume":"187","author":"Pentecost","year":"1964","unstructured":"Pentecost RLMurray RA & Brindley HH. Fatigue, insufficiency, and pathologic fractures. JAMA19641871001\u20131004. (https:\/\/doi.org\/10.1001\/jama.1964.03060260029006)"},{"key":"bib7","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"620","article-title":"Radiation-induced insufficiency fractures after pelvic irradiation for gynecologic malignancies: a systematic review","volume":"108","author":"Razavian","year":"2020","unstructured":"Razavian NLaucis ASun YSpratt DEOwen DSchonewolf CUppal SMaturen KE & Jolly S. Radiation-induced insufficiency fractures after pelvic irradiation for gynecologic malignancies: a systematic review. International Journal of Radiation Oncology, Biology, Physics2020108620\u2013634. (https:\/\/doi.org\/10.1016\/j.ijrobp.2020.05.013)"},{"key":"bib8","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"475","article-title":"Pelvic insufficiency fractures after external beam radiation therapy for gynecologic cancers: A meta-analysis and meta-regression of 3929 patients","volume":"106","author":"Sapienza","year":"2020","unstructured":"Sapienza LGSalcedo MPNing MSJhingran AKlopp AHCalsavara VFSchmeler KMLeite Gomes MJde Freitas Carvalho E & Baiocchi G. Pelvic insufficiency fractures after external beam radiation therapy for gynecologic cancers: A meta-analysis and meta-regression of 3929 patients. International Journal of Radiation Oncology, Biology, Physics2020106475\u2013484. (https:\/\/doi.org\/10.1016\/j.ijrobp.2019.09.012)"},{"key":"bib9","series-title":"Cancer","first-page":"2607","article-title":"Pelvic fractures and changes in bone mineral density after radiotherapy for cervical, endometrial, and vaginal cancer: a prospective study of 239 women","volume":"126","author":"Salcedo","year":"2020","unstructured":"Salcedo MPSood AKJhingran AEifel PJKlopp AHIyer RBFellman BMJimenez C & Schmeler KM. Pelvic fractures and changes in bone mineral density after radiotherapy for cervical, endometrial, and vaginal cancer: a prospective study of 239 women. Cancer20201262607\u20132613. (https:\/\/doi.org\/10.1002\/cncr.32807)"},{"key":"bib10","series-title":"Radiation Oncology Journal","first-page":"269","article-title":"Pelvic insufficiency fracture after radiotherapy in patients with cervical cancer in the era of PET\/CT","volume":"29","author":"Park","year":"2011","unstructured":"Park SHKim JCLee JE & Park IK. Pelvic insufficiency fracture after radiotherapy in patients with cervical cancer in the era of PET\/CT. Radiation Oncology Journal201129269\u2013276. (https:\/\/doi.org\/10.3857\/roj.2011.29.4.269)"},{"key":"bib11","series-title":"Gynecologic Oncology","first-page":"540","article-title":"Pelvic insufficiency fractures in patients with cervical and endometrial cancer treated with postoperative pelvic radiation","volume":"128","author":"Shih","year":"2013","unstructured":"Shih KKFolkert MRKollmeier MAAbu-Rustum NRSonoda YLeitao MMJrBarakat RR & Alektiar KM. Pelvic insufficiency fractures in patients with cervical and endometrial cancer treated with postoperative pelvic radiation. Gynecologic Oncology2013128540\u2013543. (https:\/\/doi.org\/10.1016\/j.ygyno.2012.12.021)"},{"key":"bib12","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"1158","article-title":"Bone density changes after radiation for extremity sarcomas: exploring the etiology of pathologic fractures","volume":"80","author":"Dhakal","year":"2011","unstructured":"Dhakal SChen JMcCance SRosier RO\u2019Keefe R & Constine LS. Bone density changes after radiation for extremity sarcomas: exploring the etiology of pathologic fractures. International Journal of Radiation Oncology, Biology, Physics2011801158\u20131163. (https:\/\/doi.org\/10.1016\/j.ijrobp.2010.04.012)"},{"key":"bib13","series-title":"Radiotherapy and Oncology","first-page":"239","article-title":"Changes in bone mineral density of lumbar spine after pelvic radiotherapy","volume":"62","author":"Chen","year":"2002","unstructured":"Chen HHWLee BFGuo HRSu WR & Chiu NT. Changes in bone mineral density of lumbar spine after pelvic radiotherapy. Radiotherapy and Oncology200262239\u2013242. (https:\/\/doi.org\/10.1016\/s0167-8140(0200002-6)"},{"key":"bib14","series-title":"Clinical Oncology","first-page":"44","article-title":"Bone density: is it affected by orchidectomy and radiotherapy given for stage I seminoma of the testis?","volume":"10","author":"Stutz","year":"1998","unstructured":"Stutz JABarry BPMaslanka WSokal MGreen DJ & Pearson D. Bone density: is it affected by orchidectomy and radiotherapy given for stage I seminoma of the testis?Clinical Oncology19981044\u201349. (https:\/\/doi.org\/10.1016\/S0936-6555(9880113-1)"},{"key":"bib15","series-title":"Clinics in Oncology","article-title":"Sacral insufficiency fracture following pelvic radiotherapy in gynaecological malignancies: development of a predictive model","volume":"27","author":"Mir","year":"2020","unstructured":"Mir RDragan ADMistry HBTsang YMPadhani AR & Hoskin P. Sacral insufficiency fracture following pelvic radiotherapy in gynaecological malignancies: development of a predictive model. Clinics in Oncology202027. (https:\/\/doi.org\/10.1016\/j.clon.2020.10.013)"},{"key":"bib16","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"694","article-title":"Fractures of the sacrum after chemoradiation for rectal carcinoma: incidence, risk factors, and radiographic evaluation","volume":"84","author":"Kim","year":"2012","unstructured":"Kim HJBoland PJMeredith DSLis EZhang ZShi WYamada YJ & Goodman KA. Fractures of the sacrum after chemoradiation for rectal carcinoma: incidence, risk factors, and radiographic evaluation. International Journal of Radiation Oncology, Biology, Physics201284694\u2013699. (https:\/\/doi.org\/10.1016\/j.ijrobp.2012.01.021)"},{"key":"bib17","series-title":"Strahlentherapie und Onkologie","article-title":"An easy way to determine bone mineral density and predict pelvic insufficiency fractures in patients treated with radiotherapy for cervical cancer","volume":"6","author":"Kurrumeli","year":"2020","unstructured":"Kurrumeli DOechsner MWeidenb\u00e4cher BBrambs CL\u00f6ffler MCombs SEBorm K & Duma MN. An easy way to determine bone mineral density and predict pelvic insufficiency fractures in patients treated with radiotherapy for cervical cancer. Strahlentherapie und Onkologie20206. (https:\/\/doi.org\/10.1007\/s00066-020-01690-0)"},{"key":"bib18","series-title":"Menopause","first-page":"416","article-title":"Bone mineral density after concurrent chemoradiation in patients with uterine cervical cancer","volume":"17","author":"Hwang","year":"2010","unstructured":"Hwang JHSong SHLee JKLee NW & Lee KW. Bone mineral density after concurrent chemoradiation in patients with uterine cervical cancer. Menopause201017416\u2013420. (https:\/\/doi.org\/10.1097\/gme.0b013e3181b9b11f)"},{"key":"bib19","series-title":"Cochrane Database of Systematic Reviews","first-page":"CD010604","article-title":"Pharmacological interventions for the prevention of insufficiency fractures and avascular necrosis associated with pelvic radiotherapy in adults","volume":"4","author":"van den Blink","year":"2018","unstructured":"van den Blink QUGarcez KHenson CCDavidson SE & Higham CE. Pharmacological interventions for the prevention of insufficiency fractures and avascular necrosis associated with pelvic radiotherapy in adults. Cochrane Database of Systematic Reviews20184CD010604. (https:\/\/doi.org\/10.1002\/14651858.CD010604.pub2)"},{"key":"bib20","series-title":"Radiation Research","first-page":"89","article-title":"Zoledronic acid prevents loss of trabecular bone after focal irradiation in mice","volume":"180","author":"Keenawinna","year":"2013","unstructured":"Keenawinna LOest MEMann KASpadaro J & Damron TA. Zoledronic acid prevents loss of trabecular bone after focal irradiation in mice. Radiation Research201318089\u201399. (https:\/\/doi.org\/10.1667\/RR3200.1)"},{"key":"bib21","series-title":"Bone","first-page":"101","article-title":"Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations","volume":"46","author":"Willey","year":"2010","unstructured":"Willey JSLivingston EWRobbins MEBourland JDTirado-Lee LSmith-Sielicki H & Bateman TA. Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations. Bone201046101\u2013111. (https:\/\/doi.org\/10.1016\/j.bone.2009.09.002)"},{"key":"bib22","series-title":"Bone","first-page":"33","article-title":"PTH1-34 alleviates radiotherapy-induced local bone loss by improving osteoblast and osteocyte survival","volume":"67","author":"Chandra","year":"2014","unstructured":"Chandra ALin TTribble MBZhu JAltman ARTseng WJZhang YAkintoye SOCengel KLiu XS, PTH1-34 alleviates radiotherapy-induced local bone loss by improving osteoblast and osteocyte survival. Bone20146733\u201340. (https:\/\/doi.org\/10.1016\/j.bone.2014.06.030)"},{"key":"bib23","series-title":"Osteoporosis International","first-page":"3","article-title":"European guidance for the diagnosis and management of osteoporosis in postmenopausal women","volume":"30","author":"Kanis","year":"2019","unstructured":"Kanis JACooper CRizzoli RReginster JY & Scientific Advisory Board of the European Society for Clinical and Economic Aspects of Osteoporosis (ESCEO) and the Committees of Scientific Advisors and National Societies of the International Osteoporosis Foundation (IOF). European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporosis International2019303\u201344. (https:\/\/doi.org\/10.1007\/s00198-018-4704-5)"},{"key":"bib24","series-title":"Journal of Clinical Oncology","first-page":"4225","article-title":"Addressing the role of obesity in endometrial cancer risk, prevention, and treatment","volume":"34","author":"Onstad","year":"2016","unstructured":"Onstad MASchmandt RE & Lu KH. Addressing the role of obesity in endometrial cancer risk, prevention, and treatment. Journal of Clinical Oncology2016344225\u20134230. (https:\/\/doi.org\/10.1200\/JCO.2016.69.4638)"},{"key":"bib25","series-title":"Nutrition Research","first-page":"1","article-title":"Obesity is a concern for bone health with aging","volume":"39","author":"Shapses","year":"2017","unstructured":"Shapses SAPop LC & Wang Y. Obesity is a concern for bone health with aging. Nutrition Research2017391\u201313. (https:\/\/doi.org\/10.1016\/j.nutres.2016.12.010)"},{"key":"bib26","series-title":"Journal of Clinical Endocrinology and Metabolism","first-page":"2562","article-title":"Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study","volume":"98","author":"Cohen","year":"2013","unstructured":"Cohen ADempster DWRecker RRLappe JMZhou HZwahlen AM\u00fcller RZhao BGuo XLang T, Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. Journal of Clinical Endocrinology and Metabolism2013982562\u20132572. (https:\/\/doi.org\/10.1210\/jc.2013-1047)"},{"key":"bib27","series-title":"Japanese Journal of Radiology","first-page":"93","article-title":"Predictive factors of posttreatment fracture by definitive radiotherapy for uterine cervical cancer","volume":"39","author":"Ishikawa","year":"2021","unstructured":"Ishikawa KYamashiro TAriga TToita TKudaka WHeianna JMaemoto HKusada TMakino WAoki Y, Predictive factors of posttreatment fracture by definitive radiotherapy for uterine cervical cancer. Japanese Journal of Radiology20213993\u201399. (https:\/\/doi.org\/10.1007\/s11604-020-01039-8)"},{"key":"bib28","series-title":"Anticancer Research","first-page":"361","article-title":"Risk factors for sacral insufficiency fractures in cervical cancer after whole pelvic radiation therapy","volume":"39","author":"Sakaguchi","year":"2019","unstructured":"Sakaguchi MMaebayashi TAizawa T & Ishibashi N. Risk factors for sacral insufficiency fractures in cervical cancer after whole pelvic radiation therapy. Anticancer Research201939361\u2013367. (https:\/\/doi.org\/10.21873\/anticanres.13120)"},{"key":"bib29","series-title":"Cancer Medicine","first-page":"3639","article-title":"Increased risk of pelvic fracture after radiotherapy in rectal cancer survivors: a propensity matched study","volume":"8","author":"Kang","year":"2019","unstructured":"Kang YMChao TFWang TH & Hu YW. Increased risk of pelvic fracture after radiotherapy in rectal cancer survivors: a propensity matched study. Cancer Medicine201983639\u20133647. (https:\/\/doi.org\/10.1002\/cam4.2030)"},{"key":"bib30","series-title":"Practical Radiation Oncology","first-page":"19","article-title":"Long-term outcomes using adjuvant pelvic intensity modulated radiation therapy (IMRT) for endometrial carcinoma","volume":"7","author":"He","year":"2017","unstructured":"He SGill BSHeron DEKelley JLSukumvanich POlawaiye ABEdwards RPComerci J & Beriwal S. Long-term outcomes using adjuvant pelvic intensity modulated radiation therapy (IMRT) for endometrial carcinoma. Practical Radiation Oncology2017719\u201325. (https:\/\/doi.org\/10.1016\/j.prro.2016.06.005)"},{"key":"bib31","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"973","article-title":"Severe late toxicities following concomitant chemoradiotherapy compared to radiotherapy alone in cervical cancer: an inter-era analysis","volume":"84","author":"Gondi","year":"2012","unstructured":"Gondi VBentzen SMSklenar KLDunn EFPetereit DGTannehill SPStraub M & Bradley KA. Severe late toxicities following concomitant chemoradiotherapy compared to radiotherapy alone in cervical cancer: an inter-era analysis. International Journal of Radiation Oncology, Biology, Physics201284973\u2013982. (https:\/\/doi.org\/10.1016\/j.ijrobp.2012.01.064)"},{"key":"bib32","series-title":"Cancer Treat Res Commun","first-page":"3","article-title":"Comparative assessment of late toxicity in patients of carcinoma cervix treated by radiotherapy versus chemo-radiotherapy - Minimum 5 years follow up","volume":"14","author":"Misra","year":"2018","unstructured":"Misra SLal PKumar Ep SRastogi NTiwari ASingh SDas KJM & Kumar S. Comparative assessment of late toxicity in patients of carcinoma cervix treated by radiotherapy versus chemo-radiotherapy - Minimum 5 years follow up. Cancer Treat Res Commun20181430\u201336."},{"key":"bib33","series-title":"Cancer","first-page":"625","article-title":"Pelvic fractures after radiotherapy for cervical cancer: implications for survivors","volume":"116","author":"Schmeler","year":"2010","unstructured":"Schmeler KMJhingran AIyer RBSun CCEifel PJSoliman PTRamirez PTFrumovitz MBodurka DC & Sood AK. Pelvic fractures after radiotherapy for cervical cancer: implications for survivors. Cancer2010116625\u2013630. (https:\/\/doi.org\/10.1002\/cncr.24811)"},{"key":"bib34","series-title":"International Journal of Radiation Oncology, Biology, Physics","first-page":"1032","article-title":"Risk factors for pelvic insufficiency fractures in locally advanced cervical cancer following intensity modulated radiation therapy","volume":"97","author":"Ramlov","year":"2017","unstructured":"Ramlov APedersen EMR\u00f8hl LWorm EFokdal LLindegaard JC & Tanderup K. Risk factors for pelvic insufficiency fractures in locally advanced cervical cancer following intensity modulated radiation therapy. International Journal of Radiation Oncology, Biology, Physics2017971032\u20131039. 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