{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T17:46:38Z","timestamp":1792691198972,"version":"4.5.0"},"reference-count":37,"publisher":"Georg Thieme Verlag KG","issue":"11","license":[{"start":{"date-parts":[[2021,11,4]],"date-time":"2021-11-04T00:00:00Z","timestamp":1635984000000},"content-version":"vor","delay-in-days":3,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Geburtshilfe Frauenheilkd"],"published-print":{"date-parts":[[2021,11]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>\n          Objective Leiomyoma with bizarre nuclei (LBN) is a variant of uterine leiomyoma, which has replaced the previous category of \u201catypical leiomyoma\u201d and must be distinguished from smooth muscle tumors of uncertain malignant potential (STUMP). However, previously published series of \u201catypical leiomyoma\u201d might have included both LBN and STUMP, due to the lack of strict diagnostic criteria. Based on such hypothesis, we aimed to define the risk of recurrence in LBN.<\/jats:p><jats:p>\n          Study Design A systematic review and meta-analysis was performed by searching 4 electronic databases for all studies assessing the outcome of patients with \u201catypical leiomyoma\u201d or LBN. The pooled absolute risk of recurrence was calculated. The included studies were subdivided into two subgroups based on the criteria used: \u201cLBN\u2009+\u2009STUMP\u201d or \u201cLBN-only\u201d.<\/jats:p><jats:p>\n          Results Twelve studies with 433 patients were included. The pooled risk of recurrence was 5.5% overall. The funnel plot showed two cluster of studies which superimposed to the two subgroups. In the LBN\u2009+\u2009STUMP cluster\/subgroup, the pooled risk of recurrence was 7.7%. In the LBN-only cluster\/subgroup, the pooled risk of recurrence was 1.9%. Statistical heterogeneity was null in all analyses.<\/jats:p><jats:p>\n          Conclusion Our results show a risk of recurrence of 1.9% for LBN; higher recurrence rates in older studies are likely due to the inclusion of STUMPs.<\/jats:p>","DOI":"10.1055\/a-1533-1651","type":"journal-article","created":{"date-parts":[[2021,11,4]],"date-time":"2021-11-04T23:41:15Z","timestamp":1636069275000},"page":"1217-1223","source":"Crossref","is-referenced-by-count":14,"title":["Risk of Recurrence in Uterine Leiomyoma with Bizarre Nuclei: a Systematic Review and Meta-Analysis"],"prefix":"10.1055","volume":"81","author":[{"given":"Antonio","family":"Travaglino","sequence":"additional","affiliation":[{"name":"Anatomic Pathology Unit, Department of Advanced Biomedical Sciences, School of Medicine, University of Naples Federico II, Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Raffone","sequence":"additional","affiliation":[{"name":"Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy"},{"name":"Division of Gynaecology and Human Reproduction Physiopathology, Department of Medical and Surgical Sciences (DIMEC), IRCCS Azienda Ospedaliero-Univeristaria di Bologna, S. Orsola Hospital, University of Bologna, Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela","family":"Santoro","sequence":"additional","affiliation":[{"name":"Pathology Unit, Department of Woman and Child Health, Agostino Gemelli University Polyclinic, Catholic University of the Sacred Heart, Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diego","family":"Raimondo","sequence":"additional","affiliation":[{"name":"Division of Gynaecology and Human Reproduction Physiopathology, Department of Medical and Surgical Sciences (DIMEC), IRCCS Azienda Ospedaliero-Univeristaria di Bologna, S. Orsola Hospital, University of Bologna, Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco Paolo","family":"Improda","sequence":"additional","affiliation":[{"name":"Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federica","family":"Cariati","sequence":"additional","affiliation":[{"name":"CEINGE-Biotecnologie Avanzate, Naples, Italy"},{"name":"Fertility Unit, Maternal-Child Department, AOU Policlinico Federico II, Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margot","family":"De Marco","sequence":"additional","affiliation":[{"name":"Department of Medicine, Surgery and Odontology Schola Medica Salernitana, University of Salerno, Baronissi, SA, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Casadio","sequence":"additional","affiliation":[{"name":"Division of Gynaecology and Human Reproduction Physiopathology, Department of Medical and Surgical Sciences (DIMEC), IRCCS Azienda Ospedaliero-Univeristaria di Bologna, S. Orsola Hospital, University of Bologna, Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renato","family":"Seracchioli","sequence":"additional","affiliation":[{"name":"Division of Gynaecology and Human Reproduction Physiopathology, Department of Medical and Surgical Sciences (DIMEC), IRCCS Azienda Ospedaliero-Univeristaria di Bologna, S. Orsola Hospital, University of Bologna, Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fulvio","family":"Zullo","sequence":"additional","affiliation":[{"name":"Gynecology and Obstetrics Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, School of Medicine, University of Naples Federico II, Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luigi","family":"Insabato","sequence":"additional","affiliation":[{"name":"Anatomic Pathology Unit, Department of Advanced Biomedical Sciences, School of Medicine, University of Naples Federico II, Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gian Franco","family":"Zannoni","sequence":"additional","affiliation":[{"name":"Division of Gynaecology and Human Reproduction Physiopathology, Department of Medical and Surgical Sciences (DIMEC), IRCCS Azienda Ospedaliero-Univeristaria di Bologna, S. Orsola Hospital, University of Bologna, Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"194","published-online":{"date-parts":[[2021,11,4]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1002\/nbm.1540","article-title":"Metabolic profile of intact tissue from uterine leiomyomas using high-resolution magic-angle-spinning 1H NMR spectroscopy","volume":"23","author":"P Mazzei","year":"2010","journal-title":"NMR Biomed"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.ejogrb.2009.02.006","article-title":"Leiomyoma pseudocapsule after pre-surgical treatment with gonadotropin-releasing hormone agonists: relationship between clinical features and immunohistochemical changes","volume":"144","author":"M De Falco","year":"2009","journal-title":"Eur J Obstet Gynecol Reprod Biol"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/j.jsgi.2006.02.008","article-title":"Preoperative treatment of uterine leiomyomas: clinical findings and expression of transforming growth factor-beta3 and connective tissue growth factor","volume":"13","author":"M De Falco","year":"2006","journal-title":"J Soc Gynecol Investig"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1055\/a-0882-4116","article-title":"Sarcoma of the Uterus. Guideline of the DGGG and OEGGG (S2k Level, AWMF Register Number 015\/074, February 2019)","volume":"79","author":"D Denschlag","year":"2019","journal-title":"Geburtshilfe Frauenheilkd"},{"key":"ref5","volume-title":"Female Genital Tumours","author":"WHO Classification of Tumours Editorial Board","year":"2020"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1016\/j.ygyno.2019.07.002","article-title":"Uterine smooth muscle tumors of unknown malignant potential: A challenging question","volume":"154","author":"A Gadducci","year":"2019","journal-title":"Gynecol Oncol"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1097\/00000478-199406000-00001","article-title":"Problematic uterine smooth muscle neoplasms. A clinicopathologic study of 213 cases","volume":"18","author":"S W Bell","year":"1994","journal-title":"Am J Surg Pathol"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1097\/00000478-199711000-00001","article-title":"Bizarre leiomyomas of the uterus: a comprehensive pathologic study of 24 cases with long-term follow-up","volume":"21","author":"K A Downes","year":"1997","journal-title":"Am J Surg Pathol"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1097\/PGP.0b013e3181a2b8d3","article-title":"Atypical leiomyomas of the uterus with long-term follow-up after myomectomy with immunohistochemical analysis for p\u200a16INK4A, p\u200a53, Ki-67, estrogen receptors, and progesterone receptors","volume":"28","author":"C O Sung","year":"2009","journal-title":"Int J Gynecol Pathol"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1097\/PAS.0b013e3182893f36","article-title":"Atypical leiomyomas of the uterus: a clinicopathologic study of 51 cases","volume":"37","author":"A Ly","year":"2013","journal-title":"Am J Surg Pathol"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1097\/PAS.0000000000000249","article-title":"Uterine leiomyomas with bizarre nuclei: a clinicopathologic study of 59 cases","volume":"38","author":"S Croce","year":"2014","journal-title":"Am J Surg Pathol"},{"key":"ref12","first-page":"7196","article-title":"Diagnostic value of progesterone receptor, p\u200a16, p\u200a53 and pHH3 expression in uterine atypical leiomyoma","volume":"8","author":"Y Liang","year":"2015","journal-title":"Int J Clin Exp Pathol"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.3892\/ol.2015.4062","article-title":"A clinicopathological study of atypical leiomyomas: Benign variant leiomyoma or smooth-muscle tumor of uncertain malignant potential","volume":"11","author":"I Kalogiannidis","year":"2016","journal-title":"Oncol Lett"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1097\/PAS.0000000000000646","article-title":"Two Subtypes of Atypical Leiomyoma: Clinical, Histologic, and Molecular Analysis","volume":"40","author":"J M Ubago","year":"2016","journal-title":"Am J Surg Pathol"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1038\/modpathol.2017.56","article-title":"Leiomyoma with bizarre nuclei: a morphological, immunohistochemical and molecular analysis of 31 cases","volume":"30","author":"J A Bennett","year":"2017","journal-title":"Mod Pathol"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1097\/PGP.0000000000000425","article-title":"Leiomyoma With Bizarre Nuclei: Clinical and Pathologic Features of 30 Patients","volume":"37","author":"M Kefeli","year":"2018","journal-title":"Int J Gynecol Pathol"},{"key":"ref17","doi-asserted-by":"publisher","DOI":"10.1007\/s12253-019-00739-5","article-title":"Leiomyoma with Bizarre Nuclei: a Study of 108 Cases Focusing on Clinicopathological Features, Morphology, and Fumarate Hydratase Alterations","author":"M Gregov\u00e1","year":"2019","journal-title":"Pathol Oncol Res"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1111\/his.13124","article-title":"The mitosis-specific marker phosphohistone-H3 (PHH3) is an independent prognosticator in uterine smooth muscle tumours: an outcome-based study","volume":"70","author":"K L Chow","year":"2017","journal-title":"Histopathology"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1097\/PAS.0b013e3181574d1e","article-title":"The Use of p\u200a16 in enhancing the histologic classification of uterine smooth muscle tumors","volume":"32","author":"K A Atkins","year":"2008","journal-title":"Am J Surg Pathol"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1097\/PAS.0b013e3181a02d1c","article-title":"Uterine smooth muscle tumors of uncertain malignant potential (STUMP): a clinicopathologic analysis of 16 cases","volume":"33","author":"P P Ip","year":"2009","journal-title":"Am J Surg Pathol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1097\/PGP.0b013e318193df97","article-title":"Mitosis-specific marker phospho-histone H3 in the assessment of mitotic index in uterine smooth muscle tumors: a pilot study","volume":"28","author":"E Veras","year":"2009","journal-title":"Int J Gynecol Pathol"},{"key":"ref22","first-page":"412","article-title":"[Smooth muscle tumor of uncertain malignant potential (STUMP)\u2013clinico-pathomorphological analysis of the cases and literature review]","volume":"83","author":"A Da\u0144ska-Bidzi\u0144ska","year":"2012","journal-title":"Ginekol Pol"},{"key":"ref23","first-page":"8136","article-title":"Uterine smooth muscle tumors of uncertain malignant potential (STUMP): pathology, follow-up and recurrence","volume":"7","author":"A Dall\u02bcAsta","year":"2014","journal-title":"Int J Clin Exp Pathol"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1038\/modpathol.2015.3","article-title":"Uterine smooth muscle tumor analysis by comparative genomic hybridization: a useful diagnostic tool in challenging lesions","volume":"28","author":"S Croce","year":"2015","journal-title":"Mod Pathol"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1002\/cjp2.11","article-title":"Loss of ATRX and DAXX expression identifies poor prognosis for smooth muscle tumours of uncertain malignant potential and early stage uterine leiomyosarcoma","volume":"1","author":"T L Slatter","year":"2015","journal-title":"J Pathol Clin Res"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"76","DOI":"10.14740\/wjon1031w","article-title":"Uterine Smooth Muscle Tumor of Uncertain Malignant Potential: Clinicopathologic-Sonographic Characteristics, Follow-Up and Recurrence","volume":"8","author":"B H Bacanakgil","year":"2017","journal-title":"World J Oncol"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1097\/01.pas.0000180424.75077.a3","article-title":"Analysis of allelic loss as an adjuvant tool in evaluation of malignancy in uterine smooth muscle tumors","volume":"30","author":"N N Esposito","year":"2006","journal-title":"Am J Surg Pathol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1097\/IGC.0000000000001178","article-title":"The Clinicopathological Study of 21 Cases With Uterine Smooth Muscle Tumors of Uncertain Malignant Potential: Centralized Review Can Purify the Diagnosis","volume":"28","author":"D Basaran","year":"2018","journal-title":"Int J Gynecol Cancer"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1111\/his.13515","article-title":"Predictors of adverse outcome in uterine smooth muscle tumours of uncertain malignant potential (STUMP): a clinicopathological analysis of 22 cases with a proposal for the inclusion of additional histological parameters","volume":"73","author":"M Gupta","year":"2018","journal-title":"Histopathology"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ejogrb.2018.06.003","article-title":"A clinicopathologic review and obstetric outcome of uterine smooth muscle tumor of uncertain malignant potential (STUMP) in a single institution","volume":"228","author":"H I Ha","year":"2018","journal-title":"Eur J Obstet Gynecol Reprod Biol"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1016\/j.jogoh.2019.03.003","article-title":"Clinicopathologic evaluation of uterine smooth muscle tumors of uncertain malignant potential (STUMP): A single center experience","volume":"48","author":"V Karata\u015fl\u0131","year":"2019","journal-title":"J Gynecol Obstet Hum Reprod"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1093\/ajcp\/aqz132","article-title":"Congruence Between 1994 WHO 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Whiting","year":"2011","journal-title":"Ann Intern Med"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"1411","DOI":"10.1007\/s12253-019-00784-0","article-title":"TCGA Molecular Subgroups in Endometrial Undifferentiated\/Dedifferentiated Carcinoma","volume":"26","author":"A Travaglino","year":"2020","journal-title":"Pathol Oncol Res"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1111\/apm.13135","article-title":"Stanford parameters stratify the risk of recurrence in gynecologic smooth muscle tumors of uncertain malignant potential","volume":"129","author":"A Travaglino","year":"2021","journal-title":"APMIS"}],"container-title":["Geburtshilfe und 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