{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,24]],"date-time":"2026-06-24T08:30:24Z","timestamp":1782289824357,"version":"3.54.5"},"reference-count":50,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2020,3,10]],"date-time":"2020-03-10T00:00:00Z","timestamp":1583798400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003725","name":"National Research Foundation of Korea","doi-asserted-by":"publisher","award":["2018R1C1B5043725"],"award-info":[{"award-number":["2018R1C1B5043725"]}],"id":[{"id":"10.13039\/501100003725","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diagnostics"],"abstract":"<jats:p>Malignancies of extragenital origin very rarely metastasize to the uterine body. Endometrium-limited metastases may pose diagnostic challenges in endometrial curettage specimens as they may be misdiagnosed as primary endometrial tumors. We investigated the clinicopathological characteristics of seven cases with endometrial-limited metastases from carcinomas of the nasopharynx (n = 1), breast (n = 2), colon (n = 2), stomach (n = 1), and appendix (n = 1). The patients\u2019 ages ranged from 36 to 71 (mean: 55.4) years. None of the patients had a remarkable gynecological history, and the presenting sign in all cases was abnormal uterine bleeding. Although myometrial involvement was absent, multiple metastases were already present in extrauterine locations such as the lung, liver, bone, abdominopelvic peritoneum, and omentum. All patients underwent ultrasonographic examination prior to endometrial curettage. The histologies of the endometrial metastases identified from the curettage specimens were identical to those of the corresponding primary tumors. Ancillary tests including immunostaining and Epstein\u2013Barr virus-encoded RNA in situ hybridization confirmed the extragenital origin. Endometrium-limited metastases from extragenital malignancies are extremely rare. They present with abnormal vaginal bleeding and mimic endometrial carcinomas of endometrioid or poorly differentiated types. Since their clinical presentations and histological features are similar to those of primary endometrial tumors, pathologists should consider the possibility of metastases while evaluating endometrial curettage specimens obtained from patients with a history of extragenital malignancies.<\/jats:p>","DOI":"10.3390\/diagnostics10030150","type":"journal-article","created":{"date-parts":[[2020,3,10]],"date-time":"2020-03-10T11:59:36Z","timestamp":1583841576000},"page":"150","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Endometrium-Limited Metastasis of Extragenital Malignancies: A Challenge in the Diagnosis of Endometrial Curettage Specimens"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2108-0575","authenticated-orcid":false,"given":"Sangjoon","family":"Choi","sequence":"first","affiliation":[{"name":"Department of Pathology and Translational Genomics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin Woo","family":"Joo","sequence":"additional","affiliation":[{"name":"Department of Pathology, Severance Hospital, Yonsei University College of Medicine, Seoul 03722, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sung-Im","family":"Do","sequence":"additional","affiliation":[{"name":"Department of Pathology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 03181, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4730-221X","authenticated-orcid":false,"given":"Hyun-Soo","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Pathology and Translational Genomics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,3,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"5465","DOI":"10.21873\/anticanres.12879","article-title":"Clinicopathological characteristics of ovarian metastasis from colorectal and pancreatobiliary carcinomas mimicking primary ovarian mucinous tumor","volume":"38","author":"Park","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_2","first-page":"264","article-title":"Malignant melanoma metastatic to the endometrium","volume":"63","author":"Bauer","year":"1984","journal-title":"OBS Gynecol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Colling, R., Lopes, T., Das, N., and Mathew, J. (2010). Endometrial metastasis of colorectal cancer with coincident endometrial adenocarcinoma. BMJ Case Rep., 2010.","DOI":"10.1136\/bcr.09.2009.2229"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1055\/s-2001-18227","article-title":"Endometrial metastasis of cutaneous melanoma\u2014A case-report bearing diagnostic difficulties","volume":"123","author":"Heinig","year":"2001","journal-title":"Zent. Gynakol."},{"key":"ref_5","first-page":"327","article-title":"A case of micropapillary breast cancer with endometrial metastasis","volume":"79","author":"Lee","year":"2010","journal-title":"Korean J. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1177\/030089169508100516","article-title":"Endometrial metastases from gastric adenocarcinoma: A case report","volume":"81","author":"Pasini","year":"1995","journal-title":"Tumori"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1177\/1066896909336442","article-title":"Colonic carcinoma metastatic to the endometrium: The importance of clinical history in averting misdiagnosis as a primary endometrial carcinoma","volume":"19","author":"Zannoni","year":"2011","journal-title":"Int. J. Surg. Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1097\/00004347-198302000-00004","article-title":"Metastases to the uterus from extrapelvic primary tumors","volume":"2","author":"Kumar","year":"1983","journal-title":"Int. J. Gynecol. Pathol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2163","DOI":"10.1002\/1097-0142(19821115)50:10<2163::AID-CNCR2820501032>3.0.CO;2-F","article-title":"Metastases to the uterine corpus from extragenital cancers. A clinicopathologic study of 63 cases","volume":"50","author":"Kumar","year":"1982","journal-title":"Cancer"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1978","DOI":"10.1002\/1097-0142(19840501)53:9<1978::AID-CNCR2820530929>3.0.CO;2-1","article-title":"Metastases to the female genital tract. Analysis of 325 cases","volume":"53","author":"Mazur","year":"1984","journal-title":"Cancer"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.21873\/anticanres.13237","article-title":"ROBO1 Expression in metastasizing breast and ovarian cancer: SLIT2-induced chemotaxis requires heparan sulfates (Heparin)","volume":"39","author":"Rezniczek","year":"2019","journal-title":"Anticancer Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"5763","DOI":"10.3748\/wjg.14.5763","article-title":"Primary signet ring cell carcinoma of the appendix: A rare case report and our 18-year experience","volume":"14","author":"Ko","year":"2008","journal-title":"World J. Gastroenterol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1111\/1759-7714.12195","article-title":"Metastases of basal-like breast invasive ductal carcinoma to the endometrium: A case report and review of the literature","volume":"6","author":"Huo","year":"2015","journal-title":"Thorac. Cancer"},{"key":"ref_14","first-page":"58","article-title":"Endometrial curettage with metastasis of a clinically inapparent stomach cancer\u2014A case report","volume":"14","author":"Neumayr","year":"1993","journal-title":"Der Pathol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.ygyno.2004.09.064","article-title":"Metastases of breast carcinoma to the uterus. Report of two cases, one harboring a primary endometrioid carcinoma, with review of the literature","volume":"96","author":"Scopa","year":"2005","journal-title":"Gynecol. Oncol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1016\/j.breast.2005.10.008","article-title":"Lobular carcinoma of the breast metastatic to the uterus in a patient under adjuvant anastrozole therapy","volume":"15","author":"Erkanli","year":"2006","journal-title":"Breast"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1097\/01.MP.0000062655.62606.86","article-title":"Metastatic breast lobular carcinoma involving tamoxifen-associated endometrial polyps: Report of two cases and review of tamoxifen-associated polypoid uterine lesions","volume":"16","author":"Houghton","year":"2003","journal-title":"Mod. Pathol."},{"key":"ref_18","first-page":"5525","article-title":"Down-regulation of inositol polyphosphate 4-phosphatase type II expression in colorectal carcinoma","volume":"37","author":"Sung","year":"2017","journal-title":"Anticancer Res."},{"key":"ref_19","first-page":"5399","article-title":"Predictive Value of Sphingosine Kinase 1 Expression in Papillary Thyroid Carcinoma","volume":"37","author":"Do","year":"2017","journal-title":"Anticancer Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e73","DOI":"10.3802\/jgo.2017.28.e73","article-title":"External validation of chemotherapy response score system for histopathological assessment of tumor regression after neoadjuvant chemotherapy in tubo-ovarian high-grade serous carcinoma","volume":"28","author":"Lee","year":"2017","journal-title":"J. Gynecol. Oncol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"663","DOI":"10.21873\/anticanres.13161","article-title":"Increased sphingosine kinase 1 expression predicts distant metastasis and poor outcome in patients with colorectal cancer","volume":"39","author":"Bae","year":"2019","journal-title":"Anticancer Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"369","DOI":"10.21873\/anticanres.13121","article-title":"Clinicopathological and molecular characteristics of mammary adenoid cystic carcinoma with adipocytic differentiation with emphasis on the Identification of a novel BRAF mutation","volume":"39","author":"Bae","year":"2019","journal-title":"Anticancer Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3551","DOI":"10.21873\/anticanres.12627","article-title":"Stromal p16 overexpression in gastric-type mucinous carcinoma of the uterine cervix","volume":"38","author":"Chung","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2883","DOI":"10.21873\/anticanres.13417","article-title":"Targeted genomic sequencing reveals novel TP53 in-frame deletion mutations leading to p53 overexpression in high-grade serous tubo-ovarian carcinoma","volume":"39","author":"Jung","year":"2019","journal-title":"Anticancer Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s00428-017-2186-z","article-title":"Clinicopathological characteristics of fallopian tube metastases from primary endometrial, cervical, and nongynecological malignancies: A single institutional experience","volume":"471","author":"Na","year":"2017","journal-title":"Virchows. Arch."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1097\/PAS.0000000000000991","article-title":"Clinicopathologic and molecular characteristics of mesonephric adenocarcinoma arising from the uterine body","volume":"43","author":"Na","year":"2019","journal-title":"Am. J. Surg. Pathol."},{"key":"ref_27","first-page":"6697","article-title":"TP53 Mutation status of tubo-ovarian and peritoneal high-grade serous carcinoma with a wild-type p53 immunostaining pattern","volume":"37","author":"Na","year":"2017","journal-title":"Anticancer Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2437","DOI":"10.21873\/anticanres.11583","article-title":"Stromal p16 overexpression in adult granulosa cell tumors of the ovary","volume":"37","author":"Na","year":"2017","journal-title":"Anticancer Res."},{"key":"ref_29","first-page":"5441","article-title":"Clinicopathological characteristics of ovarian sclerosing stromal tumor with an emphasis on TFE3 overexpression","volume":"37","author":"Park","year":"2017","journal-title":"Anticancer Res."},{"key":"ref_30","first-page":"2459","article-title":"Chemotherapy-induced endometrial pathology: Mimicry of malignancy and viral endometritis","volume":"8","author":"Kim","year":"2016","journal-title":"Am. J. Transl. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1055\/s-2007-1022960","article-title":"Uterine metastases of malignant melanoma","volume":"52","author":"Glaubitz","year":"1992","journal-title":"Geburtshilfe Frauenheilkd"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1054\/brst.2002.0447","article-title":"Uterine metastasis from infiltrating ductal carcinoma of breast in a patient receiving tamoxifen","volume":"11","author":"Meydanli","year":"2002","journal-title":"Breast"},{"key":"ref_33","first-page":"1377","article-title":"Galangin induces p53-independent S-phase arrest and apoptosis in human nasopharyngeal carcinoma cells through inhibiting PI3K-AKT signaling pathway","volume":"38","author":"Lee","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_34","first-page":"229","article-title":"Patterns of distant metastases in nasopharyngeal carcinoma","volume":"12","author":"Huang","year":"1996","journal-title":"Kaohsiung J. Med. Sci."},{"key":"ref_35","first-page":"27","article-title":"Clinical features and management of distant metastases of nasopharyngeal carcinoma","volume":"20","author":"Leung","year":"1991","journal-title":"J. Otolaryngol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1097\/00004347-199807000-00013","article-title":"Lymphoepitheliomalike carcinoma: An unusual variant of endometrial cancer. A report of two cases","volume":"17","author":"Vargas","year":"1998","journal-title":"Int. J. Gynecol. Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1111\/j.1525-1438.2007.00793.x","article-title":"Endometrial lymphoepitheliomalike carcinoma: Absence of Epstein-Barr virus genomes","volume":"17","author":"Rahimi","year":"2007","journal-title":"Int. J. Gynecol. Cancer"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1007\/s13193-015-0405-0","article-title":"Lymphoepithelioma-like carcinoma of endometrium; A rare case report","volume":"6","author":"Makannavar","year":"2015","journal-title":"Indian J. Surg. Oncol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"6405","DOI":"10.21873\/anticanres.13001","article-title":"Whole-brain radiation therapy for breast cancer patients with dural metastasis without concomitant brain metastasis and leptomeningeal Metastasis","volume":"38","author":"Sakaguchi","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_40","first-page":"2607","article-title":"Molecular mechanisms of breast cancer metastasis and potential anti-metastatic compounds","volume":"38","author":"Tungsukruthai","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1006\/gyno.1998.5126","article-title":"Signet ring breast carcinoma metastases limited to the endometrium and cervix","volume":"71","author":"Kennebeck","year":"1998","journal-title":"Gynecol. Oncol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.humpath.2005.01.013","article-title":"CK20 and CK7 protein expression in colorectal cancer: Demonstration of the utility of a population-based tissue microarray","volume":"36","author":"Hernandez","year":"2005","journal-title":"Hum. Pathol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3307","DOI":"10.1002\/cncr.10589","article-title":"Primary malignant neoplasms of the appendix: A population-based study from the surveillance, epidemiology and end-results program, 1973\u20131998","volume":"94","author":"McCusker","year":"2002","journal-title":"Cancer"},{"key":"ref_44","first-page":"601","article-title":"Neuroendocrine neoplasms of the appendix: A review of the literature","volume":"38","author":"Moris","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2264","DOI":"10.1007\/s10350-005-0196-4","article-title":"Malignancies of the appendix: Beyond case series reports","volume":"48","author":"McGory","year":"2005","journal-title":"Dis. Colon. Rectum"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"776","DOI":"10.5858\/134.5.776","article-title":"Cervical and endometrial metastases of appendiceal goblet cell carcinoid","volume":"134","author":"Pan","year":"2010","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1016\/j.ygyno.2005.01.055","article-title":"Gastric adenocarcinoma presenting as uterine metastasis\u2014A case report","volume":"97","author":"Tsoi","year":"2005","journal-title":"Gynecol. Oncol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"803","DOI":"10.3109\/00016349709024352","article-title":"Uterine metastasis from gastric cancer","volume":"76","author":"Khoury","year":"1997","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_49","first-page":"404692","article-title":"Primary endometrial Adenocarcinoma with signet-ring cells: A rarely observed case and review of the literature","volume":"2015","author":"Akkalp","year":"2015","journal-title":"Case Rep. Obstet. Gynecol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1097\/PGP.0b013e3181e20c66","article-title":"Endometrial adenocarcinoma with signet ring cells: Report of two cases of an extremely rare phenomenon","volume":"29","author":"Boyd","year":"2010","journal-title":"Int. J. Gynecol. Pathol."}],"container-title":["Diagnostics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4418\/10\/3\/150\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:05:43Z","timestamp":1760173543000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4418\/10\/3\/150"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,10]]},"references-count":50,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2020,3]]}},"alternative-id":["diagnostics10030150"],"URL":"https:\/\/doi.org\/10.3390\/diagnostics10030150","relation":{},"ISSN":["2075-4418"],"issn-type":[{"value":"2075-4418","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,10]]}}}