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Review

Diagnosis and management of uterine serous carcinoma: current strategies and clinical challenges

ORCID Icon, &
Pages 343-355 | Received 23 Feb 2020, Accepted 14 Jun 2020, Published online: 15 Jul 2020

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30.
  • Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol. 1983;15:10–17.
  • Hamilton CA, Cheung MK, Osann K, et al. Uterine papillary serous and clear cell carcinomas predict for poorer survival compared to grade 3 endometrioid corpus cancers. Br J Cancer. 2006;94:642.
  • Rauh-Hain JA, Diver E, Meyer LA, et al. Patterns of care, associations and outcomes of chemotherapy for uterine serous carcinoma: analysis of the National Cancer Database. Gynecol Oncol. 2015;139:77–83.
  • Lachance JA, Everett EN, Greer B, et al. The effect of age on clinical/pathologic features, surgical morbidity, and outcome in patients with endometrial cancer. Gynecol Oncol. 2006;101:470–475.
  • Sherman ME, Sturgeon S, Brinton LA, et al. Risk factors and hormone levels in patients with serous and endometrioid uterine carcinomas. Mod Pathol an Off J United States Can Acad Pathol Inc. 1997;10:963–968.
  • McCullough ML, Patel AV, Patel R, et al. Body mass and endometrial cancer risk by hormone replacement therapy and cancer subtype. Cancer Epidemiol Prev Biomarkers. 2008;17:73–79.
  • Bjørge T, Engeland A, Tretli S, et al. Body size in relation to cancer of the uterine corpus in 1 million Norwegian women. Int J Cancer. 2007;120:378–383.
  • McGunigal M, Liu J, Kalir T, et al. Survival differences among uterine papillary serous, clear cell and grade 3 endometrioid adenocarcinoma endometrial cancers: a National Cancer Database analysis. Int J Gynecol Cancer. 2017;27:85–92.
  • Maxwell GL, Tian C, Risinger J, et al. Racial disparity in survival among patients with advanced/recurrent endometrial adenocarcinoma: a Gynecologic Oncology Group study. Cancer Interdiscip Int J Am Cancer Soc. 2006;107:2197–2205.
  • Bregar AJ, Rauh-Hain JA, Spencer R, et al. Disparities in receipt of care for high-grade endometrial cancer: a National Cancer Data Base analysis. Gynecol Oncol. 2017;145:114–121.
  • Rauh-Hain JA, Buskwofie A, Clemmer J, et al. Racial disparities in treatment of high-grade endometrial cancer in the Medicare population. Obstet Gynecol. 2015;125(4):843–851..
  • Gehrig PA, Bae-Jump VL, Boggess JF, et al. Association between uterine serous carcinoma and breast cancer. Gynecol Oncol. 2004;94:208–211.
  • Pierce SR, Stine JE, Gehrig PA, et al. Prior breast cancer and tamoxifen exposure does not influence outcomes in women with uterine papillary serous carcinoma. Gynecol Oncol. 2017;144:531–535.
  • Chan JK, Manuel MR, Cheung MK, et al. Breast cancer followed by corpus cancer: is there a higher risk for aggressive histologic subtypes? Gynecol. Oncol. 2006;102:508–512.
  • Dewdney SB, Kizer NT, Andaya AA, et al. Uterine serous carcinoma: increased familial risk for lynch-associated malignancies. Cancer Prev Res. 2012;5:435–443.
  • Pennington KP, Walsh T, Lee M, et al. BRCA1, TP53, and CHEK2 germline mutations in uterine serous carcinoma. Cancer. 2013;119:332–338.
  • Kadan Y, Raviv O, Segev Y, et al. Impact of BRCA mutations on outcomes among patients with serous endometrial cancer. Int J Gynecol Obstet. 2018;142:91–96.
  • Slomovitz BM, Burke TW, Eifel PJ, et al. Uterine papillary serous carcinoma (UPSC): a single institution review of 129 cases. Gynecol Oncol. 2003;91:463–469.
  • Huang GS, Gebb JS, Einstein MH, et al. Accuracy of preoperative endometrial sampling for the detection of high-grade endometrial tumors. Am J Obstet Gynecol. 2007;196:243–e1.
  • Antonsen SL, Jensen LN, Loft A, et al. MRI, PET/CT and ultrasound in the preoperative staging of endometrial cancer—a multicenter prospective comparative study. Gynecol Oncol. 2013;128:300–308.
  • Gee MS, Atri M, Bandos AI, et al. Identification of distant metastatic disease in uterine cervical and endometrial cancers with FDG PET/CT: analysis from the ACRIN 6671/GOG 0233 multicenter trial. Radiology. 2018;287:176–184.
  • Olawaiye AB, Rauh-Hain JA, Withiam-Leitch M, et al. Utility of pre-operative serum CA-125 in the management of uterine papillary serous carcinoma. Gynecol Oncol. 2008;110:293–298.
  • Baek M-H, Lee S-W, Park J-Y, et al. Identification of a preoperative predictive factor for lymph node metastasis in uterine papillary serous carcinoma: long-term results from a single institution. Int J Gynecol Cancer. 2015;25:69–74.
  • Mattes MD, Lee JC, Metzger DJ, et al. The incidence of pelvic and para-aortic lymph node metastasis in uterine papillary serous and clear cell carcinoma according to the SEER registry. J Gynecol Oncol. 2015;26:19–24.
  • Todo Y, Kato H, Kaneuchi M, et al. Survival effect of para-aortic lymphadenectomy in endometrial cancer (SEPAL study): a retrospective cohort analysis. Lancet. 2010;375:1165–1172.
  • Alagkiozidis I, Weedon J, Grossman A, et al. Extent of lymph node dissection and overall survival in patients with uterine carcinosarcoma, papillary serous and endometrioid adenocarcinoma: a retrospective cohort study. Int J Surg. 2015;24:9–13.
  • Schiavone MB, Scelzo C, Straight C, et al. Survival of patients with serous uterine carcinoma undergoing sentinel lymph node mapping. Ann Surg Oncol. 2017;24:1965–1971.
  • Smith AJB, Fader AN, Tanner EJ. Sentinel lymph node assessment in endometrial cancer: a systematic review and meta-analysis. Am J Obstet Gynecol. 2017;216:459–476.
  • Luz R, MacDonald N, Mould T. Omental biopsy for surgical staging of uterine serous carcinoma. Int J Gynecol Cancer. 2016;26:1448–1454.
  • Kaban A, Topuz S, Erdem B, et al. Is omentectomy necessary for non-endometrioid endometrial cancer. Gynecol Obstet Invest. 2018;83(5):482–486.
  • Giuntoli RL, Gerardi MA, Yemelyanova AV, et al. Stage I noninvasive and minimally invasive uterine serous carcinoma: comprehensive staging associated with improved survival. Int J Gynecol Cancer. 2012;22:273–279.
  • Thomas MB, Mariani A, Cliby WA, et al. Role of cytoreduction in stage III and IV uterine papillary serous carcinoma. Gynecol Oncol. 2007;107:190–193.
  • Alagkiozidis I, Grossman A, Tang NZ, et al. Survival impact of cytoreduction to microscopic disease for advanced stage cancer of the uterine corpus: A retrospective cohort study. Int J Surg. 2015;14:61–66.
  • Lee LJ, DeMaria R, Berkowitz R, et al. Clinical predictors of long-term survival for stage IVB uterine papillary serous carcinoma confined to the abdomen. Gynecol Oncol. 2014;132:65–69.
  • Solmaz U, Mat E, Ekin A, et al. Optimal cytoreduction, depth of myometrial invasion, and age are independent prognostic factors for survival in women with uterine papillary serous and clear cell carcinomas. Int J Surg. 2016;32:71–77.
  • Wilkinson-Ryan I, Frolova AI, Liu J, et al. Neoadjuvant chemotherapy versus primary cytoreductive surgery for stage IV uterine serous carcinoma. Int J Gynecol Cancer. 2015;25:63–68.
  • Fader AN, Java J, Tenney M, et al. Impact of histology and surgical approach on survival among women with early-stage, high-grade uterine cancer: an NRG Oncology/Gynecologic Oncology Group ancillary analysis. Gynecol Oncol. 2016;143:460–465.
  • Hanley KZ, Fadare O, Fisher KE, et al. Clinical significance of positive pelvic washings in uterine papillary serous carcinoma confined to an endometrial polyp. Int J Gynecol Pathol. 2016;35:249–255.
  • Zhong X, Wang J, Kaku T, et al. Prognostic Factors of Uterine Serous Carcinoma—A Multicenter Study. Int J Gynecol Cancer. 2018;28:1138–1144.
  • Tolcher MC, Swisher EM, Medeiros F, et al. Characterization of precursor lesions in the endometrium and fallopian tube epithelium of early stage uterine serous carcinoma. Int J Gynecol Pathol Off J Int Soc Gynecol Pathol. 2015;34:57.
  • Kommoss F, Faruqi A, Gilks CB, et al. Uterine serous carcinomas frequently metastasize to the fallopian tube and can mimic serous tubal intraepithelial carcinoma. Am J Surg Pathol. 2017;41:161–170.
  • Black C, Feng A, Bittinger S, et al. Uterine papillary serous carcinoma: a single-institution review of 62 Cases. Int J Gynecol Cancer. 2016;26:133–140.
  • Qian Y, Pollom EL, Nwachukwu C, et al. Extent of lymphovascular space invasion may predict lymph node metastasis in uterine serous carcinoma. Gynecol Oncol. 2017;147:24–29.
  • Winer I, Ahmed QF, Mert I, et al. Significance of lymphovascular space invasion in uterine serous carcinoma: what matters more; extent or presence? Int J Gynecol Pathol. 2015;34:47–56.
  • Fader AN, Starks D, Gehrig PA, et al. An updated clinicopathologic study of early-stage uterine papillary serous carcinoma (UPSC). Gynecol Oncol. 2009;115:244–248.
  • Kuhn E, Wu R-C, Guan B, et al. Identification of molecular pathway aberrations in uterine serous carcinoma by genome-wide analyses. J Natl Cancer Inst. 2012;104:1503–1513.
  • Zhao S, Choi M, Overton JD, et al. Landscape of somatic single-nucleotide and copy-number mutations in uterine serous carcinoma. Proc Natl Acad Sci. 2013;110:2916–2921.
  • Levine DA, Network CGAR. Integrated genomic characterization of endometrial carcinoma. Nature. 2013;497:67.
  • Le Gallo M, O’Hara AJ, Rudd ML, et al. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat Genet. 2012;44:1310.
  • Kuhn E, Bahadirli-Talbott A, Shih I-M. Frequent CCNE1 amplification in endometrial intraepithelial carcinoma and uterine serous carcinoma. Mod Pathol. 2014;27:1014.
  • Mahdi H, Xiu J, Reddy SK, et al. Alteration in PI3K/mTOR, MAPK pathways and Her2 expression/amplification is more frequent in uterine serous carcinoma than ovarian serous carcinoma. J Surg Oncol. 2015;112:188–194.
  • Jones NL, Xiu J, Reddy SK, et al. Identification of potential therapeutic targets by molecular profiling of 628 cases of uterine serous carcinoma. Gynecol Oncol. 2015;138:620–626.
  • Mhawech‐Fauceglia P, Yan L, Liu S, et al. ER+/PR+/TFF 3+/IMP 3− immunoprofile distinguishes endometrioid from serous and clear cell carcinomas of the endometrium: a study of 401 cases. Histopathology. 2013;62:976–985.
  • Buza N, English DP, Santin AD, et al. Toward standard HER2 testing of endometrial serous carcinoma: 4-year experience at a large academic center and recommendations for clinical practice. Mod Pathol. 2013;26:1605–1612.
  • Jones NL, Xiu J, Chatterjee‐Paer S, et al. Distinct molecular landscapes between endometrioid and nonendometrioid uterine carcinomas. Int J Cancer. 2017;140:1396–1404.
  • Morice P, Leary A, Creutzberg C, et al. Endometrial cancer. Lancet. 2016;387:1094–1108.
  • Santin AD, Bellone S, Van Stedum S, et al. Amplification of c‐erbB2 oncogene: a major prognostic indicator in uterine serous papillary carcinoma. Cancer. 2005;104:1391–1397.
  • Togami S, Sasajima Y, Oi T, et al. Clinicopathological and prognostic impact of human epidermal growth factor receptor type 2 (HER 2) and hormone receptor expression in uterine papillary serous carcinoma. Cancer Sci. 2012;103:926–932.
  • Divine LM, Nguyen MR, Meller E, et al. AXL modulates extracellular matrix protein expression and is essential for invasion and metastasis in endometrial cancer. Oncotarget. 2016;7:77291.
  • Beirne JP, Quinn JE, Maxwell P, et al. BRCA1 immunohistochemical staining as a prognostic indicator in uterine serous carcinoma. Int J Gynecol Cancer. 2013;23:113–118.
  • Mahdi H, Han X, Moulton L, et al. Trends in survival of patients with uterine serous carcinoma from 1988 to 2011: a population-based study. Int J Gynecol Cancer. 2017;27:1155–1164.
  • Fader AN, Drake RD, O’Malley DM, et al. Platinum/taxane‐based chemotherapy with or without radiation therapy favorably impacts survival outcomes in stage I uterine papillary serous carcinoma. Cancer. 2009;115:2119–2127.
  • Fader AN, Nagel C, Axtell AE, et al. Stage II uterine papillary serous carcinoma: carboplatin/paclitaxel chemotherapy improves recurrence and survival outcomes. Gynecol Oncol. 2009;112:558–562.
  • Boothe D, Williams N, Odei B, et al. The addition of adjuvant chemotherapy to radiation in early-stage high-risk endometrial cancer: survival outcomes and patterns of care. Int J Gynecol Cancer. 2017;27:912–922.
  • Dietrich III CS, Modesitt SC, DePriest PD, et al. The efficacy of adjuvant platinum-based chemotherapy in Stage I uterine papillary serous carcinoma (UPSC). Gynecol Oncol. 2005;99:557–563.
  • Kelly MG, O’Malley DM, Hui P, et al. Improved survival in surgical stage I patients with uterine papillary serous carcinoma (UPSC) treated with adjuvant platinum-based chemotherapy. Gynecol Oncol. 2005;98:353–359.
  • Shinde A, Li R, Amini A, et al. Improved survival with adjuvant brachytherapy in stage IA endometrial cancer of unfavorable histology. Gynecol Oncol. 2018;151:82–90.
  • Cham S, Huang Y, Tergas AI, et al. Utility of radiation therapy for early-stage uterine papillary serous carcinoma. Gynecol Oncol. 2017;145:269–276.
  • de Boer SM, Powell ME, Mileshkin L, et al. Adjuvant chemoradiotherapy versus radiotherapy alone for women with high-risk endometrial cancer (PORTEC-3): final results of an international, open-label, multicentre, randomised, phase 3 trial. Lancet Oncol. 2018;19:295–309.
  • Randall ME, Filiaci V, McMeekin DS, et al. Phase III trial: adjuvant pelvic radiation therapy versus vaginal brachytherapy plus paclitaxel/carboplatin in high-intermediate and high-risk early-stage endometrial cancer. J Clin Oncol. 2019;37:1810.
  • Homesley HD, Filiaci V, Gibbons SK, et al. A randomized phase III trial in advanced endometrial carcinoma of surgery and volume directed radiation followed by cisplatin and doxorubicin with or without paclitaxel: a Gynecologic Oncology Group study. Gynecol Oncol. 2009;112:543–552.
  • Miller D, Filiaci V, Fleming G, et al. Randomized phase Ill noninferiority trial of first line chemotherapy for metastatic or recurrent endometrial carcinoma: A Gynecologic Oncology Group study. Gynecol Oncol. ACADEMIC PRESS INC ELSEVIER SCIENCE 525 B ST, STE 1900, SAN DIEGO, CA 92101 …. 2012;771. DOI:10.1016/j.ygyno.2012.03.034.
  • Matei D, Filiaci V, Randall ME, et al. Adjuvant chemotherapy plus radiation for locally advanced endometrial cancer. N Engl J Med. 2019;380:2317–2326.
  • Lin JF, Muñiz K, Sukumvanich P, et al. Survival advantage associated with multimodal therapy in women with node‐positive (stage‐IIIC) uterine papillary serous carcinoma: a National Cancer Database study. BJOG An Int J Obstet Gynaecol. 2016;123:1846–1852.
  • Fader AN, Roque DM, Siegel E, et al. Randomized phase II trial of carboplatin-paclitaxel versus carboplatin-paclitaxel-trastuzumab in uterine serous carcinomas that overexpress human epidermal growth factor receptor 2/neu. 2018;
  • Tortorella L, Langstraat CL, Weaver AL, et al. Uterine serous carcinoma: reassessing effectiveness of platinum-based adjuvant therapy. Gynecol Oncol. 2018;149:291–296.
  • Mahdi H, Rizzo A, Rose PG. Outcome of recurrent uterine papillary serous carcinoma treated with platinum-based chemotherapy. Int J Gynecol Cancer. 2015;25:467–473.
  • Ebeid K, Meng X, Thiel KW, et al. Synthetically lethal nanoparticles for treatment of endometrial cancer. Nat Nanotechnol. 2018;13:72.
  • Palisoul ML, Quinn JM, Schepers E, et al. Inhibition of the receptor tyrosine kinase AXL restores paclitaxel chemosensitivity in uterine serous cancer. Mol Cancer Ther. 2017;16:2881–2891.
  • Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol. 2001;2:127.
  • Santin AD, Bellone S, Gokden M, et al. Overexpression of HER-2/neu in uterine serous papillary cancer. Clin Cancer Res. 2002;8:1271–1279.
  • Verma S, Miles D, Gianni L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med. 2012;367:1783–1791.
  • English DP, Bellone S, Schwab CL, et al. T‐DM1, a novel antibody–drug conjugate, is highly effective against primary HER2 overexpressing uterine serous carcinoma in vitro and in vivo. Cancer Med. 2014;3:1256–1265.
  • Santin AD, Bellone S, Buza N, et al. Regression of metastatic, radiation/chemotherapy-resistant uterine serous carcinoma overexpressing HER2/neu with trastuzumab emtansine (TDM-1). Gynecol Oncol reports. 2017;19:10–12.
  • Black J, Menderes G, Bellone S, et al. SYD985, a novel duocarmycin-based HER2-targeting antibody–drug conjugate, shows antitumor activity in uterine serous carcinoma with HER2/Neu expression. Mol Cancer Ther. 2016;15:1900–1909.
  • Baselga J, Cortés J, Kim S-B, et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med. 2012;366:109–119.
  • El-Sahwi K, Bellone S, Cocco E, et al. In vitro activity of pertuzumab in combination with trastuzumab in uterine serous papillary adenocarcinoma. Br J Cancer. 2010;102:134–143.
  • Growdon WB, Groeneweg J, Byron V, et al. HER2 over-expressing high grade endometrial cancer expresses high levels of p95HER2 variant. Gynecol Oncol. 2015;137:160–166.
  • Todeschini P, Cocco E, Bellone S, et al. Her2/neu extracellular domain shedding in uterine serous carcinoma: implications for immunotherapy with trastuzumab. Br J Cancer. 2011;105:1176.
  • Black JD, Lopez S, Cocco E, et al. PIK3CA oncogenic mutations represent a major mechanism of resistance to trastuzumab in HER2/neu overexpressing uterine serous carcinomas. Br J Cancer. 2015;113:1020.
  • Schwab CL, Bellone S, English DP, et al. Afatinib demonstrates remarkable activity against HER2-amplified uterine serous endometrial cancer in vitro and in vivo. Br J Cancer. 2014;111:1750.
  • Schwab CL, English DP, Roque DM, et al. Neratinib shows efficacy in the treatment of HER2/neu amplified uterine serous carcinoma in vitro and in vivo. Gynecol Oncol. 2014;135:142–148.
  • Lopez S, Schwab CL, Cocco E, et al. Taselisib, a selective inhibitor of PIK3CA, is highly effective on PIK3CA-mutated and HER2/neu amplified uterine serous carcinoma in vitro and in vivo. Gynecol Oncol. 2014;135:312–317.
  • Lopez S, Cocco E, Black J, et al. Dual HER2/PIK3CA targeting overcomes single-agent acquired resistance in HER2-amplified uterine serous carcinoma cell lines in vitro and in vivo. Mol Cancer Ther. 2015;14:2519–2526.
  • Myers AP, Konstantinopoulos PA, Barry WT, et al. Phase II, 2 stage, 2 arm, PIK3CA mutation stratified trial of MK‐2206 in recurrent endometrial cancer. Int J Cancer. 2019;142:413-422.
  • Cocco E, Lopez S, Black J, et al. Dual CCNE1/PIK3CA targeting is synergistic in CCNE1-amplified/PIK3CA-mutated uterine serous carcinomas in vitro and in vivo. Br J Cancer. 2016;115:303.
  • English DP, Roque DM, Carrara L, et al. HER2/neu gene amplification determines the sensitivity of uterine serous carcinoma cell lines to AZD8055, a novel dual mTORC1/2 inhibitor. Gynecol Oncol. 2013;131:753–758.
  • Hernandez SF, Chisholm S, Borger D, et al. Ridaforolimus improves the anti-tumor activity of dual HER2 blockade in uterine serous carcinoma in vivo models with HER2 gene amplification and PIK3CA mutation. Gynecol Oncol. 2016;141:570–579.
  • Bellone S, Roque D, Cocco E, et al. Downregulation of membrane complement inhibitors CD55 and CD59 by siRNA sensitises uterine serous carcinoma overexpressing Her2/neu to complement and antibody-dependent cell cytotoxicity in vitro: implications for trastuzumab-based immunotherapy. Br J Cancer. 2012;106:1543.
  • Bellone S, Black J, English DP, et al. Solitomab, an EpCAM/CD3 bispecific antibody construct (BiTE), is highly active against primary uterine serous papillary carcinoma cell lines in vitro. Am J Obstet Gynecol. 2016;214:99–e1.
  • Makker V, Rasco D, Vogelzang NJ, et al. Lenvatinib plus pembrolizumab in patients with advanced endometrial cancer: an interim analysis of a multicentre, open-label, single-arm, phase 2 trial. Lancet Oncol. 2019;20:711–718.
  • Aghajanian C, Filiaci V, Dizon DS, et al. A phase II study of frontline paclitaxel/carboplatin/bevacizumab, paclitaxel/carboplatin/temsirolimus, or ixabepilone/carboplatin/bevacizumab in advanced/recurrent endometrial cancer. Gynecol Oncol. 2018;150:274–281.
  • Mallen AR, Filiaci VL, Levine DA, et al. Evidence for synthetic lethality between bevacizumab and chemotherapy in advanced, p53 null endometrial cancers. Gynecol Oncol. 2018;149:29–30.
  • Haines K, Huang GS. Precision Therapy for Aggressive Endometrial Cancer by Reactivation of Protein Phosphatase 2A. Cancer Res. 2019;79:4009–4010.
  • Taylor SE, O’Connor CM, Wang Z, et al. The highly recurrent PP2A Aα-subunit mutation P179R alters protein structure and impairs PP2A enzyme function to promote endometrial tumorigenesis. Cancer Res. 2019;79(16):4242–4257. canres-0218..
  • Bonazzoli E, Predolini F, Cocco E, et al. Inhibition of BET bromodomain proteins with GS-5829 and GS-626510 in uterine serous carcinoma, a biologically aggressive variant of endometrial cancer. Clin Cancer Res. 2018;24:4845–4853.
  • Roque DM, Bellone S, English DP, et al. Tubulin‐β‐III overexpression by uterine serous carcinomas is a marker for poor overall survival after platinum/taxane chemotherapy and sensitivity to epothilones. Cancer. 2013;119:2582–2592.

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