OBJECTIVES: To compare the performance of transvaginal and transabdominal ultrasound with that of the first-line staging method (contrast-enhanced computed tomography (CT)) and a novel technique, whole-body magnetic resonance imaging with diffusion-weighted sequence (WB-DWI/MRI), in the assessment of peritoneal involvement (carcinomatosis), lymph-node staging and prediction of non-resectability in patients with suspected ovarian cancer. METHODS: Between March 2016 and October 2017, all consecutive patients with suspicion of ovarian cancer and surgery planned at a gynecological oncology center underwent preoperative staging and prediction of non-resectability with ultrasound, CT and WB-DWI/MRI. The evaluation followed a single, predefined protocol, assessing peritoneal spread at 19 sites and lymph-node metastasis at eight sites. The prediction of non-resectability was based on abdominal markers. Findings were compared to the reference standard (surgical findings and outcome and histopathological evaluation). RESULTS: Sixty-seven patients with confirmed ovarian cancer were analyzed. Among them, 51 (76%) had advanced-stage and 16 (24%) had early-stage ovarian cancer. Diagnostic laparoscopy only was performed in 16% (11/67) of the cases and laparotomy in 84% (56/67), with no residual disease at the end of surgery in 68% (38/56), residual disease ≤ 1 cm in 16% (9/56) and residual disease > 1 cm in 16% (9/56). Ultrasound and WB-DWI/MRI performed better than did CT in the assessment of overall peritoneal carcinomatosis (area under the receiver-operating-characteristics curve (AUC), 0.87, 0.86 and 0.77, respectively). Ultrasound was not inferior to CT (P = 0.002). For assessment of retroperitoneal lymph-node staging (AUC, 0.72-0.76) and prediction of non-resectability in the abdomen (AUC, 0.74-0.80), all three methods performed similarly. In general, ultrasound had higher or identical specificity to WB-DWI/MRI and CT at each of the 19 peritoneal sites evaluated, but lower or equal sensitivity in the abdomen. Compared with WB-DWI/MRI and CT, transvaginal ultrasound had higher accuracy (94% vs 91% and 85%, respectively) and sensitivity (94% vs 91% and 89%, respectively) in the detection of carcinomatosis in the pelvis. Better accuracy and sensitivity of ultrasound (93% and 100%) than WB-DWI/MRI (83% and 75%) and CT (84% and 88%) in the evaluation of deep rectosigmoid wall infiltration, in particular, supports the potential role of ultrasound in planning rectosigmoid resection. In contrast, for the bowel serosal and mesenterial assessment, abdominal ultrasound had the lowest accuracy (70%, 78% and 79%, respectively) and sensitivity (42%, 65% and 65%, respectively). CONCLUSIONS: This is the first prospective study to document that, in experienced hands, ultrasound may be an alternative to WB-DWI/MRI and CT in ovarian cancer staging, including peritoneal and lymph-node evaluation and prediction of non-resectability based on abdominal markers of non-resectability. © 2021 International Society of Ultrasound in Obstetrics and Gynecology.

1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Department of Obstetrics and Gynecology Bulovka Hospital Prague Czech Republic

Department of Obstetrics and Gynecology Maternidade Alfredo da Costa Centro Hospitalar Lisboa Central Lisbon Portugal

Department of Pathology 1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Department of Radiology 1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Gynecologic Oncology Center Department of Obstetrics and Gynecology 1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Institute of Health Information and Statistics of the Czech Republic Prague Czech Republic

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Lee KR, Tavassoli FA, Prat J, Dietel M, Gersell DJ, Karseladze AI, Hauptmann S, Rutgers J, Russell P, Buckley CH, Pisani P, Schwartz P, Goldgar DE, Silva E, Caduff R, Kubik-Huch RA. Tumours of the ovary and peritoneum. In World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Breast and Female Genital Organs, Tavassoli FA, Devilee P (eds). IARC Press: Lyon, 2003; 113-202.

du Bois A, Baert T, Vergote I. Role of Neoadjuvant Chemotherapy in Advanced Epithelial Ovarian Cancer. J Clin Oncol 2019; 37: 2398-2405.

Querleu D, Planchamp F, Chiva L, Fotopoulou C, Barton D, Cibula D, Aletti G, Carinelli S, Creutzberg C, Davidson B, Harter P, Lundvall L, Marth C, Morice P, Rafii A, Ray-Coquard I, Rockall A, Sessa C, van der Zee A, Vergote I, du Bois A. European Society of Gynaecologic Oncology Quality Indicators for Advanced Ovarian Cancer Surgery. Int J Gynecol Cancer 2016; 26: 1354-1363.

Fotopoulou C, Concin N, Planchamp F, Morice P, Vergote I, du Bois A, Querleu D. Quality indicators for advanced ovarian cancer surgery from the European Society of Gynaecological Oncology (ESGO): 2020 update. Int J Gynecol Cancer 2020; 30: 436-440.

Colombo N, Sessa C, du Bois A, Ledermann J, McCluggage WG, McNeish I, Morice P, Pignata S, Ray-Coquard I, Vergote I, Baert T, Belaroussi I, Dashora A, Olbrecht S, Planchamp F, Querleu D, ESMO-ESGO Ovarian Cancer Consensus Conference Working Group. ESMO-ESGO consensus conference recommendations on ovarian cancer: pathology and molecular biology, early and advanced stages, borderline tumours and recurrent disease. Int J Gynecol Cancer 2019; 30: 672-705.

Alcázar JL, Caparros M, Arraiza M, Mínguez J, Guerriero S, Chiva L, Jurado M. Pre-operative assessment of intra-abdominal disease spread in epithelial ovarian cancer: a comparative study between ultrasound and computed tomography. Int J Gynecol Cancer 2019; 29: 227-233.

Michielsen K, Vergote I, Op de Beeck K, Amant F, Leunen K, Moerman P, Deroose C, Souverijns G, Dymarkowski S, De Keyzer F, Vandecaveye V. Whole-body MRI with diffusion-weighted sequence for staging of patients with suspected ovarian cancer: a clinical feasibility study in comparison to CT and FDG-PET/CT. Eur Radiol 2014; 24: 889-901.

Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L, Lijmer JG, Moher D, Rennie D, de Vet HC, Kressel HY, Rifai N, Golub RM, Altman DG, Hooft L, Korevaar DA, Cohen JF, Group S. STARD 2015: An Updated List of Essential Items for Reporting Diagnostic Accuracy Studies. Radiology 2015; 277: 826-832.

Fischerova D, Cibula D, Dundr P, Zikan M, Calda P, Freitag P, Slama J. Ultrasound-guided tru-cut biopsy in the management of advanced abdomino-pelvic tumors. Int J Gynecol Cancer 2008; 18: 833-837.

Zikan M, Fischerova D, Pinkavova I, Dundr P, Cibula D. Ultrasound-guided tru-cut biopsy of abdominal and pelvic tumors in gynecology. Ultrasound Obstet Gynecol 2010; 36: 767-772.

Epstein E, Van Calster B, Timmerman D, Nikman S. Subjective ultrasound assessment, the ADNEX model and ultrasound-guided tru-cut biopsy to differentiate disseminated primary ovarian cancer from metastatic non-ovarian cancer. Ultrasound Obstet Gynecol 2016; 47: 110-116.

Fischerova D. Metastatic Ovarian Tumors. In Ovarian Neoplasm Imaging, Saba L (ed). Springer Science+Business Media: Boston, MA, 2013; 335-364.

Zikan M, Fischerova D, Pinkavova I, Dundr P, Cibula D. Ultrasonographic appearance of metastatic non-gynecological pelvic tumors. Ultrasound Obstet Gynecol 2012; 39: 215-225.

Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 1982; 5: 649-655.

Prat J; FIGO Committee on Gynecologic Oncology. Staging classification for cancer of the ovary, fallopian tube, and peritoneum. Int J Gynaecol 2014; 124: 1-5.

Querleu D, Planchamp F, Chiva L, Fotopoulou C, Barton D, Cibula D, Aletti G, Carinelli S, Creutzberg C, Davidson B, Harter P, Lundvall L, Marth C, Morice P, Rafii A, Ray-Coquard I, Rockall A, Sessa C, van der Zee A, Vergote I, duBois A. European Society of Gynaecological Oncology (ESGO) Guidelines for Ovarian Cancer Surgery. Int J Gynecol Cancer 2017; 27: 1534-1542.

Fischerova D, Zikan M, Semeradova I, Slama J, Kocian R, Dundr P, Nemejcova K, Burgetova A, Dusek L, Cibula D. Ultrasound in preoperative assessment of pelvic and abdominal spread in patients with ovarian cancer: a prospective study. Ultrasound Obstet Gynecol 2017; 49: 263-274.

Fischerova D. Ultrasound scanning of the pelvis and abdomen for staging of gynecological tumors: a review. Ultrasound Obstet Gynecol 2011; 38: 246-266.

Cornelli B, Bojana C, Cibula D, Sartori E, Frühauf F, Kocian R, Indrova D, Nemejcova K, Fischerova D. OC12.03: Comparison of clinical and ultrasound characteristics in low- and high-grade serous cancer. Ultrasound Obstet Gynecol 2019; 54: 30.

Qi Z, Zhang Y, Dai Q, Xia Y, Jiang Y. Peritoneal Carcinomatosis in Primary Ovarian Cancer: Ultrasound Detection and Comparison with Computed Tomography. Ultrasound Med Biol 2017; 43: 1811-1819.

Hanbidge AE, Lynch D, Wilson SR. US of the peritoneum. Radiographics 2003; 23: 663-684; discussion 684-685.

Testa AC, Ludovisi M, Mascilini F, Di Legge A, Malaggese M, Fagotti A, Fanfani F, Salerno MG, Ercoli A, Scambia G, Ferrandina G. Ultrasound evaluation of intra-abdominal sites of disease to predict likelihood of suboptimal cytoreduction in advanced ovarian cancer: a prospective study. Ultrasound Obstet Gynecol 2012; 39: 99-105.

Ying M, Bhatia KS, Lee YP, Yuen HY, Ahuja AT. Review of ultrasonography of malignant neck nodes: greyscale, Doppler, contrast enhancement and elastography. Cancer Imaging 2014; 13: 658-669.

Ecanow JS, Abe H, Newstead GM, Ecanow DB, Jeske JM. Axillary staging of breast cancer: what the radiologist should know. Radiographics 2013; 33: 1589-1612.

Fischerova D, Garganese G, Reina H, Fragomeni SM, Cibula D, Nanka O, Rettenbacher T, Testa AC, Epstein E, Guiggi I, Fruhauf F, Manegold G, Scambia G, Valentin L. Terms, definitions and measurements to describe sonographic features of lymph nodes: consensus opinion from the Vulvar International Tumor Analysis (VITA) group. Ultrasound Obstet Gynecol 2021; 57: 861-879.

Vancauwenberghe T, Snoeckx A, Vanbeckevoort D, Dymarkowski S, Vanhoenacker FM. Imaging of the spleen: what the clinician needs to know. Singapore Med J 2015; 56: 133-144.

Buamah PK, Rake MO, Drake SR, Skillen AW. Serum CA 12-5 concentrations and CA 12-5/CEA ratios in patients with epithelial ovarian cancer. J Surg Oncol 1990; 44: 97-99.

Vergote I, du Bois A, Amant F, Heitz F, Leunen K, Harter P. Neoadjuvant chemotherapy in advanced ovarian cancer: On what do we agree and disagree? Gynecol Oncol 2013; 128: 6-11.

Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 1982; 143: 29-36.

Liu JP, Ma MC, Wu CY, Tai JY. Tests of equivalence and non-inferiority for diagnostic accuracy based on the paired areas under ROC curves. Stat Med 2006; 25: 1219-1238.

Fischerova D, Pinto P, Kocian R, Fruhauf F, Slama JT, Zikan M, Dundr P, Dusek L, Masek M, Burgetova A, Cibula D. OC14.06: Preoperative staging of advanced ovarian cancer: comparison between ultrasound, CT and WB-DWI/MRI. Ultrasound Obstet Gynecol 2017; 50: 30.

Michielsen K, Dresen R, Vanslembrouck R, De Keyzer F, Amant F, Mussen E, Leunen K, Berteloot P, Moerman P, Vergote I, Vandecaveye V. Diagnostic value of whole body diffusion-weighted MRI compared to computed tomography for pre-operative assessment of patients suspected for ovarian cancer. Eur J Cancer 2017; 83: 88-98.

Tempany CM, Zou KH, Silverman SG, Brown DL, Kurtz AB, McNeil BJ. Staging of advanced ovarian cancer: comparison of imaging modalities-report from the Radiological Diagnostic Oncology Group. Radiology 2000; 215: 761-767.

Ultrasound examiners' ability to describe ovarian cancer spread using preacquired ultrasound videoclips from a selected patient sample with high prevalence of cancer spread

Whole-body magnetic resonance imaging provides accurate staging of diffuse large B-cell lymphoma, but is less preferred by patients

Staging by imaging in gynecologic cancer and the role of ultrasound: an update of European joint consensus statements

Prediction of Surgical Outcome in Advanced Ovarian Cancer by Imaging and Laparoscopy: A Narrative Review