Dynamic contrast-enhanced ultrasound improves diagnostic performance in endometrial cancer staging.
Doppler
color
contrast-enhanced ultrasound
data accuracy
endometrial neoplasms
neoplasm staging
ultrasonography
Journal
Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology
ISSN: 1469-0705
Titre abrégé: Ultrasound Obstet Gynecol
Pays: England
ID NLM: 9108340
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
21
06
2019
revised:
13
09
2019
accepted:
20
09
2019
pubmed:
28
10
2019
medline:
26
8
2021
entrez:
25
10
2019
Statut:
ppublish
Résumé
To compare the sensitivity and specificity of conventional two-dimensional transvaginal ultrasound/power Doppler (2D-TVU/PD) alone and 2D-TVU/PD combined with dynamic contrast-enhanced ultrasound (DCE-US) in diagnosing deep myometrial invasion (MI) and cervical stromal involvement (CSI) in women with endometrial cancer (EC), and to assess the association of DCE-US semiquantitative and qualitative variables with International Federation of Gynecology and Obstetrics (FIGO) Stage ≥ IB and 'high-risk' cancer. This was a prospective study of 101 consecutive women with biopsy-confirmed EC, undergoing expert ultrasound examination at Karolinska University Hospital, a tertiary referral center. All consenting women underwent DCE-US using a 1.5-2.5-mL intravenous bolus of SonoVue contrast agent, as well as conventional 2D-TVU/PD examination. DCE-US videoclips were analyzed with regard to filling (global or focal), wash-in (prior, simultaneous or after) and wash-out (global or focal) patterns of the contrast agent in the tumor compared with the surrounding tissue, as well as semiquantitative DCE-US parameters (wash-in slope, time-to-peak, peak intensity and area under the time-intensity curve (TIC)) obtained from a TIC. The study cohort was compared with a control cohort of women with EC examined at our center according to the International Endometrial Tumor Analysis protocol using 2D-TVU/PD only, matched at a ratio of 3:1 for FIGO stage and grade. The sensitivity and specificity of 2D-TVU/PD alone in the control cohort and in combination with DCE-US in the study cohort in the diagnosis of deep MI, CSI and high-risk cancer (defined as FIGO Stage ≥ IB and/or Grade 3 endometrioid and/or non-endometrioid histology) were compared, using pathological evaluation after hysterectomy as the 'gold standard'. After exclusions, 93 women were included in the study cohort and were matched to 279 women in the control cohort. The prevalence of FIGO Stage IA, Grade 1-2 EC was 52% in both cohorts. The sensitivity of 2D-TVU/PD with DCE-US in the study cohort was higher than that of 2D-TVU/PD alone in the control cohort in diagnosing both deep MI (0.74 vs 0.62; P = 0.036) and CSI (0.75 vs 0.51; P < 0.001), whereas the specificity was not significantly different (0.87 vs 0.85 and 0.96 vs 0.95, respectively). Compared with 2D-TVU/PD alone, the specificity of 2D-TVU/PD with DCE-US was higher in detecting high-risk cancer (0.94 vs 0.85; P = 0.024) but the sensitivity did not differ (0.73 vs 0.71). High-risk cancer and FIGO Stage ≥ IB were characterized by a 'focal' filling pattern, with a 'prior' wash-in pattern and a 'focal' wash-out pattern on subjective assessment of DCE-US videoclips. All semiquantitative DCE-US parameters were significantly predictive of FIGO Stage ≥ IB but not of high-risk cancer, despite a clear trend. Compared with 2D-TVU/PD alone, combining 2D-TVU/PD with DCE-US can significantly improve the detection of deep MI and CSI in women with EC, without increasing the false-positive rate. It can also improve the correct classification of high-risk disease, mainly by increasing specificity, thereby possibly reducing the number of unnecessarily extensive surgeries by almost 10%. Semiquantitative DCE-US parameters, as well as a 'focal' filling pattern, endometrial wash-in prior to the myometrium and a 'focal' wash-out pattern, are all associated with more advanced disease. Copyright © 2019 ISUOG. Published by John Wiley & Sons Ltd.
Substances chimiques
Contrast Media
0
Types de publication
Evaluation Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
96-105Subventions
Organisme : Avtal om Läkarutbildning och Forskning
ID : 561101
Organisme : Cancer Research Foundation
ID : 154112
Informations de copyright
Copyright © 2019 ISUOG. Published by John Wiley & Sons Ltd.
Références
Colombo N, Creutzberg C, Amant F, Bosse T, González-Martín A, Ledermann J, Marth C, Nout R, Querleu D, Mirza MR, Sessa C; ESMO-ESGO-ESTRO Consensus Conference on Endometrial Cancer: diagnosis, treatment and follow-up. Ann Oncol 2016; 27: 16-41.
Dietrich CF, Averkiou MA, Correas JM, Lassau N, Leen E, Piscaglia F. An EFSUMB introduction into dynamic contrast-enhanced ultrasound (DCE-US) for quantification of tumour perfusion. Ultraschall Med 2012; 33: 344-351.
Paul Sidhu AS, Cantisani V, Dietrich CF, Helge Gilja O, Saftoiu A, Bartels E, Bertolotto M, Calliada F, Clevert D-A, Cosgrove D, Deganello A, D'Onofrio M et al. The EFSUMB Guidelines and Recommendations for the Clinical Practice of Contrast-Enhanced Ultrasound (CEUS) in Non-Hepatic Applications: Update 2017 (Long Version). Ultraschall Med 2018; 39: e2-e44.
Marret H, Sauget S, Giraudeau B, Brewer M, Ranger-Moore J, Body G, Tranquart F. Contrast-enhanced sonography helps in discrimination of benign from malignant adnexal masses. J Ultrasound Med 2004; 23: 1629-1639; quiz 1641-1642.
Testa AC, Ferrandina G, Fruscella E, Van Holsbeke C, Ferrazzi E, Leone FPG, Arduini D, Exacoustos C, Bokor D, Scambia G, Timmerman D. The use of contrasted transvaginal sonography in the diagnosis of gynecologic diseases: a preliminary study. J Ultrasound Med 2005; 24: 1267-1278.
Liu Y, Tian J-W, Xu Y, Cheng W. Role of transvaginal contrast-enhanced ultrasound in the early diagnosis of endometrial carcinoma. Chin Med J (Engl) 2012; 125: 416-421.
Song Y, Yang J-W, Liu Z, Shen K. Preoperative evaluation of endometrial carcinoma by contrast-enhanced ultrasonography. BJOG 2009; 116: 294-298.
Liu Y, Xu Y, Cheng W, Liu X. Quantitative contrast-enhanced ultrasonography for the differential diagnosis of endometrial hyperplasia and endometrial neoplasms. Oncol Lett 2016; 12: 3763-3770.
Lieng M, Qvigstad E, Dahl GF, Istre O. Flow differences between endometrial polyps and cancer: a prospective study using intravenous contrast-enhanced transvaginal color flow Doppler and three-dimensional power Doppler ultrasound. Ultrasound Obstet Gynecol 2008; 32: 935-940.
Zhou H-L, Xiang H, Duan L, Shahai G, Liu H, Li X-H, Mou R-X. Application of Combined Two-Dimensional and Three-Dimensional Transvaginal Contrast Enhanced Ultrasound in the Diagnosis of Endometrial Carcinoma. Biomed Res Int 2015; 2015: 292743.
Pálsdóttir K, Epstein E. A Pilot Study on Diagnostic Performance of Contrast-Enhanced Ultrasonography for Detection of Early Cervical Cancer. Ultrasound Med Biol 2018; 44: 1664-1671.
Hajian-Tilaki K. Sample size estimation in diagnostic test studies of biomedical informatics. J Biomed Inform 2014; 48: 193-204.
Epstein E, Fischerova D, Valentin L, Testa AC, Franchi D, Sladkevicius P, Frühauf F, Lindqvist PG, Mascilini F, Fruscio R, Haak LA, Opolskiene G, Pascual MA, Alcazar JL, Chiappa V, Guerriero S, Carlson JW, Van Holsbeke C, Giuseppe Leone FP, De Moor B, Bourne T, van Calster B, Installe A, Timmerman D, Verbakel JY, Van den Bosch T. Ultrasound characteristics of endometrial cancer as defined by International Endometrial Tumor Analysis (IETA) consensus nomenclature: prospective multicenter study. Ultrasound Obstet Gynecol 2018; 51: 818-828.
Kurman RJ, Carcangiu ML, Herrington SC, Young RH (Eds). WHO Classification of Tumours of Female Reproductive Organs (4th edn). International Agency for Research on Cancer; Lyon 2014.
Amant F, Mirza MR, Koskas M, Creutzberg CL. Cancer of the corpus uteri. Int J Gynecol Obstet 2015; 131: S96-S104.
Alcazar JL, Pineda L, Martinez-Astorquiza Corral T, Orozco R, Utrilla-Layna J, Juez L, Jurado M. Transvaginal/transrectal ultrasound for assessing myometrial invasion in endometrial cancer: a comparison of six different approaches. J Gynecol Oncol 2015; 26: 201-207.
Mascilini F, Testa AC, Van Holsbeke C, Ameye L, Timmerman D, Epstein E. Evaluating myometrial and cervical invasion in women with endometrial cancer: comparing subjective assessment with objective measurement techniques. Ultrasound Obstet Gynecol 2013; 42: 353-358.
Leone FPG, Timmerman D, Bourne T, Valentin L, Epstein E, Goldstein SR, Marret H, Parsons AK, Gull B, Istre O, Sepulveda W, Ferrazzi E, Van Den Bosch T. Terms, definitions and measurements to describe the sonographic features of the endometrium and intrauterine lesions: a consensus opinion from the International Endometrial Tumor Analysis (IETA) group. Ultrasound Obstet Gynecol 2010; 35: 103-112.
Epstein E, Van Holsbeke C, Mascilini F, Måsbäck A, Kannisto P, Ameye L, Fischerova D, Zannoni G, Vellone V, Timmerman D, Testa AC. Gray-scale and color Doppler ultrasound characteristics of endometrial cancer in relation to stage, grade and tumor size. Ultrasound Obstet Gynecol 2011; 38: 586-593.
European Medicines Agency. EPAR. https://www.ema.europa.eu/en/medicines/human/EPAR/sonovue. Accessed February 18, 2019.
Campbell I. Chi-squared and Fisher-Irwin tests of two-by-two tables with small sample recommendations. Stat Med 2007; 26: 3661-3675.
Altman DG, Bland JM. Diagnostic tests 2: Predictive values. BMJ 1994; 309: 102.
Verbakel JY, Mascilini F, Wynants L, Fischerova D, Testa AC, Franchi D, Frühauf F, Cibula D, Lindqvist PG, Fruscio R, Haak LA, Opolskiene G, Alcazar JL, Mais V, Carlson JW, Sladkevicius P, Timmerman D, Valentin L, Van Den Bosch T, Epstein E. Validation of ultrasound strategies to assess tumor extension and to predict high-risk endometrial cancer in women from the prospective IETA (International Endometrial Tumor Analysis)-4 cohort. Ultrasound Obstet Gynecol 2020; 55: 115-124.
Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986; 1: 307-310.
Tang M-X, Mulvana H, Gauthier T, Lim AKP, Cosgrove DO, Eckersley RJ, Stride E. Quantitative contrast-enhanced ultrasound imaging: a review of sources of variability. Interface Focus 2011; 1: 520-539.
Epstein E, Blomqvist L. Imaging in endometrial cancer. Best Pract Res Clin Obstet Gynaecol 2014; 28: 721-739.
Alcázar JL, Gastón B, Navarro B, Salas R, Aranda J, Guerriero S. Transvaginal ultrasound versus magnetic resonance imaging for preoperative assessment of myometrial infiltration in patients with endometrial cancer: a systematic review and meta-analysis. J Gynecol Oncol 2017; 28: 405-413.
Savelli L, Ceccarini M, Ludovisi M, Fruscella E, De Iaco PA, Salizzoni E, Mabrouk M, Manfredi R, Testa AC, Ferrandina G. Preoperative local staging of endometrial cancer: transvaginal sonography vs magnetic resonance imaging. Ultrasound Obstet Gynecol 2008; 31: 560-566.
Celik C, Ozdemir S, Kiresi D, Emlik D, Tazegül A, Esen H. Evaluation of cervical involvement in endometrial cancer by transvaginal sonography, magnetic resonance imaging and frozen section. J Obstet Gynaecol 2010; 30: 302-307.
Antonsen SL, Jensen LN, Loft A, Berthelsen AK, Costa J, Tabor A, Qvist I, Hansen MR, Fisker R, Andersen ES, Sperling L, Nielsen AL, Asmussen J, Høgdall E, Fagö-Olsen CL, Christensen IJ, Nedergaard L, Jochumsen K, Høgdall C. MRI, PET/CT and ultrasound in the preoperative staging of endometrial cancer - A multicenter prospective comparative study. Gynecol Oncol 2013; 128: 300-308.
Kottner J, Audige L, Brorson S, Donner A, Gajewski BJ, Hróbjartsson A, Roberts C, Shoukri M, Streiner DL. Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. Int J Nurs Stud 2011; 48: 661-671.
van der Putten LJM, van de Vijver K, Bartosch C, Davidson B, Gatius S, Matias-Guiu X, Glenn McCluggage W, Toledo G, van der Wurff AAM, Pijnenborg JMA, Massuger LFAG, Bulten J. Reproducibility of measurement of myometrial invasion in endometrial carcinoma. Virchows Arch 2017; 470: 63-68.
Glenn McCluggage W, Hirschowitz L, Wilson GE, Oliva E, Soslow RA, Zaino RJ. Significant variation in the assessment of cervical involvement in endometrial carcinoma: An interobserver variation study. Am J Surg Pathol 2011; 35: 289-294.
Haldorsen IS, Husby JA, Werner HMJ, Magnussen IJ, Rørvik J, Helland H, Trovik J, Salvesen OO, Espeland A, Salvesen HB. Standard 1.5-T MRI of endometrial carcinomas: Modest agreement between radiologists. Eur Radiol 2012; 22: 1601-1611.
Green RW, Valentin L, Alcazar JL, Chiappa V, Erdodi B, Franchi D, Frühauf F, Fruscio R, Guerriero S, Graupera B, Jakab A, di Legge A, Ludovisi M, Mascilini F, Pascual MA, van den Bosch T, Epstein E. Endometrial cancer off-line staging using two-dimensional transvaginal ultrasound and three-dimensional volume contrast imaging: Intermethod agreement, interrater reliability and diagnostic accuracy. Gynecol Oncol 2018; 150: 438-445.
Eriksson LSE, Lindqvist PG, Floter Radestad A, Dueholm M, Fischerova D, Franchi D, Jokubkiene L, Leone FP, Savelli L, Sladkevicius P, Testa AC, Van den Bosch T, Ameye L, Epstein E. Transvaginal ultrasound assessment of myometrial and cervical stromal invasion in women with endometrial cancer: interobserver reproducibility among ultrasound experts and gynecologists. Ultrasound Obstet Gynecol 2015; 45: 476-482.
Testa AC, Ciampelli M, Mastromarino C, Lopez R, Zannoni G, Ferrandina G, Scambia G. Intratumoral color Doppler analysis in endometrial carcinoma: Is it clinically useful? Gynecol Oncol 2003; 88: 298-303.
Strobel D, Seitz K, Blank W, Schuler A, Dietrich C, Von Herbay A, Friedrich-Rust M, Kunze G, Becker D, Will U, Kratzer W, Albert FW, Pachmann C, Dirks K, Strunk H, Greis C, Bernatik T. Contrast-enhanced ultrasound for the characterization of focal liver lesions - Diagnostic accuracy in clinical practice (DEGUM multicenter trial). Ultraschall Med 2008; 29: 499-505.
Claudon M, Dietrich CF, Choi BI, Cosgrove DO, Kudo M, Nolsoe CP, Piscaglia F, Wilson SR, Barr RG, Chammas MC, Chaubal NG, Chen MH, Clevert DA, Correas JM, Ding H, Forsberg F, Fowlkes JB, Gibson RN, Goldberg BB, Lassau N, Leen ELS, Mattrey RF, Moriyasu F, Solbiati L, Weskott HP, Xu HX. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver - Update 2012. Ultraschall Med 2013; 34: 11-29.