Improving strategies for diagnosing ovarian cancer: A summary of the International Ovarian Tumor Analysis (IOTA) studies

Ultrasound in Obstetrics and Gynecology

Volumn 41, Issue 1, 2013, Pages 9-20

  Kaijser, J ^a   Bourne, T ^a,b,c   Valentin, L ^d   Sayasneh, A ^b   Van Holsbeke, C ^a,e   Vergote, I ^a   Testa, A C ^f   Franchi, D ^g   Van Calster, B ^a,c   Timmerman, D ^a,c  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b QUEEN CHARLOTTE S AND CHELSEA HOSPITAL   (United Kingdom)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d LUND UNIVERSITY HOSPITAL   (Sweden)

^e DEPARTMENT OF CARDIOLOGY   (Belgium)

^f CATHOLIC UNIVERSITY   (Italy)

^g EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

biomarkers; decision support techniques; logistic models; ovarian neoplasms; ultrasonography

Indexed keywords

CA 125 ANTIGEN; EPIDIDYMAL SECRETORY PROTEIN;

ALGORITHM; AREA UNDER THE CURVE; BLOOD; DIFFERENTIAL DIAGNOSIS; ECHOGRAPHY; FEMALE; HUMAN; METHODOLOGY; OVARY TUMOR; PRACTICE GUIDELINE; REVIEW; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; STATISTICAL MODEL; THEORETICAL MODEL;

ALGORITHMS; AREA UNDER CURVE; CA-125 ANTIGEN; DIAGNOSIS, DIFFERENTIAL; EPIDIDYMAL SECRETORY PROTEINS; FEMALE; HUMANS; LOGISTIC MODELS; MODELS, THEORETICAL; OVARIAN NEOPLASMS; PRACTICE GUIDELINES AS TOPIC; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY;

MLCS; MLOWN;

EID: 84871571350     PISSN: 09607692     EISSN: 14690705     Source Type: Journal    
DOI: 10.1002/uog.12323     Document Type: Review

References (67)

1. Menon U, Gentry-Maharaj A, Hallett R, Ryan A, Burnell M, Sharma A, Lewis S, Davies S, Philpott S, Lopes A, Godfrey K, Oram D, Herod J, Williamson K, Seif MW, Scott I, Mould T, Woolas R, Murdoch J, Dobbs S, Amso NN, Leeson S, Cruickshank D, McGuire A, Campbell S, Fallowfield L, Singh N, Dawnay A, Skates SJ, Parmar M, Jacobs I,. Sensitivity and specificity of multimodal and ultrasound screening for ovarian cancer, and stage distribution of detected cancers: results of the prevalence screen of the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS). Lancet Oncol 2009; 10: 327-340.
2. Carley ME, Klingee CJ, Bebhart JB, Webb MJ, Wilson TO,. Laparoscopy versus laparotomy in the management of benign unilateral adnexal masses. J Am Assoc Gynecol Laparosc 2002; 9: 321-326.
3. Vergote I, De Brabanter J, Fyles A, Bertelsen K, Einhorn N, Sevelda P, Gore ME, Kaern J, Verrelst H, Sjövall K, Timmerman D, Vandewalle J, Van Gramberen M, Tropé CG,. Prognostic importance of degree of differentiation and cyst rupture in stage I invasive epithelial ovarian carcinoma. Lancet 2001; 357: 176-182.
4. Paulsen T, Kjaerheim K, Kaern J, Tretli S, Tropé C,. Improved short-term survival for advanced ovarian, tubal, and peritoneal cancer patients operated at teaching hospitals. Int J Gynecol Cancer 2006; 16 (Suppl. 1): 11-17.
5. Engelen MJ, van der Zee AG, de Vries EG, Willemse PH,. Debulking surgery for ovarian epithelial cancer performed by a gynaecological oncologist improved survival compared with less specialised surgeons. Cancer Treat Rev 2006; 32: 320-323.
6. Earle CC, Schrag D, Neville BA, Yabroff KR, Topor M, Fahey A, Trimble EL, Bodurka DC, Bristow RE, Carney M, Warren JL,. Effect of surgeon specialty on process of care and outcomes for ovarian cancer patients. J Natl Cancer Inst 2006; 98: 172-180.
7. DePriest PD, Shenson D, Fried A, Hunter JE, Andrews SJ, Gallion HH, Pavlik EJ, Kryscio RJ, van Nagell JR, Jr. A morphology index based on sonographic findings in ovarian cancer. Gynecol Oncol 1993; 51: 7-11.
8. Ferrazzi E, Zanetta G, Dordoni D, Berlanda N, Mezzopane R, Lissoni AA,. Transvaginal ultrasonographic characterization of ovarian masses: comparison of five scoring systems in a multicenter study. Ultrasound Obstet Gynecol 1997; 10: 192-197.
9. Finkler NJ, Benacerraf B, Lavin PT, Wojciechowski C, Knapp RC,. Comparison of serum CA 125, clinical impression, and ultrasound in the preoperative evaluation of ovarian masses. Obstet Gynecol 1988; 72: 659-664.
10. Granberg S, Norström A, Wikland M,. Tumors in the lower pelvis as imaged by vaginal sonography. Gynecol Oncol 1990; 37: 224-229.
11. Sassone AM, Timor-Tritsch IE, Artner A, Westhoff C, Warren WB,. Transvaginal sonographic characterization of ovarian disease: evaluation of a new scoring system to predict ovarian malignancy. Obstet Gynecol 1991; 78: 70-76.
12. Jacobs I, Oram D, Fairbanks J, Turner J, Frost C, Grudzinskas JG,. A risk of malignancy index incorporating CA 125, ultrasound and menopausal status for the accurate preoperative diagnosis of ovarian cancer. Br J Obstet Gynaecol 1990; 97: 922-929.
13. Timmerman D, Bourne TH, Tailor A, Collins WP, Verrelst, H, Vandenberghe K, Vergote I,. A comparison of methods for preoperative discrimination between malignant and benign adnexal masses: the development of a new logistic regression model. Am J Obstet Gynecol 1999; 181: 57-65.
14. Timmerman D, Verrelst H, Bourne TH, De Moor B, Collins WP, Vergote I, Vandewalle J,. Artificial neural network models for the preoperative discrimination between malignant and benign adnexal masses. Ultrasound Obstet Gynecol 1999; 13: 17-25.
15. Lu C, Van Gestel T, Suykens JA, Van Huffel S, Vergote I, Timmerman D,. Preoperative prediction of malignancy of ovarian tumors using least squares support vector machines. Artif Intell Med 2003; 28: 281-306.
16. Geomini P, Kruitwagen R, Bremer GL, Cnossen J, Mol BWJ,. The accuracy of risk scores in predicting ovarian malignancy-a systematic review. Obstet Gynecol 2009; 113: 384-394.
17. Dearking AC, Aletti GD, McGree ME, Weaver AL, Sommerfield MK, Cliby WA,. How relevant are ACOG and SGO guidelines for referral of adnexal mass? Obstet Gynecol 2007; 110: 841-848.
18. Ueland FR, Desimone CP, Seamon LG, Miller RA, Goodrich S, Podzielinski I, Sokoll L, Smith A, van Nagell JR, Jr, Zhang Z,. Effectiveness of a multivariate index assay in the preoperative assessment of ovarian tumors. Obstet Gynecol 2011; 117: 1289-1297.
19. Timmerman D, Van Calster B, Vergote I, Van Hoorde K, Van Gorp T, Valentin L, Bourne T,. Performance of the American College of Obstetricians and Gynecologists' ovarian tumor referral guidelines with a multivariate index assay. Obstet Gynecol 2011; 118: 1179-1181.
20. Mol BW, Boll D, De Kanter M, Heintz AP, Sijmons EA, Oei SG, Bal H, Brölmann HA,. Distinguishing the benign and malignant adnexal mass: an external validation of prognostic models. Gynecol Oncol 2001; 80: 162-167.
21. Ferrazzi E, Zanetta G, Dordoni D, Berlanda N, Mezzopane R, Lissoni AA,. Transvaginal ultrasonographic characterization of ovarian masses: comparison of five scoring systems in a multicenter study. Ultrasound Obstet Gynecol 1997; 10: 192-197.
22. Aslam N, Banerjee S, Carr JV, Savvas M, Hooper R, Jurkovic D,. Prospective evaluation of logistic regression models for the diagnosis of ovarian cancer. Obstet Gynecol 2000; 96: 75-80.
23. Van Holsbeke C, Van Calster B, Valentin L, Testa AC, Ferrazzi E, Dimou I, Lu C, Moerman P, Van Huffel S, Vergote I, Timmerman D,; International Ovarian Tumor Analysis Group. External validation of mathematical models to distinguish between benign and malignant adnexal tumors: a multicenter study by the International Ovarian Tumor Analysis Group. Clin Cancer Res 2007; 13: 4440-4447.
24. Valentin L, Hagen B, Tingulstad S, Eik-Nes S,. Comparison of 'pattern recognition' and logistic regression models for discrimination between benign and malignant pelvic masses: a prospective cross-validation. Ultrasound Obstet Gynecol 2001; 18: 357-65.
25. Timmerman D, Valentin L, Bourne TH, Collins WP, Verrelst H, Vergote I,. Terms, definitions and measurements to describe the sonographic features of adnexal tumors: a consensus opinion from the International Ovarian Tumor Analysis (IOTA) Group. Ultrasound Obstet Gynecol 2000; 16: 500-505.
26. Timmerman D, Testa AC, Bourne T, Ferrazzi E, Ameye L, Konstantinovic ML, Van Calster B, Collins WP, Vergote I, Van Huffel S, Valentin L,; International Ovarian Tumor Analysis Group. Logistic regression model to distinguish between the benign and malignant adnexal mass before surgery: a multicenter study by the International Ovarian Tumor Analysis Group. J Clin Oncol 2005; 23: 8794-8801.
27. Van Holsbeke C, Van Calster B, Testa AC, Domali E, Lu C, Van Huffel S, Valentin L, Timmerman D,. Prospective internal validation of mathematical models to predict malignancy in adnexal masses: results from the international ovarian tumor analysis study. Clin Cancer Res 2009; 15: 684-691.
28. Van Holsbeke C, Van Calster B, Bourne T, Ajossa S, Testa AC, Guerriero S, Fruscio R, Lissoni AA, Czekierdowski A, Savelli L, Van Huffel S, Valentin L, Timmerman D,. External validation of diagnostic models to estimate the risk of malignancy in adnexal masses. Clin Cancer Res 2012; 18: 815-825.
29. Timmerman D, Van Calster B, Testa AC, Guerriero S, Fischerova D, Lissoni AA, Van Holsbeke C, Fruscio R, Czekierdowski A, Jurkovic D, Savelli L, Vergote I, Bourne T, Van Huffel S, Valentin L,. Ovarian cancer prediction in adnexal masses using ultrasound-based logistic regression models: a temporal and external validation study by the IOTA group. Ultrasound Obstet Gynecol 2010; 36: 226-234.
30. Van Calster B, Nabney I, Timmerman D, Van Huffel S,. The Bayesian approach: a natural framework for statistical modeling. Ultrasound Obstet Gynecol 2007; 29: 485-488.
31. Van Calster B, Timmerman D, Lu C, Suykens JA, Valentin L, Van Holsbeke C, Amant F, Vergote I, Van Huffel S,. Preoperative diagnosis of ovarian tumors using Bayesian kernel-based methods. Ultrasound Obstet Gynecol 2007; 29: 496-504.
32. Timmerman D, Testa AC, Bourne T, Ameye L, Jurkovic D, Van Holsbeke C, Paladini D, Van Calster B, Vergote I, Van Huffel S, Valentin L,. Simple ultrasound-based rules for the diagnosis of ovarian cancer. Ultrasound Obstet Gynecol 2008; 31: 681-690.
33. Ameye L, Valentin L, Testa AC, Van Holsbeke C, Domali E, Van Huffel S, Vergote I, Bourne T, Timmerman D,. A scoring system to differentiate malignant from benign masses in specific ultrasound-based subgroups of adnexal tumors. Ultrasound Obstet Gynecol 2009; 33: 92-101.
34. Altman DG, Vergouwe Y, Royston P, Moons KGM,. Prognosis and prognostic research: validating a prognostic model. BMJ 2009; 338: b605.
35. König IR, Malley JD, Weimar C, Diener HC, Ziegler A,; German Stroke Study Collaboration. Practical experiences on the necessity of external validation. Stat Med 2007; 26: 5499-5511.
36. Van Calster B, Timmerman D, Valentin L, McIndoe A, Ghaem-Maghami S, Testa AC, Vergote I, Bourne T,. Triaging women with ovarian masses for surgery: observational diagnostic study to compare RCOG guidelines with an International Ovarian Tumour Analysis (IOTA) group protocol. BJOG 2012; 119: 662-671.
37. Timmerman D, Ameye L, Fischerova D, Epstein E, Melis GB, Guerriero S, Van Holsbeke C, Savelli L, Fruscio R, Lissoni AA, Testa AC, Veldman J, Vergote I, Van Huffel S, Bourne T, Valentin L,. Simple ultrasound rules to distinguish between benign and malignant adnexal masses before surgery: prospective validation by IOTA group. BMJ 2010; 341: c6839.
38. RCOG guideline: management of suspected ovarian masses in premenopausal women. December 2011. (Green top 62). http://www.rcog.org.uk [Accessed 2 December 2011].
39. Ameye L, Timmerman D, Valentin L, Paladini D, Zhang J, Van Holsbeke C, Lissoni AA, Savelli L, Veldman J, Testa AC, Amant F, Van Huffel S, Bourne T,. Clinically oriented three-step strategy to the assessment of adnexal pathology. Ultrasound Obstet Gynecol 2012; 40: 582-591.
40. Timmerman D, Van Calster B, Jurkovic D, Valentin L, Testa AC, Bernard JP, Van Holsbeke C, Van Huffel S, Vergote I, Bourne T,. Inclusion of CA-125 does not improve mathematical models developed to distinguish between benign and malignant adnexal tumors. J Clin Oncol 2007; 25: 4194-4200.
41. Van Calster B, Timmerman D, Bourne T, Testa AC, Van Holsbeke C, Domali E, Jurkovic D, Neven P, Van Huffel S, Valentin L,. Discrimination between benign and malignant adnexal masses by specialist ultrasound examination versus serum CA-125. J Natl Cancer Inst 2007; 99: 1706-1714.
42. Valentin L, Jurkovic D, Van Calster B, Testa A, Van Holsbeke C, Bourne T, Vergote I, Van Huffel S, Timmerman D,. Adding a single CA-125 measurement to ultrasound performed by an experienced examiner does not improve preoperative discrimination between benign and malignant adnexal masses. Ultrasound Obstet Gynecol 2009; 34: 345-354.
43. Van Calster B, Valentin L, Zhang J, Jurkovic D, Lissoni AA, Testa AC, Czekierdowski A, Fischerová D, Domali E, Van de Putte G, Vergote I, Van Huffel S, Bourne T, Timmerman D,. A novel approach to predict the likelihood of specific ovarian tumor pathology based on serum CA-125: a multicenter observational study. Cancer Epidemiol Biomarkers Prev 2011; 20: 2420-2428.
44. Alexandre J, Brown C, Coeffic D, Raban N, Pfisterer J, Mäenpää J, Chalchal H, Fitzharris B, Volgger B, Vergote I, Pisano C, Ferrero A, Pujade-Lauraine E,. CA-125 can be part of the tumour evaluation criteria in ovarian cancer trials: experience of the GCIG CALYPSO trial. Br J Cancer 2012; 106: 633-637.
45. Moore RG, Brown AK, Miller MC, Skates S, Allard WJ, Verch T, Steinhoff M, Messerlian G, DiSilvestro P, Granai CO, Bast RC Jr., The use of multiple novel tumor biomarkers for the detection of ovarian carcinoma in patients with a pelvic mass. Gynecol Oncol 2008; 108: 402-408.
46. Moore RG, McMeekin DS, Brown AK, DiSilvestro P, Miller MC, Allard WJ, Gajewski W, Kurman R, Bast RC Jr, Skates SJ,. A novel multiple marker bioassay utilizing HE4 and CA125 for the prediction of ovarian cancer in patients with a pelvic mass. Gynecol Oncol 2009; 112: 40-46.
47. Moore RG, Jabre-Raughley M, Brown AK, Robison KM, Miller MC, Allard WJ, Kurman RJ, Bast RC, Skates SJ,. Comparison of a novel multiple marker assay vs the Risk of Malignancy Index for the prediction of epithelial ovarian cancer in patients with a pelvic mass. Am J Obstet Gynecol 2010; 203: 228.e1- 6.
48. Bandiera E, Romani C, Specchia C, Zanotti L, Galli C, Ruggeri G, Tognon G, Bignotti E, Tassi RA, Odicino F, Caimi L, Sartori E, Santin AD, Pecorelli S, Ravaggi A,. Serum human epididymis protein 4 and risk for ovarian malignancy algorithm as new diagnostic and prognostic tools for epithelial ovarian cancer management. Cancer Epidemiol Biomarkers Prev 2011; 20: 2496-2506.
49. Kim YM, Whang DH, Park J, Kim SH, Lee SW, Park HA, Ha M, Choi KH,. Evaluation of the accuracy of serum human epididymis protein 4 in combination with CA125 for detecting ovarian cancer: a prospective case-control study in a Korean population. Clin Chem Lab Med 2011; 49: 527-534.
50. Lenhard M, Stieber P, Hertlein L, Kirschenhofer A, Fürst S, Mayr D, Nagel D, Hofmann K, Krocker K, Burges A,. The diagnostic accuracy of two human epididymis protein 4 (HE4) testing systems in combination with CA125 in the differential diagnosis of ovarian masses. Clin Chem Lab Med 2011; 49: 2081-2088.
51. Molina R, Escudero JM, Augé JM, Filella X, Foj L, Torné A, Lejarcegui J, Pahisa J,. HE4 a novel tumour marker for ovarian cancer: comparison with CA 125 and ROMA algorithm in patients with gynaecological diseases. Tumor Biol 2011; 32: 1087-1095.
52. Ruggeri G, Bandiera E, Zanotti L, Belloli S, Ravaggi A, Romani C, Bignotti E, Tassi RA, Tognon G, Galli C, Caimi L, Pecorelli S,. HE4 and epithelial ovarian cancer: comparison and clinical evaluation of two immunoassays and a combination algorithm. Clin Chim Acta 2011; 412: 1447-1453.
53. Van Gorp T, Cadron I, Despierre E, Daemen A, Leunen K, Amant F, Timmerman D, De Moor B, Vergote I,. HE4 and CA125 as a diagnostic test in ovarian cancer: prospective validation of the Risk of Ovarian Malignancy Algorithm. Br J Cancer 2011; 104: 863-870.
54. Montagnana M, Danese E, Ruzzenente O, Bresciani V, Nuzzo T, Gelati M, Salvagno GL, Franchi M, Lippi G, Guidi GC,. The ROMA (Risk of Ovarian Malignancy Algorithm) for estimating the risk of epithelial ovarian cancer in women presenting with pelvic mass: is it really useful? Clin Chem Lab Med 2011; 49: 521-525.
55. Jacob F, Meier M, Caduff R, Goldstein D, Pochechueva T, Hacker N, Fink D, Heinzelmann-Schwarz V,. No benefit from combining HE4 and CA125 as ovarian tumor markers in a clinical setting. Gynecol Oncol 2011; 121: 487-491.
56. Van Gorp T, Veldman J, Van Calster B, Cadron I, Leunen K, Amant F, Timmerman D, Vergote I,. Subjective assessment by ultrasound is superior to the risk of malignancy index (RMI) or the risk of ovarian malignancy algorithm (ROMA) in discriminating benign from malignant adnexal masses. Eur J Cancer 2012; 48: 1649-1656.
57. Van Calster B, Valentin L, Van Holsbeke C, Testa AC, Bourne T, Van Huffel S, Timmerman D,. Polytomous diagnosis of ovarian tumors as benign, borderline, primary invasive or metastatic: development and validation of standard and kernel-based risk prediction models. BMC Med Res Methodol 2010; 10: 96.
58. Van Belle VM, Van Calster B, Timmerman D, Bourne T, Bottomley C, Valentin L, Neven P, Van Huffel S, Suykens JA, Boyd S,. A mathematical model for interpretable clinical decision support with applications in gynecology. PLoS One 2012; 7: e34312.
59. Hastie T, Tibshirani R,. Generalized Additive Models. Chapman and Hall: 1990.
60. Stiggelbout AM, Van der Weijden T, De Wit MP, Frosch D, Légaré F, Montori VM, Trevena L, Elwyn G,. Shared decision making: really putting patients at the center of healthcare. BMJ 2012; 344: e256.
61. Barry MJ, Edgman-Levitan S,. Shared decision making-pinnacle of patient-centered care. N Engl J Med 2012; 366: 780-781.
62. Valentin L, Ameye L, Jurkovic D, Metzger U, Lécuru F, Van Huffel S, Timmerman D,. Which extrauterine pelvic masses are difficult to correctly classify as benign or malignant on the basis of ultrasound findings and is there a way of making a correct diagnosis? Ultrasound Obstet Gynecol 2006; 27: 438-444.
63. Valentin L, Ameye L, Savelli L, Fruscio R, Leone FP, Czekierdowski A, Lissoni AA, Fischerova D, Guerriero S, Van Holsbeke C, Van Huffel S, Timmerman D,. Adnexal masses difficult to classify as benign or malignant using subjective assessment of gray-scale and Doppler ultrasound findings: logistic regression models do not help. Ultrasound Obstet Gynecol 2011; 38: 456-465.
64. Sladkevicius P, Jokubkiene L, Valentin L,. Contribution of morphological assessment of the vessel tree by three-dimensional ultrasound to a correct diagnosis of malignancy in ovarian masses. Ultrasound Obstet Gynecol 2007; 30: 874-882.
65. Nunes N, Yazbek J, Ambler G, Hoo W, Naftalin J, Jurkovic D,. A prospective evaluation of the IOTA Logistic Regression Model (LR2) for the diagnosis of ovarian cancer. Ultrasound Obstet Gynecol 2012; 40: 355-359.
66. Valentin L, Ameye L, Testa A, Lécuru F, Bernard JP, Paladini D, Van Huffel S, Timmerman D,. Ultrasound characteristics of different types of adnexal malignancies. Gynecol Oncol 2006; 102: 41-48.
67. Fathallah K, Huchon C, Bats AS, Metzger U, Lefrère-Belda MA, Bensaid C, Lécuru F,. External validation of simple ultrasound rules of Timmerman on 122 ovarian tumors. Gynecol Obstet Fertil 2011; 39: 477-481.