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Evaluating the risk of ovarian cancer before surgery using the ADNEX model to differentiate between benign, borderline, early and advanced stage invasive, and secondary metastatic tumours: prospective multicentre diagnostic study
Open accessAbstract
OBJECTIVES: To develop a risk prediction model to preoperatively discriminate between benign, borderline, stage I invasive, stage II-IV invasive, and secondary metastatic ovarian tumours. DESIGN: Observational diagnostic study using prospectively collected clinical and ultrasound data. SETTING: 24 ultrasound centres in 10 countries. PARTICIPANTS: Women with an ovarian (including para-ovarian and tubal) mass and who underwent a standardised ultrasound examination before surgery. The model was developed on 3506 patients recruited between 1999 and 2007, temporally validated on 2403 patients recruited between 2009 and 2012, and then updated on all 5909 patients. MAIN OUTCOME MEASURES: Histological classification and surgical staging of the mass. RESULTS: The Assessment of Different NEoplasias in the adneXa (ADNEX) model contains three clinical and six ultrasound predictors: age, serum CA-125 level, type of centre (oncology centres v other hospitals), maximum diameter of lesion, proportion of solid tissue, more than 10 cyst locules, number of papillary projections, acoustic shadows, and ascites. The area under the receiver operating characteristic curve (AUC) for the classic discrimination between benign and malignant tumours was 0.94 (0.93 to 0.95) on temporal validation. The AUC was 0.85 for benign versus borderline, 0.92 for benign versus stage I cancer, 0.99 for benign versus stage II-IV cancer, and 0.95 for benign versus secondary metastatic. AUCs between malignant subtypes varied between 0.71 and 0.95, with an AUC of 0.75 for borderline versus stage I cancer and 0.82 for stage II-IV versus secondary metastatic. Calibration curves showed that the estimated risks were accurate. CONCLUSIONS: The ADNEX model discriminates well between benign and malignant tumours and offers fair to excellent discrimination between four types of ovarian malignancy. The use of ADNEX has the potential to improve triage and management decisions and so reduce morbidity and mortality associated with adnexal pathology.
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“The ADNEX model, developed by the International Ovarian Tumor Analysis (IOTA) consortium (authors BVC and DT are part of this consortium), preoperatively estimates the probability of malignancy in women with an ovarian tumour who are scheduled for surgery. 31”
From Evaluation of performance measures in predictive artificial intelligence models to support medical decisions: overview and guidance (2025) · cites this paper as [31]
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“ADNEX was developed on the data from 5909 individuals recruited between 1999 and 2012 in 24 secondary and tertiary care centres from 10 countries (Italy, Belgium, Sweden, Czech Republic, Poland, France, United Kingdom, China, Spain, and Canada).”
From Evaluation of performance measures in predictive artificial intelligence models to support medical decisions: overview and guidance (2025) · cites this paper as [31]
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Citations
Cites
(1990) · Choice Reviews Online · doi:10.5860/choice.27-3338 · Cited by 35,305
Hosmer, D. W., & Lemeshow, S. (2000) · doi:10.1002/0471722146 · Cited by 20,302
Siegel, R., Ma, J., Zou, Z., & Jemal, A. (2014) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21208 · Cited by 11,499
SEER Cancer Statistics Review, 1975-2003
Ries, L. A. G., Harkins, D., Krapcho, M. F., Mariotto, A. B., Miller, B., Feuer, E. J., Clegg, L. X., Eisner, M. P., Horner, M., Howlader, N., et al. (2006) · Digital Archive @ GSU · Cited by 11,404
Regression Modeling Strategies
Harrell, F. E. (2001) · Springer series in statistics · doi:10.1007/978-1-4757-3462-1 · Cited by 9,270
Sterne, J. A. C., White, I. R., Carlin, J. B., Spratt, M., Royston, P., Kenward, M. G., Wood, A. M., & Carpenter, J. R. (2009) · BMJ · doi:10.1136/bmj.b2393 · Cited by 7,299
Signet-Ring Cell Carcinoma of the Colon: A Case Report and Review of the Literature
Park, P. Y., Goldin, T. A., Chang, J. C. S., Markman, M. M., & Kundranda, M. N. (2015) · Case Reports in Oncology · doi:10.1159/000441772 · Cited by 5,273
Clinical Prediction Models: A Practical Approach to Development, Validation, and Updating
Steyerberg, E. W. (2019) · Statistics for Biology and Health · doi:10.1007/978-3-030-16399-0 · Cited by 3,281
Rubin, M., & Stephen, C. D. (1993) · Cited by 3,149
Rao, S. J. (2003) · Journal of the American Statistical Association · doi:10.1198/jasa.2003.s263 · Cited by 1,967
Prognosis and prognostic research: validating a prognostic model
Altman, D. G., Vergouwe, Y., Royston, P., & Moons, K. G. M. (2009) · BMJ · doi:10.1136/bmj.b605 · Cited by 1,436
Effect of Screening on Ovarian Cancer Mortality
Buys, S. S. (2011) · JAMA · doi:10.1001/jama.2011.766 · Cited by 1,326
Heintz, A. P. M., Odicino, F. E., Maisonneuve, P., QUINN, M., BENEDET, J., CREASMAN, W., Ngan, H., Pecorelli, S., & Beller, U. (2006) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(06)60033-7 · Cited by 1,277
Timmerman, D., Valentin, L., Bourne, T., Collins, W. P., Verrelst, H., & Vergote, I. B. (2000) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2000.00287.x · Cited by 999
Jacobs, I. J., Oram, D., Fairbanks, J., TURNER, J., Frost, C. D., & Grudzinskas, J. G. (1990) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1990.tb02448.x · Cited by 959
Moore, R. G., McMeekin, D. S., Brown, A., DiSilvestro, P., Miller, M. C., Allard, W. J., Gajewski, W. H., Kurman, R. J., Bast, R. C., & Skates, S. J. (2008) · Gynecologic Oncology · doi:10.1016/j.ygyno.2008.08.031 · Cited by 875
Menon, U., Gentry‐Maharaj, A., Hallett, R., Ryan, A., Burnell, M., Sharma, A., Lewis, S., Davies, S., Philpott, S., Lopes, A. D. B., et al. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(09)70026-9 · Cited by 836
Berrino, F., Angelis, R. D., Sant, M., Rosso, S., Bielska‐Lasota, M., Coebergh, J. W. W., & Santaquilani, M. (2007) · The Lancet Oncology · doi:10.1016/s1470-2045(07)70245-0 · Cited by 806
Clinical Prediction Models: A Practical Approach to Development, Validation and Updating
Mann, C. J. H. (2009) · Kybernetes · doi:10.1108/k.2009.06738fae.002 · Cited by 794
Hennessy, B. T., Coleman, R. L., & Markman, M. M. (2009) · The Lancet · doi:10.1016/s0140-6736(09)61338-6 · Cited by 645
Vergote, I. B., Brabanter, J. D., Fyles, A., Bertelsen, K., Einhorn, N., Sevelda, P., Gore, M. E., Kærn, J., Verrelst, H., SjÖvall, K., et al. (2001) · The Lancet · doi:10.1016/s0140-6736(00)03590-x · Cited by 622
Predictive value of statistical models.
Van Houwelingen, J. C., & Le Cessie, S. (1990) · Statistics in Medicine · doi:10.1002/sim.4780091109 · Cited by 621
Simple ultrasound-based rules for the diagnosis of ovarian cancer
Timmerman, D., Testa, A. C., Bourne, T., Ameye, L., Jurkovic, D., Van Holsbeke, C., Paladini, D., Van Calster, B., Vergote, I., Van Huffel, S., et al. (2008) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.5365 · Cited by 613
Self-citationRoyston, P. J., & Sauerbrei, W. (2008) · Cited by 601
Timmerman, D., Ameye, L., Fischerová, D., Epstein, E., Melis, G. B., Guerriero, S., Holsbeke, C. V., Savelli, L., Fruscio, R., Lissoni, A. A., et al. (2010) · BMJ · doi:10.1136/bmj.c6839 · Cited by 486
Timmerman, D., Testa, A. C., Bourne, T., Ferrazzi, E. M., Ameye, L., Konstantinovic, M. L., CALSTER, B. V., Collins, W. P., Vergote, I. B., Huffel, S. V., et al. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.01.7632 · Cited by 480
Effect of Surgeon Specialty on Processes of Care and Outcomes for Ovarian Cancer Patients
Earle, C. C., Schrag, D., Neville, B. A., Yabroff, K. R., Topor, M. A., Fahey, A., Trimble, E. L., Bodurka, D. C., Bristow, R. E., Carney, M. E., et al. (2006) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djj019 · Cited by 415
Surgery by consultant gynecologic oncologists improves survival in patients with ovarian carcinoma
Engelen, M. J. A., Kos, H. E., Willemse, P. H. B., Aalders, J. G., de Vries, E. G. E., Schaapveld, M., Otter, R., & van der Zee, A. G. J. (2005) · Cancer · doi:10.1002/cncr.21616 · Cited by 305
A randomized study of screening for ovarian cancer: a multicenter study in Japan
Kobayashi, H., YAMADA, Y., Sado, T., Sakata, M., Yoshida, S., Kawaguchi, R., Kanayama, S., Shigetomi, H., Haruta, S., Tsuji, Y., et al. (2007) · International Journal of Gynecological Cancer · doi:10.1111/j.1525-1438.2007.01035.x · Cited by 276
Adherence to Treatment Guidelines for Ovarian Cancer as a Measure of Quality Care
Bristow, R. E., Chang, J. J., Ziogas, A., & Anton‐Culver, H. (2013) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e3182922a17 · Cited by 223
Kaijser, J., Sayasneh, A., Hoorde, K. V., Ghaem‐Maghami, S., Bourne, T., Timmerman, D., & CALSTER, B. V. (2013) · Human Reproduction Update · doi:10.1093/humupd/dmt059 · Cited by 219
Kaijser, J., Bourne, T., Valentin, L., Sayasneh, A., Holsbeke, C. V., Vergote, I. B., Testa, A. C., Franchi, D., CALSTER, B. V., & Timmerman, D. (2012) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.12323 · Cited by 199
Daraï, É., Fauvet, R., Uzan, C., Gouy, S., Duvillard, P., & Morice, P. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms047 · Cited by 199
Timmerman, D., CALSTER, B. V., Testa, A. C., Guerriero, S., Fischerová, D., Lissoni, A. A., Holsbeke, C. V., Fruscio, R., Czekierdowski, A., Jurkovic, D., et al. (2010) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7636 · Cited by 197
Bristow, R. E., Chang, J. J., Ziogas, A., Randall, L. M., & Anton‐Culver, H. (2013) · Gynecologic Oncology · doi:10.1016/j.ygyno.2013.12.017 · Cited by 172
European Federation of Societies for Ultrasound in Medicine and Biology
(2006) · Ultraschall in der Medizin - European Journal of Ultrasound · doi:10.1055/s-2006-933605 · Cited by 147
Centralisation of services for gynaecological cancers — A Cochrane systematic review
Woo, Y. L., Kyrgiou, M., Bryant, A., Everett, T. R., & Dickinson, H. O. (2012) · Gynecologic Oncology · doi:10.1016/j.ygyno.2012.04.012 · Cited by 133
Testa, A. C., Kaijser, J., Wynants, L., Fischerová, D., Holsbeke, C. V., Franchi, D., Savelli, L., Epstein, E., Czekierdowski, A., Guerriero, S., et al. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.333 · Cited by 121
Holsbeke, C. V., CALSTER, B. V., Testa, A. C., Domali, E., Lü, C., Huffel, S. V., Valentin, L., & Timmerman, D. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0113 · Cited by 113
Multicentre external validation of IOTA prediction models and RMI by operators with varied training
Sayasneh, A., Wynants, L., Preisler, J., Kaijser, J., Johnson, S., Stalder, C. M., Husicka, R., Abdallah, Y., Raslan, F., Drought, A., et al. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.224 · Cited by 112
Jacobs, I. J., Oram, D., Fairbanks, J., Turner, J. E., Frost, C. D., & Grudzinskas, J. G. (1991) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(91)90345-6 · Cited by 111
Pejovic, T. B., & Nezhat, F. R. (2011) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2011.07.013 · Cited by 107
Timmerman, D., CALSTER, B. V., Jurkovic, D., Valentin, L., Testa, A. C., Bernard, J. P., Holsbeke, C. V., Huffel, S. V., Vergote, I. B., & Bourne, T. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.09.5943 · Cited by 96
Extending the c‐statistic to nominal polytomous outcomes: the Polytomous Discrimination Index
CALSTER, B. V., Belle, V. V., Vergouwe, Y., Timmerman, D., Huffel, S. V., & Steyerberg, E. W. (2012) · Statistics in Medicine · doi:10.1002/sim.5321 · Cited by 94
Specialized Care and Survival of Ovarian Cancer Patients in The Netherlands: Nationwide Cohort Study
Vernooij, F., Heintz, A. P. M., Witteveen, P. O., der Loo, M. V. D. H., Coebergh, J. W. W., & van der Graaf, Y. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn033 · Cited by 92
Assessing the discriminative ability of risk models for more than two outcome categories
CALSTER, B. V., Vergouwe, Y., Looman, C. W. N., Belle, V. V., Timmerman, D., & Steyerberg, E. W. (2012) · European Journal of Epidemiology · doi:10.1007/s10654-012-9733-3 · Cited by 92
Assessing calibration of multinomial risk prediction models
Hoorde, K. V., Vergouwe, Y., Timmerman, D., Huffel, S. V., Steyerberg, E. W., & CALSTER, B. V. (2014) · Statistics in Medicine · doi:10.1002/sim.6114 · Cited by 65
A note on the estimation of the multinomial logistic model with correlated responses in SAS
Kuß, O., & McLerran, D. (2007) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2007.06.002 · Cited by 64
Comparison of seven immunoassays for the quantification of CA 125 antigen in serum
Davelaar, E. M., van Kamp, G. J., Verstraeten, R. A., & Kenemans, P. (1998) · Clinical Chemistry · doi:10.1093/clinchem/44.7.1417 · Cited by 50
Patterns of care in surgery for ovarian cancer in Europe
Verleye, L., Vergote, I. B., & van der Zee, A. G. J. (2010) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2010.06.006 · Cited by 45
CALSTER, B. V., Valentin, L., Holsbeke, C. V., Zhang, J., Jurkovic, D., Lissoni, A. A., Testa, A. C., Czekierdowski, A., Fischerová, D., Domali, E., et al. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0422 · Cited by 41
Dungan, J. S. (2011) · Yearbook of Obstetrics Gynecology and Women s Health · doi:10.1016/j.yobg.2011.05.044 · Cited by 39
CALSTER, B. V., Valentin, L., Holsbeke, C. V., Testa, A. C., Bourne, T., Huffel, S. V., & Timmerman, D. (2010) · BMC Medical Research Methodology · doi:10.1186/1471-2288-10-96 · Cited by 37
A Randomized Study of Screening for Ovarian Cancer: A Multicenter Study in Japan
Kobayashi, H., Yamada, Y., Sado, T., Sakata, M., Yoshida, S., Kawaguchi, R., Kanayama, S., Shigetomi, H., Haruta, S., Tsuji, Y., et al. (2008) · Obstetrical & Gynecological Survey · doi:10.1097/01.ogx.0000333238.05419.56 · Cited by 29
Screening for data clustering in multicenter studies: the residual intraclass correlation
Wynants, L., Timmerman, D., Bourne, T., Huffel, S. V., & CALSTER, B. V. (2013) · BMC Medical Research Methodology · doi:10.1186/1471-2288-13-128 · Cited by 27 · cited 1×
“to what extent the values of the variables varied between centres after controlling for tumour histology, in order to favour predictors with limited heterogeneity.(5) Finally, we aimed to include some baseline information on centre type, in order to improve the calibration of the estimated probabilities.”
BackgroundNunes, N., Ambler, G., Hoo, W., Naftalin, J., Foo, X., Widschwendter, M., & Jurkovic, D. (2013) · International Journal of Gynecological Cancer · doi:10.1097/igc.0b013e3182a6171a · Cited by 18
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Andreotti, R. F., Timmerman, D., Strachowski, L. M., Froyman, W., Benacerraf, B. R., Bennett, G. L., Bourne, T., Brown, D. L., Coleman, B. G., Frates, M. C., et al. (2019) · Radiology · doi:10.1148/radiol.2019191150 · Cited by 530
van den Goorbergh, R., van Smeden, M., Timmerman, D., & CALSTER, B. V. (2022) · Journal of the American Medical Informatics Association · doi:10.1093/jamia/ocac093 · Cited by 427
Timmerman, D., CALSTER, B. V., Testa, A. C., Savelli, L., Fischerová, D., Froyman, W., Wynants, L., Holsbeke, C. V., Epstein, E., Franchi, D., et al. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.01.007 · Cited by 337
Meys, E. M. J., Kaijser, J., Kruitwagen, R. F. P. M., Slangen, B. F. M., CALSTER, B. V., Aertgeerts, B., Verbakel, J. Y. J., Timmerman, D., & Gorp, T. V. (2016) · European Journal of Cancer · doi:10.1016/j.ejca.2016.01.007 · Cited by 281
“Someof thesehavenotbeenvalidatedextensivelybut seem promising, such as the ADNEX-model [83].”
BackgroundClinical Use of Cancer Biomarkers in Epithelial Ovarian Cancer
Sölétormos, G., Duffy, M. J., Hassan, S. O. A., Verheijen, R. H. M., Tholander, B., Bast, R. C., Gaarenstroom, K. N., Sturgeon, C. M., Bonfrèr, J. M. G., Petersen, P. H., et al. (2015) · International Journal of Gynecological Cancer · doi:10.1097/igc.0000000000000586 · Cited by 255
“Assessment of Different NEoplasias in the adneXa.(33) The National Institute for Health and Care Excellence has introduced guidelines for early detection of ovarian cancer in symptomatic women for use by general practitioners.”
Metadata
- Authors
- Van Calster, B., Van Hoorde, K., Valentin, L., Testa, A. C., Fischerova, D., Van Holsbeke, C., Savelli, L., Franchi, D., Epstein, E., Kaijser, J., Van Belle, V., Czekierdowski, A., Guerriero, S., Fruscio, R., Lanzani, C., Scala, F., Bourne, T., Timmerman, D., & International Ovarian Tumour Analysis (IOTA) group
- Affiliations
- Lund University (SE)
- Università Cattolica del Sacro Cuore (IT)
- IRCCS Azienda Ospedliero-Universitaria di Bologna Policlinico di Sant'Orsola (IT)
- European Institute of Oncology (IT)
- Karolinska University Hospital (SE)
- Universitair Ziekenhuis Leuven (BE)
- Medical University of Lublin (PL)
- Azienda Ospedaliero-Universitaria Cagliari (IT)
- University of Milan (IT)
- Istituto Nazionale Tumori IRCCS "Fondazione G. Pascale" (IT)
- ORCID
- Venue
- BMJ
- Publisher
- BMJ
- Published
- 2014-10-15
- Volume
- 349
- Issue
- oct07 3
- Pages
- g5920-g5920
- ISSN
- 1756-1833 (ISSN-L)
- PMC
- PMC4198550
- OpenAlex
- W2099878111
- Cited by
- 510
- References
- 57
- Citations by year
- 2026: 52 · 2025: 60 · 2024: 70 · 2023: 54 · 2022: 55 · 2021: 59 · 2020: 36 · 2019: 24 · 2018: 30 · 2017: 19 · 2016: 27 · 2015: 19 · 2014: 4
- FWCI
- 27.87
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- BMJ (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion, cc-by-nc)
- Lirias (KU Leuven) (submittedVersion, cc-by-nc)
- UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion, other-oa)
- Lund University Publications (Lund University) (submittedVersion, other-oa)
- HighWire Press Open Archive (submittedVersion)
- PubliCatt (Università Cattolica del Sacro Cuore) (submittedVersion, cc-by-nc)
- Spiral (Imperial College London) (submittedVersion, other-oa)
- Funders
- National Institute for Health and Care Research
- Imperial College London
- Imperial College Healthcare NHS Trust
- Fonds Wetenschappelijk Onderzoek (G049312N)
- iMinds
- Malmö Högskola
- Skånes universitetssjukhus
- Vlaamse regering (G049312N)
- Medical Research Council
- Topics
- Health Sciences › Medicine › Oncology › Ovarian cancer diagnosis and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
- Health Sciences › Medicine › Pathology and Forensic Medicine › Breast Lesions and Carcinomas
- Keywords
- ovarian cancer, ADNEX model, preoperative risk prediction, ovarian ultrasonography, borderline ovarian tumors, CA125, surgical staging, adnexal mass, triage
- MeSH terms
- Adnexal Diseases, Adult, Female, Humans, Neoplasm Staging, Ovarian Neoplasms, Predictive Value of Tests, Prospective Studies, Ultrasonography, Models, Statistical, Risk Assessment
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