Please wait a minute...
IMR Press CEOG EJGO JIN RCM JOMH JMCM BRI
European Journal of Gynaecological Oncology  2020, Vol. 41 Issue (3): 368-374    DOI: 10.31083/j.ejgo.2020.03.5197
Original Research Previous articles | Next articles
Is the Risk of Malignancy Index a predictive tool for preoperative differentiation between borderline ovarian tumor and ovarian cancer?
S.R Oh1, J.-W. Park1()
1Department of Obstetrics and Gynecology, Dong-A University Medical Center, Dong-A University, College of Medicine, Busan, 49201, South Korea
Download:  PDF(210KB)  ( 199 ) Full text   ( 6 )
Export:  BibTeX | EndNote (RIS)      
Abstract  

Purpose: To determine an appropriate Risk of Malignancy Index (RMI) cutoff value by comparative analysisof the four malignancy risk indices for distinguishing between borderline ovarian tumor (BOT) and ovarian cancer (OC). Materials and Methods: Retrospective analysis of the medical records of 339 patients (115 BOTsand 224 OCs). Results: There were no significant differences in the area under the ROC curve (AUC) for RMI 1, RMI 2, RMI 3, and RMI 4 (0.792, 0.791, 0.785, and 0.785, respectively). However, the diagnostic capability of the RMI was significantly greater than that of other factors. Conclusion: This study is the first to investigate the performance of the four Risk of Malignancy Indices for distinguishing between BOT and invasive OC. Although there were no significant differences between RMI scores, the RMIs were very effective at predicting an accurate preoperative diagnosis in patients with all BOT and OC histotypes.
Key words:  Risk of Malignancy Index      Preoperative diagnosis      Borderline ovarian tumor      Ovarian cancer     
Submitted:  27 February 2019      Accepted:  03 June 2019      Published:  15 June 2020     
Fund: Dong-A University
*Corresponding Author(s):  J.-W. Park     E-mail:  obgypjw@dau.ac.kr
Service
E-mail this article
Add to citation manager
E-mail Alert
RSS
Articles by authors
Oh S.R   
Park J.-W.   

Cite this article: 

S.R Oh, J.-W. Park. Is the Risk of Malignancy Index a predictive tool for preoperative differentiation between borderline ovarian tumor and ovarian cancer?. European Journal of Gynaecological Oncology, 2020, 41(3): 368-374.

URL: 

https://ejgo.imrpress.com/EN/10.31083/j.ejgo.2020.03.5197     OR     https://ejgo.imrpress.com/EN/Y2020/V41/I3/368

Table 1  - Distribution of diagnosis and stages in 339 patients presenting with a BOT and OC.
Diagnosis N (%) Stage N (%)
Premenopausal (n = 174) Postmenopausal (n = 165) I II III IV Total (n = 339)
BOT?
Mucinous 58 (71.6) 26 (76.5) 84 0 0 0 84 (73.1)
Serous 21 (26.0) 4 (11.8) 24 0 0 1 25 (21.7)
Seromucinous 1 (1.2) 1 (2.9) 2 0 0 0 2 (1.7)
Clear cell 0 (0.0) 2 (5.9) 2 0 0 0 2 (1.7)
Endometrioid 1 (1.2) 0 (0.0) 1 0 0 0 1 (0.9)
Brener 0 (0.0) 1 (2.9) 1 0 0 0 1 (0.9)
Total BOT cases 81 (100) 34 (100) 114 0 0 1 115 (100)
OC?
Serous 49 (52.6) 73 (55.7) 26 7 82 7 122 (54.5)
Mucinous 15 (16.1) 15 (11.5) 20 3 7 0 30 (13.4)
Endometrioid 14 (15.1) 10 (7.6) 9 6 9 0 24 (10.7)
Clear cell 11 (11.8) 11 (8.4) 14 2 6 0 22 (9.7)
Malignant mixed müllerian tumor 2 (2.2) 5 (3.8) 2 0 4 1 7 (3.2)
Transitional cell carcinoma 1 (1.1) 6 (4.6) 2 2 3 0 7 (3.2)
Squamous cell carcinoma 1 (1.1) 3 (2.2) 2 2 0 0 4 (1.8)
Undifferentiated 0 (0.0) 3 (2.2) 2 0 1 0 3 (1.3)
Seromucinous 0 (0.0) 1 (0.8) 1 0 0 0 1 (0.4)
Peritoneal carcinoma 0 (0.0) 1 (0.8) 0 0 1 0 1 (0.4)
Small cell carcinoma 0 (0.0) 1 (0.8) 1 0 0 0 1 (0.4)
Papillary adenocarcinoma 0 (0.0) 1 (0.8) 0 0 1 0 1 (0.4)
X-müllerian adenosarcoma 0 (0.0) 1 (0.8) 0 1 0 0 1 (0.4)
Total OC cases 93 (100) 131 (100) 79 23 114 8 224 (100)
Table 2  - The distribution of BOT and OC cases by age, menopausal status, ultrasound score, tumor size, and serum CA 125.
Variables BOT OC Significance level
N 115 (33.9%) N = 224 (66.1%) Test p
Age (years) 41.37 ± 17.64 52.22 ± 14.64 χ2 < 0.001
Menopausal status
Premenopausal 81 (70.4%) 93 (41.5%) χ2 < 0.001
Postmenopausal 34 (29.6%) 131 (58.5%)
Ultrasound score χ2 < 0.001
0 7(6.1%) 0 (0%)
1 41 (35.7%) 49 (21.9%)
2 51 (44.3%) 96 (42.9%)
3 11 (9.6%) 54 (24.1%)
4
5		 5 (4.3%)
0 (0%)		 23 (10.3%)
2 (0.9%)
Tumor size 16.46 ± 8.65 11.49 ± 5.95 χ2 < 0.001
CA 125 (IU/ml) 95.41 ± 185.12 659.98 ± 831.67 U-test < 0.001
Table 3  - Sensitivity, Specificity, and Positive (PPV) and Negative (NPV) Predictive Values for predicting malignancy at different cutoff levels of four malignancy risk indices (RMI 1, RMI 2, RMI 3, and RMI 4).
Cutoff Sensitivity (%) Specificity (%) PPV (%) NPV (%)
RMI 1 170 59.1 77.2 57.1 78.6
200 65.2 75.5 57.7 80.9
230 70.4 71.4 55.9 82.5
260 73.9 69.2 55.2 83.8
290 74.8 67.0 53.8 83.8
RMI 2 280 74.8 67.9 54.4 84.0
310 74.8 66.5 53.4 83.7
340 80.0 66.1 54.8 86.6
370 80.0 65.2 54.1 86.4
400 80.0 63.4 52.9 86.1
RMI 3 170 59.1 77.2 57.1 78.7
200 65.2 75.5 57.7 80.9
230 70.4 71.4 55.9 82.5
260 73.9 69.2 55.2 83.8
290 74.8 67.0 53.8 83.8
RMI 4 530 84.4 61.2 52.7 88.4
580 86.1 61.2 53.2 89.6
630 87.8 60.7 53.4 90.7
680 88.7 58.9 52.6 91.0
730 90.4 58.0 52.5 92.2
Table 4  - The predictive performance of serum CA 125, menopausal status, tumor size, ultrasound score, and RMIs in AUROC for discrimination between BOT and OC groups.
Variables AUROC? Asymptomatic 95% Confidence Interval p-value
Lower bound Upper bound
RMI 1 0.792 0.745 0.838 < 0.001
RMI 2 0.791 0.744 0.838 < 0.001
RMI 3 0.785 0.738 0.832 < 0.001
RMI 4 0.785 0.737 0.832 < 0.001
CA 125 0.739 0.689 0.785 < 0.001
Menopause 0.645 0.591 0.696 < 0.001
Tumor size 0.672 0.620 0.722 < 0.001
Ultrasound 0.655 0.601 0.705 < 0.001
Figure 1.  — Receiver operating characteristic (ROC) curves of the individual predictors showing the relationship between sensitivity and specificity of serum CA 125 level, menopause score, tumor size, ultrasound score, and RMI in the discrimination between BOTs and OCs.

[1] Vernooij F.P.M., Witteveen P.O., van der Heiden ., van der Loo M., Coebergh J., van der Graaf Y.: "Specialized care and survival of ovarian cancer patients in The Netherlands: nationwide cohort study". J. Natl. Cancer Inst., 2008, 100, 399.
doi: 10.1093/jnci/djn033 pmid: 18334710
[2] Bristow R.E., Chang J., Ziogas A., Randall L.M., Anton Culver H.: "High-volume ovarian cancer care: survival impact and disparities in access for advanced-stage disease". Gynecol. Oncol., 2014, 132, 403.
doi: 10.1016/j.ygyno.2013.12.017
[3] Verleye L., Vergote I., Van Der Zee A.: "Patterns of care in surgery for ovarian cancer in Europe". Eur. J. Surg. Oncol., 2010, 36, 108.
[4] Trillsch F., Mahner S., Ruetzel J., Harter P., Ewald Riegler N., Jaenicke F., et al.: "Clinical management of borderline ovarian tumors". Expert. Rev. Anticancer Ther., 2010, 10, 1115.
doi: 10.1586/era.10.90 pmid: 20645700
[5] Skírnisdóttir I., Garmo H., Wilander E., Holmberg L.: "Borderline ovarian tumors in Sweden 1960-2005: trends in incidence and age at diagnosis compared to ovarian cancer". Int. J. Cancer, 2008, 123, 1897.
doi: 10.1002/ijc.23724 pmid: 18661518
[6] Sherman M.E., Mink P.J., Curtis R., Cote T.R., Brooks S., Hartge P., et al.: "Survival among women with borderline ovarian tumors and ovarian carcinoma: A population-based analysis". Cancer, 2004, 100, 1045.
doi: 10.1002/cncr.20080 pmid: 14983501
[7] Daraï E., Fauvet R., Uzan C., Gouy S., Duvillard P., Morice P.: "Fertility and borderline ovarian tumor: a systematic review of conservative management, risk of recurrence and alternative options". Hum. Reprod. Update., 2012, 19, 151.
doi: 10.1093/humupd/dms047 pmid: 23242913
[8] Jacobs I., Oram D., Fairbanks J., Turner J., Frost C., Grudzinskas J.: "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.
doi: 10.1111/j.1471-0528.1990.tb02448.x pmid: 2223684
[9] Tingulstad S., Hagen B., Skjeldestad F.E., Onsrud M., Kiserud T., Halvorsen T., et al.: "Evaluation of a risk of malignancy index based on serum CA125, ultrasound findings and menopausal status in the pre‐operative diagnosis of pelvic masses". Br. J. Obstet. Gynaecol., 1996, 103, 826.
doi: 10.1111/j.1471-0528.1996.tb09882.x pmid: 8760716
[10] Tingulstad S., Hagen B., Skjeldestad F.E., Halvorsen T., Nustad K., Onsrud M.: "The risk-of-malignancy index to evaluate potential ovarian cancers in local hospitals". Obstet. Gynecol., 1999, 93, 448.
pmid: 10074998
[11] Yamamoto Y., Yamada R., Oguri H., Maeda N., Fukaya T.: "Comparison of four malignancy risk indices in the preoperative evaluation of patients with pelvic masses". Eur. J. Obstet. Gynecol. Reprod. Biol., 2009, 144, 163.
doi: 10.1016/j.ejogrb.2009.02.048
[12] Enakpene C.A., Omigbodun A.O., Goecke T.W., Odukogbe A., Beckmann M.W.: "Preoperative evaluation and triage of women with suspicious adnexal masses using risk of malignancy index". J. Obstet. Gynaecol. Res., 2009, 35, 131.
doi: 10.1111/j.1447-0756.2008.00869.x pmid: 19215560
[13] Alanbay İ, Akturk E., Coksuer H., Ercan M., Karaşahin E., Dede M., et al.: "Comparison of risk of malignancy index (RMI), CA125, CA 19-9, ultrasound score, and menopausal status in borderline ovarian tumor". Gynecol. Endocrinol., 2012, 28, 478.
doi: 10.3109/09513590.2011.633663
[14] Yenen M.C., Alanbay I., Aktürk E., Ercan C.M., Coksuer H., Karaşahin E., et al.: "Comparison of risk of malignancy indices; RMI 1-4 in borderline ovarian tumor". Eur. J. Gynaecol. Oncol., 2012, 33, 168.
[15] FIGO Committee on Gynecologic Oncology: "Current FIGO staging for cancer of the vagina, fallopian tube, ovary, and gestational trophoblastic neoplasia". Int. J. Gynecol. Obstet., 2009, 105, 3.
doi: 10.1016/j.ijgo.2008.12.015
[16] Cadron I., Leunen K., Van Gorp T., Amant F., Neven P., Vergote I.: "Management of borderline ovarian neoplasms". J. Clin. Oncol., 2007, 25, 2928.
doi: 10.1200/JCO.2007.10.8076 pmid: 17617524
[17] Camatte S., Morice P., Atallah D., Pautier P., Lhommé C., Haie meder C., et al.: "Lymph node disorders and prognostic value of nodal involvement in patients treated for a borderline ovarian tumor: an analysis of a series of 42 lymphadenectomies". J. Am. Coll. Surg., 2002, 195, 332.
doi: 10.1016/s1072-7515(02)01250-4 pmid: 12229940
[18] Suprasert P., Khunamornpong S., Phusong A., Settakorn J., Siriaungkul S.: "Accuracy of intra-operative frozen sections in the diagnosis of ovarian masses". Asian. Pac. J. Cancer Prev., 2008, 9, 737.
pmid: 19256769
[19] Dadzan M., Tavassoli F.: "Accuracy of frozen section in borderline ovarian tumor". Rev. Clin. Med., 2015, 2, 72.
[20] Togashi K.: "Ovarian cancer: the clinical role of US, CT, and MRI". Eur.Radiol., 2003, 13, L87.
[21] Valentin L., Ameye L., Testa A., Lécuru F., Bernard J., Paladini D., et al.: "Ultrasound characteristics of different types of adnexal malignancies". Gynecol. Oncol., 2006, 102, 41.
doi: 10.1016/j.ygyno.2005.11.015 pmid: 16386783
[22] Exacoustos C., Romanini M., Rinaldo D., Amoroso C., Szabolcs B., Zupi E., et al.: "Preoperative sonographic features of borderline ovarian tumors". Ultrasound. Obstet. Gynecol., 2005, 25, 50.
doi: 10.1002/uog.1823 pmid: 15619309
[23] Emoto M., Udo T., Obama H., Eguchi F., Hachisuga T., Kawarabayashi T.: "The blood flow characteristics in borderline ovarian tumors based on both color Doppler ultrasound and histopathological analyses". Gynecol. Oncol., 1998, 70, 351.
doi: 10.1006/gyno.1998.5076 pmid: 9790787
[24] Valentin L.: "Pattern recognition of pelvic masses by gray‐scale ultrasound imaging: the contribution of Doppler ultrasound". Ultrasound Obstet. Gynecol., 1999, 14, 338.
doi: 10.1046/j.1469-0705.1999.14050338.x pmid: 10623994
[25] Fischerova D., Zikan M., Dundr P., Cibula D.: "Diagnosis, treatment, and follow-up of borderline ovarian tumors". Oncologist, 2012, 17, 1515.
doi: 10.1634/theoncologist.2012-0139
[26] deSouza N.M., O'Neill R., McIndoe G.A., Dina R., Soutter W.P.: "Borderline tumors of the ovary: CT and MRI features and tumor markers in differentiation from stage I disease". Am. J. Roentgenol., 2005, 184, 999.
doi: 10.2214/ajr.184.3.01840999
[27] Lalwani N., Shanbhogue A.K., Vikram R., Nagar A., Jagirdar J., Prasad S.R.: "Current update on borderline ovarian neoplasms". Am. J. Roentgenol., 2010, 194, 330.
doi: 10.2214/AJR.09.3936
[28] Risum S., Høgdall C., Loft A., Berthelsen A.K., Høgdall E., Nedergaard L., et al.: "The diagnostic value of PET/CT for primary ovarian cancer-a prospective study". Gynecol. Oncol., 2007, 105, 145.
doi: 10.1016/j.ygyno.2006.11.022 pmid: 17229460
[29] Jung D., Choi H., Ju W., Kim S., Choi K.: "Discordant MRI/FDG-PET imaging for the diagnosis of borderline ovarian tumors". Int. J. Gynecol. Cancer, 2008, 18, 637.
doi: 10.1111/j.1525-1438.2007.01116.x pmid: 17944914
[30] Moore R.G., Brown A.K., Miller M.C., Skates S., Allard W.J., Verch T., et al.: "The use of multiple novel tumor biomarkers for the detection of ovarian carcinoma in patients with a pelvic mass". Gynecol. Oncol., 2008, 108, 402.
doi: 10.1016/j.ygyno.2007.10.017 pmid: 18061248
[31] Moore R.G., Jabre Raughley M., Brown A.K., Robison K.M., Miller M.C., Allard W.J., et al.: "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". Obstet. Gynecol., 2010, 203, 228.
[32] Van Calster B., Van Hoorde K., Valentin L., Testa A.C., Fischerova D., Van Holsbeke C., et al.: "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". BMJ, 2014, 349, 5920.
[1] Buse Güler, Merve Çamlıbel, Samiye Mete. What Do Relatives of Turkish Women with Ovarian Cancer Share on Websites? : A Qualitative Research[J]. European Journal of Gynaecological Oncology, 2020, 41(5): 732-738.
[2] Yudi Mulyana Hidayat, Gatot Nyarumenteng Adhipurnawan Winarno, Maringan Diapari Lumban Tobing, Arieff Kustiandi, Kemala Isnainiasih Mantilidewi, Sofie Rifayani Krisnadi. The Role of Akt2 and CA-125 Serum Levels as Predictors for Successful Cytoreduction in Epithelial Ovarian Cancer Surgery[J]. European Journal of Gynaecological Oncology, 2020, 41(5): 739-744.
[3] Lingyun Zhai, Lixin Zeng, Hongru Jiang, Wei Li. Effects of a cyclooxygenase-1-selective inhibitor in combination with taxol or cisplatin on cyclin D1, apoptosis, and vascular endothelial growth factor in a xenograft model of ovarian cancer[J]. European Journal of Gynaecological Oncology, 2020, 41(5): 779-784.
[4] Qinglian Ma, Wenjie Yan, Jing Yang, Haiyan Wang, Weixiang Wang, Minghui Dong. Functional interpretation of ovarian cancer in correlation with ISGF3 expression pattern[J]. European Journal of Gynaecological Oncology, 2020, 41(5): 769-773.
[5] Silvia Ortega, José Angel Mínguez, José Manuel Aramendía, Marta Santisteban, Fernando Martinez-Regueira, Pablo Martí-Cruchaga, Juan Luis Alcázar, Matías Jurado. The impact of secondary cytoreductive surgery on survival in first recurrence of platinum sensitive epithelial ovarian cancer[J]. European Journal of Gynaecological Oncology, 2020, 41(4): 523-530.
[6] Jae Hong Sang, Soo-Ho Chung. Is it enough in ovarian cancer staging surgery to laparoscopic surgery? Comparison of surgical methods[J]. European Journal of Gynaecological Oncology, 2020, 41(4): 541-544.
[7] Sigit Purbadi, Gregorius Tanamas, Lisa Novianti. Advanced stage ovarian cancer survival in Jakarta[J]. European Journal of Gynaecological Oncology, 2020, 41(4): 587-590.
[8] Gen-Hai Zhu, Kang Wang, Lan Hong, Xin-Hui Fu, Fu-Jin Liu, Hai-Yan Huang. Safety and efficacy of fertility-sparing surgery for an orthotopic xenograft model of epithelial ovarian cancer in nude mice[J]. European Journal of Gynaecological Oncology, 2020, 41(4): 609-616.
[9] Xifang Lv, Amanguli, Ping Yang. The role of sodium hydrosulfide in the proliferation and apoptosis of exogenous SB203580 pre-treated human ovarian cancer cells[J]. European Journal of Gynaecological Oncology, 2020, 41(4): 622-628.
[10] F. Oyama, Y. Asano, H. Shimoda, K. Horie, J. Watanabe, Y. Yokoayama. Morphological analysis of peritoneal dissemination of ovarian cancer based on levels of carbonyl reductase 1 expression[J]. European Journal of Gynaecological Oncology, 2020, 41(3): 352-360.
[11] C.J. Heesterbeek, A.M. Thijs, R.H.M. Hermans, D. Boll, G.-J. Creemers. Bevacizumab in combination with metronomic oral cyclophosphamide: an effective and well-tolerated treatment for patients with recurrent ovarian cancer[J]. European Journal of Gynaecological Oncology, 2020, 41(3): 364-367.
[12] T. Shoji, E. Takatori, M. Kagabu, M. Futagami, Y. Yokoyama, H. Tokunaga, N. Yaegashi, T. Ohta, T. Watanabe, T Sugiyama. Relationship between usefulness of irinotecan and pegylated liposomal doxorubicin therapy and the UGT1A1 genotype in patients with recurrent ovarian cancer (TGCU 104 study)[J]. European Journal of Gynaecological Oncology, 2020, 41(3): 380-385.
[13] Emine Karabuk, Burak Karadag, Ceyda Karadag, M. Faruk Kose, M. Murat Naki, E. Nilufer Guler. The outcomes of fertility sparing surgery in epithelial ovarian cancer[J]. European Journal of Gynaecological Oncology, 2020, 41(3): 391-395.
[14] Chenchen Zhu, Hanyuan Liu, Zhen Shen, Yanhu Xie, Tianjiao Zhang, Björn Nashan, Dabao Wu, Ying Zhou. Treatment and survival outcomes from epithelial ovarian cancer in women aged 65 years or older[J]. European Journal of Gynaecological Oncology, 2020, 41(3): 415-421.
[15] L.D. Gutierrez-Castañeda, J.F. Polo, C. Carmona, D. Sanabria, D.M. Caballero, A. Jutinico, R. Parra-Medina. Expression of heat shock protein Hsp 27 in ovarian carcinoma[J]. European Journal of Gynaecological Oncology, 2020, 41(2): 221-226.
No Suggested Reading articles found!
ABOUT
EJGO
Editorial board
Subscriptions
Contact us
ARTICLES
Current issue
Archive
Alerts
RSS feeds
INFO FOR
Author instructions
Reviewer instructions
Reference style & template
Print ISSN: 0392-2936
Online ISSN: 2709-0086
Copyright © 2021 IMR PRESS.