Skip to main content
Top
Published in: Journal of Ovarian Research 1/2017

Open Access 01-12-2017 | Research

Identification of factors that impact recurrence in patients with borderline ovarian tumors

Authors: Xi Chen, Chenyan Fang, Tao Zhu, Ping Zhang, Aijun Yu, Shihua Wang

Published in: Journal of Ovarian Research | Issue 1/2017

Login to get access

Abstract

Background

The lack of consensus around best practices for management of borderline ovarian tumors (BOT) is, in part, to the lack of available data and of clarity in interpreting relationships among various factors that impact outcomes. The objective of this study was to identify clinicopathological factors that impact prognosis of patients with borderline ovarian tumors (BOT) and to address features of this disease with the objective of providing clarity in decision making around management of BOT.

Results

A total of 178 BOT patients were included in this study, with a median age of 43 years and a median follow-up time of 37 months. Thirty-two (18.0%) recurrences and 5 (2.8%) deaths were observed in this study group. Multivariate analysis showed that fertility-preserving surgery (P = 0.0223 for bilateral cystectomy) and invasive implants (P = 0.0030) were significantly associated with worse PFS, whereas lymphadenectomy (P = 0.0129) was related to improved PFS. No factors were found to be associated with OS due to the limited number of deaths. In addition, patients with serous BOT more commonly had abnormal levels of CA125, while patients with mucinous BOT more commonly had abnormal levels of CEA. Patients with abnormal levels of CA125, or CA19-9, or HE4 had significantly larger tumor sizes.

Conclusions

Our study reveals the impact of certain types of fertility-preserving surgery, lymphadenectomy and invasive implants on PFS of BOT patients. Blood cancer markers may be associated with histology and size of BOT. Our findings may assist in selection of optimum treatment for BOT patients.
Appendix
Available only for authorised users
Literature
1.
go back to reference Skirnisdottir 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(8):1897–901.CrossRefPubMed Skirnisdottir 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(8):1897–901.CrossRefPubMed
2.
go back to reference Akeson M, Zetterqvist BM, Dahllof K, Jakobsen AM, Brannstrom M, Horvath G. Population-based cohort follow-up study of all patients operated for borderline ovarian tumor in western Sweden during an 11-year period. Int J Gynecol Cancer. 2008;18(3):453–9.CrossRefPubMed Akeson M, Zetterqvist BM, Dahllof K, Jakobsen AM, Brannstrom M, Horvath G. Population-based cohort follow-up study of all patients operated for borderline ovarian tumor in western Sweden during an 11-year period. Int J Gynecol Cancer. 2008;18(3):453–9.CrossRefPubMed
3.
go back to reference Benedet JL, Bender H, Jones 3rd H, Ngan HY, Pecorelli S. FIGO staging classifications and clinical practice guidelines in the management of gynecologic cancers. FIGO Committee on Gynecologic Oncology. Int J Gynaecol Obstet. 2000;70(2):209–62.CrossRefPubMed Benedet JL, Bender H, Jones 3rd H, Ngan HY, Pecorelli S. FIGO staging classifications and clinical practice guidelines in the management of gynecologic cancers. FIGO Committee on Gynecologic Oncology. Int J Gynaecol Obstet. 2000;70(2):209–62.CrossRefPubMed
4.
5.
go back to reference Tinelli R, Tinelli A, Tinelli FG, Cicinelli E, Malvasi A. Conservative surgery for borderline ovarian tumors: a review. Gynecol Oncol. 2006;100(1):185–91.CrossRefPubMed Tinelli R, Tinelli A, Tinelli FG, Cicinelli E, Malvasi A. Conservative surgery for borderline ovarian tumors: a review. Gynecol Oncol. 2006;100(1):185–91.CrossRefPubMed
6.
go back to reference Trillsch F, Mahner S, Woelber L, Vettorazzi E, Reuss A, Ewald-Riegler N, de Gregorio N, Fotopoulou C, Schmalfeldt B, Burges A, et al. Age-dependent differences in borderline ovarian tumours (BOT) regarding clinical characteristics and outcome: results from a sub-analysis of the Arbeitsgemeinschaft Gynaekologische Onkologie (AGO) ROBOT study. Ann Oncol. 2014;25(7):1320–7.CrossRefPubMed Trillsch F, Mahner S, Woelber L, Vettorazzi E, Reuss A, Ewald-Riegler N, de Gregorio N, Fotopoulou C, Schmalfeldt B, Burges A, et al. Age-dependent differences in borderline ovarian tumours (BOT) regarding clinical characteristics and outcome: results from a sub-analysis of the Arbeitsgemeinschaft Gynaekologische Onkologie (AGO) ROBOT study. Ann Oncol. 2014;25(7):1320–7.CrossRefPubMed
7.
go back to reference Morris RT, Gershenson DM, Silva EG, Follen M, Morris M, Wharton JT. Outcome and reproductive function after conservative surgery for borderline ovarian tumors. Obstet Gynecol. 2000;95(4):541–7.PubMed Morris RT, Gershenson DM, Silva EG, Follen M, Morris M, Wharton JT. Outcome and reproductive function after conservative surgery for borderline ovarian tumors. Obstet Gynecol. 2000;95(4):541–7.PubMed
8.
go back to reference Tazelaar HD, Bostwick DG, Ballon SC, Hendrickson MR, Kempson RL. Conservative treatment of borderline ovarian tumors. Obstet Gynecol. 1985;66(3):417–22.PubMed Tazelaar HD, Bostwick DG, Ballon SC, Hendrickson MR, Kempson RL. Conservative treatment of borderline ovarian tumors. Obstet Gynecol. 1985;66(3):417–22.PubMed
9.
go back to reference Shih KK, Zhou Q, Huh J, Morgan JC, Iasonos A, Aghajanian C, Chi DS, Barakat RR, Abu-Rustum NR. Risk factors for recurrence of ovarian borderline tumors. Gynecol Oncol. 2011;120(3):480–4.CrossRefPubMed Shih KK, Zhou Q, Huh J, Morgan JC, Iasonos A, Aghajanian C, Chi DS, Barakat RR, Abu-Rustum NR. Risk factors for recurrence of ovarian borderline tumors. Gynecol Oncol. 2011;120(3):480–4.CrossRefPubMed
10.
go back to reference Zanetta G, Rota S, Chiari S, Bonazzi C, Bratina G, Mangioni C. Behavior of borderline tumors with particular interest to persistence, recurrence, and progression to invasive carcinoma: a prospective study. J Clin Oncol. 2001;19(10):2658–64.CrossRefPubMed Zanetta G, Rota S, Chiari S, Bonazzi C, Bratina G, Mangioni C. Behavior of borderline tumors with particular interest to persistence, recurrence, and progression to invasive carcinoma: a prospective study. J Clin Oncol. 2001;19(10):2658–64.CrossRefPubMed
11.
go back to reference Kane A, Uzan C, Rey A, Gouy S, Camatte S, Pautier P, Lhomme C, Haie-Meder C, Duvillard P, Morice P. Prognostic factors in patients with ovarian serous low malignant potential (borderline) tumors with peritoneal implants. Oncologist. 2009;14(6):591–600.CrossRefPubMed Kane A, Uzan C, Rey A, Gouy S, Camatte S, Pautier P, Lhomme C, Haie-Meder C, Duvillard P, Morice P. Prognostic factors in patients with ovarian serous low malignant potential (borderline) tumors with peritoneal implants. Oncologist. 2009;14(6):591–600.CrossRefPubMed
12.
go back to reference Uzan C, Kane A, Rey A, Gouy S, Duvillard P, Morice P. Outcomes after conservative treatment of advanced-stage serous borderline tumors of the ovary. Ann Oncol. 2010;21(1):55–60.CrossRefPubMed Uzan C, Kane A, Rey A, Gouy S, Duvillard P, Morice P. Outcomes after conservative treatment of advanced-stage serous borderline tumors of the ovary. Ann Oncol. 2010;21(1):55–60.CrossRefPubMed
13.
go back to reference Fauvet R, Boccara J, Dufournet C, David-Montefiore E, Poncelet C, Darai E. Restaging surgery for women with borderline ovarian tumors: results of a French multicenter study. Cancer. 2004;100(6):1145–51.CrossRefPubMed Fauvet R, Boccara J, Dufournet C, David-Montefiore E, Poncelet C, Darai E. Restaging surgery for women with borderline ovarian tumors: results of a French multicenter study. Cancer. 2004;100(6):1145–51.CrossRefPubMed
14.
go back to reference Obermair A, Tang A, Kondalsamy-Chennakesavan S, Ngan H, Zusterzeel P, Quinn M, Carter J, Leung Y, Janda M. Nomogram to predict the probability of relapse in patients diagnosed with borderline ovarian tumors. International journal of gynecological cancer : official journal of the International Gynecological Cancer Society. 2013;23(2):264–7.CrossRef Obermair A, Tang A, Kondalsamy-Chennakesavan S, Ngan H, Zusterzeel P, Quinn M, Carter J, Leung Y, Janda M. Nomogram to predict the probability of relapse in patients diagnosed with borderline ovarian tumors. International journal of gynecological cancer : official journal of the International Gynecological Cancer Society. 2013;23(2):264–7.CrossRef
15.
go back to reference Chen RF, Li J, Zhu TT, Yu HL, Lu X. Fertility-sparing surgery for young patients with borderline ovarian tumors (BOTs): single institution experience. J Ovarian Res. 2016;9:16.CrossRefPubMedPubMedCentral Chen RF, Li J, Zhu TT, Yu HL, Lu X. Fertility-sparing surgery for young patients with borderline ovarian tumors (BOTs): single institution experience. J Ovarian Res. 2016;9:16.CrossRefPubMedPubMedCentral
16.
go back to reference Palomba S, Zupi E, Russo T, Falbo A, Del Negro S, Manguso F, Marconi D, Tolino A, Zullo F. Comparison of two fertility-sparing approaches for bilateral borderline ovarian tumours: a randomized controlled study. Hum Reprod. 2007;22(2):578–85.CrossRefPubMed Palomba S, Zupi E, Russo T, Falbo A, Del Negro S, Manguso F, Marconi D, Tolino A, Zullo F. Comparison of two fertility-sparing approaches for bilateral borderline ovarian tumours: a randomized controlled study. Hum Reprod. 2007;22(2):578–85.CrossRefPubMed
18.
go back to reference Snider DD, Stuart GC, Nation JG, Robertson DI. Evaluation of surgical staging in stage I low malignant potential ovarian tumors. Gynecol Oncol. 1991;40(2):129–32.CrossRefPubMed Snider DD, Stuart GC, Nation JG, Robertson DI. Evaluation of surgical staging in stage I low malignant potential ovarian tumors. Gynecol Oncol. 1991;40(2):129–32.CrossRefPubMed
19.
go back to reference Winter 3rd WE, Kucera PR, Rodgers W, McBroom JW, Olsen C, Maxwell GL. Surgical staging in patients with ovarian tumors of low malignant potential. Obstet Gynecol. 2002;100(4):671–6.PubMed Winter 3rd WE, Kucera PR, Rodgers W, McBroom JW, Olsen C, Maxwell GL. Surgical staging in patients with ovarian tumors of low malignant potential. Obstet Gynecol. 2002;100(4):671–6.PubMed
20.
go back to reference Rao GG, Skinner E, Gehrig PA, Duska LR, Coleman RL, Schorge JO. Surgical staging of ovarian low malignant potential tumors. Obstet Gynecol. 2004;104(2):261–6.CrossRefPubMed Rao GG, Skinner E, Gehrig PA, Duska LR, Coleman RL, Schorge JO. Surgical staging of ovarian low malignant potential tumors. Obstet Gynecol. 2004;104(2):261–6.CrossRefPubMed
21.
go back to reference Camatte S, Morice P, Thoury A, Fourchotte V, Pautier P, Lhomme C, Duvillard P, Castaigne D. Impact of surgical staging in patients with macroscopic “stage I” ovarian borderline tumours: analysis of a continuous series of 101 cases. Eur J Cancer. 2004;40(12):1842–9.CrossRefPubMed Camatte S, Morice P, Thoury A, Fourchotte V, Pautier P, Lhomme C, Duvillard P, Castaigne D. Impact of surgical staging in patients with macroscopic “stage I” ovarian borderline tumours: analysis of a continuous series of 101 cases. Eur J Cancer. 2004;40(12):1842–9.CrossRefPubMed
22.
go back to reference Matsuo K, Machida H, Takiuchi T, Grubbs BH, Roman LD, Sood AK, Gershenson DM. Role of hysterectomy and lymphadenectomy in the management of early-stage borderline ovarian tumors. Gynecol Oncol. 2017;144(3):496–502.CrossRefPubMed Matsuo K, Machida H, Takiuchi T, Grubbs BH, Roman LD, Sood AK, Gershenson DM. Role of hysterectomy and lymphadenectomy in the management of early-stage borderline ovarian tumors. Gynecol Oncol. 2017;144(3):496–502.CrossRefPubMed
23.
go back to reference McKenney JK, Balzer BL, Longacre TA. Lymph node involvement in ovarian serous tumors of low malignant potential (borderline tumors): pathology, prognosis, and proposed classification. Am J Surg Pathol. 2006;30(5):614–24.CrossRefPubMed McKenney JK, Balzer BL, Longacre TA. Lymph node involvement in ovarian serous tumors of low malignant potential (borderline tumors): pathology, prognosis, and proposed classification. Am J Surg Pathol. 2006;30(5):614–24.CrossRefPubMed
24.
go back to reference Ureyen I, Karalok A, Tasci T, Turkmen O, Boran N, Tulunay G, Turan T. The Factors Predicting Recurrence in Patients With Serous Borderline Ovarian Tumor. International journal of gynecological cancer : official journal of the International Gynecological Cancer Society. 2016;26(1):66–72.CrossRef Ureyen I, Karalok A, Tasci T, Turkmen O, Boran N, Tulunay G, Turan T. The Factors Predicting Recurrence in Patients With Serous Borderline Ovarian Tumor. International journal of gynecological cancer : official journal of the International Gynecological Cancer Society. 2016;26(1):66–72.CrossRef
25.
go back to reference Prat J, De Nictolis M. Serous borderline tumors of the ovary: a long-term follow-up study of 137 cases, including 18 with a micropapillary pattern and 20 with microinvasion. Am J Surg Pathol. 2002;26(9):1111–28.CrossRefPubMed Prat J, De Nictolis M. Serous borderline tumors of the ovary: a long-term follow-up study of 137 cases, including 18 with a micropapillary pattern and 20 with microinvasion. Am J Surg Pathol. 2002;26(9):1111–28.CrossRefPubMed
26.
go back to reference Boran N, Cil AP, Tulunay G, Ozturkoglu E, Koc S, Bulbul D, Kose MF. Fertility and recurrence results of conservative surgery for borderline ovarian tumors. Gynecol Oncol. 2005;97(3):845–51.CrossRefPubMed Boran N, Cil AP, Tulunay G, Ozturkoglu E, Koc S, Bulbul D, Kose MF. Fertility and recurrence results of conservative surgery for borderline ovarian tumors. Gynecol Oncol. 2005;97(3):845–51.CrossRefPubMed
27.
go back to reference Park JY, Kim DY, Kim JH, Kim YM, Kim KR, Kim YT, Nam JH. Micropapillary pattern in serous borderline ovarian tumors: does it matter? Gynecol Oncol. 2011;123(3):511–6.CrossRefPubMed Park JY, Kim DY, Kim JH, Kim YM, Kim KR, Kim YT, Nam JH. Micropapillary pattern in serous borderline ovarian tumors: does it matter? Gynecol Oncol. 2011;123(3):511–6.CrossRefPubMed
28.
go back to reference Cusido M, Balaguero L, Hernandez G, Falcon O, Rodriguez-Escudero FJ, Vargas JA, Vidart JA, Zamora L, Monera M, Alonso A, et al. Results of the national survey of borderline ovarian tumors in Spain. Gynecol Oncol. 2007;104(3):617–22.CrossRefPubMed Cusido M, Balaguero L, Hernandez G, Falcon O, Rodriguez-Escudero FJ, Vargas JA, Vidart JA, Zamora L, Monera M, Alonso A, et al. Results of the national survey of borderline ovarian tumors in Spain. Gynecol Oncol. 2007;104(3):617–22.CrossRefPubMed
29.
go back to reference Morice P, Camatte S, Rey A, Atallah D, Lhomme C, Pautier P, Pomel C, Cote JF, Haie-Meder C, Duvillard P, et al. Prognostic factors for patients with advanced stage serous borderline tumours of the ovary. Ann Oncol. 2003;14(4):592–8.CrossRefPubMed Morice P, Camatte S, Rey A, Atallah D, Lhomme C, Pautier P, Pomel C, Cote JF, Haie-Meder C, Duvillard P, et al. Prognostic factors for patients with advanced stage serous borderline tumours of the ovary. Ann Oncol. 2003;14(4):592–8.CrossRefPubMed
30.
go back to reference Seidman JD, Kurman RJ. Ovarian serous borderline tumors: a critical review of the literature with emphasis on prognostic indicators. Hum Pathol. 2000;31(5):539–57.CrossRefPubMed Seidman JD, Kurman RJ. Ovarian serous borderline tumors: a critical review of the literature with emphasis on prognostic indicators. Hum Pathol. 2000;31(5):539–57.CrossRefPubMed
31.
go back to reference Bell DA, Longacre TA, Prat J, Kohn EC, Soslow RA, Ellenson LH, Malpica A, Stoler MH, Kurman RJ. Serous borderline (low malignant potential, atypical proliferative) ovarian tumors: workshop perspectives. Hum Pathol. 2004;35(8):934–48.CrossRefPubMed Bell DA, Longacre TA, Prat J, Kohn EC, Soslow RA, Ellenson LH, Malpica A, Stoler MH, Kurman RJ. Serous borderline (low malignant potential, atypical proliferative) ovarian tumors: workshop perspectives. Hum Pathol. 2004;35(8):934–48.CrossRefPubMed
32.
33.
go back to reference Trope C, Kaern J, Vergote IB, Kristensen G, Abeler V. Are borderline tumors of the ovary overtreated both surgically and systemically? A review of four prospective randomized trials including 253 patients with borderline tumors. Gynecol Oncol. 1993;51(2):236–43.CrossRefPubMed Trope C, Kaern J, Vergote IB, Kristensen G, Abeler V. Are borderline tumors of the ovary overtreated both surgically and systemically? A review of four prospective randomized trials including 253 patients with borderline tumors. Gynecol Oncol. 1993;51(2):236–43.CrossRefPubMed
34.
go back to reference Faluyi O, Mackean M, Gourley C, Bryant A, Dickinson HO. Interventions for the treatment of borderline ovarian tumours. Cochrane Database Syst Rev. 2010;9:CD007696. Faluyi O, Mackean M, Gourley C, Bryant A, Dickinson HO. Interventions for the treatment of borderline ovarian tumours. Cochrane Database Syst Rev. 2010;9:CD007696.
35.
go back to reference Sutton GP, Bundy BN, Omura GA, Yordan EL, Beecham JB, Bonfiglio T. Stage III ovarian tumors of low malignant potential treated with cisplatin combination therapy (a Gynecologic Oncology Group study). Gynecol Oncol. 1991;41(3):230–3.CrossRefPubMed Sutton GP, Bundy BN, Omura GA, Yordan EL, Beecham JB, Bonfiglio T. Stage III ovarian tumors of low malignant potential treated with cisplatin combination therapy (a Gynecologic Oncology Group study). Gynecol Oncol. 1991;41(3):230–3.CrossRefPubMed
36.
go back to reference Vasconcelos I, Olschewski J, Braicu I, Sehouli J. A meta-analysis on the impact of platinum-based adjuvant treatment on the outcome of borderline ovarian tumors with invasive implants. Oncologist. 2015;20(2):151–8.CrossRefPubMedPubMedCentral Vasconcelos I, Olschewski J, Braicu I, Sehouli J. A meta-analysis on the impact of platinum-based adjuvant treatment on the outcome of borderline ovarian tumors with invasive implants. Oncologist. 2015;20(2):151–8.CrossRefPubMedPubMedCentral
37.
go back to reference Song T, Lee YY, Choi CH, Kim TJ, Lee JW, Bae DS, Kim BG. Histologic distribution of borderline ovarian tumors worldwide: a systematic review. J Gynecol Oncol. 2013;24(1):44–51.CrossRefPubMedPubMedCentral Song T, Lee YY, Choi CH, Kim TJ, Lee JW, Bae DS, Kim BG. Histologic distribution of borderline ovarian tumors worldwide: a systematic review. J Gynecol Oncol. 2013;24(1):44–51.CrossRefPubMedPubMedCentral
38.
go back to reference Kurman RJ, Shih Ie M. Pathogenesis of ovarian cancer: lessons from morphology and molecular biology and their clinical implications. Int J Gynecol Pathol. 2008;27(2):151–60.PubMedPubMedCentral Kurman RJ, Shih Ie M. Pathogenesis of ovarian cancer: lessons from morphology and molecular biology and their clinical implications. Int J Gynecol Pathol. 2008;27(2):151–60.PubMedPubMedCentral
39.
go back to reference Messalli EM, Grauso F, Balbi G, Napolitano A, Seguino E, Torella M. Borderline ovarian tumors: features and controversial aspects. Eur J Obstet Gynecol Reprod Biol. 2013;167(1):86–9.CrossRefPubMed Messalli EM, Grauso F, Balbi G, Napolitano A, Seguino E, Torella M. Borderline ovarian tumors: features and controversial aspects. Eur J Obstet Gynecol Reprod Biol. 2013;167(1):86–9.CrossRefPubMed
40.
go back to reference Gotlieb WH, Soriano D, Achiron R, Zalel Y, Davidson B, Kopolovic J, Novikov I, Ben-Baruch G. CA 125 measurement and ultrasonography in borderline tumors of the ovary. Am J Obstet Gynecol. 2000;183(3):541–6.CrossRefPubMed Gotlieb WH, Soriano D, Achiron R, Zalel Y, Davidson B, Kopolovic J, Novikov I, Ben-Baruch G. CA 125 measurement and ultrasonography in borderline tumors of the ovary. Am J Obstet Gynecol. 2000;183(3):541–6.CrossRefPubMed
41.
go back to reference Ayhan A, Guven S, Guven ES, Kucukali T. Is there a correlation between tumor marker panel and tumor size and histopathology in well staged patients with borderline ovarian tumors? Acta Obstet Gynecol Scand. 2007;86(4):484–90.CrossRefPubMed Ayhan A, Guven S, Guven ES, Kucukali T. Is there a correlation between tumor marker panel and tumor size and histopathology in well staged patients with borderline ovarian tumors? Acta Obstet Gynecol Scand. 2007;86(4):484–90.CrossRefPubMed
42.
go back to reference Tang A, Kondalsamy-Chennakesavan S, Ngan H, Zusterzeel P, Quinn M, Carter J, Leung Y, Obermair A. Prognostic value of elevated preoperative serum CA125 in ovarian tumors of low malignant potential: a multinational collaborative study (ANZGOG0801). Gynecol Oncol. 2012;126(1):36–40.CrossRefPubMed Tang A, Kondalsamy-Chennakesavan S, Ngan H, Zusterzeel P, Quinn M, Carter J, Leung Y, Obermair A. Prognostic value of elevated preoperative serum CA125 in ovarian tumors of low malignant potential: a multinational collaborative study (ANZGOG0801). Gynecol Oncol. 2012;126(1):36–40.CrossRefPubMed
Metadata
Title
Identification of factors that impact recurrence in patients with borderline ovarian tumors
Authors
Xi Chen
Chenyan Fang
Tao Zhu
Ping Zhang
Aijun Yu
Shihua Wang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2017
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/s13048-017-0316-5

Other articles of this Issue 1/2017

Journal of Ovarian Research 1/2017 Go to the issue