Fertility Sparing Surgery and Borderline Ovarian Tumours
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
Statistical Analysis
3. Results
3.1. Recurrence of BOTs
3.1.1. Serous Borderline Ovarian Tumours
3.1.2. Sero-Mucinous Borderline Ovarian Tumours
4. Discussion
4.1. Ultrasound-Guided Ovarian Wedge Resection
4.2. Reproductive Outcomes
4.3. Strengths and Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Lheureux, S.; Braunstein, M.; Oza, A.M. Epithelial ovarian cancer: Evolution of management in the era of precision medicine. CA Cancer J. Clin. 2019, 69, 280–304. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Delle Marchette, M.; Ceppi, L.; Andreano, A.; Bonazzi, C.M.; Buda, A.; Grassi, T.; Giuliani, D.; Sina, F.; Lamanna, M.; Bianchi, T.; et al. Oncologic and fertility impact of surgical approach for borderline ovarian tumours treated with fertility sparing surgery. Eur. J. Cancer 2019, 111, 61–68. [Google Scholar] [CrossRef]
- Fischerova, D.; Zikan, M.; Dundr, P.; Cibula, D. Diagnosis, treatment, and follow-up of borderline ovarian tumors. Oncologist 2012, 17, 1515. [Google Scholar] [CrossRef] [Green Version]
- Maramai, M.; Barra, F.; Menada, M.V.; Stigliani, S.; Moioli, M.; Costantini, S.; Ferrero, S. Borderline ovarian tumours: Management in the era of fertility-sparing surgery. Ecancermedicalscience 2020, 14, 1031. [Google Scholar] [CrossRef] [PubMed]
- Tropé, C.G.; Kaern, J.; Davidson, B. Borderline ovarian tumours. Best Pract. Res. Clin. Obstet. Gynaecol. 2012, 26, 325–336. [Google Scholar] [CrossRef]
- Gershenson, D.M. Management of borderline ovarian tumours. Best Pract. Res. Clin. Obstet. Gynaecol. 2017, 41, 49–59. [Google Scholar] [CrossRef]
- Hauptmann, S.; Friedrich, K.; Redline, R.; Avril, S. Ovarian borderline tumors in the 2014 WHO classification: Evolving concepts and diagnostic criteria. Virchows Arch. 2017, 470, 125–142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abascal-Saiz, A.; Sotillo-Mallo, L.; de Santiago, J.; Zapardiel, I. Management of borderline ovarian tumours: A comprehensive review of the literature. Ecancermedicalscience 2014, 8, 403. [Google Scholar]
- Du Bois, A.d.; Ewald-Riegler, N.; Du Bois, O.; Harter, P. Borderline tumors of the ovary-a systematic review. Geburtshilfe Frauenheilkd. 2009, 69, 807–833. [Google Scholar] [CrossRef]
- 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, 330–336. [Google Scholar] [CrossRef] [PubMed]
- Gouthaman, S.; Kothari, S.; Vijayaraghavan, J.; Pitani, R.S. Analysis of Morbidity, Mortality and Survival Pattern Following Surgery for Borderline Ovarian and Malignant Ovarian Tumour in Tertiary Care Centre. J. Obstet. Gynecol. India 2021, 71, 297–303. [Google Scholar] [CrossRef]
- Huchon, C.; Bourdel, N.; Wahab, C.A.; Azaïs, H.; Bendifallah, S.; Bolze, P.A.; Brun, J.L.; Canlorbe, G.; Chauvet, P.; Chereau, E.; et al. Borderline ovarian tumors: French guidelines from the CNGOF. Part 1. Epidemiology, biopathology, imaging and biomarkers. J. Gynecol. Obstet. Hum. Reprod. 2021, 50, 101965. [Google Scholar] [CrossRef] [PubMed]
- Morice, P. Borderline tumours of the ovary and fertility. Eur. J. Cancer 2006, 42, 149–158. [Google Scholar] [CrossRef]
- Burger, C.; Prinssen, H.; Baak, J.; Wagenaar, N.; Kenemans, P. The management of borderline epithelial tumors of the ovary. Int. J. Gynecol. Cancer 2000, 10, 181–197. [Google Scholar] [CrossRef]
- 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, 1897–1901. [Google Scholar] [CrossRef] [PubMed]
- Jones, B.P.; Saso, S.; Farren, J.; El-Bahrawy, M.; Ghaem-Maghami, S.; Smith, J.R.; Yazbek, J. Ultrasound-guided laparoscopic ovarian wedge resection in recurrent serous borderline ovarian tumours. Int. J. Gynecol. Cancer 2017, 27, 1813–1818. [Google Scholar] [CrossRef] [PubMed]
- Jones, B.; Saso, S.; Farren, J.; El-Bahrawy, M.; Smith, J.; Yazbek, J. Intraoperative ultrasound-guided laparoscopic ovarian-tissue-preserving surgery for recurrent borderline ovarian tumor. Ultrasound Obstet. Gynecol. 2017, 50, 405–406. [Google Scholar] [CrossRef] [PubMed]
- Uzan, C.; Muller, E.; Kane, A.; Rey, A.; Gouy, S.; Bendiffallah, S.; Duvillard, P.; Fauvet, R.; Darai, E.; Morice, P. Prognostic factors for recurrence after conservative treatment in a series of 119 patients with stage I serous borderline tumors of the ovary. Ann. Oncol. 2014, 25, 166–171. [Google Scholar] [CrossRef]
- Trillsch, F.; Mahner, S.; Ruetzel, J.D.; Harter, P.; Ewald-Riegler, N.; Jaenicke, F.; Du Bois, A. Clinical management of borderline ovarian tumors. Expert Rev. Anticancer. Ther. 2010, 10, 1115–1124. [Google Scholar] [CrossRef]
- Donnez, J.; Munschke, A.; Berliere, M.; Pirard, C.; Jadoul, P.; Smets, M.; Squifflet, J. Safety of conservative management and fertility outcome in women with borderline tumors of the ovary. Fertil. Steril. 2003, 79, 1216–1221. [Google Scholar] [CrossRef]
- Morice, P.; Camatte, S.; El Hassan, J.; Pautier, P.; Duvillard, P.; Castaigne, D. Clinical outcomes and fertility after conservative treatment of ovarian borderline tumors. Fertil. Steril. 2001, 75, 92–96. [Google Scholar] [PubMed]
- Pereira, A.; Pérez-Medina, T.; Magrina, J.F.; Magtibay, P.M.; Rodríguez-Tapia, A.; Peregrin, I.; Mendizabal, E.; Ortiz-Quintana, L. International Federation of gynecology and obstetrics staging classification for cancer of the ovary, fallopian tube, and peritoneum: Estimation of survival in patients with node-positive epithelial ovarian cancer. Int. J. Gynecol. Cancer 2015, 25, 49–54. [Google Scholar] [CrossRef]
- Fauvet, R.; Boccara, J.; Dufournet, C.; Poncelet, C.; Darai, E. Laparoscopic management of borderline ovarian tumors: Results of a French multicenter study. Ann. Oncol. 2005, 16, 403–410. [Google Scholar]
- Plett, H.; Harter, P.; Ataseven, B.; Heitz, F.; Prader, S.; Schneider, S.; Heikaus, S.; Fisseler-Eckhoff, A.; Kommoss, F.; Lax, S.F.; et al. Fertility-sparing surgery and reproductive-outcomes in patients with borderline ovarian tumors. Gynecol. Oncol. 2020, 157, 411–417. [Google Scholar] [CrossRef] [PubMed]
- Lou, T.; Yuan, F.; Feng, Y.; Wang, S.; Bai, H.; Zhang, Z. The safety of fertility and ipsilateral ovary procedures for borderline ovarian tumors. Oncotarget 2017, 8, 115718. [Google Scholar] [CrossRef]
- Romagnolo, C.; Gadducci, A.; Sartori, E.; Zola, P.; Maggino, T. Management of borderline ovarian tumors: Results of an Italian multicenter study. Gynecol. Oncol. 2006, 101, 255–260. [Google Scholar] [CrossRef]
- Morice, P.; Uzan, C.; Fauvet, R.; Gouy, S.; Duvillard, P.; Darai, E. Borderline ovarian tumour: Pathological diagnostic dilemma and risk factors for invasive or lethal recurrence. Lancet Oncol. 2012, 13, e103–e115. [Google Scholar] [CrossRef]
- De Gregorio, N.; Baumann, K.H.; Keyver-Paik, M.D.; Reuss, A.; Canzler, U.; Wollschlaeger, K.; Kommoss, F.; Forner, D.; Peters, M.; Schroeder, W.; et al. Outcome of patients with borderline ovarian tumors: Results of the multicenter AGO ROBOT study. Am. Soc. Clin. Oncol. 2012, 30, 5005. [Google Scholar]
- Du Bois, A.; Ewald-Riegler, N.; de Gregorio, N.; Reuss, A.; Mahner, S.; Fotopoulou, C.; Kommoss, F.; Schmalfeldt, B.; Hilpert, F.; Fehm, T.; et al. Borderline tumours of the ovary: A cohort study of the Arbeitsgemeinschaft Gynäkologische Onkologie (AGO) Study Group. Eur. J. Cancer 2013, 49, 1905–1914. [Google Scholar]
- Karlsen, N.M.S.; Karlsen, M.A.; Høgdall, E.; Nedergaard, L.; Christensen, I.J.; Høgdall, C. Relapse and disease specific survival in 1143 Danish women diagnosed with borderline ovarian tumours (BOT). Gynecol. Oncol. 2016, 142, 50–53. [Google Scholar] [CrossRef]
- 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, 2658–2664. [Google Scholar]
- Park, J.-Y.; Kim, D.-Y.; Kim, J.-H.; Kim, Y.-M.; Kim, Y.-T.; Nam, J.-H. Surgical management of borderline ovarian tumors: The role of fertility-sparing surgery. Gynecol. Oncol. 2009, 113, 75–82. [Google Scholar] [CrossRef] [PubMed]
- Yinon, Y.; Beiner, M.E.; Gotlieb, W.H.; Korach, Y.; Perri, T.; Ben-Baruch, G. Clinical outcome of cystectomy compared with unilateral salpingo-oophorectomy as fertility-sparing treatment of borderline ovarian tumors. Fertil. Steril. 2007, 88, 479–484. [Google Scholar] [CrossRef]
- Vasconcelos, I.; de Sousa Mendes, M. Conservative surgery in ovarian borderline tumours: A meta-analysis with emphasis on recurrence risk. Eur. J. Cancer 2015, 51, 620–631. [Google Scholar] [CrossRef] [PubMed]
- Kuroda, M.; Kuroda, K.; Arakawa, A.; Fukumura, Y.; Kitade, M.; Kikuchi, I.; Kumakiri, J.; Matsuoka, S.; Brosens, I.A.; Brosens, J.J.; et al. Histological assessment of impact of ovarian endometrioma and laparoscopic cystectomy on ovarian reserve. J. Obstet. Gynaecol. Res. 2012, 38, 1187–1193. [Google Scholar] [PubMed]
- Jones, B.; Rees, R.; Saso, S.; Stalder, C.; Smith, J.; Yazbek, J. Ultrasound-guided laparoscopic ovarian preserving surgery to treat anti-NMDA receptor encephalitis. BJOG Int. J. Obstet. Gynaecol. 2017, 124, 337–341. [Google Scholar]
- Darai, E.; Teboul, J.; Fauconnier, A.; Scoazec, J.-Y.; Benifla, J.; Madelenat, P. Management and outcome of borderline ovarian tumors incidentally discovered at or after laparoscopy. Acta Obstet. Gynecol. Scand. 1998, 77, 451–457. [Google Scholar]
- Candotti, G.; Peiretti, M.; Mangili, G.; Bergamini, A.; Candiani, M.; Cioffi, R.; Mais, V.; Rabaiotti, E.; Bocciolone, L. What women want: Fertility sparing surgery in borderline ovarian tumours patients and pregnancy outcome. Eur. J. Surg. Oncol. 2020, 46, 888–892. [Google Scholar] [PubMed]
Feature | FSS n (%) | Non-FSS n (%) |
---|---|---|
Unilocular solid | 14 (15.6%) | 21 (25.6%) |
Unilocular | 3 | 2 |
(3.3%) | (2.4%) | |
Multilocular | 17 (18.9%) | 14 (17.1%) |
Other features | 2 (2.2%) | 2 (2.4%) |
Data unattainable | 54 (60.0%) | 43 (52.4%) |
Median maximum diameter (mm) (IQR) | 115 (104.0) | 110 (104.5) |
Feature | FSS n (%) | Non-FSS n (%) |
---|---|---|
Other histological feature | 16 (17.8%) | 26 (31.7%) |
Microinvasion | 9 (10.0%) | 8 (9.8%) |
Micro-papillary pattern | 14 (15.6%) | 14 (17.1%) |
Implants | 8 (8.9%) | 11 (13.4%) |
Data unattainable | 43 (47.8%) | 23 (28.0%) |
Staging | ||
1 | 69 (76.7%) | 60 (73.1%) |
2 | 4 (4.4%) | 5 (6.1%) |
3 | 5 (5.5%) | 14 (17.1%) |
4 | 1 (1.1%) | 1 (1.2%) |
Data unattainable | 11 (12.2%) | 2 (2.4%) |
Surgery n (%) | Serous (n = 120) | Mucinous (n = 43) | Sero-Mucinous (n = 9) | p Value |
---|---|---|---|---|
Laparotomy | 88 (73.3%) | 34 (79.1%) | 6 (66.6%) | 0.689 |
Laparoscopy | 32 (26.7%) | 9 (20.9%) | 3 (33.3%) | 0.737 |
Fertility-Sparing Surgery | 54 (45.0%) | 30 (69.8%) | 6 (66.7%) | 0.666 |
Complete Debulking | 66 (55.0%) | 13 (30.2%) | 3 (33.3%) | 0.009 * |
Disease Removed Intact | 117 (97.5%) | 41 (95.3%) | 9 (100%) | 0.013 * |
Residual Disease | 3 (2.5%) | 2 (4.7%) | 0 | 0.000 * |
Fertility-Sparing Surgery | ||||
Unilateral Salpingo-oophorectomy | 11 (9.2%) | 5 (11.6%) | 4 (44.4%) | 0.001 * |
Ovarian Cystectomy | 24 (20.0%) | 9 (20.9%) | 0 | 0.001 * |
Ultrasound-guided ovarian wedge resection | 3 (2.5%) | 0 | 1 (11.1%) | 0.203 |
Type of Surgery | Total Number Performed | Number of Recurrences | Recurrence Rate (%) |
---|---|---|---|
Unilateral salpingo-oophorectomy | 20 | 6 | 30.0 |
Ovarian cystectomy | 33 | 10 | 30.3 |
Ultrasound-guided ovarian wedge resection | 4 | 0 | 0 |
Other fertility-sparing surgical procedure (including combined procedures) | 33 | 7 | 21.2 |
All fertility-sparing surgery | 90 | 23 | 25.6 |
Complete debulking | 78 | 6 | 7.7 |
Not documented | 4 | 0 | 0 |
Fertility Sparing Surgery | X2 | p Value |
---|---|---|
Unilateral salpingo-oophorectomy v. Ovarian cystectomy | 2.93 | 0.182 |
Unilateral salpingo-oophorectomy v. Ultrasound-guided ovarian wedge resection | Non calculable | Non calculable |
Ultrasound-guided ovarian wedge resection v. Ovarian cystectomy | Non calculable | Non calculable |
Fertility-sparing surgery v. non-fertility-sparing surgery | 20.61 | 0.000 * |
Variable | X2 | p Value |
---|---|---|
Type of surgery (e.g., Fertility Sparing Surgery or Non-Fertility Sparing Surgery) | 9.9 | 0.002 * |
Age at diagnosis | 7.0 | 0.99 |
Histological subtype at diagnosis | 21.5 | 0.000 * |
Staging of disease at diagnosis | 8.0 | 0.87 |
Reproductive Outcome | Serous (n = 120) | Mucinous (n = 43) | Sero-Mucinous (n = 9) | Total (n) |
---|---|---|---|---|
Total number of pregnancies (n) | ||||
Spontaneous and IVF | 37 | 15 | 3 | 55 |
Spontaneous pregnancies only n (%) | ||||
Total number of women of reproductive age achieving pregnancy | 15/68 (22.1%) | 6/31 (19.4%) | 2/7 (28.6%) | 23/106 (21.6%) |
Total number of spontaneous conceptions by women achieving spontaneous pregnancy (n) | 30 | 11 | 2 | 43 |
Outcome of spontaneous pregnancies (per conception) n (%) | ||||
Miscarriage | 7 (23.3%) | 5 (45.4%) | 0 | 12/43 (27.9%) |
Successful livebirth | 23 (76.7%) | 6 (54.5%) | 2 (100%) | 31/43 (72.1%) |
IVF pregnancies only n (%) | ||||
Number of women attempting IVF | 7/68 (10.3%) | 2/31 (6.5%) | 1/7 (14.3%) | 10/106 (9.4%) |
Number of cycles | 7 | 4 | 1 | 12 |
Outcome of IVF pregnancies (per cycle) n (%) | ||||
Miscarriage | 1 (14.3%) | 2 (50.0%) | 1 (100%) | 4/12 (33.3%) |
Successful livebirth | 5 (71.4%) | 1 (25.0%) | 0 | 6/12 (50.0%) |
Unsuccessful implantation | 1 (14.3%) | 0 | 0 | 1/12 (8.3%) |
Ectopic pregnancy | 0 | 1 (25.0%) | 0 | 1/12 (8.3%) |
Patient | Age | Gravida | Parity | Initial Surgery | 1st Recurrence | 2nd Recurrence | 3rd Recurrence | Attempt of Pregnancy after FSS | Cryopreserved Oocytes or Embryo Post-FSS | No. of Pregnancies after FSS | Pregnancy Outcome after FSS |
---|---|---|---|---|---|---|---|---|---|---|---|
Serous | |||||||||||
1 | 38 | 0 | 0 | UGOWR | - | - | - | No | No | 0 | - |
2 | 22 | 0 | 0 | UGOWR | - | - | - | No | No | 0 | - |
3 | 29 | 0 | 0 | UGOWR | - | - | - | No | No | 0 | - |
4 | 30 | 0 | 0 | USO and contralateral UGOWR | USO and total Infra-colic Omenectomy | - | - | No | Yes | 0 | - |
5 | 23 | 0 | 0 | Infra-colectomy, ablation of pelvic deposits & UGOWR | - | - | - | No | Yes | 0 | - |
6 | 33 | 3 | 2 | USO | UGOWR | Conservative | - | Yes | No | 1 (Spontaneous) | Miscarriage |
7 | 23 | 0 | 0 | USO | UGOWR | - | - | Yes | Yes | 1 (IVF Twins) | Livebirth |
8 | 35 | 1 | 1 | Ovarian Cystectomy | UGOWR | UGOWR | UGOWR | Yes | Yes | 1 (Spontaneous) | Livebirth |
9 | 31 | 0 | 0 | Partial Oophorectomy | UGOWR | Conservative | - | Yes | Yes | 0 | - |
10 | 33 | 0 | 0 | Ovarian Cystectomy | UGOWR | - | - | No | Yes | 0 | - |
11 | 22 | 0 | 0 | USO and contralateral ovarian biopsy | UGOWR | - | - | No | Yes | 0 | - |
Sero-Mucinous | |||||||||||
12 | 26 | 0 | 0 | UGOWR | - | - | - | No | No | 0 | - |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kasaven, L.S.; Chawla, M.; Jones, B.P.; Al-Memar, M.; Galazis, N.; Ahmed-Salim, Y.; El-Bahrawy, M.; Lavery, S.; Saso, S.; Yazbek, J. Fertility Sparing Surgery and Borderline Ovarian Tumours. Cancers 2022, 14, 1485. https://doi.org/10.3390/cancers14061485
Kasaven LS, Chawla M, Jones BP, Al-Memar M, Galazis N, Ahmed-Salim Y, El-Bahrawy M, Lavery S, Saso S, Yazbek J. Fertility Sparing Surgery and Borderline Ovarian Tumours. Cancers. 2022; 14(6):1485. https://doi.org/10.3390/cancers14061485
Chicago/Turabian StyleKasaven, Lorraine S., Mehar Chawla, Benjamin P. Jones, Maya Al-Memar, Nicolas Galazis, Yousra Ahmed-Salim, Mona El-Bahrawy, Stuart Lavery, Srdjan Saso, and Joseph Yazbek. 2022. "Fertility Sparing Surgery and Borderline Ovarian Tumours" Cancers 14, no. 6: 1485. https://doi.org/10.3390/cancers14061485