Een blik op de toekomst van eierstokkanker na herval
De bekendste en meteen ook meest voorkomende kanker bij vrouwen is borstkanker. De dodelijkste vorm van gynaecologische kankers is echter diens minder bekende broertje ovariumkanker. Vijf jaar na een nieuwe diagnose van borstkanker is nog ongeveer 90 procent van de patiënten in leven, waar dat voor ovariumkanker gemiddeld de helft is. Bovendien zal ongeveer tachtig procent van deze patiënten hervallen na een eerste diagnose. Eens hervallen is genezing zo goed als zeker niet meer mogelijk.
Bij nieuw gediagnosticeerde ovariumkanker is chirurgie de basispijler van behandeling, terwijl de rol van chirurgie in de setting van herval al langer een bron van discussie is. Met de recente publicatie van twee grote studies (GOG213 en DESKTOP III), die een eventueel langere overleving na herbehandeling met chirurgie onderzochten, breekt een moment van kritische toetsing en evaluatie aan.
Kanker alomtegenwoordig
Een kennis of naaste gediagnosticeerd met kanker, is eerder de regel dan de uitzondering. In 2018 werden maar liefst 70.468 nieuwe diagnosen van kanker geregistreerd. Concreet betekent dit dat ongeveer één op drie mannen en één op vier vrouwen deze diagnose krijgt voor hun 75ste verjaardag. Kanker is alomtegenwoordig in onze maatschappij en dat zorgt er ook voor dat veel tijd en geld voor wetenschappelijk onderzoek wordt vrijgemaakt voor deze veelzijdige ziekte.
Niet alleen wordt gezocht naar innovatieve therapieën, ook huidige therapieën worden kritisch geëvalueerd. Gezien de hoge hervalpercentages binnen eierstokkanker, vaak in combinatie met de ongeneeslijkheid van de ziekte, is naast een zo lang mogelijke overleving kunnen bieden, het behoud en verbeteren van de levenskwaliteit de hoofdprioriteit.
Nieuwe studieresultaten
De behandeling van eierstokkanker bij herval bestaat steeds uit chemotherapie, vaak in combinatie met chirurgie. De gebruikte chirurgische techniek bij eierstokkanker noemt men debulking. Deze uitgebreide chirurgie met uitruiming van alle aanwezige tumornesten in de hele buikholte vergt een zeer langdurige en nauwgezette operatie, waarbij ook vaak de verwijdering van verschillende organen nodig is. Patiënten die dit ondergaan, staan voor een lange revalidatie met verschillende (vaak definitieve) ongemakken zoals diarree en mindere opname van voedingsstoffen met nood aan voeding via infusen. Deze chirurgie is dus enkel te verantwoorden indien die ook de levensverwachting verlengt en/of de last van symptomen vermindert.
Hoewel alle ogen gericht waren op de recent gepubliceerde studies, werd geen eenduidig antwoord gevonden op de vraag of patiënten met hervallen ziekte debulking chirurgie moeten krijgen en zo ja, voor welke patiënten dit de beste therapie is. Beide studies trokken een verschillende conclusie over een mogelijk overlevingsvoordeel wanneer patiënten vergeleken werden die wel of net geen chirurgie ondergingen. Uit beide studies bleek een overlevingsvoordeel voor patiënten bij wie alle zichtbare (en zelfs microscopische) tumoren werden verwijderd, vergeleken met vrouwen die chirurgie ondergingen maar bij wie nog tumorresten achterbleven.
De juiste setting
Deze resultaten laten ons dus wat op onze honger zitten, maar één conclusie blijkt alvast getrokken: het verwijderen van alle tumornesten is van cruciaal belang wanneer besloten wordt tot chirurgie over te gaan. Concreet betekent dit dat vóór het uitvoeren van de ingreep moet worden bepaald of een patiënte een geschikte kandidate is. Er moet vooraf bepaald worden of de voor- en nadelen van de ingreep tegen elkaar opwegen en een inschatting van de haalbaarheid van totale verwijdering van tumoren moet gebeuren. Daarnaast is een getrainde chirurg met kennis van zaken en voldoende ervaring essentieel.
Een algemene trend binnen onze moderne gezondheidszorg is de centralisatie van bepaalde zorg en ingrepen, met het oog op het voorzien van kwalitatievere patiëntenzorg en ziektebehandeling. De grote voordelen van centralisatie zijn onder andere specifieke expertise, de mogelijkheid tot wetenschappelijk onderzoek, specifieke evaluaties, trainingen (zowel voor artsen als paramedisch en verzorgend personeel) en de uitrusting van het centrum waarin de ingrepen gebeuren. Hoewel de voltooide studies geen pasklaar antwoord gaven op de selectie van patiënten, bleek eens te meer de nood aan secure en gespecialiseerde aanpak.
Wat brengt de toekomst?
Het gebrek aan een duidelijk antwoord zorgt echter ook voor heel wat nieuwe vragen. Met nieuw onderzoek komen ook nieuwe methoden om kanker vroeg op te sporen (denk maar aan screening door mammografie en echo bij borstkanker of uitstrijkjes voor baarmoederhalskanker) en nieuwe therapiemogelijkheden in beeld. Enkele van deze nieuwe moleculen zijn PARP inhibitoren en bevacizumab, die respectievelijk een doelgerichte kankertherapie op DNA niveau en op niveau van bloedvoorziening voor een kankercel zijn. Met deze nieuwe medicatie hopen wetenschappers een nieuwe behandeling van eierstokkanker te vinden, die minder bijwerkingen heeft en dus minder belastend is op de levenskwaliteit van de patiënt.
Nieuwe medicatie die minder zware bijwerkingen heeft dan chemotherapie en uitgebreide chirurgie, die patiëntes een comfortabelere behandelingsperiode geeft, die van eierstokkanker een chronische maar controleerbare ziekte maakt, klinkt wetenschappers (en patiënten) als muziek in de oren. Het blijft belangrijk om vrouwen die hervallen met eierstokkanker te behandelen met aandacht voor ziektecontrole enerzijds en levenskwaliteit anderzijds. Of chirurgie een rol speelt in de behandeling moet steeds heel persoonlijk per patiënte bekeken worden.
Bibliografie
1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74.
2. Coleman RL, Spirtos NM, Enserro D, Herzog TJ, Sabbatini P, Armstrong DK, et al. Secondary Surgical Cytoreduction for Recurrent Ovarian Cancer. N Engl J Med. 2019;381(20):1929-39.
3. Bois AD, editor Randomized controlled phase III study evaluating the impact of secondary cytoreductive surgery in recurrent ovarian cancer: the final analysis of AGO DESKTOP III/ENGOT ov20. ASCO; 2020.
4. Zang R, editor A Randomized Phase 3 Trial of Secondary Cytoreductin in Late Recurrent Ovarian Cancer: A Shanghai Gynecologic Oncologic Group Study. ASCO; 2020.
5. WHO. Cancer 2020 [Available from: https://www.who.int/health-topics/cancer.
6. Cancer IAfRo. All Cancers Fact Sheet 2019 [Available from: http://gco.iarc.fr/today/data/factsheets/cancers/39-All-cancers-fact-sheet.pdf.
7. Registry BC. Cijfers over kanker [Available from: http://kankerregister.org/Cijfers_over_kanker.
8. Kanker St. Kanker in cijfers [Available from: https://www.kanker.be/alles-over-kanker/kanker-cijfers.
9. Registry BC. Belgium: Females, number of invasive tumours by primary site and age group in 2016 2018 [Available from: Belgium: Females, number of invasive tumours by primary site and age group in 2016.
10. Raimundo L, Ramos H, Loureiro JB, Calheiros J, Saraiva L. BRCA1/P53: Two strengths in cancer chemoprevention. Biochim Biophys Acta Rev Cancer. 2020;1873(1):188339.
11. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21(3):309-22.
12. Tabassum DP, Polyak K. Tumorigenesis: it takes a village. Nat Rev Cancer. 2015;15(8):473-83.
13. Lisio MA, Fu L, Goyeneche A, Gao ZH, Telleria C. High-Grade Serous Ovarian Cancer: Basic Sciences, Clinical and Therapeutic Standpoints. Int J Mol Sci. 2019;20(4).
14. Hoffman BL, Schorge JO, Bradshaw KD, Halvorson LM, Schaffer JI, Corton MM. Williams Gynecology, Third Edition: McGraw-Hill Education; 2016.
15. Lheureux S, Gourley C, Vergote I, Oza AM. Epithelial ovarian cancer. Lancet. 2019;393(10177):1240-53.
16. Lheureux S, Braunstein M, Oza AM. Epithelial ovarian cancer: Evolution of management in the era of precision medicine. CA Cancer J Clin. 2019;69(4):280-304.
17. Belgian Cancer Registry. Cancer Fact Sheet Ovarian Cancer 2016 [Available from: http://kankerregister.org/media/docs/CancerFactSheets/2016/Cancer_Fact_Sheet_OvarianCancer_2016.pdf.
18. Belgian Cancer Registry. Cancer burden. 2016.
19. Schorge JO, McCann C, Del Carmen MG. Surgical debulking of ovarian cancer: what difference does it make? Rev Obstet Gynecol. 2010;3(3):111-7.
20. Berek JS, Kehoe ST, Kumar L, Friedlander M. Cancer of the ovary, fallopian tube, and peritoneum. Int J Gynaecol Obstet. 2018;143 Suppl 2:59-78.
21. Colombo N, Van Gorp T, Parma G, Amant F, Gatta G, Sessa C, et al. Ovarian cancer. Crit Rev Oncol Hematol. 2006;60(2):159-79.
22. Makar AP, Trope CG, Tummers P, Denys H, Vandecasteele K. Advanced Ovarian Cancer: Primary or Interval Debulking? Five Categories of Patients in View of the Results of Randomized Trials and Tumor Biology: Primary Debulking Surgery and Interval Debulking Surgery for Advanced Ovarian Cancer. Oncologist. 2016;21(6):745-54.
23. Kaldawy A, Segev Y, Lavie O, Auslender R, Sopik V, Narod SA. Low-grade serous ovarian cancer: A review. Gynecol Oncol. 2016;143(2):433-8.
24. Oda K, Hamanishi J, Matsuo K, Hasegawa K. Genomics to immunotherapy of ovarian clear cell carcinoma: Unique opportunities for management. Gynecol Oncol. 2018;151(2):381-9.
25. Olawaiye AB, Boruta DM. Management of women with clear cell endometrial cancer: A Society of Gynecologic Oncology (SGO) review. Gynecol Oncol. 2009;113(2):277-83.
26. Mabuchi S, Sugiyama T, Kimura T. Clear cell carcinoma of the ovary: molecular insights and future therapeutic perspectives. J Gynecol Oncol. 2016;27(3):e31.
27. Cannistra SA. Cancer of the ovary. N Engl J Med. 2004;351(24):2519-29.
28. Griffiths CT, Parker LM, Fuller AF, Jr. Role of cytoreductive surgical treatment in the management of advanced ovarian cancer. Cancer Treat Rep. 1979;63(2):235-40.
29. Griffiths CT. Surgical resection of tumor bulk in the primary treatment of ovarian carcinoma. Natl Cancer Inst Monogr. 1975;42:101-4.
30. Winter WE, 3rd, Maxwell GL, Tian C, Carlson JW, Ozols RF, Rose PG, et al. Prognostic factors for stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol. 2007;25(24):3621-7.
31. Horowitz NS, Miller A, Rungruang B, Richard SD, Rodriguez N, Bookman MA, et al. Does aggressive surgery improve outcomes? Interaction between preoperative disease burden and complex surgery in patients with advanced-stage ovarian cancer: an analysis of GOG 182. J Clin Oncol. 2015;33(8):937-43.
32. du Bois A, Reuss A, Pujade-Lauraine E, Harter P, Ray-Coquard I, Pfisterer J. Role of surgical outcome as prognostic factor in advanced epithelial ovarian cancer: a combined exploratory analysis of 3 prospectively randomized phase 3 multicenter trials: by the Arbeitsgemeinschaft Gynaekologische Onkologie Studiengruppe Ovarialkarzinom (AGO-OVAR) and the Groupe d'Investigateurs Nationaux Pour les Etudes des Cancers de l'Ovaire (GINECO). Cancer. 2009;115(6):1234-44.
33. Vergote I, Coens C, Nankivell M, Kristensen GB, Parmar MKB, Ehlen T, et al. Neoadjuvant chemotherapy versus debulking surgery in advanced tubo-ovarian cancers: pooled analysis of individual patient data from the EORTC 55971 and CHORUS trials. Lancet Oncol. 2018;19(12):1680-7.
34. Vergote I, Tropé CG, Amant F, Kristensen GB, Ehlen T, Johnson N, et al. Neoadjuvant Chemotherapy or Primary Surgery in Stage IIIC or IV Ovarian Cancer. New England Journal of Medicine. 2010;363(10):943-53.
35. Kehoe S, Hook J, Nankivell M, Jayson GC, Kitchener H, Lopes T, et al. Primary chemotherapy versus primary surgery for newly diagnosed advanced ovarian cancer (CHORUS): an open-label, randomised, controlled, non-inferiority trial. Lancet. 2015;386(9990):249-57.
36. Onda T, Satoh T, Saito T, Kasamatsu T, Nakanishi T, Nakamura K, et al. Comparison of treatment invasiveness between upfront debulking surgery versus interval debulking surgery following neoadjuvant chemotherapy for stage III/IV ovarian, tubal, and peritoneal cancers in a phase III randomised trial: Japan Clinical Oncology Group Study JCOG0602. Eur J Cancer. 2016;64:22-31.
37. Vergote IB, Van Nieuwenhuysen E, Vanderstichele A. How to Select Neoadjuvant Chemotherapy or Primary Debulking Surgery in Patients With Stage IIIC or IV Ovarian Carcinoma. J Clin Oncol. 2016;34(32):3827-8.
38. Vergote I, de Wever I, Tjalma W, Van Gramberen M, Decloedt J, Van Dam P. Interval debulking surgery: an alternative for primary surgical debulking? Semin Surg Oncol. 2000;19(1):49-53.
39. Gill SE, McGree ME, Weaver AL, Cliby WA, Langstraat CL. Optimizing the treatment of ovarian cancer: Neoadjuvant chemotherapy and interval debulking versus primary debulking surgery for epithelial ovarian cancers likely to have suboptimal resection. Gynecol Oncol. 2017;144(2):266-73.
40. Biacchi D, Accarpio F, Ansaloni L, Macrì A, Ciardi A, Federici O, et al. Upfront debulking surgery versus interval debulking surgery for advanced tubo-ovarian high-grade serous carcinoma and diffuse peritoneal metastases treated with peritonectomy procedures plus HIPEC. Journal of Surgical Oncology. 2019;120(7):1208-19.
41. Oza AM, Cook AD, Pfisterer J, Embleton A, Ledermann JA, Pujade-Lauraine E, et al. Standard chemotherapy with or without bevacizumab for women with newly diagnosed ovarian cancer (ICON7): overall survival results of a phase 3 randomised trial. Lancet Oncol. 2015;16(8):928-36.
42. Spiliotis J, Halkia E, Lianos E, Kalantzi N, Grivas A, Efstathiou E, et al. Cytoreductive surgery and HIPEC in recurrent epithelial ovarian cancer: a prospective randomized phase III study. Ann Surg Oncol. 2015;22(5):1570-5.
43. Fujiwara K, Markman M, Morgan M, Coleman RL. Intraperitoneal carboplatin-based chemotherapy for epithelial ovarian cancer. Gynecol Oncol. 2005;97(1):10-5.
44. OncoLink Team. Intraperitoneal Chemotherapy (IP Chemo) 2019 [Available from: https://www.oncolink.org/cancer-treatment/cancer-medications/overview/intraperitoneal-chemotherapy-ip-chemo.
45. van Driel WJ, Koole SN, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RHM, et al. Hyperthermic Intraperitoneal Chemotherapy in Ovarian Cancer. New England Journal of Medicine. 2018;378(3):230-40.
46. Alberts DS, Liu PY, Hannigan EV, O'Toole R, Williams SD, Young JA, et al. Intraperitoneal cisplatin plus intravenous cyclophosphamide versus intravenous cisplatin plus intravenous cyclophosphamide for stage III ovarian cancer. N Engl J Med. 1996;335(26):1950-5.
47. Markman M, Bundy BN, Alberts DS, Fowler JM, Clark-Pearson DL, Carson LF, et al. Phase III trial of standard-dose intravenous cisplatin plus paclitaxel versus moderately high-dose carboplatin followed by intravenous paclitaxel and intraperitoneal cisplatin in small-volume stage III ovarian carcinoma: an intergroup study of the Gynecologic Oncology Group, Southwestern Oncology Group, and Eastern Cooperative Oncology Group. J Clin Oncol. 2001;19(4):1001-7.
48. Armstrong DK, Bundy B, Wenzel L, Huang HQ, Baergen R, Lele S, et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med. 2006;354(1):34-43.
49. Walker JL, Brady MF, Wenzel L, Fleming GF, Huang HQ, DiSilvestro PA, et al. Randomized Trial of Intravenous Versus Intraperitoneal Chemotherapy Plus Bevacizumab in Advanced Ovarian Carcinoma: An NRG Oncology/Gynecologic Oncology Group Study. J Clin Oncol. 2019;37(16):1380-90.
50. Colombo N, Sessa C, du Bois A, Ledermann J, McCluggage WG, McNeish I, et al. ESMO–ESGO consensus conference recommendations on ovarian cancer: pathology and molecular biology, early and advanced stages, borderline tumours and recurrent disease††These consensus statements were developed by the European Society for Medical Oncology (ESMO) and the European Society of Gynaecological Oncology (ESGO) and are published jointly in the Annals of Oncology and the International Journal of Gynecological Cancer. The two societies nominated participants who attended the consensus conference and co-authored the final manuscript. Annals of Oncology. 2019;30(5):672-705.
51. Ledermann JA, Raja FA, Fotopoulou C, Gonzalez-Martin A, Colombo N, Sessa C. Newly diagnosed and relapsed epithelial ovarian carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up†. Annals of Oncology. 2013;24:vi24-vi32.
52. Rustin GJ, van der Burg ME, Griffin CL, Guthrie D, Lamont A, Jayson GC, et al. Early versus delayed treatment of relapsed ovarian cancer (MRC OV05/EORTC 55955): a randomised trial. Lancet. 2010;376(9747):1155-63.
53. Coleman RL, Brady MF, Herzog TJ, Sabbatini P, Armstrong DK, Walker JL, et al. Bevacizumab and paclitaxel-carboplatin chemotherapy and secondary cytoreduction in recurrent, platinum-sensitive ovarian cancer (NRG Oncology/Gynecologic Oncology Group study GOG-0213): a multicentre, open-label, randomised, phase 3 trial. Lancet Oncol. 2017;18(6):779-91.
54. Harter P, Sehouli J, Reuss A, Hasenburg A, Scambia G, Cibula D, et al. Prospective validation study of a predictive score for operability of recurrent ovarian cancer: the Multicenter Intergroup Study DESKTOP II. A project of the AGO Kommission OVAR, AGO Study Group, NOGGO, AGO-Austria, and MITO. Int J Gynecol Cancer. 2011;21(2):289-95.
55. Harter P, du Bois A, Hahmann M, Hasenburg A, Burges A, Loibl S, et al. Surgery in recurrent ovarian cancer: the Arbeitsgemeinschaft Gynaekologische Onkologie (AGO) DESKTOP OVAR trial. Ann Surg Oncol. 2006;13(12):1702-10.
56. Markman M, Rothman R, Hakes T, Reichman B, Hoskins W, Rubin S, et al. Second-line platinum therapy in patients with ovarian cancer previously treated with cisplatin. J Clin Oncol. 1991;9(3):389-93.
57. Harter P, Reuss A, Sehouli J, Chiva L, du Bois A. Brief Report About the Role of Hyperthermic Intraperitoneal Chemotherapy in a Prospective Randomized Phase 3 Study in Recurrent Ovarian Cancer From Spiliotis et al. Int J Gynecol Cancer. 2017;27(2):246-7.
58. Tewari KS, Burger RA, Enserro D, Norquist BM, Swisher EM, Brady MF, et al. Final Overall Survival of a Randomized Trial of Bevacizumab for Primary Treatment of Ovarian Cancer. J Clin Oncol. 2019;37(26):2317-28.
59. Burger RA, Brady MF, Bookman MA, Walker JL, Homesley HD, Fowler J, et al. Phase III trial of bevacizumab (BEV) in the primary treatment of advanced epithelial ovarian cancer (EOC), primary peritoneal cancer (PPC), or fallopian tube cancer (FTC): A Gynecologic Oncology Group study. Journal of Clinical Oncology. 2010;28(18_suppl):LBA1-LBA.
60. Perren TJ, Swart AM, Pfisterer J, Ledermann JA, Pujade-Lauraine E, Kristensen G, et al. A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med. 2011;365(26):2484-96.
61. Aghajanian C, Goff B, Nycum LR, Wang YV, Husain A, Blank SV. Final overall survival and safety analysis of OCEANS, a phase 3 trial of chemotherapy with or without bevacizumab in patients with platinum-sensitive recurrent ovarian cancer. Gynecol Oncol. 2015;139(1):10-6.
62. Pujade-Lauraine E, Hilpert F, Weber B, Reuss A, Poveda A, Kristensen G, et al. Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: The AURELIA open-label randomized phase III trial. J Clin Oncol. 2014;32(13):1302-8.
63. Norquist BM, Brady MF, Harrell MI, Walsh T, Lee MK, Gulsuner S, et al. Mutations in Homologous Recombination Genes and Outcomes in Ovarian Carcinoma Patients in GOG 218: An NRG Oncology/Gynecologic Oncology Group Study. Clin Cancer Res. 2018;24(4):777-83.
64. da Cunha Colombo Bonadio RR, Fogace RN, Miranda VC, Diz M. Homologous recombination deficiency in ovarian cancer: a review of its epidemiology and management. Clinics (Sao Paulo). 2018;73(suppl 1):e450s.
65. Krishnan V, Berek JS, Dorigo O. Immunotherapy in ovarian cancer. Current Problems in Cancer. 2017;41(1):48-63.
66. Buechel M, Herzog TJ, Westin SN, Coleman RL, Monk BJ, Moore KN. Treatment of patients with recurrent epithelial ovarian cancer for whom platinum is still an option. Ann Oncol. 2019;30(5):721-32.
67. Berek JS, Hacker NF, Lagasse LD, Nieberg RK, Elashoff RM. Survival of patients following secondary cytoreductive surgery in ovarian cancer. Obstet Gynecol. 1983;61(2):189-93.
68. Benedetti Panici P, De Vivo A, Bellati F, Manci N, Perniola G, Basile S, et al. Secondary cytoreductive surgery in patients with platinum-sensitive recurrent ovarian cancer. Ann Surg Oncol. 2007;14(3):1136-42.
69. Gronlund B, Lundvall L, Christensen IJ, Knudsen JB, Hogdall C. Surgical cytoreduction in recurrent ovarian carcinoma in patients with complete response to paclitaxel-platinum. Eur J Surg Oncol. 2005;31(1):67-73.
70. Leitao MM, Jr., Kardos S, Barakat RR, Chi DS. Tertiary cytoreduction in patients with recurrent ovarian carcinoma. Gynecol Oncol. 2004;95(1):181-8.
71. Scarabelli C, Gallo A, Carbone A. Secondary cytoreductive surgery for patients with recurrent epithelial ovarian carcinoma. Gynecol Oncol. 2001;83(3):504-12.
72. Tay EH, Grant PT, Gebski V, Hacker NF. Secondary cytoreductive surgery for recurrent epithelial ovarian cancer. Obstet Gynecol. 2002;99(6):1008-13.
73. Eisenkop SM, Friedman RL, Wang HJ. Secondary cytoreductive surgery for recurrent ovarian cancer. A prospective study. Cancer. 1995;76(9):1606-14.
74. Eisenkop SM, Friedman RL, Spirtos NM. The role of secondary cytoreductive surgery in the treatment of patients with recurrent epithelial ovarian carcinoma. Cancer. 2000;88(1):144-53.
75. Sehouli J, Richter R, Braicu EI, Buhling KJ, Bahra M, Neuhaus P, et al. Role of secondary cytoreductive surgery in ovarian cancer relapse: who will benefit? A systematic analysis of 240 consecutive patients. J Surg Oncol. 2010;102(6):656-62.
76. Zang RY, Li ZT, Tang J, Cheng X, Cai SM, Zhang ZY, et al. Secondary cytoreductive surgery for patients with relapsed epithelial ovarian carcinoma: who benefits? Cancer. 2004;100(6):1152-61.
77. Bristow RE, Puri I, Chi DS. Cytoreductive surgery for recurrent ovarian cancer: a meta-analysis. Gynecol Oncol. 2009;112(1):265-74.
78. Morris M, Gershenson DM, Wharton JT, Copeland LJ, Edwards CL, Stringer CA. Secondary cytoreductive surgery for recurrent epithelial ovarian cancer. Gynecol Oncol. 1989;34(3):334-8.
79. Munkarah A, Levenback C, Wolf JK, Bodurka-Bevers D, Tortolero-Luna G, Morris RT, et al. Secondary cytoreductive surgery for localized intra-abdominal recurrences in epithelial ovarian cancer. Gynecol Oncol. 2001;81(2):237-41.
80. LOROCSON study: Late Onset Recurrent Ovarian Cancer: Surgery Or Not - ISRCTN
[LOROCSON study: Late Onset Recurrent Ovarian Cancer: Surgery Or Not
]. Available from: http://www.isrctn.com/ISRCTN50678517.
81. van de Laar R, Zusterzeel PL, Van Gorp T, Buist MR, van Driel WJ, Gaarenstroom KN, et al. Cytoreductive surgery followed by chemotherapy versus chemotherapy alone for recurrent platinum-sensitive epithelial ovarian cancer (SOCceR trial): a multicenter randomised controlled study. BMC Cancer. 2014;14:22.
82. van de Laar R, Kruitwagen RFPM, Zusterzeel PLM, Van Gorp T, Massuger LFAG. Correspondence: Premature Stop of the SOCceR Trial, a Multicenter Randomized Controlled Trial on Secondary Cytoreductive Surgery. International Journal of Gynecologic Cancer. 2017;27(1):2-.
83. DESKTOP III - study design [Available from: https://clinicaltrials.gov/ct2/show/record/NCT01166737.
84. DESKTOP III - graphs [Available from: clinicaloptions.com
85. Baek MH, Lee SW, Park JY, Rhim CC, Kim DY, Suh DS, et al. Preoperative Predictive Factors for Complete Cytoreduction and Survival Outcome in Epithelial Ovarian, Tubal, and Peritoneal Cancer After Neoadjuvant Chemotherapy. Int J Gynecol Cancer. 2017;27(3):420-9.
86. Angioli R, Capriglione S, Aloisi A, Ricciardi R, Scaletta G, Lopez S, et al. A Predictive Score for Secondary Cytoreductive Surgery in Recurrent Ovarian Cancer (SeC-Score): A Single-Centre, Controlled Study for Preoperative Patient Selection. Ann Surg Oncol. 2015;22(13):4217-23.
87. Frederick PJ, Ramirez PT, McQuinn L, Milam MR, Weber DM, Coleman RL, et al. Preoperative factors predicting survival after secondary cytoreduction for recurrent ovarian cancer. Int J Gynecol Cancer. 2011;21(5):831-6.
88. Ducoulombier S, Golfier F, Colomban O, Benayoun D, Bolze PA, Tod M, et al. Modeling CA-125 During Neoadjuvant Chemotherapy for Predicting Optimal Cytoreduction and Relapse Risk in Ovarian Cancer. Anticancer Res. 2017;37(12):6879-86.
89. Bae J, Lim MC, Choi JH, Song YJ, Lee KS, Kang S, et al. Prognostic factors of secondary cytoreductive surgery for patients with recurrent epithelial ovarian cancer. J Gynecol Oncol. 2009;20(2):101-6.
90. Fan XM, Zhang J, Niu SH, Li KX, Song CZ. Secondary cytoreductive surgery in recurrent epithelial ovarian cancer: A prognostic analysis with 103 cases. Int J Surg. 2017;38:61-6.
91. Mahner S, Woelber L, Jung S, Eulenburg CZ, Ihnen M, Schwarz J, et al. Prognostic significance of CA-125 in the management of patients with recurrent epithelial ovarian carcinoma selected for secondary cytoreduction. Anticancer Res. 2009;29(7):2817-21.
92. Onda T, Yoshikawa H, Yasugi T, Yamada M, Matsumoto K, Taketani Y. Secondary cytoreductive surgery for recurrent epithelial ovarian carcinoma: proposal for patients selection. Br J Cancer. 2005;92(6):1026-32.
93. Minaguchi T, Satoh T, Matsumoto K, Sakurai M, Ochi H, Onuki M, et al. Proposal for selection criteria of secondary cytoreductive surgery in recurrent epithelial ovarian, tubal, and peritoneal cancers. Int J Clin Oncol. 2016;21(3):573-9.
94. Gil-Ibanez B, Oskay-Ozcelik G, Richter R, Fotopoulou C, Braicu EI, Neuhaus P, et al. Predictive factors in relapsed ovarian cancer for complete tumor resection. Anticancer Res. 2011;31(8):2583-7.
95. Fanfani F, Monterossi G, Fagotti A, Gallotta V, Costantini B, Vizzielli G, et al. Positron emission tomography-laparoscopy based method in the prediction of complete cytoreduction in platinum-sensitive recurrent ovarian cancer. Ann Surg Oncol. 2015;22(2):649-54.
96. Funt SA, Hricak H, Abu-Rustum N, Mazumdar M, Felderman H, Chi DS. Role of CT in the management of recurrent ovarian cancer. AJR Am J Roentgenol. 2004;182(2):393-8.
97. Lenhard SM, Burges A, Johnson TR, Kirschenhofer A, Bruns C, Linke R, et al. Predictive value of PET-CT imaging versus AGO-scoring in patients planned for cytoreductive surgery in recurrent ovarian cancer. Eur J Obstet Gynecol Reprod Biol. 2008;140(2):263-8.
98. Chi DS, McCaughty K, Diaz JP, Huh J, Schwabenbauer S, Hummer AJ, et al. Guidelines and selection criteria for secondary cytoreductive surgery in patients with recurrent, platinum-sensitive epithelial ovarian carcinoma. Cancer. 2006;106(9):1933-9.
99. Tian WJ, Chi DS, Sehouli J, Trope CG, Jiang R, Ayhan A, et al. A risk model for secondary cytoreductive surgery in recurrent ovarian cancer: an evidence-based proposal for patient selection. Ann Surg Oncol. 2012;19(2):597-604.
100. van de Laar R, Massuger LF, Van Gorp T, IntHout J, Zusterzeel PL, Kruitwagen RF. External validation of two prediction models of complete secondary cytoreductive surgery in patients with recurrent epithelial ovarian cancer. Gynecol Oncol. 2015;137(2):210-5.
101. Cowan RA, Eriksson AGZ, Jaber SM, Zhou Q, Iasonos A, Zivanovic O, et al. A comparative analysis of prediction models for complete gross resection in secondary cytoreductive surgery for ovarian cancer. Gynecol Oncol. 2017;145(2):230-5.
102. Du Bois A, editor How to Identify the “Right” Patient for Surgery in Recurrent Ovarian Cancer. 11th International Symposium Advanced Ovarian Cancer; 2017.
103. Fuh KC, Shin JY, Kapp DS, Brooks RA, Ueda S, Urban RR, et al. Survival differences of Asian and Caucasian epithelial ovarian cancer patients in the United States. Gynecol Oncol. 2015;136(3):491-7.
104. Bogani G, Tagliabue E, Signorelli M, Ditto A, Martinelli F, Chiappa V, et al. A score system for complete cytoreduction in selected recurrent ovarian cancer patients undergoing secondary cytoreductive surgery: predictors- and nomogram-based analyses. J Gynecol Oncol. 2018;29(3):e40.
105. Laas E, Luyckx M, De Cuypere M, Selle F, Darai E, Querleu D, et al. Secondary complete cytoreduction in recurrent ovarian cancer: benefit of optimal patient selection using scoring system. Int J Gynecol Cancer. 2014;24(2):238-46.
106. Laga T, Lambrechts S, Laenen A, Van Nieuwenhuysen E, Han SN, Vergote I. Positive DESKTOP and Tian Scores Systems Are Adequate to Predict Optimal (R0) Secondary Debulking Surgery in Ovarian Cancer, But a Negative Score Does Not Preclude Secondary Surgery. Int J Gynecol Cancer. 2018;28(4):721-8.
107. Fagotti A, Costantini B, Petrillo M, Vizzielli G, Fanfani F, Margariti PA, et al. Cytoreductive surgery plus HIPEC in platinum-sensitive recurrent ovarian cancer patients: a case-control study on survival in patients with two year follow-up. Gynecol Oncol. 2012;127(3):502-5.
108. Fagotti A, Costantini B, Vizzielli G, Perelli F, Ercoli A, Gallotta V, et al. HIPEC in recurrent ovarian cancer patients: morbidity-related treatment and long-term analysis of clinical outcome. Gynecol Oncol. 2011;122(2):221-5.
109. Munoz-Casares FC, Rufian S, Rubio MJ, Diaz CJ, Diaz R, Casado A, et al. The role of hyperthermic intraoperative intraperitoneal chemotherapy (HIPEC) in the treatment of peritoneal carcinomatosis in recurrent ovarian cancer. Clin Transl Oncol. 2009;11(11):753-9.
110. Le Brun JF, Campion L, Berton-Rigaud D, Lorimier G, Marchal F, Ferron G, et al. Survival benefit of hyperthermic intraperitoneal chemotherapy for recurrent ovarian cancer: a multi-institutional case control study. Ann Surg Oncol. 2014;21(11):3621-7.
111. Safra T, Grisaru D, Inbar M, Abu-Abeid S, Dayan D, Matceyevsky D, et al. Cytoreduction surgery with hyperthermic intraperitoneal chemotherapy in recurrent ovarian cancer improves progression-free survival, especially in BRCA-positive patients- a case-control study. J Surg Oncol. 2014;110(6):661-5.
112. Spiliotis J, Prodromidou A, Kopanakis N, Ferfelios M, Raptis A, Terra A, et al. The role of repeated cytoreductive surgery plus HIPEC in peritoneal carcinomatosis recurrence: A retrospective analysis. Pleura Peritoneum. 2018;3:sA324-sA5.
113. Batista TP. Comment on: Surgery and HIPEC in Recurrent Epithelial Ovarian Cancer: A Prospective Randomized Phase III Study. Ann Surg Oncol. 2017;24(Suppl 3):630.
114. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 2014;15(8):852-61.
115. Pujade-Lauraine E, Ledermann JA, Selle F, Gebski V, Penson RT, Oza AM, et al. Olaparib tablets as maintenance therapy in patients with platinum-sensitive, relapsed ovarian cancer and a BRCA1/2 mutation (SOLO2/ENGOT-Ov21): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol. 2017;18(9):1274-84.
116. Mirza MR, Monk BJ, Herrstedt J, Oza AM, Mahner S, Redondo A, et al. Niraparib Maintenance Therapy in Platinum-Sensitive, Recurrent Ovarian Cancer. New England Journal of Medicine. 2016;375(22):2154-64.
117. Coleman RL, Oza AM, Lorusso D, Aghajanian C, Oaknin A, Dean A, et al. Rucaparib maintenance treatment for recurrent ovarian carcinoma after response to platinum therapy (ARIEL3): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2017;390(10106):1949-61.
118. Penson RT, Valencia RV, Cibula D, Colombo N, Leath CA, 3rd, Bidziński M, et al. Olaparib Versus Nonplatinum Chemotherapy in Patients With Platinum-Sensitive Relapsed Ovarian Cancer and a Germline BRCA1/2 Mutation (SOLO3): A Randomized Phase III Trial. J Clin Oncol. 2020;38(11):1164-74.
119. Gallagher JR, Heap KJ, Carroll S. Real world occurrence of top three clinical-trial reported adverse events of PARP inhibitor niraparib maintenance therapy in platinumsensitive, recurrent ovarian cancer, a national retrospective observational study of a 200 mg/day starting-dose cohort. Annals of Oncology. 2018;29:viii351-viii2.
120. Berek JS, Matulonis UA, Peen U, Ghatage P, Mahner S, Redondo A, et al. Safety and dose modification for patients receiving niraparib. Annals of Oncology. 2018;29(8):1784-92.
121. Stockler MR, Hilpert F, Friedlander M, King MT, Wenzel L, Lee CK, et al. Patient-reported outcome results from the open-label phase III AURELIA trial evaluating bevacizumab-containing therapy for platinum-resistant ovarian cancer. J Clin Oncol. 2014;32(13):1309-16.
122. Furnes B, Svensen R, Helland H, Ovrebo K. Challenges and outcome of surgery for bowel obstruction in women with gynaecologic cancer. International Journal of Surgery. 2016;27:158-64.
123. Fotopoulou C, Braicu EI, Kwee SL, Kuhberg M, Richter R, Pietzner K, et al. Salvage surgery due to bowel obstruction in advanced or relapsed ovarian cancer resulting in short bowel syndrome and long-life total parenteral nutrition: surgical and clinical outcome. Int J Gynecol Cancer. 2013;23(8):1495-500.
124. Fotopoulou C, Haidopoulos D. Extraperitoneal en bloc intestinal resection as palliative surgery for treatment refractory bowel obstruction in ovarian cancer relapse. Int J Gynecol Cancer. 2020.
125. Falcone F, Scambia G, Benedetti Panici P, Signorelli M, Cormio G, Giorda G, et al. Tertiary cytoreductive surgery in recurrent epithelial ovarian cancer: A multicentre MITO retrospective study. Gynecol Oncol. 2017;147(1):66-72.
126. Fotopoulou C, Richter R, Braicu IE, Schmidt SC, Neuhaus P, Lichtenegger W, et al. Clinical outcome of tertiary surgical cytoreduction in patients with recurrent epithelial ovarian cancer. Ann Surg Oncol. 2011;18(1):49-57.
127. Fanfani F, Fagotti A, Ercoli A, Gallotta V, Chiantera V, Restaino S, et al. Is There a Role for Tertiary (TCR) and Quaternary (QCR) Cytoreduction in Recurrent Ovarian Cancer? Anticancer Res. 2015;35(12):6951-5.
128. Fotopoulou C, Zang R, Gultekin M, Cibula D, Ayhan A, Liu D, et al. Value of tertiary cytoreductive surgery in epithelial ovarian cancer: an international multicenter evaluation. Ann Surg Oncol. 2013;20(4):1348-54.
129. Shih KK, Chi DS, Barakat RR, Leitao Jr MM. Beyond tertiary cytoreduction in patients with recurrent epithelial ovarian, fallopian tube, or primary peritoneal cancer. Gynecol Oncol. 2010;116(3):364-9.
130. Bacalbasa N, Balescu I, Dima S, Brasoveanu V, Popescu I. The Role of Quaternary Cytoreduction in Recurrent Epithelial Ovarian Cancer: A Single-center Experience. Anticancer Res. 2015;35(6):3519-23.
131. Fotopoulou C, Savvatis K, Kosian P, Braicu IE, Papanikolaou G, Pietzner K, et al. Quaternary cytoreductive surgery in ovarian cancer: does surgical effort still matter? Br J Cancer. 2013;108(1):32-8.
