Clinical parameters affecting survival outcomes in patients with low-grade serous ovarian carcinoma: an international multicentre analysis

Taymaa May; Marcus Bernardini; Stephanie Lheureux; Katja K H Aben; Elisa V Bandera; Matthias W Beckmann; Javier Benitez; Andrew Berchuck; Line Bjørge; Michael E Carney; Daniel W Cramer; Anna deFazio; Thilo Dörk; Diana M Eccles; Michael Friedlander; María Jose García; Ellen L Goode; Alexander Hein; Claus K Høgdall; Allan Jensen; Sharon Johnatty; Catherine J Kennedy; Lambertus A Kiemeney; Susanne K Kjær; Jolanta Kupryjańczyk; Keitaro Matsuo; Valerie McGuire; Francesmary Modugno; Lisa E Paddock; Tanja Pejovic; Catherine M Phelan; Marjorie J Riggan; Cristina Rodriguez-Antona; Joseph H Rothstein; Weiva Sieh; Honglin Song; Kathryn L Terry; Anne M van Altena; Adriaan Vanderstichele; Ignace Vergote; Liv Cecilie Vestrheim Thomsen; Penelope M Webb; Nicolas Wentzensen; Lynne R Wilkens; Argyrios Ziogas; Haiyan Jiang; Alicia Tone; Ovarian Cancer Association and the Australian Ovarian Cancer Study Group

doi:10.1503/cjs.017020

Clinical parameters affecting survival outcomes in patients with low-grade serous ovarian carcinoma: an international multicentre analysis

Can J Surg. 2023 Jun 27;66(3):E310-E320. doi: 10.1503/cjs.017020. Print 2023 May-Jun.

Authors

Taymaa May¹, Marcus Bernardini², Stephanie Lheureux², Katja K H Aben², Elisa V Bandera², Matthias W Beckmann², Javier Benitez², Andrew Berchuck², Line Bjørge², Michael E Carney², Daniel W Cramer², Anna deFazio², Thilo Dörk², Diana M Eccles², Michael Friedlander², María Jose García², Ellen L Goode², Alexander Hein², Claus K Høgdall², Allan Jensen², Sharon Johnatty², Catherine J Kennedy², Lambertus A Kiemeney², Susanne K Kjær², Jolanta Kupryjańczyk², Keitaro Matsuo², Valerie McGuire², Francesmary Modugno², Lisa E Paddock², Tanja Pejovic², Catherine M Phelan², Marjorie J Riggan², Cristina Rodriguez-Antona², Joseph H Rothstein², Weiva Sieh², Honglin Song², Kathryn L Terry², Anne M van Altena², Adriaan Vanderstichele², Ignace Vergote², Liv Cecilie Vestrheim Thomsen², Penelope M Webb², Nicolas Wentzensen², Lynne R Wilkens², Argyrios Ziogas², Haiyan Jiang², Alicia Tone²; Ovarian Cancer Association and the Australian Ovarian Cancer Study Group

Affiliations

¹ From the Division of Gynecologic Oncology, University Health Network, Princess Margaret Cancer Centre, Toronto, Ont. (May, Bernardini, Tone); the Department of Obstetrics and Gynecology, University of Toronto, Toronto, Ont. (May, Bernardini); the Division of Medical Oncology, Department of Medicine, Princess Margaret Cancer Centre, Toronto, Ont. (Lheureux); the Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Australia (Johnatty); the Population Health Department, QIMR Berghofer Medical Research Institute, Brisbane, Australia (Webb); the Department of Medical Oncology, Prince of Wales Hospital, Sydney, Australia (Friedlander); the Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen Nuremberg, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany (Beckmann, Hein); the Division of Hematology and Oncology, Department of Medicine, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, Calif. (Fasching); the Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology and Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium (Vanderstichele, Vergote); the Human Cancer Genetics Programme, Spanish National Cancer Research Centre (CNIO), Madrid, Spain (Benitez, García, Rodriguez-Antona); the Biomedical Network on Rare Diseases (CIBERER), Madrid, Spain (Benitez, García, Rodriguez-Antona); the Department of Obstetrics and Gynecology, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii (Carney); the Gynaecology Research Unit, Hannover Medical School, Hanover, Germany (Dörk); the Women's Cancer Research Center, Magee-Womens Research Institute and Hillman Cancer Center, Pittsburgh, Penn. (Modugno); the Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, Penn. (Modugno); the Division of Molecular Medicine, Aichi Cancer Center Research Institute, Nagoya, Japan (Matsuo); the Department of Epidemiology, Nagoya University Graduate School of Medicine, Nagoya, Japan (Matsuo); the Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark (Jensen, Kjær); the Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark (Kjær); the Department of Health Sciences Research, Mayo Clinic, Rochester, Minn. (Goode); the Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii (Wilkens); the Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Fla. (Phelan); the Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC (Berchuck, Riggan); the Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, Mass. (Cramer, Terry); the Harvard T.H. Chan School of Public Health, Boston, Mass. (Cramer, Terry); the Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ (Bandera); the New Jersey Department of Health and Senior Services, Mercerville, NJ (Paddock); the School of Public Health, University of Medicine and Dentistry of New Jersey, Piscataway, NJ (Paddock); the Department of Gynecology and Obstetrics, Haukeland University Horpital, Bergen, Norway (Bjørge, Vestrheim Thomsen); the Centre for Cancer Biomarkers CCBIO, Department of Clinical Science, University of Bergen, Bergen, Norway (Bjørge, Vestrheim Thomsen); the Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands (Aben, Kiemeney); the Netherlands Comprehensive Cancer Organisation, Utrecht, The Netherlands (Aben); the Department of Gynaecology, Radboud University Medical Center, Nijmegen, The Netherlands (van Altena); the Department of Obstetrics and Gynecology, Oregon Health & Science University, Portland, Ore. (Pejovic); the Knight Cancer Institute, Oregon Health & Science University, Portland, Ore. (Pejovic); the Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md. (Wentzensen); The Juliane Marie Centre, Department of Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark (C. Høgdall); the Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK (Song); the Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK (Eccles); the Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, Calif. (McGuire); the Department of Genetics and Genomic Sciences, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY (Rothstein, Sieh); the Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, Calif. (Ziogas); the Centre for Cancer Research, The Westmead Institute for Medical Research, The University of Sydney, Sydney, Australia (deFazio, Kennedy); the Department of Gynaecological Oncology, Westmead Hospital, Sydney, Australia (deFazio, Kennedy); the Department of Pathology and Laboratory Diagnostics, the Maria Sklodowska-Curie Institute - Oncology Center, Warsaw, Poland (Kupryjanczyk); and the Department of Biostatistics, Princess Margaret Cancer Centre, Toronto, Ont. (Jiang) Taymaa.May@uhn.ca.
² From the Division of Gynecologic Oncology, University Health Network, Princess Margaret Cancer Centre, Toronto, Ont. (May, Bernardini, Tone); the Department of Obstetrics and Gynecology, University of Toronto, Toronto, Ont. (May, Bernardini); the Division of Medical Oncology, Department of Medicine, Princess Margaret Cancer Centre, Toronto, Ont. (Lheureux); the Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Australia (Johnatty); the Population Health Department, QIMR Berghofer Medical Research Institute, Brisbane, Australia (Webb); the Department of Medical Oncology, Prince of Wales Hospital, Sydney, Australia (Friedlander); the Department of Gynecology and Obstetrics, Comprehensive Cancer Center Erlangen Nuremberg, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany (Beckmann, Hein); the Division of Hematology and Oncology, Department of Medicine, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, Calif. (Fasching); the Division of Gynecologic Oncology, Department of Obstetrics and Gynaecology and Leuven Cancer Institute, University Hospitals Leuven, Leuven, Belgium (Vanderstichele, Vergote); the Human Cancer Genetics Programme, Spanish National Cancer Research Centre (CNIO), Madrid, Spain (Benitez, García, Rodriguez-Antona); the Biomedical Network on Rare Diseases (CIBERER), Madrid, Spain (Benitez, García, Rodriguez-Antona); the Department of Obstetrics and Gynecology, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii (Carney); the Gynaecology Research Unit, Hannover Medical School, Hanover, Germany (Dörk); the Women's Cancer Research Center, Magee-Womens Research Institute and Hillman Cancer Center, Pittsburgh, Penn. (Modugno); the Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, Penn. (Modugno); the Division of Molecular Medicine, Aichi Cancer Center Research Institute, Nagoya, Japan (Matsuo); the Department of Epidemiology, Nagoya University Graduate School of Medicine, Nagoya, Japan (Matsuo); the Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark (Jensen, Kjær); the Department of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark (Kjær); the Department of Health Sciences Research, Mayo Clinic, Rochester, Minn. (Goode); the Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, Hawaii (Wilkens); the Department of Cancer Epidemiology, Moffitt Cancer Center, Tampa, Fla. (Phelan); the Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, NC (Berchuck, Riggan); the Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, Boston, Mass. (Cramer, Terry); the Harvard T.H. Chan School of Public Health, Boston, Mass. (Cramer, Terry); the Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ (Bandera); the New Jersey Department of Health and Senior Services, Mercerville, NJ (Paddock); the School of Public Health, University of Medicine and Dentistry of New Jersey, Piscataway, NJ (Paddock); the Department of Gynecology and Obstetrics, Haukeland University Horpital, Bergen, Norway (Bjørge, Vestrheim Thomsen); the Centre for Cancer Biomarkers CCBIO, Department of Clinical Science, University of Bergen, Bergen, Norway (Bjørge, Vestrheim Thomsen); the Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands (Aben, Kiemeney); the Netherlands Comprehensive Cancer Organisation, Utrecht, The Netherlands (Aben); the Department of Gynaecology, Radboud University Medical Center, Nijmegen, The Netherlands (van Altena); the Department of Obstetrics and Gynecology, Oregon Health & Science University, Portland, Ore. (Pejovic); the Knight Cancer Institute, Oregon Health & Science University, Portland, Ore. (Pejovic); the Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md. (Wentzensen); The Juliane Marie Centre, Department of Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark (C. Høgdall); the Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK (Song); the Cancer Sciences Academic Unit, Faculty of Medicine, University of Southampton, Southampton, UK (Eccles); the Department of Health Research and Policy - Epidemiology, Stanford University School of Medicine, Stanford, Calif. (McGuire); the Department of Genetics and Genomic Sciences, Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY (Rothstein, Sieh); the Department of Epidemiology, Genetic Epidemiology Research Institute, University of California Irvine, Irvine, Calif. (Ziogas); the Centre for Cancer Research, The Westmead Institute for Medical Research, The University of Sydney, Sydney, Australia (deFazio, Kennedy); the Department of Gynaecological Oncology, Westmead Hospital, Sydney, Australia (deFazio, Kennedy); the Department of Pathology and Laboratory Diagnostics, the Maria Sklodowska-Curie Institute - Oncology Center, Warsaw, Poland (Kupryjanczyk); and the Department of Biostatistics, Princess Margaret Cancer Centre, Toronto, Ont. (Jiang).

Abstract
in English, French

Background: Women with low-grade ovarian serous carcinoma (LGSC) benefit from surgical treatment; however, the role of chemotherapy is controversial. We examined an international database through the Ovarian Cancer Association Consortium to identify factors that affect survival in LGSC.

Methods: We performed a retrospective cohort analysis of patients with LGSC who had had primary surgery and had overall survival data available. We performed univariate and multivariate analyses of progression-free survival and overall survival, and generated Kaplan-Meier survival curves.

Results: Of the 707 patients with LGSC, 680 (96.2%) had available overall survival data. The patients' median age overall was 54 years. Of the 659 patients with International Federation of Obstetrics and Gynecology stage data, 156 (23.7%) had stage I disease, 64 (9.7%) had stage II, 395 (59.9%) had stage III, and 44 (6.7%) had stage IV. Of the 377 patients with surgical data, 200 (53.0%) had no visible residual disease. Of the 361 patients with chemotherapy data, 330 (91.4%) received first-line platinum-based chemotherapy. The median follow-up duration was 5.0 years. The median progression-free survival and overall survival were 43.2 months and 110.4 months, respectively. Multivariate analysis indicated a statistically significant impact of stage and residual disease on progression-free survival and overall survival. Platinum-based chemotherapy was not associated with a survival advantage.

Conclusion: This multicentre analysis indicates that complete surgical cytoreduction to no visible residual disease has the most impact on improved survival in LGSC. This finding could immediately inform and change practice.

Contexte:: L’efficacité du traitement chirurgical du carcinome séreux de bas grade (CSBG) de l’ovaire est reconnue, mais l’intérêt de la chimiothérapie est controversé. Nous avons cherché à déterminer les facteurs qui influencent la survie au CSBG dans une base de données internationale de l’Ovarian Cancer Association Consortium.

Méthodes:: Nous avons mené une analyse de cohorte rétrospective de patientes atteintes de CSBG ayant subi une chirurgie initiale. À partir de leurs données de survie globale, nous avons effectué des analyses univariées et multivariées de la survie sans progression et de la survie globale et avons généré des courbes de Kaplan–Meier relatives à la survie.

Résultats:: Les données de survie globale de 680 (96,2 %) patientes atteintes de CSBG sur 707 (âge médian 54 ans) étaient disponibles. Des 659 patientes pour qui on avait des données sur le stade selon la classification de la Fédération internationale de gynécologie et d’obstétrique, 156 (23,7 %) étaient atteintes d’un cancer de stade I, 64 (9,7 %) de stade II, 395 (59,9 %) de stade III et 44 (6,7 %) de stade IV. Les données chirurgicales de 377 patientes ont permis de déterminer que 200 (53 %) n’avaient aucune maladie résiduelle visible. Des 361 patientes avec des données de chimiothérapie, 330 (91,4 %) avaient reçu une chimiothérapie à base de platine en première intention. Le suivi médian a duré 5 ans, avec une survie sans progression et une survie globale médianes de 43,2 mois et de 110,4 mois, respectivement. Selon l’analyse multivariée, le stade et la maladie résiduelle ont un impact significatif sur la survie sans progression et la survie globale, alors que la chimiothérapie à base de platine n’a été associée à aucun avantage sur la survie.

Conclusion:: Cette analyse multicentrique indique que la cytoréduction chirurgicale complète, résultant en l’élimination de toute maladie résiduelle, est l’intervention qui améliore le plus la survie au CSBG. Ce résultat peut guider un changement de pratique immédiat.

Publication types

Multicenter Study

MeSH terms

Cystadenocarcinoma, Serous* / drug therapy
Cystadenocarcinoma, Serous* / surgery
Female
Humans
Kaplan-Meier Estimate
Middle Aged
Neoplasm Staging
Ovarian Neoplasms* / drug therapy
Ovarian Neoplasms* / surgery
Retrospective Studies

Abstract in English, French

Publication types

MeSH terms

Grants and funding

Abstract
in English, French