Skip to main content
Top

Detailed analysis of the histology-specific impact of ascites volume on the outcome of epithelial ovarian cancer: a multi-institutional retrospective cohort study

Unlock free access to practice-relevant journal articles

Join our community of medical professionals and register now to access a handpicked selection of journal articles from Springer's Medical portfolio. 

Looking for something specific?

Find articles from over 500 clinical journals from Springer with the search function.

About journals on Springer Medicine

The range of medical journals on Springer Medicine is extremely diverse. It includes the current editions and archives of around 500 English-language journals from almost all medical disciplines published by Springer. 

The specialist literature is usually available both online in full text and as a PDF for download. The online view is optimized in such a way that the specialist texts can be read comfortably on all screen sizes, from desktops to tablets to smartphones. We also include features to support your use of the journals for your research, such as bookmark setting.

Whether you’re interested in internal medicine, surgery, general medicine, gynecology, orthopedics, neurology, or pediatrics, there are excellent journals in almost every subject area, such as the BMC Series, Diabetologia, Breast Cancer Research, Current Obesity Reports, CNS Drugs and many others, all of which are an integral part of the everyday life of doctors across Europe. 

The breadth of content from this suite of journals allows the Springer Medicine team to collect and deliver broad-ranging content across the full spectrum of medical knowledge, with a special focus on topics highlighted by these leading journals and their editorial boards and specialist authors. This guarantees a high quality of content and ensures that our readers are offered the most relevant topics in their respective specialist area. 

Our experienced clinical content managers constantly monitor the needs of medical professionals to provide up-to-date reports from international congresses, expert interviews, and a range of digestible content on emerging topics in the field of medicine.

Published in:

Open Access 01-12-2024 | Research

Detailed analysis of the histology-specific impact of ascites volume on the outcome of epithelial ovarian cancer: a multi-institutional retrospective cohort study

Authors: Shohei Iyoshi, Mariko Kimura, Masato Yoshihara, Atsushi Kunishima, Emiri Miyamoto, Hiroki Fujimoto, Kazuhisa Kitami, Kazumasa Mogi, Kaname Uno, Sho Tano, Nobuhisa Yoshikawa, Ryo Emoto, Shigeyuki Matsui, Hiroaki Kajiyama

Published in: BMC Cancer | Issue 1/2024

Login to get access

Abstract

Background

The accumulation of ascites is a major symptom of ovarian cancer. The volume of ascites is a pathophysiological indicator of the peritoneal environment, such as inflammation and fibrosis; however, the relationship between the volume of ascites and oncological outcomes remains unclear. We herein retrospectively examined the effects of the volume of ascites on the prognosis of epithelial ovarian cancer in a multi-institutional large cohort using the stratification of clinical characteristics and statistical adjustment methods.

Methods

Of 5,268 patients with ovarian tumors in the Tokai Ovarian Tumor Study Group between 1986 and 2020, we included 1,966 cases of epithelial ovarian cancer and examined the relationship between the volume of ascites at the initial surgery and the prognosis of patients. We performed a multivariate analysis and propensity score weighting for covariate adjustments to precisely estimate the prognostic impact of ascites accumulation. A subgroup analysis was also performed to examine differences in the prognostic implications of ascites accumulation among histotypes.

Results

A reservoir of 100 mL of ascites was confirmed as the cut-off value in our cohort. A Kaplan-Meyer analysis with propensity score adjustments indicated that the accumulation of more than 100 mL of ascites shortened overall survival. The multivariate analysis revealed that the increased accumulation of 100 mL of ascites was an independent prognostic factor for overall survival (HR 1.242; 95% CI 1.050–1.470; P = 0.012). The subgroup analysis showed the prognostic significance of ascites accumulation in mucinous and endometrioid histologies.

Conclusions

The accumulation of even a low to intermediate volume of ascites (≥ 100 mL) was confirmed to be an independent poor prognostic factor in epithelial ovarian cancer. Furthermore, its prognostic impact differed among histotypes.
Appendix
Available only for authorised users
Literature
1.
2.
3.
go back to reference Lengyel E. Ovarian Cancer Development and Metastasis. Am J Pathol. 2010;09:177:1053–64.CrossRef Lengyel E. Ovarian Cancer Development and Metastasis. Am J Pathol. 2010;09:177:1053–64.CrossRef
4.
go back to reference Motohara T, Masuda K, Morotti M, Zheng Y, El-Sahhar S, Chong KY, et al. An evolving story of the metastatic voyage of ovarian cancer cells: cellular and molecular orchestration of the adipose-rich metastatic microenvironment. Oncogene 4/. 2019;38:2885–98.CrossRef Motohara T, Masuda K, Morotti M, Zheng Y, El-Sahhar S, Chong KY, et al. An evolving story of the metastatic voyage of ovarian cancer cells: cellular and molecular orchestration of the adipose-rich metastatic microenvironment. Oncogene 4/. 2019;38:2885–98.CrossRef
5.
go back to reference Uno K, Iyoshi S, Yoshihara M, Kitami K, Mogi K, Fujimoto H et al. Metastatic voyage of Ovarian Cancer cells in Ascites with the assistance of various Cellular Components. Int J Mol Sci. 2022;23. Uno K, Iyoshi S, Yoshihara M, Kitami K, Mogi K, Fujimoto H et al. Metastatic voyage of Ovarian Cancer cells in Ascites with the assistance of various Cellular Components. Int J Mol Sci. 2022;23.
6.
go back to reference van Baal JOAM, Van de Vijver KK, Nieuwland R, van Noorden CJF, van Driel WJ, Sturk A, et al. The histophysiology and pathophysiology of the peritoneum. Tissue Cell. 2017;49:95–105.CrossRefPubMed van Baal JOAM, Van de Vijver KK, Nieuwland R, van Noorden CJF, van Driel WJ, Sturk A, et al. The histophysiology and pathophysiology of the peritoneum. Tissue Cell. 2017;49:95–105.CrossRefPubMed
7.
go back to reference Aziz MAAE, Agarwal K, Dasari S, Mitra AAK. Productive cross-talk with the Microenvironment: a critical step in Ovarian Cancer Metastasis. Cancers. 2019;11. Aziz MAAE, Agarwal K, Dasari S, Mitra AAK. Productive cross-talk with the Microenvironment: a critical step in Ovarian Cancer Metastasis. Cancers. 2019;11.
8.
go back to reference Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat Rev Cancer. 2005;5:355–66.CrossRefPubMed Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat Rev Cancer. 2005;5:355–66.CrossRefPubMed
9.
go back to reference Feigenberg T, Clarke B, Virtanen C, Plotkin A, Letarte M, Rosen B, et al. Molecular profiling and clinical outcome of high-grade serous ovarian cancer presenting with low- versus high-volume ascites. Biomed Res Int. 2014;2014:367103.CrossRefPubMedPubMedCentral Feigenberg T, Clarke B, Virtanen C, Plotkin A, Letarte M, Rosen B, et al. Molecular profiling and clinical outcome of high-grade serous ovarian cancer presenting with low- versus high-volume ascites. Biomed Res Int. 2014;2014:367103.CrossRefPubMedPubMedCentral
10.
go back to reference Coosemans AN, Baert T, D’Heygere V, Wouters R, DE Laet L, VAN Hoylandt A, et al. Increased immunosuppression is related to increased amounts of Ascites and Inferior Prognosis in Ovarian Cancer. Anticancer Res. 2019;39:5953–62.CrossRefPubMed Coosemans AN, Baert T, D’Heygere V, Wouters R, DE Laet L, VAN Hoylandt A, et al. Increased immunosuppression is related to increased amounts of Ascites and Inferior Prognosis in Ovarian Cancer. Anticancer Res. 2019;39:5953–62.CrossRefPubMed
11.
go back to reference Nasioudis D, Byrne M, Ko EM, Haggerty AF, Cory L, Giuntoli RL, Ii, et al. Ascites volume at the time of primary debulking and overall survival of patients with advanced epithelial ovarian cancer. Int J Gynecol Cancer. 2021;31:1579–83.CrossRefPubMed Nasioudis D, Byrne M, Ko EM, Haggerty AF, Cory L, Giuntoli RL, Ii, et al. Ascites volume at the time of primary debulking and overall survival of patients with advanced epithelial ovarian cancer. Int J Gynecol Cancer. 2021;31:1579–83.CrossRefPubMed
12.
go back to reference Nasioudis D, Byrne M, Ko E, Haggerty A, Cory L, Giuntoli R, et al. Ascites volume at the time of primary debulking and overall survival of patients with advanced-stage epithelial ovarian cancer. Gynecol Oncol. 2021;162:S91.CrossRef Nasioudis D, Byrne M, Ko E, Haggerty A, Cory L, Giuntoli R, et al. Ascites volume at the time of primary debulking and overall survival of patients with advanced-stage epithelial ovarian cancer. Gynecol Oncol. 2021;162:S91.CrossRef
13.
go back to reference Szender JB, Emmons T, Belliotti S, Dickson D, Khan A, Morrell K, et al. Impact of ascites volume on clinical outcomes in ovarian cancer: a cohort study. Gynecol Oncol. 2017;146:491–7.CrossRefPubMedPubMedCentral Szender JB, Emmons T, Belliotti S, Dickson D, Khan A, Morrell K, et al. Impact of ascites volume on clinical outcomes in ovarian cancer: a cohort study. Gynecol Oncol. 2017;146:491–7.CrossRefPubMedPubMedCentral
14.
go back to reference Quan Q, Zhou S, Liu Y, Yin W, Liao Q, Ren S, et al. Relationship between ascites volume and clinical outcomes in epithelial ovarian cancer. J Obstet Gynaecol Res. 2021;47:1527–35.CrossRefPubMed Quan Q, Zhou S, Liu Y, Yin W, Liao Q, Ren S, et al. Relationship between ascites volume and clinical outcomes in epithelial ovarian cancer. J Obstet Gynaecol Res. 2021;47:1527–35.CrossRefPubMed
15.
go back to reference Janco JMT, Glaser G, Kim B, McGree ME, Weaver AL, Cliby WA, et al. Development of a prediction model for residual disease in newly diagnosed advanced ovarian cancer. Gynecol Oncol. 2015;138:70–7.CrossRefPubMed Janco JMT, Glaser G, Kim B, McGree ME, Weaver AL, Cliby WA, et al. Development of a prediction model for residual disease in newly diagnosed advanced ovarian cancer. Gynecol Oncol. 2015;138:70–7.CrossRefPubMed
17.
go back to reference Chen VW, Ruiz B, Killeen JL, Coté TR, Wu XC, Correa CN. Pathology and classification of ovarian tumors. Cancer. 2003;97(10 Suppl):2631–42.CrossRefPubMed Chen VW, Ruiz B, Killeen JL, Coté TR, Wu XC, Correa CN. Pathology and classification of ovarian tumors. Cancer. 2003;97(10 Suppl):2631–42.CrossRefPubMed
18.
go back to reference Zeppernick F, Meinhold-Heerlein I. The new FIGO staging system for ovarian, fallopian tube, and primary peritoneal cancer. Arch Gynecol Obstet. 2014;290:839–42.CrossRefPubMed Zeppernick F, Meinhold-Heerlein I. The new FIGO staging system for ovarian, fallopian tube, and primary peritoneal cancer. Arch Gynecol Obstet. 2014;290:839–42.CrossRefPubMed
19.
go back to reference Tokunaga H, Shimada M, Ishikawa M, Yaegashi N. TNM classification of gynaecological malignant tumours, eighth edition: changes between the seventh and eighth editions. Jpn J Clin Oncol. 2019;49:311–20.CrossRefPubMed Tokunaga H, Shimada M, Ishikawa M, Yaegashi N. TNM classification of gynaecological malignant tumours, eighth edition: changes between the seventh and eighth editions. Jpn J Clin Oncol. 2019;49:311–20.CrossRefPubMed
21.
go back to reference Komiyama S, Katabuchi H, Mikami M, Nagase S, Okamoto A, Ito K, et al. Japan Society of Gynecologic Oncology guidelines 2015 for the treatment of ovarian cancer including primary peritoneal cancer and fallopian tube cancer. Int J Clin Oncol. 2016;21:435–46.CrossRefPubMed Komiyama S, Katabuchi H, Mikami M, Nagase S, Okamoto A, Ito K, et al. Japan Society of Gynecologic Oncology guidelines 2015 for the treatment of ovarian cancer including primary peritoneal cancer and fallopian tube cancer. Int J Clin Oncol. 2016;21:435–46.CrossRefPubMed
22.
go back to reference Suzuki S, Kajiyama H, Shibata K, Ino K, Nawa A, Sakakibara K, et al. Is there any association between retroperitoneal lymphadenectomy and survival benefit in ovarian clear cell carcinoma patients? Ann Oncol. 2008;19:1284–7.CrossRefPubMed Suzuki S, Kajiyama H, Shibata K, Ino K, Nawa A, Sakakibara K, et al. Is there any association between retroperitoneal lymphadenectomy and survival benefit in ovarian clear cell carcinoma patients? Ann Oncol. 2008;19:1284–7.CrossRefPubMed
23.
go back to reference Rustin GJS, Vergote I, Eisenhauer E, Pujade-Lauraine E, Quinn M, Thigpen T, et al. Definitions for response and progression in ovarian cancer clinical trials incorporating RECIST 1.1 and CA 125 agreed by the Gynecological Cancer Intergroup (GCIG). Int J Gynecol Cancer. 2011;21:419–23.CrossRefPubMed Rustin GJS, Vergote I, Eisenhauer E, Pujade-Lauraine E, Quinn M, Thigpen T, et al. Definitions for response and progression in ovarian cancer clinical trials incorporating RECIST 1.1 and CA 125 agreed by the Gynecological Cancer Intergroup (GCIG). Int J Gynecol Cancer. 2011;21:419–23.CrossRefPubMed
24.
go back to reference Rosenbaum PR, Rubin DB. Reducing Bias in Observational studies using subclassification on the Propensity score. J Am Stat Assoc. 1984;79:516–24.CrossRef Rosenbaum PR, Rubin DB. Reducing Bias in Observational studies using subclassification on the Propensity score. J Am Stat Assoc. 1984;79:516–24.CrossRef
25.
go back to reference Yoshihara M, Uno K, Tano S, Mayama M, Ukai M, Kondo S, et al. The efficacy of recombinant human soluble thrombomodulin for obstetric disseminated intravascular coagulation: a retrospective study. Crit Care. 2015;19:369.CrossRefPubMedPubMedCentral Yoshihara M, Uno K, Tano S, Mayama M, Ukai M, Kondo S, et al. The efficacy of recombinant human soluble thrombomodulin for obstetric disseminated intravascular coagulation: a retrospective study. Crit Care. 2015;19:369.CrossRefPubMedPubMedCentral
26.
go back to reference Manning-Geist BL, Hicks-Courant K, Gockley AA, Clark RM, Del Carmen MG, Growdon WB et al. A novel classification of residual disease after interval debulking surgery for advanced-stage ovarian cancer to better distinguish oncologic outcome. Am J Obstet Gynecol. 2019;221:326.e1-326.e7. Manning-Geist BL, Hicks-Courant K, Gockley AA, Clark RM, Del Carmen MG, Growdon WB et al. A novel classification of residual disease after interval debulking surgery for advanced-stage ovarian cancer to better distinguish oncologic outcome. Am J Obstet Gynecol. 2019;221:326.e1-326.e7.
27.
go back to reference Dabi Y, Huchon C, Ouldamer L, Bendifallah S, Collinet P, Bricou A, et al. Patients with stage IV epithelial ovarian cancer: understanding the determinants of survival. J Transl Med. 2020;18:134.CrossRefPubMedPubMedCentral Dabi Y, Huchon C, Ouldamer L, Bendifallah S, Collinet P, Bricou A, et al. Patients with stage IV epithelial ovarian cancer: understanding the determinants of survival. J Transl Med. 2020;18:134.CrossRefPubMedPubMedCentral
28.
go back to reference Li Y, Mao AS, Seo BR, Zhao X, Gupta SK, Chen M, et al. Compression-induced dedifferentiation of adipocytes promotes tumor progression. Sci Adv. 2020;01:6:eaax5611.CrossRef Li Y, Mao AS, Seo BR, Zhao X, Gupta SK, Chen M, et al. Compression-induced dedifferentiation of adipocytes promotes tumor progression. Sci Adv. 2020;01:6:eaax5611.CrossRef
29.
go back to reference Shohei, Iyoshi Masato, Yoshihara Kae, Nakamura Mai, Sugiyama Yoshihiro, Koya Kazuhisa, Kitami Kaname, Uno Kazumasa, Mogi Sho, Tano Hiroyuki, Tomita Keiji, Kajiwara Masayasu, Taki Shigehiro, Yamaguchi Akihiro, Nawa Hiroaki, Kajiyama (2021) Pro‐tumoral behavior of omental adipocyte‐derived fibroblasts in tumor microenvironment at the metastatic site of ovarian cancer Abstract International Journal of Cancer 149(11) 1961-1972. https://doi.org/10.1002/ijc.v149.11. Shohei, Iyoshi Masato, Yoshihara Kae, Nakamura Mai, Sugiyama Yoshihiro, Koya Kazuhisa, Kitami Kaname, Uno Kazumasa, Mogi Sho, Tano Hiroyuki, Tomita Keiji, Kajiwara Masayasu, Taki Shigehiro, Yamaguchi Akihiro, Nawa Hiroaki, Kajiyama (2021) Pro‐tumoral behavior of omental adipocyte‐derived fibroblasts in tumor microenvironment at the metastatic site of ovarian cancer Abstract International Journal of Cancer 149(11) 1961-1972. https://​doi.​org/​10.​1002/​ijc.​v149.​11.
Metadata
Title
Detailed analysis of the histology-specific impact of ascites volume on the outcome of epithelial ovarian cancer: a multi-institutional retrospective cohort study
Authors
Shohei Iyoshi
Mariko Kimura
Masato Yoshihara
Atsushi Kunishima
Emiri Miyamoto
Hiroki Fujimoto
Kazuhisa Kitami
Kazumasa Mogi
Kaname Uno
Sho Tano
Nobuhisa Yoshikawa
Ryo Emoto
Shigeyuki Matsui
Hiroaki Kajiyama
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2024
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-024-13218-1