Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer

Abstract Background Malignant ascites is prevalent in advanced‐stage ovarian cancer and may facilitate identification of the drivers of muscle loss. This study aimed to evaluate the association of ascites with changes in systemic inflammation and muscle after treatment of advanced‐stage ovarian canc...

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Main Authors: Chia‐Sui Weng, Wan‐Chun Huang, Chih‐Long Chang, Ya‐Ting Jan, Tze‐Chien Chen, Jie Lee
Format: Article
Language:English
Published: Wiley 2023-10-01
Series:Journal of Cachexia, Sarcopenia and Muscle
Subjects:
Online Access:https://doi.org/10.1002/jcsm.13289
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author Chia‐Sui Weng
Wan‐Chun Huang
Chih‐Long Chang
Ya‐Ting Jan
Tze‐Chien Chen
Jie Lee
author_facet Chia‐Sui Weng
Wan‐Chun Huang
Chih‐Long Chang
Ya‐Ting Jan
Tze‐Chien Chen
Jie Lee
author_sort Chia‐Sui Weng
collection DOAJ
description Abstract Background Malignant ascites is prevalent in advanced‐stage ovarian cancer and may facilitate identification of the drivers of muscle loss. This study aimed to evaluate the association of ascites with changes in systemic inflammation and muscle after treatment of advanced‐stage ovarian cancer. Methods We evaluated 307 patients with advanced‐stage (III/IVA) ovarian cancer who underwent primary debulking surgery and adjuvant platinum‐based chemotherapy between 2010 and 2019. The changes in skeletal muscle index (SMI) and radiodensity (SMD) were measured using pre‐surgery and post‐chemotherapy portal‐venous phase contrast‐enhanced computed tomography scans at L3. Systemic inflammation was measured using albumin levels, prognostic nutritional index (PNI), neutrophil‐lymphocyte ratio (NLR), and platelet‐lymphocyte ratio (PLR). Primary endpoint was the changes in SMI and SMD after treatment. Linear regression analysis was used to test associations between muscle change and other covariates. Mediation analysis was used to determine the mediator. Results The median (range) age was 53 (23–83) years. The median duration (range) of follow‐up was 5.2 (1.1–11.3) years. Overall, 187 (60.9%) patients had ascites. The changes in muscle and systemic inflammatory markers after treatment were significantly different between patients with and without ascites (SMI: −3.9% vs. 2.2%, P < 0.001; SMD: −4.0% vs. −0.4%, P < 0.001; albumin: −4.4% vs. 2.1%, P < 0.001; PNI: −8.4% vs. −0.1%, P < 0.001; NLR: 20.6% vs. −29.4%, P < 0.001; and PLR: 1.7% vs. −19.4%, P < 0.001). The changes in SMI and SMD were correlated with the changes in albumin, PNI, NLR, and PLR (all P < 0.001). In multiple linear regression, ascites and NLR changes were negatively while albumin change was positively correlated with SMI change (ascites: β = −3.19, P < 0.001; NLR change: β = −0.02, P = 0.003; albumin change: β = 0.37, P < 0.001). Ascites and NLR changes were negatively while PNI change was positively correlated with SMD change (ascites: β = −1.28, P = 0.02; NLR change: β = −0.02, P < 0.001; PNI change: β = 0.11, P = 0.04). In mediation analysis, ascites had a direct effect on SMI change (P < 0.001) and an indirect effect mediated by NLR change (indirect effects = −1.61, 95% confidence interval [CI]: −2.22 to −1.08) and albumin change (indirect effects = −2.92, 95% CI: −4.01 to −1.94). Ascites had a direct effect on SMD change (P < 0.001) and an indirect effect mediated by NLR change (indirect effects = −1.76, 95% CI: −2.34 to −1.22) and PNI change (indirect effects = −2.00, 95% CI: −2.79 to −1.36). Conclusions Malignant ascites was associated with enhanced systemic inflammation and muscle loss after primary debulking surgery and adjuvant chemotherapy in advanced‐stage ovarian cancer. The association between ascites and muscle loss may be mediated by systemic inflammation.
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spelling doaj.art-85e3c33fb8bc439ebe0d402f8e43e2882023-10-13T01:32:12ZengWileyJournal of Cachexia, Sarcopenia and Muscle2190-59912190-60092023-10-011452114212510.1002/jcsm.13289Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancerChia‐Sui Weng0Wan‐Chun Huang1Chih‐Long Chang2Ya‐Ting Jan3Tze‐Chien Chen4Jie Lee5Department of Obstetrics and Gynecology MacKay Memorial Hospital Taipei TaiwanDepartment of Obstetrics and Gynecology MacKay Memorial Hospital Taipei TaiwanDepartment of Obstetrics and Gynecology MacKay Memorial Hospital Taipei TaiwanDepartment of Radiology MacKay Memorial Hospital Taipei TaiwanDepartment of Obstetrics and Gynecology MacKay Memorial Hospital Taipei TaiwanDepartment of Medicine MacKay Medical College New Taipei City TaiwanAbstract Background Malignant ascites is prevalent in advanced‐stage ovarian cancer and may facilitate identification of the drivers of muscle loss. This study aimed to evaluate the association of ascites with changes in systemic inflammation and muscle after treatment of advanced‐stage ovarian cancer. Methods We evaluated 307 patients with advanced‐stage (III/IVA) ovarian cancer who underwent primary debulking surgery and adjuvant platinum‐based chemotherapy between 2010 and 2019. The changes in skeletal muscle index (SMI) and radiodensity (SMD) were measured using pre‐surgery and post‐chemotherapy portal‐venous phase contrast‐enhanced computed tomography scans at L3. Systemic inflammation was measured using albumin levels, prognostic nutritional index (PNI), neutrophil‐lymphocyte ratio (NLR), and platelet‐lymphocyte ratio (PLR). Primary endpoint was the changes in SMI and SMD after treatment. Linear regression analysis was used to test associations between muscle change and other covariates. Mediation analysis was used to determine the mediator. Results The median (range) age was 53 (23–83) years. The median duration (range) of follow‐up was 5.2 (1.1–11.3) years. Overall, 187 (60.9%) patients had ascites. The changes in muscle and systemic inflammatory markers after treatment were significantly different between patients with and without ascites (SMI: −3.9% vs. 2.2%, P < 0.001; SMD: −4.0% vs. −0.4%, P < 0.001; albumin: −4.4% vs. 2.1%, P < 0.001; PNI: −8.4% vs. −0.1%, P < 0.001; NLR: 20.6% vs. −29.4%, P < 0.001; and PLR: 1.7% vs. −19.4%, P < 0.001). The changes in SMI and SMD were correlated with the changes in albumin, PNI, NLR, and PLR (all P < 0.001). In multiple linear regression, ascites and NLR changes were negatively while albumin change was positively correlated with SMI change (ascites: β = −3.19, P < 0.001; NLR change: β = −0.02, P = 0.003; albumin change: β = 0.37, P < 0.001). Ascites and NLR changes were negatively while PNI change was positively correlated with SMD change (ascites: β = −1.28, P = 0.02; NLR change: β = −0.02, P < 0.001; PNI change: β = 0.11, P = 0.04). In mediation analysis, ascites had a direct effect on SMI change (P < 0.001) and an indirect effect mediated by NLR change (indirect effects = −1.61, 95% confidence interval [CI]: −2.22 to −1.08) and albumin change (indirect effects = −2.92, 95% CI: −4.01 to −1.94). Ascites had a direct effect on SMD change (P < 0.001) and an indirect effect mediated by NLR change (indirect effects = −1.76, 95% CI: −2.34 to −1.22) and PNI change (indirect effects = −2.00, 95% CI: −2.79 to −1.36). Conclusions Malignant ascites was associated with enhanced systemic inflammation and muscle loss after primary debulking surgery and adjuvant chemotherapy in advanced‐stage ovarian cancer. The association between ascites and muscle loss may be mediated by systemic inflammation.https://doi.org/10.1002/jcsm.13289Malignant ascitesOvarian cancerSkeletal muscleSurvivalSystemic inflammation
spellingShingle Chia‐Sui Weng
Wan‐Chun Huang
Chih‐Long Chang
Ya‐Ting Jan
Tze‐Chien Chen
Jie Lee
Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer
Journal of Cachexia, Sarcopenia and Muscle
Malignant ascites
Ovarian cancer
Skeletal muscle
Survival
Systemic inflammation
title Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer
title_full Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer
title_fullStr Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer
title_full_unstemmed Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer
title_short Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced‐stage ovarian cancer
title_sort association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced stage ovarian cancer
topic Malignant ascites
Ovarian cancer
Skeletal muscle
Survival
Systemic inflammation
url https://doi.org/10.1002/jcsm.13289
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