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

IF 8.9 1区医学

Journal of Cachexia, Sarcopenia and Muscle Pub Date : 2023-07-28 DOI:10.1002/jcsm.13289

Chia-Sui Weng, Wan-Chun Huang, Chih-Long Chang, Ya-Ting Jan, Tze-Chien Chen, Jie Lee

{"title":"Association of malignant ascites with systemic inflammation and muscle loss after treatment in advanced-stage ovarian cancer","authors":"Chia-Sui Weng, Wan-Chun Huang, Chih-Long Chang, Ya-Ting Jan, Tze-Chien Chen, Jie Lee","doi":"10.1002/jcsm.13289","DOIUrl":null,"url":null,"abstract":"<div>\n \n \n <section>\n \n <h3> Background</h3>\n \n <p>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.</p>\n </section>\n \n <section>\n \n <h3> Methods</h3>\n \n <p>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.</p>\n </section>\n \n <section>\n \n <h3> Results</h3>\n \n <p>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%, <i>P</i> < 0.001; SMD: −4.0% vs. −0.4%, <i>P</i> < 0.001; albumin: −4.4% vs. 2.1%, <i>P</i> < 0.001; PNI: −8.4% vs. −0.1%, <i>P</i> < 0.001; NLR: 20.6% vs. −29.4%, <i>P</i> < 0.001; and PLR: 1.7% vs. −19.4%, <i>P</i> < 0.001). The changes in SMI and SMD were correlated with the changes in albumin, PNI, NLR, and PLR (all <i>P</i> < 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, <i>P</i> < 0.001; NLR change: β = −0.02, <i>P</i> = 0.003; albumin change: β = 0.37, <i>P</i> < 0.001). Ascites and NLR changes were negatively while PNI change was positively correlated with SMD change (ascites: β = −1.28, <i>P</i> = 0.02; NLR change: β = −0.02, <i>P</i> < 0.001; PNI change: β = 0.11, <i>P</i> = 0.04). In mediation analysis, ascites had a direct effect on SMI change (<i>P</i> < 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 (<i>P</i> < 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).</p>\n </section>\n \n <section>\n \n <h3> Conclusions</h3>\n \n <p>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.</p>\n </section>\n </div>","PeriodicalId":186,"journal":{"name":"Journal of Cachexia, Sarcopenia and Muscle","volume":"14 5","pages":"2114-2125"},"PeriodicalIF":8.9000,"publicationDate":"2023-07-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jcsm.13289","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Cachexia, Sarcopenia and Muscle","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/jcsm.13289","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}

引用次数: 0

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.

Abstract Image

查看原文本刊更多论文

晚期癌症治疗后恶性腹水与全身炎症和肌肉损失的相关性。

背景：恶性腹水在晚期癌症中普遍存在，可能有助于识别肌肉损失的驱动因素。本研究旨在评估晚期癌症治疗后腹水与全身炎症和肌肉变化的关系。方法：我们评估了307例癌症晚期（III/IVA）患者，他们在2010年至2019年间接受了初级减瘤手术和辅助铂基化疗。使用术前和化疗后L3的门静脉期对比增强计算机断层扫描测量骨骼肌指数（SMI）和放射密度（SMD）的变化。使用白蛋白水平、预后营养指数（PNI）、中性粒细胞淋巴细胞比率（NLR）和血小板淋巴细胞比率（PLR）测量全身炎症。主要终点是治疗后SMI和SMD的变化。线性回归分析用于检验肌肉变化和其他协变量之间的相关性。使用中介分析来确定调解员。结果：中位（范围）年龄为53岁（23-83岁）。随访的中位持续时间（范围）为5.2年（1.1-11.3）。总的来说，187名（60.9%）患者有腹水。有腹水和无腹水患者治疗后肌肉和全身炎症标志物的变化有显著差异（SMI:3.9%vs.2.2%，P结论：晚期卵巢癌症在初次减瘤手术和辅助化疗后，恶性腹水与全身炎症增强和肌肉损失有关。腹水与肌肉损失之间的联系可能是由全身炎症介导的。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Journal of Cachexia, Sarcopenia and Muscle Medicine-Orthopedics and Sports Medicine

自引率

12.40%

发文量

期刊介绍： The Journal of Cachexia, Sarcopenia, and Muscle is a prestigious, peer-reviewed international publication committed to disseminating research and clinical insights pertaining to cachexia, sarcopenia, body composition, and the physiological and pathophysiological alterations occurring throughout the lifespan and in various illnesses across the spectrum of life sciences. This journal serves as a valuable resource for physicians, biochemists, biologists, dieticians, pharmacologists, and students alike.