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Wang LJ, Lei CL, Wang TA, Lin ZF, Feng SJ, Wei T, Li YQ, Shen MR, Li Y, Liao LF. Prognostic value of the preoperative systemic immune-inflammation nutritional index in patients with gastric cancer. World J Clin Oncol 2025; 16:102294. [DOI: 10.5306/wjco.v16.i4.102294] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/14/2024] [Revised: 12/04/2024] [Accepted: 01/21/2025] [Indexed: 03/26/2025] Open
Abstract
BACKGROUND Gastric cancer (GC) is the fifth most common cancer and the third leading cause of cancer-related deaths in China. Many patients with GC frequently experience symptoms related to the disease, including anorexia, nausea, vomiting, and other discomforts, and often suffer from malnutrition, which in turn negatively affects perioperative safety, prognosis, and the effectiveness of adjuvant therapeutic measures. Consequently, some nutritional indicators such as nutritional risk index (NRI), prognostic nutritional index (PNI), and systemic immune-inflammatory-nutritional index (SIINI) can be used as predictors of the prognosis of GC patients.
AIM To examine the prognostic significance of PNI, NRI, and SIINI in postoperative patients with GC.
METHODS A retrospective analysis was conducted on the clinical data of patients with GC who underwent surgical treatment at the Guangxi Medical University Cancer Hospital between January 2010 and December 2018. The area under the receiver operating characteristic (ROC) curve was assessed using ROC curve analysis, and the optimal cutoff values for NRI, PNI, and SIINI were identified using the You-Review-HTMLden index. Survival analysis was performed using the Kaplan-Meier method. In addition, univariate and multivariate analyses were conducted using the Cox proportional hazards regression model.
RESULTS This study included a total of 803 patients. ROC curves were used to evaluate the prognostic ability of NRI, PNI, and SIINI. The results revealed that SIINI had superior predictive accuracy. Survival analysis indicated that patients with GC in the low SIINI group had a significantly better survival rate than those in the high SIINI group (P < 0.05). Univariate analysis identified NRI [hazard ratio (HR) = 0.68, 95% confidence interval (CI): 0.52-0.89, P = 0.05], PNI (HR = 0.60, 95%CI: 0.46-0.79, P < 0.001), and SIINI (HR = 2.10, 95%CI: 1.64-2.69, P < 0.001) as prognostic risk factors for patients with GC. However, multifactorial analysis indicated that SIINI was an independent risk factor for the prognosis of patients with GC (HR = 1.65, 95%CI: 1.26-2.16, P < 0.001).
CONCLUSION Analysis of clinical retrospective data revealed that SIINI is a valuable indicator for predicting the prognosis of patients with GC. Compared with NRI and PNI, SIINI may offer greater application for prognostic assessment.
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Affiliation(s)
- Li-Jing Wang
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Cai-Lu Lei
- School of Pharmaceutical Science, Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Ting-An Wang
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Zhi-Feng Lin
- School of Pharmaceutical Science, Guangxi Medical University, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Shi-Jie Feng
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Tao Wei
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Yan-Qin Li
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Meng-Ru Shen
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Yan Li
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Liu-Feng Liao
- Department of Pharmacy, Guangxi Medical University Cancer Hospital, Nanning 530021, Guangxi Zhuang Autonomous Region, China
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Pan H, Sun H, Zuo Y, Zhao R, Xue Y, Song H. The prealbumin-CD19 + index predicts surgical survival in patients with GC. BMC Cancer 2025; 25:359. [PMID: 40016677 PMCID: PMC11866875 DOI: 10.1186/s12885-025-13715-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/02/2024] [Accepted: 02/11/2025] [Indexed: 03/01/2025] Open
Abstract
OBJECTIVE This study aimed to establish a prealbumin (PALB)-CD19+ index that combines nutritional and immune statuses to comprehensively evaluate the prognosis of GC patients undergoing surgery. METHODS A total of 389 patients who were diagnosed with GC and who underwent surgical procedures at our institution between January 2016 and December 2020 were included in this study. Among them, 97 patients underwent subtotal gastrectomy, 271 underwent total gastrectomy, and 21 underwent palliative resection. The PALB-CD19+ index was developed using Cox regression analysis and regression coefficients, and LASSO regression analysis was employed to eliminate multicollinearity. Receiver operating characteristic (ROC) curves were used to calculate optimal cut-off values, and the prognostic value of different indices was compared using the area under the curve (AUC). Cox regression analysis was further utilized to identify independent prognostic factors. Survival analysis was conducted to explore differences in progression-free survival (PFS) and overall survival (OS) among patient groups. Finally, the prognostic significance of relevant factors was validated using a nomogram. RESULTS This study included 389 patients, 276 males and 113 females, with a mean age of 59.10 ± 10.19 years. Cox analysis identified PALB and CD19+ as significant factors influencing survival, forming the basis for the PALB-CD19+ index. The cut-off values for PALB and CD19+ were determined to be 230.50 mg/L and 15.40%, respectively. Cox regression analysis confirmed that the PALB-CD19+ index was an independent prognostic factor for both PFS and OS. Survival analysis demonstrated that patients with a lower PALB-CD19+ index had significantly shorter PFS and OS (χ² = 45.54, P < 0.001; χ² = 47.69, P < 0.001). Subgroup analysis across different TNM stages further validated the prognostic value of the PALB-CD19+ index (all P < 0.05). Nomograms incorporating the PALB-CD19+ index showed high accuracy, with concordance indices (C-index) in the training and validation cohorts approaching or exceeding 0.8. CONCLUSIONS The PALB-CD19+ index exhibits potential prognostic value in predicting surgical outcomes in GC patients. Its ability to integrate nutritional and immune parameters may provide clinicians with a novel and comprehensive tool for identifying high-risk patients and guiding personalized treatment strategies.
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Affiliation(s)
- Hongming Pan
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin, Heilongjiang, 150081, China
| | - Hao Sun
- Department of Breast Surgery, Sixth Affiliated Hospital of Harbin Medical University, Harbin, 150023, China
| | - Yanjiao Zuo
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin, Heilongjiang, 150081, China
| | - Ruihu Zhao
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin, Heilongjiang, 150081, China
| | - Yingwei Xue
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin, Heilongjiang, 150081, China
| | - Hongjiang Song
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin, Heilongjiang, 150081, China.
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3
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He H, Ma Y, Liu G, Liu S, Liu Q, Yao J, Huang C, Liu J, Zhou L, Wang T, Wang T, Wang N, Deng X, Wang Y. Early oral feeding post gastrectomy in gastric cancer: quasi-experimental study. BMJ Support Palliat Care 2025:spcare-2024-005183. [PMID: 39965902 DOI: 10.1136/spcare-2024-005183] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/12/2024] [Accepted: 02/06/2025] [Indexed: 02/20/2025]
Abstract
OBJECTIVE This study aims to investigate the safety and feasibility of early oral feeding in patients with gastric cancer after gastrectomy. METHODS A total of 135 patients with gastric cancer who would receive gastrectomy were enrolled in the study, with 61 in early oral feeding group and 74 in control group. Outcomes included nutrient intake, nutritional status, gastrointestinal functions and symptoms, pain, physical activity time, clinical outcomes and inflammation markers. RESULTS In comparison with control group, patients in early oral feeding group had significantly higher compliance rates of oral energy and protein intake, lower needs of parenteral nutrition and shorter postoperative oral feeding start time during hospitalisation. Moreover, the compliance rate of oral protein intake at 1 week after discharge was higher in patients with gastric cancer of early oral feeding group compared with control group. The gastrointestinal function was better in early oral feeding group, evidenced by shorter time to the first flatus and dwell time for gastric tube. CONCLUSION This study demonstrated that early oral feeding is safe and can significantly improve oral energy and oral protein intake and gastrointestinal functions during hospitalisation in patients with gastric cancer who received gastrectomy, as well as the oral protein intake after discharge. TRIAL REGISTRATION Chinese Clinical Trial Registry: ChiCTR2300069202.
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Affiliation(s)
- Haiyan He
- Department of Nursing, Army Medical University Daping Hospital, Chongqing, China
| | - Yuanyuan Ma
- Department of Nursing, Army Medical University Daping Hospital, Chongqing, China
| | - Guo Liu
- Department of Trauma Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Shuying Liu
- Department of Trauma Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Qin Liu
- Department of Gastrointestinal Colorectal and Anal Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Juan Yao
- Department of Intensive Care Unit, Army Medical University Daping Hospital, Chongqing, China
| | - Chengcheng Huang
- Department of Gastrointestinal Colorectal and Anal Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Jie Liu
- Department of Clinical Nutrition, Army Medical University Daping Hospital, Chongqing, China
| | - Liang Zhou
- Department of Field Surgery Research, Army Medical University Daping Hospital, Chongqing, China
| | - Ting Wang
- Department of Intensive Care Unit, Army Medical University Daping Hospital, Chongqing, China
| | - Teng Wang
- Department of Gastrointestinal Colorectal and Anal Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Na Wang
- Department of Trauma Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Xiaolian Deng
- Department of Gastrointestinal Colorectal and Anal Surgery, Army Medical University Daping Hospital, Chongqing, China
| | - Yaling Wang
- Nursing Department, Army Medical University Daping Hospital, Chongqing, China
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Seid A, Debebe Z, Ayelign A, Abeje M, Endris BS, Assefa M, Jemal A. Malnutrition Diagnosed by Patient-Generated Subjective Global Assessment and the Risk of All-Cause Mortality in Adults With Gastrointestinal Cancer: A Systematic Review and Meta-Analysis. J Hum Nutr Diet 2025; 38:e70012. [PMID: 39817621 DOI: 10.1111/jhn.70012] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2024] [Revised: 12/23/2024] [Accepted: 12/30/2024] [Indexed: 01/18/2025]
Abstract
INTRODUCTION Several reviews have highlighted that the Patient-Generated Subjective Global Assessment (PG-SGA) is the best diagnostic tool for assessing nutritional status in cancer patients. However, previous meta-analyses summarizing the prevalence of malnutrition and overall survival in patients with gastrointestinal (GI) cancer are quite limited. This study aims to determine the overall prevalence and association between malnutrition, as defined by the PG-SGA, and mortality in adults with GI cancer. METHODS A comprehensive systematic review of articles published from 2005 to 2023 was conducted using Google Scholar, PubMed, Web of Sciences and Scopus. The PRISMA guideline was followed to organize the entire content. A random-effects meta-analysis model using R Studio was performed to quantify the pooled proportion and hazard ratios (HRs). Publication bias was assessed using Egger's test and funnel plots. Heterogeneity was evaluated using I2 and Baujat plots. This study was registered in PROSPERO under the protocol number CRD42023465685. RESULTS In this study, 46 publications with 23,235 participants were included in the final meta-analysis. The overall prevalence of malnutrition among adults with GI cancer, as determined by the PG-SGA, was 61% (95% CI: 51%-70%, I2 = 99%). The pooled prevalence of moderate and severe malnutrition were 38% (95% CI: 31%-45%, I2 = 96%) and 21% (95% CI: 13%-31%, I2 = 98%), respectively. By cancer type, malnutrition was more common in patients with oesophageal cancer (78%, 95% CI: 45%-94%, I2 = 99%) and gastric cancer (75%, 95% CI: 68%-81%, I2 = 87%). Additionally, the overall risk (pooled HR) of malnutrition on mortality among GI cancer patients was 2.02 (95% CI: 1.63%-2.5%, I2 = 23%). CONCLUSION Malnutrition is common in adults with GI cancer and doubles the risk of all-cause mortality. These results emphasize the importance of ongoing efforts in prevention, early assessment, and intervention for malnutrition to minimize mortality rates.
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Affiliation(s)
- Awole Seid
- Center for Food Science and Nutrition, College of Natural and Computational Sciences, Addis Ababa University, Addis Ababa, Ethiopia
- Department of Adult Health Nursing, College of Medicine and Health Sciences, Bahir Dar University, Bahir Dar, Ethiopia
| | - Zelalem Debebe
- Center for Food Science and Nutrition, College of Natural and Computational Sciences, Addis Ababa University, Addis Ababa, Ethiopia
| | - Abebe Ayelign
- Department of Internal Medicine, School of Medicine, College of Medicine and Health Sciences, Bahir Dar University, Bahir Dar, Ethiopia
| | - Melsew Abeje
- Department of Nutrition and Dietetics, School of Public Health, Addis Ababa University, Addis Ababa, Ethiopia
| | - Bilal Shikur Endris
- Department of Nutrition and Dietetics, Addis Ababa University, Addis Ababa, Ethiopia
| | - Mathewos Assefa
- Department of Oncology, School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia
| | - Ahmedin Jemal
- Department of Surveillance and Health Services Research, American Cancer Society, Atlanta, Georgia, USA
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Ghelardi F, Fucà G, Cavalli C, Shitara K, Cohen R, Ambrosini M, Maron SB, Cerantola R, Nasca V, Liberti GD, Zambelli L, Palazzo M, Salati M, Aoki Y, Kawazoe A, Cowzer D, Lonardi S, André T, Randon G, Pietrantonio F. The Prognostic Nutritional Index in patients with microsatellite instability-high metastatic gastric or gastroesophageal cancers receiving immune checkpoint inhibitors. Dig Liver Dis 2025; 57:23-29. [PMID: 38772790 DOI: 10.1016/j.dld.2024.05.005] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/18/2024] [Revised: 04/22/2024] [Accepted: 05/06/2024] [Indexed: 05/23/2024]
Abstract
BACKGROUND Microsatellite instability high (MSI-H) and/or mismatch repair deficient (dMMR) status is the strongest predictive factor for immune checkpoint inhibitors (ICIs) benefit in patients with metastatic gastroesophageal cancer (mGC). Primary resistance to ICIs is a relevant issue, but prognostic and predictive factors are lacking. MATERIALS AND METHODS In this multinational, retrospective cohort of patients with MSI-H/dMMR mGC treated with ICIs without chemotherapy we collected baseline laboratory values to establish the prognostic nutritional index (PNI). We evaluated the association between baseline PNI with the activity and efficacy of ICIs. RESULTS At a median follow-up of 31.6 months, median progression-free survival (PFS) and 2-year PFS rate were not reached and 73.6 % in the PNI-high subgroup versus 6.3 months and 38.3 % in the PNI-low one (HR 0.32, 95 % CI: 0.16-0.61, p < .001). Median overall survival (OS) and 2-year OS rate were not reached and 81.9 % in the PNI-high subgroup versus 24.4 months and 50.5 % in the PNI-low one (HR 0.26, 95 % CI: 0.12-0.56, p < .001). In multivariable models, high PNI was associated with longer PFS and OS (HR 0.30, 95 % CI: 0.15-0.61, p <0.001 and 0.37, 95 % CI: 0.15-0.91, p = .031). CONCLUSIONS High PNI is associated with longer PFS and OS, in patients with MSI-H mGC receiving ICIs. Patients with low baseline PNI may benefit from intensive therapeutic approaches.
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Affiliation(s)
- Filippo Ghelardi
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Giovanni Fucà
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Chiara Cavalli
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Kohei Shitara
- Department of Gastroenterology and Gastrointestinal Oncology, National Cancer Center Hospital East, Chiba, Japan
| | - Romain Cohen
- Sorbonne Université, INSERM, Unité Mixte de Recherche Scientifique 938 and SIRIC CURAMUS, Centre de Recherche Saint-Antoine, Equipe Instabilité des Microsatellites et Cancer, Equipe labellisée par la Ligue Nationale contre le Cancer, Paris, France
| | - Margherita Ambrosini
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Steven B Maron
- Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, USA
| | - Riccardo Cerantola
- Medical Oncology 1, Veneto Institute of Oncology IOV-IRCCS, Padova, Italy
| | - Vincenzo Nasca
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Giorgia Di Liberti
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Luca Zambelli
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Michele Palazzo
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Massimiliano Salati
- Division of Oncology, Department of Oncology and Hematology, University Hospital of Modena, Modena, Italy; PhD Program Clinical and Experimental Medicine, University of Modena and Reggio Emilia, Modena, Italy
| | - Yu Aoki
- Department of Gastroenterology and Gastrointestinal Oncology, National Cancer Center Hospital East, Chiba, Japan
| | - Akihito Kawazoe
- Department of Gastroenterology and Gastrointestinal Oncology, National Cancer Center Hospital East, Chiba, Japan
| | - Darren Cowzer
- Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, USA
| | - Sara Lonardi
- Medical Oncology 3, Istituto Oncologico Veneto IOV-IRCCS, Padova, Italy
| | - Thierry André
- Sorbonne Université, INSERM, Unité Mixte de Recherche Scientifique 938 and SIRIC CURAMUS, Centre de Recherche Saint-Antoine, Equipe Instabilité des Microsatellites et Cancer, Equipe labellisée par la Ligue Nationale contre le Cancer, Paris, France
| | - Giovanni Randon
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
| | - Filippo Pietrantonio
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy.
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Jo Y, Puri S, Haaland B, Coletta AM, Chipman JJ, Embrey K, Kerrigan KC, Patel SB, Moynahan K, Gumbleton M, Akerley WL. Augmenting Prognostication: Utilizing Activity Trackers to Enhance Survival Prediction in Metastatic Non-Small Cell Lung Cancer. Clin Lung Cancer 2025; 26:29-38. [PMID: 39572323 DOI: 10.1016/j.cllc.2024.10.001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2024] [Revised: 09/20/2024] [Accepted: 10/03/2024] [Indexed: 01/06/2025]
Abstract
INTRODUCTION/BACKGROUND Prognostication by performance status (PS) assessment is a fundamental element of treatment decisions and clinical trial design in oncology, but it is limited by subjectivity and potential miscommunication between patient, physician, and family. Activity tracker offers the potential to collect a broad range of patient-generated data to supplement the assessment of PS. PATIENTS AND METHODS Patients with metastatic NSCLC (mNSCLC) participated in a single institute, prospective, observational feasibility study conducted at Huntsman Cancer Institute. Patients were given a Fitbit® activity tracker, which collects their steps taken, distance moved, heart rate, and activity intensity. At baseline, PS was assessed by physicians and patients, and demographics and clinical data were collected. We defined novel indices of health: Heart rate Activity zone Mismatch (HAM) and excessive Sedentary Heart Rate (eSHR). We used multivariable Cox proportional hazards models adjusted for age, sex, and treatment line to estimate and test the prognostic ability of clinical and fitness metrics on overall survival (OS). Each prognostic model was evaluated using Harrell's concordance index (C-index). RESULTS Fifty-five patients with mNSCLC were enrolled. The median OS was 10.4 months (95% CI: 7.2, 15.2). PS-physician (HR = 2.0; P < .001) and Fitbit metrics were associated with OS, including daily total steps (1,000-steps) (HR = 0.8; P = .004), HAM (HR = 2; P = .02), eSHR (HR = 0.3; P = .001). The prognostic model that includes PS-physician was associated with the best concordance (C-index = 0.75), followed by daily total distance (C-index = 0.74) and steps (C-index = 0.73) CONCLUSIONS: Tracker-based measures were prognostic of survival in mNSCLC and may be useful as a supplement or alternative to PS in practice and clinical trials.
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Affiliation(s)
- Yeonjung Jo
- Department of Population Health Sciences, Division of Biostatistics, University of Utah, UT, 84112; Cancer Biostatistics, Huntsman Cancer Institute, University of Utah, UT, 84112
| | - Sonam Puri
- The Department of Thoracic Oncology, Moffitt Cancer Center, Tampa, FL, 33612.
| | | | - Adriana M Coletta
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112; Department of Health and Kinesiology, University of Utah, Salt Lake City, UT 84112
| | - Jonathan J Chipman
- Department of Population Health Sciences, Division of Biostatistics, University of Utah, UT, 84112; Cancer Biostatistics, Huntsman Cancer Institute, University of Utah, UT, 84112
| | - Kelsey Embrey
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112
| | - Kathleen C Kerrigan
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112
| | - Shiven B Patel
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112
| | - Kelly Moynahan
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112
| | - Matthew Gumbleton
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112
| | - Wallace L Akerley
- The Division of Medical Oncology, Huntsman Cancer Institute, University of Utah, Salt Lake City, UT, 84112
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Valencia G, Roque K, Rioja P, Huamán JA, Colomo V, Sánchez J, Calle C, Mantilla R, Morante Z, Fuentes H, Vidaurre T, Neciosup S, De Mello RA, Gómez HL, Fernández-Díaz AB, Berrocal A, Castaneda C. Impact on Survival with Immunotherapy and Evaluation of Biomarkers in Peruvian Patients with Advanced Melanoma. Onco Targets Ther 2024; 17:871-886. [PMID: 39507408 PMCID: PMC11540283 DOI: 10.2147/ott.s483753] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/21/2024] [Accepted: 10/10/2024] [Indexed: 11/08/2024] Open
Abstract
Introduction Advanced malignant melanoma is a very aggressive disease, historically with poor prognosis before the new advances with immunotherapy and targeted therapies that have changed the standard of care, especially in cutaneous melanoma. Peru has aggressive features such as higher rates of acral lentiginous melanoma (ALM) subtype with historically shorter survival. Methods This study describes Peruvian patients with advanced melanoma treated with immunotherapy (nivolumab) in two oncological institutions (public and private), including the discussion of the impact on overall survival (OS) divided by subtype (with incidence in ALM histology) and potential biomarkers that could be related to prognosis. Results We found that immunotherapy is safe, and improves progression-free survival (PFS), OS and objective response rate (ORR) in our patients, with lower benefit in ALM histology. No prognostic blood inflammatory biomarkers were detected. Discussion There is very limited data of Peruvian patients with metastatic melanoma treated with immunotherapy, especially the outcomes in ALM histology. Our goal is to share an example of the impact of immunotherapy in a Latin American (LATAM) population considered as an unsatisfied group with an enormous need of novel treatments and biomarkers.
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Affiliation(s)
- Guillermo Valencia
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Grupo de Estudios Clínicos Oncológicos del Perú (GECOPERU), Lima, Peru
| | - Katia Roque
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Ninth of July University (UNINOVE), Sao Paulo, Brazil
| | - Patricia Rioja
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Grupo de Estudios Clínicos Oncológicos del Perú (GECOPERU), Lima, Peru
| | - José Andrés Huamán
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
| | | | - Jorge Sánchez
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
| | - Cindy Calle
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
| | - Raúl Mantilla
- Universidad Nacional Federico Villarreal, Lima, Peru
| | - Zaida Morante
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Grupo de Estudios Clínicos Oncológicos del Perú (GECOPERU), Lima, Peru
| | - Hugo Fuentes
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Grupo de Estudios Clínicos Oncológicos del Perú (GECOPERU), Lima, Peru
- Ninth of July University (UNINOVE), Sao Paulo, Brazil
- Universidad Nacional Federico Villarreal, Lima, Peru
- Universidad de Piura, Piura, Peru
| | - Tatiana Vidaurre
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
| | - Silvia Neciosup
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Grupo de Estudios Clínicos Oncológicos del Perú (GECOPERU), Lima, Peru
| | | | - Henry L Gómez
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Grupo de Estudios Clínicos Oncológicos del Perú (GECOPERU), Lima, Peru
- Universidad Peruana Cayetano Heredia, Lima, Peru
| | | | | | - Carlos Castaneda
- Medical Oncology Department, Instituto Nacional de Enfermedades Neoplásicas (INEN), Lima, Peru
- Oncosalud – AUNA, Lima, Peru
- Universidad Científica del Sur, Lima, Peru
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Yang Y, Wang Z, Xin D, Guan L, Yue B, Zhang Q, Wang F. Analysis of the treatment efficacy and prognostic factors of PD-1/PD-L1 inhibitors for advanced gastric or gastroesophageal junction cancer: a multicenter, retrospective clinical study. Front Immunol 2024; 15:1468342. [PMID: 39512347 PMCID: PMC11540680 DOI: 10.3389/fimmu.2024.1468342] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/21/2024] [Accepted: 10/08/2024] [Indexed: 11/15/2024] Open
Abstract
Introduction Immune checkpoint inhibitors (ICIs) have transformed advanced gastric cancer treatment, yet patient responses vary, highlighting the need for effective biomarkers. Common markers, such as programmed cell death ligand-1 (PD-L1), microsatellite instability/mismatch repair (MSI/MMR), tumor mutational burden, tumor-infiltrating lymphocytes, and Epstein-Barr virus, face sampling challenges and high costs. This study seeks practical, minimally invasive biomarkers to enhance patient selection and improve outcomes. Methods This multicenter retrospective study analyzed 617 patients with advanced gastric or gastroesophageal junction cancer treated with programmed cell death protein-1 (PD-1)/PD-L1 inhibitors from January 2019 to March 2023. Clinical data and peripheral blood marker data were collected before and after treatment. The primary endpoints were overall survival (OS) and progression-free survival (PFS); the secondary endpoints included the objective response rate (ORR) and disease control rate (DCR). Least absolute shrinkage and selection operator (LASSO)-Cox and LASSO logistic regression analyses identified independent factors for OS, PFS, and ORR. Predictive nomograms were validated using receiver operating characteristic (ROC) curves, areas under the curve (AUCs), C-indices, and calibration curves, with clinical utility assessed via decision curve analysis (DCA), net reclassification improvement (NRI), and integrated discrimination improvement (IDI). Results OS-related factors included treatment line, T stage, ascites, pretreatment indirect bilirubin (pre-IBIL), posttreatment CA125, CA199, CA724, and the PLR. PFS-related factors included treatment lines, T stage, metastatic sites, pre-IBIL, posttreatment globulin (GLOB), CA125, and CA199 changes. ORR-related factors included treatment line, T stage, N stage, liver metastasis, pretreatment red cell distribution width-to-platelet ratio (RPR), CA125, and CA724 changes. The nomograms showed strong predictive performance and clinical utility. Conclusions Early treatment, lower T stage, the absence of ascites, and lower pre-IBIL, post-CA125, CA199, CA724, and PLR correlate with better OS. Factors for improved PFS include early treatment, lower T stage, fewer metastatic sites, and lower pre-IBIL, post-GLOB, and post-CA125 levels. Nomogram models can help identify patients who may benefit from immunotherapy, providing valuable clinical guidance.
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Affiliation(s)
- Yuanyuan Yang
- Department of Medical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
| | - Zhe Wang
- Department of Oncology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
- Department of Clinical Medicine, The First Clinical Medical College, Zhengzhou University, Zhengzhou, China
| | - Dao Xin
- Department of Oncology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Lulu Guan
- Department of Oncology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
| | - Bingtong Yue
- Department of Clinical Medicine, The First Clinical Medical College, Zhengzhou University, Zhengzhou, China
| | - Qifan Zhang
- Department of Oncology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
- Department of Clinical Medicine, The First Clinical Medical College, Zhengzhou University, Zhengzhou, China
| | - Feng Wang
- Department of Oncology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
- Henan Key Laboratory of Chronic Disease Prevention and Therapy & Intelligent Health Management, Zhengzhou, China
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He L, Li J, Li X, Wang X, Yan Q. Inflammatory status predicts prognosis in patients with gastric cancer with early pyloric stenosis who underwent radical resection: A propensity score‑matching analysis. Oncol Lett 2024; 28:355. [PMID: 38881714 PMCID: PMC11176888 DOI: 10.3892/ol.2024.14488] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/08/2023] [Accepted: 04/26/2024] [Indexed: 06/18/2024] Open
Abstract
The inflammatory status of patients is closely related to their nutritional status, and the impact of inflammatory status on patients with pyloric stenosis remains unclear. The present study aimed to investigate the impact of inflammatory status on the prognosis of patients with gastric cancer with early pyloric stenosis who underwent radical resection. A retrospective analysis included 242 patients with gastric cancer who underwent radical resection at the Affiliated Hospital of Southwest Medical University between July 2016 and December 2020. All patients were diagnosed with early pyloric stenosis. Correlation analysis was used to assess variations among different factors, and survival analysis was conducted to evaluate differences in overall survival (OS). To identify independent prognostic indicators, both univariate and multivariate Cox regression analyses were performed, addressing potential multicollinearity using Lasso analysis. Propensity score matching (PSM) was employed to eliminate potential confounding factors. Additionally, a prognostic risk model and nomogram based on inflammatory indicators were developed to comprehensively explore their impact on prognosis. Initial survival analysis revealed significant associations between neutrophil-to-lymphocyte ratio (NLR; χ2=10.522, P<0.001), systemic immune-inflammation index (SII; χ2=6.733, P=0.025), systemic inflammation response index (SIRI; χ2=15.490, P<0.001) and OS of the patients, while there was no significant survival difference among patients with different platelet-to-lymphocyte ratio (PLR; χ2=2.561, P=0.050). SIRI not only had the highest area under the curve but was also found to be an independent prognostic indicator (hazard ratio=1.851, P=0.046) in the present study. Following PSM on SIRI, a total of 174 patients were included in the subsequent analysis. Time-receiver operating characteristic and survival curves for SIRI after PSM consistently demonstrated its robust prognostic predictive capability. Furthermore, the prognostic risk model based on SIRI and the nomogram incorporating SIRI both exhibited high prognostic value. Inflammatory status was significantly associated with the prognosis of patients with gastric cancer with early pyloric stenosis who underwent radical resection. The NLR, SII and SIRI could all predict patient outcomes. Moreover, SIRI exhibited the highest prognostic value among the inflammatory indices and has been identified as an independent prognostic factor in the present study.
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Affiliation(s)
- Lijuan He
- Health Management Center, The Affiliated Hospital, Southwest Medical University, Luzhou, Sichuan 646000, P.R. China
| | - Jie Li
- Department of Cardiology, Ordos Central Hospital, Baotou Medical College, Ordos, Inner Mongolia Autonomous Region 017000, P.R. China
| | - Xiaohong Li
- Health Management Center, The Affiliated Hospital, Southwest Medical University, Luzhou, Sichuan 646000, P.R. China
| | - Xin Wang
- Department of Gastrointestinal Surgery, The Affiliated Hospital, Southwest Medical University, Luzhou, Sichuan 646000, P.R. China
| | - Qiong Yan
- Department of Gastroenterology, The Affiliated Hospital, Southwest Medical University, Luzhou, Sichuan 646000, P.R. China
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10
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Hou S, Song D, Hao R, Li L, Zhang Y, Zhu J. Prognostic relevance of prognostic nutritional indices in gastric or gastro-esophageal junction cancer patients receiving immune checkpoint inhibitors: a systematic review and meta-analysis. Front Immunol 2024; 15:1382417. [PMID: 38966640 PMCID: PMC11222392 DOI: 10.3389/fimmu.2024.1382417] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/05/2024] [Accepted: 06/06/2024] [Indexed: 07/06/2024] Open
Abstract
Background The Prognostic Nutritional Index (PNI) has become an important predictive tool for assessing patients' nutritional status and immune competence. It is widely used in prognostic evaluations for various cancer patients. However, the prognostic relevance of the Prognostic Nutritional Index (PNI) in gastric or gastro-esophageal junction cancer patients (GC/GEJC) undergoing immune checkpoint inhibitors (ICIs) treatment remains unclear. This meta-analysis aimed to determine the prognostic impact of PNI in this specific patient cohort. Methods We conducted a thorough literature search, covering prominent databases such as PubMed, Embase, Web of Science, SpringerLink, and the Cochrane Library. The search spanned from the inception of these databases up to December 5, 2023. Employing the 95% confidence interval and Hazard Ratio (HR), the study systematically evaluated the relationship between PNI and key prognostic indicators, including the objective remission rate (ORR), disease control rate (DCR), overall survival (OS) and progression-free survival (PFS) in GC/GEJC patients undergoing ICI treatment. Results Eight studies comprising 813 eligible patients were selected. With 7 studies consistently demonstrating superior Overall Survival (OS) in the high-Prognostic Nutritional Index (PNI) group compared to their low-PNI counterparts (HR 0.58, 95% CI: 0.47-0.71, P<0.001). Furthermore, the results derived from 6 studies pointed out that the significant correlation between he low-PNI and poorer progression-free survival (PFS) (HR 0.58, 95% CI: 0.47-0.71, P<0.001). Subgroup analyses were performed to validate the robustness of the results. In addition, we conducted a meta-analysis of three studies examining the correlation between PNI and objective response rate/disease control rate (ORR/DCR) and found that the ORR/DCR was significantly superior in the high PNI group (ORR: RR: 1.24, P=0.002; DCR: RR: 1.43, P=0.008). Conclusion This meta-analysis indicates that the low-PNI in GC/GEJC patients undergoing ICI treatment is significantly linked to worse OS and PFS. Therefore, PNI can serve as a prognostic indicator of post-treatment outcomes in patients with GC receiving ICIs. Further prospective studies are required to assess the reliability of these findings. Systematic review registration https://inplasy.com/, identifier INPLASY202450133.
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Affiliation(s)
- Shufu Hou
- Department of General Surgery, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
- Key Laboratory of Metabolism and Gastrointestinal Tumor, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
| | - Dandan Song
- Department of Neurology, Shandong Province Third Hospital, Jinan, China
| | - Ruiqi Hao
- Department of General Surgery, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
- Key Laboratory of Metabolism and Gastrointestinal Tumor, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
| | - Linchuan Li
- Department of General Surgery, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
- Key Laboratory of Metabolism and Gastrointestinal Tumor, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
| | - Yun Zhang
- Department of General Surgery, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
- Key Laboratory of Metabolism and Gastrointestinal Tumor, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
| | - Jiankang Zhu
- Department of General Surgery, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
- Key Laboratory of Metabolism and Gastrointestinal Tumor, The First Affiliated Hospital of Shandong First Medical University, Jinan, China
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Wang C, Yang D. Effect of different preoperative nutritional treatments on postoperative recovery and clinical outcomes in patients with gastric cancer and early gastric outlet obstruction. Oncol Lett 2024; 27:214. [PMID: 38572061 PMCID: PMC10988191 DOI: 10.3892/ol.2024.14348] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/15/2023] [Accepted: 02/20/2024] [Indexed: 04/05/2024] Open
Abstract
Patients with gastric cancer and early gastric outlet obstruction often experience malnutrition and require various nutritional support strategies. This study aimed to evaluate the impact of different preoperative nutritional treatments on their postoperative recovery and prognosis. The present retrospective study collected data from 467 patients with gastric cancer and early gastric outlet obstruction who underwent surgery at Harbin Medical University Cancer Hospital (Harbin, China) between January 2016 and December 2018. All patients received preoperative nutritional treatment, with a mean treatment duration of 8.23±2.33 days. The present study analyzed associations and survival in different groups using χ2, independent-samples t-test, ANOVA and log-rank tests. Furthermore, single- and multi-factor survival analyses were conducted and nomograms and calibration curves constructed to investigate factors influencing patient survival. In this study, 230 patients (49.3%) received only parenteral nutrition (PN; Group 1), 162 patients (34.7%) received PN combined with enteral nutrition (EN; Group 2) and 75 patients (16.0%) received PN combined with a full- or semi-liquid diet (Group 3). No significant differences in clinical and pathological parameters were observed among the groups. However, Group 2 showed significant advantages in postoperative recovery, including faster time to first postoperative bowel sounds, flatus and bowel movement. Survival analysis indicated that Group 3 had shorter progression-free survival (χ2=30.485) and overall survival (χ2=31.249). Preoperative nutritional treatment was identified as an independent prognostic factor. Preoperative PN combined with EN proved advantageous for postoperative recovery of patients with gastric cancer and early gastric outlet obstruction. Furthermore, PN combined with full- or semi-liquid diets may not have fully met the nutritional needs of these patients, resulting in less favorable clinical outcomes.
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Affiliation(s)
- Caixia Wang
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
| | - Dameng Yang
- Department of Gastrointestinal Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
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12
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Pergialiotis V, Thomakos N, Papalios T, Lygizos V, Vlachos DE, Rodolakis A, Haidopoulos D. Prognostic Nutritional Index as a Predictive Biomarker of Post-Operative Infectious Morbidity in Gynecological Cancer Patients: A Prospective Cohort Study. Nutr Cancer 2024; 76:364-371. [PMID: 38369888 DOI: 10.1080/01635581.2024.2318827] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/24/2023] [Revised: 02/01/2024] [Accepted: 02/02/2024] [Indexed: 02/20/2024]
Abstract
Malnutrition significantly impacts the post-operative process of gynecological cancer patients. A prominent variable for determining perioperative morbidity is the Prognostic Nutritional Index (PNI). To investigate PNI's predictive value on the risk of post-operative infections, we conducted a prospective cohort study involving women who underwent surgery for gynecological malignancies. Out of the 208 patients enrolled, 28 (13.5%) were malnourished and post-operative infections occurred in 43 patients. Notably, there was a significant difference in PNI between patients who developed infections and those who did not (p = 0.027), as well as between malnourished patients and those with normal nutritional status (p = 0.043). Univariate analysis showed that preoperative PNI predicts the risk of post-operative infections better than post-operative white blood cell count (AUC of 0.562 vs 0.375). However, the most accurate diagnostic results in the multivariate analysis were obtained from random forest and classification tree models (AUC of 0.987 and 0.977, respectively). Essentially, PNI and post-operative white blood cell count provided the best information gain according to rank probabilities. In conclusion, PNI appears to be a critical parameter that merits further investigation during the preoperative evaluation of gynecological malignancies.
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Affiliation(s)
- Vasilios Pergialiotis
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
| | - Nikolaos Thomakos
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
| | - Theodoros Papalios
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
| | - Vasilios Lygizos
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
| | - Dimitrios Efthimios Vlachos
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
| | - Alexandros Rodolakis
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
| | - Dimitrios Haidopoulos
- First Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, "Alexandra" General Hospital, Athens, Greece
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13
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Niu Z, Yan B. Prognostic and clinicopathological effect of the prognostic nutritional index (PNI) in patients with cervical cancer: a meta-analysis. Ann Med 2023; 55:2288705. [PMID: 38039954 PMCID: PMC10836274 DOI: 10.1080/07853890.2023.2288705] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/11/2023] [Accepted: 11/22/2023] [Indexed: 12/03/2023] Open
Abstract
BACKGROUND Numerous studies have explored whether the prognostic nutritional index (PNI) can predict the prognosis of cervical cancer (CC); however, their findings remain controversial. This meta-analysis focused on evaluating the relationship between the PNI and the prognosis of patients with CC. METHODS Relevant articles were collected from specific databases up to March 16, 2023. The relationship between the PNI and survival outcomes in patients with CC was estimated using combined hazard ratios (HRs) and associated 95% confidence intervals (CIs). The association of the PNI with clinicopathological features in patients with CC was assessed by combining odds ratios (ORs) and associated 95% CIs. RESULTS Nine articles with 2508 cases were included in the meta-analysis. According to our pooled findings, a decreased PNI showed a significant association with worse overall survival (OS) (HR = 2.98, 95% CI = 2.22-3.99, p < .001) as well as progression-free survival (PFS) (HR = 2.43, 95% CI = 1.92-3.07, p < .001) in patients with CC. The subgroup analysis indicated that the results were reliable. Moreover, the decreased PNI showed a significant association with the presence of lymph node metastasis (LN metastasis, OR = 1.53, 95% CI = 1.04-82.24, p = .030) and maximum tumor size >4 cm (OR = 1.73, 95% CI = 1.21-2.46, p = .002). However, the PNI was not significantly associated with histology, differentiation, or FIGO stage. CONCLUSION In this study, a low PNI predicted dismal OS and PFS in patients with CC, who also tend to suffer from LN metastasis and larger tumor size. PNI is a promising biomarker for predicting the prognosis of patients with CC in clinical practice.
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Affiliation(s)
- Zheng Niu
- Department of Gynecology, Affiliated Hangzhou First People’s Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China
| | - Bing Yan
- Department of Pharmacy, The First Affiliated Hospital of Huzhou University, Huzhou, Zhejiang, China
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Zhang R, Zhao H, Wang P, Guo Z, Liu C, Qu Z. Hepatocellular carcinoma immune prognosis score predicts the clinical outcomes of hepatocellular carcinoma patients receiving immune checkpoint inhibitors. BMC Cancer 2023; 23:1181. [PMID: 38041022 PMCID: PMC10693152 DOI: 10.1186/s12885-023-11678-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/23/2023] [Accepted: 11/24/2023] [Indexed: 12/03/2023] Open
Abstract
OBJECTIVE The predictive biomarkers of immune checkpoint inhibitors (ICIs) in hepatocellular carcinoma (HCC) still need to be further explored. This study aims to establish a new immune prognosis biomarker to predict the clinical outcomes of hepatocellular carcinoma patients receiving immune checkpoint inhibitors. METHODS The subjects of this study were 151 HCC patients receiving ICIs at Harbin Medical University Cancer Hospital from January 2018 to December 2021. This study collected a wide range of blood parameters from patients before treatment and used Cox's regression analysis to identify independent prognostic factors in blood parameters, as well as their β coefficient. The hepatocellular carcinoma immune prognosis score (HCIPS) was established through Lasso regression analysis and COX multivariate analysis. The cut-off value of HCIPS was calculated from the receiver operating characteristic (ROC) curve. Finally, the prognostic value of HCIPS was validated through survival analysis, stratified analyses, and nomograms. RESULTS HCIPS was composed of albumin (ALB) and thrombin time (TT), with a cut-off value of 0.64. There were 56 patients with HCIPS < 0.64 and 95 patients with HCIPS ≥ 0.64, patients with low HCIPS were significantly related to shorter progression-free survival (PFS) (13.10 months vs. 1.63 months, P < 0.001) and overall survival (OS) (14.83 months vs. 25.43 months, P < 0.001). HCIPS has also been found to be an independent prognostic factor in this study. In addition, the stratified analysis found a significant correlation between low HCIPS and shorter OS in patients with tumor size ≥ 5 cm (P of interaction = 0.032). The C-index and 95% CI of the nomograms for PFS and OS were 0.730 (0.680-0.779) and 0.758 (0.711-0.804), respectively. CONCLUSIONS As a new score established based on HCC patients receiving ICIs, HCIPS was significantly correlated with clinical outcomes in patients with ICIs and might serve as a new biomarker to predict HCC patients who cloud benefit from ICIs.
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Affiliation(s)
- Rujia Zhang
- Department of Operating Room, The Second Affiliated Hospital of Harbin Medical University, Harbin Medical University, Harbin, 150086, Heilongjiang, China
| | - Haoran Zhao
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, 150081, Heilongjiang, China
| | - Peng Wang
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, 150081, Heilongjiang, China
| | - Zuoming Guo
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, 150081, Heilongjiang, China
| | - Chunxun Liu
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, 150081, Heilongjiang, China
| | - Zhaowei Qu
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, 150081, Heilongjiang, China.
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15
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Liu C, Zhao H, Wang P, Guo Z, Qu Z. The combination of circulating IgM and geriatric nutritional risk index predicts the prognostic of hepatocellular carcinoma patients who underwent immune checkpoint inhibitors. Int Immunopharmacol 2023; 123:110704. [PMID: 37506504 DOI: 10.1016/j.intimp.2023.110704] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2023] [Revised: 07/22/2023] [Accepted: 07/23/2023] [Indexed: 07/30/2023]
Abstract
OBJECTIVE Immune checkpoint inhibitors (ICIs) have shown promise in hepatocellular carcinoma (HCC) treatment. With the increasing use of ICIs in cancer treatment, identifying biomarkers that can predict the prognosis of patients receiving ICIs is of great importance. We aimed to investigate the potential of circulating immunoglobulins and the combination of Geriatric Nutritional Risk Index (GNRI) with IgM to predict prognosis in patients with HCC who received ICIs. METHODS Clinical and pathological data were collected from 101 patients with HCC who were administered ICIs and underwent circulating immunoglobulin testing between January 2018 and December 2021. Survival analysis, Cox regression analysis, and nomogram construction were performed to evaluate the prognostic value of the indicators. RESULTS In the preliminary survival analysis, we observed a significant correlation between patient prognosis and IgM levels. Patients with low IgM had shorter survival times. Upon combining the GNRI with IgM, patients with low GNRI and IgM levels had shorter progression-free survival (PFS) and overall survival (OS) (P < 0.001). Additionally, GNRI-IgM had the highest area under the curve (AUC) and was identified as an independent prognostic marker in this study. The C-indices of the nomograms for PFS and OS were 0.797 (0.734-0.860) and 0.827 (0.778-0.876), respectively. CONCLUSIONS IgM was significantly associated with the prognosis of patients with HCC receiving ICIs. The combination of the GNRI with IgM provided superior prognostic value and served as an independent prognostic marker. The GNRI-IgM can be used to effectively identify patients with HCC who are responsive to ICIs.
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Affiliation(s)
- Chunxun Liu
- Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, China
| | - Haoran Zhao
- Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, China
| | - Peng Wang
- Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, China
| | - Zuoming Guo
- Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, China
| | - Zhaowei Qu
- Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, China.
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Liu C, Zhao H, Zhang R, Guo Z, Wang P, Qu Z. Prognostic value of nutritional and inflammatory markers in patients with hepatocellular carcinoma who receive immune checkpoint inhibitors. Oncol Lett 2023; 26:437. [PMID: 37664652 PMCID: PMC10472048 DOI: 10.3892/ol.2023.14024] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/28/2023] [Accepted: 07/31/2023] [Indexed: 09/05/2023] Open
Abstract
The emergence of immune checkpoint inhibitors (ICIs) has provided a new treatment option for patients with hepatocellular carcinoma (HCC). However, further evaluation is needed for determining biomarkers for the use of ICIs. The present study evaluated the prognostic value of certain nutritional and inflammatory markers in patients with HCC who received ICIs. In the present study, the clinical data of 151 patients with HCC who received ICIs at Harbin Medical University Cancer Hospital from January 2019 to December 2021 were collected. The blood parameters of all patients before treatment were collected to evaluate certain nutritional and inflammatory markers, including the prognostic nutrition index (PNI), nutritional risk index (NRI), geriatric NRI (GNRI), systemic immune-inflammation index (SII), systemic inflammation response index (SIRI) and advanced lung cancer inflammation index (ALI). Patients were grouped using the cut-off value calculated using receiver operating characteristic (ROC) curves, and the relationship between these biomarkers and prognosis was evaluated through survival analysis. Furthermore, the prognostic value of these biomarkers was assessed through multivariate Cox regression analysis and construction of nomograms. Finally, time-ROC curves were plotted to compare the differences in predicting prognosis between the biomarkers. In the preliminary survival analysis, all inflammatory and nutritional markers included in the present study were significantly associated with the prognosis of HCC in patients who received ICIs. Similar results were obtained in a subgroup analysis of patients with different Barcelona Clinic Liver Cancer (BCLC) stages. Multivariate Cox regression analysis demonstrated that GNRI, PNI, BCLC stage and Tumor-Node-Metastasis (TNM) stage were significantly associated with progression-free survival (PFS), whereas GNRI, BCLC stage and TNM stage were also significantly associated with overall survival (OS). Furthermore, the time-ROC curves indicated that nutritional indicators had a higher prognostic value in all indexes, especially GNRI. The C-index (95% confidence interval) of the nomograms for predicting the survival probability of patients who received ICIs were 0.801 (0.746-0.877) and 0.823 (0.761-0.898) for PFS and overall OS, respectively, which also showed high accuracy. In conclusion, the present study demonstrated that PNI, GNRI, NRI, SII, SIRI and ALI were all related to the efficacy of ICIs in HCC and could serve as non-invasive biomarkers for ICI treatment effectiveness. Moreover, compared with inflammatory markers, nutritional markers had greater predictive ability, with GNRI being the biomarker with the best prognostic value.
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Affiliation(s)
- Chunxun Liu
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
| | - Haoran Zhao
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
| | - Rujia Zhang
- Department of Operating Room, The Second Affiliated Hospital of Harbin Medical University, Harbin Medical University, Harbin, Heilongjiang 150086, P.R. China
| | - Zuoming Guo
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
| | - Peng Wang
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
| | - Zhaowei Qu
- Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China
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17
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Zhang L, Ma W, Qiu Z, Kuang T, Wang K, Hu B, Wang W. Prognostic nutritional index as a prognostic biomarker for gastrointestinal cancer patients treated with immune checkpoint inhibitors. Front Immunol 2023; 14:1219929. [PMID: 37545502 PMCID: PMC10401046 DOI: 10.3389/fimmu.2023.1219929] [Citation(s) in RCA: 17] [Impact Index Per Article: 8.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/09/2023] [Accepted: 06/19/2023] [Indexed: 08/08/2023] Open
Abstract
Objective Our study represents the first meta-analysis conducted to evaluate the prognostic utility of the baseline prognostic nutritional index (PNI) in patients with gastrointestinal cancer (GIC) who received immune checkpoint inhibitor (ICI) therapy. Methods We searched PubMed, the Cochrane Library, EMBASE, and Google Scholar until April 23, 2023, to obtain relevant articles for this study. Our analysis examined several clinical outcomes, including overall survival (OS), progression-free survival (PFS), objective response rate (ORR), and disease control rate (DCR). Results In this analysis, a total of 17 articles with 2883 patients were included. Our pooled results indicated that patients with high PNI levels had longer OS (HR: 0.530, 95% CI: 0.456-0.616, p < 0.001) and PFS (HR: 0.740, 95% CI: 0.649-0.844, p < 0.001), as well as higher ORR (OR: 1.622, 95% CI: 1.251-2.103, p < 0.004) and DCR (OR: 1.846, 95% CI: 1.428-2.388, p < 0.001). Subgroup analysis showed that PNI cutoff values of 40 to 45 showed greater predictive potential. Subgroup analysis also confirmed that the above findings still hold true in patients with esophageal cancer, gastric cancer, and hepatocellular carcinomas. Conclusion The PNI were reliable predictors of outcomes in GIC patients treated with ICIs.
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Affiliation(s)
- Lilong Zhang
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
| | - Wangbin Ma
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
| | - Zhendong Qiu
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
| | - Tianrui Kuang
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
| | - Kunpeng Wang
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
| | - Baohong Hu
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
| | - Weixing Wang
- Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan, China
- Key Laboratory of Hubei Province for Digestive System Disease, Wuhan, China
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Du Z, Sun H, Zhao R, Deng G, Pan H, Zuo Y, Huang R, Xue Y, Song H. Combined with prognostic nutritional index and IgM for predicting the clinical outcomes of gastric cancer patients who received surgery. Front Oncol 2023; 13:1113428. [PMID: 37361569 PMCID: PMC10289403 DOI: 10.3389/fonc.2023.1113428] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/01/2022] [Accepted: 05/25/2023] [Indexed: 06/28/2023] Open
Abstract
Objective Although the survival rate of patients who undergo surgery for gastric cancer has greatly improved, still many patients have a poor prognosis. This retrospective study aimed to investigate the predictive ability of the PNI-IgM score, a combined prognostic nutritional index (PNI), and immunoglobulin M (IgM), on the prognosis of patients undergoing surgery for gastric cancer. Methods 340 patients with gastric cancer who underwent surgery from January 2016 to December 2017 were selected. The PNI-IgM score ranged from 1 to 3: score of 1, low PNI (< 48.45) and low IgM (< 0.87); score of 2, low PNI and high IgM, or high PNI and low IgM; score of 3, high PNI and high IgM. We compared the differences in disease-free survival (DFS) and overall survival (OS) among the three groups, while univariate and multivariate analyses calculated prognostic factors for DFS and OS. In addition, the nomograms were constructed based on the results of multivariate analysis to estimate the 1-, 3- and 5-year survival probability. Results There were 67 cases in the PNI-IgM score 1 group, 160 cases in the PNI-IgM score 2 group, and 113 cases in the PNI-IgM score 3 group. The median survival times of DFS in the PNI-IgM score group 1, the PNI-IgM score group 2, and the PNI-IgM score group 3 were 62.20 months, not reached, and not reached, and 67.57 months vs. not reached vs. not reached in three groups for OS. Patients in the PNI-IgM score group 1 had a lower DFS than the PNI-IgM score group 2 (HR = 0.648, 95% CI: 0.418-1.006, P = 0.053) and the PNI-IgM score group 3 (HR = 0.337, 95% CI: 0.194-0.585, P < 0.001). In stratified analysis, PNI-IgM score 1 had a worse prognosis in the age < 60 years group and CA724 < 2.11 U/m group. Conclusion PNI-IgM score is a novel combination of nutritional and immunological markers that can be used as a sensitive biological marker for patients with gastric cancer who undergo surgery. The lower the PNI-IgM score, the worse the prognosis.
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Sun H, Wang H, Pan H, Zuo Y, Zhao R, Huang R, Xue Y, Song H. CD19 (+) B Cell Combined with Prognostic Nutritional Index Predicts the Clinical Outcomes of Patients with Gastric Cancer Who Underwent Surgery. Cancers (Basel) 2023; 15:cancers15092531. [PMID: 37173997 PMCID: PMC10177131 DOI: 10.3390/cancers15092531] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2023] [Revised: 04/21/2023] [Accepted: 04/27/2023] [Indexed: 05/15/2023] Open
Abstract
(1) Background: The aim of this study was to explore the predictive ability of lymphocyte subsets for the prognosis of gastric cancer patients who underwent surgery and the prognostic value of CD19 (+) B cell combined with the Prognostic Nutritional Index (PNI). (2) Methods: This study involved 291 patients with gastric cancer who underwent surgery at our institution between January 2016 and December 2017. All patients had complete clinical data and peripheral lymphocyte subsets. Differences in clinical and pathological characteristics were examined using the Chi-square test or independent sample t-tests. The difference in survival was evaluated using Kaplan-Meier survival curves and the Log-rank test. Cox's regression analysis was performed to identify independent prognostic indicators, and nomograms were used to predict survival probabilities. (3) Results: Patients were categorized into three groups based on their CD19 (+) B cell and PNI levels, with 56 cases in group one, 190 cases in group two, and 45 cases in group three. Patients in group one had a shorter progression-free survival (PFS) (HR = 0.444, p < 0.001) and overall survival (OS) (HR = 0.435, p < 0.001). CD19 (+) B cell-PNI had the highest area under the curve (AUC) compared with other indicators, and it was also identified as an independent prognostic factor. Moreover, CD3 (+) T cell, CD3 (+) CD8 (+) T cell, and CD3 (+) CD16 (+) CD56 (+) NK T cell were all negatively correlated with the prognosis, while CD19 (+) B cell was positively associated with the prognosis. The C-index and 95% confidence interval (CI) of nomograms for PFS and OS were 0.772 (0.752-0.833) and 0.773 (0.752-0.835), respectively. (4) Conclusions: Lymphocyte subsets including CD3 (+) T cell, CD3 (+) CD8 (+) T cell, CD3 (+) CD16 (+) CD56 (+) NK T cell, and CD19 (+) B cell were related to the clinical outcomes of patients with gastric cancer who underwent surgery. Additionally, PNI combined with CD19 (+) B cell had higher prognostic value and could be used to identify patients with a high risk of metastasis and recurrence after surgery.
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Affiliation(s)
- Hao Sun
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Huibo Wang
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Hongming Pan
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Yanjiao Zuo
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Ruihu Zhao
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Rong Huang
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Yingwei Xue
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
| | - Hongjiang Song
- Harbin Medical University Cancer Hospital, Harbin Medical University, 150 Haping Road, Nangang District, Harbin 150081, China
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Lee DS, Kim CW, Kim HY, Ku YM, Won YD, Lee SL, Sun DS. Association between Posttreatment Serum Platelet-to-Lymphocyte Ratio and Distant Metastases in Patients with Hepatocellular Carcinoma Receiving Curative Radiation Therapy. Cancers (Basel) 2023; 15:cancers15071978. [PMID: 37046639 PMCID: PMC10092989 DOI: 10.3390/cancers15071978] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/23/2023] [Revised: 03/07/2023] [Accepted: 03/23/2023] [Indexed: 03/29/2023] Open
Abstract
Background: We sought to investigate whether serum immune and inflammatory parameters can help to predict distant metastasis (DM) in patients with unresectable hepatocellular carcinoma (HCC) undergoing curative radiation therapy (RT). Methods: A total of 76 RT courses were analyzed. The following variables were included in the analysis: systemic inflammation index, neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio (PLR), prognostic nutritional index (PNI), absolute lymphocyte count, lymphocyte-to-monocyte ratio, albumin, albumin-to-alkaline phosphatase ratio, RT-related parameters, and levels of total protein, hemoglobin, α-fetoprotein, and PIVKA-II. Distant control (DC) and overall survival (OS) rates were calculated and compared. Results: The mean age was 61.4 years, and most patients were men (n = 62, 81.6%). The median RT fraction number and fractional doses were 12 (range, 4–30) and 5 (range, 2–12) Gy, respectively. With a median follow-up of 12 (range, 3.1–56.7) months, the 1-year DC and OS rates were 64.4% and 55.2%, respectively. The development of DM significantly deteriorated OS (p = 0.013). In the multivariate analysis, significant independent prognostic indicators for DC and OS rates were the highest posttreatment PLR (≤235.7 vs. >235.7, p = 0.006) and the lowest posttreatment PNI (≤25.4 vs. >25.4, p < 0.001), respectively. Conclusions: Posttreatment serum PLR might be helpfully used as a predictive biomarker of DM in unresectable HCC patients undergoing RT. Future research is necessary to confirm our findings.
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Affiliation(s)
- Dong Soo Lee
- Department of Radiation Oncology, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea
- Correspondence:
| | - Chang Wook Kim
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea; (C.W.K.); (H.Y.K.)
| | - Hee Yeon Kim
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea; (C.W.K.); (H.Y.K.)
| | - Young-Mi Ku
- Department of Radiology, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea; (Y.-M.K.); (Y.D.W.); (S.-L.L.)
| | - Yoo Dong Won
- Department of Radiology, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea; (Y.-M.K.); (Y.D.W.); (S.-L.L.)
| | - Su-Lim Lee
- Department of Radiology, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea; (Y.-M.K.); (Y.D.W.); (S.-L.L.)
| | - Der Sheng Sun
- Division of Oncology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul 06591, Republic of Korea;
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