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Chen J, Huang X, Wei Q, Liu S, Song W, Liu M. The relationship between systemic therapies and low skeletal muscle mass in patients with intermediate and advanced hepatocellular carcinoma. Front Immunol 2025; 16:1557839. [PMID: 40109345 PMCID: PMC11919905 DOI: 10.3389/fimmu.2025.1557839] [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: 01/09/2025] [Accepted: 02/17/2025] [Indexed: 03/22/2025] Open
Abstract
Background Low skeletal muscle mass (LSMM) has been associated with poor prognosis in hepatocellular carcinoma (HCC) patients receiving systemic therapy. However, its impact across different treatment regimens remains unclear. Methods A retrospective study analyzed 714 patients with intermediate and advanced HCC, divided into immunotherapy (I, n=85), target-immunotherapy combination (I+T, n=545), and targeted therapy (T, n=84) groups based on treatment. Skeletal muscle was assessed via computed tomography (CT) at the third lumbar vertebral level (L3) before and after 3 months of treatment. LSMM was evaluated by the third lumbar skeletal muscle index (L3-SMI) using a predefined threshold. Patients were stratified by baseline values and treatment changes. Kaplan-Meier and Cox models were used to compare overall survival (OS) and progression-free survival (PFS). Results There was no significant difference in the loss of muscle mass among the three groups of LSMM patients; whereas, non-LSMM(NLSMM) patients in group T lost more muscle mass than those in group I (P=0.040).In the I+T group, patients who achieved an objective response (ORR) had less muscle mass loss than those without (P=0.013), while the changes in muscle mass for patients in the I group and T group were unrelated to treatment response. Baseline or post-treatment LSMM was associated with poorer median OS, especially in the I+T group. Progressive LSMM was linked to shorter median PFS (4.9 vs 5.7 months) and OS (9.8 vs 16.5 months), with similar results in the I+T group (mPFS, 4.2 vs. 5.8 months; mOS, 9.7 vs 16.1 months). Patients with LSMM had a higher incidence of treatment-related SAEs, particularly ascites and fatigue. Conclusion In patients with combined LSMM in hepatocellular carcinoma, muscle loss did not significantly differ between those treated with I, I+T, and T; however, T treatment contributed to muscle mass loss in NLSMM patients. Greater muscle loss correlated with poorer treatment outcomes and increased SAEs, and baseline, post-treatment, and progressive LSMM were linked to significantly worse prognoses, particularly with combined treatment regimens.
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Affiliation(s)
- Jingjing Chen
- Department of Oncology, Beijing You'an Hospital, Capital Medical University, Beijing, China
| | - Xueying Huang
- Department of Oncology, Beijing You'an Hospital, Capital Medical University, Beijing, China
| | - Qiaoxin Wei
- Department of Oncology, Beijing You'an Hospital, Capital Medical University, Beijing, China
| | - Songtao Liu
- Department of Oncology, Beijing You'an Hospital, Capital Medical University, Beijing, China
| | - Wenyan Song
- Department of Imaging, Beijing You'an Hospital, Capital Medical University, Beijing, China
| | - Mei Liu
- Department of Oncology, Beijing You'an Hospital, Capital Medical University, Beijing, China
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Ricci F, Benelli L, Pasqualetto M, Laudazi M, Pugliese L, Volpe M, Cerimele C, Di Donna C, Garaci F, Chiocchi M. Beyond the Obesity Paradox: Analysis of New Prognostic Factors in Transcatheter Aortic Valve Implantation Procedure. J Cardiovasc Dev Dis 2024; 11:368. [PMID: 39590211 PMCID: PMC11594374 DOI: 10.3390/jcdd11110368] [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: 09/11/2024] [Revised: 11/10/2024] [Accepted: 11/12/2024] [Indexed: 11/28/2024] Open
Abstract
SCOPE The main purpose of our study was to collect computed tomography (CT) measurements of fat parameters that are significantly related to body mass index (BMI) and evaluate the associations of these measurements and sarcopenia with early and long-term complications after transcatheter aortic valve implantation (TAVI) in order to investigate the existence of the so-called 'obesity paradox' and the role of sarcopenia in this phenomenon. MATERIALS AND METHODS We analyzed the significance of fat CT measurements in 85 patients undergoing the TAVI procedure and compared these with each other, as well as with quantified CT BMI and fat density measurements. Secondly, we evaluated the associations of BMI, CT measurements of fat, and CT evaluations of skeletal muscle mass with early and long-term complications after 24 months of post-TAVI follow-up. RESULTS We found positive and significant relationships between fat CT measurements with each other and with BMI and a negative and significant relation between fat density and fat quantity. By comparing the CT measurements of fat and skeletal muscle mass with early and long-term complications after TAVI, we confirmed the existence of the 'obesity paradox' and the poor effect of sarcopenia after the TAVI procedure. CONCLUSIONS We confirm that overweight and obesity are good prognostic factors, and sarcopenia is a poor prognostic factor for outcomes following the TAVI procedure. We focused on the scientific validation of an easy and fast way to measure fat and skeletal muscle mass using CT to better predict the outcomes of patients undergoing TAVI.
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Affiliation(s)
| | - Leonardo Benelli
- Department of Biomedicine and Prevention Division of Diagnostic Imaging, University of Rome “Tor Vergata”, Viale Oxford 81, 00133 Rome, Italy; (F.R.); (M.P.); (M.L.); (L.P.); (M.V.); (C.C.); (C.D.D.); (F.G.); (M.C.)
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Li Z, Zhao Y, Xie Y, Zhang L, Sun Y, Yang K, Duan S, Yu X, Shen Z, Jiang W. Impact of CT-relevant skeletal muscle parameters on post-liver transplantation survival in patients with hepatocellular carcinoma. Hepatol Int 2024; 18:1516-1527. [PMID: 39003652 DOI: 10.1007/s12072-024-10708-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/22/2024] [Accepted: 06/14/2024] [Indexed: 07/15/2024]
Abstract
BACKGROUND The specific CT-related skeletal muscle parameters predictive of postoperative survival in liver transplant (LT) patients with hepatocellular carcinoma (HCC) remain unclear. There is increasing evidence supporting the role of fatty acids and their lipid intermediates in regulating skeletal muscle mass and function, the relationship between lipoprotein subfractions and body composition remains unclear. METHODS Adult patients with HCC who underwent LT between January 2015 and September 2022 were retrospectively analyzed. CT parameters, including skeletal muscle index (SMI), psoas muscle index (PMI), skeletal muscle density (SMD), visceral and subcutaneous adipose tissue (VAT and SAT), and the VAT/SAT ratio at the L3 level, and lipid profiles, were assessed prior to LT. RESULTS Of the 284 LT patients with HCC, 224 underwent CT (L3 level) within 3 months of LT, and 82 (37%) were diagnosed with myosteatosis. Patients with myosteatosis exhibited significantly lower 1- and 3-year survival rates (p = 0.002, p = 0.01), a trend persisting even beyond the Milan criteria (p = 0.004, p = 0.04). After adjusting for covariates, SMD demonstrated a significant negative correlation with post-transplant survival (HR: 0.90, [95% Confidence Interval(CI): 0.83-0.98], C-statistic: 0.78, p = 0.009). Pearson's correlation analysis revealed a positive correlation between high-density lipoprotein cholesterol (HDL-C) and apolipoprotein A1(ApoA1) levels and SMD. Multivariate stepwise regression analysis demonstrated that every 10 Hounsfield unit decrease in SMD was associated with a 0.16 mmol/L decrease in HDL-C and a 0.18 g/L decrease in ApoA1. CONCLUSION Routine abdominal CT scans for assessing skeletal muscle density before LT were significantly associated with post-transplant mortality. Furthermore, abnormal HDL-C and ApoA1 levels before LT were associated with myosteatosis.
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Affiliation(s)
- Zhaoxian Li
- School of Medicine, Nankai University, Tianjin, China
- Department of Liver Transplantation, Tianjin First Central Hospital, Nankai District, No. 24 Fukang Road, Tianjin, China
| | - Yumeng Zhao
- School of Medicine, Nankai University, Tianjin, China
| | - Yan Xie
- Department of Liver Transplantation, Tianjin First Central Hospital, Nankai District, No. 24 Fukang Road, Tianjin, China
- Laboratory of Molecular and Treatment of Liver Cancer, Tianjin First Central Hospital, Tianjin, China
| | - Li Zhang
- Department of Liver Transplantation, Tianjin First Central Hospital, Nankai District, No. 24 Fukang Road, Tianjin, China
- Laboratory of Molecular and Treatment of Liver Cancer, Tianjin First Central Hospital, Tianjin, China
| | - Yanyan Sun
- Department of Liver Transplantation, Tianjin First Central Hospital, Nankai District, No. 24 Fukang Road, Tianjin, China
| | - Kai Yang
- First Central Clinical School, Tianjin Medical University, Tianjin, China
| | - Shaoxian Duan
- First Central Clinical School, Tianjin Medical University, Tianjin, China
| | - Xinghui Yu
- School of Medicine, Nankai University, Tianjin, China
| | - Zhongyang Shen
- School of Medicine, Nankai University, Tianjin, China.
- Department of Liver Transplantation, Tianjin First Central Hospital, Nankai District, No. 24 Fukang Road, Tianjin, China.
- Laboratory of Molecular and Treatment of Liver Cancer, Tianjin First Central Hospital, Tianjin, China.
| | - Wentao Jiang
- School of Medicine, Nankai University, Tianjin, China.
- Department of Liver Transplantation, Tianjin First Central Hospital, Nankai District, No. 24 Fukang Road, Tianjin, China.
- Laboratory of Molecular and Treatment of Liver Cancer, Tianjin First Central Hospital, Tianjin, China.
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Reichelt S, Merle U, Klauss M, Kahlert C, Lurje G, Mehrabi A, Czigany Z. Shining a spotlight on sarcopenia and myosteatosis in liver disease and liver transplantation: Potentially modifiable risk factors with major clinical impact. Liver Int 2024; 44:1483-1512. [PMID: 38554051 DOI: 10.1111/liv.15917] [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: 11/10/2023] [Revised: 03/07/2024] [Accepted: 03/17/2024] [Indexed: 04/01/2024]
Abstract
Muscle-wasting and disease-related malnutrition are highly prevalent in patients with chronic liver diseases (CLD) as well as in liver transplant (LT) candidates. Alterations of body composition (BC) such as sarcopenia, myosteatosis and sarcopenic obesity and associated clinical frailty were tied to inferior clinical outcomes including hospital admissions, length of stay, complications, mortality and healthcare costs in various patient cohorts and clinical scenarios. In contrast to other inherent detrimental individual characteristics often observed in these complex patients, such as comorbidities or genetic risk, alterations of the skeletal muscle and malnutrition are considered as potentially modifiable risk factors with a major clinical impact. Even so, there is only limited high-level evidence to show how these pathologies should be addressed in the clinical setting. This review discusses the current state-of-the-art on the role of BC assessment in clinical outcomes in the setting of CLD and LT focusing mainly on sarcopenia and myosteatosis. We focus on the disease-related pathophysiology of BC alterations. Based on these, we address potential therapeutic interventions including nutritional regimens, physical activity, hormone and targeted therapies. In addition to summarizing existing knowledge, this review highlights novel trends, and future perspectives and identifies persisting challenges in addressing BC pathologies in a holistic way, aiming to improve outcomes and quality of life of patients with CLD awaiting or undergoing LT.
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Affiliation(s)
- Sophie Reichelt
- Department of General, Visceral, Thoracic and Vascular Surgery, University Hospital of Bonn, Bonn, Germany
| | - Uta Merle
- Department of Gastroenterology and Hepatology, University Hospital Heidelberg, Heidelberg, Germany
| | - Miriam Klauss
- Department of Radiology, University Hospital Heidelberg, Heidelberg, Germany
| | - Christoph Kahlert
- Department of General, Visceral and Transplantation Surgery, University Hospital Heidelberg, Heidelberg, Germany
| | - Georg Lurje
- Department of General, Visceral and Transplantation Surgery, University Hospital Heidelberg, Heidelberg, Germany
- Department of Surgery, Campus Charité Mitte | Campus Virchow-Klinikum, Charité - Universitätsmedizin Berlin, Berlin, Germany
| | - Arianeb Mehrabi
- Department of General, Visceral and Transplantation Surgery, University Hospital Heidelberg, Heidelberg, Germany
| | - Zoltan Czigany
- Department of General, Visceral and Transplantation Surgery, University Hospital Heidelberg, Heidelberg, Germany
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Sun W, Yin X, Liu X, Wei J, Yu M, Li W, Ding X, Chen J. The clinical significance of sarcopenia in patients with hepatocellular carcinoma treated with lenvatinib and PD-1 inhibitors. Front Immunol 2024; 15:1380477. [PMID: 38698848 PMCID: PMC11063286 DOI: 10.3389/fimmu.2024.1380477] [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: 02/01/2024] [Accepted: 04/08/2024] [Indexed: 05/05/2024] Open
Abstract
Background and aim Sarcopenia has gained considerable attention in the context of hepatocellular carcinoma, as it has been correlated with a poorer prognosis among patients undergoing sorafenib or lenvatinib treatment for hepatocellular carcinoma (HCC). The clinical significance of sarcopenia in first-line advanced HCC patients treated with lenvatinib and programmed death-1 (PD-1) inhibitors needs to be clarified. Methods Sarcopenia was diagnosed using CT (Computed tomography) or MRI (Magnetic Resonance Imaging), with the psoas muscle index (PMI) as the surrogate marker. Patients were grouped based on sarcopenia presences, and a comparative analysis examined characteristics, adverse events, and prognosis. The Cox regression analysis was applied to identify independent prognostic factors for survival, while nomograms were constructed to predict 1-year survival. Results Among 180 patients, 46 had sarcopenia. Patients with baseline sarcopenia demonstrated significantly inferior median progression-free survival (mPFS) (3.0 vs. 8.3 months) and median overall survival (mOS) (7.3 vs. 21.6 months). The same results for mPFS (3.3 vs. 9.2 months) and mOS (9.4 vs. 24.2 months) were observed in patients who developed sarcopenia after treatment. Furthermore, significantly higher grade 3 or higher adverse events (AEs) (73.91% vs 41.79%, p<0.001) were recorded in the sarcopenia group compared to the non-sarcopenia group. In the multivariate analysis, distant metastasis, elevated PLR and CRP levels, and low PMI remained independent predictive factors for poor OS. Additionally, skeletal muscle loss remained a significant independent risk factor for PFS. We developed a nomogram incorporating these four indicators, which predicted 12-month survival with a C-index of 0.853 (95% CI, 0.791 - 0.915), aligning well with actual observations. Conclusion The prognosis of patients with HCC and sarcopenia is significantly worse when treated with lenvatinib and PD-1 inhibitors. The combination regimen of lenvatinib plus PD-1 inhibitors should be cautiously recommended due to the inferior prognosis and higher AEs.
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Affiliation(s)
| | | | | | | | | | | | - Xiaoyan Ding
- Department of Cancer Center, Beijing Ditan Hospital, Capital Medical University, Beijing, China
| | - Jinglong Chen
- Department of Cancer Center, Beijing Ditan Hospital, Capital Medical University, Beijing, China
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Wu MY, Yeh CH, Liao CC, Chen CL, Wang CC, Lin CC, Chang WC, Cheng YF, Ou HY. Sarcopenia Affects Liver Regeneration and Long-Term Survival Rate After Living-Donor Liver Transplantation in Patients With Hepatocellular Carcinoma. Transplant Proc 2024; 56:573-580. [PMID: 38326205 DOI: 10.1016/j.transproceed.2023.12.008] [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: 08/14/2023] [Revised: 12/12/2023] [Accepted: 12/28/2023] [Indexed: 02/09/2024]
Abstract
PURPOSE Despite technological and immunologic innovations, some living-donor liver transplant (LDLT) recipients still face poor liver regeneration. Sarcopenia is often recognized as a biomarker for poor outcomes in surgical patients. This study aimed to evaluate associations between sarcopenia and liver regeneration in LDLT recipients. MATERIALS AND METHODS This retrospective review included consecutive patients who had received LDLT at Chang Gung Memorial Hospital between 2005 and 2017. Sarcopenia was assessed using the psoas muscle index (PMI) in cross-sectional images. Receiver operating characteristic curve analysis was used to determine the ability of PMI to predict relatively poor survival rates. Correlations between liver regeneration and sarcopenia were evaluated using regression analysis. RESULTS A total of 109 LDLT recipients were included. The 1-, 3-, 5, 10-, and 15-year survival rates were 93.7%, 84.8%, 79.7%, 74.7%, and 73.3% in males and 93.3%, 83.3%, 83.3%, 71.4%, and 71.4% in females. PMIs were significantly different based on 10- and 15-year overall survival rates (P = .001 and P = .000) in male patients. Receiver operating characteristic curve analysis revealed the PMI cutoff point at 6.7 cm2/m2 (sensitivity = 48.3%, specificity = 81%, AUC (area under the ROC curve) = 0.685) based on 10-year survival. Linear regression analysis revealed that PMI was significantly associated with liver regeneration in males (P = .013). CONCLUSIONS Sarcopenia and low PMI are associated with poor liver regeneration and long-term survival after LDLT in male patients. Further studies, including sarcopenia with conventional scores, may help to more reliably predict liver regeneration and mortality among LDLT patients with hepatocellular carcinoma.
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Affiliation(s)
- Mei-Yun Wu
- College of Nursing, Kaohsiung Medical University, Kaohsiung, Taiwan; Department of Nursing, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Cheng-Hsi Yeh
- Department of Surgery, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chien-Chang Liao
- Department of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan; Department of Diagnostic Radiology, Kaohsiung Municipal Feng Shan Hospital - Under the management of Chang Gung Medical Foundation, Kaohsiung, Taiwan
| | - Chao-Long Chen
- Department of Surgery, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chih-Chi Wang
- Department of Surgery, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chih-Che Lin
- Department of Surgery, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Wan-Ching Chang
- Department of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Yu-Fan Cheng
- Department of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Hsin-You Ou
- Department of Diagnostic Radiology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, Taiwan.
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Li Y, Chen J, Tang Y, Lin T, Song T. Effect of pretransplant sarcopenia on patient and graft outcomes in solid organ transplant recipients: A systematic review and meta-analysis. Asian J Surg 2024; 47:1723-1733. [PMID: 38169165 DOI: 10.1016/j.asjsur.2023.12.118] [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: 09/14/2023] [Revised: 11/10/2023] [Accepted: 12/15/2023] [Indexed: 01/05/2024] Open
Abstract
The relationship between sarcopenia and prognosis in solid organ transplantation recipients (SOTr) remains unverified. We aimed to quantify the prevalence of pretransplant sarcopenia and its effect on patient and graft survival in SOTr. We used PubMed, EMBASE, Cochrane Library and Web of Science to search relevant studies published in English (from inception to December 31, 2021). Prospective and retrospective cohort studies that reported the prevalence of sarcopenia before transplant or the association between sarcopenia and clinical outcomes in SOTr were included. Primary outcomes were the prevalence of sarcopenia and its impact on patient and graft survival. Secondary outcomes included perioperative complications, acute rejection, length of hospital stay, length of intensive care unit stay (ICU LOS) and early readmission. Thirty-nine studies involving 5792 patients were included. Pooled prevalence of sarcopenia amongst SOTr candidates was 40 % (95 % confidence interval [CI]: 34%-47 % and I2 = 97 %). Sarcopenia was associated with increased risk of death (hazard ratio [HR] = 1.87, 95 % CI: 1.46-2.41 and I2 = 60 %), poor graft survival (HR = 1.71, 95 % CI: 1.16-2.54 and I2 = 57 %) and increased liver graft loss (HR = 1.43, 95 % CI: 1.03-1.99 and I2 = 38 %). Patients with sarcopenia demonstrated increased incidence of perioperative complications (risk ratio [RR] = 1.34, 95 % CI: 1.17-1.53 and I2 = 40 %), long ICU LOS (mean difference = 2.31 days, 95 % CI: 0.58-4.04 and I2 = 97 %) and decreased risk of acute rejection (RR = 0.61, 95 % CI: 0.42-0.89 and I2 = 0 %). In Conclusion, sarcopenia is prevalent in SOTr candidates and associated with death and graft loss. Identifying sarcopenia before transplantation and intervening may improve long-term outcomes.
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Affiliation(s)
- Yue Li
- Department of Urology, West China Hospital, Sichuan University, Chengdu, 61004, China; Transplant Center, West China Hospital, Sichuan University, Chengdu, 61004, China
| | - Jie Chen
- Department of Radiology, West China Hospital, Sichuan University, Chengdu, 61004, China
| | - Yangming Tang
- Department of Urology, West China Hospital, Sichuan University, Chengdu, 61004, China; Transplant Center, West China Hospital, Sichuan University, Chengdu, 61004, China
| | - Tao Lin
- Department of Urology, West China Hospital, Sichuan University, Chengdu, 61004, China; Transplant Center, West China Hospital, Sichuan University, Chengdu, 61004, China
| | - Turun Song
- Department of Urology, West China Hospital, Sichuan University, Chengdu, 61004, China; Transplant Center, West China Hospital, Sichuan University, Chengdu, 61004, China.
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Peng H, Lei SY, Fan W, Dai Y, Zhang Y, Chen G, Xiong TT, Liu TZ, Huang Y, Wang XF, Xu JH, Luo XH. Assessing recent recurrence after hepatectomy for hepatitis B-related hepatocellular carcinoma by a predictive model based on sarcopenia. World J Gastroenterol 2024; 30:1727-1738. [PMID: 38617742 PMCID: PMC11008376 DOI: 10.3748/wjg.v30.i12.1727] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/27/2023] [Revised: 01/30/2024] [Accepted: 03/13/2024] [Indexed: 03/28/2024] Open
Abstract
BACKGROUND Sarcopenia may be associated with hepatocellular carcinoma (HCC) following hepatectomy. But traditional single clinical variables are still insufficient to predict recurrence. We still lack effective prediction models for recent recurrence (time to recurrence < 2 years) after hepatectomy for HCC. AIM To establish an interventable prediction model to estimate recurrence-free survival (RFS) after hepatectomy for HCC based on sarcopenia. METHODS We retrospectively analyzed 283 hepatitis B-related HCC patients who underwent curative hepatectomy for the first time, and the skeletal muscle index at the third lumbar spine was measured by preoperative computed tomography. 94 of these patients were enrolled for external validation. Cox multivariate analysis was per-formed to identify the risk factors of postoperative recurrence in training cohort. A nomogram model was developed to predict the RFS of HCC patients, and its predictive performance was validated. The predictive efficacy of this model was evaluated using the receiver operating characteristic curve. RESULTS Multivariate analysis showed that sarcopenia [Hazard ratio(HR) = 1.767, 95%CI: 1.166-2.678, P < 0.05], alpha-fetoprotein ≥ 40 ng/mL (HR = 1.984, 95%CI: 1.307-3.011, P < 0.05), the maximum diameter of tumor > 5 cm (HR = 2.222, 95%CI: 1.285-3.842, P < 0.05), and hepatitis B virus DNA level ≥ 2000 IU/mL (HR = 2.1, 95%CI: 1.407-3.135, P < 0.05) were independent risk factors associated with postoperative recurrence of HCC. Based on the sarcopenia to assess the RFS model of hepatectomy with hepatitis B-related liver cancer disease (SAMD) was established combined with other the above risk factors. The area under the curve of the SAMD model was 0.782 (95%CI: 0.705-0.858) in the training cohort (sensitivity 81%, specificity 63%) and 0.773 (95%CI: 0.707-0.838) in the validation cohort. Besides, a SAMD score ≥ 110 was better to distinguish the high-risk group of postoperative recurrence of HCC. CONCLUSION Sarcopenia is associated with recent recurrence after hepatectomy for hepatitis B-related HCC. A nutritional status-based prediction model is first established for postoperative recurrence of hepatitis B-related HCC, which is superior to other models and contributes to prognosis prediction.
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Affiliation(s)
- Hong Peng
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Si-Yi Lei
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Wei Fan
- Department of Hepatobiliary Surgery, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Yu Dai
- Department of Hepatobiliary Surgery, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Yi Zhang
- Department of Hepatobiliary Surgery, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Gen Chen
- Department of Hepatobiliary Surgery, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Ting-Ting Xiong
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Tian-Zhao Liu
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Yue Huang
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Xiao-Feng Wang
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Jin-Hui Xu
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
| | - Xin-Hua Luo
- Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang 550002, Guizhou Province, China
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Jiang MJ, Wu MC, Duan ZH, Wu J, Xu XT, Li J, Meng QH. Prevalence and clinical impact of sarcopenia in liver transplant recipients: A meta-analysis. World J Gastroenterol 2024; 30:956-968. [PMID: 38516245 PMCID: PMC10950632 DOI: 10.3748/wjg.v30.i8.956] [Citation(s) in RCA: 3] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/16/2023] [Revised: 01/03/2024] [Accepted: 02/01/2024] [Indexed: 02/26/2024] Open
Abstract
BACKGROUND The prevalence of sarcopenia in patients undergoing liver transplantation (LT) remains to be determined partly because of different diagnostic criteria. Sarcopenia has recently been recognized as a new prognostic factor for predicting outcomes in LT candidates. AIM To estimate the prevalence of sarcopenia and evaluate its clinical effect on LT candidates. METHODS This systematic search was conducted in PubMed, Web of Science, Embase, and Cochrane Library for original English-language articles that investigated the prevalence and influence of sarcopenia in patients undergoing LT from database inception to November 30, 2022. Cohort studies of the definition of sarcopenia that estimate sarcopenia prevalence and evaluate its effect on clinical outcomes and the risk of mortality were included. RESULTS Twenty-five studies involving 7760 patients undergoing LT were included. The pooled prevalence of sarcopenia in patients undergoing LT was 40.7% [95% confidence intervals (95%CI): 32.1-49.6]. The 1-, 3-, and 5-year cumulative probabilities of post-LT survival in patients with preoperative sarcopenia were all lower than those without sarcopenia (P < 0.05). Sarcopenia was associated with an increased risk of post-LT mortality in patients undergoing LT (adjusted hazard ratio: 1.58; 95%CI: 1.21-2.07). Patients with preoperative sarcopenia had a longer intensive care unit stay, a high risk ratio of sepsis, and serious post-LT complications than those without sarcopenia. CONCLUSION Sarcopenia is prevalent in a substantial proportion of patients undergoing LT and is strongly and independently associated with higher a risk of mortality risk.
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Affiliation(s)
- Min-Jie Jiang
- Department of Hepatology, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
| | - Mu-Chen Wu
- Department of Hepatology, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
| | - Zhong-Hui Duan
- Department of Emergency, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
| | - Jing Wu
- Department of Hepatology, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
| | - Xiao-Tong Xu
- Department of Hepatology, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
| | - Juan Li
- Department of Hepatology, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
| | - Qing-Hua Meng
- Department of Hepatology, Beijing You-An Hospital, Capital Medical University, Beijing 100069, China
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10
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Liu J, Luo H, Huang L, Wang J. Prevalence of sarcopenia among patients with hepatocellular carcinoma: A systematic review and meta‑analysis. Oncol Lett 2023; 26:283. [PMID: 37274463 PMCID: PMC10236145 DOI: 10.3892/ol.2023.13869] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/11/2022] [Accepted: 04/05/2023] [Indexed: 06/06/2023] Open
Abstract
Sarcopenia is a common condition in patients with hepatocellular carcinoma (HCC). Sarcopenia affects the prognosis of patients with HCC and reduces their quality of life. However, to date, there has been no systematic review and meta-analysis to assess the prevalence of sarcopenia in patients with HCC, to the best of our knowledge. PubMed, Embase, Web of Science and the Cochrane Library were comprehensively screened for relevant literature published from March 2001 to June 2022. A random effect analysis was conducted to pool the incidence rates for each study. Subgroup and meta-regression analyses were used to investigate the latent sources of heterogeneities. The Newcastle-Ottawa Scale was used to estimate the quality of the included studies. The I2 statistic was used to evaluate heterogeneity between studies. In total, 48 studies encompassing 8,959 patients were included in the meta-analysis. The results of the present meta-analysis showed that nearly half (42%) of the patients with HCC had sarcopenia (95% CI, 0.36-0.48). The morbidity of sarcopenia in studies with a high proportion of males (45%) was higher compared with the morbidity observed in studies with a lower proportion of males (37%). In addition, the incidence rate in younger patients (46%) was found to be higher compared with the incidence rate in older patients (39%). In conclusion, the findings in the present systematic review revealed that a large number of patients with HCC suffer from sarcopenia, indicating the necessity of developing screening and intervention measures to improve the outcome in these patients.
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Affiliation(s)
- Jiye Liu
- Department of Family Medicine, Shengjing Hospital of China Medical University, Shenyang, Liaoning 110000, P.R. China
- Department of Rehabilitation Medicine, Huludao Central Hospital, Huludao, Liaoning 125000, P.R. China
| | - Hanyong Luo
- Department of Family Medicine, Shengjing Hospital of China Medical University, Shenyang, Liaoning 110000, P.R. China
| | - Letian Huang
- Department of Oncology, Shengjing Hospital of China Medical University, Shenyang, Liaoning 110000, P.R. China
| | - Jiahe Wang
- Department of Family Medicine, Shengjing Hospital of China Medical University, Shenyang, Liaoning 110000, P.R. China
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11
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Kuo MH, Tseng CW, Hsu CS, Chen YC, Kao IT, Wu CY, Shao SC. Prevalence and Effect of Low Skeletal Muscle Mass among Hepatocellular Carcinoma Patients Undergoing Systemic Therapy: A Systematic Review and Meta-Analysis. Cancers (Basel) 2023; 15:cancers15092426. [PMID: 37173893 PMCID: PMC10177136 DOI: 10.3390/cancers15092426] [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: 03/13/2023] [Revised: 04/17/2023] [Accepted: 04/20/2023] [Indexed: 05/15/2023] Open
Abstract
Low skeletal muscle mass (LSMM) is associated with poor outcomes in hepatocellular carcinoma (HCC) patients. With the emergence of new systemic therapeutics, understanding the effect of LSMM on HCC treatment outcomes is critically important. This systematic review and meta-analysis investigates the prevalence and effect of LSMM among HCC patients undergoing systemic therapy as reported in studies identified in searches of the PubMed and Embase databases published through 5 April 2023. The included studies (n = 20; 2377 HCC patients undergoing systemic therapy) reported the prevalence of LSMM assessed by computer tomography (CT) and compared the survival outcomes [overall survival (OS) or progression-free survival (PFS)] between HCC patients with and without LSMM. The pooled prevalence of LSMM was 43.4% (95% CI, 37.0-50.0%). A random-effects meta-analysis showed that HCC patients receiving systemic therapy with comorbid LSMM had a lower OS (HR, 1.70; 95% CI, 1.46-1.97) and PFS (HR, 1.32; 95% CI, 1.16-1.51) than did those without. Subgroup analysis according to systemic therapy type (sorafenib, lenvatinib, or immunotherapy) yielded similar results. In conclusion, LSMM is prevalent among HCC patients undergoing systemic therapy and is associated with poorer survival. Early intervention or prevention strategies to improve muscle mass may be necessary for this patient population.
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Affiliation(s)
- Meng-Hsuan Kuo
- Department of Pharmacy, Dalin Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Chia-Yi 62247, Taiwan
| | - Chih-Wei Tseng
- School of Medicine, Tzu Chi University, Hualien 97004, Taiwan
- Division of Gastroenterology, Department of Internal Medicine, Dalin Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Chia-Yi 62247, Taiwan
| | - Ching-Sheng Hsu
- School of Medicine, Tzu Chi University, Hualien 97004, Taiwan
- Division of Gastroenterology, Department of Internal Medicine, Dalin Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Chia-Yi 62247, Taiwan
- School of Post-Baccalaureate Chinese Medicine, Tzu Chi University, Hualien 97004, Taiwan
| | - Yen-Chun Chen
- School of Medicine, Tzu Chi University, Hualien 97004, Taiwan
- Division of Gastroenterology, Department of Internal Medicine, Dalin Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Chia-Yi 62247, Taiwan
| | - I-Ting Kao
- Department of Pharmacy, Dalin Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Chia-Yi 62247, Taiwan
| | - Chen-Yi Wu
- Department of Pharmacy, Dalin Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Chia-Yi 62247, Taiwan
| | - Shih-Chieh Shao
- Department of Pharmacy, Keelung Chang Gung Memorial Hospital, Keelung 20401, Taiwan
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12
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Fuochi E, Anastasio L, Lynch EN, Campani C, Dragoni G, Milani S, Galli A, Innocenti T. Main factors influencing long-term outcomes of liver transplantation in 2022. World J Hepatol 2023; 15:321-352. [PMID: 37034235 PMCID: PMC10075010 DOI: 10.4254/wjh.v15.i3.321] [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: 10/18/2022] [Revised: 11/24/2022] [Accepted: 02/22/2023] [Indexed: 04/11/2023] Open
Abstract
Liver transplant (LT) outcomes have markedly improved in the recent decades, even if long-term morbidity and mortality are still considerable. Most of late deaths are independent from graft function and different comorbidities, including complications of metabolic syndrome and de novo neoplasms, seem to play a key role in determining long-term outcomes in LT recipients. This review discusses the main factors associated with late mortality and suggests possible strategies to improve long-term management and follow-up after liver transplantation. In particular, the reduction of drug toxicity, the use of tools to identify high-risk patients, and setting up a multidisciplinary team also for long-term management of LT recipients may further improve survival after liver transplantation.
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Affiliation(s)
- Elisa Fuochi
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
| | - Lorenzo Anastasio
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
| | - Erica Nicola Lynch
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
| | - Claudia Campani
- Department of Experimental and Clinical Medicine, University of Florence, Florence 50134, Italy
| | - Gabriele Dragoni
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
- Department of Medical Biotechnologies, University of Siena, Siena 53100, Italy
| | - Stefano Milani
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
| | - Andrea Galli
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
| | - Tommaso Innocenti
- Gastroenterology Research Unit, Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
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Couderc AL, Liuu E, Boudou-Rouquette P, Poisson J, Frelaut M, Montégut C, Mebarki S, Geiss R, ap Thomas Z, Noret A, Pierro M, Baldini C, Paillaud E, Pamoukdjian F. Pre-Therapeutic Sarcopenia among Cancer Patients: An Up-to-Date Meta-Analysis of Prevalence and Predictive Value during Cancer Treatment. Nutrients 2023; 15:nu15051193. [PMID: 36904192 PMCID: PMC10005339 DOI: 10.3390/nu15051193] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/03/2023] [Revised: 02/18/2023] [Accepted: 02/21/2023] [Indexed: 03/08/2023] Open
Abstract
This study will address the prevalence of pre-therapeutic sarcopenia (PS) and its clinical impact during cancer treatment among adult cancer patients ≥ 18 years of age. A meta-analysis (MA) with random-effect models was performed via a MEDLINE systematic review, according to the PRISMA statement, focusing on articles published before February 2022 that reported observational studies and clinical trials on the prevalence of PS and the following outcomes: overall survival (OS), progression-free survival (PFS), post-operative complications (POC), toxicities (TOX), and nosocomial infections (NI). A total of 65,936 patients (mean age: 45.7-85 y) with various cancer sites and extensions and various treatment modes were included. Mainly defined by CT scan-based loss of muscle mass only, the pooled prevalence of PS was 38.0%. The pooled relative risks were 1.97, 1.76, 2.70, 1.47, and 1.76 for OS, PFS, POC, TOX, and NI, respectively (moderate-to-high heterogeneity, I2: 58-85%). Consensus-based algorithm definitions of sarcopenia, integrating low muscle mass and low levels of muscular strength and/or physical performance, lowered the prevalence (22%) and heterogeneity (I2 < 50%). They also increased the predictive values with RRs ranging from 2.31 (OS) to 3.52 (POC). PS among cancer patients is prevalent and strongly associated with poor outcomes during cancer treatment, especially when considering a consensus-based algorithm approach.
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Affiliation(s)
- Anne-Laure Couderc
- Internal Medicine Geriatrics and Therapeutic Unit, APHM, 13009 Marseille, France
- CNRS, EFS, ADES, Aix-Marseille University, 13015 Marseille, France
| | - Evelyne Liuu
- Department of Geriatrics, CHU Poitiers, 86000 Poitiers, France
- CIC1402 INSERM Unit, Poitiers University Hospital, 86000 Poitiers, France
| | - Pascaline Boudou-Rouquette
- Ariane Program, Department of Medical Oncology, Cochin Hospital, Paris Cancer Institute CARPEM, APHP, 75014 Paris, France
- INSERM U1016-CNRS UMR8104, Cochin Institute, Paris Cancer Institute CARPEM, Paris Cité University, 75015 Paris, France
| | - Johanne Poisson
- Department of Geriatrics, Georges Pompidou European Hospital, Paris Cancer Institute CARPEM, APHP, 75015 Paris, France
- Faculty of Health, Paris Cité University, 75006 Paris, France
| | - Maxime Frelaut
- Department of Medical Oncology, Gustave Roussy Institute, 94805 Villejuif, France
| | - Coline Montégut
- Internal Medicine Geriatrics and Therapeutic Unit, APHM, 13009 Marseille, France
- Coordination Unit for Geriatric Oncology (UCOG), PACA West, 13009 Marseille, France
| | - Soraya Mebarki
- Department of Geriatrics, Georges Pompidou European Hospital, Paris Cancer Institute CARPEM, APHP, 75015 Paris, France
| | - Romain Geiss
- Department of Medical Oncology, Curie Institute, 92210 Saint-Cloud, France
| | - Zoé ap Thomas
- Department of Cancer Medicine, Gustave Roussy Institute, 94805 Villejuif, France
| | - Aurélien Noret
- Department of Geriatrics, Georges Pompidou European Hospital, Paris Cancer Institute CARPEM, APHP, 75015 Paris, France
| | - Monica Pierro
- Department of Geriatrics, Georges Pompidou European Hospital, Paris Cancer Institute CARPEM, APHP, 75015 Paris, France
| | - Capucine Baldini
- Drug Development Department, Gustave Roussy Institute, 94805 Villejuif, France
| | - Elena Paillaud
- Department of Geriatrics, Georges Pompidou European Hospital, Paris Cancer Institute CARPEM, APHP, 75015 Paris, France
- INSERM, IMRB, Clinical, Epidemiology and Ageing, Université Paris-Est Creteil, 94010 Creteil, France
| | - Frédéric Pamoukdjian
- Department of Geriatrics, Avicenne Hospital, APHP, 93000 Bobigny, France
- INSERM UMR_S942 Cardiovascular Markers in Stressed Conditions MASCOT, Sorbonne Paris Nord University, 93000 Bobigny, France
- Correspondence:
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14
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Guo Y, Ren Y, Zhu L, Yang L, Zheng C. Association between sarcopenia and clinical outcomes in patients with hepatocellular carcinoma: an updated meta-analysis. Sci Rep 2023; 13:934. [PMID: 36650190 PMCID: PMC9845331 DOI: 10.1038/s41598-022-27238-z] [Citation(s) in RCA: 24] [Impact Index Per Article: 12.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/09/2022] [Accepted: 12/28/2022] [Indexed: 01/18/2023] Open
Abstract
Although numerous studies have reported the association between sarcopenia and the prognosis of hepatocellular carcinoma (HCC) patients, there is lack of a newer and more comprehensive meta-analysis. Herein, a comprehensive literature search was performed on PubMed, Web of Science, the Cochrane Library, and Embase databases to identify relevant studies published up to February 2022. The outcomes were overall survival (OS), recurrence, progression-free survival, tumor response, severe postoperative complications, and toxicity of drugs. A total of 57 studies involving 9790 HCC patients were included in the meta-analysis. The pooled prevalence of sarcopenia in HCC patients was 41.7% (95% CI 36.2-47.2%). Results demonstrated that sarcopenia was significantly associated with impaired OS (HR: 1.93, 95% CI 1.73-2.17, P < 0.001), higher risk of tumor recurrence (HR: 1.75, 95% CI 1.56-1.96, P < 0.001), lower objective response rate (OR: 0.37 95% CI 0.17-0.81, P = 0.012), and more drug-related adverse events (OR: 2.23, 95% CI 1.17-4.28, P = 0.015) in HCC patients. The subgroup analyses revealed that the OS of patients at the early stage of tumor was more severely affected by sarcopenia than for patients at other stages. Moreover, the presence of cirrhosis and Child Pugh class B increased the hazard of mortality from sarcopenia. This study has shown that sarcopenia is highly associated with poor prognosis in HCC patients. In addition, cirrhosis and poor liver functional reserve increase the danger of sarcopenia. OS was more impaired in HCC patients with sarcopenia at early stage of tumor than at other tumor stages.
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Affiliation(s)
- Yusheng Guo
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, No. 1277 Jiefang Avenue, Wuhan, 430022, China.,Hubei Key Laboratory of Molecular Imaging, Wuhan, 430022, China
| | - Yanqiao Ren
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, No. 1277 Jiefang Avenue, Wuhan, 430022, China.,Hubei Key Laboratory of Molecular Imaging, Wuhan, 430022, China
| | - Licheng Zhu
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, No. 1277 Jiefang Avenue, Wuhan, 430022, China.,Hubei Key Laboratory of Molecular Imaging, Wuhan, 430022, China
| | - Lian Yang
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, No. 1277 Jiefang Avenue, Wuhan, 430022, China. .,Hubei Key Laboratory of Molecular Imaging, Wuhan, 430022, China.
| | - Chuansheng Zheng
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, No. 1277 Jiefang Avenue, Wuhan, 430022, China. .,Hubei Key Laboratory of Molecular Imaging, Wuhan, 430022, China.
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15
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Guo Y, Ren Y, Wu F, Dong X, Zheng C. Prognostic impact of sarcopenia in patients with hepatocellular carcinoma treated with PD-1 inhibitor. Therap Adv Gastroenterol 2022; 15:17562848221142417. [PMID: 36600683 PMCID: PMC9806410 DOI: 10.1177/17562848221142417] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/09/2022] [Accepted: 11/14/2022] [Indexed: 12/28/2022] Open
Abstract
BACKGROUND Sarcopenia is a progressive generalized loss of skeletal muscle mass commonly observed in advanced stages of cancer. OBJECTIVE To assess the relationship between sarcopenia and the prognosis of patients with hepatocellular carcinoma (HCC) treated with a programmed cell death 1 (PD-1) inhibitor. DESIGN This is a retrospective study. METHODS This study included patients with HCC treated with camrelizumab between 1 March 2020 and 1 December 2021. The skeletal muscle area at the L3 vertebra middle level was used to calculate the skeletal muscle index. Propensity score matching (PSM) analysis was used to balance the variables between the two groups. RESULTS In all, 97 patients with HCC were included in the study, with 46 and 51 patients in the sarcopenia group and the non-sarcopenia group, respectively. The baseline characteristics of albumin, Child-Pugh class, albumin-bilirubin score, neutrophil-to-lymphocyte ratio, and platelet-to-lymphocyte ratio were significantly different between the two groups. In total, 26 patients from each group (n = 52) were selected after the PSM analysis. The progression-free survival (PFS) in the non-sarcopenia group was significantly longer than that in the sarcopenia group before and after PSM analysis (6.5 versus 4.8 months, p = 0.038). In addition, the disease control rate was similar before and after PSM analysis (57.7% versus 69.2%, p = 0.388). The objective response rate in the non-sarcopenia group tended to be higher than that in the sarcopenia group (11.5% versus 30.8%, p = 0.090, after PSM), but no statistically significant difference was found. The median overall survival (OS) in the non-sarcopenia group tended to longer than it in the sarcopenia group before PSM without significant differences (16.3 versus 11.3 months, p = 0.090) and the median OS was similar between the two groups after PSM (16.3 versus 16.8 months, p = 0.735). CONCLUSIONS HCC patients with sarcopenia tended to have higher levels of inflammation and lower levels of albumin than patients without sarcopenia. Sarcopenia is associated with a shorter PFS in HCC patients treated with PD-1 inhibitor.
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Affiliation(s)
| | | | | | - Xiangjun Dong
- Department of Radiology, Union Hospital, Tongji
Medical College, Huazhong University of Science and Technology, 1277 Jiefang
Avenue, Wuhan, Hubei 430022, China,Hubei Province Key Laboratory of Molecular
Imaging, Wuhan, China
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16
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Xu T, Zhang SM, Wu HM, Wen XM, Qiu DQ, Yang YY, Wang LZ, Zhu WB, He LS, Li JJ. Prognostic significance of prognostic nutritional index and systemic immune-inflammation index in patients after curative breast cancer resection: a retrospective cohort study. BMC Cancer 2022; 22:1128. [PMID: 36329394 PMCID: PMC9632068 DOI: 10.1186/s12885-022-10218-x] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/18/2022] [Accepted: 10/24/2022] [Indexed: 11/06/2022] Open
Abstract
BACKGROUND Nutritional status and inflammation are closely associated with poor outcome in malignant tumors. However, the prognostic impact of postoperative in these variables on breast cancer (BC) remains inconclusive. We aimed to determine whether prognostic nutritional index (PNI), systemic immune-inflammation index (SII), neutrophil-lymphocyte ratio (NLR) and platelet-lymphocyte ratio (PLR) affect two long-term outcomes among patients after curative resection of BC. METHODS We retrospectively reviewed 508 patients with BC treated with curative surgery between February 5, 2013 and May 26, 2020. All patients were divided into 3 groups based on tertiles (T1-T3) of PNI, SII, NLR, and PLR. The effects of four indexes on disease-free survival (DFS) and overall survival (OS) have been evaluated using Cox proportional hazards models and Kaplan-Meier method. RESULTS Compared with PNI-lowest cases, patients with highest PNI showed significantly longer DFS (multivariate adjusted hazard ratio [HR] = 0.37, 95% confident interval [CI] 0.19-0.70, P for trend = 0.002), whereas higher PLR seemed to be marginally associated with poorer DFS (P for trend = 0.086 and 0.074, respectively). Subgroup analyses indicate the potential modification effects of family history of BC and radiotherapy on the prognosis value of PNI to DFS in BC patients (P for interaction = 0.004 and 0.025, respectively). In addition, the levels of three inflammatory indices, namely SII, NLR, and PLR might be positively related with increased age at diagnosis (all P for trend < 0.001). CONCLUSIONS A high PNI was associated with better DFS, supporting its roles as prognostic parameters for patients with BC. The nutritional status and systemic immune may exert great effects on patient prognosis. Further studies are warrant to explore the prognosis value of PLR.
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Affiliation(s)
- Tai Xu
- grid.459766.fDepartment of Breast Surgery, Meizhou People’s Hospital, No.63 Huangtang Road, Meijiang District, Meizhou, Guangdong 541000 People’s Republic of China ,grid.459766.fGuangdong Provincial Key Laboratory of Precision Medicine and Clinical Translational Research of Hakka Population, Meizhou People’s Hospital, Meizhou, Guangdong People’s Republic of China
| | - Si-Ming Zhang
- grid.459766.fDepartment of Breast Surgery, Meizhou People’s Hospital, No.63 Huangtang Road, Meijiang District, Meizhou, Guangdong 541000 People’s Republic of China
| | - He-Ming Wu
- grid.459766.fGuangdong Provincial Key Laboratory of Precision Medicine and Clinical Translational Research of Hakka Population, Meizhou People’s Hospital, Meizhou, Guangdong People’s Republic of China ,grid.459766.fCenter for Precision Medicine, Meizhou People’s Hospital, Meizhou, Guangdong People’s Republic of China
| | - Xiao-Min Wen
- grid.459766.fClinical Laboratory Center, Meizhou People’s Hospital, Meizhou, Guangdong People’s Republic of China
| | - Dong-Qin Qiu
- grid.459766.fDepartment of Breast Surgery, Meizhou People’s Hospital, No.63 Huangtang Road, Meijiang District, Meizhou, Guangdong 541000 People’s Republic of China
| | - Yu-Yang Yang
- grid.459766.fDepartment of Breast Surgery, Meizhou People’s Hospital, No.63 Huangtang Road, Meijiang District, Meizhou, Guangdong 541000 People’s Republic of China
| | - Li-Zhen Wang
- grid.459766.fDepartment of Breast Surgery, Meizhou People’s Hospital, No.63 Huangtang Road, Meijiang District, Meizhou, Guangdong 541000 People’s Republic of China
| | - Wen-Biao Zhu
- grid.459766.fDepartment of Pathology, Meizhou People’s Hospital, Meizhou, Guangdong People’s Republic of China
| | - Li-Shan He
- grid.459766.fClinical Pharmaceutics Room, Meizhou People’s Hospital, Meizhou, Guangdong People’s Republic of China
| | - Jian-Juan Li
- grid.459766.fDepartment of Breast Surgery, Meizhou People’s Hospital, No.63 Huangtang Road, Meijiang District, Meizhou, Guangdong 541000 People’s Republic of China
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17
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Radu P, Ebadi M, Montano-Loza AJ, Dufour JF. What Is the Role of Body Composition Assessment in HCC Management? Cancers (Basel) 2022; 14:5290. [PMID: 36358709 PMCID: PMC9656561 DOI: 10.3390/cancers14215290] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/01/2022] [Revised: 10/23/2022] [Accepted: 10/24/2022] [Indexed: 10/06/2023] Open
Abstract
In the last decade, body composition (BC) assessment has emerged as an innovative tool that can offer valuable data concerning nutritional status in addition to the information provided by the classical parameters (i.e., body mass index, albumin). Furthermore, published data have revealed that different types of body composition are associated with different outcomes. For example, abnormalities of skeletal muscle, a common finding in cirrhotic and oncologic patients, are associated with poor outcome (i.e., high morbidity and high mortality). The disposition (visceral/subcutaneous adipose tissue) and radiodensity of adipose tissue proved to also be determinant factors for HCC outcome. Despite all the advantages, BC assessment is not part of the standard pre-therapeutic workup. The main reasons are the high heterogeneity of data, the paucity of prospective studies, the lack of a standard assessment method, and the interpopulation variation of BC. This paper aims to review the available evidence regarding the role of BC as a prognostic tool in the HCC population undergoing various therapies.
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Affiliation(s)
- Pompilia Radu
- Department of Visceral Surgery and Medicine, Inselspital, Bern University Hospital, University of Bern, 3008 Bern, Switzerland
| | - Maryam Ebadi
- Division of Gastroenterology & Liver Unit, University of Alberta, Edmonton, AB T6G 2X8, Canada
| | - Aldo J. Montano-Loza
- Division of Gastroenterology & Liver Unit, University of Alberta, Edmonton, AB T6G 2X8, Canada
| | - Jean Francois Dufour
- Department for BioMedical Research, Visceral Surgery and Medicine, University of Bern, 3008 Bern, Switzerland
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18
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Perisetti A, Goyal H, Yendala R, Chandan S, Tharian B, Thandassery RB. Sarcopenia in hepatocellular carcinoma: Current knowledge and future directions. World J Gastroenterol 2022; 28:432-448. [PMID: 35125828 PMCID: PMC8790553 DOI: 10.3748/wjg.v28.i4.432] [Citation(s) in RCA: 48] [Impact Index Per Article: 16.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/19/2021] [Revised: 06/29/2021] [Accepted: 01/11/2022] [Indexed: 02/06/2023] Open
Abstract
Liver cancer is the second most occurring cancer worldwide and is one of the leading causes of cancer-related deaths. Hepatocellular carcinoma (HCC) is the most common (80%-90%) type among malignant liver cancers. Sarcopenia occurs very early in HCC and can predict and provide an opportunity to improve muscle health before engaging in the treatment options such as loco-regional, systemic, and transplant management. Multiple prognostic stating systems have been developed in HCC, such as Barcelona Clinic Liver Cancer, Child-Pugh score and Albumin-Bilirubin grade. However, the evaluation of patients' performance status is a major limitation of these scoring systems. In this review, we aim to summarize the current knowledge and recent advances about the role of sarcopenia in cirrhosis in general, while focusing specifically on HCC. Additionally, the role of sarcopenia in predicting clinical outcomes and prognostication in HCC patients undergoing loco-regional therapies, liver resection, liver transplantation and systematic therapy has been discussed. A literature review was performed using databases PubMed/MEDLINE, EMBASE, Cochrane, Web of Science, and CINAHL on April 1, 2021, to identify published reports on sarcopenia in HCC. Sarcopenia can independently predict HCC-related mortality especially in patients undergoing treatments such as loco-regional, surgical liver transplantation and systemic therapies. Basic research is focused on evaluating a balance of anabolic and catabolic pathways responsible for muscle health. Early clinical studies have shown promising results in methods to improve sarcopenia in HCC which can potentially increase prognosis in these patients. As sarcopenia occurs very early in HCC, it can predict and provide an opportunity to improve muscle health before engaging in the treatment options such as loco-regional, systemic, and transplant management. Further, sarcopenia measurement can obviate the confounding caused by the abdominal ascites in these patients. The use of sarcopenia can add to the existing scoring systems to better prognosticate the HCC.
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Affiliation(s)
- Abhilash Perisetti
- Department of Internal Medicine, Gastroenterology and Hepatology Division, University of Arkansas for Medical Sciences, Little Rock, AR 72205, United States
- Department of Interventional Oncology and Surgical Endoscopy, Parkview Health, Fort Wayne, IN 46825, United States
| | - Hemant Goyal
- Department of Internal Medicine, The Wright Center for Graduate Medical Education, The Wright Center for Graduate Medical Education, Scranton, PA 18501, United States
| | - Rachana Yendala
- Department of Hematology and Oncology, Conway Regional Medical Center, Conway, AR 72034, United States
| | - Saurabh Chandan
- Department of Internal Medicine, Gastroenterology and Hepatology Division, CHI Creighton University Medical Center, Omaha, NE 68107, United States
| | - Benjamin Tharian
- Department of Internal Medicine, Gastroenterology and Hepatology Division, University of Arkansas for Medical Sciences, Little Rock, AR 72205, United States
| | - Ragesh Babu Thandassery
- Department of Medicine, Central Arkansas Veterans Healthcare System, Little Rock, AR 72205, United States
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19
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Guz M, Jeleniewicz W, Cybulski M. An Insight into miR-1290: An Oncogenic miRNA with Diagnostic Potential. Int J Mol Sci 2022; 23:1234. [PMID: 35163157 PMCID: PMC8835968 DOI: 10.3390/ijms23031234] [Citation(s) in RCA: 16] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2021] [Revised: 01/11/2022] [Accepted: 01/19/2022] [Indexed: 12/12/2022] Open
Abstract
For more than two decades, the view of the roles of non-coding RNAs (ncRNAs) has been radically changing. These RNA molecules that are transcribed from our genome do not have the capacity to encode proteins, but are critical regulators of gene expression at different levels. Our knowledge is constantly enriched by new reports revealing the role of these new molecular players in the development of many pathological conditions, including cancer. One of the ncRNA classes includes short RNA molecules called microRNAs (miRNAs), which are involved in the post-transcriptional control of gene expression affecting various cellular processes. The aberrant expression of miRNAs with oncogenic and tumor-suppressive function is associated with cancer initiation, promotion, malignant transformation, progression and metastasis. Oncogenic miRNAs, also known as oncomirs, mediate the downregulation of tumor-suppressor genes and their expression is upregulated in cancer. Nowadays, miRNAs show promising application in diagnosis, prediction, disease monitoring and therapy response. Our review presents a current view of the oncogenic role of miR-1290 with emphasis on its properties as a cancer biomarker in clinical medicine.
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Affiliation(s)
- Małgorzata Guz
- Department of Biochemistry and Molecular Biology, Medical University of Lublin, 20-093 Lublin, Poland; (W.J.); (M.C.)
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20
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Tan Y, Duan T, Li B, Zhang B, Zhu Y, Yan K, Song J, Lv T, Yang J, Jiang L, Yang J, Wen T, Yan L. Sarcopenia defined by psoas muscle index independently predicts long-term survival after living donor liver transplantation in male recipients. Quant Imaging Med Surg 2022; 12:215-228. [PMID: 34993073 DOI: 10.21037/qims-21-314] [Citation(s) in RCA: 22] [Impact Index Per Article: 7.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/21/2021] [Accepted: 06/25/2021] [Indexed: 02/05/2023]
Abstract
Background The effect of sarcopenia on long-term outcomes in recipients after living donor liver transplantation (LDLT), including overall survival and hepatocellular carcinoma (HCC) recurrence, remains unclear, especially in China. Methods From 2009 to 2015, 117 adult patients underwent LDLT in our center. In all, 82 patients who had computed tomography images reaching the third lumbar vertebra level within 1 month of LDLT were included; 70 male patients were included in the final analysis after excluding 12 female patients because of poor performance of the calculated cutoff value. Sarcopenia was defined according to the psoas muscle index (PMI) cutoff value, which was calculated based on dynamic time-dependent outcomes using X-tile software. Cox proportional hazards models were used to assess multivariate-adjusted hazards ratios (HRs) to seek potential correlations between sarcopenia and posttransplant outcomes. Results According to the cutoff value of PMI (6.25 cm2/m2), 38 patients (54.3%) were diagnosed with sarcopenia. After an average of 63.3 months of follow-up, 21 patients died after LDLT, 16 in the sarcopenia group and 5 in the non-sarcopenia group, respectively. Sarcopenia was identified as being significantly associated with worse posttransplant overall survival in multivariate analysis, resulting in an HR of 3.22 [95% confidence interval (CI), 1.15-8.98]. Among the 50 recipients with HCC, sarcopenia was significantly associated with HCC recurrence in univariate analysis (HR 2.87, 95% CI, 1.06-7.80) but was not detected as an independent risk factor of HCC recurrence in multivariate analysis, although a trend (tendency)towards significance was observed (HR 2.60, 95% CI, 0.95-7.10; P=0.062). Conclusions Sarcopenia defined by PMI is a feasible and reliable independent predictor of posttransplant overall survival in male LDLT candidates. However, its correlation with posttransplant HCC recurrence remains uncertain.
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Affiliation(s)
- Yifei Tan
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Ting Duan
- Department of Radiology, West China Hospital of Sichuan University, Chengdu, China
| | - Bo Li
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Bohan Zhang
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Yunfeng Zhu
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Ke Yan
- West China School of Public Health, Sichuan University, Chengdu, China
| | - Jiulin Song
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Tao Lv
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Jian Yang
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Li Jiang
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Jiayin Yang
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Tianfu Wen
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
| | - Lunan Yan
- Liver Transplantation Center, Department of Liver Surgery, West China Hospital of Sichuan University, Chengdu, China
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21
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Lim J, Kim KW, Ko Y, Jang IY, Lee YS, Chung YH, Lee HC, Lim YS, Kim KM, Shim JH, Choi J, Lee D. The role of muscle depletion and visceral adiposity in HCC patients aged 65 and over undergoing TACE. BMC Cancer 2021; 21:1164. [PMID: 34715813 PMCID: PMC8557070 DOI: 10.1186/s12885-021-08905-2] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2021] [Accepted: 10/19/2021] [Indexed: 11/29/2022] Open
Abstract
Background The incidence of hepatocellular carcinoma (HCC) has been increasing among the elderly populations. Trans-arterial chemoembolization (TACE), a widely used first-line non-curative therapy for HCCs is an issue in geriatrics. We investigated the prognosis of elderly HCC patients treated with TACE and determined the factors that affect the overall survival. Methods We included 266 patients who were older than 65 years and had received TACE as initial treatment for HCC. We analyzed the skeletal muscle index (SMI) and visceral-to-subcutaneous fat ratio (VSR) around the third lumbar vertebrae using computed tomography scans. Muscle depletion with visceral adiposity (MDVA) was defined by falling below the median SMI and above the median VSR value sex-specifically. We evaluated the overall survival in association with MDVA and other clinical factors. Results The mean age was 69.9 ± 4.5 years, and 70.3% of the patients were men. According to the Barcelona Clinic Liver Cancer (BCLC) staging system, 29, 136, and 101 patients were classified as BCLC 0, A, and B stages, respectively, and 79 (29.7%) had MDVA. During the median follow-up of 4.1 years, patients with MDVA had a shorter life expectancy than those without MDVA (P = 0.007) even though MDVA group had a higher objective response rate after the first TACE (82.3% vs. 75.9%, P = 0.035). Multivariate analysis revealed that MDVA (Hazard ratio [HR] 1.515) age (HR 1.057), liver function (HR 1.078), tumor size (HR 1.083), serum albumin level (HR 0.523), platelet count (HR 0.996), tumor stage (stage A, HR 1.711; stage B, HR 2.003), and treatment response after the first TACE treatment (HR 0.680) were associated with overall survival. Conclusions MDVA is a critical prognostic factor for predicting survival in the elderly patients with HCC who have undergone TACE. Supplementary Information The online version contains supplementary material available at 10.1186/s12885-021-08905-2.
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Affiliation(s)
- Jihye Lim
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea
| | - Kyung Won Kim
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Yousun Ko
- Biomedical Research Center, Asan Institute for Life Sciences, Asan Medical Center, Seoul, Republic of Korea
| | - Il-Young Jang
- Division of Geriatrics, Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Yung Sang Lee
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Young-Hwa Chung
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Han Chu Lee
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Young-Suk Lim
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Kang Mo Kim
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Ju Hyun Shim
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Jonggi Choi
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea.,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Danbi Lee
- Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-ro 44-gil, Songpa-gu, Seoul, 05505, Republic of Korea. .,Asan Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea.
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22
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Han B, Ding H, Zhao S, Zhang Y, Wang J, Zhang Y, Gu J. Potential Role of Adjuvant Lenvatinib in Improving Disease-Free Survival for Patients With High-Risk Hepatitis B Virus-Related Hepatocellular Carcinoma Following Liver Transplantation: A Retrospective, Case Control Study. Front Oncol 2020; 10:562103. [PMID: 33365268 PMCID: PMC7750628 DOI: 10.3389/fonc.2020.562103] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/14/2020] [Accepted: 11/04/2020] [Indexed: 12/24/2022] Open
Abstract
BACKGROUND AND AIM Although liver transplantation (LT) is one of the most effective treatments for the patients with hepatocellular carcinoma (HCC), the high-risk patients suffer from a high ratio of tumor recurrence after LT. Lenvatinib, as a novel targeted drug, has shown an excellent effect in the treatment of advanced HCC, but there is no study on its effect in preventing HCC recurrence in the patients undergoing transplantation. Therefore, this study was designed to evaluate the role of adjuvant lenvatinib in preventing recurrence of high-risk LT recipients with HBV-related HCC. METHODS We retrospectively analyzed 23 high-risk patients consisting of lenvatinib group (n=14) and control group (n=9) with HBV-related HCC who underwent LT in our center. Disease-free survival (DFS) and HCC recurrence of the two groups were compared. The adverse events (AEs) and drug tolerance of lenvatinib were evaluated. RESULTS The median DFS in lenvatinib group was 291 (95%CI 204-516) days, significantly longer than 182 (95%CI 56-537) days in control group (P=0.04). Three patients in lenvatinib group (21.4%) and five patients in control group (55.6%) had short-term HCC recurrence (P=0.11). All patients in lenvatinib group could tolerate oral lenvatinib for at least three cycles except six cases (42.9%) of dose reduction and 1 case of interruption (14.3%). Thirteen patients (92.9%) taking lenvatinib experienced AEs. The most common AEs were hypertension (64.3%) and proteinuria (42.9%), and the most serious AEs were Grade 3 for 4 cases (28.5%) according to common terminology criteria for adverse events (CTCAE) version 5.0. Additionally, no influence of lenvatinib on the dosage and blood concentration of FK506 was observed. CONCLUSIONS Adjuvant lenvatinib had a potential benefit on prolonging the DFS and reducing the recurrence of high-risk HBV-related HCC patients following liver transplantation with an acceptable drug safety and patient tolerance.
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Affiliation(s)
- Bing Han
- Department of Transplantation, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of General Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Han Ding
- Department of Transplantation, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of General Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Shuai Zhao
- Department of Transplantation, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of General Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Yichi Zhang
- Department of Transplantation, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of General Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Jian Wang
- Department of Transplantation, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of General Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Yue Zhang
- Department of Bioinformatics and Biostatistics, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China
| | - Jinyang Gu
- Department of Transplantation, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
- Department of General Surgery, Xinhua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China
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Serum Myostatin Predicts the Risk of Hepatocellular Carcinoma in Patients with Alcoholic Cirrhosis: A Multicenter Study. Cancers (Basel) 2020; 12:cancers12113347. [PMID: 33198216 PMCID: PMC7697795 DOI: 10.3390/cancers12113347] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/31/2020] [Accepted: 11/10/2020] [Indexed: 02/08/2023] Open
Abstract
Background and Aim: Previous studies reported that serum myostatin is associated with sarcopenia. We aimed to elucidate the association between serum myostatin levels and hepatocellular carcinoma (HCC) development in patients with alcoholic liver cirrhosis (ALC). Methods: This retrospective, multicenter study assessed 1077 Asian ALC patients enrolled from 2007 to 2017. The primary endpoint was the development of HCC within 5 years. Cox proportional hazards model analyses were used to assess the association of serum myostatin levels and HCC development. The time-dependent areas under the receiver operating characteristic curve (AUROC) of serum myostatin for 5-year HCC development were calculated. Serum myostatin levels were measured using an enzyme-linked immunosorbent assay with samples collected on the index date. Results: During a median follow-up of 2.5 years, 5-year cumulative HCC incidence rates were 6.7% in the total population. The median level of serum myostatin was 3.3 ng/mL (interquartile, 2.1-5.2 ng/mL). The AUROC of serum myostatin for 5-year HCC development was 0.78 (95% confidence interval [CI], 0.76-0.81). In Cox proportional hazards model analyses, age, gender, platelet counts, and serum myostatin levels were independent risk factors for HCC development (adjusted hazard ratios [HRs] of age, male gender, platelet counts, and serum myostatin: 1.03, 2.79, 0.996, 1.18, respectively; all p < 0.05). Patients with high myostatin levels had a significantly higher risk of 5-year HCC development than those with low myostatin levels (HR 7.53, p < 0.001). Conclusion: Higher serum myostatin levels were significantly associated with a higher risk of developing HCC in ALC patients, which could identify high-risk patients who need stringent surveillance.
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Badran H, Elsabaawy MM, Ragab A, Abdelhafiz Aly R, Alsebaey A, Sabry A. Baseline Sarcopenia is Associated with Lack of Response to Therapy, Liver Decompensation and High Mortality in Hepatocellular Carcinoma Patients. Asian Pac J Cancer Prev 2020; 21:3285-3290. [PMID: 33247686 PMCID: PMC8033124 DOI: 10.31557/apjcp.2020.21.11.3285] [Citation(s) in RCA: 17] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/21/2020] [Accepted: 11/22/2020] [Indexed: 02/05/2023] Open
Abstract
OBJECTIVE hepatocellular carcinoma (HCC) is a dreadful complication of liver cirrhosis. Aim was to study the effect of sarcopenia on the survival in patients with HCC. METHODS we included 262 patients and were followed up for 12 months. Sarcopenia was calculated by skeletal muscle index (SMI). Sarcopenia was defined by SMI ≤39 cm2/m2 for women and ≤50 cm2/m2 for men. RESULTS patients with sarcopenia (n= 113, 43.1%) were older, mainly males, Child-Pugh class B and smokers. Patients with sarcopenia had lower survival than those without (10.09 vs. 11.72 months). Survival was also lower in Barcelona clinic liver cancer stage C than B and A (9.02 vs. 11.21 vs. 11.89 months). Age and sarcopenia were hazardous of mortality (p <0.05). There was statistically significant difference of serial SMI in patients without baseline sarcopenia unlike patients with baseline sarcopenia. On follow up patients with sarcopenia had higher incidence of ascites (45% vs. 20.4%), spontaneous bacterial peritonitis (21.7% vs. 11.6%), hepatic encephalopathy (28% vs. 11.5%) and bleeding (22.9% vs. 12.7%). Totally patients with sarcopenia had higher incidence of progressive HCC (39% vs. 25.5%). CONCLUSION Sarcopenia is associated with lack of response to therapy, liver decompensation and higher mortality in hepatocellular carcinoma patients.
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Affiliation(s)
- Hanaa Badran
- Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Shebeen El-Koom, Egypt.
| | - Maha Mohammad Elsabaawy
- Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Shebeen El-Koom, Egypt.
| | - Amr Ragab
- Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Shebeen El-Koom, Egypt.
| | - Rasha Abdelhafiz Aly
- Department of Diagnostic Medical Imaging and Interventional Radiology; National Liver Institute, Menoufia University, Shebeen El-Koom, Egypt.
| | - Ayman Alsebaey
- Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Shebeen El-Koom, Egypt.
| | - Aliaa Sabry
- Department of Hepatology and Gastroenterology, National Liver Institute, Menoufia University, Shebeen El-Koom, Egypt.
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25
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Marasco G, Serenari M, Renzulli M, Alemanni LV, Rossini B, Pettinari I, Dajti E, Ravaioli F, Golfieri R, Cescon M, Festi D, Colecchia A. Clinical impact of sarcopenia assessment in patients with hepatocellular carcinoma undergoing treatments. J Gastroenterol 2020; 55:927-943. [PMID: 32748172 PMCID: PMC7519899 DOI: 10.1007/s00535-020-01711-w] [Citation(s) in RCA: 69] [Impact Index Per Article: 13.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/11/2020] [Accepted: 07/15/2020] [Indexed: 02/04/2023]
Abstract
Changes in body composition are associated with poor outcomes in cancer patients including hepatocellular carcinoma (HCC). Sarcopenia, defined as the loss of skeletal muscle mass, quality and function, has been associated with a higher rate of complications and recurrences in patients with cirrhosis and HCC. The assessment of patient general status before HCC treatment, including the presence of sarcopenia, is a key-point for achieving therapy tolerability and to avoid short- and long-term complications leading to poor patients' survival. Thus, we aimed to review the current literature evaluating the role of sarcopenia assessment related to HCC treatments and to critically provide the clinicians with the most recent and valuable evidence. As a result, sarcopenia can be predictive of poor outcomes in patients undergoing liver resection, transplantation and systemic therapies, offering the chance to clinicians to improve the muscular status of these patients, especially those with high-grade sarcopenia at high risk of mortality. Further studies are needed to clarify the predictive value of sarcopenia in other HCC treatment settings and to evaluate its role as an additional staging tool for identifying the most appropriate treatment. Besides, interventional studies aiming at increasing the skeletal muscle mass for reducing complications and increasing the survival in patients with HCC are needed.
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Affiliation(s)
- Giovanni Marasco
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy.
| | - Matteo Serenari
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Matteo Renzulli
- Radiology Unit, Sant'Orsola Malpighi Hospital, Via Albertoni 4, 40138, Bologna, Italy
| | - Luigina Vanessa Alemanni
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Benedetta Rossini
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Irene Pettinari
- Radiology Unit, Sant'Orsola Malpighi Hospital, Via Albertoni 4, 40138, Bologna, Italy
| | - Elton Dajti
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Federico Ravaioli
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Rita Golfieri
- Radiology Unit, Sant'Orsola Malpighi Hospital, Via Albertoni 4, 40138, Bologna, Italy
| | - Matteo Cescon
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Davide Festi
- Department of Medical and Surgical Sciences, University of Bologna, Via Massarenti 9, 40126, Bologna, Italy
| | - Antonio Colecchia
- Gastroenterology Unit, University Hospital Borgo Trento, Verona, Italy
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Pommergaard HC, Rostved AA, Adam R, Rasmussen A, Salizzoni M, Bravo MAG, Cherqui D, De Simone P, Houssel-Debry P, Mazzaferro V, Soubrane O, García-Valdecasas JC, Prous JF, Pinna AD, O'Grady J, Karam V, Duvoux C, Thygesen LC. Mortality after Transplantation for Hepatocellular Carcinoma: A Study from the European Liver Transplant Registry. Liver Cancer 2020; 9:455-467. [PMID: 32999871 PMCID: PMC7506266 DOI: 10.1159/000507397] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/20/2019] [Accepted: 02/17/2020] [Indexed: 02/04/2023] Open
Abstract
BACKGROUND AND AIMS Prognosis after liver transplantation differs between hepatocellular carcinoma (HCC) arising in cirrhotic and non-cirrhotic livers and aetiology is poorly understood. The aim was to investigate differences in mortality after liver transplantation between these patients. METHODS We included patients from the European Liver Transplant Registry transplanted due to HCC from 1990 to November 2016 and compared cirrhotic and non-cirrhotic patients using propensity score (PS) calibration of Cox regression estimates to adjust for unmeasured confounding. RESULTS We included 22,787 patients, of whom 96.5% had cirrhosis. In the unadjusted analysis, non-cirrhotic patients had an increased risk of overall mortality with a hazard ratio (HR) of 1.37 (95% confidence interval [CI] 1.23-1.52). However, the HR approached unity with increasing adjustment and was 1.11 (95% CI 0.99-1.25) when adjusted for unmeasured confounding. Unadjusted, non-cirrhotic patients had an increased risk of HCC-specific mortality (HR 2.62, 95% CI 2.21-3.12). After adjustment for unmeasured confounding, the risk remained significantly increased (HR 1.62, 95% CI 1.31-2.00). CONCLUSIONS Using PS calibration, we showed that HCC in non-cirrhotic liver has similar overall mortality, but higher HCC-specific mortality. This may be a result of a more aggressive cancer form in the non-cirrhotic liver as higher mortality could not be explained by tumour characteristics or other prognostic variables.
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Affiliation(s)
- Hans-Christian Pommergaard
- Department of Surgical Gastroenterology and Transplantation, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark,*Hans-Christian Pommergaard, Department of Surgical Gastroenterology and Transplantation, Rigshospitalet, University of Copenhagen, Blegdamsvej 9, DK–2100 Copenhagen (Denmark),
| | - Andreas Arendtsen Rostved
- Department of Surgical Gastroenterology and Transplantation, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
| | - René Adam
- Department of Hepatobiliary Surgery, Cancer, and Transplantation, AP-HP, Hôpital Universitaire Paul Brousse, Inserm U935, Université Paris-Sud, Villejuif, France
| | - Allan Rasmussen
- Department of Hepatobiliary Surgery, Cancer, and Transplantation, AP-HP, Hôpital Universitaire Paul Brousse, Inserm U935, Université Paris-Sud, Villejuif, France
| | - Mauro Salizzoni
- Liver Transplant Centre and General Surgery, A.O.U. Città della Salute e della Scienza di Torino, Molinette Hospital, Turin, Italy
| | | | - Daniel Cherqui
- Department of Hepatobiliary Surgery, Cancer, and Transplantation, AP-HP, Hôpital Universitaire Paul Brousse, Inserm U935, Université Paris-Sud, Villejuif, France
| | - Paolo De Simone
- Hepatobiliary Surgery and Liver Transplantation Unit, University of Pisa Medical School Hospital, Pisa, Italy
| | - Pauline Houssel-Debry
- Service de Chirurgie Hépatobiliaire et Digestive, Hôpital Pontchaillou, Centre Hospitalier Université de Rennes 1, and INSERM, UMR991, Foie, Métabolisme et Cancer, Université de Rennes 1, Rennes, France
| | - Vincenzo Mazzaferro
- University of Milan and Division of Gastrointestinal Surgery and Liver Transplantation, Istituto Nazionale Tumori, Fondazione IRCCS, Milan, Italy
| | - Olivier Soubrane
- Department of HPB Surgery and Liver Transplant, Beaujon Hospital, Clichy, University Denis Diderot, Paris, France
| | | | - Joan Fabregat Prous
- Unitat de Cirurgia Hepato-bilio-pancreàtica, Hospital Universitari de Bellvitge, Barcelona, Spain
| | - Antonio D. Pinna
- General Surgery and Transplant Division, S. Orsola Hospital, University of Bologna, Bologna, Italy
| | - John O'Grady
- Institute of Liver Studies, King's College Hospital, London, United Kingdom
| | - Vincent Karam
- Department of Hepatobiliary Surgery, Cancer, and Transplantation, AP-HP, Hôpital Universitaire Paul Brousse, Inserm U935, Université Paris-Sud, Villejuif, France
| | - Christophe Duvoux
- Department of Hepatology and Liver Transplant Unit, Henri Mondor Hospital, Paris Est University, Créteil, France
| | - Lau Caspar Thygesen
- National Institute of Public Health, University of Southern Denmark, Copenhagen, Denmark
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The prognostic nutritional index and postoperative complications after curative lung cancer resection: A retrospective cohort study. J Thorac Cardiovasc Surg 2020; 160:276-285.e1. [DOI: 10.1016/j.jtcvs.2019.10.105] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/28/2019] [Revised: 09/09/2019] [Accepted: 10/01/2019] [Indexed: 12/23/2022]
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Impact of Body Composition on the Risk of Hepatocellular Carcinoma Recurrence After Liver Transplantation. J Clin Med 2019; 8:jcm8101672. [PMID: 31614892 PMCID: PMC6832484 DOI: 10.3390/jcm8101672] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/30/2019] [Revised: 09/20/2019] [Accepted: 10/11/2019] [Indexed: 12/12/2022] Open
Abstract
BACKGROUND Body composition parameters are reported to influence the risk of hepatocellular carcinoma (HCC) recurrence after liver resection, yet data on patients undergoing liver transplantation are scarce. The aim of this study was to evaluate the impact of the amount of abdominal adipose tissue and skeletal muscles on the risk of HCC recurrence after liver transplantation. METHODS This was a retrospective observational study performed on 77 HCC patients after liver transplantation. Subcutaneous fat area (SFA), visceral fat area, psoas muscle area and total skeletal muscle area were assessed on computed tomography on the level of L3 vertebra and divided by square meters of patient height. The primary outcome measure was five-year recurrence-free survival. RESULTS Recurrence-free survival in the entire cohort was 95.7%, 90.8%, and 86.5% after one, three, and five years post-transplantation, respectively. SFA was significantly associated with the risk of HCC recurrence (p = 0.013), whereas no significant effects were found for visceral fat and skeletal muscle indices. The optimal cut-off for SFA for prediction of recurrence was 71.5 cm2/m2. Patients with SFA < 71.5 cm2/m2 and ≥71.5 cm2/m2 exhibited five-year recurrence-free survival of 96.0% and 55.4%, respectively (p = 0.001). CONCLUSIONS Excessive amount of subcutaneous adipose tissue is a risk factor for HCC recurrence after liver transplantation and may be considered in patient selection process.
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Ooi PH, Hager A, Mazurak VC, Dajani K, Bhargava R, Gilmour SM, Mager DR. Sarcopenia in Chronic Liver Disease: Impact on Outcomes. Liver Transpl 2019; 25:1422-1438. [PMID: 31242345 DOI: 10.1002/lt.25591] [Citation(s) in RCA: 94] [Impact Index Per Article: 15.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/25/2019] [Accepted: 06/24/2019] [Indexed: 12/11/2022]
Abstract
Malnutrition is a common complication in patients with end-stage liver disease (ESLD) awaiting liver transplantation (LT). Malnutrition and sarcopenia overlap in etiology and outcomes, with sarcopenia being defined as reduced skeletal muscle mass and muscle function. The purpose of this review was to identify the prevalence of sarcopenia with and without obesity in adults and children with ESLD and to assess the methodological considerations in sarcopenia diagnosis and the association of sarcopenia with pre- and post-LT outcomes. A total of 38 articles (35 adult and 3 pediatric articles) retrieved from PubMed or Web of Science databases were included. In adults, the prevalence rates of pre-LT sarcopenia, pre-LT sarcopenic obesity (SO), post-LT sarcopenia, and post-LT SO were 14%-78%, 2%-42%, 30%-100%, and 88%, respectively. Only 2 adult studies assessed muscle function in patients diagnosed with sarcopenia. The presence of pre-LT sarcopenia is associated with higher wait-list mortality, greater postoperative mortality, higher infection risk and postoperative complications, longer intensive care unit (ICU) stay, and ventilator dependency. The emerging pediatric data suggest that sarcopenia is prevalent in pre- and post-LT periods. In 1 pediatric study, sarcopenia was associated with poor growth, longer perioperative length of stay (total/ICU) and ventilator dependency, and increased rehospitalization in children after LT. In conclusion, there is a high prevalence of sarcopenia in adults and children with ESLD. Sarcopenia is associated with adverse clinical outcomes. The present review is limited by heterogeneity in the definition of sarcopenia and in the methodological approaches in assessing sarcopenia. Future studies are needed to standardize the sarcopenia diagnosis and muscle function assessment, particularly in the pediatric population, to enable early identification and treatment of sarcopenia in adults and children with ESLD.
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Affiliation(s)
- Poh Hwa Ooi
- Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, Alberta, Canada
| | - Amber Hager
- Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, Alberta, Canada
| | - Vera C Mazurak
- Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, Alberta, Canada
| | - Khaled Dajani
- Department of General Surgery, University of Alberta, Edmonton, Alberta, Canada
| | - Ravi Bhargava
- Department of Radiology and Diagnostic Imaging, Walter C. Mackenzie Health Sciences Centre, University of Alberta, Edmonton, Alberta, Canada
| | - Susan M Gilmour
- Pediatrics, University of Alberta, Edmonton, Alberta, Canada.,Division of Pediatric Gastroenterology and Nutrition/Transplant Services, The Stollery Children's Hospital, Alberta Health Services, Edmonton, Alberta, Canada
| | - Diana R Mager
- Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, Alberta, Canada.,Pediatrics, University of Alberta, Edmonton, Alberta, Canada
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