Albumin‑bilirubin grade is an independent prognostic factor for small lung cell cancer
- Authors:
- Published online on: December 15, 2023 https://doi.org/10.3892/mco.2023.2710
- Article Number: 12
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Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Lung cancer is one of the most common types of cancer, accounting for ~11.6% of all types of cancer. Small cell lung cancer (SCLC), as a subtype, accounts for 15% of lung cancer (1,2) SCLC is a rapidly progressing and highly aggressive neuroendocrine cancer with a 5-year survival rate of only 7% and is sensitive to initial chemotherapy and radiotherapy (3-5). Patients with SCLC are divided into limited stage and extensive stage. Limited stage refers to the lesion being confined to one side of the chest cavity and the cancer spreading to the pleural effusion and lymph nodes on the same side. Extensive stage refers to lesion spread beyond the same chest cavity, including malignant pleural effusions and pericardial effusions, lymph node metastases on the contralateral hilar or clavicle, or other parts of the body. The dichotomized staging system and TNM staging are important predictors for the prognosis of SCLC. Some clinical variables such as performance status, age, weight loss, stage, and serum lactate dehydrogenase (LDH) are also considered to predict the prognosis of SCLC. Some researchers have studied deep into the gene level to explore the targets associated with lung cancer (6). However, there are no standardized prognostic parameters (7). Therefore, it is important to explore accurate prognostic factors for SCLC. According to previous studies (8-10), liver function may be an important factor in the prognosis of various malignancies. Currently, the Child-Pugh score is the most important scoring system for evaluation of liver function (11). The Child-Pugh score was based on the total bilirubin, albumin, prothrombin time, and the clinical findings of encephalopathy and ascites. It was graded as 5-6 points for Child-Pugh-A; 7-9 points for Child-Pugh-B; and 10-15 points for Child-Pugh-C. However, it is not suitable for patients with SCLC, as most patients will merely be assigned to Child Pugh-A (12). Albumin-bilirubin (ALBI) grade, which has been used to evaluate liver function, was first described by Johnson et al (12) in 2015 as an indicator of liver dysfunction in patients with hepatocellular carcinoma. Several studies have demonstrated the prognostic value of ALBI grade in hepatocellular carcinoma (8,12,13), as well as in intrahepatic cholangiocarcinomas, pancreatic cancer, and gastric cancer (9,10,14). Furthermore, there has been a study describing the significance of ALBI grade in non-small cell lung cancer (15). However, the significance of ALBI grade in SCLC has not yet been elucidated. The present study aimed to explore the prognostic impact of ALBI grade in patients with SCLC.
Patients and methods
Patient and data collection
The present study retrospectively analyzed all patients with SCLC treated at the Department of Thoracic Surgery in Hebei General Hospital between April 2015 and August 2021. The patients were followed up throughout the clinical course for at least four months, and the cutoff date for data collection was December 31, 2021. Pre-treatment clinical information and social history were extracted from the hospital's electronic medical records. All the patients included in the present study were pathologically diagnosed with SCLC and there were no other malignant tumors and immune-related serious diseases or adverse factors affecting blood routine or biochemical indexes such as hematologic diseases, liver diseases and kidney diseases before treatment. The clinical data of the patients before receiving treatment were obtained before chemotherapy and surgery. Patients with incomplete test index results, inaccurate clinical data and failure of follow-up were excluded. End point of assessment was patient overall survival (OS), which is the time from diagnosis of SCLC to mortality and the secondary endpoint was progression free survival (PFS), PFS is defined as the time from initiation of therapy to disease progression. Patients with significant radiographic progression, markedly elevated tumor markers, or distant metastases were considered for PFS analyses and a total of 135 patients were included in the sample.
The present study conducted follow-up visits through outpatient clinics, hospitalizations and phone calls. The follow-up interval was 1 month. Follow-up rate was 96.3% and two consecutive losses to follow-up were defined as death with the date of death defined as the date of the last follow-up. The clinicopathological variables including sex, age, smoking status, TNM staging, body mass index (BMI), PS, Charlson comorbidity index (CCI) and whether undergoing surgery, chemotherapy or radiotherapy were recorded by the electronic medical record system. Laboratory parameters including lactate dehydrogenase (LDH), neutrophil to lymphocyte ratio (NLR), systemic inflammation index (SII), platelet to lymphocyte ratio (PLR), prognostic nutrition index (PNI), carcinoembryonic antigen (CEA) and neuron-specific enolase (NSE) were obtained from the clinical laboratory of Hebei General Hospital.
Statistical analysis
ALBI grade was calculated by the following formula: 0.66x log10 [total bilirubin (µmol/l)]-0.085 [albumin (ALB) (g/l)]11. SII was calculated as PLT x NLR (16). PNI was calculated as 10x serum albumin level (g/dl) +0.005x total lymphocyte count (per mm3) (17). In a previous study, ALBI scores were divided into three scales: grade 1 (ALBI score ≤-2.60), grade 2 (-2.60<ALBI score ≤-1.39), and grade 3 (-1.39<ALBI score)14. As far as the original cut-off value is specified according to liver cancer, it is necessary to find a cut-off value which is more suitable for SCLC. Therefore, cut-off values for ALBI grade, LDH, NLR, SII, PLR, CEA, NSE were determined using receiver operating characteristic (ROC) curve analysis, which can estimate optimal sensitivity, specificity, and the area under the curve (AUC) for prediction of mortality from all causes. Pearson correlation, Chi-square test and Fisher exact test were used to compare continuous and categorical variables. Cumulative cancer specific survival curves were calculated using the Kaplan-Meier method, and differences were assessed using Log rank test. The Cox proportional hazard model was used to evaluate the predictive power of potential prognostic variables, and the hazard ratios (HR) estimated from the Cox analysis reported as relative risks with corresponding 95% confidence intervals. To eliminate the influence of confounding factors, propensity score matching (PSM) was applied. Statistical analyses were performed using the IBM SPSS statistics software program, version 22.0 (IBM Corp.). P<0.05 was considered to indicate a statistically significant difference.
Results
Patient characteristics
In the present study, 135 patients pathologically diagnosed as SCLC were enrolled. The median age was 65 years (64.24±9.71; range=14-82 years). A total of 102 patients (76%) were male and 82 patients (61%) had a history of smoking. A total of 54 patients (40%) were in limited stage. A total of 77 patients (57%) had a BMI of less than 25. As for PS scores, 1 patient (1%) had a PS score of 0, 85 patients (63%) of 1, and 43 patients (32%) scored 2. A total of 64 patients (47%) scored CCI as 0, and 68 patients (50%) scored as 1-2.
Clinicopathological characteristics associated with ALBI grade
The optimal cutoff point resulted from ROC curve analysis of ALBI grade for the layering of OS in SCLC was determined to be-2.55 (Fig. 1A), which was in close conformity with the ALBI grade 1 and 2 boundaries (-2.60). Thus, the patients were classified as follows: Group 1 (n=87, 64.4%) with pre-treatment ALBI grade ≤-2.55 for an improved hepatic reserve and group 2 (n=48, 35.6%) with ALBI grade >-2.55. Optimal cutoff points of LDH, NLR, SII, PLR, CEA, NSE were 191.45, 3.519, 874.428, 281.896, 10.29, 23.84, respectively (Fig. 1B). The relationship between baseline characteristics and ALBI grade are shown in Table I. There was a significant association between ALBI grade and age, LDH, NLR, PNI and NSE. No significant differences were observed in terms of sex, smoking, staging, BMI, PS, CCI, surgery, SII, PLR, chemotherapy, radiotherapy and CEA.
The median PFS rates in group 1 and group 2 were 8.4 months and 5.9 months, respectively. PFS was significantly improved in group 1 than in group 2 (P<0.001 using the log-rank test, Fig. 2A). The median OS rates in group 1 and group 2 were 14.6 months and 9.2 months, respectively. OS was significantly improved in group 1 compared with in group 2 (P<0.001 using the log-rank test, Fig. 2B).
Univariate and multivariate analysis of PFS and OS
Univariate analysis revealed sex, age, smoking, staging, BMI, surgery, LDH, NLR, PLR, chemotherapy, CEA, NSE and ALBI grade as significant factors for PFS. Multivariate analysis revealed that sex, surgery, LDH, chemotherapy and ALBI grade are independent risk factors for PFS (Table II). Univariate analyses showed that sex, age, smoking, staging, BMI, surgery, LDH, PLR, Chemotherapy, CEA, NSE, PNI and ALBI grade are significant factors for OS while multivariate analysis revealed surgery, LDH, BMI, chemotherapy and ALBI grade as independent risk factors for OS (Table III).
ALBI grade and survival in propensity score matching analysis
To further validate the impact of ALBI grade on survival results in SCLC, a PSM analysis was employed to equalize background information of the patients. The caliper value was set as 0.15. As a result, 26 paired patients were extracted from the two groups. The relationship between baseline characteristics and ALBI grade after PSM are shown in Table IV. There were no differences in characteristics of the patients among the two groups. Univariate analysis showed that group 1 had a significantly longer PFS (HR 2.258, 95% CI 1.013-5.034, P=0.041, Fig. 3A) and OS (HR 2.591, 95% CI 1.154-5.814, P=0.017, Fig. 3B) than group 2. Multivariate analysis suggested that ALBI grade after PSM is an independent prognostic factor of PFS (HR 2.379, 95% CI 1.045-5.412, P=0.039, Table V) and OS (HR 3.496, 95% CI 1.416-8.635, P=0.007, Table VI).
Discussion
The present study retrospectively investigated the impact of pre-treatment ALBI grade on the prognosis of SCLC. It clarified that ALBI grade is an important prognostic factor of PFS and OS in univariate and multivariate analysis. To the best of the authors' knowledge, this is the first study to show the prognostic importance of ALBI grade in patients with SCLC. The results showed that ALBI grade was highly associated with age and LDH. The two factors showed prognostic power in patients with SCLC, which may be as confounding factors and cause a bias in the present study. In order to eliminate the influence of confounding factors, PSM was performed. After matching, ALBI grade proved to be an independent prognostic factor for the prognosis of SCLC. Sex, age, smoking, BMI and several clinical parameters were indicated to have prognostic power in patients with SCLC from univariate analysis before PSM. However, those factors showed no statistical difference after PSM, which may be due to the synergy with other factors including ALBI.
The liver can be partly regarded as an immune organ as it contains a large number of immune cells (18). Previous studies have indicated that impaired liver function has important effects on the systemic immune response in alcoholic liver injury and viral hepatitis (19,20). It is reported that decreased liver function can cause changes in T cell repertoires which play an important role in cellular immunity, and the effect may take place from the early stage of cirrhosis (20,21). As a result, the anti-tumor immune response of patients with liver disease may be weaker than normal patients. ALBI grade, as an indicator of liver function, can closely reflect the immune status of the whole body (22,23). Thus, ALBI grade may have a predictive power on anti-tumor immune response. In addition, studies have proved that a decrease of albumin, which compose the ALBI, can be an indicator of decreased liver reserve and increased inflammatory response in the tumor microenvironment (24,25). Hypoalbuminemia has been reported to indicate inflammation and prognosis in patients with non-small cell lung cancer (NSCLC) (26). Inflammation and immunity can affect the tumor microenvironment by influencing the formation of blood vessels (27,28), thereby further affecting the prognosis of SCLC. Therefore, the immune inflammatory response is considered to have prognostic power on patients with SCLC, which could be one of the mechanisms of the prognostic effect of ALBI grade (15,29).
Several inflammatory indicators were recorded and analyzed including NLR, SII and PLR, which have been proved to be important in predicting the prognosis of lung cancer, according to previous reports (30-32). NLR showed predictive effect of PFS in univariate analysis and PLR showed predictive effect of both PFS and OS. However, neither of the two factors had statistical significance in multivariate analysis. The results indicated that although immunity and inflammation have a predictive effect on the prognosis of SCLC, they may not have independent prognostic power. There may be synergistic factors that interact with immune inflammatory responses. This also reflects that there are other mechanisms for the prognostic effect of ALBI on patients with SCLC.
Nutrition and metabolism play an important role in tumor progression. Malnutrition in cancer patients can impair quality of life and response to treatment (33). BMI, PNI and ALB, which can reflect nutrition and metabolism to a certain extent, have been proved to be important parameters for assessing nutritional status (34-37). According to previous studies, these three factors are closely associated with the survival rate of advanced lung cancer (26,35-38). Therefore, they may have prognostic use for patients with SCLC. Previous studies have shown that weight loss in patients with advanced cancer may increase the risk of mortality (39,40). In the present study, BMI ≥25 indicated longer PFS and OS, and PNI ≥40 indicated longer OS. This confirmed that nutritional status has a certain effect on the prognosis of patients with SCLC. In addition, liver function can also reflect nutrition and metabolism (41). Bilirubin plays an important role in liver metabolism. Li et al (42) reported that elevated serum bilirubin levels are associated with improved survival in patients with NSCLC. There is evidence that serum bilirubin levels are associated with incidence and mortality of lung cancer in smokers (43). Therefore, to a large extent, bilirubin may be able to evaluate the prognosis of patients with SCLC. ALBI grade, consisting of albumin and bilirubin, may reflect the nutrition and metabolism status in patients with SCLC, which may be a mechanism of the prognostic effect.
One of the most important indicators in ALBI is ALB, which can directly affect the value of ALBI. ALB can bind and transport various endogenous and exogenous substances and promote their transport in the circulation (44). In addition, ALB can bind to a variety of drugs, affecting their release in target tissues (45). Previous studies (46,47) showed that ALB levels may affect the benefit of chemotherapy in elderly cancer patients. The present study also found that higher ALB levels and lower ALBI levels were associated with longer PFS and OS.
In addition, LDH has been reported as a prognostic indicator of SCLC and it can also predict the response to treatment of patients with SCLC (48). This may be due to the estimation ability of LDH on tumor burden. In the present study, LDH showed independent prognostic power for both PFS and OS of patients with SCLC. The results of the present study also indicated that LDH is strongly correlated with ALBI grade. Following PSM, LDH showed no statistical significance in multivariate analysis, which indicated that LDH may have a similar mechanism to ALBI grade in affecting the prognosis of SCLC. Therefore, it is hypothesized that ALBI grade can predict the effect of medication on patients with SCLC. Chemotherapy is currently one of the most important medical treatments for SCLC. The present study confirmed that chemotherapy can be an independent prognostic factor for SCLC. In addition, the importance of ALBI grade to predict the therapeutic effect of chemotherapy has been previously reported in hepatocellular carcinomas and gastric cancer (13,14,49) Therefore, ALBI grade may be predictive of the effectiveness of chemotherapy or post-recurrence chemotherapy on patients with SCLC to achieve prognostic evaluation effect.
In the present study, a total of 81 patients had distant metastases, mostly bone metastases, brain metastases and abdominal organ metastases. Only 15 patients had liver metastases, although ALBI values may have an effect in these patients with liver metastases. However, the main purpose of the present study was to discuss the relationship between ALBI and the prognosis of patients with SCLC, so it was considered that this would not affect the final results of the present study.
However, there are several limitations to the present study. First, this is a single-center retrospective study and there may be bias on patient selection and data collection. Second, the small number of samples may lead to poor credibility of the hypothesis. Large-scale prospective studies and experiments are needed to consolidate the conclusion of the present study and further explore the mechanism.
The present study showed that pre-treatment ALBI grade can be an independent prognostic factor in SCLC, of which the mechanisms may be associated with the immune inflammatory responses, nutrition and the response to chemotherapy.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
SL carried out experimental design and data statistics. QZ provided experimental guidance and result analysis. ZW was a major contributor to writing the manuscript. XZ conducted experimental design and helped write the manuscript. SL and ZB confirm the authenticity of all the raw data. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The Ethical Committee of Hebei General Hospital approved the present study and informed consent was waived (approval no. 2022061). The authors confirm the confidentiality of the data maintained and compliance with the Declaration of Helsinki.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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