Research ArticleClinical Studies

Prognostic Impact of a Novel Albumin-Platelet Index as Selection Criterion for Hepatic Resection in Intermediate Stage Hepatocellular Carcinoma

KYOHEI YUGAWA, TAKASHI MAEDA, SHIGEYUKI NAGATA, AKIHIRO SAKAI, KENJI TAKETANI, SHOHEI YAMAGUCHI, KOZO KONISHI and KENKICHI HASHIMOTO
Anticancer Research April 2023, 43 (4) 1835-1842; DOI: https://doi.org/10.21873/anticanres.16337

Abstract

Background/Aim: Hepatic resection for Barcelona Clinic Liver Cancer (BCLC) stage B (intermediate-stage) hepatocellular carcinoma (HCC) is not recommended by BCLC treatment algorithms. We sought to develop a new prognostic model for determining appropriate treatment strategies in patients with intermediate-stage HCC. Patients and Methods: This single-center retrospective study included patients who underwent hepatic resection for HCC between 2000 and 2018. A total of 498 patients were classified according to the BCLC staging system (0, n=116; A, n=319; B, n=63). The predictive impact for surgical outcomes was evaluated using receiver operating characteristic (ROC) curves. Based on a survival outcome probability formula, a new predictive model was established. Results: The preoperative albumin level and platelet count were the strongest diagnostic values in patients with intermediate-stage HCC (areas under the ROC curves, AUCs: 0.710 and 0.676, respectively). Logistic regression analysis provided the albumin–platelet index [API; 156.2×albumin (g/dl)+platelet count (×109/l)] was defined as a new prognostic model for the probability of poor survival. The optimal cutoff value (781.2; AUC 0.755) divided patients with BCLC-B into B1 (>781.2, n=27) and B2 (≤781.2, n=36) categories. Patients in substage B2 had a significantly worse prognosis than patients in other stages (p<0.0001), whereas there was no difference in prognosis between patients in substage B1 and those in other stages. Conclusion: The API stratifies prognosis in patients with intermediate-stage HCC. For subgroup B1, hepatic resection can be considered a radical treatment, even for intermediate-stage HCC.

Key Words:

Hepatocellular carcinoma (HCC) is the most common primary liver neoplasm, the sixth most common neoplasm overall, and the third leading cause of death from cancer (1). Several staging systems have been proposed to define the prognosis and recommend the best treatment options for patients with HCC (2, 3). The Barcelona Clinic Liver Cancer (BCLC) staging system provides to determine patient prognosis and informs specific treatment algorithms based on tumor status, including the number, size, and location of tumors, as well as underlying liver function (4). Hepatic resection remains the main radical treatment for patients with resectable HCC (5, 6). According to the BCLC staging system, only patients with very early (BCLC stage 0) and early stage (BCLC stage A) HCC should undergo hepatic resection, while patients with the intermediate stage (BCLC stage B) and advanced stage (BCLC stage C) HCC are recommended to receive transarterial chemoembolization (TACE) or systemic treatment (7).

Because the BCLC stage B shows considerable heterogeneity (includes up to three tumors where at least one is >3 cm in diameter, more than three tumors of any size), several surgeons have questioned the indications of hepatic resection in the classification of BCLC stage B. The patients with BCLC stage B HCC can differ in background factors such as tumor number, size, biomarkers, as well as liver function. To date, several prognostic factors have been identified for patients with resectable HCC (8, 9). However, very few studies have clarified risk stratifications focusing on preoperative liver functional parameters for resected BCLC stage B HCC. Herein, our goal was to reveal the prognostic utility of common laboratory tests in predicting surgical outcomes and to establish an easily calculated criterion for decision-making of hepatic resection in patients who undergo hepatic resection even for intermediate-stage HCC.

Patients and Methods

Patients and ethics. This study included all patients who underwent hepatic resection for primary HCC at Hiroshima Red Cross Hospital and Atomic-bomb Survivors Hospital in Japan between January 2000 and December 2018. Patients did not receive preoperative chemotherapy or radiation and were selected retrospectively. Details of the surgical technique and patient selection criteria were described previously (8, 10). Anonymized preoperative and postoperative clinical data for all patients were obtained from electronic and paper records. The ethics committee of our hospital approved this study under the ethical guidelines of the Japanese government (approval number: 2021-029), and all patients provided consent for the use of their clinical data in this research.

Data collection and follow-up survey. Preoperative serum samples were collected within 1 month before hepatic resection for HCC. Tumor markers (alpha-fetoprotein, AFP and des-gamma-carboxy prothrombin, DCP) and levels of total bilirubin, albumin, international normalized ratio of prothrombin time (PT-INR), aspartate aminotransferase (AST), alanine aminotransferase (ALT), and platelet count were measured before surgery. A preoperative indocyanine green dye retention rate at 15 min (ICG-R15) was calculated by linear regression from the plasma concentrations of indocyanine green at 15 min. A follow-up survey was conducted after surgery, as previously described (11).

Statistical analysis. Data analysis process was previously described (10). Data were calculated as means, medians, frequencies, and percentages. We used the Mann-Whitney U-test and the Kruskal-Wallis test to compare continuous variables. We used the χ2 test or Fisher’s exact test to compare categorical variables. We performed the receiver operating characteristic (ROC) curve analysis of various predictive markers. The area under the ROC curve (AUC) was established for determining optimal cutoff values to analyze 5-year overall survival (OS). We used the Kaplan-Meier method to calculate cumulative OS and recurrence-free survival (RFS) rates, and we used the log-rank test to evaluate the differences between the curves. OS was calculated as the time from the date of surgery to the date of either the last follow-up or death. To identify postoperative prognostic factors, we included variables significant in univariable analyses in the overall multivariable Cox proportional model. All statistical tests were two-sided, and a p-value of <0.05 indicated significance. All analyses were performed with JMP14 software (SAS Institute, Cary, NC, USA).

Results

Patients’ characteristics and survival using BCLC staging. Table I summarizes the patients’ baseline characteristics according to the BCLC staging system. Of the 498 patients, 116 (23.3%), 319 (64.1%), and 63 (12.6%) patients were classified as BCLC stage 0, A, and B, respectively. The median age was significantly younger in the BCLC stage B group than in the BCLC stage 0 and A groups (0 vs. B, p=0.0320 and A vs. B, p=0.0356). Serum albumin level was significantly lower in BCLC stage B than in BCLC stage 0 (median 4.1 vs. 3.9, p=0.0214). Additionally, AST and ALT levels were higher in BCLC stage B than BCLC stage 0 and A (AST, 0 vs. B, p=0.0208 and A vs. B, p=0.0169; ALT, 0 vs. B, p=0.0234 and A vs. B, p=0.0145, respectively). The serum AFP level was significantly higher in BCLC stage B than in BCLC stage 0 and A (0 vs. B, p<0.0001 and A vs. B, p=0.0087). Regarding postoperative factors, the patients with BCLC stage B HCC had poorly differentiation and positivity of microscopic intrahepatic metastasis than those with BCLC stage 0 HCC (16.4% vs. 36.5%, p=0.0024 and 6.0% vs. 23.8%, p=0.0005, respectively). Histological liver cirrhosis was more frequent in patients with BCLC stage B than in those with BCLC stage A (41.4% vs. 60.3%, p=0.0057). The 5-year OS rates for stage 0, A and B patients with HCC were 86.9, 73.8 and 56.1%, respectively. The 5-year RFS rates were 49.1, 35.1 and 16.9%, respectively. There was a significant difference in OS and RFS between BCLC stages (in log-rank tests, p<0.0001, Figure 1).

View this table:
Table I.

Characteristics of the hepatocellular carcinoma patients categorized according to the Barcelona Clinic Liver Cancer staging system.

Figure 1.
Figure 1.

Overall and recurrence-free survival of patients with HCC after hepatic resection according to BCLC staging system. HCC, Hepatocellular carcinoma; BCLC, Barcelona Clinic Liver Cancer stage.

ROC analysis for OS and a formula established from preoperative laboratory factors. Table II summarizes the ROC curve analysis of each parameter in patients with BCLC stage B HCC. Of the preoperative factors, serum albumin level and platelet count were the strongest predictors of poor OS compared to the other factors examined [albumin, AUC 0.710, 95% confidence interval (CI)=0.537-0.838, p=0.0069; platelet count, AUC 0.676, 95% CI=0.503-0.811, p=0.0089]. Logistic regression analysis yielded a formula for the probability of poor OS consisting of serum albumin level and platelet count, which showed a significantly lower p-value and high values of AUCs. The probability of poor OS for patients with BCLC stage B HCC was then calculated as follows:

Embedded Image

where 156.2×albumin (g/dl)+platelet (×109/l) was defined as the albumin–platelet index (API). This formula estimates the probability of poor OS for patients with BCLC stage B HCC. The API was the most accurate predictor of poor OS compared with the other models (cutoff value 781.2, AUC 0.755, sensitivity 87.0%, specificity 60.0%, p=0.0009). On the basis of these findings, the API was selected for further examination in patients with BCLC stage B HCC.

View this table:
Table II.

Receiver operating characteristic curve analysis to evaluate the predictive value of each preoperative factors for 5-year overall survival in patients with Barcelona Clinic Liver Cancer stage B hepatocellular carcinoma.

Relationships between clinicopathological characteristics and API in BCLC stage B HCC. The API cutoff value of 781.2 was calculated using ROC curve analysis. Using this cutoff value, 27 (42.9%) and 36 patients (57.1%) were subclassified to BCLC-B1 (API >781.2) and B2 (API ≤781.2) subgroups, respectively, among the patients with BCLC stage B HCC. The clinicopathological characteristics of these patients are summarized in Table III. Overall, compared to the B1 subgroup, the B2 subgroup had significantly higher median levels of serum total bilirubin (0.6 vs. 0.9 mg/dl, p=0.0097), AST (34 vs. 55 IU/l, p=0.0001), ALT (30 vs. 52 IU/l, p=0.0003), PT-INR (1.02 vs. 1.10, p<0.0001), ICG-R15 (12.6% vs. 21.0%, p=0.0112) and AFP (9.0 vs. 59.5 ng/ml, p<0.0001). Moreover, the patients with substage B2 HCC had worse differentiation (22.2% vs. 47.2%, p=0.0414) and histological liver cirrhosis (37.0% vs. 77.8%, p=0.0011) than those with substage B1 HCC.

View this table:
Table III.

Comparison of clinicopathological variables among patients with Barcelona Clinic Liver Cancer stage B1 and B2 hepatocellular carcinoma.

BCLC substage B1 and B2 HCC patient survival. The Kaplan-Meier curves for patients with BCLC substage B1 and B2 subdivided by API revealed that OS and RFS (in log-rank tests, both p<0.0001) were significantly shorter in patients with substage B2 than in those with other BCLC stages (Figure 2). Of note, the OS was clearly stratified between patients in the substages B1 and B2; 5-year OS among patients with BCLC substage B1 and B2 was 84.9% and 38.7% (p<0.0001), respectively. The OS differed significantly in the BCLC subgroups (0 vs. B2, p<0.0001; A vs. B2, p<0.0001). The 5-year RFS of patients with BCLC substage B1 and B2 was 33.0% and 6.3% (p=0.0677), respectively. The RFS also differed significantly compared to the BCLC subgroup (0 vs. B2, p<0.0001; A vs. B2, p<0.0001). Thus, patients with BCLC substage B2 had worse OS and RFS. Interestingly, there was no difference in survival between patients undergoing hepatic resection for BCLC stage A and B1 HCC (for OS, A vs. B1, p=0.2708; for RFS, A vs. B1, p=0.1267).

Figure 2.
Figure 2.

Overall and recurrence-free survival of patients with HCC after hepatic resection according to BCLC subgroup B1 and B2. HCC, Hepatocellular carcinoma; BCLC, Barcelona Clinic Liver Cancer stage.

Univariate and multivariate analyses of prognostic factors for OS. According to Cox’s univariable proportional hazards analysis, the significant prognostic factors for shorter OS were high serum AFP level (≥400 ng/ml), the presence of intrahepatic metastases, and low API (≤781.2). In multivariable analysis, low API (hazard ratio=4.57, 95% CI=1.76-11.8, p=0.0018) was the only significant prognostic factor for shorter OS in patients with BCLC stage B HCC (Table IV).

View this table:
Table IV.

Univariate and multivariate analyses for predictors of overall survival in patients with Barcelona Clinic Liver Cancer stage B hepatocellular carcinoma (Cox proportional hazards analysis).

Discussion

This study used ROC analysis to evaluate which preoperative laboratory variables had the strongest prognostic values in patients who underwent curative hepatic resection for intermediate-stage HCC. Of the preoperative factors, serum albumin level and platelet count were the best predictors of poor survival. Logistic regression analysis yielded a model to determine the probability of poor survival, which included the API. Then, the patients with intermediate-stage HCC were categorized into B1 (high API) and B2 (low API) based on the results of this index. The OS of patients with BCLC substage B1 did not differ from that of patients with BCLC stage 0 and A. Even among patients with intermediate-stage HCC, hepatic resection could be considered an initial treatment option for patients with BCLC substage B1.

The updated (2022) BCLC staging system recommends TACE or systemic treatment for patients with intermediate-stage HCC (7). Conversely, Japanese clinical guidelines recommend several treatments for BCLC stage B HCC, including hepatic resection, depending on the clinical situation (3). Thus, the BCLC intermediate-stage includes a heterogeneous patient population with different background factors such as tumor size and number, as well as underlying liver function, which are required to subdivide stage B for predicting prognosis and recommending optimal treatments. Recently, Bolondi et al. (12) and Kudo et al. (13) proposed a modified BCLC staging model for prognostic prediction in patients with intermediate-stage HCC who underwent TACE. However, these criteria were limited in helping surgeons make hepatic resection decisions because of the subdivision dedicated to TACE. There is an urgent and unmet need for a BCLC stage B subclassification system suitable for hepatic resection. Hepatic resection produces a better prognosis than other treatment modalities and should be considered a radical treatment for patients with BCLC stage B (14-17). However, hepatic resection requires careful consideration for patients with intermediate-stage HCC.

Decision-making criteria of hepatectomy for intermediate-stage HCC have been elucidated in several studies. Wada et al. divided BCLC stage B into three subtypes according to tumor size (cutoff, 5 cm) and numbers (cutoff, four tumors) and showed that surgery can provide a favorable outcome for selected patients with intermediate-stage HCC (18). Similar to that study, Tsilimigras et al. indicated that tumor burden scores calculated using tumor size and number can be candidates for resection (19). Kamiyama et al. suggested that tumor number combined with tumor markers (AFP and DCP) can be an effective classified criterion when considering hepatic resection (20). Thus, tumor activities such as tumor size, number, and markers are significant factors for predicting prognosis in patients who underwent resection for intermediate-stage HCC. Meanwhile, it is important to evaluate both tumor status and preoperative liver function.

Very few studies have focused on preoperative liver function for considering surgical indications according to BCLC criteria. Zhang et al. reported the subclassification of BCLC stage B HCC using tumor size and number and PT (21). Tada et al. suggested that hepatic resection should be considered in patients with a Child–Pugh score of 5 and with fewer than two tumors, even with BCLC stage B HCC (17). In the current study, the API-consisting of serum albumin level and platelet count-was identified as the superior predictor of poor long-term outcomes in patients with intermediate-stage HCC. To the best of our knowledge, the accuracy of the combination of albumin level and platelet count for predicting surgical outcomes has not been evaluated in patients with BCLC stage B HCC. This is the first study to establish a predictive model from liver function parameters.

When hepatic resection selection criteria are developed, it is better to separate oncological staging and underlying liver function because the liver function is strongly correlated with treatment choice, which may affect the survival outcomes. In the current study, only preoperative laboratory factors were analyzed. Serum albumin level and platelet count were the most accurate predictors of survival. Yamamoto et al. established a predictive formula that included albumin level and platelet count for short-term surgical outcomes (22). Additionally, Shindoh et al. revealed that combined models of serum albumin level and platelet count predicted long-term surgical outcomes in patients with HCC (23). Fujita et al. indicated that albumin level and platelet count were correlated with prognosis because these factors reflected liver fibrosis in patients with HCC (24). We used preoperative serum albumin level and platelet count to develop a simple and useful criterion for surgical decision-making, even in patients with intermediate-stage HCC.

This study has some limitations. First, this was a single-center long-term retrospective study that included patients treated with postoperative ablation, endovascular treatment, or molecularly targeted drugs. Second, our ROC curve analysis of the API for assessing the cutoff value for poor outcomes might not have been completely accurate, because the sample size is small. Larger prospective studies including an external independent cohort may be required to confirm the validity of the API. Finally, we did not examine the detailed mechanisms underlying the associations between serum albumin level, platelet count, and outcomes, such as the biological progression of fibrosis and HCC. We will investigate these mechanisms in the future.

Conclusion

A low API was significantly associated with poor surgical outcomes compared with other predictive models in patients with BCLC stage B HCC. The API was used to categorize BCLC stage B into subgroup B1 (high API) and B2 (low API), and the OS of patients with BCLC substage B1 did not differ from that of patients with BCLC stage 0 and A. Based on our findings, the API, simply consisting of albumin level and platelet count, could be useful to select ideal candidates for hepatic resection. Even in patients with BCLC-B HCC, hepatic resection could be considered as one of the initial treatment options for patients with BCLC substage B1.

Acknowledgements

Source of funding is not applicable. The Authors would like to thank Enago (www.enago.jp) for the English language review.

Footnotes

  • Authors’ Contributions

    Study concept: K.Y and T.M. Study design: K.Y and T.M. Data acquisition: K.Y, A.S, and T.M. Data analysis and interpretation: K.Y, S.N, A.S, K.T, S.Y, K.K, and K.H. Statistical analysis: K.Y and T.M. Manuscript preparation: K.Y and T.M. Manuscript editing: K.Y and T.M. Manuscript review: All Authors.

  • Conflicts of Interest

    The Authors declare no conflicts of interest.

  • Received January 8, 2023.
  • Revision received January 27, 2023.
  • Accepted February 4, 2023.

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Prognostic Impact of a Novel Albumin-Platelet Index as Selection Criterion for Hepatic Resection in Intermediate Stage Hepatocellular Carcinoma
KYOHEI YUGAWA, TAKASHI MAEDA, SHIGEYUKI NAGATA, AKIHIRO SAKAI, KENJI TAKETANI, SHOHEI YAMAGUCHI, KOZO KONISHI, KENKICHI HASHIMOTO
Anticancer Research Apr 2023, 43 (4) 1835-1842; DOI: 10.21873/anticanres.16337
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