Skip to main content
Download PDF

Prognostic impact of albumin-bilirubin score in predicting the long-term survival of distal cholangiocarcinoma after radical surgery

World Journal of Surgical Oncology volume 23, Article number: 160 (2025) Cite this article

Abstract

Background

The Albumin-Bilirubin Score (ALBI) serves as an indicator of nutritional status and is a widely recognized prognostic biomarker in cancer patients. The purpose of this research is to evaluate the association between ALBI and survival outcomes in patients with distal cholangiocarcinoma (dCCA) after radical surgery, and develop a nomogram model based on the ALBI to predict individual survival.

Methods

A total of 177 individuals with dCCA receiving surgery from Jan 2011 to Jan 2022 were enrolled in the research. The association between ALBI and clinicopathologic factors was investigated. The impact of ALBI on recurrence-free survival (RFS) and overall survival (OS) was evaluated by Kaplan–Meier curves and Cox proportional hazards models. Nomograms based on ALBI and other prognostic variables screened by multivariate analysis were produced in predicting RFS and OS of dCCA patients following radical surgery, and the nomograms were evaluated by the consistency index (C-index), calibration curve and decision curve analysis (DCA) curve.

Results

The optimal cut-off value for ALBI was -1.67, and the area under the ROC curve (AUC) was 0.71. The High-ALBI group had a considerably shorter RFS and OS (P < 0.001). Multivariate analysis revealed that the ALBI, degree of differentiation, portal vein invasion, and lymph node invasion were significant prognostic factors for RFS, and that the ALBI, CA19-9, degree of differentiation, lymph node invasion, and portal vein invasion were significant prognostic factors for OS. The nomograms were constructed based on these significant prognostic factors. The calibration curves displayed good consistency between actual and predicted probability. Nomograms based on these variables have better discriminant ability in predicting RFS and OS compared with the American Joint Committee on Cancer (AJCC) TNM stage. Moreover, the scores predicted by the nomogram enabled patient stratification into low-points and high-points groups. Kaplan–Meier curves demonstrated that patients in the high-points group had considerably better prognoses than those in the low-points group (p < 0.001).

Conclusion

ALBI was an independent prognostic factor in predicting RFS and OS of dCCA patients after radical surgery. The nomograms based on ALBI can provide reliable, personalized survival prediction for dCCA.

Introduction

Distal cholangiocarcinoma (dCCA) is a malignancy originating from the distal segment of the common bile duct to the ampulla of Vater, constituting 20%− 40% of all cholangiocarcinoma [1, 2]. Notably, the incidence of dCCA is markedly higher in Asian countries as compared with Western nations [3]. Pancreatoduodenectomy (PD) is the most effective and standardized method in dealing with dCCA compared with other surgical procedures. Patients suffering from dCCA following radical surgery may achieve 5-year survival rates ranging from 13 to 54% [4], whereas those who do not have surgical resection experience a considerably lower 5-year survival rate of merely 3% [5]. Although comprehensive treatment regimens have shown significant effects in improving overall prognosis [6,7,8], radical surgical resection remains the primary treatment option for patients with dCCA. Consequently, precise prognostic assessment of dCCA patients following radical surgery plays a pivotal role in shaping more refined and effective treatment protocols.

The preoperative nutritional state has a considerable impact on the prognosis of cancer patients [9, 10]. Although ALBI, a novel nutritional evaluation score, has demonstrated its prognostic impact in several types of tumors [11, 12], its relationship with the survival outcomes of dCCA remains unexplored. Albumin is the main protein synthesized by the liver, reflecting its synthetic function, while total bilirubin is a metabolic waste product of the liver, with elevated levels typically indicating liver dysfunction. These two factors are combined in the ALBI score, which provides a comprehensive assessment of liver function and can predict clinical outcomes of patients. Therefore, we believe that a higher ALBI score may reflect poorer liver function, which may affect the long-term prognosis of patients with dCCA. Physicians may apply nomograms, predictive models capable of integrating several prognostic signals, to boost the accuracy of forecasting patient survival [13,14,15]. Despite the widespread use of nomograms in various prognostic assessments, few have been developed for predicting the survival outcomes of dCCA patients.

Therefore, this study proposes to explore the impact of ALBI on the survival outcomes of dCCA patients following radical surgery, and to create an innovative nomogram that integrates ALBI and other clinicopathological factors for predicting RFS and OS in dCCA patients. The findings of the research are likely to inform more effective treatment strategies for physicians.

Materials and methods

Patient selection

We conducted a retrospective assessment of clinical data and follow-up information from 177 patients based on specific inclusion and exclusion criteria. Inclusion criteria included: (1) patients who underwent surgery in the Department of Hepatobiliary Surgery at Beijing Chaoyang Hospital from January 2011 to January 2022; (2) preoperative imaging confirming dCCA; (3) patients who underwent radical PD or PD with allogeneic venous replacement; (4) postoperative pathology confirmed bile duct adenocarcinoma. Exclusion criteria included: (1) survival of less than one month; (2) presence of distant metastases; (3) absence of surgery; (4) multiple primary malignancies.

Data collection and follow-up

All dCCA patients received blood routine and liver function testing 3–7 days before surgery. The ALBI score was computed using the formula: ALBI = (log10 total bilirubin [μmol/L] × 0.66) + (albumin [g/L] ×  − 0.0852) [16]. According to the optimal cut-off value for the ALBI score, all patients were categorized into two groups: ≤ –1.67 as Low-ALBI group and > –1.67 as High-ALBI group.

Demographic data, preoperative medical records, and pathology findings were obtained. Preoperative biliary drainage was performed in selected dCCA patients based on specific clinical indications [17]. All patients received adjuvant chemotherapy postoperatively in accordance with the guidelines established by the National Comprehensive Cancer Network [18]. Postoperative follow-ups included regular radiological scans and blood testing. Any new lesion suggesting a recurrence of the initial dCCA was categorized as postoperative recurrence and diagnosed using clinical assessment, which included computed tomography, magnetic resonance imaging, and bone scintigraphy, or by pathology as appropriate. RFS was defined as the period from the original operation to the first reported recurrence and all death. Postoperative OS was calculated from the operation date to the date of death from any cause.

Ethics and informed consent

The Ethics Committee of Beijing Chao-Yang Hospital approved the study protocol (Approval No. 2020-D- 301) and waived the requirement for informed consent for the use of anonymized patient data. This study conforms to the provisions of the Declaration of Helsinki. All information was collected after obtaining written informed consent from the participants.

Statistical analysis

Continuous variables were summarized employing either the mean and standard deviation (SD) or the median and interquartile range (IQR), while categorical variables were tested using Chi-square tests or Fisher’s exact tests. Kaplan–Meier curves were applied to examine survival outcomes with log-rank testing. The Cox proportional hazards model was utilized for both univariate and multivariate studies to uncover independent prognostic variables. A significance level of P < 0.05 was employed. We built nomograms utilizing the independent prognostic variables. The consistency index (C-index), calibration curves, and DCA curves were applied to assess the nomogram's accuracy. Statistical analysis was performed using SPSS (IBM 22.0) and R 4.3.1 software.

Results

Associations between clinicopathological factors and the ALBI score

The study included 177 dCCA patients who experienced aggressive surgery, comprising 105 males and 72 females with an average age of 66 years. A total of 51 patients (28.8%) experienced postoperative complications. Among these complications, biochemical fistula occurred in 19 cases (10.7%), clinically relevant pancreatic fistula was observed in 13 cases (7.3%), and hemorrhage was noted in 7 cases (4.0%). Additionally, abdominal infection was present in 6 cases (3.4%), and disturbance of gastric emptying was found in 6 cases (3.4%).

Patients were classified into two groups based on the best cut-off value of the ROC curve using preoperative ALBI and the 1-year overall survival rate: the Low-ALBI group (ALBI ≤ –1.67, n = 93) and the High-ALBI group (ALBI > − 1.67, n = 84). The area under the ROC curve for ALBI was 0.71, indicating a sensitivity of 60.3% and a specificity of 77.0% (Fig. 1). As demonstrated in Table 1, the preoperative albumin level was significantly greater in the Low-ALBI group, and the total bilirubin and ALBI score were significantly lower compared with the High-ALBI group. There were no significant differences between the two groups in other clinicopathological characteristics.

Fig. 1
figure 1

ROC curves for ALBI in dCCA patients. The ROC curve using preoperative ALBI and the 1-year overall survival rate yielded an area under the curve (AUC) of 0.71 (95% CI = 0.63–0.79; P < 0.001), with an optimal cutoff value of − 1.67

Full size image
Table 1 Demographics and clinicopathological characteristics of dCCA patients
Full size table

Correlation between the ALBI grade and survival outcomes

Among the patients included in this study, the median RFS duration was 22 months, with corresponding RFS rates of 65.6%, 38.9%, and 32.0% at 1, 3, and 5 years, respectively. The median OS duration was 26 months, with OS rates at 1, 3, and 5 years following radical surgery of 80.0%, 35.83%, and 27.5%, respectively. In the Kaplan–Meier analysis of RFS and OS based on the ALBI score, the High-ALBI group displayed significantly improved RFS and OS (P < 0.001) compared to the Low-ALBI group. The median RFS for patients in the High-ALBI and Low-ALBI groups was 14 and 50 months, with corresponding 1-, 3-, and 5-year RFS rates of 55.8%, 23.5%, 11.7%, and 74.2%, 52.1%, 48.4%, respectively (Fig. 2A). The median OS in the two groups was 18 and 38 months, with 1-, 3-, and 5-year OS rates of 68.6%, 20.3%, 10.1%, and 90.2%, 50.1%, 43.1%, respectively (Fig. 2B).

Fig. 2
figure 2

Kaplan–Meier survival curves for RFS and OS in dCCA patients. A Median RFS times in the High-ALBI and Low-ALBI groups were 14 and 50 months, respectively (P < 0.001). B Median OS times in the High-ALBI and Low-ALBI groups were 18 and 38 months, respectively (P < 0.001)

Full size image

Univariate and multivariate analysis of prognostic factors for RFS and OS

In univariate Cox regression, albumin, total bilirubin, ALBI, CA19 - 9, degree of differentiation, lymph node invasion, and portal vein invasion were significant for RFS and OS (P < 0.05). In the multivariate Cox regression of OS, the ALBI (HR: 2.091; 95%CI: 1.294–3.377; P = 0.003), CA19 - 9(HR: 1.655; 95%CI: 1.067–2.569; P = 0.025), degree of differentiation(HR: 1.556; 95%CI: 1.047–2.312; P = 0.029), lymph node invasion (HR: 2.312; 95%CI: 1.562–3.421; P < 0.001), and portal vein invasion (HR: 2.182; 95%CI: 1.293–3.683; P = 0.003) were independent prognostic factors (Table 2).In the multivariate Cox regression of RFS, the ALBI (HR: 2.073; 95%CI: 1.261–3.408; P = 0.004), degree of differentiation(HR: 1.597; 95%CI: 1.056–2.415; P = 0.027), lymph node invasion (HR: 2.700; 95%CI: 1.791–4.070; P < 0.001), and portal vein invasion (HR: 1.800; 95%CI: 1.035–3.128; P = 0.037) were independent prognostic factors (Table 3).

Table 2 Univariable and multivariable analysis of the prognostic factors for RFS
Full size table
Table 3 Univariable and multivariable analysis of the prognostic factors for OS
Full size table

Construction of the prognostic nomogram

Using a multivariable COX regression analysis, we developed nomograms for predicting 1-year, 3-year, and 5-year RFS and OS in dCCA patients (Fig. 3A-B). The RFS nomogram has a C-index value of 0.74, while the OS nomogram's C-index value is 0.75, suggesting their accurate prognostic prediction capability. Calibration curves indicate that the predictions of the 5-year survival probability models for RFS and OS closely correspond with the actual observations (Fig. 4A-B). Furthermore, DCA curves were built to test the prediction ability of the nomograms in comparison to the AJCC TNM stage. The results demonstrated a significantly greater benefit from our model compared to the TNM stage (Fig. 4C-D). Each factor was assigned points based on the nomogram, and the total points were calculated by summing the assigned points for all factors. Patients were classified into low-point and high-point groups according to specified cutoff values in the RFS and OS nomograms (215.4 and 262.3, respectively). Kaplan–Meier survival curves (Fig. 5A-B) demonstrated that patients in the high-point group exhibited markedly superior prognoses compared to those in the low-point group (p < 0.001).

Fig. 3
figure 3

Nomograms developed based on multivariate Cox analysis. A Nomogram for predicting RFS in dCCA patients. B Nomogram for predicting OS in dCCA patients

Full size image
Fig. 4
figure 4

Development of the nomograms for dCCA patients. A Calibration curve for 5-year RFS. B Calibration curve for 5-year OS. C Decision curve analysis (DCA) curve for 5-year RFS. D DCA curve for 5-year OS

Full size image
Fig. 5
figure 5

Kaplan–Meier survival curves for risk groups. A Kaplan–Meier survival curve for RFS in high-point and low-point groups. B Kaplan–Meier survival curve for OS in high-point and low-point groups

Full size image

Discussion

As a malignant tumor emerging from the epithelium distal to the insertion of the cystic duct, dCCA may rapidly infiltrate the biliary tree in a short period, and it’s crucial to treat with dCCA in an early stage [19]. With the advancement of chemotherapy and radiology, radical surgery remains the foundation of curative therapy for dCCA. The surgical excision of dCCA typically involves a pancreaticoduodenectomy and lymphadenectomy of nodes surrounding the common bile duct and porta hepatis [20]. In a large cohort of cholangiocarcinoma patients who had surgical resection, 78% of those with dCCA achieved R0 resection [21]. In addition to surgical details, the preoperative nutritional status and pathological findings significantly impact postoperative complications and the survival outcomes of patients with dCCA after surgery [22].

Due to the anatomical location of the primary tumor, the majority of advanced-stage dCCA patients present at the hospital with obstructive jaundice in a malnourished state. Furthermore, surgery causes an inflammatory response corresponding with the level of surgical trauma, prompting a metabolic stress response. Preoperative nutritional assessment plays a vital role in advising physicians to establish appropriate treatment regimens. While some research has explored some nutritional evaluation tools in dCCA [23,24,25], the effect of ALBI in dCCA still needs more evaluation.

ALBI, a novel nutritional status scoring system, is derived from the values of albumin and total bilirubin. ALBI has a great effect on the prognosis of some malignant tumors [26,27,28]. The result above with in consistent with our study, low-ALBI was an independent prognostic factor in predicting the OS of dCCA patients. Additionally, we observed that patients in Low-ALBI group have a much longer RFS.

As a part of ALBI, albumin was usually defined as a simple yet efficient indication for reflecting the body’s nutritional state, which plays a key role in cancer cell immunological responses. Previous studies have consistently identified serum albumin as a significant prognostic factor in a wide range of malignancies [29, 30]. Furthermore, hypoalbuminemia impairs the systemic immune system while boosting tumor cell growth. Research has demonstrated that reduced serum albumin levels may be induced by pro-inflammatory cytokines, which affect albumin synthesis by hepatocytes [31, 32]. Numerous studies have indicated that low preoperative serum albumin levels are linked to poor OS in patients with intrahepatic and perihilar cholangiocarcinoma [33, 34]. The univariate analysis of albumin in our study also indicates the potential predictive ability of OS and RFS in dCCA.

Hyperbilirubinemia was associated with dysfunction of the liver, kidneys, and immune system, and heightened gut mucosa permeability [35]. Recent studies have indicated a significant correlation between low serum bilirubin levels following biliary drainage and reduced mortality rates [36, 37]. However, despite performing preoperative biliary drainage to reduce total bilirubin levels, full liver function recovery may take 4–6 weeks. From the univariate analysis of our study, a high level of total bilirubin may have a negative effect on the prognosis of dCCA. A retrospective study analyzing 115 perihilar cholangiocarcinoma patients arrived at a similar conclusion. Patients with low preoperative bilirubin levels exhibited significantly superior OS and RFS rates compared to patients with high preoperative bilirubin levels [38].

Apart from the ALBI reflecting the nutritional status of dCCA patients, CA19 - 9 and tumor differentiation represent tumor malignancy from some perspective. Some previous studies have found a relationship between CA19 - 9 and the survival of dCCA [39, 40]. Patients who had poor differentiation tend to have poor overall survival and early recurrence [41,42,43]. Besides, the invasion of the portal vein and lymph node also reflects the malignancy of the tumor and results in a poor prognosis in dCCA patients [44, 45]. We must consider all these nutritional and oncological factors in predicting survival in a more accurate method.

Nomograms have been developed and demonstrated superior accuracy compared to conventional staging systems in predicting prognosis for certain cancers [46, 47]. Therefore, we constructed a prognostic nomogram that integrates nutritional status and oncological factors for patients with dCCA following radical surgery. The nomogram exhibited strong predictive performance for survival, which was verified by the C-index and calibration curve. Comparing the nomogram to the AJCC staging system revealed that the nomogram exhibited superior predictive accuracy and greater clinical utility. Using the scores predicted by the nomogram, patients could be categorized into two groups. The Kaplan–Meier data revealed significant differences in RFS and OS between these two groups. Given the dismal prognosis of the low-points group, patients in this category should receive heightened care. The nomogram can enable clinicians in early prognosis evaluation, guide adjuvant treatment options, and stratify patients based on the anticipated risk score.

The research has several limitations that should be addressed in future research. First, the relatively small sample size from a single-center cohort may limit the generalizability and accuracy of our findings. The results might not fully reflect the broader population of dCCA patients, and larger, multi-center studies are needed to validate these conclusions. Second, due to the limited sample size, we were unable to conduct both internal and external validation of the nomograms. This step is crucial to ensure the robustness and applicability of the predictive model across diverse patient populations. In future studies, we aspire to validate the ALBI score in diverse patient cohorts and utilize these findings to guide the design of future clinical trials.

Conclusion

In conclusion, ALBI was an independent prognostic factor in predicting RFS and OS of dCCA patients after radical surgery. The nomograms based on ALBI can provide reliable, personalized survival prediction for patients with dCCA following radical surgery.

Data availability

All data generated or analyzed during this study are included in this article.

References

  1. Rizvi S, Gores GJ. Pathogenesis, diagnosis, and management of cholangiocarcinoma. Gastroenterology. 2013 Dec;145(6):1215–29. Epub 2013/10/22. https://doiorg.publicaciones.saludcastillayleon.es/10.1053/j.gastro.2013.10.013. Cited in: Pubmed; PMID 24140396.

  2. Nakeeb A, Pitt HA, Sohn TA, Coleman J, Abrams RA, Piantadosi S, Hruban RH, Lillemoe KD, Yeo CJ, Cameron JL. Cholangiocarcinoma. A spectrum of intrahepatic, perihilar, and distal tumors. Ann Surg. 1996 Oct;224(4):463–73; discussion 473–5. Epub 1996/10/01. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/00000658-199610000-00005. Cited in: Pubmed; PMID 8857851.

  3. Khan SA, Tavolari S, Brandi G. Cholangiocarcinoma: Epidemiology and risk factors. Liver Int. 2019 May;39 Suppl 1:19–31. Epub 2019/03/10. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/liv.14095. Cited in: Pubmed; PMID 30851228.

  4. Zhou Y, Liu S, Wu L, Wan T. Survival after surgical resection of distal cholangiocarcinoma: A systematic review and meta-analysis of prognostic factors. Asian J Surg. 2017 Apr;40(2):129–138. Epub 2015/09/05. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.asjsur.2015.07.002. Cited in: Pubmed; PMID 26337377.

  5. Strijker M, Belkouz A, van der Geest LG, van Gulik TM, van Hooft JE, de Meijer VE, Haj Mohammad N, de Reuver PR, Verheij J, de Vos-Geelen J, Wilmink JW, Groot Koerkamp B, Klumpen HJ, Besselink MG, Dutch Pancreatic Cancer G. Treatment and survival of resected and unresected distal cholangiocarcinoma: a nationwide study. Acta Oncol. 2019 Jul;58(7):1048–1055. Epub 2019/03/26. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/0284186X.2019.1590634. Cited in: Pubmed; PMID 30907207.

  6. Rizzo A, Brandi G. BILCAP trial and adjuvant capecitabine in resectable biliary tract cancer: reflections on a standard of care. Expert Rev Gastroenterol Hepatol. 2021 May;15(5):483–485. Epub 2020/12/15. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/17474124.2021.1864325. Cited in: Pubmed; PMID 33307876.

  7. Carloni R, Rizzo A, Ricci AD, Federico AD, De Luca R, Guven DC, Yalcin S, Brandi G. Targeting tumor microenvironment for cholangiocarcinoma: Opportunities for precision medicine. Transl Oncol. 2022 Nov;25:101514. Epub 2022/08/18. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.tranon.2022.101514. Cited in: Pubmed; PMID 35977458.

  8. Rizzo A, Frega G, Ricci AD, Palloni A, Abbati F, S DEL, Deserti M, Tavolari S, Brandi G. Anti-EGFR Monoclonal Antibodies in Advanced Biliary Tract Cancer: A Systematic Review and Meta-analysis. In Vivo. 2020 Mar-Apr;34(2):479–488. Epub 2020/03/01. https://doiorg.publicaciones.saludcastillayleon.es/10.21873/invivo.11798. Cited in: Pubmed; PMID 32111744.

  9. Narimatsu H, Yaguchi YT. The Role of Diet and Nutrition in Cancer: Prevention, Treatment, and Survival. Nutrients. 2022 Aug 14;14(16). Epub 2022/08/27. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/nu14163329. Cited in: Pubmed; PMID 36014835.

  10. Sahin TK, Ayasun R, Rizzo A, Guven DC. Prognostic Value of Neutrophil-to-Eosinophil Ratio (NER) in Cancer: A Systematic Review and Meta-Analysis. Cancers (Basel). 2024 Oct 31;16(21). Epub 2024/11/13. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/cancers16213689. Cited in: Pubmed; PMID 39518127.

  11. Hiraoka A, Kumada T, Michitaka K, Kudo M. Newly Proposed ALBI Grade and ALBI-T Score as Tools for Assessment of Hepatic Function and Prognosis in Hepatocellular Carcinoma Patients. Liver Cancer. 2019 Oct;8(5):312–325. Epub 2019/11/27. https://doiorg.publicaciones.saludcastillayleon.es/10.1159/000494844. Cited in: Pubmed; PMID 31768342.

  12. Matsukane R, Watanabe H, Hata K, Suetsugu K, Tsuji T, Egashira N, Nakanishi Y, Okamoto I, Ieiri I. Prognostic significance of pre-treatment ALBI grade in advanced non-small cell lung cancer receiving immune checkpoint therapy. Sci Rep. 2021 Jul 23;11(1):15057. Epub 2021/07/25. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41598-021-94336-9. Cited in: Pubmed; PMID 34301991.

  13. Tang YY, Zhao YN, Zhang T, Chen ZY, Ma XL. Comprehensive radiomics nomogram for predicting survival of patients with combined hepatocellular carcinoma and cholangiocarcinoma. World J Gastroenterol. 2021 Nov 7;27(41):7173–7189. Epub 2021/12/11. https://doiorg.publicaciones.saludcastillayleon.es/10.3748/wjg.v27.i41.7173. Cited in: Pubmed; PMID 34887636.

  14. Jiang S, Zhao R, Li Y, Han X, Liu Z, Ge W, Dong Y, Han W. Prognosis and nomogram for predicting postoperative survival of duodenal adenocarcinoma: A retrospective study in China and the SEER database. Sci Rep. 2018 May 21;8(1):7940. Epub 2018/05/23. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41598-018-26145-6. Cited in: Pubmed; PMID 29786691.

  15. Liu Q, Li J, Liu F, Yang W, Ding J, Chen W, Wei Y, Li B, Zheng L. A radiomics nomogram for the prediction of overall survival in patients with hepatocellular carcinoma after hepatectomy. Cancer Imaging. 2020 Nov 16;20(1):82. Epub 2020/11/18. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s40644-020-00360-9. Cited in: Pubmed; PMID 33198809.

  16. Johnson PJ, Berhane S, Kagebayashi C, Satomura S, Teng M, Reeves HL, O'Beirne J, Fox R, Skowronska A, Palmer D, Yeo W, Mo F, Lai P, Inarrairaegui M, Chan SL, Sangro B, Miksad R, Tada T, Kumada T, Toyoda H. Assessment of liver function in patients with hepatocellular carcinoma: a new evidence-based approach-the ALBI grade. J Clin Oncol. 2015 Feb 20;33(6):550–8. Epub 2014/12/17. https://doiorg.publicaciones.saludcastillayleon.es/10.1200/JCO.2014.57.9151. Cited in: Pubmed; PMID 25512453.

  17. Elmunzer BJ, Maranki JL, Gomez V, Tavakkoli A, Sauer BG, Limketkai BN, Brennan EA, Attridge EM, Brigham TJ, Wang AY. ACG Clinical Guideline: Diagnosis and Management of Biliary Strictures. Am J Gastroenterol. 2023 Mar 1;118(3):405–426. Epub 2023/03/03. https://doiorg.publicaciones.saludcastillayleon.es/10.14309/ajg.0000000000002190. Cited in: Pubmed; PMID 36863037.

  18. Chiorean EG, Chiaro MD, Tempero MA, Malafa MP, Benson AB, Cardin DB, Christensen JA, Chung V, Czito B, Dillhoff M, Donahue TR, Dotan E, Fountzilas C, Glazer ES, Hardacre J, Hawkins WG, Klute K, Ko AH, Kunstman JW, LoConte N, Lowy AM, Masood A, Moravek C, Nakakura EK, Narang AK, Nardo L, Obando J, Polanco PM, Reddy S, Reyngold M, Scaife C, Shen J, Truty MJ, Vollmer C, Wolff RA, Wolpin BM, Rn BM, Lubin S, Darlow SD. Ampullary Adenocarcinoma, Version 1.2023, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2023 Jul;21(7):753–782. Epub 2023/07/12. https://doiorg.publicaciones.saludcastillayleon.es/10.6004/jnccn.2023.0034. Cited in: Pubmed; PMID 37433437.

  19. Valle JW, Kelley RK, Nervi B, Oh DY, Zhu AX. Biliary tract cancer. Lancet. 2021 Jan 30;397(10272):428–444. Epub 2021/02/01. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/S0140-6736(21)00153-7. Cited in: Pubmed; PMID 33516341.

  20. Dickson PV, Behrman SW. Distal cholangiocarcinoma. Surg Clin North Am. 2014 Apr;94(2):325–42. Epub 2014/04/01. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.suc.2013.12.004. Cited in: Pubmed; PMID 24679424.

  21. DeOliveira ML, Cunningham SC, Cameron JL, Kamangar F, Winter JM, Lillemoe KD, Choti MA, Yeo CJ, Schulick RD. Cholangiocarcinoma: thirty-one-year experience with 564 patients at a single institution. Ann Surg. 2007 May;245(5):755–62. Epub 2007/04/26. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/01.sla.0000251366.62632.d3. Cited in: Pubmed; PMID 17457168.

  22. Ethun CG, Le N, Lopez-Aguiar AG, Pawlik TM, Poultsides G, Tran T, Idrees K, Isom CA, Fields RC, Krasnick BA, Weber SM, Salem A, Martin RCG, Scoggins CR, Shen P, Mogal HD, Schmidt C, Beal E, Hatzaras I, Shenoy R, Russell MC, Maithel SK. Pathologic and Prognostic Implications of Incidental versus Nonincidental Gallbladder Cancer: A 10-Institution Study from the United States Extrahepatic Biliary Malignancy Consortium. Am Surg. 2017 Jul 1;83(7):679–686. Epub 2017/07/26. Cited in: Pubmed; PMID 28738935.

  23. Kim HJ, Kim CY, Hur YH, Koh YS, Kim JC, Kim HJ, Cho CK. Prognostic factors for survival after curative resection of distal cholangiocarcinoma: perineural invasion and lymphovascular invasion. Surg Today. 2014 Oct;44(10):1879–86. Epub 2014/02/19. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00595-014-0846-z. Cited in: Pubmed; PMID 24535697.

  24. Terasaki F, Sugiura T, Okamura Y, Ito T, Yamamoto Y, Ashida R, Ohgi K, Uesaka K. Use of preoperative controlling nutritional status (CONUT) score as a better prognostic marker for distal cholangiocarcinoma after pancreatoduodenectomy. Surg Today. 2021 Mar;51(3):358–365. Epub 2020/08/08. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00595-020-02098-0. Cited in: Pubmed; PMID 32761459.

  25. Kitasato A, Kuroki T. Significance of inflammatory and nutritional markers as prognostic predictors in patients with resected distal cholangiocarcinoma. Asian J Surg. 2021 Dec;44(12):1574–1576. Epub 2021/09/11. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.asjsur.2021.08.021. Cited in: Pubmed; PMID 34503876.

  26. Zhang ZQ, Xiong L, Zhou JJ, Miao XY, Li QL, Wen Y, Zou H. Ability of the ALBI grade to predict posthepatectomy liver failure and long-term survival after liver resection for different BCLC stages of HCC. World J Surg Oncol. 2018 Oct 16;16(1):208. Epub 2018/10/18. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12957-018-1500-9. Cited in: Pubmed; PMID 30326907.

  27. Mao S, Yu X, Shan Y, Fan R, Wu S, Lu C. Albumin-Bilirubin (ALBI) and Monocyte to Lymphocyte Ratio (MLR)-Based Nomogram Model to Predict Tumor Recurrence of AFP-Negative Hepatocellular Carcinoma. J Hepatocell Carcinoma. 2021;8:1355–1365. Epub 2021/11/23. https://doiorg.publicaciones.saludcastillayleon.es/10.2147/JHC.S339707. Cited in: Pubmed; PMID 34805014.

  28. Kudo M. Newly Developed Modified ALBI Grade Shows Better Prognostic and Predictive Value for Hepatocellular Carcinoma. Liver Cancer. 2022 Jan;11(1):1–8. Epub 2022/03/01. https://doiorg.publicaciones.saludcastillayleon.es/10.1159/000521374. Cited in: Pubmed; PMID 35222503.

  29. Wu N, Chen G, Hu H, Pang L, Chen Z. Low pretherapeutic serum albumin as a risk factor for poor outcome in esophageal squamous cell carcinomas. Nutr Cancer. 2015;67(3):481–5. Epub 2015/02/24. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/01635581.2015.1004726. Cited in: Pubmed; PMID 25706773.

  30. Onate-Ocana LF, Aiello-Crocifoglio V, Gallardo-Rincon D, Herrera-Goepfert R, Brom-Valladares R, Carrillo JF, Cervera E, Mohar-Betancourt A. Serum albumin as a significant prognostic factor for patients with gastric carcinoma. Ann Surg Oncol. 2007 Feb;14(2):381–9. Epub 2006/12/13. https://doiorg.publicaciones.saludcastillayleon.es/10.1245/s10434-006-9093-x. Cited in: Pubmed; PMID 17160496.

  31. Peters SJ, Vanhaecke T, Papeleu P, Rogiers V, Haagsman HP, van Norren K. Co-culture of primary rat hepatocytes with rat liver epithelial cells enhances interleukin-6-induced acute-phase protein response. Cell Tissue Res. 2010 Jun;340(3):451–7. Epub 2010/04/23. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00441-010-0955-y. Cited in: Pubmed; PMID 20411395.

  32. Honda H, Qureshi AR, Heimburger O, Barany P, Wang K, Pecoits-Filho R, Stenvinkel P, Lindholm B. Serum albumin, C-reactive protein, interleukin 6, and fetuin a as predictors of malnutrition, cardiovascular disease, and mortality in patients with ESRD. Am J Kidney Dis. 2006 Jan;47(1):139–48. Epub 2005/12/27. https://doiorg.publicaciones.saludcastillayleon.es/10.1053/j.ajkd.2005.09.014. Cited in: Pubmed; PMID 16377395.

  33. Shen J, Wen T, Li C, Yan L, Li B, Yang J. The Prognostic Prediction Role of Preoperative Serum Albumin Level in Patients with Intahepatic Cholangiocarcinoma Following Hepatectomy. Dig Dis. 2018;36(4):306–313. Epub 2018/04/20. https://doiorg.publicaciones.saludcastillayleon.es/10.1159/000487479. Cited in: Pubmed; PMID 29672305.

  34. Waghray A, Sobotka A, Marrero CR, Estfan B, Aucejo F, Narayanan Menon KV. Serum albumin predicts survival in patients with hilar cholangiocarcinoma. Gastroenterol Rep (Oxf). 2017 Feb;5(1):62–66. Epub 2016/07/09. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/gastro/gow021. Cited in: Pubmed; PMID 27389416.

  35. Nagino M, Takada T, Miyazaki M, Miyakawa S, Tsukada K, Kondo S, Furuse J, Saito H, Tsuyuguchi T, Yoshikawa T, Ohta T, Kimura F, Ohta T, Yoshitomi H, Nozawa S, Yoshida M, Wada K, Amano H, Miura F, Japanese Association of Biliary S, Japanese Society of Hepato-Biliary-Pancreatic S, Japan Society of Clinical O. Preoperative biliary drainage for biliary tract and ampullary carcinomas. J Hepatobiliary Pancreat Surg. 2008;15(1):25–30. Epub 2008/02/16. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00534-007-1277-7. Cited in: Pubmed; PMID 18274841.

  36. Abdel Wahab M, Fathy O, Elghwalby N, Sultan A, Elebidy E, Abdalla T, Elshobary M, Mostafa M, Foad A, Kandeel T, Abdel Raouf A, Salah T, Abu Zeid M, Abu Elenein A, Gad Elhak N, ElFiky A, Ezzat F. Resectability and prognostic factors after resection of hilar cholangiocarcinoma. Hepatogastroenterology. 2006 Jan-Feb;53(67):5–10. Epub 2006/03/02. Cited in: Pubmed; PMID 16506367.

  37. Belghiti J, Ogata S. Preoperative optimization of the liver for resection in patients with hilar cholangiocarcinoma. HPB (Oxford). 2005;7(4):252–3. Epub 2008/03/12. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/13651820500372335. Cited in: Pubmed; PMID 18333201.

  38. Li CX, Zhang H, Wang K, Wang X, Li XC. Preoperative Bilirubin Level Predicts Overall Survival and Tumor Recurrence After Resection for Perihilar Cholangiocarcinoma Patients. Cancer Manag Res. 2019;11:10157–10165. Epub 2019/12/11. https://doiorg.publicaciones.saludcastillayleon.es/10.2147/CMAR.S230620. Cited in: Pubmed; PMID 31819648.

  39. Xu S, Zhang XP, Zhao GD, Zhao ZM, Gao YX, Hu MG, Tan XL, Liu R. Development and validation of an online calculator to predict early recurrence and long-term survival in patients with distal cholangiocarcinoma after pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci. 2022 Nov;29(11):1214–1225. Epub 2021/10/23. https://doiorg.publicaciones.saludcastillayleon.es/10.1002/jhbp.1058. Cited in: Pubmed; PMID 34676993.

  40. Sallinen V, Siren J, Makisalo H, Lehtimaki TE, Lantto E, Kokkola A, Nordin A. Differences in Prognostic Factors and Recurrence Patterns After Curative-Intent Resection of Perihilar and Distal Cholangiocarcinomas. Scand J Surg. 2020 Sep;109(3):219–227. Epub 2019/02/23. https://doiorg.publicaciones.saludcastillayleon.es/10.1177/1457496919832150. Cited in: Pubmed; PMID 30791825.

  41. Wellner UF, Shen Y, Keck T, Jin W, Xu Z. The survival outcome and prognostic factors for distal cholangiocarcinoma following surgical resection: a meta-analysis for the 5-year survival. Surg Today. 2017 Mar;47(3):271–279. Epub 2016/05/30. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00595-016-1362-0. Cited in: Pubmed; PMID 27236779.

  42. Andrianello S, Paiella S, Allegrini V, Ramera M, Pulvirenti A, Malleo G, Salvia R, Bassi C. Pancreaticoduodenectomy for distal cholangiocarcinoma: surgical results, prognostic factors, and long-term follow-up. Langenbecks Arch Surg. 2015 Jul;400(5):623–8. Epub 2015/07/03. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00423-015-1320-0. Cited in: Pubmed; PMID 26134446.

  43. Guilbaud T, Girard E, Lemoine C, Schlienger G, Alao O, Risse O, Berdah S, Chirica M, Moutardier V, Birnbaum DJ. Intra-pancreatic distal cholangiocarcinoma and pancreatic ductal adenocarcinoma: a common short and long-term prognosis? Updates Surg. 2021 Apr;73(2):439–450. Epub 2021/01/25. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s13304-021-00981-0. Cited in: Pubmed; PMID 33486711.

  44. Lyu S, Li L, Zhao X, Ren Z, Cao D, He Q. Prognostic impact of lymph node parameters in distal cholangiocarcinoma after pancreaticoduodenectomy. World J Surg Oncol. 2020 Oct 8;18(1):262. Epub 2020/10/10. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12957-020-02040-1. Cited in: Pubmed; PMID 33032609.

  45. Maeta T, Ebata T, Hayashi E, Kawahara T, Mizuno S, Matsumoto N, Ohta S, Nagino M, Nagoya Surgical Oncology G. Pancreatoduodenectomy with portal vein resection for distal cholangiocarcinoma. Br J Surg. 2017 Oct;104(11):1549–1557. Epub 2017/08/08. https://doiorg.publicaciones.saludcastillayleon.es/10.1002/bjs.10596. Cited in: Pubmed; PMID 28782798.

  46. Liu J, Wu P, Lai S, Wang J, Hou H, Zhang Y. Prognostic models for upper urinary tract urothelial carcinoma patients after radical nephroureterectomy based on a novel systemic immune-inflammation score with machine learning. BMC Cancer. 2023 Jun 22;23(1):574. Epub 2023/06/23. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12885-023-11058-z. Cited in: Pubmed; PMID 37349696.

  47. Zhao F, Yang D, He J, Ju X, Ding Y, Li X. Establishment and validation of a prognostic nomogram for extrahepatic cholangiocarcinoma. Front Oncol. 2022;12:1007538. Epub 2022/12/13. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fonc.2022.1007538. Cited in: Pubmed; PMID 36505787.

Download references

Acknowledgements

None.

Funding

None.

Author information

Author notes

  1. Jin-Can Huang and You-Wei Ma contribute equally to this manuscript and share the first authorship.

Authors and Affiliations

  1. Hepatobiliary, Pancreas & Spleen Surgery Department, Beijing Chao-Yang Hospital, Capital Medical University, Beijing, 100020, P. R. China

    Jin-Can Huang, You-Wei Ma, Han-Xuan Wang, Ren Lang & Tao Jiang

Authors
  1. Jin-Can Huang
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. You-Wei Ma
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Han-Xuan Wang
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Ren Lang
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Tao Jiang
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

JC Huang and YW Ma drafted the manuscript and performed the statistical analysis; HX Wang searched articles and collected the data; RL and TJ designed, revised, and guided this study. All authors have read and approved the final manuscript.

Corresponding authors

Correspondence to Ren Lang or Tao Jiang.

Ethics declarations

Ethics approval and consent to participate

This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of Beijing Chao-Yang Hospital (No. 2020-D- 301) and individual consent for this retrospective analysis was waived.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, JC., Ma, YW., Wang, HX. et al. Prognostic impact of albumin-bilirubin score in predicting the long-term survival of distal cholangiocarcinoma after radical surgery. World J Surg Onc 23, 160 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12957-025-03813-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12957-025-03813-2

Keywords

World Journal of Surgical Oncology

ISSN: 1477-7819

Contact us