Zeng D, Wen NY, Wang YQ, Cheng NS, Li B. Prognostic roles nutritional index in patients with resectable and advanced biliary tract cancers. World J Gastroenterol 2025; 31(6): 97697 [DOI: 10.3748/wjg.v31.i6.97697]
Corresponding Author of This Article
Nan-Sheng Cheng, PhD, Division of Biliary Surgery, Department of General Surgery, West China Hospital, Sichuan University, No. 37 Guoxue Alley, Wuhou District, Chengdu 610041, Sichuan Province, China. nanshengcheng@yeah.net
Research Domain of This Article
Geriatrics & Gerontology
Article-Type of This Article
Systematic Reviews
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Di Zeng, Ning-Yuan Wen, Yao-Qun Wang, Nan-Sheng Cheng, Bei Li, Division of Biliary Surgery, Department of General Surgery, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
Di Zeng, Ning-Yuan Wen, Yao-Qun Wang, Nan-Sheng Cheng, Bei Li, Research Center for Biliary Diseases, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
Author contributions: Zeng D conceptualized and designed the research; curated and analyzed the data; developed the methodology; conducted investigations; prepared the original draft; and led the review and editing of the manuscript; Wen NY contributed to the conceptualization, formal analysis, and investigation, as well as the critical review and editing of the manuscript; Wang YQ was involved in investigations and contributed to the critical review and editing of the manuscript; Li B provided essential methodological support, supervised the project, and contributed to the manuscript review; Cheng NS secured funding for the research, supervised the entire project, and contributed to the manuscript review. Both Li B and Cheng NS have made critical and indispensable contributions as co-corresponding authors. Li B provided vital support in methodological design, supervised the research process, and ensured the scientific rigor of the manuscript. Cheng NS played a pivotal role in overseeing the project's progression, securing funding, interpreting results, and revising the manuscript. Their collaboration was instrumental in shaping the manuscript and bringing it to publication.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
PRISMA 2009 Checklist statement: The authors have read the PRISMA 2009 Checklist, and the manuscript was prepared and revised according to the PRISMA 2009 Checklist.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Nan-Sheng Cheng, PhD, Division of Biliary Surgery, Department of General Surgery, West China Hospital, Sichuan University, No. 37 Guoxue Alley, Wuhou District, Chengdu 610041, Sichuan Province, China. nanshengcheng@yeah.net
Received: June 5, 2024 Revised: October 24, 2024 Accepted: December 16, 2024 Published online: February 14, 2025 Processing time: 218 Days and 20.9 Hours
Abstract
BACKGROUND
Biliary tract cancer (BTC) is a rare, aggressive malignancy with increasing incidence and poor prognosis. Identifying preoperative prognostic factors is crucial for effective risk-benefit assessments and patient stratification. The prognostic nutritional index (PNI), which reflects immune-inflammatory and nutritional status, has shown prognostic value in various cancers, but its significance in BTC remains unclear.
AIM
To assess the prognostic value of the preoperative PNI in BTC patients, with a focus on overall survival (OS) and disease-free survival (DFS).
METHODS
Comprehensive searches were conducted in the PubMed, EMBASE, and Web of Science databases from inception to April 2024. The primary outcomes of interest focused on the associations between the preoperative PNI and the prognosis of BTC patients, specifically OS and disease-free survival (DFS). Statistical analyses were conducted via STATA 17.0 software.
RESULTS
Seventeen studies encompassing 4645 patients met the inclusion criteria. Meta-analysis revealed that a low PNI was significantly associated with poorer OS [hazard ratio (HR) 1.91, 95%CI: 1.59-2.29; P < 0.001] and DFS (HR 1.93, 95%CI: 1.39-2.67; P < 0.001). Subgroup analyses revealed consistent results across BTC subtypes (cholangiocarcinoma and gallbladder cancer) and stages (resectable and advanced). Sensitivity analyses confirmed the robustness of these findings, and no significant publication bias was detected.
CONCLUSION
This study demonstrated that a low preoperative PNI predicts poor OS and DFS in BTC patients, highlighting its potential as a valuable prognostic tool. Further prospective studies are needed to validate these findings and enhance BTC patient management.
Core Tip: Preoperative prognostic nutritional index (PNI) serves as a valuable prognostic tool for patients with biliary tract cancer (BTC). Our meta-analysis, comprising 17 studies and 4645 patients, reveals that low preoperative PNI significantly correlates with poorer overall survival and disease-free survival in BTC patients, irrespective of subtype or stage. These findings underscore the importance of incorporating PNI assessment into preoperative evaluations for effective risk stratification and personalized treatment strategies in BTC. Further prospective studies are warranted to validate these results and optimize patient management approaches.
Citation: Zeng D, Wen NY, Wang YQ, Cheng NS, Li B. Prognostic roles nutritional index in patients with resectable and advanced biliary tract cancers. World J Gastroenterol 2025; 31(6): 97697
Biliary tract cancer (BTC), which includes gallbladder carcinoma, intrahepatic cholangiocarcinoma (CCA), perihilar CCA, distal CCA, and ampullary carcinoma, is a rare and aggressive malignancy[1]. The incidence of BTC has been increasing in recent decades[2]. Although complete surgical resection remains the only curative treatment for BTC[3], the majority of patients are diagnosed too late for this option because of the nonspecific nature of early-stage symptoms[4]. Despite advancements in surgical techniques and adjuvant chemotherapy, the prognosis for BTC patients remains poor[5]. The challenges in early detection are compounded by the high rates of local and distant recurrence, even after surgical resection with negative margins. Consequently, the prognosis for advanced BTC is particularly poor, with a five-year overall survival (OS) rate of only approximately 5%[6]. Therefore, identifying preoperative prognostic factors is essential for conducting more effective risk-benefit assessments and facilitating patient stratification for precision medicine[7]. Establishing reliable prognostic biomarkers is crucial not only for improving surgical planning but also for tailoring treatment strategies on the basis of individual risk levels, thereby increasing patient outcomes. Therefore, new predictive biomarkers are urgently needed.
Malnutrition is a common issue among cancer patients and significantly impacts disease progression and treatment outcomes, particularly in patients with BTC[8]. Patients with BTC often experience severe nutritional deficiencies due to tumor-induced metabolic changes and treatment-related side effects. These deficiencies can compromise immune function, leading to increased infection rates, prolonged hospital stays, elevated risk of complications, and a greater likelihood of mortality[9]. Despite the recognition of these challenges, the relationship between nutritional status and prognosis in BTC remains unclear, highlighting a critical gap in current research[10]. The prognostic nutritional index (PNI), a multiparametric indicator based on the serum albumin (ALB) concentration and peripheral lymphocyte count, has been shown to reflect both immune-inflammatory and nutritional status[11]. Although the PNI has been associated with prognosis in various gastrointestinal cancers, its specific prognostic significance in BTC remains underexplored[12-14]. Therefore, understanding the role of PNI in BTC could provide insights into the management of these patients and underscore the necessity for targeted interventions to improve nutritional status and clinical outcomes.
In this study, we focused on assessing the prognostic significance of the preoperative PNI in patients with resectable and advanced BTCs. Although many primary studies have reported associations between the PNI and the prognosis of BTC[15], high-level evidence, such as meta-analyses that can be used to systematically review and consolidate the evidence for the prognostic value of the PNI in BTC, is lacking. This work is the first comprehensive meta-analysis to investigate the prognostic value of the preoperative PNI in BTC, offering valuable insights for prognostic prediction in these patients.
MATERIALS AND METHODS
Literature search
This systematic review was prospectively registered in the International Prospective Register of Systematic Reviews under the ID CRD42024534979 and adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Two independent reviewers, Zeng D and Wen NY, systematically searched PubMed, EMBASE, and Web of Science from inception to April 2024, limiting the results to English-language publications. Any discrepancies between Zeng D and Wen NY were resolved through consultation with a third reviewer, Wang YQ, to achieve consensus.
Inclusion and exclusion criteria
Inclusion criteria: Patients diagnosed with BTC through pathological examination.
Studies were eligible for inclusion if they examined the correlation of preoperative biomarkers, such as the PNI, with patient outcomes in terms of prognosis.
The studies furnished hazard ratios (HR) alongside their respective 95%CI, elucidating the influence of the preoperative biomarker PNI on patient OS and disease-free survival (DFS).
Exclusion criteria: Patients pathologically diagnosed with benign or borderline BTC or other gastrointestinal tumors were excluded.
Studies that did not assess at least one of the following preoperative biomarkers – PNI - were excluded.
Studies lacking sufficient data, including those without reported postoperative survival times or essential statistics such as HR, odds ratios (OR), or relative risks, were excluded from the analysis.
Statistical analysis
Survival data were analyzed using HRs and their corresponding 95%CI through multivariate regression analysis, whereas categorical variables were assessed using ORs. Statistical heterogeneity was evaluated using Cochrane’s Q-test and I2 statistics, with thresholds for low, moderate, and high heterogeneity set to 25%, 50%, and 75%, respectively. Regardless of the heterogeneity level, a random-effects model was employed for the analysis.
Subsequent subgroup analyses were performed to explore potential sources of heterogeneity, including the specific types of BTC [CCA and gallbladder cancer (GBC)], as well as the progression stages of BTC, specifically analyzing advanced BTC and resectable BTC separately. P < 0.05 was considered to indicate a significant difference. Publication bias was assessed using funnel plots and Egger’s test. All statistical analyses were conducted using STATA 17.0 software.
Quality assessment of studies
Two independent investigators, Zeng D and Wen NY, assessed the quality of the included studies via the Newcastle-Ottawa Scale (NOS), evaluating criteria such as case selection, cohort comparability, and exposure risk assessment. Only studies that achieved a score of six or higher on the NOS were included in the final meta-analysis.
RESULTS
Literature search
From an initial pool of 1866 articles retrieved from electronic databases (PubMed, EMBASE, and Web of Science), duplicates and unrelated studies were excluded, leaving 268 full-text articles for eligibility review. After a detailed evaluation, 17 studies met the inclusion criteria for qualitative analysis. The main characteristics of these studies are summarized in Table 1. The PRISMA flow diagram outlining the article selection process is presented in Figure 1.
The meta-analysis encompassed data from 4645 patients with biliary cancers, derived from studies published between 2016 and 2024. Among these, 15 studies investigated the relationship between the PNI and OS, while 4 examined its connection to DFS. Regarding cancer subtypes, 5 studies focused on BTC, 9 on CCA, and 3 on GBC. The quality of the studies, as assessed by the NOS, ranged from 7 to 9, indicating a generally high methodological quality (Table 2).
Table 2 Results of quality assessment using the Newcastle-Ottawa Scale for cohort studies.
Ref.
Selection
Comparability
Outcome
NOS score
Representativeness of the exposed cohort
Selection of the non-exposed cohort
Ascertainment of exposure
Demonstration that outcome of interest was not present at start of study
Comparability of cohorts based on the design or analysis
Association between the PNI and OS of BTC patients
Seventeen studies explored the link between PNI and OS in patients with BTC. Of these, 13 studies reported that a reduced PNI was independently correlated with worse OS, whereas 4 studies found no significant impact of PNI on OS. A pooled analysis of all 17 studies showed that PNI values below the cutoff were associated with worse OS (HR 1.91, 95%CI: 1.59-2.29, P < 0.001). However, some heterogeneity was detected among the studies (I2 = 55.2%; Figure 2A).
Figure 2 Impact of a prognostic nutritional index below the cutoff value.
A: On overall survival; B: On disease-free survival. HR: Hazard ratio.
Correlation between the PNI and DFS of BTC patients
Four studies were included in the analysis of the association between the PNI and DFS prognosis in BTC. Among these, three studies identified a significant association between low PNI and poorer DFS, while one study did not observe a significant effect. The pooled analysis of the four studies indicated that lower PNI values were predictive of worse DFS outcomes (HR 1.93, 95%CI: 1.39-2.67, P < 0.001), with no heterogeneity detected (I² = 0%; Figure 2B).
Subgroup analysis based on major categories of BTC: CCA and GBC
Five studies evaluated BTC without distinguishing between CCA and GBC. Their findings indicated that patients with lower PNI thresholds experienced significantly worse OS (HR: 2.72, 95%CI: 1.97-3.76, P < 0.001; Figure 3A), with no heterogeneity detected across the studies (I2 = 0%).
Figure 3 Impact of a prognostic nutritional index below the cutoff value on overall survival in biliary tract cancers.
A: Impact of a prognostic nutritional index (PNI) below the cutoff value on overall survival in patients with biliary tract cancer [including cholangiocarcinoma (CCA) and gallbladder cancer (GBC) patients]; B: Impact of the PNI cutoff value on overall survival in patients with CCA; C: Impact of a PNI below the cutoff value on overall survival in patients with GBC. HR: Hazard ratio.
For nine studies focusing on CCA, the combined results highlighted a clear association between decreased PNI levels and shorter OS, showing a hazard ratio of 1.54 (95%CI: 1.32-1.81, P < 0.001; Figure 3B). Minimal heterogeneity was observed among these studies (I2 = 10.9%).
Similarly, three studies examined GBC, where the pooled analysis revealed a strong connection between low PNI measures and less favorable OS outcomes, yielding a hazard ratio of 2.25 (95%CI: 1.36-3.72, P < 0.001; Figure 3C). These studies demonstrated low heterogeneity (I2 = 21.2%).
Subgroup analysis on tumor resectability
Among the 17 included studies, 14 studies focused on BTC limited to resectable cases, whereas the remaining 3 studies examined BTC at the advanced stage with unresectable cases. In all studies targeting resectable cases, the pooled analysis revealed that PNI values below the defined cutoff were predictive of poorer OS, with an HR of 1.84 (95%CI: 1.52-2.24, P < 0.001; Figure 4A). For the 3 studies examining BTC at the advanced stage, the pooled analysis revealed that PNI values below the defined cutoff were predictive of poorer OS, yielding an HR of 2.25 (95%CI: 1.36-3.72, P = 0.001; Figure 4B). We have summarized the key findings of the results in Figure 5.
Figure 4 Impact of a prognostic nutritional index on overall survival in gallbladder cancer.
A: Impact of a prognostic nutritional index (PNI) below the cutoff value on overall survival in patients with resectable gallbladder cancer (GBC); B: Impact of a PNI below the cutoff value on overall survival in advanced GBC patients. HR: Hazard ratio.
In sensitivity analyses, we rigorously applied a random-effects model to methodically exclude each study, thus confirming the robustness of PNI's prognostic role in OS and DFS among BTC patients. These analyses were conducted using StataMP 17 software (StataCorp. 2022). The findings were further validated by robust sensitivity analyses, reinforcing their consistency and reliability. Detailed results of these sensitivity analyses for each prognostic factor are provided in the Supplementary Figures 1 and 2.
Publication bias
In analyses evaluating the relationship between PNI and OS, the symmetrical funnel plots demonstrated a low likelihood of publication bias. Furthermore, Egger’s regression test confirmed the absence of significant bias (Supplementary Figures 3 and 4).
For studies assessing the connection between PNI and DFS, the funnel plots similarly reflected minimal publication bias. This was further supported by Egger’s regression test, which yielded a non-significant P value of 0.798 (Supplementary Figures 5 and 6).
DISCUSSION
Cancer patients often suffer from malnutrition due to the adverse effects tumors impose on the digestive system[16]. However, the mechanisms behind tumor-induced malnutrition are complex, involving a delicate interplay between the tumor and the host[17]. Consequently, identifying patients at risk of malnutrition and poor prognosis remains a challenging area of study.
Many nutrition and inflammation-based markers, such as the PNI, Controlling Nutritional Status score, systemic inflammation score, and Glasgow prognostic score, have been reported as preoperative prognostic biomarkers in various cancers[18,19]. Among these biomarkers, we are most interested in the PNI, which is calculated based on total lymphocyte counts and serum ALB levels, because a major advantage of the PNI as a reliable prognostic indicator is that it not only directly correlates with ALB levels but also reflects the patient's immune status. Previously, a randomized study demonstrated that comprehensive nutritional support during concurrent radiochemotherapy improves therapeutic efficacy and short-term prognosis in esophageal cancer patients[20]. Additionally, early nutritional and psychological interventions have been shown to reduce mortality by 32% in advanced esophageal cancer patients[21]. Furthermore, studies have consistently shown that a low PNI correlates with shorter OS in various types of cancers[22,23]. However, comprehensive studies that summarize the prognostic significance of the PNI in BTC patients are currently lacking. Supplementing this area with relevant research is also the primary objective of our study.
Our investigation, which included 17 primary sources, revealed that a decrease in the PNI adversely affects both OS and DFS among patients with BTC. Subsequent subgroup analyses examining BTC subtypes (CCA, GBC) and the resectability of BTC provide additional support for our findings. The prognostic value of the PNI in patients with BTC can be understood through several key mechanisms. First, the systemic inflammatory response has been shown to play a significant role in the initiation, invasive growth, and metastasis of cancer[24,25]. The total lymphocyte count, a critical component of the PNI, reflects the immune status of a patient. Lymphocytes, especially tumor-infiltrating lymphocytes (TILs), are crucial elements of the immune microenvironment and consist of CD8+ and CD4+ cells[26]. These TILs induce cancer cell apoptosis and inhibit cancer cell proliferation. Therefore, lymphocytes play essential roles in cell-mediated antitumor immune reactions and tumor immunological surveillance by inducing cancer cell apoptosis and inhibiting cancer cell proliferation[27]. Low lymphocyte counts result in poor immunological responses within the tumor microenvironment, leading to cancer progression. In addition to the lymphocyte count, the serum ALB level in the PNI is indicative of a patient's nutritional status. Malnutrition is common among cancer patients, with approximately 40% to 80% of these patients experiencing malnutrition during their disease course[28]. Low serum ALB levels are associated with malnutrition and weight loss, which negatively impact the survival and recovery of cancer patients. Consequently, low ALB levels often predict poor prognosis in cancer patients[28]. Taken together, a low PNI, reflecting both compromised immune function and poor nutritional status, is correlated with unfavorable long-term survival in BTC patients. Furthermore, a low PNI may result from lymphopenia, indicating that immune system impairment and inhibition are associated with poor survival outcomes in cancer patients[24]. In summary, the mechanisms underlying the prognostic value of the PNI in BTC involve both immune function and nutritional status. Low lymphocyte counts and low serum ALB levels contribute to poor immunological responses and malnutrition, respectively, leading to unfavorable survival outcomes. Thus, the PNI serves as a reliable prognostic indicator for long-term survival in BTC patients. To further investigate the biological mechanisms by which nutritional and immune status, as reflected in the PNI, influences BTC progression, future studies should focus on identifying pathways linking these factors to tumor behavior and patient outcomes. Specifically, research could explore how interventions aimed at improving the PNI - such as nutritional support, immunonutrition, and physical rehabilitation - affect systemic inflammation and the immune response. This understanding will further our knowledge of BTC progression and inform clinical practices that integrate the PNI as a critical marker for managing this aggressive malignancy. Future studies should consider combining the PNI with other biomarkers, such as inflammatory markers and genetic profiles, to provide a more comprehensive prognostic assessment. Research has explored the prognostic value of inflammatory markers in resectable BTC, and this multifaceted approach may enhance risk stratification and personalized therapeutic strategies.
The clinical significance of our research lies in the early prediction of poor prognosis, which can effectively inform preoperative or intraoperative individualized surgical plans. This value has been validated by experienced scholars in the field[29]. As mentioned above, a low PNI often indicates systemic inflammation and progressive nutritional decline, leading to poorer survival outcomes. Perioperative nutritional support is recommended to increase the nutritional status of patients with hepatobiliary pancreatic carcinoma, a group with a high prevalence of malnutrition[30]. Preoperative immunonutrition has been shown to attenuate the perioperative inflammatory response[31]. Consequently, administering immunonutrition to patients with a low PNI is promising for improving their prognosis. Further studies are warranted to explore the relationship between immunonutrition and this inflammation-based prognostic score, thus refining the management of patients with BTC and a low PNI. To improve the PNI and potentially increase survival in BTC patients, specific preoperative interventions could be tested. These interventions may include comprehensive nutritional support, such as high-protein, high-calorie diets, and immunonutrition, which utilize specific nutrients to increase immune function and reduce inflammation. Additionally, prehabilitation exercise programs aimed at improving fitness and muscle mass could improve nutritional status, whereas anti-inflammatory treatments might help mitigate systemic inflammation. Psychological support could also play a role in reducing stress-related immune suppression. Collectively, these targeted strategies have the potential to improve PNI and overall patient outcomes.
In our analysis, three primary limitations merit consideration. Firstly, the retrospective design of all collected studies may inherently introduce selection bias into the reported findings. Secondly, the inconsistency in PNI threshold values, despite approximately 67% clustering between 42 and 46, could partially account for heterogeneity across studies. Additionally, the predominance of studies conducted in Asian populations restricts the applicability of the findings to broader, diverse populations. Consequently, well-designed, large-scale prospective cohort studies are essential to confirm the independent prognostic role of PNI in BTC. Future studies should also focus on validating the PNI as a universal prognostic marker across various subtypes of BTC. Given the variability in PNI cutoff values and the predominance of studies conducted in Asian populations, establishing the significance of the PNI in diverse populations is essential to help standardize the PNI as a reliable prognostic tool applicable to a broader range of BTC patients. This meta-analysis represents the first comprehensive investigation of the prognostic value of the preoperative PNI in patients with BTC, providing invaluable insights for prognostic prediction in these patients.
CONCLUSION
To summarize, this meta-analysis demonstrated a significant correlation between low pretreatment PNI and reduced OS and DFS among BTC patients. Consequently, PNI emerges as a valuable adjunct for prognostic assessment and high-risk patient identification in BTC. Nevertheless, given the existing limitations, additional well-designed prospective studies are warranted to confirm the validity of our findings.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B, Grade B, Grade C
Novelty: Grade B, Grade B, Grade C
Creativity or Innovation: Grade B, Grade B, Grade C
Scientific Significance: Grade B, Grade B, Grade B
P-Reviewer: Rehman R; Wang P; Xing Y S-Editor: Li L L-Editor: A P-Editor: Zheng XM
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