Guo XY, Zhang JZ, Guo T, Huang XR, Zhu DS, Zhang Z, Zheng H, Yu YH, Zhang ZW. Textbook outcome as a predictor of long-term prognosis in ampullary cancer: A retrospective cohort study. World J Gastroenterol 2026; 32(48): 122776 [DOI: 10.3748/wjg.122776]
Corresponding Author of This Article
Zhi-Wei Zhang, Division of Hepato-Pancreato-Biliary Surgery, Tongji Hospital, Tongji Medical College of Huazhong University of Science and Technology, No. 1095 Jiefang Avenue, Wuhan 430000, Hubei Province, China. zhiweizhang@tjh.tjmu.edu.cn
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Gastroenterology & Hepatology
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research-article
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Xin-Yi Guo, Jing-Zhao Zhang, Tong Guo, Xiao-Rui Huang, Deng-Sheng Zhu, Zhen Zhang, Huan Zheng, Ya-Hong Yu, Zhi-Wei Zhang, Division of Hepato-Pancreato-Biliary Surgery, Tongji Hospital, Tongji Medical College of Huazhong University of Science and Technology, Wuhan 430000, Hubei Province, China
Co-corresponding authors: Ya-Hong Yu and Zhi-Wei Zhang.
Author contributions: Zhang ZW, Yu YH, and Guo XY contributed to the conceptualization; Zhang JZ and Huang XR participated in the methodology of the manuscript and the formal analysis; Guo XY was involved in data curation, and contributed to writing original draft; Zheng H, Zhang Z, and Zhu DS contributed to the investigation; Zhang ZW and Yu YH took part in supervision as co-corresponding authors; Zhang ZW and Guo T contributed to funding acquisition. All authors have read and approved the final manuscript.
AI contribution statement: AI tools (specifically ChatGPT) was used solely for linguistic refinement, grammar checking, and formatting assistance during manuscript preparation. No AI tool was used to generate research data, perform statistical analyses, interpret results, or formulate scientific conclusions. All AI-assisted outputs were critically reviewed, verified, and revised by the authors, who take full responsibility for the final content of the manuscript.
Institutional review board statement: The study was reviewed and approved by the Tongji Hospital Institutional Review Board, No. TJ-IRB202510069.
Informed consent statement: As the study used only retrospectively collected, de-identified clinical data and involved no additional interventions, the requirement for written informed consent was waived by the Ethics Committee in accordance with Chinese legislation.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
STROBE statement: The authors have read the STROBE Statement-checklist of items, and the manuscript was prepared and revised according to the STROBE Statement-checklist of items.
Data sharing statement: The data underlying this article will be shared on reasonable request to the corresponding author.
Corresponding author: Zhi-Wei Zhang, Division of Hepato-Pancreato-Biliary Surgery, Tongji Hospital, Tongji Medical College of Huazhong University of Science and Technology, No. 1095 Jiefang Avenue, Wuhan 430000, Hubei Province, China. zhiweizhang@tjh.tjmu.edu.cn
Received: April 28, 2026 Revised: June 18, 2026 Accepted: June 29, 2026 Published online: December 28, 2026 Processing time: 189 Days and 20 Hours
Abstract
BACKGROUND
Ampullary cancer (AC) is a rare gastrointestinal malignancy originating from the ampulla of Vater, and pancreaticoduodenectomy (PD) represents the standard curative treatment. Given the low incidence of this disease, the determinants of long-term survival have not been fully characterized. Textbook outcome (TO), a composite metric of perioperative treatment quality, has emerged as an important benchmark for assessing postoperative outcomes. However, whether TO achievement is associated with long-term oncological prognosis in AC patients undergoing PD remains elusive.
AIM
To evaluate the rate of TO achievement and its prognostic value for long-term survival outcomes in AC patients undergoing PD.
METHODS
This retrospective cohort study consecutively enrolled 347 patients with AC who underwent PD at Tongji Hospital between January 2012 and December 2022. Survival outcomes were analyzed using Kaplan-Meier curves. Cox proportional hazards models were applied to assess the association between TO achievement and overall survival (OS) as well as disease-free survival (DFS). In addition, 1:1 propensity score matching was performed to compare differences in TO achievement rates between laparoscopic and open PD.
RESULTS
Among 347 patients with AC who underwent PD, 230 (66.3%) achieved TO. The component with the lowest achievement rate was “absence of severe complications (Clavien-Dindo ≥ III)” (84.1%). The median OS was 64.2 months [95% confidence interval (CI): 50.5-93.9], and the median DFS was 44.3 months (95%CI: 33.9-57.9). Recurrence occurred in 119 patients (34.2%). The superior mesenteric artery nodal region was the most common site of locoregional recurrence, whereas the liver was the predominant site of distant metastasis. TO achievement was associated with better OS (hazard ratio = 0.61, 95%CI: 0.44-0.84, P = 0.002) and showed a borderline association with improved DFS (hazard ratio = 0.75, 95%CI: 0.56-0.99, P = 0.044). Advanced T/N stage, perineural invasion, elevated carbohydrate antigen 19-9 (> 37 U/mL), and positive surgical margins were independently associated with worse OS and DFS, while poor tumor differentiation independently predicted worse OS. No statistically significant difference in TO achievement was observed between laparoscopic and open PD after propensity score matching.
CONCLUSION
In patients with AC undergoing PD, TO achievement reflects optimal perioperative care and is associated with improved long-term outcomes. Given its dual value in quality assessment and prognostic stratification, improving TO achievement rates should be considered a key target for surgical quality improvement in PD.
Core Tip: This retrospective cohort study of 347 patients with ampullary cancer demonstrated that achieving textbook outcome (TO) following pancreaticoduodenectomy was associated with improved long-term survival. Additionally, propensity score matching revealed no statistically significant difference in TO achievement between the laparoscopic and open approaches. Given its dual value as both a comprehensive perioperative quality metric and long-term prognostic indicator, enhancing TO achievement rates should be prioritized as a central objective in pancreaticoduodenectomy-specific quality improvement initiatives.
Citation: Guo XY, Zhang JZ, Guo T, Huang XR, Zhu DS, Zhang Z, Zheng H, Yu YH, Zhang ZW. Textbook outcome as a predictor of long-term prognosis in ampullary cancer: A retrospective cohort study. World J Gastroenterol 2026; 32(48): 122776
Ampullary cancer (AC), originating from the ampulla of Vater, represents a distinct subtype among periampullary cancers. Despite accounting for only 0.2%-0.5% of all gastrointestinal cancers and 7% of all periampullary cancers, its unique anatomical location and biological behavior confer substantial clinical importance[1,2]. Radical resection remains the only potentially curative treatment, with pancreaticoduodenectomy (PD) representing the standard surgical approach[3]. Compared with pancreatic head carcinoma and distal cholangiocarcinoma, AC typically presents with early obstructive jaundice due to its anatomical location, facilitating diagnosis at earlier stages and resulting in higher resection rates, as well as improved overall survival (OS)[4,5]. However, due to the rarity of AC, research on determinants of long-term survival remains limited, particularly regarding the impact of perioperative treatment quality on oncological outcomes, which has yet to be fully elucidated.
Textbook outcome (TO), a composite measure of perioperative treatment quality, has emerged as a critical benchmark in surgical oncology. Unlike conventional single-endpoint assessments, TO integrates multiple dimensions of optimal recovery[6]. In 2020, the Dutch Pancreatic Cancer Group (DPCG) established a standardized definition of TO in the field of pancreatic surgery based on international expert consensus[7]. This definition primarily applied to quality assessment for PD and distal pancreatectomy. Despite heterogeneous definitions across surgical subspecialties, current evidence indicates that TO achievement reflects optimal short-term postoperative recovery and is associated with improved long-term survival in patients with gallbladder, esophageal, gastric, and hepatocellular malignancies[8-11]. However, in PD, a hallmark procedure of pancreatic surgery, the relationship between TO achievement and long-term oncological outcomes remains incompletely characterized. Particularly for AC, whether TO predicts long-term survival remains to be established. Therefore, this study evaluated the association between TO achievement and long-term oncological outcomes in patients with AC undergoing PD, aiming to provide novel evidence to inform postoperative management and risk stratification.
MATERIALS AND METHODS
Patients and design
This retrospective cohort study included consecutive patients who underwent PD between January 1, 2012, and December 31, 2022, identified from a continuously maintained pancreatic surgery database. Inclusion criteria were: (1) Curative-intent PD; (2) Histopathological confirmation of AC; and (3) Availability of complete clinical, pathological, and follow-up data. Exclusion criteria were: (1) Synchronous primary malignancies at other sites; and (2) Intraoperative conversion from laparoscopic to open approach. Ultimately, 347 patients were included. Pathological staging was determined according to the 8th edition of the TNM staging system of the American Joint Committee on Cancer. The study was reviewed and approved by the Tongji Hospital Institutional Review Board, No. TJ-IRB202510069.
Definition of TO
Postoperative complications following PD, including postpancreatectomy hemorrhage (PPH)[12], postoperative pancreatic fistula (POPF)[13], and bile leak (BL)[14], were defined according to the consensus criteria of the International Study Group of Pancreatic Surgery (ISGPS) and the International Study Group of Liver Surgery. Postoperative complications were graded according to the Clavien-Dindo grading system into mild (grades I-II) and severe (grade ≥ III)[15]. TO was defined, following the 2020 DPCG consensus, as the absence of POPF (ISGPS grade B/C), PPH (ISGPS grade B/C), and BL (International Study Group of Liver Surgery grade B/C), severe complications (Clavien-Dindo ≥ III), in-hospital or 30-day mortality, and readmission within 30 days after discharge[16].
Data collection
Data were extracted from a continuously maintained pancreatic surgery database using a standardized case report form. The following variables were collected: Demographic characteristics [age, sex, body mass index (BMI)]; tumor-related variables (serum tumor markers, tumor size, differentiation, perineural invasion, TNM stage); preoperative variables (preoperative biliary drainage, percutaneous transhepatic cholangiography and drainage, endoscopic nasobiliary drainage, preoperative endoscopic ultrasonography, preoperative imaging features); intraoperative variables (surgical approach, operative time, estimated blood loss, pancreatic texture, method of pancreaticojejunostomy, margin status, concomitant organ resection); and postoperative outcomes (postoperative nasogastric tube removal, first oral food intake, and first off-bed activity; POPF, BL, PPH, complications of Clavien-Dindo grade ≥ III, in-hospital or 30-day mortality, and readmission within 30 days after discharge).
Follow-up
In the continuously maintained pancreatic surgery database, all patients with AC were followed according to a standardized postoperative follow-up protocol through scheduled outpatient visits or telephone interviews. Patients were followed up every 6 months during the first 2 years and annually thereafter for up to 5 years. Evaluations included physical examination, serum tumor markers [carcinoembryonic antigen (CEA) and carbohydrate antigen 19-9 (CA19-9)], and non-contrast chest and abdominal computed tomography (CT). For patients with abnormal findings during routine follow-up, including suspicious imaging findings, abnormally elevated tumor markers, or recurrence-related symptoms, contrast-enhanced CT was further required to confirm the suspected lesions. For patients who did not complete outpatient follow-up, telephone contact was initiated to confirm survival status. Survival data were obtained from electronic medical records or telephone follow-up records; in cases of discrepant information, the final determination was made after independent review by two investigators.
Outcomes
The primary objective was to evaluate the association between TO achievement and OS as well as disease-free survival (DFS). Secondary objectives included assessing the TO achievement rate and its temporal trends, as well as exploring the impact of laparoscopic vs open surgery on TO achievement. OS was defined as the time from the date of surgery to death from any cause or the date of last follow-up. DFS was defined as the interval from surgery to first documented recurrence or death, whichever occurred first. Local recurrence was defined as recurrence confined to the surgical bed and the adjacent regional lymph node stations (12, 13, 14, and 17), whereas recurrence involving non-regional lymph nodes or distant organs was classified as distant metastasis[17].
Statistical analysis
All variables included in the final analytical dataset were complete, with no missing values identified. Therefore, no imputation was performed. Statistical analyses were conducted using R (version 4.3.1). Continuous variables following a normal distribution were summarized as mean ± SD and were analyzed using independent samples t tests. Continuous variables with a non-normal distribution were presented as median with interquartile range (IQR) and compared using Mann-Whitney U or Kruskal-Wallis tests, as appropriate. Categorical variables were reported as n (%), and compared using Pearson’s χ2 or Fisher’s exact test, as appropriate. CA19-9 and CEA were dichotomized at 37 U/mL and 5 ng/mL, respectively, according to commonly used clinical reference thresholds[18].
Survival outcomes were estimated using Kaplan-Meier (KM) curves, and between-group differences were assessed by the log-rank test. Univariable and multivariable Cox proportional hazards regression models were used to evaluate prognostic factors for OS and DFS, with hazard ratios (HRs) and 95% confidence intervals (CIs) reported. Variables with P < 0.05 in univariable analyses, as well as clinically relevant variables, were included in the multivariable Cox regression models. To avoid collinearity, TNM stage and its components (T and N stages) were not entered simultaneously into the same multivariable model. T and N stages were included as separate covariates in the primary models, whereas a sensitivity analysis was performed by substituting them with TNM stage. The proportional hazards assumption was assessed using Schoenfeld residuals. Given the long recruitment period of the study, temporal sensitivity analysis was performed to evaluate the robustness of the results. The results of all sensitivity analyses and Schoenfeld residual tests were presented in Supplementary Tables 1-4.
The Cochran-Armitage trend test was used to evaluate the temporal trend in the annual TO achievement rate during the study period. The relationship between surgical approach (laparoscopic vs open) and TO achievement was explored using propensity score matching (PSM). Specifically, 1:1 nearest-neighbor matching was performed with a caliper of 0.15 standard deviations to minimize selection bias. Matching covariates included demographics (sex, age, BMI), oncological factors (T stage, N stage, TNM stage, CA19-9, CEA), and past procedural history (previous abdominal surgery, biliary drainage). After matching, covariate balance between groups was assessed using standardized mean differences (SMDs), with SMD < 0.1 indicating adequate balance[19]. All statistical tests were two-sided, and P < 0.05 was considered statistically significant.
RESULTS
Baseline characteristics
The cohort comprised 347 patients (54.5% female) with a median age of 58 years (IQR: 51-64) and BMI of 21.7 kg/m2 (IQR: 20.3-23.6). Previous abdominal surgery was present in 33% of patients. Preoperatively, 35% of patients underwent biliary drainage (30% percutaneous transhepatic cholangiography and drainage, 5% endoscopic nasobiliary drainage), 60% had elevated CA19-9 levels, and 18% had elevated CEA levels. All patients underwent PD (51% open, 49% laparoscopic) after excluding those requiring conversion from laparoscopic to open surgery. Intraoperatively, median operative time was 320 minutes (IQR: 260-390), and median estimated blood loss was 150 mL (IQR: 60-350). Duct-to-mucosa anastomosis was the most commonly used technique of pancreaticojejunostomy (51%). Positive resection margin occurred in 6.1% of patients, and additional organ resection was performed in 3.2%. Regarding tumor characteristics, median tumor size was 2 cm (IQR: 1.5-3.0), with poor tumor differentiation in 33% and perineural invasion in 9.2%.
Significant differences between the TO and non-TO groups were observed only with respect to operative time, method of pancreaticojejunostomy, positive resection margin, postoperative nasogastric tube removal, first oral food intake, and first off-bed activity (all P < 0.05). Detailed comparisons of clinicopathological characteristics between the two groups are presented in Table 1.
Table 1 Baseline characteristics of patients with or without achieving textbook outcome after pancreaticoduodenectomy, n (%)/median (interquartile range).
Among 347 patients with AC, 230 achieved TO (66.3%). To further assess the attainability of TO component, we calculated the achievement rates for the six TO metrics (Figure 1A). The results revealed that “no in-hospital or 30-day mortality” and “no BL” were the most frequently met criteria (both 97.7%). In contrast, “no severe complications (Clavien-Dindo ≥ III)” had the lowest achievement rate (84.1%).
Figure 1 Textbook outcome achievement after pancreaticoduodenectomy for ampullary cancer and annual trends during the study period.
A: Achievement rates of individual textbook outcome components and the overall textbook outcome rate after pancreaticoduodenectomy; B: Annual surgical volume of patients with ampullary cancer undergoing pancreaticoduodenectomy and annual textbook outcome rates from 2012 to 2022; C: Annual number of patients who failed to achieve textbook outcome and the distribution of non-textbook outcome events from 2012 to 2022. POPF: Postoperative pancreatic fistula; PPH: Postpancreatectomy hemorrhage; AC: Ampullary cancer; TO: Textbook outcome.
Between 2012 and 2022, the annual TO rate increased steadily from 58.6% to 77.1% (Figure 1B). The Cochran-Armitage trend test showed that this increasing trend was statistically significant (P for trend = 0.045). During this period, the annual surgical volume for PD in patients with AC remained relatively stable (29-35 cases/year), with the exception of 2021 (25 cases) due to the coronavirus disease 2019 pandemic.
To identify drivers of this improvement, we examined the annual composition of non-TO events (Figure 1C). Severe complications (Clavien-Dindo ≥ III) and POPF consistently constituted the majority of non-TO events throughout the study period, whereas mortality, 30-day readmission, BL, and PPH remained rare. Overall, no individual component exhibited a clear and sustained downward trend over time. Consequently, the improvement in TO was more likely driven primarily by an overall reduction in non-TO events, rather than by the isolated improvement in any single adverse outcome.
OS
For the entire cohort, median follow-up was 54.6 months, and median OS was 64.2 months (95%CI: 50.5-93.9). The 1-, 3-, and 5-year OS rates were 85.5% (95%CI: 81.8%-89.3%), 61.3% (95%CI: 56.1%-67.0%), and 52.7% (95%CI: 47.2%-58.8%), respectively. KM curves demonstrated significantly superior OS in the TO group compared with the non-TO group (P < 0.0001; Figure 2). The 1-, 3-, and 5-year OS rates in the TO group were 90.6% (95%CI: 86.9%-94.5%), 67.4% (95%CI: 61.3%-74.2%), and 59.5% (95%CI: 52.9%-66.9%), respectively; whereas the corresponding rates in the non-TO group were 75.3% (95%CI: 67.8%-83.7%), 49.1% (95%CI: 40.4%-59.7%), and 38.9% (95%CI: 30.2%-50.2%).
Figure 2 Kaplan-Meier curves for overall survival after pancreaticoduodenectomy in patients with ampullary cancer.
A: Overall survival curve for the entire cohort of patients with ampullary cancer (n = 347); B: Overall survival curves stratified by textbook outcome achievement. Survival differences between groups were compared using the log-rank test. The numbers at risk are shown below the plots. TO: Textbook outcome.
Univariable and multivariable analyses for OS are summarized in Table 2. In the univariable analysis, TO achievement, tumor differentiation, T stage, N stage, perineural invasion, elevated CA19-9, and positive resection margins were significantly associated with OS (all P < 0.05). Multivariable analysis revealed that poor tumor differentiation, advanced T stage, advanced N stage, perineural invasion, elevated CA19-9, and positive resection margins were independent risk factors for OS, whereas TO achievement remained independently associated with better OS (HR = 0.61, 95%CI: 0.44-0.84, P = 0.002).In the sensitivity model in which T and N stages were replaced by TNM stage, the association between TO achievement and OS remained materially unchanged (HR = 0.63, 95%CI: 0.46-0.87, P = 0.005; Supplementary Table 1). Similarly, after additional adjustment for surgical year to account for potential temporal changes during the 10-year recruitment period, the association between TO and OS remained consistent (HR = 0.61, 95%CI: 0.44-0.84, P = 0.003; Supplementary Table 2).
Table 2 Factors associated with overall survival and disease-free survival identified by univariable and multivariable Cox regression, median (interquartile range).
Median DFS was 44.3 months (95%CI: 33.9-57.9). The 1-, 3-, and 5-year DFS rates were 80.0% (95%CI: 75.9%-84.4%), 53.8% (95%CI: 48.5%-59.6%), and 43.3% (95%CI: 38.0%-49.4%), respectively. KM analysis demonstrated significantly improved DFS in the TO group compared with the non-TO group (P < 0.001; Figure 3). The 1-, 3-, and 5-year DFS rates in the TO group were 85.0% (95%CI: 80.5%-89.8%), 59.2% (95%CI: 52.9%-66.3%), and 48.2% (95%CI: 41.7%-55.8%), respectively, compared with 70.0% (95%CI: 62.1%-79.0%), 42.9% (95%CI: 34.4%-53.5%), and 33.5% (95%CI: 25.4%-44.4%) in the non-TO group.
Figure 3 Kaplan–Meier curves for disease-free survival after pancreaticoduodenectomy in patients with ampullary cancer.
A: Disease-free survival curve for the entire cohort of patients with ampullary cancer (n = 347); B: Disease-free survival curves stratified by textbook outcome achievement. Survival differences between groups were compared using the log-rank test. The numbers at risk are shown below the plots. TO: Textbook outcome.
During follow-up, disease recurrence occurred in 119 patients (34.2%), comprising 14 with isolated locoregional recurrence, 34 with combined locoregional and distant recurrence, and 71 with isolated distant metastasis. Among 48 patients with locoregional recurrence, the superior mesenteric artery (SMA) nodal region was the most common site; among 105 with distant metastasis, the liver was the predominant site.
Univariable and multivariable analyses for DFS are summarized in Table 2. In the univariable analysis, TO achievement, tumor differentiation, T stage, N stage, perineural invasion, elevated CA19-9, and positive resection margins were significantly associated with DFS (all P < 0.05). Multivariable analysis revealed that advanced T stage, advanced N stage, perineural invasion, elevated CA19-9, and positive resection margins were independent risk factors for DFS, whereas TO achievement showed a modest but statistically significant association with improved DFS (HR = 0.75, 95%CI: 0.56-0.99, P = 0.044). In the sensitivity model in which T and N stages were replaced by TNM stage, the association between TO achievement and DFS remained consistent with the primary analysis (HR = 0.70, 95%CI: 0.50-0.99, P = 0.042; Supplementary Table 1). Similarly, in the temporal sensitivity analysis, the association between TO achievement and DFS remained consistent (HR = 0.74, 95%CI: 0.56-0.99, P = 0.047; Supplementary Table 2).
Comparison of TO between laparoscopic and open surgery
We further examined the association between surgical approach (laparoscopic vs open) and TO achievement. Given the retrospective nature of this study, surgical approach was not randomly assigned, but rather determined by a comprehensive preoperative assessment of surgical complexity and tumor burden. Consequently, patients with relatively lower technical difficulty were more likely to undergo laparoscopic surgery, introducing potential selection bias. To minimize confounding, we performed PSM to balance baseline characteristics between the laparoscopic and open groups.
Before matching, 169 patients underwent laparoscopic PD and 178 underwent open PD. Significant baseline imbalances were observed, with the open group exhibiting higher N stage (P < 0.001) and more advanced TNM stage (P < 0.001). In addition, the SMDs for sex, BMI, T stage, and preoperative drainage exceeded 0.1, indicating substantial covariate imbalance. After 1:1 matching, 111 patients remained in each group. Baseline characteristics were well balanced between groups (Table 3), with Love plots confirming that all SMDs were below 0.1 (Supplementary Figure 1).
Table 3 Characteristics of patients before and after propensity score matching, n (%)/median (interquartile range).
In the matched cohort, TO achievement rates were comparable between laparoscopic and open surgery (72% vs 66%, P = 0.40; Table 4). No significant differences were observed for any individual TO component (all P > 0.05). Regarding other perioperative outcomes, the laparoscopic approach was associated with longer operative time (330 minutes vs 310 minutes, P = 0.033) but reduced estimated blood loss (100 mL vs 250 mL, P = 0.018). Additionally, the laparoscopic group demonstrated faster postoperative recovery, with shorter time to first off-bed activity (3 days vs 4 days, P < 0.001), earlier nasogastric tube removal (3 days vs 4 days, P = 0.008), and earlier first oral food intake (5 days vs 6 days, P = 0.020; Table 4).
Table 4 Comparison of textbook outcome between laparoscopic and open pancreaticoduodenectomy, n (%)/median (interquartile range).
This study identified four major findings. First, among patients with AC who underwent PD, the TO achievement rate was 66.3%, with “absence of severe complications (Clavien-Dindo ≥ III)” representing the most challenging component. Second, TO achievement was independently associated with improved OS, whereas its association with improved DFS was more modest but remained statistically significant. Third, disease recurrence occurred in 34.2% of patients. Locoregional recurrence predominantly involved the SMA nodal region, whereas the liver was the primary site of distant metastasis. Fourth, no statistically significant difference in TO achievement was observed between laparoscopic and open PD after PSM.
Reported TO rates following PD vary widely, ranging from 21.7% to 82.5% (pooled estimate 55.7%) according to a recent meta-analysis[20]. Such inter-institutional variation reflects the substantial technical complexity of this procedure. PD represents one of the most technically demanding operations in abdominal surgery, characterized by a steep learning curve, approximately 52 cases are required to achieve technical proficiency in laparoscopic PD, and 94 cases to reach mastery[21]. Prior studies have demonstrated that overcoming this learning curve correlates with higher TO achievement[16]. In addition to technical factors, systematic management of perioperative complications and institutional PD volume also significantly influence TO achievement[22]. The Miami International Evidence-Based Guidelines suggest a threshold of 20 minimally invasive PDs annually to distinguish high- from low-volume centers[23]. High-volume PD centers were associated with superior TO achievement rates[24]. In the present study, our TO achievement rate of 66.3% aligns with published ranges yet exceeds the pooled average. As a national high-volume hepatopancreatobiliary center, our institution maintains high PD surgical volume, an established learning curve, and comprehensive perioperative management protocols, which collectively contribute to our relatively high TO achievement rate.
Analysis of the individual TO components revealed that the absence of severe complications (Clavien-Dindo ≥ III) was the least frequently achieved criterion, consistent with prior reports[7,16]. In fact, under the TO definition proposed by DPCG, the absence of severe complications is typically the most difficult individual criterion to achieve[7,16,24]. This pattern likely reflects that severe complications represent an aggregate endpoint encompassing multiple adverse events, including percutaneous drainage, angiographic intervention, endoscopic procedures, or reoperation, rather than an isolated outcome, thereby rendering prevention more complex than for other individual metrics. Consequently, optimizing TO achievement necessitates prioritizing the prevention and management of major complications through comprehensive strategies encompassing rigorous preoperative assessment, refined operative technique, and enhanced postoperative surveillance with early intervention protocols.
Despite heterogeneous definitions across surgical subspecialties, accumulating evidence indicates that TO achievement is associated with improved long-term survival in gallbladder, esophageal, gastric, hepatocellular, and colorectal malignancies[8-11]. However, in PD, a hallmark procedure of pancreatic surgery, existing studies have predominantly focused on determinants of TO achievement, whereas its prognostic value for long-term oncological outcomes, particularly in ampullary carcinoma, remains poorly characterized. This phenomenon may be attributed to two factors. First, prior TO studies commonly aggregated heterogeneous pathologies undergoing PD; this “surgical homogenization” obscures distinct prognostic disparities, precluding accurate assessment of the prognostic value of TO[7,16,22,25]. Second, common malignancies treated with PD, such as pancreatic head adenocarcinoma and distal cholangiocarcinoma, exhibit aggressive biological behavior with early metastatic propensity and dismal prognosis. Within this abbreviated timeframe, TO may have insufficient time to demonstrate its cumulative impact on long-term oncological outcomes[3,26,27]. To the best of our knowledge, this study represented the first comprehensive evaluation of the independent association between TO achievement and long-term oncological outcomes in patients with AC undergoing PD. Our data demonstrated that TO group exhibited significantly superior 1-, 3-, and 5-year OS rates compared with the non-TO group. Similar patterns were observed for DFS. When interpreting the relationship between TO achievement and long-term survival, its potential conceptual limitations should be considered. TO is a composite postoperative outcome that includes major postoperative complications, mortality, and readmission. Therefore, the survival difference between the TO and non-TO groups may partly reflect reverse causality; that is, early postoperative adverse events may themselves lead to poorer long-term outcomes while also classifying patients into the non-TO group, rather than TO acting as an independent causal determinant of prognosis. Accordingly, TO should be interpreted as an integrated indicator reflecting surgical quality and perioperative recovery, and as a tool to assist postoperative long-term survival risk stratification, rather than being overinterpreted as a directly modifiable causal factor for oncological outcomes. In addition, the prognostic implications of TO achievement may differ between OS and DFS. DFS primarily reflects tumor recurrence or progression, whereas OS is a more comprehensive endpoint that is influenced not only by tumor recurrence but also by perioperative recovery, postoperative complications, tolerance to subsequent therapy, and non-cancer-related mortality risk[28,29]. The TO definition used in the present study mainly includes indicators reflecting perioperative safety and postoperative recovery, such as severe postoperative complications, postoperative mortality, and readmission, all of which are closely related to long-term survival[29]. However, this definition does not include recurrence-related oncological factors, such as negative resection margins or completion of adjuvant therapy[30,31]. Therefore, the association between TO and DFS may be weaker than that between TO and OS. In the present study, TO achievement was independently and consistently associated with better OS, whereas its association with DFS was statistically borderline, further supporting the conceptual distinction between these two clinical endpoints.
Among periampullary cancers, AC demonstrates superior OS compared with pancreatic adenocarcinoma and distal cholangiocarcinoma[32]. However, postoperative recurrence remains a significant clinical concern[3]. In this cohort, the recurrence rate was 34.2%, consistent with previously reported rates of 37%-48.4%[1,33,34]. Notably, further analysis showed that SMA nodal region was the most common site of local recurrence. Previous study on recurrence patterns after surgery for AC has also reported that nodular recurrence around the mesenteric vessels is the most common pattern of locoregional recurrence, with 58.8% (10/17) of such recurrences located on the left side of the SMA[35]. Together, these findings suggest that the peri-SMA region may represent an important anatomical site of residual micrometastatic disease or locoregional recurrence after PD. This finding may also be explained by the anatomical pathway of lymphatic spread in AC. Kayahara et al[36] observed that No. 13 lymph nodes, namely the posterior pancreatic head lymph nodes, were the most common site of lymph node metastasis in AC, followed by No. 14 lymph nodes, which are located around the SMA and superior mesenteric vein. Another study similarly identified No. 13 lymph nodes as the most frequent site of lymph node metastasis[37]. These findings suggest that locoregional recurrence in AC may be associated with residual disease within the lymphatic drainage pathway extending from the posterior pancreatic head to the perivascular lymphatic tissue around the SMA and superior mesenteric vein. Therefore, meticulous dissection of peri-SMA tissues and adequate regional lymphadenectomy should be emphasized during surgery to improve local control. Arterial-first PD or total mesopancreas excision may facilitate more complete clearance of peri-SMA soft tissue and lymphatic tissue, thereby increasing the R0 resection rate, improving lymph node yield, and potentially reducing the risk of local recurrence[38-40]. In addition, the relatively high proportion of SMA-region recurrence among local recurrences suggests that postoperative imaging surveillance should not focus solely on the pancreatic bed or liver metastasis, but should also include careful assessment of the SMA root and peri-SMA nodal region. This may be particularly important for patients with high-risk pathological features, such as lymph node metastasis, positive resection margins, perineural invasion, poor differentiation, or advanced T/N stage. Collectively, these findings highlight the potential value of standardized peri-SMA dissection, locoregional control, and targeted imaging surveillance in the postoperative management of AC.
Multivariate analysis of recurrence risk factors identified advanced T and N stages, perineural invasion, elevated CA19-9, and positive resection margins as independent predictors of poor DFS; conversely, TO achievement served as an independent protective factor. In addition to TO, a large multicenter study by Moekotte et al[33] found that all these factors, along with lymphovascular invasion and pancreatobiliary subtype, increase recurrence risk. Park et al[41] reported that large tumor size, lymph node metastasis, and the pancreatobiliary subtype were associated with very early postoperative recurrence (< 6 months). These findings underscore the important role of histological classification in recurrence risk stratification. Therefore, for patients with these high-risk features who do not achieve TO, more intensive postoperative surveillance and monitoring should be considered to facilitate earlier detection of recurrence.
TO is essentially a composite perioperative quality indicator, and its achievement may be influenced by factors such as surgical technique, learning curve, perioperative management, and surgical approach[20]. Although the definition of TO itself does not distinguish between laparoscopic and open surgery, differences in perioperative safety and quality between minimally invasive and open PD have long been important clinical concerns in pancreatic surgery[42]. Therefore, when evaluating TO as a relatively novel integrated quality indicator, we considered it necessary to perform an exploratory analysis to preliminarily assess whether surgical approach may influence the likelihood of TO achievement. Prior to PSM, TO rates were higher in the laparoscopic vs open group (70.4% vs 62.4%), though this finding requires cautious interpretation and does not substantiate that minimally invasive approaches improve TO achievement. As surgical approach allocation was non-random, significant baseline differences existed: Open surgery patients typically presented with advanced tumor stages, higher surgical complexity, and more extensive resections, all factors independently associated with reduced TO achievement[43,44]. After matching, this difference was no longer statistically significant. This aligns with a recent meta-analysis of TO outcomes following radical resection for cholangiocarcinoma, suggesting that surgical approach itself may not be an independent determinant of TO achievement[9]. However, the present findings only indicate that no statistically significant difference in TO achievement was detected between laparoscopic and open PD in this cohort; they should not be interpreted as evidence of equivalence between the two surgical approaches in terms of TO achievement. Given the limited sample sizes of both the laparoscopic and open groups, particularly after matching, this study was underpowered to exclude clinically meaningful differences between the two surgical approaches.
The lack of adjuvant treatment data represents an important limitation. AC is clinically heterogeneous, and expert consensus recommends that adjuvant treatment be tailored to histological subtype. Colorectal cancer-based chemotherapy regimens may be used for intestinal-type tumors, whereas treatment strategies for pancreatobiliary or mixed-type tumors may be extrapolated from pancreatic and biliary tract malignancies[3]. However, the role of adjuvant therapy in AC remains controversial. The ESPAC-3 randomized controlled trial is one of the largest phase III studies evaluating adjuvant therapy in AC and other periampullary cancers. In that trial, patients with ampullary, bile duct, and other periampullary cancers were randomly assigned to 5-fluorouracil plus folinic acid, gemcitabine, or observation. A total of 297 patients with AC were randomized, with 100, 92, and 105 patients in the three groups, respectively, and the corresponding median survival times were 57.8, 70.8, and 40.6 months. However, the study did not separately report statistical comparisons between treatment groups within the AC subgroup[45]. Although some studies have reported survival benefits associated with adjuvant therapy, many others have failed to demonstrate clear improvements in recurrence or survival outcomes[46-48]. A recent retrospective study by Kang et al[48] showed that 5-fluorouracil plus folinic acid-based adjuvant chemotherapy did not improve OS or recurrence-free survival. Therefore, the true benefit of adjuvant therapy in AC remains to be further validated by large-scale randomized controlled trials. In addition, adjuvant therapy may be closely related to TO achievement. TO achievement reflects favorable early postoperative recovery. Patients who fail to achieve TO because of severe postoperative complications or readmission may be less likely to receive timely adjuvant therapy or may have reduced tolerance to subsequent systemic treatment[49]. Conversely, patients who achieve TO may be more likely to recover sufficiently to receive planned adjuvant therapy. Therefore, the observed association between TO achievement and long-term survival in this study may be partly mediated or confounded by differences in postoperative adjuvant treatment. Future studies should collect more detailed adjuvant treatment information to more accurately clarify the relationships among TO achievement, postoperative adjuvant therapy, and long-term oncological outcomes in AC.
This study has several limitations. First, adjuvant chemotherapy and radiotherapy may significantly influence long-term survival and recurrence outcomes in patients with AC. Therefore, the lack of detailed adjuvant treatment data represents an important limitation of this study. Second, the prolonged study period may have introduced temporal variation in surgical techniques, perioperative management protocols, and pathological assessment standards. Although a sensitivity analysis was performed and all patients were uniformly restaged according to the American Joint Committee on Cancer 8th edition criteria, residual confounding related to temporal trends cannot be fully excluded. Third, molecular and histological subtype data were unavailable, precluding further assessment of their impact on tumor biology and prognosis. Finally, inherent to its retrospective design, this study is subject to information bias and potential data incompleteness.
Nevertheless, to our knowledge, this represents the first systematic evaluation of TO achievement in relation to long-term oncological outcomes in AC. Our findings offer novel evidence regarding both perioperative quality and prognostic stratification. Specifically, TO serves not only as a critical quality indicator following PD, but also correlates closely with long-term survival and recurrence patterns; thus, optimizing TO rates may improve immediate recovery while potentially favorably impacting oncological outcomes. Prospective validation and TO-directed risk stratification strategies are warranted to establish definitive clinical utility.
CONCLUSION
In patients with AC undergoing PD, TO achievement reflects optimal perioperative care and is associated with improved long-term outcomes. Given its dual value in quality assessment and prognostic stratification, improving TO achievement rates should be considered a key target for surgical quality improvement in PD.
Bhandare MS, Varty GP, Reddy Obili RC, Chopde A, Pawar A, Krishnakumar K, Yadav S, Ostwal V, Ramaswamy A, Bhargava P, Chaudhari V, Shrikhande SV. CA 19-9 Surveillance Detects Recurrences Early and Contributes to Improvement in Survival in Resected Ampullary Cancers: Analysis of 572 Cases.Ann Surg. 2026;283:286-296.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 4][Cited by in RCA: 3][Article Influence: 3.0][Reference Citation Analysis (3)]
van Roessel S, Mackay TM, van Dieren S, van der Schelling GP, Nieuwenhuijs VB, Bosscha K, van der Harst E, van Dam RM, Liem MSL, Festen S, Stommel MWJ, Roos D, Wit F, Molenaar IQ, de Meijer VE, Kazemier G, de Hingh IHJT, van Santvoort HC, Bonsing BA, Busch OR, Groot Koerkamp B, Besselink MG; Dutch Pancreatic Cancer Group. Textbook Outcome: Nationwide Analysis of a Novel Quality Measure in Pancreatic Surgery.Ann Surg. 2020;271:155-162.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 246][Cited by in RCA: 238][Article Influence: 39.7][Reference Citation Analysis (1)]
Yang SQ, Zou RQ, Dai Y, Liu F, Hu HJ, Li FY. Predictors and prognostic impact of textbook outcome in patients with biliary tract cancer after hepatectomy: a systematic review and meta-analysis.Int J Surg. 2025.
[RCA] [PubMed] [DOI] [Full Text][Reference Citation Analysis (0)]
Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M, Allen P, Andersson R, Asbun HJ, Besselink MG, Conlon K, Del Chiaro M, Falconi M, Fernandez-Cruz L, Fernandez-Del Castillo C, Fingerhut A, Friess H, Gouma DJ, Hackert T, Izbicki J, Lillemoe KD, Neoptolemos JP, Olah A, Schulick R, Shrikhande SV, Takada T, Takaori K, Traverso W, Vollmer CM, Wolfgang CL, Yeo CJ, Salvia R, Buchler M; International Study Group on Pancreatic Surgery (ISGPS). The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After.Surgery. 2017;161:584-591.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 3570][Cited by in RCA: 3498][Article Influence: 388.7][Reference Citation Analysis (13)]
Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, Fan ST, Yokoyama Y, Crawford M, Makuuchi M, Christophi C, Banting S, Brooke-Smith M, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Nimura Y, Figueras J, DeMatteo RP, Büchler MW, Weitz J. Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery.Surgery. 2011;149:680-688.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 1695][Cited by in RCA: 1650][Article Influence: 110.0][Reference Citation Analysis (15)]
Wu Y, Peng B, Liu J, Yin X, Tan Z, Liu R, Hong D, Zhao W, Wu H, Chen R, Li D, Huang H, Miao Y, Liu Y, Liang T, Wang W, Yuan J, Li S, Zhang H, Wang M, Qin R; Minimally Invasive Treatment Group in the Pancreatic DiseaseBranch of China’s International Exchange and Promotion Association for Medicine and Healthcare (MITG-P-CPAM). Textbook outcome as a composite outcome measure in laparoscopic pancreaticoduodenectomy: a multicenter retrospective cohort study.Int J Surg. 2023;109:374-382.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 22][Cited by in RCA: 26][Article Influence: 8.7][Reference Citation Analysis (2)]
Mazzola M, Giani A, Veronesi V, Bernasconi DP, Benedetti A, Magistro C, Bertoglio CL, De Martini P, Ferrari G. Multidimensional evaluation of the learning curve for totally laparoscopic pancreaticoduodenectomy: a risk-adjusted cumulative summation analysis.HPB (Oxford). 2023;25:507-517.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 8][Reference Citation Analysis (0)]
Partelli S, Fermi F, Fusai GK, Tamburrino D, Lykoudis P, Beghdadi N, Dokmak S, Wiese D, Landoni L, Reich F, Busch ORC, Napoli N, Jang JY, Kwon W, Armstrong T, Allen PJ, He J, Javed A, Sauvanet A, Bartsch DK, Salvia R, van Dijkum EJMN, Besselink MG, Boggi U, Kim SW, Wolfgang CL, Falconi M. The Value of Textbook Outcome in Benchmarking Pancreatoduodenectomy for Nonfunctioning Pancreatic Neuroendocrine Tumors.Ann Surg Oncol. 2024;31:4096-4104.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 4][Cited by in RCA: 14][Article Influence: 7.0][Reference Citation Analysis (1)]
Asbun HJ, Moekotte AL, Vissers FL, Kunzler F, Cipriani F, Alseidi A, D'Angelica MI, Balduzzi A, Bassi C, Björnsson B, Boggi U, Callery MP, Del Chiaro M, Coimbra FJ, Conrad C, Cook A, Coppola A, Dervenis C, Dokmak S, Edil BH, Edwin B, Giulianotti PC, Han HS, Hansen PD, van der Heijde N, van Hilst J, Hester CA, Hogg ME, Jarufe N, Jeyarajah DR, Keck T, Kim SC, Khatkov IE, Kokudo N, Kooby DA, Korrel M, de Leon FJ, Lluis N, Lof S, Machado MA, Demartines N, Martinie JB, Merchant NB, Molenaar IQ, Moravek C, Mou YP, Nakamura M, Nealon WH, Palanivelu C, Pessaux P, Pitt HA, Polanco PM, Primrose JN, Rawashdeh A, Sanford DE, Senthilnathan P, Shrikhande SV, Stauffer JA, Takaori K, Talamonti MS, Tang CN, Vollmer CM, Wakabayashi G, Walsh RM, Wang SE, Zinner MJ, Wolfgang CL, Zureikat AH, Zwart MJ, Conlon KC, Kendrick ML, Zeh HJ, Hilal MA, Besselink MG; International Study Group on Minimally Invasive Pancreas Surgery (I-MIPS). The Miami International Evidence-based Guidelines on Minimally Invasive Pancreas Resection.Ann Surg. 2020;271:1-14.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 425][Cited by in RCA: 385][Article Influence: 64.2][Reference Citation Analysis (1)]
Kwon J, Kang CM, Jang JY, Yoon YS, Kwon HJ, Choi IS, Kim HJ, Shin SH, Kang SH, Moon HH, Hwang DW, Kim SC; Korean Study Group on Minimally Invasive Pancreatic Surgery (K-MIPS). Perioperative textbook outcomes of minimally invasive pancreatoduodenectomy: a multicenter retrospective cohort analysis in a Korean minimally invasive pancreatic surgery registry.Int J Surg. 2024;110:4249-4258.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 10][Reference Citation Analysis (0)]
Henry AC, van Dongen JC, van Goor IWJM, Smits FJ, Nagelhout A, Besselink MG, Busch OR, Bonsing BA, Bosscha K, van Dam RM, Festen S, Groot Koerkamp B, van der Harst E, de Hingh IH, van der Kolk M, Liem MSL, de Meijer VE, Patijn GA, Roos D, Schreinemakers JM, Wit F, Daamen LA, van Santvoort HC, Molenaar IQ, van Eijck CHJ. Impact of complications after resection of pancreatic cancer on disease recurrence and survival, and mediation effect of adjuvant chemotherapy: nationwide, observational cohort study.BJS Open. 2023;7:zrac174.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 28][Reference Citation Analysis (0)]
Stoop TF, Sugawara T, Oba A, Feld IM, van Roessel S, van Veldhuisen E, Wu YHA, Nishino J, Ali M, Alseidi A, Sauvanet A, Mirabella A, Sa Cunha A, Kokkola A, Groot Koerkamp B, Pietrasz D, Kleive D, Butturini G, Malleo G, van Laarhoven HWM, Frigerio I, Dembinski J, He J, Gagnière J, Kleeff J, Ramia JM, Roberts KJ, Labori KJ, Marino MV, Falconi M, B Mortensen M, Lesurtel M, Bonds M, Chatzizacharias N, Strobel O, Turrini O, Griffin O, Franklin O, Pfeiffer P, Schulick RD, Salvia R, de Wilde RF, Dokmak S, Rodriguez Franco S, Augustinus S, Burgdorf SK, Crippa S, Hackert T, Tarvainen T, Burns WR, Messersmith W, Wilmink JW, Burkhart RA, Del Chiaro M, Besselink MG; Scientific Committee of the European-African Hepato-Pancreato-Biliary Association (E-AHPBA) and International Collaboration on Advanced Pancreatic Cancer. Adjuvant Chemotherapy After Resection of Localized Pancreatic Adenocarcinoma Following Preoperative FOLFIRINOX.JAMA Oncol. 2025;11:276-287.
[RCA] [PubMed] [DOI] [Full Text] [Full Text (PDF)][Cited by in Crossref: 9][Cited by in RCA: 12][Article Influence: 12.0][Reference Citation Analysis (1)]
Russell TB, Labib PL, Denson J, Ausania F, Pando E, Roberts KJ, Kausar A, Mavroeidis VK, Marangoni G, Thomasset SC, Frampton AE, Lykoudis P, Maglione M, Alhaboob N, Bari H, Smith AM, Spalding D, Srinivasan P, Davidson BR, Bhogal RH, Croagh D, Dominguez I, Thakkar R, Gomez D, Silva MA, Lapolla P, Mingoli A, Porcu A, Shah NS, Hamady ZZR, Al-Sarrieh B, Serrablo A, Aroori S; RAW Study Collaborators. Predictors of actual five-year survival and recurrence after pancreatoduodenectomy for ampullary adenocarcinoma: results from an international multicentre retrospective cohort study.HPB (Oxford). 2023;25:788-797.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 2][Cited by in RCA: 7][Article Influence: 2.3][Reference Citation Analysis (3)]
Moekotte AL, Lof S, Van Roessel S, Fontana M, Dreyer S, Shablak A, Casciani F, Mavroeidis VK, Robinson S, Khalil K, Gradinariu G, Mowbray N, Al-Sarireh B, Fusai GK, Roberts K, White S, Soonawalla Z, Jamieson NB, Salvia R, Besselink MG, Abu Hilal M. Histopathologic Predictors of Survival and Recurrence in Resected Ampullary Adenocarcinoma: International Multicenter Cohort Study.Ann Surg. 2020;272:1086-1093.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 54][Cited by in RCA: 56][Article Influence: 9.3][Reference Citation Analysis (0)]
Zhang X, Sun C, Li Z, Wang T, Zhao L, Niu P, Guo C, Che X, Chen Y, Zhao D. Long-term survival and pattern of recurrence in ampullary adenocarcinoma patients after curative Whipple's resection: a retrospective cohort study in the National Cancer Center in China.Am J Cancer Res. 2022;12:4062-4073.
[PubMed] [DOI]
Lee JH, Lee KG, Ha TK, Jun YJ, Paik SS, Park HK, Lee KS. Pattern analysis of lymph node metastasis and the prognostic importance of number of metastatic nodes in ampullary adenocarcinoma.Am Surg. 2011;77:322-329.
[PubMed] [DOI]
Wang M, Li D, Chen R, Huang X, Li J, Liu Y, Liu J, Cheng W, Chen X, Zhao W, Li J, Tan Z, Huang H, Li D, Zhu F, Qin T, Ma J, Yu G, Zhou B, Zheng S, Tang Y, Han W, Meng L, Ke J, Feng F, Chen B, Yin X, Chen W, Ma H, Xu J, Liu Y, Lin R, Dong Y, Yu Y, Liu J, Zhang H, Qin R; Minimally Invasive Treatment Group in the Pancreatic Disease Branch of China's International Exchange and Promotion Association for Medicine and Healthcare (MITG-P-CPAM). Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours: a multicentre, open-label, randomised controlled trial.Lancet Gastroenterol Hepatol. 2021;6:438-447.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 223][Cited by in RCA: 209][Article Influence: 41.8][Reference Citation Analysis (2)]
Hobeika C, Cauchy F, Fuks D, Barbier L, Fabre JM, Boleslawski E, Regimbeau JM, Farges O, Pruvot FR, Pessaux P, Salamé E, Soubrane O, Vibert E, Scatton O; AFC-LLR-2018 study group. Laparoscopic versus open resection of intrahepatic cholangiocarcinoma: nationwide analysis.Br J Surg. 2021;108:419-426.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 44][Cited by in RCA: 48][Article Influence: 9.6][Reference Citation Analysis (1)]
Brustia R, Laurent A, Goumard C, Langella S, Cherqui D, Kawai T, Soubrane O, Cauchy F, Farges O, Menahem B, Hobeika C, Rhaiem R, Sommacale D, Okumura S, Hofmeyr S, Ferrero A, Pruvot FR, Regimbeau JM, Fuks D, Vibert E, Scatton O; AFC-ICC-2009; AFC-LLR-2018; PRS-2019 Study group. Laparoscopic versus open liver resection for intrahepatic cholangiocarcinoma: Report of an international multicenter cohort study with propensity score matching.Surgery. 2022;171:1290-1302.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 17][Cited by in RCA: 27][Article Influence: 6.8][Reference Citation Analysis (0)]
Neoptolemos JP, Moore MJ, Cox TF, Valle JW, Palmer DH, McDonald AC, Carter R, Tebbutt NC, Dervenis C, Smith D, Glimelius B, Charnley RM, Lacaine F, Scarfe AG, Middleton MR, Anthoney A, Ghaneh P, Halloran CM, Lerch MM, Oláh A, Rawcliffe CL, Verbeke CS, Campbell F, Büchler MW; European Study Group for Pancreatic Cancer. Effect of adjuvant chemotherapy with fluorouracil plus folinic acid or gemcitabine vs observation on survival in patients with resected periampullary adenocarcinoma: the ESPAC-3 periampullary cancer randomized trial.JAMA. 2012;308:147-156.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 531][Cited by in RCA: 482][Article Influence: 34.4][Reference Citation Analysis (2)]
Creativity or innovation: Grade B, Grade B, Grade B
Scientific significance: Grade A, Grade A, Grade B
P-Reviewer: Liu Q, PhD, China; Reaño-Paredes G, Academic Fellow, Adjunct Professor, Associate Faculty, FACS, MD, Principal Investigator, Peru S-Editor: Wu S L-Editor: A P-Editor: Zhang YL
