Xie QF, Long LS, Luo YY, Lu MT, Ming WK, Zhao LY, Liu H. Long-term survival outcomes of duodenal adenocarcinoma: A cohort study with 15-year single-center experience. World J Gastrointest Surg 2025; 17(2): 101365 [DOI: 10.4240/wjgs.v17.i2.101365]
Corresponding Author of This Article
Hao Liu, MD, PhD, Associate Professor, Department of General Surgery, Nanfang Hospital, Southern Medical University, North No. 1838 Guangzhou Ave., Guangzhou 510515, Guangdong Province, China. liuhaofbi@163.com
Research Domain of This Article
Oncology
Article-Type of This Article
Retrospective Cohort Study
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/
Qing-Feng Xie, Lian-Sheng Long, Yang-Yang Luo, Meng-Ting Lu, Li-Ying Zhao, Hao Liu, Department of General Surgery, Nanfang Hospital, Southern Medical University, Guangzhou 510515, Guangdong Province, China
Lian-Sheng Long, Department of General Surgery, General Hospital of Southern Theater Command, Guangzhou 510515, Guangdong Province, China
Wai-Kit Ming, Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong 999077, China
Co-first authors: Qing-Feng Xie and Lian-Sheng Long.
Co-corresponding authors: Wai-Kit Ming and Hao Liu.
Author contributions: Xie QF and Long LS contribute equally to this study as co-first authors; Ming WK and Liu H contribute equally to this study as co-corresponding authors; all authors were involved in concept and design; Xie QF, Chen T, Luo YY were involved in data acquisition, analysis or interpretation; Xie QF, Chen T, Luo YY, Lu MT were involved in drafting of the manuscript; Liu H, Zhao LY, Ming WK were involved in modification of important knowledge content of manuscript; Xie QF and Liu H were involved in statistical analysis; Ming WK was involved in administrative, technical or material support.
Supported by Natural Science Foundation of Guangdong Province of China, No. 2023A1515010785; Key Clinical Technique of Guangzhou, No. 2023P-ZD01; and Clinical Research Program of Nanfang Hospital, Southern Medical University, No. 2021CR003.
Institutional review board statement: The study was conducted in accordance with the Declaration of Helsinki and was approved by the ethical committee of the related institution (NFEC-2024-171).
Informed consent statement: We have obtained informed consent from patients for this clinical study.
Conflict-of-interest statement: All the authors declare no conflicts of interest, financial or otherwise.
Data sharing statement: Data were obtained from duodenal cancer database of Nanfang Hospital, Guangzhou, China, so data sharing does not apply to 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.
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: Hao Liu, MD, PhD, Associate Professor, Department of General Surgery, Nanfang Hospital, Southern Medical University, North No. 1838 Guangzhou Ave., Guangzhou 510515, Guangdong Province, China. liuhaofbi@163.com
Received: September 12, 2024 Revised: October 25, 2024 Accepted: November 25, 2024 Published online: February 27, 2025 Processing time: 132 Days and 5.6 Hours
Abstract
BACKGROUND
Duodenal adenocarcinoma (DA), a rare gastrointestinal malignancy, lacks clear natural history and management strategies. This study aimed to investigate the long-term outcomes of patients with DA, focusing on long-term survival and the impact of tumor characteristics, surgery, and adjuvant therapy.
AIM
To bridge this knowledge gap, we conducted a hospital-based cohort study in our 15-year experience with DA aimed at investigating the long-term outcomes of the patients with DA, along with analyzing the impact of the tumor characteristics, operations and adjuvant therapy on survival outcomes.
METHODS
A retrospective analysis of 208 patients diagnosed with non-ampullary DA at a single institution between 2009 and 2023 was performed. This study used SPSS 26.0 software to make a comprehensive statistical analysis of demographic characteristics, clinical presentation, treatment modalities, and survival outcomes. The effectiveness of surgical resection and adjuvant therapy in 5-year oval survival (OS) and disease-free survival was evaluated using Kaplan-Meier survival curves, the Cox proportional hazards model, and statistical comparisons of survival distributions.
RESULTS
The median OS time for the cohort was 39 months, with 3- and 5-year OS rates of 51.2% and 43.6%, respectively. Radical resection was performed in 82.6% of cases, and was significantly associated with an improved 5-year OS, with a rate of 57.8%. Adjuvant therapy showed a survival benefit in the specific patient subsets, particularly in tumor stage II or III tumors, with an improved OS. Adjuvant therapy (hazard ratio= 2.71, 95% confidence interval: 1.30-5.62, P = 0.008), pancreatic invasion and advanced tumor stage were identified as significant predictors of OS in multivariate analyses.
CONCLUSION
Radical operation for DA is associated with a remarkable improvement in the 5-year OS. Importantly, postoperative adjuvant therapy can significantly prolong the OS time in patients with radical operation, especially in patients with stage III. It highlights the necessity for early diagnosis, tailored surgical approaches, and a nuanced understanding of the role of adjuvant therapy.
Core Tip: Numerous meta-analyses and systematic reviews have delved into the treatment of duodenal adenocarcinoma (DA), yet the majority of the studies retrospective, single-center, and small sample size series, particularly in China. To bridge this knowledge gap, we conducted a hospital-based cohort study in our 15-year experience with DA aimed at investigating the long-term outcomes of the patients with DA, along with analyzing the impact of the tumor characteristics, operations and adjuvant therapy on survival outcomes.
Citation: Xie QF, Long LS, Luo YY, Lu MT, Ming WK, Zhao LY, Liu H. Long-term survival outcomes of duodenal adenocarcinoma: A cohort study with 15-year single-center experience. World J Gastrointest Surg 2025; 17(2): 101365
Duodenal adenocarcinoma (DA) remains a relatively rare and enigmatic entity within the realm of gastrointestinal malignancies, accounting for less than 1% of all gastrointestinal cancers yet comprising over 50% of small bowel cancers[1]. This scarcity contributes to the disease's poorly delineated natural history and the persistent ambiguities surrounding optimal management strategies. DA is often compared to colorectal cancer because it shares a location in the gastrointestinal tract and exhibit similar molecular features and potential pathways for tumor development[2,3]. Generally Speaking, the location of the tumor and its genomic profile are recognized as significant factors affecting the prognosis of colorectal cancer and small bowel adenocarcinomas[4,5]. This underscores the necessity of treating the results of each DA treatment modalities as a distinct entity.
The treatment of DA faces several challenges, including the absence of established guidelines based on scientific evidence worldwide, difficulties in early detection due to the rarity of the disease and lack of specific screening markers, and limited evidence supporting various treatment modalities[6,7]. Surgical resection is the only potentially curative treatment for DA. The complexity of the surgery, often involving pancreaticoduodenectomy (PD), has evolved over the years, with advancements in perioperative care and surgical techniques contributing to reduced morbidity and mortality rates, yet without a uniform improvement in long-term survival outcomes[7-9]. Adjuvant therapy, encompassing chemotherapy and radiation, has been explored as a means to improve survival, particularly in cases with adverse pathological features such as lymph node involvement or advanced stage at diagnosis[10]. Despite this rationale, the efficacy of adjuvant treatment in DA remains controversial. There are no randomized controlled trials comparing the efficacy of surgery alone vs perioperative adjuvant therapy for DA. All of the studies were retrospective comparisons of outcomes of surgery alone vs combined surgery, so there may be selection bias in patients[11-13].
Numerous meta-analyses and systematic reviews have delved into the treatment of DA, yet the majority of the studies retrospective, single-center, and small sample size series, particularly in China[14,15]. To bridge this knowledge gap, we conducted a hospital-based cohort study in our 15-year experience with DA aimed at investigating the long-term outcomes of the patients with DA, along with analyzing the impact of the tumor characteristics, operations and adjuvant therapy on survival outcomes.
MATERIALS AND METHODS
This retrospective analysis was conducted to elucidate the long-term survival outcomes of patients diagnosed with non-ampullary DA. The study spanned over a 15-year period, from 2009 to 2023, capturing a comprehensive dataset that reflects advancements in diagnostic and therapeutic strategies over time. The cohort consisted of 208 patients, meticulously selected to provide a robust dataset for analyzing survival outcomes and identifying prognostic factors influencing overall survival (OS) and disease-free survival (DFS). Stage of DA according to American Joint Committee on Cancer (AJCC) 8th edition of small bowel adenocarcinoma, which included patients with positive lymph nodes.
Patient selection
The patients included in this study were drawn from a hospital-based cohort and included cases diagnosed and treated at the facility. Inclusion criteria were histologically confirmed non-ampulla DA, including all stages of disease at diagnosis. Patients were excluded if they had ampulla cancer or other forms of gastrointestinal cancer, had incomplete medical records, or lost follow-up shortly after diagnosis. This rigorous selection process ensured the homogeneity of the study population and the relevance of the findings to non-ampulla DA.
Data collection
Comprehensive data collection was a cornerstone of this study, ensuring a broad and detailed dataset for analysis. Information was gathered retrospectively from the electronic medical records, pathology reports, and radiological images. The data included demographic characteristics [age, gender, body mass index (BMI)], clinical presentation (symptoms, tumor location, stage at diagnosis), treatment modalities (surgical intervention, adjuvant therapy), and survival outcomes (length of survival, recurrence).
Key variables were meticulously recorded, including preoperative laboratory values (e.g., CEA, CA19-9 levels), details of the surgical procedure (extent of resection, lymph node dissection), pathological findings (tumor differentiation, lymphovascular invasion, perineural invasion), and genetic markers when available (KRAS mutation, dMMR/MSI-H). This comprehensive dataset allowed for a nuanced analysis of factors influencing patient outcomes.
Treatment modalities
The treatment modalities employed for managing non-ampullary DA were detailed in this study to understand their impact on survival. Radical operation means that the tumor specimen after surgical resection is confirmed by pathological examination that the surgical margin is clean and no tumor remains. Radical surgical methods include radical PD and endoscopic mucosal resection, and palliative surgical methods include gastrojejunostomy and endoscopic stent implantation. Radical operation was also recorded in detail including the extent of excision and the mode of lymph node dissection. Information was also recorded on adjuvant therapy, which is generally based on fluorouracil and platinum-based drugs and lasts 4-6 cycles. This information is critical because the study was designed to evaluate the effectiveness of different treatment strategies in improving long-term survival in patients with non-ampulla DA.
Statistical analysis
This study used SPSS 26.0 software to make a comprehensive statistical analysis of all the collected data. Survival outcomes, including OS and DFS, were calculated from the date of diagnosis to the date of death or last follow-up for OS and from the date of diagnosis to the date of disease recurrence or last follow-up for DFS. Kaplan-Meier survival curves were generated to illustrate survival trends over time, and log-rank tests were used to compare survival distributions among different patient subgroups[16]. The Cox proportional hazards model was utilized to identify the independent prognostic factors affecting survival. Variables considered in the model included demographic factors (age, gender), clinical characteristics (BMI, jaundice, hemorrhage, anemia), preoperative laboratory values, treatment details (radical operation, adjuvant therapy), and pathological findings (AJCC stage, tumor differentiation, lymph node involvement). Hazard ratios (HRs) and 95% confidence intervals (95%CIs) were calculated to estimate the strength of association between each variable and survival outcomes[17]. The study has been reported in line with the STROCSS criteria[18].
Ethical considerations
The study was conducted in accordance with the Declaration of Helsinki and was approved by the ethical committee of the related institution (NFEC-2024-171). The study was registered at ClinicalTrials.gov (NCT06443086).
RESULTS
A total of 208 patients pathologically diagnosed with non-ampullary DA between 2009 and 2023 were included in present study (Figure 1). The cohort's demographic and clinical characteristics indicate a median age of 60.67 years old. Notably, the gender distribution showed a slight male predominance, consistent with broader trends in gastrointestinal cancers. Radical resection was performed in 82.56% of the cases, Among 142 patients who underwent radical operation, 46 patients (32.21%) had postoperative complications, 32 patients (69.57%) were tested positive for lymph node resection, the main complications were incisional infection, abdominal abscess and pancreatic fistula. Lymph node metastasis was present in 51 (39.92%) patients. Pathological results showed that 111 patients (53.37%) had advanced tumors, with tumor stages of III and IV. After radical operation, 26 patients (18.31%) received adjuvant chemotherapy. The main adjuvant chemotherapy methods were capox regimen and folfox regimen based on 5-fluorouracil and oxaliplatin. Several of the patients with MSI-H received immunotherapy as part of subsequent treatment. In our study, only a small number of DA patients underwent genetic testing for KRAS, Her-2, and MSI, so there was no discussion of genetic markers in our results. The other surgery-related conditions and pathological variables are shown in (Table 1).
Among the 208 patients diagnosed with DA, the median OS of all patients was 39 months; the 3- and 5-year OS rates were 51.2% and 43.6%, respectively (Figure 2A); The median DFS was 22 months; and the 3-year and 5-year DFS rates were 43.2% and 38.7%, respectively (Figure 2B). The median OS of patients undergoing radical operation was 87 months; the 3- and 5-year OS rates were 66.5% and 57.8% (Figure 2C); the median DFS rates were 59 months; and the 3- and 5-year DFS rates were 51.2% and 45.6%, respectively (Figure 2D). Stage I patients did not achieve a median OS of 87 months at stage II, 20 months at stage III, and 9 months at stage IV (P < 0.001, Figure 2E). Stage I patients did not achieve median DFS, 82 months at stage II, 11 months at stage III, and 8 months at stage IV; P < 0.001, Figure 2F). A total of 142 patients underwent radical surgical resection, including 91 patients with stage II and III tumors, 26 patients with postoperative adjuvant therapy, and 65 patients without adjuvant therapy. There was a significant difference in the OS (P = 0.014, Figure 3A) and the DFS (P = 0.048, Figure 3B) between the adjuvant therapy and non-adjuvant therapy in stage II and III patients. There was no statistically significant difference in the OS (P = 0.236, Figure 3C) and DFS (P = 0.559, Figure 3D) between the adjuvant therapy and non-adjuvant therapy in stage II patients. There was a significant difference in OS (P = 0.017, Figure 3E) and DFS (P = 0.135, Figure 3F) between the adjuvant therapy and non-adjuvant therapy in stage III patients.
Figure 2 Overall survival of duodenal carcinoma patients.
A: The median overall survival (OS) of 208 patients with duodenal adenocarcinoma (DA); B: The median disease-free survival (DFS) of 208 patients with DA; C: The median OS of 142 patients with radical operation; D: The median DFS of 142 patients with radical operation; E: The median OS of patients with stage I, II, III, and IV DA; F: Median DFS of patients with stage I, II, III, and IV DA.
Figure 3 Survival of patients with duodenal carcinoma undergoing adjuvant therapy.
A: Overall survival (OS) in patients with stage II and stage III duodenal adenocarcinoma (DA) compared with and without adjuvant therapy; B: Disease-free survival (DFS) in patients with stage II and stage III DA compared with and without adjuvant therapy; C: OS in patients with stage II DA compared with and without adjuvant therapy; D: Adjuvant therapy in patients with stage II and stage III DFS with and without treatment; E: OS with and without treatment in patients with stage III; F: DFS with and without treatment in patients with stage III.
Survival outcomes varied across the cohort, with an overall median survival time of 39 months. The survival rates at different time points provide insight into the disease's trajectory, with 1-, 3-, and 5-year OS rates of 78.5%, 51.2%, and 43.6%, respectively. Multivariate analysis was conducted to identify significant predictors of survival, revealing advanced tumor stage, pancreatic invasion and adjuvant therapy as key factors. Adjuvant therapy was associated with decreased mortality (HR 0.40, 95%CI: 0.19-0.81, P = 0.008) whereas Pancreatic invasion was associated with increased mortality (HR 2.68, 95%CI: 1.41-5.11, P = 0.003; Table 2).
Table 2 Uni- and multivariate analysis for overall survival.
Characteristics
Univariate analysis
Multivariate analysis
Hazard ratio
P value
Hazard ratio
P value
Age (years; ≥ 65 vs < 65 = 1.00)
1.01 (0.99-1.02)
0.24
Gender, female (vs male = 1.00)
0.80 (0.54-1.21)
0.30
CA199 (U/mL; ≥ 37 vs < 37 = 1.00)
2.92 (1.96-4.33)
< 0.001
1.10 (0.60-2.01)
0.76
Radical operation (vs without radical operation = 1.00)
4.912 (2.98-8.11)
< 0.001
AJCC stage IV (vs AJCC stage I-III = 1.00)
3.04 (2.40-3.86)
< 0.001
4.75 (2.70-8.47)
< 0.001
Postoperative complications (vs without postoperative complications = 1.00)
1.22 (0.77-1.95)
0.40
Pancreatic invasion (vs without Pancreatic invasion = 1.00)
Adjuvant therapy (vs without adjuvant therapy = 1.00)
2.52 (1.23-5.15)
0.01
2.71 (1.30-5.62)
0.008
DISCUSSION
In the present study, the 5-year survival rate after curative resection of non-ampullary DA was 57.8%. The 1-, 3- and 5-year survival rates were comparable to previously published reports, although some of these reports included patients with periampullary tumors[19,20]. The crude survival curves stratified for administration of adjuvant therapy reached a significant difference, and in the multivariable analysis the adjuvant therapy was also detected to be associated with improved survival, supporting the use of capox or folfox as adjuvant therapy for advanced diseases[21,22].
Surgical resection emerges as the cornerstone of potentially curative treatment for DA. PD is currently recognized as the most radical surgical method, but PD has high complexity, high risk and high incidence of postoperative complications[23]. Compared with duodenal segectomy, the length of hospital stay is shorter and the rate of postoperative complications and mortality is lower. Adriano's study reported the efficacy of duodenal segectomy in the treatment of DA of the third and fourth parts of the duodenum, which was superior to PD[24].
However, some studies have shown that PD (Whipple surgery) is superior to duodenectomy in OS[25]. In our retrospective cohort study, the median OS after radical operation was 87 months, and the 3- and 5-year OS rates were 66.5% and 57.8%, respectively. This result is similar to the 3-and 5-year OS rates of 66.3% and 58.2% reported in a retrospective study by Jensen et al[7]. In another study of 47 patients with DA, the 5-year OS rate for patients undergoing radical surgical removal was 51%[26]. Surprisingly, lymph node status, a critical prognostic factor in many cancers, did not significantly influence survival outcomes in certain studies, suggesting a potential reevaluation of its role in DA treatment planning.
The choice of adjuvant therapy remains a contentious issue, with data indicating a nuanced benefit. For instance, patients with tumor stage II and III showed improved median OS times with adjuvant therapy compared to those without adjuvant therapy. This suggests a selective benefit of adjuvant therapy, potentially improving the outcomes in specific patient subsets. However, the effectiveness and selection criteria for adjuvant therapy, including chemotherapy, warrant further investigation to tailor approaches that maximize patient survival while considering the quality of life. A national study in Japan looked at 1083 patients with non-ampulla duodenal cancer who underwent surgery at 114 training institutions accredited by the Japanese Society for Hepatobiliary and Pancreatic Surgery between 2008 and 2017, and across the cohort, no survival benefit was observed in patients who received adjuvant therapy compared to patients who underwent surgery alone. However, in the matched cohort, there was a significant improvement in DFS at 6 months of adjuvant therapy[13] (median: 43.5 months vs 22.5 months, P = 0.016). In our cohort study, the median OS was 63 months with adjuvant therapy and 21 months without adjuvant therapy, and the 5-year OS was 43.2% with adjuvant therapy and 28.6% without adjuvant therapy (P = 0.014 ),which was more favorable than that reported previously. In a study conducted at M.D. Anderson Cancer Center, 54 patients diagnosed with radical resection of small bowel cancer were retrospectively evaluated. The results of survival analysis showed that adjuvant chemotherapy improved DFS (P = 0.05), but did not have a statistically significant benefit on OS[27]. In the present study, the median DFS with adjuvant therapy was 24 months and the median overall DFS without adjuvant therapy was 12 months (P = 0.048), adjuvant chemotherapy appears to significantly improve survival.
The present study was limited by the inherited retrospective nature with all its inherited biases, underscoring the need for the prospective studies to better understand and optimize therapy strategies[28].
In conclusion, radical resection for DA is associated with a remarkable improvement in the 5-year OS, with a rate of 57.8%. Importantly, adjuvant therapy in patients who underwent radical surgery may be associated with a survival benefit. The interplay of surgical resection, tumor characteristics, and adjuvant therapy in influencing outcomes highlights the complex nature of DA therapy. Early diagnosis, tailored surgical approaches, and a nuanced understanding of the role of adjuvant therapy are pivotal in improving patient survival[29]. Future research focusing on large-scale, prospective studies and the exploration of molecular characteristics of DA will be crucial in advancing therapy paradigms, offering hope for improved outcomes in this challenging malignancy[30].
CONCLUSION
Duodenal adenocarcinoma currently lacks a clear natural history and treatment strategy, and we conducted a hospital-based cohort study over 15 years of DA treatment experience to investigate long-term outcomes in patients with DA. The study concluded that radical operation was associated with a significant improvement in 5-year OS, and postoperative adjuvant therapy may be associated with a survival benefit. Future research should focus on large-scale, prospective clinical studies to further explore long-term survival of duodenal adenocarcinoma.
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 C
Novelty: Grade C
Creativity or Innovation: Grade B
Scientific Significance: Grade B
P-Reviewer: Avudaiappan AP S-Editor: Lin C L-Editor: A P-Editor: Zhang L
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