Yuan XB, Sun G, Niu J, Dong L, Sui Y, Lv YZ. Metastatic lymph node distribution and pathology correlations in upper and lower gastric cancer patients: A multicenter retrospective study. World J Gastrointest Oncol 2025; 17(2): 98803 [DOI: 10.4251/wjgo.v17.i2.98803]
Corresponding Author of This Article
Gang Sun, MD, PhD, Associate Chief Physician, Associate Professor, Department of General Surgery, The No. 967 Hospital of PLA Joint Logistics Support Force, No. 89 Maolin Street, Dalian 116000, Liaoning Province, China. neomoon@yeah.net
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective 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/
Xian-Bei Yuan, Gang Sun, Department of General Surgery, No. 967 Hospital of the People's Liberation Army Joint Logistics Support Force, Dalian 116000, Liaoning Province, China
Jun Niu, Department of Trauma Surgery, The No. 967 Hospital of People's Liberation Army Joint Logistics Support Force, Dalian 116000, Liaoning Province, China
Lei Dong, Department of General Surgery, The First Affiliated Hospital of Dalian Medical University, Dalian 116000, Liaoning Province, China
Yi Sui, Department of General Surgery, The Fifth People's Hospital of Shenyang, Shenyang 110000, Liaoning Province, China
Yong-Zhu Lv, Department of General Surgery, The Fifth People's Hospital of Dalian, Dalian 116000, Liaoning Province, China
Author contributions: Yuan XB contributed to the manuscript writing, data collection and analysis; Sun G and Niu J were involved in the conceptualization and supervision of this study; Sui Y, Dong L, Lv YZ and Sui provided multicenter data support. All authors have read and approved the final version to be published.
Institutional review board statement: This study was reviewed and approved by the Medical Ethics Committee of The No. 967 Hospital of PLA Joint Logistics Support Force, the leading unit for this project.
Informed consent statement: The analysis used anonymous clinical data that were obtained after each patient agreed to treatment by written informed consent.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest related to this article.
Data sharing statement: The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
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: Gang Sun, MD, PhD, Associate Chief Physician, Associate Professor, Department of General Surgery, The No. 967 Hospital of PLA Joint Logistics Support Force, No. 89 Maolin Street, Dalian 116000, Liaoning Province, China. neomoon@yeah.net
Received: July 6, 2024 Revised: October 17, 2024 Accepted: October 25, 2024 Published online: February 15, 2025 Processing time: 196 Days and 5.8 Hours
Abstract
BACKGROUND
Gastric cancer (GC) poses a significant threat to public health. However, the clinicopathological features and tumor biological behaviors vary among the GC patients, leading to individual variations in lymph node metastasis. Consequently, the stratification of lymph node dissection according to the specific type, particularly upper GC, has emerged as a prominent area of research.
AIM
To investigate the distribution of metastatic lymph nodes in patients with upper and lower GC and to analyze the differences in related pathological elements and prognosis.
METHODS
Differential analysis between upper and lower GC patients with various clinicopathological factors was performed using the chi-square test and rank-sum test. Logistic regression models were used to identify risk factors for GC lymph node metastasis, while Cox regression models were used to analyze risk factors affecting patient prognosis. The Kaplan-Meier method was used to construct survival curves associated with prognostic risk factors for GC.
RESULTS
Significant differences were observed between the two GC populations regarding tumor diameter, histological grade, pT stage, pN stage, tumor-node-metastasis (pTNM) stage, vascular invasion, and adjuvant chemotherapy usage (all P < 0.05). Lymph node metastasis rates were highest for Siewert type II patients in groups Nos. 1, 3, 2 and 7; for Siewert type III patients in groups Nos. 3, 1, 2 and 7; and for other/unclassified patients in groups Nos. 1, 3, 7, 2. In the lower GC samples, the sequences were Nos. 3, 6, 7, 4. Pathological type, pT stage, pTNM stage, and positive vascular invasion were independent risk factors for development of lymph node metastasis. Age, pathological type, pT stage, pN stage, pTNM stage, vascular invasion, and absence of adjuvant chemotherapy were identified as independent prognostic factors.
CONCLUSION
Upper GC showed a significantly higher malignancy grade and different lymph node metastasis pattern than lower GC.
Core Tip: Upper gastric cancer (GC) has a significantly greater degree of malignancy than lower GC. In upper GC, the rate of lymph node metastasis was greater in groups Nos. 1, 2, 3 and 7 among the different subtypes. In lower GC, the rate of lymph node metastasis was greater in groups Nos. 3–8. Pathological type, histological grade, pT stage, tumor-node-metastasis (pTNM) stage, and vascular invasion independently influenced the occurrence of lymph node metastasis. Age, pathological type, pT stage, pN stage, pTNM stage, vascular invasion, and absence of adjuvant chemotherapy independently influenced prognosis.
Citation: Yuan XB, Sun G, Niu J, Dong L, Sui Y, Lv YZ. Metastatic lymph node distribution and pathology correlations in upper and lower gastric cancer patients: A multicenter retrospective study. World J Gastrointest Oncol 2025; 17(2): 98803
Gastric cancer (GC) is a multifactorial disease in which both environmental and genetic factors affect its development. This complexity often results in poor prognosis, as patients are frequently diagnosed at middle to late stages[1]. Despite being the fifth most common cancer globally (approximately 5.6%) and the fourth leading cause of cancer-related deaths (approximately 7.7%), epidemiological evidence indicates a global decline in annual GC cases. This decline is attributed to the proliferation of preventive screening and enhanced hygienic dietary conditions. However, the incidence of upper GCs is increasing annually[2]. Upper and lower GCs are delineated by a line that divides the gastric curvature into three equal parts, joining the upper and lower thirds of the stomach and greater curvature. Given the differences in clinicopathological characteristics and tumor biology across GC sites, there is a trend toward individualized lymph node metastasis patterns that may influence prognosis. Consequently, the study of metastatic lymph node status in upper and lower GCs has emerged as a research focus in recent years[3-5]. For these reasons, this study aimed to delineate the distribution of metastatic lymph nodes in upper and lower GCs by examining differences in related pathological elements and their prognostic implications.
MATERIALS AND METHODS
Patients
A total of 1806 patients who underwent radical GC surgery at the First Affiliated Hospital of Dalian Medical University, No. 967 The Hospital of the People's Liberation Army Joint Logistics Support Force, the Fifth People's Hospital of Shenyang and the Fifth People's Hospital of Dalian, comprising 817 patients with upper GC and 989 patients with lower GC, were selected from January 2005 to December 2020. The enrolled patients had no prior gastric surgery, harbored no additional tumors beyond the primary cancer, had not received neoadjuvant therapy, showed no distant organ metastases on imaging, underwent R0 radical gastric surgery as confirmed by pathology, and had ≥ 16 lymph nodes resected postoperatively. The exclusion criteria included emergency exploration, palliative surgery, multicentric GC, and residual GC. The follow-up information was complete, and the survival time was recorded accurately.
Methods
Site delineation for upper GC followed the universally recognized Siewert typing system[6]. For GC, site delineation adhered to the 6th edition of the Guidelines for the Treatment of GC by the Japanese Gastric Cancer Association (JGCA)[7]. Pathological typing was guided by the 2019 edition of the World Health Organization Classification of Tumors of the Digestive System[8]. Pathological staging conformed to the 8th edition of the tumor-node-metastasis (TNM) classification by the American Joint Committee on Cancer and the Union for International Cancer Control[9].
Data on sex, age, tumor diameter, pathological type, histological grade, pT stage, pN stage, pTNM stage, surgical method, adjuvant chemotherapy, vascular invasion, and lymph node metastasis were extracted from the hospital medical records. Follow-up commenced upon GC diagnosis via pathological examination, occurring every 3–6 mo for the first 2 years postoperatively and subsequently every 6–12 mo thereafter. The primary endpoint observed was patient survival or death, delineated as overall survival.
Statistical analysis
The statistical methods of this study were reviewed by Dr. Sui from The No. 967 Hospital of PLA Joint Logistics Support Force. SPSS version 24.0 was used for statistical analysis. Differential analysis between upper and lower GC patients across various clinicopathological factors was performed utilizing the χ² test and rank-sum test. Logistic regression models were used to identify risk factors influencing GC lymph node metastasis, while Cox regression models were used to analyze risk factors affecting patient prognosis. The Kaplan-Meier method was used to construct survival curves associated with prognostic risk factors for GC. To mitigate the influence of confounding variables and retain potentially significant predictors, variables with P < 0.1 in the univariate analysis were included in the multivariate analysis. Statistical significance was set at P < 0.05.
RESULTS
Differential clinicopathological characteristics of upper and lower GCs
Comparative analysis between upper and lower GCs revealed significant differences in tumor diameter, histological grade, pT stage, pN stage, pTNM stage, vascular invasion, and adjuvant chemotherapy usage (all P < 0.05). Among patients with a tumor diameter > 4 cm, low or undifferentiated histology, T4 stage, N3 stage, stage III, and vascular invasion, upper GC patients exhibited significantly greater proportions than lower GC patients, indicating a greater degree of malignancy in upper GC patients. The data are presented in Table 1.
Table 1 Comparative analysis of clinicopathological factors in upper vs lower gastric cancer, n (%).
Patterns of lymph node metastasis in upper and lower GCs
For patients with Siewert type II upper GC, the percentages of patients with lymph node metastasis in the top four groups, in descending order, were 42.47% in Group No. 1, 37.44% in Group No. 3, 29.68% in Group No. 2 and 27.85% in Group No. 7. Among the Siewert type III upper GC patients, the four groups with the most lymph node metastasis were Group No. 3 (41.11%), Group No. 1 (38.73%), Group No. 2 (30.43%) and Group No. 7 (28.06%). For upper GC patients categorized as other/unclassified, the leading four groups in terms of lymph node metastasis rates were Group No. 1 (42.03%), Group No. 3 (39.13%), Group No. 7 (29.28%) and Group No. 2 (28.41%). In lower GC, the six groups leading to lymph node metastasis rates were Group No. 3 (41.46%), Group No. 6 (39.13%), Group No. 7 (25.58%), Group No. 4 (23.15%), Group No. 5 (21.03%) and Group No. 8 (19.72%). The data are detailed in Table 2.
Table 2 Lymph node metastasis distribution patterns in upper vs lower gastric cancer groups.
Groups
Upper gastric cancer (n = 817)
Lower gastric cancer (n = 989)
Siewert type II (n = 219)
Siewert type III (n = 253)
Other/unclassified (n = 345)
Cases/ratio
Cases/ratio
Cases/ratio
Cases/ratio
1
93 (42.47)
98 (38.73)
145 (42.03)
52 (5.26)
2
65 (29.68)
77 (30.43)
98 (28.41)
25 (2.53)
3
82 (37.44)
104 (41.11)
135 (39.13)
410 (41.46)
4
32 (14.61)
35 (13.83)
53 (15.36)
229 (23.15)
5
28 (12.78)
32 (12.65)
41 (11.88)
208 (21.03)
6
16 (7.31)
13 (5.14)
18 (5.22)
387 (39.13)
7
61 (27.85)
71 (28.06)
101 (29.28)
253 (25.58)
8
23 (10.50)
32 (12.65)
35 (10.14)
195 (19.72)
9
20 (9.13)
19 (7.51)
39 (11.30)
72 (7.28)
10
11 (5.02)
15 (5.93)
19 (5.51)
12 (1.21)
11
25 (11.42)
31 (12.25)
37 (10.72)
22 (2.22)
12
2 (0.91)
4 (1.58)
3 (0.87)
32 (3.24)
13
0
1 (0.40)
1 (0.29)
9 (0.91)
14
0
0
1 (0.29)
7 (0.71)
15
0
0
0
8 (0.81)
16
0
0
0
2 (0.20)
17
0
0
0
0
18
0
0
0
0
19
0
0
0
0
20
0
0
0
0
110
16 (7.31)
0
8 (2.32)
0
111
12 (5.48)
0
9 (2.61)
0
112
0
0
0
0
Associations between lymph node metastasis and clinicopathological variables in GC patients
Univariate logistic regression analysis identified the pathological type of signet ring cell carcinoma; moderately differentiated, poorly differentiated, or undifferentiated tumor status; pT stage, T2 to T4; pTNM stage, II or III; and positive vascular invasion as risk factors for lymph node metastasis. Multivariate logistic regression analysis revealed that the pathological type of signet-ring cell carcinoma; moderately differentiated, poorly differentiated, or undifferentiated tumor status; pT stage, T2 to T4; pTNM stage, II or III; and vascular invasion status remained independent risk factors for lymph node metastasis. The data are shown in Table 3.
Table 3 Analysis of risk factors for lymph node metastasis using logistic regression models.
Correlation analysis of clinicopathological factors with GC prognosis
Univariate Cox regression analysis identified factors such as age > 60 years, upper GC status, moderate to undifferentiated tumor grade, pT stage T2 to T4, pN stage N1 to N3, pTNM stage II and III, positive vascular invasion, and the absence of adjuvant chemotherapy as risk factors influencing prognosis. Multivariate Cox regression analysis revealed that age > 60 years, adenocarcinoma status, signet ring cell carcinoma status, pT stages T3 and T4, pN stages N1–N3, pTNM stage III, vascular invasion, and absence of adjuvant chemotherapy were independent risk factors for patient prognosis. The data are shown in Table 4, and survival curves for the risk factors affecting patient prognosis are presented in Figure 1.
A total of 817 patients who were diagnosed with upper GC and 989 with lower GC were included in this study, for a total of 1806 patients. Among patients with upper GC, the mean age was 64.91 ± 12.86 years, with a male-to-female ratio of approximately 2.11:1, whereas among patients with lower GC, the mean age was 66.15 ± 12.49 years, with a male-to-female ratio of approximately 1.79:1. Epidemiological evidence indicates that the male-to-female ratio of GC is generally approximately 2:1. Although the overall incidence of GC is declining annually, the incidence of upper GC is increasing annually[2]. Our findings are consistent with these observations, indicating a potential shift toward younger demographics in upper GC incidence and a heightened risk in male patients. Our study revealed that tumors > 4 cm accounted for 44.6% of upper GC cases, which was significantly greater than the 26.9% of lower GC cases. Regarding the pT stage, 64.5% of upper GC patients were classified into the T3/4 stage, surpassing the 59.6% in lower GC patients. In the T4 stage, 31.8% of patients with upper GC were classified as such, significantly exceeding the 11.7% in lower GC, which suggests a greater propensity for upper GC to exhibit more infiltrative growth and greater malignancy than lower GC.
Regarding lymph node metastasis patterns, our study revealed that for upper GC, metastasis rates were significantly greater in lymph node groups Nos. 1, 2, 3 and 7 across different subtypes, whereas for lower GCs, groups Nos. 3–8 exhibited elevated metastasis rates. These findings are consistent with prior research[10,11], highlighting the importance of clinicians diligently evaluating lymph node metastasis in these specified groups during surgical resection and pathological examination. Currently, for adenocarcinoma of the esophagogastric junction (AEG), where the tumor is centrally located within 2 cm of the esophagogastric junction, including specific cases of Siewert type I and type II AEG, the extent of mediastinal lymph node dissection is still under debate. According to the sixth edition of the Guidelines for the Treatment of GC issued by the JGCA[7], several Japanese studies have identified a correlation between the mediastinal lymph node metastasis rate and the extent of esophageal invasion by the tumor. For tumors invading ≤ 2 cm of the esophagus, clearance of the lower mediastinum lymph nodes (No. 110) is recommended, while for those invading > 4 cm, clearance of lymph nodes in groups Nos. 106recR and 107–112 is advised. Our study revealed that the rates of lymph node metastasis in Groups Nos. 110–112 of Siewert type II AEGs were 7.31%, 5.48% and 0%, respectively. However, high-quality evidence from evidence-based medicine supporting the survival benefit of mediastinal lymph node clearance remains insufficient, necessitating further research.
Our study revealed pathological type, histological grade, pT stage, pTNM stage, and vascular invasion as independent risk factors for lymph node metastasis, with no correlation with sex, age, tumor diameter, or tumor location. In research by Zhang et al[12], pathological type, pT stage, lymphatic invasion, and venous invasion were also identified as independent risk factors for lymph node metastasis. Other studies have demonstrated that lymph node metastasis is not associated with the tumor site[13,14]. Additionally, certain studies have suggested a possible relationship between tumor diameter and lymph node metastasis[15]. Chen et al[16] performed a multifactorial analysis revealing age, sex, tumor diameter, infiltration depth, histological grade, and neural invasion as independent risk factors for lymph node metastasis in early GC patients. These findings indicate a need for more evidence-based research into the risk factors for lymph node metastasis in GC patients, highlighting the significant correlation between tumor biological behavior and lymph node metastasis.
Our study identified age, pathological type, pT stage, pN stage, pTNM stage, vascular invasion, and the absence of adjuvant chemotherapy as independent risk factors influencing GC prognosis. Caliskan Yildirim et al[17] found through multifactorial analysis that in N3-stage GC, lymph node metastasis rate, histological grade, and adjuvant chemotherapy were independent prognostic factors. Tian et al[18] determined that histological grade, pTNM stage, and adjuvant chemotherapy are independent risk factors for GC prognosis. Muneoka et al[19] identified age at surgery, tumor infiltration depth, tumor location, and lymph node metastasis as independent risk factors for disease-free survival in patients with progressive GC. Multiple studies[20-22] have highlighted lymph node metastasis as a crucial prognostic factor for GC. A Spanish study[23] demonstrated that age is not an independent predictor of disease-free survival in patients with GC. This suggests that the role of age as an independent prognostic factor in GC may lack sufficient clinical evidence, whereas lymph node metastasis, pTNM stage, and histological grade serve as reliable predictors of outcomes.
Given the inherent limitations of retrospective studies, our study is subject to selection bias. In categorizing adjuvant chemotherapy and surgical modalities, simple groupings were utilized owing to the absence of detailed clinical information. Moreover, our study did not discuss disease-free survival among tumor patients.
CONCLUSION
Upper GC has been shown to possess a significantly greater degree of malignancy than lower GC. In upper GC, the rate of lymph node metastasis was greater in Groups Nos. 1, 2, 3 and 7 among the different subtypes. In lower GC, the rate of lymph node metastasis was greater in groups Nos. 3–8. Pathological type, histological grade, pT stage, pTNM stage, and vascular invasion independently influenced the occurrence of lymph node metastasis. Age, pathological type, pT stage, pN stage, pTNM stage, vascular invasion, and absence of adjuvant chemotherapy independently influenced patient prognosis.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Oncology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade A
Novelty: Grade A
Creativity or Innovation: Grade B
Scientific Significance: Grade B
P-Reviewer: Rodrigues de Bastos D S-Editor: Liu H L-Editor: A P-Editor: Xu ZH
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