Retrospective Study Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Surg. Jun 27, 2024; 16(6): 1637-1646
Published online Jun 27, 2024. doi: 10.4240/wjgs.v16.i6.1637
Analysis of lymph node metastasis and survival prognosis in early gastric cancer patients: A retrospective study
Dong-Yuan Liu, Department of General Surgery, The 971st Hospital of Chinese People's Liberation Army, Qingdao 266071, Shandong Province, China
Jin-Jin Hu, Department of Chest Surgery, Feicheng People's Hospital, Feicheng 271600, Shandong Province, China
Yong-Quan Zhou, Department of Gastrointestinal Surgery, Zhongshan Hospital of Fudan University, Shanghai 200032, China
Ai-Rong Tan, Department of Oncology, Qingdao Municipal Hospital, Qingdao 266000, Shandong Province, China
ORCID number: Yong-Quan Zhou (0000-1114-2425-1257); Ai-Rong Tan (0009-0009-5115-9365).
Author contributions: Liu DY wrote the manuscript; Hu JJ and Zhou YQ collected the data; Tan AR guided the study; All authors reviewed, edited, and approved the final manuscript and revised it critically for important intellectual content, gave final approval of the version to be published, and agreed to be accountable for all aspects of the work.
Institutional review board statement: This study has been approved by the Clinical medical Research Ethics Committee of Zhongshan Hospital of Fudan University.
Informed consent statement: This study has obtained the consent and signed informed consent of the patients and their families.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: The technical appendix, statistical code, and dataset are available from the corresponding author at airongtan0425@outlook.com.
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: Ai-Rong Tan, MM, Doctor, Department of Oncology, Qingdao Municipal Hospital, No. 5 Donghai Middle Road, Shinan District, Qingdao 266000, Shandong Province, China. airongtan0425@outlook.com
Received: January 30, 2024
Revised: April 8, 2024
Accepted: May 6, 2024
Published online: June 27, 2024
Processing time: 151 Days and 10.8 Hours

Abstract
BACKGROUND

Early gastric cancer (EGC) is a common malignant tumor of the digestive system, and its lymph node metastasis and survival prognosis have been concerning. By retrospectively analyzing the clinical data of EGC patients, we can better understand the status of lymph node metastasis and its impact on survival and prognosis.

AIM

To evaluate the prognosis of EGC patients and the factors that affect lymph node metastasis.

METHODS

The clinicopathological data of 1011 patients with EGC admitted to our hospital between January 2015 and December 2023 were collected in a retrospective cohort study. There were 561 males and 450 females. The mean age was 58 ± 11 years. The patient underwent radical gastrectomy. The status of lymph node metastasis in each group was determined according to the pathological examination results of surgical specimens. The outcomes were as follows: (1) Lymph node metastasis in EGC patients; (2) Analysis of influencing factors of lymph node metastasis in EGC; and (3) Analysis of prognostic factors in patients with EGC. Normally distributed measurement data are expressed as mean ± SD, and a t test was used for comparisons between groups. The data are expressed as absolute numbers or percentages, and the chi-square test was used for comparisons between groups. Rank data were compared using a nonparametric rank sum test. A log-rank test and a logistic regression model were used for univariate analysis. A logistic stepwise regression model and a Cox stepwise regression model were used for multivariate analysis. The Kaplan-Meier method was used to calculate the survival rate and construct survival curves. A log-rank test was used for survival analysis.

RESULTS

Analysis of influencing factors of lymph node metastasis in EGC. The results of the multifactor analysis showed that tumor length and diameter, tumor site, tumor invasion depth, vascular thrombus, and tumor differentiation degree were independent influencing factors for lymph node metastasis in patients with EGC (odds ratios = 1.80, 1.49, 2.65, 5.76, and 0.60; 95%CI: 1.29–2.50, 1.11–2.00, 1.81–3.88, 3.87-8.59, and 0.48-0.76, respectively; P < 0.05). Analysis of prognostic factors in patients with EGC. All 1011 patients with EGC were followed up for 43 (0–13) months. The 3-year overall survival rate was 97.32%. Multivariate analysis revealed that age > 60 years and lymph node metastasis were independent risk factors for prognosis in patients with EGC (hazard ratio = 9.50, 2.20; 95%CI: 3.31-27.29, 1.00-4.87; P < 0.05). Further analysis revealed that the 3-year overall survival rates of gastric cancer patients aged > 60 years and ≤ 60 years were 99.37% and 94.66%, respectively, and the difference was statistically significant (P < 0.05). The 3-year overall survival rates of patients with and without lymph node metastasis were 95.42% and 97.92%, respectively, and the difference was statistically significant (P < 0.05).

CONCLUSION

The lymph node metastasis rate of EGC patients was 23.64%. Tumor length, tumor site, tumor infiltration depth, vascular cancer thrombin, and tumor differentiation degree were found to be independent factors affecting lymph node metastasis in EGC patients. Age > 60 years and lymph node metastasis are independent risk factors for EGC prognosis.

Key Words: Gastric neoplasms, Lymph node metastasis, Prognosis, Influencing factor, Retrospective study

Core Tip: The clinical data of patients with early gastric cancer (EGC) were retrospectively analyzed to investigate the lymph node metastasis and its influence on survival and prognosis. We will focus on the incidence of lymph node metastasis in patients with EGC and the correlation between the number of metastatic lymph nodes and the survival of patients. The results of this study are helpful to further understand the pathological characteristics of EGC patients and their impact on prognosis, and provide scientific basis for developing personalized treatment and improving the quality of life of patients.



INTRODUCTION

Early gastric cancer (EGC) is an adenocarcinoma that is limited to the gastric mucosa or submucosa, regardless of tumor size and lymph node metastasis[1-3]. In recent years, with the continuous improvement in the diagnosis and treatment of gastric cancer in our country, the detection rate of early-stage gastric cancer has been continuously increasing, and the 5-year survival rate is > 90%. Although the prognosis of EGC patients is good, the 5-year survival rate of EGC patients with lymph node metastasis is significantly lower than that of patients without lymph node metastasis[4]. The status of lymph node metastasis determines the treatment of EGC and affects the prognosis.

EGC research revealed that a large number of poorly differentiated cases involved the lower part of the stomach. This observation sparked our interest in a retrospective analysis of lymph node metastasis and survival outcomes in EGC patients. In clinical practice, low-differentiated cases typically show more aggressive characteristics, and their tendency to appear in the lower part of the stomach has attracted our attention[5]. There are several possible reasons. First, the lower part of the stomach has a more complex anatomical structure due to its anatomical location, close to the pylorus and gastric antrum, which may complicate the growth and spread of tumors in the lower part of the stomach. Additionally, the lower part of the stomach has more mucosal structure than the upper part. The submucosal tissue is also less dense, which may make it easier for tumor cells to enter lymphatic and blood vessels[6]. In addition, disease factors specific to the lower stomach, such as atrophic gastritis and Helicobacter pylori infection, may also be associated with low differentiation in gastric cancer and lymph node metastasis.

Early stomach cancer is the early stage of cancer, when the cancer cells are mostly confined to the stomach wall and have not yet spread to the lymph nodes or beyond[7]. Lymph node metastasis is an important sign of gastric cancer progression, which means that cancer cells enter lymphatic vessels from the primary site, reach lymph nodes, and continue to grow and spread. The occurrence and degree of lymph node metastasis have important influences on the prognosis of gastric cancer patients[8-10]. With the progress of medical technology, the diagnosis rate of EGC has improved, but lymph node metastasis is still a key factor affecting the prognosis of patients[11]. The presence of lymph node metastases in EGC can provide valuable information about the patient's prognosis and help physicians develop a more precise treatment plan. Studying the relationship between lymph node metastasis and the prognosis of EGC patients is helpful for further understanding the development of gastric cancer and providing clinicians with more targeted treatment recommendations to improve the survival rate and quality of life of patients[12-14]. Moreover, for patients with EGC with lymph node metastasis, effective treatments, such as surgery, chemotherapy, and radiotherapy, should be actively adopted to curb the spread of cancer cells and improve the cure rate[15].

Both anatomical pathways and tumor biology can help us understand the basic principle of lymph node metastasis, which is more concentrated in the first station. Anatomically, the lymphatic system forms specific channels in the body that direct tissue fluid and cellular waste from tissues to lymph nodes. When cancer cells invade lymphatic vessels and penetrate their walls, they usually first travel along an anatomical path to the nearest lymph node, the "first stop" of lymphatic metastasis. Tumor biology also influences this pattern; for example, tumor cells within lymphatic vessels may be influenced by specific factors that make them more inclined to stay and grow in specific lymph nodes along the anatomical path.

This study retrospectively analyzed the clinicopathological data of 1011 patients with EGC admitted to our department between January 2015 and December 2023 to explore the factors affecting lymph node metastasis and the prognosis of EGC patients.

MATERIALS AND METHODS
General clinical data analysis

The clinicopathological data of 1011 patients with EGC were collected in a prospective cohort study. There were 561 males and 450 females. The mean age was 58 ± 11 years. Among the 1011 patients, 577 had a tumor length ≤ 2 cm, and 434 had a length > 2 cm. The tumors were highly differentiated in 214 patients, moderately differentiated in 296 patients, and poorly differentiated in 501 patients. The tumors were located in the upper part of the stomach in 90 patients, the middle part of the stomach in 193 patients, and the lower part of the stomach in 728 patients. The depth of tumor invasion was mucosa (stage T1a) in 446 patients and submucosa (stage T1b) in 565 patients.

This study was approved by our hospital, and patients and their families signed informed consent forms.

Inclusion criteria: (1) A postoperative pathological examination confirmed EGC; (2) A radical gastrectomy was performed; (3) No antitumor therapy was administered before surgery; and (4) Complete clinicopathological data were available.

Exclusion criteria: (1) A postoperative pathological examination confirmed advanced gastric cancer; (2) Patients with a preoperative history of neoadjuvant therapy; (3) Other malignant tumors; (4) Gastric stump cancer; (5) Recurrent cancer; (6) Special types of gastric tumors, such as lymphoma, neuroendocrine tumors, and stromal tumors; and (7) Clinicopathological data were missing.

Research methods

The patient underwent radical gastrectomy. According to the pathological examination results of surgical specimens, lymph node metastasis in each group was determined according to the statistics of the 13th edition of the gastric cancer treatment protocol.

Observation indicators and evaluation criteria

Observation indicators: (1) Lymph node metastasis in EGC includes the lymph node metastasis rate, lymph node metastasis rate in different T stages, lymph node metastasis in different groups, and lymph node metastasis in different locations; (2) Analysis of influencing factors of lymph node metastasis in EGC: Sex, age, body mass index (BMI), family history of gastric cancer, smoking history, drinking history, tumor length, tumor site, tumor invasion depth, vascular cancer thrombus, nerve invasion, and tumor differentiation degree; and (3) Analysis of factors influencing the prognosis of patients with EGC: Number of patients with follow-up, follow-up time, and survival of patients. The clinicopathologic factors included sex, age, BMI, family history of gastric cancer, smoking history, drinking history, tumor length, tumor site, depth of tumor invasion, vascular cancer thrombus, nerve invasion, degree of tumor differentiation, and lymph node metastasis.

Evaluation criteria: The T and N stages were determined according to the American Joint Commission on Cancer (AJCC) 8th edition tumor-node-metastasis (TNM) staging criteria. The system classifies patients into different stages based on the primary tumor, lymph node metastasis, and distant metastasis status. Specifically, the T stage reflects the size and aggressiveness of the primary tumor in the stomach, the N stage reflects the presence of lymph node metastasis, and the M stage reflects the presence of distant metastasis. We retrospectively analyzed the patients' clinical data, classified them according to the AJCC-TNM staging system, and recorded the number of patients, clinical features, and lymph node metastasis in each stage group.

Follow-up visit

Follow-up was conducted by outpatient visits or telephone to determine the survival of patients, and the follow-up time was up to May 2023.

Statistical analysis

SPSS 25.0 statistical software was used for the analysis. Normally distributed measurement data are expressed as mean ± SD, and a t test was used for comparisons between groups. The data are expressed as absolute numbers or percentages, and the chi-square test was used for comparisons between groups. Rank data were compared using a nonparametric rank sum test. A log-rank test and a logistic regression model were used for univariate analysis. A logistic stepwise regression model and a Cox stepwise regression model were used for multivariate analysis. The Kaplan-Meier method was used to calculate the survival rate and construct survival curves. A log-rank test was used for survival analysis. P < 0.05 was considered to indicate statistical significance.

RESULTS
Lymph node metastasis in EGC

In 1011 patients with early-stage gastric cancer, the rate of lymph node metastasis was 23.64% (239/1011), among which the rate of lymph node metastasis was 11.88% (53/446) in patients with stage T1a disease and 32.92% (186/565) in patients with stage T1b disease. In 239 patients with lymph node metastasis, lymph node metastasis was mainly concentrated in the first-station lymph node, and in groups 1, 2, 3, 4, 5, 6, 7, 8, 9, and 10, lymph node metastasis was 7, 11, 135, 59, 39, 91, 6, 8, 8, 8, and 6, respectively. The same patient may have multiple lymph node metastases. Lymph node metastasis at different tumor sites: 4, 2, and 1 patients were included in the 2nd, 3rd, and 5th groups of upper gastric tumors, respectively. There were 3, 7, 36, 15, 3, and 5 patients with lymph node metastasis in groups 1, 2, 3, 3, 6, 4, 4, and 6, respectively. There were 4, 97, 44, 35, and 86 patients with lymph node metastasis in groups 1, 3, 4, 5, and 6, respectively.

Analysis of influencing factors of lymph node metastasis in EGC

One-way analysis revealed that the factors that affected lymph node metastasis in EGC patients were tumor differentiation, tumor length, tumor location, tumor invasion depth, vascular thrombus, and tumor differentiation. Sex, age, BMI, family history of gastric cancer, smoking history, and drinking history were not correlated with lymph node metastasis in patients with EGC (P > 0.05; Table 1).

Table 1 Univariate analysis of lymph node metastasis in 1011 patients with early gastric cancer.
Clinicopathological factors
Assignment
Lymph node metastasis (n = 239)
No lymph node metastasis (n = 772)
χ²
P value
Sex
        Male11314300.060.809
        Female0108342
Age
        ≤ 60 yr old01314320.100.755
        > 60 yr old1108340
BMI
        ≤ 24 kg/m²11625390.560.511
        > 24 kg/m²077233
Family history of gastric cancer
        Yes1922840.230.633
        No0147488
Smoking history
        Yes1842660.040.845
        No0155506
Drinking history
        Yes1671911.040.308
        No0172581
Tumor size
        ≤ 2 cm09947831.29< 0.001
        > 2 cm1140294
Tumor location
        Upper part of the stomach168415.82< 0.001
        Mid-stomach250143
        Lower part of the stomach3183545
Tumor invasion depth
        Mucosal lining05339361.11< 0.001
        Submucosa1186379
Vasculatogenic cancer thrombus
        No010264157.26< 0.001
        Yes1137708
Nerve invasion
        No0212413.83< 0.001
        Yes1218748
Degree of tumor differentiation
        Low differentiation1125376Z = -2.450.014
        Medium differentiation288208
        High differentiation326188

The results of the multifactor analysis showed that tumor length, tumor location, tumor invasion depth, vascular cancer thrombus, and tumor differentiation degree were independent factors affecting lymph node metastasis in EGC patients (P < 0.05; Table 2).

Table 2 Multivariate analysis of lymph node metastasis in 1011 patients with early gastric cancer.
Clinicopathological factors
Regression coefficients
SE
Wald
OR
95%CI
P value
Tumor diameter0.590.1712.151.801.29-2.50< 0.001
Tumor site0.400.157.101.491.11-1.000.008
Depth of tumor invasion0.970.2024.842.651.81-3.88< 0.001
Vasculatogenic cancer thrombus1.750.2073.995.763.87-8.59< 0.001
Degree of tumor differentiation-0.500.1218.680.600.48-0.76< 0.001
Analysis of factors influencing the prognosis of patients with EGC

All 1011 patients with EGC were followed up for 43 (0–13) months. The 3-year overall survival rate was 97.32%. Univariate analysis revealed that age, vascular thrombus, and lymph node metastasis were factors related to the prognosis of EGC patients (P < 0.05). Sex, BMI, family history of gastric cancer, smoking history, drinking history, tumor length, tumor site, depth of tumor invasion, nerve invasion, and degree of tumor differentiation were not correlated with the prognosis of EGC patients (P > 0.05; Table 3).

Table 3 Univariate analysis of prognosis in 1011 patients with early gastric cancer.
Clinicopathological factors
Assignment
Cases
3-year overall survival rate (%)
χ²
P value
Sex
        Male156196.61.890.169
        Female045098.0
Age
        ≤ 60 yr old056398.95.950.015
        > 60 yr old144897.3
BMI
        ≤ 24 kg/m²070197.40.760.384
        > 24 kg/m²131096.9
Family history of gastric cancer
        Yes137696.61.690.193
        No063599.3
Smoking history
        Yes135097.91.420.233
        No066198.8
Drinking history
        Yes125898.81.090.297
        No075398.4
Tumor length
        ≤ 2 cm057797.50.140.708
        > 2 cm143496.9
Tumor location
        Upper part of the stomach19097.40.570.752
        Mid-stomach219398.1
        Lower part of the stomach372898.2
Tumor invasion depth
        Mucosal lining044698.03.390.066
        Submucosa156596.6
Vasculatogenic cancer thrombus
        No016697.85.260.022
        Yes184594.4
Nerve invasion
        No04598.80.300.587
        Yes196695.1
Degree of tumor differentiation
        Low differentiation150197.74.210.122
        Medium differentiation229697.6
        High differentiation321495.6
Lymph node metastases
        No077297.97.110.008
        Yes123995.0

The results of multivariate analysis showed that age > 60 years and lymph node metastasis were independent risk factors for the prognosis of EGC patients (P < 0.05; Table 4). Further analysis revealed that the 3-year overall survival rates of gastric cancer patients aged > 60 years and ≤ 60 years were 99.37% and 94.66%, respectively, and the difference was statistically significant (χ² = 25.33, P < 0.001; Figure 1A). The 3-year overall survival rates of patients with and without lymph node metastasis were 95.42% and 97.92%, respectively, and the difference was statistically significant (χ² = 5.69, P = 0.017; Figure 1B).

Figure 1
Figure 1 Overall survival curves of patients. A: Postoperative overall survival curves of patients aged < 60 years and > 60 years with early gastric cancer; B: Overall survival curve of patients with early gastric cancer without lymph node metastasis and with lymph node metastasis.
Table 4 Multivariate analysis of prognosis in 1011 patients with early gastric cancer.
Clinicopathological factors
Regression coefficients
SE
Wald
RR
95%CI
P value
Age > 60 yr2.250.5417.479.53.31-27.29< 0.001
Lymph node metastases0.790.403.812.21.00-4.870.049
DISCUSSION

The main treatment methods for EGC include simple surgery and endoscopic resection[16]. Compared with surgical resection, endoscopic resection has the advantages of less trauma and a greater postoperative quality of life and is the preferred treatment for EGC[17]. However, the risk of tumor recurrence after endoscopic resection is greater than that after surgical resection because the lymph nodes cannot be removed. Therefore, for EGC patients with lymph node metastasis, surgical operations are still needed to achieve radical resection of the tumor[18-20]. Lymph node metastasis is also a key factor affecting the prognosis of patients with EGC. The results of this study showed that the 3-year overall survival rate of patients with lymph node metastasis was significantly lower than that of patients without lymph node metastasis[21]. Therefore, accurately predicting the risk of lymph node metastasis in EGC and understanding the law of lymph node metastasis in EGC are conducive to selecting appropriate surgical methods and improving therapeutic efficacy.

The results of this study showed that the lymph node metastasis rate of EGC patients was 23.64% (239/1011), which was similar to the findings of other studies[22]. There are many factors affecting lymph node metastasis in EGC, among which vascular invasion, depth of tumor invasion, and tumor size are recognized as influencing factors[23]. Multifactor analysis in this study showed that the length of the tumor, its location, its invasion depth, the presence of a vascular cancer thrombus, and its degree of differentiation were all separate factors that affected lymph node metastasis in EGC patients[24]. Among the many factors related to lymph node metastasis in EGC, the indicators that can be used for preoperative evaluation include tumor length, tumor site, and tumor invasion depth[25-27]. Preoperative operators can use endoscopic ultrasound and gastroscopy to accurately evaluate EGC and guide the selection of appropriate treatment[28].

The results of this study showed that lymph node metastasis in EGC patients was mainly concentrated in the first station lymph node[29]. The rate of lymph node metastasis differed among different tumor sites, and the rate of lymph node metastasis differed among groups[30]. Although the patterns of lymph node metastasis differed among the different sites of EGC, Group 3 lymph node metastasis was detected in all of the patients, which should be the focus of further studies. One study examined the clinical and pathological information of 33 people with EGC who had lymph node metastasis. Group 3 had the most lymph node metastasis, followed by Group 4. This is consistent with the results of this study. D2 lymph node dissection has become the standard surgical procedure for advanced gastric cancer[31-33].

The results showed that lymph node metastasis in gastric cancer was affected by the degree of tumor differentiation, the depth of invasion, and the extent of lymphatic vessel invasion. In particular, patients with low differentiation, deep invasion, and obvious lymphatic vessel invasion were more likely to have lymph node metastasis. In addition, the patient's age, sex, comorbidities, and other factors may also affect the incidence and prognosis of lymph node metastasis.

Lymph node metastasis in EGC is mainly concentrated in the first-station lymph node, and most patients with EGC may have excessive lymph node dissection[34]. In summary, this study revealed that we need to determine whether a patient has lymph node metastasis before surgery for early-stage gastric cancer, to ensure that the right lymph node dissection is performed to the greatest extent possible after radical treatment, and to improve the overall survival of patients[35]. The results of this study showed that age > 60 years and lymph node metastasis were independent risk factors affecting the prognosis of patients with EGC[36]. Further analysis revealed statistically significant differences in 3-year overall survival rates between patients aged > 60 years and those aged ≤ 60 years with and without lymph node metastasis[37]. Another study showed that vascular thrombus is an independent risk factor affecting the prognosis of patients with EGC and can be used as a reference index for postoperative adjuvant treatment. Age is an important predictor of the prognosis of gastric cancer patients, and there are significant differences in clinicopathological features and prognostic factors among different age groups[38]. Lymph node metastasis is an independent risk factor for the postoperative prognosis of gastric cancer patients and can better guide the diagnosis and treatment of postoperative patients[39-41]. This study revealed that people over 60 years old who have EGC and who undergo postoperative pathological examination that revealed lymph node metastasis should receive additional chemotherapy or radiotherapy after surgery to help them live longer.

CONCLUSION

In summary, the rate of lymph node metastasis in EGC patients was 23.64%. Tumor length, tumor site, tumor invasion depth, vascular cancer thrombin, and tumor differentiation degree were found to be independent factors affecting lymph node metastasis in EGC patients. Age > 60 years and lymph node metastasis are independent risk factors for EGC patients.

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 B

Creativity or Innovation: Grade B

Scientific Significance: Grade C

P-Reviewer: Morya AK, India S-Editor: Li L L-Editor: A P-Editor: Che XX

References
1.  Dong D, Fang MJ, Tang L, Shan XH, Gao JB, Giganti F, Wang RP, Chen X, Wang XX, Palumbo D, Fu J, Li WC, Li J, Zhong LZ, De Cobelli F, Ji JF, Liu ZY, Tian J. Deep learning radiomic nomogram can predict the number of lymph node metastasis in locally advanced gastric cancer: an international multicenter study. Ann Oncol. 2020;31:912-920.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 90]  [Cited by in F6Publishing: 188]  [Article Influence: 47.0]  [Reference Citation Analysis (0)]
2.  Li GZ, Doherty GM, Wang J. Surgical Management of Gastric Cancer: A Review. JAMA Surg. 2022;157:446-454.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 80]  [Article Influence: 40.0]  [Reference Citation Analysis (0)]
3.  Liu Y, Zhai E, Chen J, Qian Y, Zhao R, Ma Y, Liu J, Huang Z, Cai S. m(6) A-mediated regulation of PBX1-GCH1 axis promotes gastric cancer proliferation and metastasis by elevating tetrahydrobiopterin levels. Cancer Commun (Lond). 2022;42:327-344.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 19]  [Article Influence: 9.5]  [Reference Citation Analysis (0)]
4.  Zhang G, Gao Z, Guo X, Ma R, Wang X, Zhou P, Li C, Tang Z, Zhao R, Gao P. CAP2 promotes gastric cancer metastasis by mediating the interaction between tumor cells and tumor-associated macrophages. J Clin Invest. 2023;133.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 6]  [Reference Citation Analysis (0)]
5.  Wu L, Zheng Y, Liu J, Luo R, Wu D, Xu P, Li X. Comprehensive evaluation of the efficacy and safety of LPV/r drugs in the treatment of SARS and MERS to provide potential treatment options for COVID-19. Aging (Albany NY). 2021;13:10833-10852.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 2]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
6.  Li Y, Liu C, Zhang X, Huang X, Liang S, Xing F, Tian H. CCT5 induces epithelial-mesenchymal transition to promote gastric cancer lymph node metastasis by activating the Wnt/β-catenin signalling pathway. Br J Cancer. 2022;126:1684-1694.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 24]  [Cited by in F6Publishing: 24]  [Article Influence: 12.0]  [Reference Citation Analysis (0)]
7.  Qian Y, Zhai E, Chen S, Liu Y, Ma Y, Chen J, Liu J, Qin C, Cao Q, Cai S. Single-cell RNA-seq dissecting heterogeneity of tumor cells and comprehensive dynamics in tumor microenvironment during lymph nodes metastasis in gastric cancer. Int J Cancer. 2022;151:1367-1381.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 15]  [Article Influence: 7.5]  [Reference Citation Analysis (0)]
8.  Huang Y, Pan M, Deng Z, Ji Y, Chen B. How useful is sentinel lymph node biopsy for the status of lymph node metastasis in cT1N0M0 gastric cancer? A systematic review and meta-analysis. Updates Surg. 2021;73:1275-1284.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 1]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
9.  Wu L, Zhong Y, Wu D, Xu P, Ruan X, Yan J, Liu J, Li X. Immunomodulatory Factor TIM3 of Cytolytic Active Genes Affected the Survival and Prognosis of Lung Adenocarcinoma Patients by Multi-Omics Analysis. Biomedicines. 2022;10.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
10.  Chen X, Chen Y, Li T, Liang W, Huang H, Su H, Sui C, Hu Y, Chen H, Lin T, Chen T, Zhao L, Liu H, Li G, Yu J. Diabetes mellitus promoted lymph node metastasis in gastric cancer: a 15-year single-institution experience. Chin Med J (Engl). 2022;135:950-961.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 3]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
11.  Guo X, Gu J, Xue A, Song S, Liu B, Gao X, Chang L, Ruan Y. Loss of GNE Predicts Lymph Node Metastasis in Early Gastric Cancer. Cells. 2022;11.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
12.  Li X, Zhai J, Shen Y, Zhang T, Wang Y, He Y, You Q, Shen L. Tumor-derived IL-8 facilitates lymph node metastasis of gastric cancer via PD-1 up-regulation in CD8(+) T cells. Cancer Immunol Immunother. 2022;71:3057-3070.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Reference Citation Analysis (0)]
13.  Xiao J, Shen K, Liu K, Wang Y, Fan H, Cheng Q, Zhou X, Hu L, Wang G, Xu Z, Yang L. Obesity promotes lipid accumulation in lymph node metastasis of gastric cancer: a retrospective case-control study. Lipids Health Dis. 2022;21:123.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 4]  [Reference Citation Analysis (0)]
14.  Cai F, Dong Y, Wang P, Zhang L, Yang Y, Liu Y, Wang X, Zhang R, Liang H, Sun Y, Deng J. Risk assessment of lymph node metastasis in early gastric cancer: Establishment and validation of a Seven-point scoring model. Surgery. 2022;171:1273-1280.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 1]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
15.  Wu L, Liu Q, Ruan X, Luan X, Zhong Y, Liu J, Yan J, Li X. Multiple Omics Analysis of the Role of RBM10 Gene Instability in Immune Regulation and Drug Sensitivity in Patients with Lung Adenocarcinoma (LUAD). Biomedicines. 2023;11.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
16.  Díaz Del Arco C, Ortega Medina L, Estrada Muñoz L, García Gómez de Las Heras S, Fernández Aceñero MJ. Pathologic Lymph Node Staging of Gastric Cancer. Am J Clin Pathol. 2021;156:749-765.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 1]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
17.  Ma D, Zhang Y, Shao X, Wu C, Wu J. PET/CT for Predicting Occult Lymph Node Metastasis in Gastric Cancer. Curr Oncol. 2022;29:6523-6539.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 11]  [Reference Citation Analysis (0)]
18.  Wu L, Zhong Y, Yu X, Wu D, Xu P, Lv L, Ruan X, Liu Q, Feng Y, Liu J, Li X. Selective poly adenylation predicts the efficacy of immunotherapy in patients with lung adenocarcinoma by multiple omics research. Anticancer Drugs. 2022;33:943-959.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 8]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
19.  Yang Q, Feng S, Liu H, Zhang X, Cao J, Zhu Y, Zheng H, Song H. Clinicopathological features and lymph node metastasis risk in early gastric cancer with WHO criteria in China: 304 cases analysis. Ann Diagn Pathol. 2021;50:151652.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
20.  Yao J, Zhang Y, Xia Y, Zhu C, Wen X, Liu T, Da M. PRRX1 promotes lymph node metastasis of gastric cancer by regulating epithelial-mesenchymal transition. Medicine (Baltimore). 2021;100:e24674.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Reference Citation Analysis (0)]
21.  Kotecha K, Singla A, Townend P, Merrett N. Association between neutrophil-lymphocyte ratio and lymph node metastasis in gastric cancer: A meta-analysis. Medicine (Baltimore). 2022;101:e29300.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Reference Citation Analysis (0)]
22.  Wang X, Chen Y, Gao Y, Zhang H, Guan Z, Dong Z, Zheng Y, Jiang J, Yang H, Wang L, Huang X, Ai L, Yu W, Li H, Dong C, Zhou Z, Liu X, Yu G. Predicting gastric cancer outcome from resected lymph node histopathology images using deep learning. Nat Commun. 2021;12:1637.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 53]  [Article Influence: 17.7]  [Reference Citation Analysis (0)]
23.  Yang J, Wu Q, Xu L, Wang Z, Su K, Liu R, Yen EA, Liu S, Qin J, Rong Y, Lu Y, Niu T. Integrating tumor and nodal radiomics to predict lymph node metastasis in gastric cancer. Radiother Oncol. 2020;150:89-96.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 17]  [Cited by in F6Publishing: 30]  [Article Influence: 7.5]  [Reference Citation Analysis (0)]
24.  Wang B, Zhang Y, Qing T, Xing K, Li J, Zhen T, Zhu S, Zhan X. Comprehensive analysis of metastatic gastric cancer tumour cells using single-cell RNA-seq. Sci Rep. 2021;11:1141.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 27]  [Article Influence: 9.0]  [Reference Citation Analysis (0)]
25.  Zhou CM, Wang Y, Ye HT, Yan S, Ji M, Liu P, Yang JJ. Machine learning predicts lymph node metastasis of poorly differentiated-type intramucosal gastric cancer. Sci Rep. 2021;11:1300.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 16]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
26.  Wu L, Zheng Y, Ruan X, Wu D, Xu P, Liu J, Li X. Long-chain noncoding ribonucleic acids affect the survival and prognosis of patients with esophageal adenocarcinoma through the autophagy pathway: construction of a prognostic model. Anticancer Drugs. 2022;33:e590-e603.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 12]  [Article Influence: 6.0]  [Reference Citation Analysis (0)]
27.  Milhomem LM, Milhomem-Cardoso DM, da Mota OM, Mota ED, Kagan A, Filho JBS. Risk of lymph node metastasis in early gastric cancer and indications for endoscopic resection: is it worth applying the east rules to the west? Surg Endosc. 2021;35:4380-4388.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 4]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
28.  Zhao B, Huang R, Lu H, Mei D, Bao S, Xu H, Huang B. Risk of lymph node metastasis and prognostic outcome in early gastric cancer patients with mixed histologic type. Curr Probl Cancer. 2020;44:100579.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 11]  [Article Influence: 2.8]  [Reference Citation Analysis (0)]
29.  Watanabe A, McKendry GJ, Yip L, Donnellan F, Hamilton TD. Risk of lymph node metastasis in early gastric cancer for a Western population. J Surg Oncol. 2023;127:791-797.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
30.  Wu L, Li X, Qian X, Wang S, Liu J, Yan J. Lipid Nanoparticle (LNP) Delivery Carrier-Assisted Targeted Controlled Release mRNA Vaccines in Tumor Immunity. Vaccines (Basel). 2024;12.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
31.  Khalayleh H, Kim YW, Yoon HM, Ryu KW. Assessment of Lymph Node Metastasis in Patients With Gastric Cancer to Identify Those Suitable for Middle Segmental Gastrectomy. JAMA Netw Open. 2021;4:e211840.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
32.  Zhu H, Wang G, Zheng J, Zhu H, Huang J, Luo E, Hu X, Wei Y, Wang C, Xu A, He X. Preoperative prediction for lymph node metastasis in early gastric cancer by interpretable machine learning models: A multicenter study. Surgery. 2022;171:1543-1551.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 3]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
33.  Ren MH, Qi XS, Chu YN, Yu YN, Chen YQ, Zhang P, Mao T, Tian ZB. Risk of Lymph Node Metastasis and Feasibility of Endoscopic Treatment in Ulcerative Early Gastric Cancer. Ann Surg Oncol. 2021;28:2407-2417.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 6]  [Cited by in F6Publishing: 6]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
34.  Yang J, Wang L, Qin J, Du J, Ding M, Niu T, Li R. Multi-view learning for lymph node metastasis prediction using tumor and nodal radiomics in gastric cancer. Phys Med Biol. 2022;67.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
35.  Wu L, Li H, Liu Y, Fan Z, Xu J, Li N, Qian X, Lin Z, Li X, Yan J. Research progress of 3D-bioprinted functional pancreas and in vitro tumor models. Int J Bioprinting. 2024;10:1256.  [PubMed]  [DOI]  [Cited in This Article: ]
36.  Chen J, Zhao G, Wang Y. Analysis of lymph node metastasis in early gastric cancer: a single institutional experience from China. World J Surg Oncol. 2020;18:57.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 12]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
37.  Li S, Zhao Z, Yang H, Wang D, Sun W, Li S, Zhang Z, Fu W. Construction and Validation of a Nomogram for the Preoperative Prediction of Lymph Node Metastasis in Gastric Cancer. Cancer Control. 2021;28:10732748211027160.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 3]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
38.  Wu L, Chen X, Zeng Q, Lai Z, Fan Z, Ruan X, Li X, Yan J. NR5A2 gene affects the overall survival of LUAD patients by regulating the activity of CSCs through SNP pathway by OCLR algorithm and immune score. Heliyon. 2024;10:e28282.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
39.  Lu H, Zhao B, Huang R, Sun Y, Zhu Z, Xu H, Huang B. Central lymph node metastasis is predictive of survival in advanced gastric cancer patients treated with D2 lymphadenectomy. BMC Gastroenterol. 2021;21:15.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 4]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
40.  de Jongh C, Triemstra L, van der Veen A, Brosens LAA, Luyer MDP, Stoot JHMB, Ruurda JP, van Hillegersberg R; LOGICA Study Group. Pattern of lymph node metastases in gastric cancer: a side-study of the multicenter LOGICA-trial. Gastric Cancer. 2022;25:1060-1072.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 7]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
41.  Zhang M, Ding C, Xu L, Feng S, Ling Y, Guo J, Liang Y, Zhou Z, Chen Y, Qiu H. A nomogram to predict risk of lymph node metastasis in early gastric cancer. Sci Rep. 2021;11:22873.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4]  [Cited by in F6Publishing: 6]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]