Wang SY, Wang JH, Chen RK, Yuan Z, Cui H, Wei B, Cui JX. Mapping the landscape of gastric signet ring cell carcinoma: Overcoming hurdles and charting new paths for advancement. World J Clin Oncol 2025; 16(2): 98983 [DOI: 10.5306/wjco.v16.i2.98983]
Corresponding Author of This Article
Bo Wei, MD, Chief Doctor, Department of General Surgery, The First Medical Center, Chinese PLA General Hospital, No. 28 Fuxing Road, Beijing 100853, China. weibo@301hospital.com.cn
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Scientometrics
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/
Shu-Yuan Wang, Jing-Hang Wang, Zhen Yuan, Hao Cui, School of Medicine, Nankai University, Tianjin 300071, China
Jing-Hang Wang, Run-Kai Chen, Zhen Yuan, Hao Cui, Bo Wei, Jian-Xin Cui, Department of General Surgery, The First Medical Center, Chinese PLA General Hospital, Beijing 100853, China
Co-first authors: Shu-Yuan Wang and Jing-Hang Wang.
Co-corresponding authors: Bo Wei and Jian-Xin Cui.
Author contributions: Wang SY and Wang JH contribute equally to this study as co-first authors; Cui JX and Wei B contribute equally to this study as co-corresponding authors; Wang SY contributed to design of the study, data analysis and design; Wang JH contributed to data collection, figure revision and draft manuscript; Chen RK, Cui H and Yuan Z contributed to make significant revisions to the thesis; Cui JX and Wei B contributed to fund and approval of the final version of the paper.
Supported by National Natural Science Foundation of China, No. 82073192, and No. 82273231; and Beijing Science and Technology Program, No. Z221100007422125.
Conflict-of-interest statement: The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
PRISMA 2009 Checklist statement: The authors have read the PRISMA 2009 Checklist, and the manuscript was prepared and revised according to the PRISMA 2009 Checklist.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Bo Wei, MD, Chief Doctor, Department of General Surgery, The First Medical Center, Chinese PLA General Hospital, No. 28 Fuxing Road, Beijing 100853, China. weibo@301hospital.com.cn
Received: July 10, 2024 Revised: September 26, 2024 Accepted: November 13, 2024 Published online: February 24, 2025 Processing time: 153 Days and 20.1 Hours
Abstract
BACKGROUND
In recent years, the global prevalence of gastric cancer (GC) has witnessed a progressive decrease, accompanied by a step-growth in the incidence of gastric signet ring cell carcinoma (GSRCC). As precision medicine concepts progress, GSRCC, a distinct sub-type of GC, has drawn considerable attention from researchers. However, there still persist some controversies regarding the associated research findings.
AIM
To summarize the current obstacles and potential future directions for research on GSRCC.
METHODS
To begin with, all literature related to GSRCC published from January 1, 2004 to December 31, 2023 was subjected to bibliometric analysis in this article. Additionally, this paper analyzed the research data using CiteSpace, GraphPad Prism v8.0.2, and VOSviewer, which was obtained from the Web of Science Core Collection database. The analysis results were visually represented.
RESULTS
This study provided a comprehensive overview of the statistical characteristics of the 995 English articles related to GSRCC, including cited references, authors, journals, countries, institutions, and keywords. The popular keywords and clusters contain "prognosis", "survival", "expression", "histology", and "chemotherapy".
CONCLUSION
The prognosis, precise definition and classification, as well as chemoresistance of GSRCC, continue to be crucial areas of ongoing research, whose directions are closely tied to advancements in molecular biology research on GSRCC.
Core Tip: In this paper, the bibliometric analysis method was employed to analyze articles on the study of gastric signet ring cell carcinoma (GSRCC), and the analysis results were presented visually. The prognosis, precise definition and classification, as well as chemoresistance of GSRCC, keep up to be focal points of current research. Advancements in molecular biology research on GSRCC are indispensable for future progress in this area.
Citation: Wang SY, Wang JH, Chen RK, Yuan Z, Cui H, Wei B, Cui JX. Mapping the landscape of gastric signet ring cell carcinoma: Overcoming hurdles and charting new paths for advancement. World J Clin Oncol 2025; 16(2): 98983
Gastric cancer (GC) is an extremely malignant disease, ranking fifth in global incidence and fourth in cancer-related mortality worldwide. Furthermore, GC demonstrates a significant degree of heterogeneity[1,2]. In recent years, the incidence rate of GC in most locations worldwide has declined dramatically, mainly due to the remarkable success achieved in the treatment of Helicobacter pylori infection[3,4]. However, gastric signet ring cell carcinoma (GSRCC), as a unique sub-type of gastric cancer, is on the rise in prevalence in Asia, Europe, and the United States[5]. Despite the increasing understanding of the epidemiological, pathological, histological, and molecular biological characteristics of GSRCC in recent years, as well as the rapid advancement of diagnostic and therapeutic approaches, research in the field of GRSCC continues to encounter numerous obstacles[6].
GSRCC is a specific type of low cohesiveness (PC) GC characterized by the presence of substantial cytoplasmic mucins and eccentrically located in crescent-shaped nuclei when observed under a microscope. According to Lauren's classification[7], GSRCC is categorized as a sub-type of diffuse gastric cancer. The Japanese Gastric Cancer Association (JGCA)[8] classifies GSRCC as a type of poorly differentiated adenocarcinoma. Since the fourth edition, the World Health Organization (WHO) classification[9] criteria have identified GSRCC as a sub-type of PC cancer. According to the latest classification of the WHO[10], PC types are further divided into two sub-types: one is the signet ring cell carcinoma (SRCC) sub-type, which is featured by the presence of signet ring cells (SRC) exceeding 90%, and the second is PC (PC-NOS), which is unspecified. Currently, different studies use different classification standards, which to some extent results in inconsistent research conclusions[11].
Compared to other types of GC, GSRCC presents unique characteristics, such as a younger age of onset, a higher incidence in female patients, a greater proportion of patients presenting at advanced stages, a higher likelihood of lymph node and peritoneal metastasis, as well as a more rapid disease progression[12-14]. Despite numerous studies investigating the prognostic factors of GSRCC, the results remain inconsistent. To be specific, some research indicates that GSRCC exhibits a more favorable prognosis compared to other forms of gastric cancer. Conversely, other studies have found that GSRCC is associated with a less favorable prognosis[13,15-17]. In recent years, there has been a surge of interest in studying the responsiveness of GSRCC to neoadjuvant therapy in recent years, resulting in a substantial amount of research[17-22].
Bibliometric analysis is a quantitative method used to assess the body of literature published in public databases over some time[23]. By integrating bibliometric analysis with visualization tools, the findings can be effectively presented using charts, thereby enhancing researchers' comprehension of the current research status and potential future advancements in the field. The purpose of this study is to conduct a bibliometric analysis of research related to GSRCC, so as to illustrate the present research status in this field and determine the prospects for future research. Furthermore, this study aims to encourage further exploration of contemporary controversial issues.
MATERIALS AND METHODS
The Web of Science Core Collection (WoSCC) database is renowned for its exceptional accuracy in classifying document types, rendering it a preferred resource for literature analysis when compared to other databases[24]. Therefore, the literature search in this paper was conducted exclusively within this database. On January 8, 2024, we searched WoSCC for all articles related to the application of GSRCC between January 1, 2004 and January 31, 2024, using the following search query: [(TS = (gastric signet-ring cell carcinoma)) OR TS = (GSRCC)] OR TS = (gastric signet ring cell carcinoma). The inclusion criteria for this study are as follows: (1) Comprehensive literary works specifically related to GSRCC; (2) Articles and reviews written in English; and (3) Articles published between January 1, 2004 and January 31, 2024. The exclusion criteria are outlined as follows: (1) Works that are not directly related to GSRCC; and (2) Literature sources such as conference abstracts, news stories, brief reports, and similar materials. The methodology used for literature screening and search is illustrated in Figure 1.
GraphPad Prism v 8.0.2 was employed in this study to analyze and graphically represent the annual publication trends and paper ratios. Furthermore, the analysis and visualization of scientific knowledge maps were conducted using CiteSpace (6.1.6R 64-bit Advanced Edition) and VOSviewer (version 1.6.18). Specifically, VOSviewer v1.6.17, developed by van Eck et al[25] in 2010, is a Java-based, open-source software designed for analyzing extensive literature datasets and visualizing the results in the form of maps. Professor Chen[26] developed the CiteSpace (6.1.6R) software to visualize research outcomes in a specific field by creating co-citation network maps, aiming to uncover emerging concepts and assess existing technologies within an experimental framework, thereby enhancing users' understanding of knowledge domains, research frontiers, trends, and facilitating the prediction of future research directions.
RESULTS
Annual growth trend of publications
The analysis revealed that between January 1, 2004, and January 31, 2024, the WoSCC database contained a total of 995 publications related to GSRCC. To be specific, this includes 898 articles, accounting for 93.48% of the total publications, and 97 reviews, representing 6.52% of the total. The scholarly output on GSRCC spans 63 countries and regions, includes 1258 institutions, as well as credits 5553 authors. Since 2004, the annual number of papers published has been steadily increasing (Figure 2), which were divided into three stages. First of all, from 2004 to 2016, there was a slow growth phase with annual publication numbers remaining below 50, indicating limited interest among researchers in this field. Secondly, between 2017 and 2019, there was a gradual increase in publication volumes, reflecting a growing scholarly curiosity in this subject. Finally, following 2020, there was a significant surge in the number of publications on this particular topic, peaking in 2022. This suggests a substantial increase in and focus on this field after 2020.
Figure 2 Annual growth trend of publications on gastric signet ring cell carcinoma from January 1, 2004 to January 31, 2024.
Analysis of countries/regions and institutions
Research on the GSRCC has been conducted across 63 nations and areas. Supplementary Figure 1 demonstrates the annual publication volumes of the top ten countries over the past decade. The five countries with the highest publication volumes in this specific field are China, Japan, the United States, South Korea, and Italy. Together, China and Japan account for 45.72% of the total publications, substantially surpassing other countries (Table 1). The United States ranks fourth globally with a citation-to-publication ratio of 33.02, and its papers have been cited 4722 times, which is significantly more than any other top-10 publishing country. China leads in publication count with 247 articles and ranks fourth in terms of citations with 2763 citations. However, its citation-to-publication ratio of 11.19 is relatively low, displaying that the quality of some of its published papers may not be as high as those of other top-performing countries. The collaboration networks depicted in Figure 3 emphasize the tight connections between high-output countries, particularly China and Japan. China maintains close cooperation with countries such as South Korea, France, and Canada, while Japan has stronger collaborative ties with the United States, Germany, Italy, as well as several other nations. Currently, China and Japan are recognized as leaders in this field, attributed to their substantial publication volumes and frequent citations.
Figure 3 National collaborative network for publications related to gastric signet ring cell carcinoma.
Countries are represented by nodes. Partnerships are represented by lines. The node area expands as the number of publications increases. China has close cooperation with countries such as South Korea, France, and Canada, whereas Japan has even closer collaborations with the United States, Germany, Italy, and other countries.
Table 1 The top 10 most published countries/regions.
Rank
Country/region
Article counts
Centrality
Percentage (%)
Citation
Citation per publication
1
China
247
0.02
24.82
2763
11.19
2
Japan
208
0.17
20.90
3680
17.69
3
USA
143
0.37
14.37
4722
33.02
4
South Korea
127
0.05
12.76
3198
25.18
5
Italy
50
0.11
5.03
1153
23.06
6
Turkey
44
0.00
4.42
281
6.39
7
Germany
33
0.10
3.32
993
30.09
8
France
27
0.06
2.71
1431
53.00
9
England
22
0.05
2.21
1840
83.64
10
Canada
22
0.03
2.21
1291
58.68
As shown in Table 2, 1258 institutions systematically published articles on GSRCC. Yonsei University had the highest number of publications, with a total of 32 papers and 907 citations, yielding an average of 28.34 citations per paper. The Yonsei University Health System achieved the second highest ranking, with a total of 31 publications, 905 citations, and an average of 29.19 citations per paper. Following closely behind was the Chinese Academy of Medical Sciences - Peking Union Medical College, which took the third position with 23 papers, 248 citations, and an average of 10.78 citations per paper. After conducting further analysis, we found a tendency for institutions from different countries/regions to collaborate more frequently with their respective national counterparts (Supplementary Figure 2). Therefore, we advocate for fostering enhanced collaboration between institutions across different countries to break down academic barriers.
The top 10 journals with the highest output are detailed in Table 3. Leading the pack is the World Journal of Gastroenterology with 41 publications, accounting for 5.13% of the total, followed by Gastric Cancer with 39 papers (4.37%) and Frontiers in Oncology with 21 (3.41%). The Annals of Surgical Oncology contributes 20 papers, representing 1.55% of the total. Among the top ten journals, Gastric Cancer boasts the highest impact factor (IF) of 7.4. Moreover, 70% of these journals are classified as Q1 or Q2. The impact of a journal is measured by its co-citation frequency, indicating its influence within the scientific community. As displayed in Figure 4A and Table 4, Gastric Cancer is the most frequently co-cited journal, with 475 instances, followed by Cancer (398) and the World Journal of Gastroenterology (386). The Journal of Clinical Oncology, which has been cited 308 times, ranks among the top 10 most co-cited journals and boasts the highest IF of 45.4. Additionally, 90% of the articles are classified as Q1/Q2.
Figure 4 Visualization of journals related to gastric signet ring cell.
A: Network visualization of co-cited journals. The size of the circle indicates the number of co-citations. The journals most frequently co-cited are Gastric Cancer, followed closely by Cancer and World Journal of Gastroenterology; B: A dual-map overlay presents journals related to gastric signet ring cell carcinoma with citing journals displayed on the left and cited journals on the right. The colored paths between them illustrate the citation relationships. Research published in molecular/biology/immunology journals is predominantly cited by journals in the molecular/biology/genetics field, while research published in medicine/medical/clinical is mainly cited by journals in the molecular/biology/genetics as well as health/nursing/medicine fields.
The thematic distribution of academic publications is depicted in the dual-map overlay (Figure 4B). The colored trajectories represent reference paths, with the citing journals positioned on the left and the cited journals on the right. The display results show three primary colored reference paths: Research published in molecular/biology/immunology journals is predominantly cited by journals in the molecular/biology/genetics field, while journals in the domains of molecular/biology/genetics/health/nursing/medicine primarily refer to research published in the field of medicine/medical/clinical.
Analysis of authors
The top 10 writers who published articles on GSRCC are listed in Table 5 according to their publication count ranking. Collectively, these authors have contributed a total of 129 publications, accounting for 12.96% of the total literature on this topic. Sung Hoon Noh is the leading author with 21 papers, followed closely by Yong Chan Lee with 18, and Jie-Hyun Kim with 15. Further analysis indicates that 8 out of the top 10 authors hail from South Korea, while one each originates from France and the United States. The network between authors has been visualized using CiteSpace (Supplementary Figure 3).
The top ten authors with the highest number of co-citations and citations are illustrated in Table 5. Among them, 31 authors have been cited more than 50 times, demonstrating that their research is highly valued and influenced. Supplementary Figure 4 visualizes the relationship among co-cited authors in the field of GSRCC. The largest nodes correspond to the authors with the highest number of co-citations, namely Pekka Laurén (189 citations), the JGCA (130 citations), as well as Guillaume Piessen (126 citations).
Analysis of co-cited references
The co-cited reference network from 2004 to 2023 comprises 822 nodes and 3268 linkages (Supplementary Figure 5). The paper titled "Differential Prognostic Implications of Gastric Signet Ring Cell Carcinoma: Stage Adjusted Analysis From a Single High-volume Center in Asia"[13], published in Annals of Surgery (IF = 10.1) is the most frequently referenced article among the top 10 most co-cited papers (Supplementary Table 1). Chon Hong Jae is the first author of this paper. The study primarily focuses on examining the clinical pathological characteristics and prognosis of SRCC in the context of the disease status of GC patients, with a particular emphasis on distinguishing between early-stage GC and advanced-stage GC. In addition, we conducted an analysis of the clustering of co-cited references and generated a timeline view of these co-cited references (Figure 5). It is also found that early hot research fields include "prophylactic gastrectomy", "syndecan-1", "tubular adenocarcinoma", and "NADPH oxidase 1". "Signet ring cell", "FDG-PET", "recurrence", "diffuse", "CDH1", as well as "colorectum" are mid-term research hotspots. Currently, the hot topics and trends in this field include "Poorly cohesive", "lobular breast cancer", and "gastrectomy".
Figure 5 Visualization of co-cited references related to gastric signet ring cell carcinoma.
A: Knowledge map of co-cited references. Different colors represent distinct clusters; B: Timeline view of co-cited references related to GSRCC. “Prophylactic gastrectomy”, “syndecan-1”, “tubular adenocarcinoma”, as well as “NADPH oxidase 1” are among the early research hotspots. “Signet ring cell”, “FDG-PET”, “recurrence”, “diffuse”, “CDH1”, and “colorectum” are considered as mid-term research hot topics. “Poorly cohesive”, “lobular breast cancer”, and “gastrectomy” currently represent the hot topics and trends in this field.
Analysis of keywords
By analyzing keywords, one can quickly comprehend the status and development direction of a particular field. The VOSviewer analysis of keyword co-occurrence indicates that the keyword "prognosis" is the most prevalent (174), followed by "survival" (133), "expression" (113), and "histology" (87; Table 6). After filtering out irrelevant keywords, a network was established consisting of 178 keywords appearing at least 8 times. This process led to the identification of 6 distinct clusters: "Signet-ring cell carcinoma", "cdh1", "lymph node metastasis", "gastric cancer", "preoperative chemotherapy", "helicobacter pylori", "stomach neoplasms", "skin metastasis", as well as "carbohydrate". A volcano plot was generated using CiteSpace to visually illustrate the shifts in research hotspots over time (Figure 6).
Figure 6 The keyword clustering volcano plot visually demonstrates how research hotspots evolve and shift over time.
Burst analysis of co-cited references and keywords
Using CiteSpace, the 50 most important citation bursts in the field of GSRCC were identified. The article titled "Signet-ring cell carcinoma of the stomach: impact on prognosis and specific therapeutic challenge"[27] published in the World Journal of Gastroenterology boasted the highest citation rate (18.05). In this article, the authors conducted a comprehensive analysis of the latest data on the epidemiology, carcinogenesis, prognosis, and targeted therapy strategies of early and late stage GSRCC, as well as hereditary diffuse GC. Of the total 50 references, 49 were published between 2004 and 2023, indicating a high citation frequency for these articles over the two decades. It is worth noting that 13 of these works are currently experiencing a surge in citation activity (Supplementary Figure 6), displaying that research on GSRCC will continue to stimulate interest in the academic community in the forthcoming years.
Our attention was directed toward the top 50 keywords that demonstrated the most substantial bursts among the 432 strongest burst keywords in this category (Supplementary Figure 7). These keywords currently represent the core research area in the field and offer promising directions for future studies.
DISCUSSION
Country, institution and author
China has made a notable contribution to the study of GSRCC, as evidenced by its substantial publication output among the 63 nations or regions engaged in research on this topic over the past decade. This is also correlated with China's large population and, most importantly, the high incidence rate of GC[28,29]. The prevalence of gastric cancer in East Asia has significantly contributed to advancements in research on GRSCC[28]. The affiliations of literature, including the countries and institutions involved, are frequently intertwined with the background and profiles of authors. Consequently, the bibliometric analysis outcomes presented above demonstrate a discernible level of correlation among these different elements. For instance, China and South Korea are ranked among the top five countries in terms of publication output. Furthermore, five Chinese institutions and three South Korean institutions are listed within the top 10 in terms of publication volume. Although the total publication volumes in South Korea are lower than those in China, both Yonsei University and Yonsei University Health System in South Korea rank among the top two in terms of publication and citation counts. This to some extent reflects that compared to other research institutions in South Korea, these two universities place more emphasis on research related to GSRCC. As for the writers, it is noteworthy that 8 out of the top 10 authors with the highest publication volume are from South Korea. In addition, Sung Hoon Noh, who has the most publications, is also affiliated with Yonsei University. Sung Hoon Noh and colleagues[13] published a study in the Annals of Surgery (IF = 10.1) titled "Differential Prognostic Implications of Gastric Signet Ring Cell Carcinoma: Stage-Adjusted Analysis from a Single High-Volume Center in Asia", which is the most cited publication on GSRCC. This study analyzed the clinical-pathological characteristics and prognosis of GSRCC at various stages of progression and found that the prognosis of GSRCC progressively deteriorates with disease progression. In another study, Kim et al[30] demonstrated that the presence of tubular elements in GSRCC is associated with a higher likelihood of lymph node metastasis in poorly cohesive, submucosa-invasive early gastric carcinoma (EGC). This discovery provides valuable insights into forecasting the biological characteristics of EGC.
Some conclusions can be drawn from the inconsistencies among countries, institutions, and authors. Despite Japan ranking second in the number of publications related to GSRCC, none of the top ten institutions or authors publishing such papers are from Japan. This partially indicates that, although Japanese research institutions attach importance to GSRCC-related research, none of them has achieved a particularly prominent standing in this field compared to other domestic institutions, unlike Yonsei University and Yonsei University Health System in South Korea. While the United States does not have the highest number of publications, its 4722 citations exceed those of other countries or regions, indicating the exceptional quality of research on GSRCC in the United States. Notably, Harvard University ranks eighth in publications but third in total citations. These results emphasize the outstanding quality of research on GSRCC conducted by Harvard University.
The above analysis in this article indicates that the leading countries in GSRCC-related research are predominantly located in economically developed regions such as Western Europe, North America, and East Asia. This distribution highlights the necessity of substantial financial support for medical research, which is closely associated with the economic status of the area. The relatively high level of medical care in these economically prosperous regions enables patients to receive screenings and interventions in the early stages of disease progression, which in turn significantly affects the diagnosis, treatment, and prognosis of SRCC.
Journal
More than 20 articles on GSRCC research have been published in the World Journal of Gastroenterology, Gastric Cancer, Frontiers in Oncology, and Annals of Surgical Oncology, all of which are classified as Journal Citation Reports Q1 or Q2. However, analysis of journal co-citations reveals that Frontiers in Oncology is the only one among these four journals that is not in the top 10 most frequently cited, showing that the quality of some articles in this journal may be lower than the other three widely recognized journals. So, researchers can be guided in choosing journals for publication and staying up-to-date with the latest GSRCC research. The dual-map overlay shows that journals in molecular biology/genetics tend to cite research from the fields of molecular biology/immunology, while those in molecular biology/genetics/health/nursing/medicine frequently cite work originating from medicine/medical/clinical fields, indicating that current research on GSRCC is predominantly focused on the translation and correlation between basic research findings and clinical applications.
Reference
The literature co-citation analysis highlights that the association between GSRCC and prognosis is a prominent focus in the top 10 most frequently referenced articles. The most cited article conducted a retrospective analysis using the clinical records of 7667 patients including 1646 GSRCC patients who underwent radical gastrectomy between 2001 and 2010 from a single center in Asia[13]. The study suggests that the prognosis of GSRCC is influenced by the stage of disease progression, with better early prognosis and poorer late prognosis. The larger sample size has, to a certain extent, increased the credibility of the results, which may be the reason why this article is frequently cited by researchers. The findings of this study also underscore, to a certain degree, the significance of early diagnosis and prompt intervention in improving the prognosis for patients with GSRCC. In clinical practice, timely curative treatment may be more necessary for early discovered GSRCC compared to other types of GC. However, the study only involved GC patients who underwent radical resection and did not include patients with distant metastasis who could not undergo surgical resection. Therefore, it cannot comprehensively reflect the prognosis of GSRCC. Furthermore, considering the differences in the biological characteristics of gastric cancer between Asia and Western countries, where GC of the gastroesophageal junction and the upper stomach are more predominant, the study may not adequately reflect the prognosis of GSRCC in Western countries. Thus, future multi-regional and multi-center studies with more comprehensive patient staging are needed to elucidate the prognostic features of GSRCC. An article titled "Consensus on the pathological definition and classification of poorly cohesive gastric carcinoma"[5], published in Gastric Cancer (IF = 7.4), argues that the lack of standardized definitions for sub-types of GC continues to ongoing controversies regarding the prognosis of GSRCC. The consensus primarily clarifies two points: firstly, the classification of GC should adhere to the latest WHO classification; secondly, it is advisable to categorize only those WHO PC carcinomas that contain a minimum of 90% poorly cohesive cells exhibiting SRC morphology as SRCC. PC carcinomas with an SRC component (SRC 90% and > 10%) and unspecified PC carcinomas not otherwise specified (SRC < 10%) should be employed to further classify all other non-SRCC PC types. This consensus provides a well-thought-out and reliable source for defining and categorizing GSRCC. Given the tendency of distant metastasis and invasion in GSRCC, the proportion of SRC components within the tumor should also be regarded as a factor in determining clinical treatment plans, which in turn emphasizes the need for a unified and explicit classification criterion for GSRCC.
The analysis of co-cited reference clustering and the timeline view of co-cited references reveals that early research hot topics included "prophylactic gastrectomy", "syndecan-1", "tubular adenocarcinoma", and "NADPH oxidase 1". Mid-term research centered on "signet ring cell", "FDG-PET", "recurrence", "diffuse", "CDH1", as well as "colorectum". Current hot topics encompass "poorly cohesive", "lobular breast cancer", and "gastrectomy". According to Lauren’s classification, GSRCC belongs to the "diffuse type". Based on the WHO categorization criteria[10], GSRCC is presently categorized as a type of cancer that is poorly cohesive. The characteristics of most cancer cells are significant cytoplasmic mucins and eccentrically located nuclei. The occurrence of tumors in GSRCC is distinct from that of tubular adenocarcinoma, featuring the loss of intercellular adhesion molecules and excessive accumulation of mucins in the cytoplasm at the cellular level[31]. E-cadherin plays a critical role in establishing and protecting the epithelial cell layers by facilitating intercellular adhesion interactions[32]. Mutations that inactivate the CDH1 gene encoding E-cadherin can lead to the loss of E-cadherin, which hinders the normal localization and stability of E-cadherin on the plasma membrane, thereby leading to the disruption of intercellular connections. As a result of this disruption, it facilitates the invasive growth and metastasis of tumors. One of the distinctive cellular phenotypes linked to this disruption is the abundant aggregation of SRCs[33,34].
Hereditary diffuse GC (HDGC) is typically caused by germline mutations in the CDH1 gene. Individuals with HDGC have a 70% lifetime risk of developing late stage diffuse-type GC and an increased risk of lobular breast cancer[35]. The feature of early HDGC with CDH1 germline mutations is the presence of several microscopic foci of intramucosal SRCC[36,37]. Besides, the presence of in situ SRCs and Pagetoid diffusion of SRC under the lining of gastric fovea/glandular epithelium can be observed[38]. It is recommended to perform genetic testing on patients with in situ SRC and/or SRC Pagetoid diffusion in the stomach to identify CDH1 mutations[39]. Prophylactic total gastrectomy is currently advised to manage GC risk in patients diagnosed with pathogenic CDH1 mutations[35,39]. The current consensus regarding the optimal timing for surgery is during early adulthood, generally between 20 and 30 years old[35]. Given the significant impact of this treatment on the future well-being of patients, the decision to undergo surgery necessitates comprehensive discussions, careful consideration of both advantages and disadvantages, as well as adequate preparation. A comprehensive study of surgical and postoperative clinical outcomes is crucial for effective preoperative discussions with patients[40].
Syndecan-1, like E-cadherin, is a cellular adhesion molecule involved in intercellular adhesion and extracellular matrix binding[41]. Huang et al[42] conducted a comparison of syndecan-1 and E-cadherin expression across various cell phenotypes, observing a notable decrease of syndecan-1 expression in the gastric type, in contrast to the expression of E-cadherin. The expression of Syndecan-1 was also markedly decreased in poorly differentiated carcinoma or SRCC compared to papillary adenocarcinoma and tubular adenocarcinoma within DGC. Tominaga et al[43] discovered that NADPH oxidase 1 and NOX organizer 1 (NOXO1) were not present in normal gastric tissues. However, they were co-expressed in chronic atrophic gastritis and both intestinal and diffuse types of GC, including GSRCC, indicating that NOXO1 may serve as a potential marker for GC progression. Recent advancements in sequencing technology have facilitated the identification of a growing number of molecular pathways associated with the occurrence, progression, and heterogeneity of GSRCC[44-46]. Zhao et al[47] employed single-cell sequencing technology to discover that microseminoprotein-beta can function as a marker for confirming the presence of moderately/poorly differentiated GC and GSRCC. Investigating molecular biology plays a significant role in improving the accuracy of diagnosing and treating GSRCC. In the future, precise treatment of GSRCC will require further exploration of more specific and high-quality markers.
Several studies have demonstrated that the poorer prognosis of GSRCC compared to non-SRCC is partly due to its higher postoperative recurrence rate. Lee et al[48] retrospectively analyzed the clinical data of 764 GC patients who had undergone curative resection. The data analysis revealed that patients with T3 and T4 stages with neural invasion had a significantly elevated rate of postoperative peritoneal recurrence with SRCC compared to those without SRCC (28.7% vs 13.7%; P = 0.001). However, there was no significant difference in the incidence of postoperative peritoneal recurrence among individuals who did not belong to stage T3 or T4. Kong et al[49] further suggested that patients diagnosed with GSRCC who underwent total gastrectomy and D2 lymph node dissection had a decreased recurrence-free survival rate, which they attributed to invasive cytological features of SRCs.
18F-FDG positron emission tomography (PET)/computed tomography (CT) can be used to monitor the progression and recurrence of postoperative GC in that it provides both morphological and functional information concurrently[50,51]. Given the heterogeneity of GC, several studies have investigated the varying levels of 18F-FDG uptake among different histological types of GC, including GSRCC. Certain research findings indicate that the rate of 18F-FDG absorption in SRCC is relatively lower than that in non-SRCC. This disparity, to a certain extent, enhances the sensitivity and specificity of 18F-FDG PET/CT in diagnosing non-SRCC compared to SRCC[51-53]. In recent years, novel contrast agents have been increasingly applied in the clinical diagnosis of GC. A multicenter retrospective study conducted by Chen et al[54] demonstrated that [68Ga] Ga-FAPI PET exhibited higher maximum standard uptake values and tumor-to-background ratios in the diagnosis of primary tumors, positive lymph nodes, bone, and visceral metastases, in comparison to 18F-FDG PET. A case report by Fan et al[55] also yielded similar findings, and other FAP-based tracers have demonstrated superior diagnostic capabilities compared to 18F-FDG in GSRCC[56,57].
Keyword
Keywords reflect the research directions of all the literature included in this study, while reference analysis mirrors the research interests of articles that have been frequently cited by researchers. There exists a certain level of correlation between these two elements. We can deduce that if a keyword has a high frequency of occurrence and also appears regularly in reference analysis, then it indicates that this keyword represents a prevalent research topic. Based on the high-frequency keyword list derived from keyword analysis, "prognosis" is the hottest keyword, with "survival" ranking second and also belonging to the category of prognosis. The paper titled "Differential Prognostic Implications of Gastric Signet Ring Cell Carcinoma: Stage Adjusted Analysis From a Single High-volume Center in Asia"[13] in Annals of Surgery (IF = 10.1) is the most frequently cited reference among the top 10 most co-cited articles (Supplementary Table 1). Among the 50 most reliable citation bursts in the field of GSRCC, the article titled "Signet-ring cell carcinoma of the stomach: impact on prognosis and specific therapeutic challenge"[27] published in the World Journal of Gastroenterology exhibited the highest citation rate (18.05). Both of the aforementioned articles concentrate on the prognosis of GSRCC. At present, it is widely believed that GSRCC has a similar or even better prognosis for EGC compared to other forms of GC, and numerous researches have confirmed this perspective[58,59], including a large retrospective study involving 1520 EGC patients[60]. As for advanced GC, there currently exists some controversy, with findings from some studies indicating that the prognosis of GSRCC is poorer compared to other histological types[61-64]. However, a large retrospective study conducted by Taghavi et al[12], which included 10246 American GC patients, revealed that although GSRCC is more commonly observed in advanced disease stages compared to other histological types of GC, it did not display a worse prognosis across different stages. On basis of the above results, we believe that it is crucial to further refine the definition and staging of GSRCC to better guide its clinical treatment.
"Expression" ranks as the third most frequent keyword. With the progress of sequencing technology and gene editing techniques, researchers are no longer confined to studying cancer at the cellular phenotype level; They now have the capability to delve into the genetic level to explore the characteristics of gene expression in cancer cells. This approach investigates the mechanisms that drive the development of various types of cancer and their implications for clinical treatment[65,66]. Togasaki et al[67] discovered that the removal of Wnt and R-spondin (WR) from the culture medium resulted in the transformation of PC-NOS organoids into cells that exhibited the morphology of SRCC. Moreover, the reintroduction of WR into the culture media resulted in the reversal of the morphology of TP53 gene-mutated SRCC to PC-NOS, allowing for subsequent proliferation. This study unveiled a possible molecular mechanism for the development of GSRCC. Chen et al[68] conducted an analysis of the immune microenvironment of tumors by using single-cell sequencing technology and proteomics. The study demonstrated that SRCC shows a decreased response to adaptive immunity compared to non-SRCC. Furthermore, it elucidated the impact of chemokine (C-X-C motif) ligand 13 on the immunological milieu of GSRCC. In recent years, as cancer treatment has shifted towards personalized and precision medicine, we believe that studying the gene expression of GSRCC to identify highly specific expressed genes that can guide the diagnosis and precision treatment of GSRCC represents one of the future research areas.
The term "chemotherapy" is among the top five most frequently keywords. According to a retrospective study by Lemoine et al[19], which included 230 patients with locally advanced or metastatic GC undergoing chemotherapy, patients with SRCC demonstrated a lower degree of benefit from chemotherapy compared to those with non-SRCC. Regarding postoperative chemotherapy, the majority of studies suggest that GSRCC patients do not experience significant benefits from adjuvant chemotherapy[18,69]. A controlled clinical trial led by Messager et al[15], involving 3010 patients with GC, revealed that patients with GSRCC did not derive any advantages from neoadjuvant chemotherapy and had a shorter median survival time following this treatment. Research by Li et al[18] also reached a similar conclusion.
The mechanism of cancer chemoresistance has been a focal point in cancer treatment for a considerable time. Given its unique characteristics in histology and gene expression, researchers have also pondered whether GSRCC possesses distinct chemoresistance mechanisms. Through transcriptome sequencing, Phoo et al[70] uncovered that Aldo-Ketoreductase 1C1 and 1C3 play a role in mediating the resistance of GSRCC to cisplatin by regulating autophagy. Shu et al[45] performed whole-genome sequencing on 32 matched specimens of GSRCC and found that patients with the CLDN18-ARHGAP26/6 fusion had a worse prognosis and did not respond favorably to oxaliplatin/ fluoropyrimidine-based treatment. We believe that given the increasing attention, researchers have given to tumor drug resistance mechanisms in recent years, studying the unique drug resistance mechanisms of GSRCC is likely to emerge as a future hot research direction.
Limitation
Due to the inherent limitations of bibliometric analysis methods, this study inevitably faces certain constraints: (1) The publications cited in this study are exclusively sourced from the WoSCC database. All articles included in the study are written in English, which may result in partial representativeness of the available literature; (2) Our evaluation criteria for included articles primarily focus on their impact, which may result in overlooking other factors that could influence the results; (3) Compared to the later published articles, early published articles have relatively more opportunities to be viewed and cited, leading to a certain bias in our analysis results. In subsequent investigations, more precise and all-encompassing research must be conducted to evaluate the current research status of GSRCC; (4) Individual differences, clinical symptoms, and treatment responses of patients were not fully considered in this study, which are also of great significance for the research and treatment of GSRCC; (5) This study may not comprehensively capture the characteristics and trends of interdisciplinary research in the analysis, and insufficient attention is given to the intersection and integration of different disciplines; and (6) The study mentioned the influencing factors and co-citation situations of some journals, but it lacks an in-depth evaluation and analysis of the research quality of the literature itself, such as the scientificity of the research methods and the reliability of the research findings. Further research, such as meta-analyses, is required to evaluate the quality and credibility of the findings in studies related to GSRCC.
CONCLUSION
The study conducts a bibliometric analysis of articles on GSRCC and presents the analysis results visually. In summary, prognosis continues to be a key topic in GSRCC research, although currently, there is still a controversy surrounding the prognosis of GSRCC, which is partly attributed to the lack of a unified definition for this cancer type. In the future, it is imperative to establish a standard classification method for differentiating the various sub-types of GC, enabling precise and effective treatment for patients with GSRCC. Given the high invasiveness of GSRCC, there will be an increasing need for more precise diagnostic methods in the future for early detection and continuous monitoring of the disease. The chemoresistance of GSRCC is another urgent issue that needs to be addressed, requiring attention from researchers. We firmly believe that addressing the aforementioned issues necessitates advancements in molecular biology research on GSRCC, as basic research will pave the way for more effective clinical treatments in the future.
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 D
Novelty: Grade B
Creativity or Innovation: Grade C
Scientific Significance: Grade C
P-Reviewer: Wang C S-Editor: Lin C L-Editor: A P-Editor: Zhao YQ
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