Introduction

Lung cancer is one of the leading causes of cancer-related deaths worldwide, accounting for approximately 1.8 million new cases and 1.6 million deaths each year [1]. Surgical resection remains the primary treatment for early-stage non-small cell lung cancer (NSCLC), with lobectomy being the standard procedure for most patients [2]. However, for patients with compromised lung function or other comorbidities, a less invasive surgical approach, such as segmentectomy or wedge resection, may be more appropriate [3]. Segmentectomy, also known as sublobectomy or anatomical segmental resection, involves the removal of a specific bronchopulmonary segment, preserving more lung parenchyma than lobectomy [4].

In recent years, there has been a growing interest in sublobectomy as a potential alternative to lobectomy for early-stage NSCLC, particularly for patients with small, peripheral tumors [5]. Several studies have reported comparable oncological outcomes between segmentectomy and lobectomy for tumors less than 2 cm in size [6,7,8,9,10]. Moreover, sublobectomy has been associated with better preservation of lung function, shorter hospital stays, and fewer postoperative complications compared to lobectomy [8, 11].

Given the increasing importance of sublobectomy in the management of early-stage NSCLC, it is crucial to understand the current state of research in this field. Bibliometric analysis is a useful tool for evaluating the scientific impact of research articles and identifying trends in a specific research area [12]. To the best of our knowledge, no bibliometric analysis has been conducted on the top-cited articles related to sublobectomy in NSCLC surgery.

In this study, we aimed to perform a bibliometric analysis of the 100 most-cited articles on sublobectomy for NSCLC. We sought to identify the most influential articles, authors, institutions, and countries in this field, as well as to analyze the trends in research topics and methodologies. This information may help guide future research efforts and inform clinical decision-making in the management of early-stage NSCLC.

Materials and methods

Study design

This study aimed to conduct a bibliometric analysis of the top 100 highly cited articles on sublobectomy for NSCLC. In this study, “sublobectomy” is defined to include both anatomical segmentectomy and wedge resection. The bibliometric analysis was performed to identify the most influential articles, authors, institutions, and countries in this field, as well as to analyze the trends and characteristics of these articles.

Data source and search strategy

A comprehensive literature search was conducted using the Web of Science (WoS) database to identify the top 100 highly cited articles on sublobectomy for NSCLC. The search was performed on March 12, 2023, to ensure the most recent and accurate data. The search terms used were "segmentectomy NSCLC" OR "segmentectomy non-small cell lung cancer" OR "sublobar resection NSCLC" OR "sublobar resection non-small cell lung cancer" OR "limited resection NSCLC" OR "limited resection non-small cell lung cancer" OR "sublobectomy NSCLC" OR "sublobectomy non-small cell lung cancer". The search was limited to articles published in English.

Selection criteria

The search results were sorted by the number of citations, and the top 100 highly cited articles were selected for further analysis. The inclusion criteria were: (1) articles focusing on sublobectomy for NSCLC, (2) articles published in English. The exclusion criteria were: (1) articles not related to sublobectomy for NSCLC, (2) articles focusing on other surgical procedures or treatments for lung cancer, (3) articles published in languages other than English.

Article selection and data extraction

The initial search results were screened by two independent reviewers based on the title and abstract. Any disagreements between the reviewers were resolved through discussion or consultation with a third reviewer. The full texts of the potentially eligible articles were then assessed for eligibility based on the inclusion and exclusion criteria. The top 100 highly cited articles were selected based on the total citation count.

The following data were extracted from the selected articles: (1) title, (2) author(s), (3) year of publication, (4) journal, (5) country of origin, (6) institution, (7) total citation count, (8) keywords, and (9) centrality of keywords.

Data analysis

Descriptive statistics were used to analyze the data. The frequency of articles by year of publication, journal, author, institution, and country were calculated. The total number of citations were also calculated for each article.

Network analysis

A network analysis was performed to visualize the relationships among keywords, authors, institutions, and countries of the top 100 highly cited articles. The network analysis was conducted using CiteSpace software (version 6.1.R1). The nodes in the network represented the keywords, authors, institutions, or countries, and the links between the nodes represented the co-citation or co-authorship relationships. The size of the nodes and the thickness of the links were proportional to the number of citations or co-citation/co-authorship relationships, respectively.

Results

The top 100 most cited articles for sublobectomy studies were published from 1994 to 2022. The number of citations ranged from 51 to 795, including a total of 14,355 citations as of March 12, 2023. 3 literatures are cited more than 500 times, and 19 pieces of literature are cited more than 200 times (Table 1). When divided into five years, the period with the most significant distribution of literature was 2014–2018, with 35 published articles (Fig. 1). Annals of Thoracic Surgery accounted for the highest percentage of articles in the top 100 most cited articles, with 27 articles. According to the latest 2021 Impact Factor (IF) released in 2022, the top 5 journals are Lancet, Lancet Respiratory Medicine, British Medical Journal, Journal of Clinical Oncology, Journal of Thoracic Oncology (Table 2). The 100 most cited articles were categorized as 93 original articles (including 82 retrospective research and 11 prospective research) and 7 reviews.

Table 1 The top 100 most cited articles on sublobectomy
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Fig. 1
figure 1

5-year interval for 100 most cited articles of sublobectomy

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Table 2 Journals and their impact factors included in the 100 most cited articles on sublobectomy
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Among authors of the top 100 most cited works, the top five are Okada Morihito, Landreneau Rodney J, Luketich James D, Fernando Hiran C, Keenan Rj and Landreneau Rj (tied for 5th), with 1410, 1393, 1264, 952, and 829 citations, respectively. Considering both the number of articles included, the top five authors with the most published articles are Landreneau Rodney J, Luketich James D, Fernando Hiran C, Schuchert Matthew J, Okada Morihito and Pennathur Arjun (tied for 5th), with 11, 9,7,7and 6 articles (Table 3). The 100 most cited articles come from 155 organizations, with the top five being University of Pittsburgh, Brigham & Women’s Hospital, National Cancer Center, Mayo Clinic and Niigata Cancer Center (Fig. 2). The 100 most cited articles come from 13 countries. The top five countries of most cited papers are the U.S.A, Japan, China, Australia, and England (Table 4 & Fig. 3).

Table 3 Authors that contributed 4 or more articles in 100 most cited articles on sublobectomy
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Fig. 2
figure 2

Citespace network of co-cited authorship and organization in the field of sublobectomy for NSCLC. Every circle represents one author or organization. Size of circle is positively linked to cited counts of the authors and organizations, links between two circles represents a collaboration between two authors or organizations on the same article. Frequency of collaborations were presented by line thickness

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Table 4 Countries of origin with 3 or more papers included in the 100 most cited articles on sublobectomy
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Fig. 3
figure 3

Time-Zone view of high-frequency countries of top 100 most cited articles. The image displays the evolution of high-frequency countries of top 100 most cited articles over time, from 1994 to 2022. The size of the nodes corresponds to the occurrence frequency of these keywords

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Of the 100 articles in this study, the top 10 keywords are limited resection, lobectomy, survival, carcinoma, recurrence, randomized trial, radiotherapy, lung cancer, outcome, 2 cm. Through CiteSpace analysis, we found that limited resection, lobectomy, carcinoma, randomized trial and survival became high-density keywords (Fig. 4).

Fig. 4
figure 4

Citespace network of co-occurrence networks of keywords in the field of sublobectomy for NSCLC. Every circle represents one keyword. Size of circle is positively linked to cited counts of the keywords, links between two circles represents a collaboration between two keywords on the same article. Frequency of collaborations were presented by line thickness

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Discussion

With the gradual popularization of chest computed tomography (CT) as a means of health checkups, more and more NSCLC are being discovered in the form of small nodules. When facing this situation, both young and elderly patients need to completely remove the tumor while preserving as much lung function as possible. Therefore, sublobectomy has gradually entered the field of vision of thoracic surgeons. Recently, more and more studies have focused on sublobectomy for the treatment of NSCLC. We have constructed this bibliometric analysis specifically for sublobectomy, trying to sort out the current status of existing sublobectomy research by summarizing the most 100 cited articles on sublobectomy and providing a practical reference for future sublobectomy research. While there have been recent bibliometric studies in related fields [13], our research offers a fresh and valuable contribution to the literature. Our study's significance stems from its comprehensive coverage of a vast array of publications and its up-to-date analysis, which reflects the latest trends in the field.

Several studies have demonstrated that sublobectomy can achieve similar oncological outcomes as lobectomy for NSCLC while preserving more lung function [3, 11]. A recent meta-analysis by Zhang et al. [14] showed that segmentectomy had a lower incidence of postoperative complications and better preservation of pulmonary function compared to lobectomy. However, some studies have reported a higher local recurrence rate after sublobectomy [7, 15]. Therefore, the choice between sublobectomy and lobectomy should be based on tumor size, location, and patient's lung function.

The 2 cm size criterion for sublobectomy has been widely accepted in clinical practice. This cutoff is based on the assumption that tumors smaller than 2 cm have a lower risk of lymph node metastasis and can be adequately treated with sublobectomy [16]. However, recent studies have challenged this notion, suggesting that sublobectomy may be appropriate for tumors larger than 2 cm in selected patients [6, 17]. For example, a study by Altorki et al. [18] demonstrated that segmentectomy was non-inferior to lobectomy for tumors up to 3 cm in size; The JCOG1211 study found that ground-glass nodules below 3 cm could also be considered for treatment with sublobectomy [9]. Further research is needed to refine the selection criteria for sublobectomy and to identify the optimal surgical approach for individual patients.

The importance of prospective randomized controlled trials (RCTs) in the field of sublobectomy cannot be overstated. RCTs provide the highest level of evidence for clinical decision-making and can help to establish the optimal surgical approach for early-stage NSCLC [19]. Several RCTs, such as the JCOG0802/WJOG4607L study [8], JCOG1211 study [9] and the CALGB 140503 study [10], have demonstrated that sublobectomy is not inferior to lobectomy for small-sized non-small cell lung cancer. Given the clinical significance of the above study, the findings are likely to rewrite future guidelines for the surgical treatment of NSCLC.

Sublobectomy and radiotherapy are two common treatment options for early-stage NSCLC. Radiotherapy uses high-energy radiation to destroy cancer cells, with stereotactic body radiotherapy (SBRT) being a popular choice for inoperable patients [20]. However, segmentectomy may offer better regional control comparing SBRT [21]. Radiotherapy has the advantage of being a non-invasive treatment, making it more suitable for patients with poor lung function or other comorbidities [22]. The choice between sublobectomy and radiotherapy should be based on individual patient factors, including tumor size, location, and overall health status.

The United States and Japan are the top two countries with the most highly cited publications. Both countries have made significant contributions to the development and popularization of segmentectomy. Japanese researchers have been pioneers in the field, with several landmark studies on sublobectomy published by Japanese institutions [23, 24], and recently Japanese researchers have also released blockbuster research results [8, 9]. In the United States, the National Cancer Institute has sponsored several clinical trials on segmentectomy, such as the ACOSOG Z4032 trial [25] and the aforementioned CALGB 140503 study [10]. The collaboration between researchers from these two countries has greatly advanced our understanding of segmentectomy and its role in the treatment of early-stage NSCLC. It is noteworthy that the largest number of studies on sublobectomy were published between 2014–2018. We believe this is related to the exploration of optimal surgical approaches for early stage NSCLC that began in the early 21st century, as well as the widespread adoption of minimally invasive thoracic surgery techniques.

In the realm of bibliometric analysis, it is imperative to acknowledge the potential limitations and drawbacks that may arise in the course of conducting research. While the quantitative assessment of scientific literature offers valuable insights into the development and dissemination of knowledge, it is not without its shortcomings. One of the primary concerns in this domain is the overemphasis on bibliometric indicators, such as citation counts and impact factors, which may inadvertently lead to a skewed representation of research quality and significance. Furthermore, the inherent biases in citation practices, including self-citation and preferential attachment, can exacerbate the disparities in the visibility and recognition of scholarly works. Additionally, the reliance on quantitative metrics may overlook the nuances and complexities of scientific research, as it fails to capture the qualitative aspects of knowledge production, such as the context, novelty, and interdisciplinary nature of the studies.

Conclusion

The first 100 most cited articles in the field of sublobectomy research were included in the bibliometric analysis, and a series of analyses were conducted. Most of the top 100 most cited articles are original and dominated by retrospective research. Of the included literature, Annals of Thoracic Surgery was the journal with the most publications The most published and cited works are from the United States. In recent years, research on sublobectomy for NSCLC has gradually shifted focus to patient prognosis and comparison of efficacy with other treatment modalities. Researchers have attempted to improve the evidence-based medicine level of sublobectomy through prospective clinical trials, in order to establish its role in the treatment of NSCLC. As the inaugural bibliometric analysis in the field of sublobectomy, our study not only pioneers the way for future research but also surfaces novel focal points that may captivate the attention of subsequent investigators. We anticipate that our findings will stimulate a deeper exploration into these areas, ultimately leading to the discovery of additional clinically meaningful outcomes within the domain of sublobectomy.