The 100 most cited papers on thymoma: a bibliometric analysis

Abstract

Objectives

The aim of this bibliometric analysis was twofold: to identify the 100 most cited research articles on thymoma and to highlight future research opportunities in light of past and current research efforts.

Methods

The Web of Science database was queried to identify the 100 most cited articles on thymoma. Imformations relevant to scientific research were extracted and analyzed: first author, journal, impact factor, type of article, year of publication, country, organization and keywords.

Results

The publication year of the top 100 most cited articles ranged from 1981 to 2018, and the number of citations ranged from 97 to 1182. Most of the included articles are original (75/100) and are mainly retrospective studies (52/75). The United States has the most published articles and citations, and the Annals of Thoracic Surgery is the most sourced journal (n = 16). Through VOSviewer analysis, high-density keywords mainly come from thymic carcinoma/invasive thymoma management, immune-related diseases, and laboratory research.

Conclusions

To our knowledge, this is the first bibliometric study on thymoma. We found most of the top 100 most cited articles are original and retrospective research. The United States has the published and cited works. Presently, the hot keywords for thymoma research has gradually tilted towards immune-related diseases and laboratory research.

Introduction

Thymoma is the most common mediastinum tumor, but it is still rare. In previous studies, thymoma was classified as a type of thymic epithelial tumor and was analyzed in conjunction with thymic carcinoma. With the continuous deepening of follow-up research, people have gradually found that thymoma and thymic carcinoma are two different neoplasms, and there are great differences in biological behavior, clinical manifestations, and treatment methods. As a result, many medical centers have conducted much research on thymoma. After the publication of the first literature on thymoma [1], the literature in this area became increasingly affluent.

Scientific analysis of influential literature in a field can help us better understand the hot spots and recent advances in that field. Bibliometrics is a statistical approach to assessing the impact of published literature on any field [2, 3]. Recently, there has been more and more research on bibliometrics in medicine, of which citation analysis is the most commonly used method [4,5,6]. Citation analysis can reflect the impact of literature in the field and tap the most influential literature to help us better understand the research hot spots and latest advances in the field.

There has been bibliometric analysis on thymic epithelial tumors [7]. However, to our knowledge, there is currently no bibliometric analysis specifically for thymoma. Therefore, considering the specificity of thymoma in thymic epithelial tumors, we conducted this study. This study aimed to identify and analyze the characteristics of the 100 most cited articles related to thymoma.

Materials and methods

Identifying the top 100 most cited articles

We identified articles through the Web of Science (WOS) database, considered one of the most popular and well-established resources for clinical researchers interested in citation analysis [8], in June 2022. Keywords included "thymoma," "thymoma surgery," "thymoma chemotherapy," "thymoma radiotherapy," "thymoma treatment," "thymoma management," "thymoma malignancies," "thymic epithelial tumors," with no limitation on time, abstract availability, study type, or research subjects. Articles were ranked based on the total citations received from the databases. Previous studies frequently combined thymoma and thymic carcinoma into thymic epithelial tumors. Therefore, we included studies that covered both thymic carcinoma and thymoma in the screening process and studies that specifically targeted thymoma.

Article analysis

Three reviewers screened and extracted the statistical data from the included literature in this study. For the 100 most cited articles, the author, country, institution, year of publication, publication journal of each article, the latest 2021 journal impact factor (IF) released in 2022, keywords, and type of literature are summarized.

VOSviewer (Leiden University, Leiden, Netherlands) was used to construct networks: co-authorship analysis of countries/organizations/authors, co-citation analysis of journals, citation analysis of articles, and co-occurrence analysis of keywords. Further, the first 100 keywords of the frequency were presented in two visualizations (overlay and density visualization) of the co-occurrence analysis to identify key terms in thymoma research, including studies conducted entirely on thymoma, and studies that were predominantly thymoma or had specific analyses for thymoma, although covering other thymic epithelial tumours.

Results

The top 100 most cited articles for thymoma studies were published from 1981 to 2018. The number of citations ranged from 97 to 1182, including a total of 17,049 citations as of June 2, 2022 (Table 1). One literature is cited more than 1000 times, and 22 pieces of literature are cited more than 200 times. When divided into five years, the period with the most significant distribution of literature was 2001–2005, with 29 published articles (Fig. 1). Annals of Thoracic Surgery accounted for the highest percentage of articles in the top 100 most cited articles, with 16 articles. According to the latest 2021 IF released in 2022, the top 5 journals are Journal of Clinical Oncology, Journal of Thoracic Oncology, Clinical Cancer Research, Neurology and Annals of Neurology (Table 2). The 100 most cited articles were categorized as 75 original articles, 19 reviews, 4 guideline/consensus/statement, 1 case report, and 1 communication/note (Table 3).

Table 1 The top 100 most cited articles on thymoma

Fig. 1

5-year interval for 100 most cited articles of thymoma

Table 2 Journals and their impact factors publishing more than 2 articles in the 100 most cited articles on thymoma

Table 3 Article type and study design composing the 100 most cited articles on thymoma

Among authors of the top 100 most cited works, the top five are Monden Y, Masaoka A, Nakahara K, Tanioka T, and Loehrer Pj, with 2309, 1832, 1715, 1182, and 828 citations, respectively. Considering both the number of articles and the number of citations, the top five authors with the most published articles are Monden Y, Nakahara K, Loehrer Pj, Masaoka A, and Marx A, with 6, 5, 5, 4, and 4 articles (Table 4). The 100 most cited articles come from 17 countries. The top five countries are the U.S.A, Japan, Italy, England, France, and Germany (Table 5). The 100 most cited articles come from 198 organizations, with the top five being Osaka University, Tokushima University, National Cancer Institute, Memorial Sloan Kettering Cancer Center and Indiana University.

Table 4 Authors that contributed 3 or more articles in 100 most cited articles on thymoma

Table 5 Continents and countries of origin in the 100 most cited articles on thymoma

Of the 100 articles in this study, the top 10 keywords are invasive thymoma, thymic carcinoma, prognosis, classification, radiotherapy, surgery, therapy, thymic epithelial tumors, myasthenia gravis, clinicopathological features, and prognostic factors. Through VOSviewer analysis, we found that thymic carcinoma, invasive thymoma, surgery, radiotherapy, and myasthenia gravis became high-density keywords (Fig. 2). Furthermore, the keywords related to basic research (growth-factor receptor, immunohistochemistry, and KIT) and immune disease (systemic-lupus-erythematosus, lichen-planus, t-cells, and red-cell aplasia) have increased in recent years.

Fig. 2

Co-occurrence analysis of keywords. A Distribution of keywords according to average publication year (blue: earlier, yellow: later). B Distribution of keywords according to the mean frequency of appearance. Keywords in yellow occurred with the highest frequency

Discussion

Thymoma is a vital part of thymic epithelial tumors, and with continuous study, it has gradually been found to have different characteristics from other thymic epithelial tumors. Therefore, to explore the most concerned and cutting-edge hotspots in the field of thymoma research, we have constructed this bibliometric analysis specifically for thymoma, trying to sort out the current status of existing thymoma research by summarizing the most 100 cited articles on thymoma and providing a practical reference for future thymoma research. Although previous bibliometric study on thymic epithelial tumors have been published [7], our study differs from its list of top 100 highly cited articles, authors and country of publication, given the large differences between thymoma and thymic carcinoma. In addition,our study also further analyzes the keywords of included papers, hoping to help the development of future studies related to thymoma.

Original articles accounted for 3/4 (75/100) of the literature included in this study. However, it is important to note that most of these (52/75) were retrospective studies, which we believe is associated with a lower incidence of thymoma. The lower incidence makes conducting prospective studies on thymoma challenging, but 12 works are still prospective studies. The most cited article in this study was the publication by Masaoka et al., which followed 96 patients with thymoma for up to 10 years and explored the effects of staging and different treatment modalities [9]. Of the top 100 most cited works, the top 10 were original retrospective studies. Prospective studies are mainly aimed at chemoradiotherapy for thymoma. However, they were all single-arm studies, and there are studies of postoperative radiotherapy for thymoma patients who had a complete resection [10]. The study is still ongoing, and the results are worth expecting.

The United States has the highest number of published and cited in the top 100 most cited articles, reaching 41 and 6786, respectively. However, the top three most cited articles are from Japan. All of these articles were retrospective studies with large sample sizes, and all patients were followed up for a long time (up to 44 years) [9, 11, 12]. Therefore, their research results are significant for diagnosing and treating thymoma. We believe this is related to differences in the pooled incidence of thymoma in different races. For example, based on the Surveillance, Epidemiology, and End Results (SEER) database, the incidence of thymic tumors in North America is 2.14 per 1 million, and the incidence of thymic tumors in Asians (3.74 per 1 million) is higher than that of the Caucasian ethnic group (1.89 per 1 million), so thymoma in Asian populations are relatively more common. Hence, relatively large sample size studies on thymoma are also easier to conduct. We believe that slow patterns of recurrent metastasis, developments in pathological molecular techniques, and the emergence of innovative therapeutic concepts and measures have led to higher quality researches in the field of thymoma in the first decade of the twenty-first century than in other periods.

Through VOSviewer analysis, thymic carcinoma and invasive thymoma are the two keywords with higher density. Since both are attributed to thymic epithelial tumors, thymoma and thymic carcinoma are often studied together in the existing literature. For example, the International Agency for Research on Cancer (IARC) published the WHO classification of thymic epithelial tumors in March 2015, based on a multidisciplinary symposium organized by the International Thymic Malignancy Interest Group (ITMIG) in December 2011 [13]. Thymoma is an inert tumor that occurs, develops, metastasizes, and recurs more slowly. However, some thymomas have the characteristic of aggressive growth. Therefore, the treatment and prognosis of invasive thymoma have become a hot topic in thymoma research. Recent studies of invasive thymoma have focused on more minimally invasive surgical modalities [14] and treatment for neoplasm with intravascular growth [15,16,17].

Surgery is currently the first choice for thymoma treatment, and its position in treating thymoma and even thymic epithelial tumors has been recognized [9, 11, 18]. However, in recent years, research on the treatment of thymoma has gradually focused on radiotherapy and chemotherapy, with more prospective studies and randomized controlled trials [10, 19,20,21]. Currently, immunotherapy studies on thymoma have also been published, and higher PD-L1 expression was linked with a better response to treatment with immune checkpoint inhibitors but with a relatively high incidence of immune-related adverse events. Therefore, immunotherapy is not yet the standard adjuvant therapy for thymoma, and large sample size studies are required to confirm its safety.

Many studies have found that thymoma is associated with autoimmune diseases, especially myasthenia gravis. Therefore, myasthenia gravis has become one of the hot keywords in this study. In addition, immune disease-related words such as systemic-lupus-erythematosus, lichen-planus, t-cells, and red-cell aplasia also appeared in the top 100 keywords, and according to VOSviewer cluster analysis, the frequency of such words has gradually increased in recent years. Our team has also found that surgery has a certain effect on treating non-myasthenia Gravis autoimmune diseases [22]. Similarly, laboratory research on thymoma has gradually increased in recent years, and since 2000, the number of highly cited laboratory studies on thymoma has gradually increased. In total, 11 laboratory studies were included in this study, and KIT, interleukin-1alpha, PD-1/PD-L1, and titin antibodies were the hot spots. It can be seen that the research on thymoma is no longer limited to the characteristics of clinical pathology and the prognosis of treatment. The horizontal study of the association of thymoma with other diseases and the longitudinal study of the molecular gene mechanism of thymoma is receiving increasing attention.

There are several limitations to our study. First, although we used an authoritative database to identify articles, articles have different numbers of citations in different databases due to coverage differences. Therefore, there is a certain bias in the selection of literature. Second, citation analysis may not be a perfect measure of an article's impact on its field. Since the number of citations usually increases with time, the earlier articles potentially have an artificially higher impact than the more recent articles. In any case, citation analysis is still the best measurement for studies, and it can reflect the value of old articles in this field to some extent. Third, we cannot exclude self-citation from journals and authors.

Conclusion

The first 100 most cited articles in the field of thymoma 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. Although the most published and cited works are from the United States, the top 3 most cited articles are from Japan. Presently, the high-density keywords of thymoma research mainly come from thymic carcinoma/invasive thymoma, treatment regimen (surgery and chemoradiotherapy), immune-related diseases, and laboratory research. However, in recent years, the hot spot for thymoma research has gradually tilted towards immune-related diseases and laboratory research. This is the first bibliometric analysis of thymoma, and we hope that the findings of this study will provide guidance and inspiration for future thymoma research.