Bibliometric analysis and visualization of global research trends in primary thyroid lymphoma via CiteSpace

Introduction

Thyroid lymphoma (TL), a rare malignancy, has garnered increased attention over recent decades. It represents 1–5% of thyroid tumors (1) and less than 3% of extranodal lymphomas (2), with an estimated incidence of one in a million (3). Primary thyroid lymphoma (PTL) accounts for the majority of TL cases, in contrast to the less common extranodal lymphomas affecting the thyroid (4). Previously, the diagnostic evaluation of PTL was constrained, frequently resulting in errors due to limited material sampling or the absence of notable histologic heterogeneity (5). Recently, the development of complementary techniques such as immunohistochemistry (IHC), immunocytochemistry (ICC), flow cytometry (FC), molecular testing, cytogenetic analysis, and positron emission tomography (PET) has significantly enhanced the sensitivity of PTL diagnosis (6-9). Concurrently, these advancements have refined the classification of PTL. The two predominant subtypes are diffuse large B-cell lymphoma (DLBCL) and mucosa-associated lymphoid tissue (MALT) lymphoma, with DLBCL comprising approximately 70% of PTL cases (10). DLBCL is the most aggressive subtype, with over half of patients presenting with a rapidly enlarging neck mass, often accompanied by symptoms such as dysphagia, wheezing, hoarseness, and neck pressure (11). Conversely, fever, night sweats, and weight loss are less frequently observed (12,13). In contrast, the biological behavior of MALT is relatively indolent, resulting in prolonged periods of asymptomaticity for most patients (14).

Historically, owing to constraints in diagnostic techniques and therapeutic approaches, the prognosis of PTL was considerably poorer compared to other thyroid malignancies, often being closely linked with specific histological subtypes. For instance, the 5-year survival rate of DLBCL has been reported to be of as low as 35% (3). The optimal treatment approach for PTL remains controversial due to its specific origin, biological behavior, rarity, and the absence of large prospective randomized controlled trials. Nevertheless, the guiding principle is to tailor therapy based on histological subtype and staging. Radiotherapy, chemotherapy, or a combination thereof have been suggested as the optimal treatment modalities for DLBCL (15), while surgical intervention is primarily recommended for cases of MALT lymphoma or in instances of urgent airway obstruction relief (16,17). In certain investigations, adjuvant surgical interventions alongside targeted therapy involving radiotherapy and chemotherapy have been proposed to enhance patient prognosis (2). The global accumulation of research expertise in the treatment of PTL, facilitated by the extensive utilization of radiotherapy, chemotherapy, and targeted therapy, may unveil emerging trends and focal points in PTL research. The evolution of these studies over time and the identification of key roles and guiding significance are essential inquiries that warrant exploration. Insights gleaned from such investigations could prove instrumental in refining the clinical diagnosis and treatment strategies for PTL.

While traditional literature reviews provide a narrative or descriptive recount of past research, they often lack the analytical depth and comprehensive visualization provided by bibliometric analysis. Bibliometrics utilizes publication data to describe relationships within literature, identify trends, and highlight research hotspots across various fields (18-20). This method, therefore, allows for a quantitative analysis of the literature, offering a more objective and expansive understanding of research trends over time (21,22). Prof. Chen C. developed CiteSpace, a bibliometric tool used in this study for the first time on PTL research. Using CiteSpace (19), we aim to systematically analyze and visualize the co-citation networks, thereby uncovering the evolving trends and focal points in PTL research that traditional reviews might overlook. Insights from this analysis could be instrumental in refining clinical diagnosis and treatment strategies for PTL, emphasizing the guiding significance of quantitative bibliometric methods in medical research.

Methods

Methods and search strategy

On January 1, 2024, we conducted a literature search on PTL spanning from 2000 to 2023 using the Web of Science Core Collection (WoSCC). All medical subject headings terms were acquired by querying the MeSH database, followed by the elimination of duplicate keywords and their linkage. Included publications encompassed articles or reviews within the specified search period of 2000 to 2023, with English being the restricted language. The search formula was constructed as follows: (((TS=(primary thyroid lymphoma)) AND PY=(2000-2023)) AND DT=(Article OR Review)) AND LA=(English). We downloaded and saved the literature in the “Full Record and Cited References” format, eliminating duplicates, resulting in an initial pool of 736 articles. Subsequently, we imported these 736 articles obtained from WoSCC into EndNote for further screening, as depicted in Figure 1 illustrating the literature processing flow.

Figure 1 Literature screening process. WoSCC, Web of Science Core Collection.

Inclusion and exclusion criteria

Inclusion criteria: (I) articles must be pertinent to PTL or involve patients with PTL, irrespective of gender or age; (II) articles should report on at least one of the following endpoints: epidemiology, diagnostic methods, etiology, pathology, treatments, among others.

Exclusion criteria: (I) studies involving patients whose TL was not PTL but resulted from metastases of other lymphomas; (II) articles that merely mention PTL without describing or analyzing the specified outcomes; (III) duplicate studies, conference abstracts, reviews, or letters; (IV) studies for which the full text is not available; (V) literature not published in English.

Bibliometric analysis

Upon applying the inclusion and exclusion criteria, 281 publications were identified and imported into CiteSpace 6.2.R4 for in-depth bibliometric analysis. CiteSpace was utilized to transform and time-slice the data from January 2000 to December 2023, employing a one-year slice to systematically visualize the progression and trends within the research landscape. We set parameters to focus on the Top50 cited articles or those scoring high on the G-index for each slice, which allowed for an analysis of the most impactful studies. The analytical process in CiteSpace involved thresholding, modeling, pruning, merging, and mapping of the data to create initial visualization charts. These charts were composed of nodes and linear connections, with each node symbolizing an article or study, and the node’s size reflecting its frequency of occurrence or citation impact. Adjustments were made to node positions and connections to enhance the clarity and intuitiveness of the visualization, ensuring significant themes and influential works were easily identifiable.

Our bibliometric indicators included citation counts, co-citation analysis, and keyword occurrence frequency. We specifically analyzed co-citation networks to identify key themes, evolving trends, and central authors or articles within the PTL research community. This method provided not only a quantitative assessment of the literature but also qualitative insights into the relationships and thematic shifts over the observed period.

Statistical analysis

This study utilized bibliometric and network analysis techniques to investigate the research landscape of PTL. Specifically, the software CiteSpace (6.2.R4) was used to conduct the following analyses:

• Co-citation analysis: this method helped identify the most frequently cited articles, authors, and journals within the PTL research community, revealing key themes and influential works.
• Network analysis: this involved the mapping of relationships between authors, institutions, and countries to identify collaborative networks and influential research centers.
• Trend analysis: publication trends over time were analyzed using curvilinear regression to assess the growth trajectory of research in this field.
• Keyword analysis: frequency of keyword occurrence was calculated to determine emerging hotspots and shifts in research focus.

Each of these methods contributes to the statistical exploration of bibliographic data, helping to quantify relationships and trends within the scholarly literature on PTL. No traditional statistical tests (e.g., t-tests, chi-square) were applied as the data pertains to publication metrics and thematic saturation rather than experimental outcomes.

Results

Growth trend in publications

We represented the annual publication volume as a scatterplot, onto which a polynomial was fitted to discern trends. As illustrated in Figure 2, the number of articles on PTL exhibited a fluctuating upward trend from 2000 to 2023. Notably, the years 2007, 2009, and 2019 recorded significant annual growth rates in publications, at 50.00%, 64.29%, and 50.00%, respectively. The year with the fewest publications was 2000, recording only 5 articles (1.78%), while 2023 saw the highest number of publications, with 25 articles (8.90%). Through curve fitting analysis, we observed that the recent number of articles on PTL remained low and the growth trend was gradual. This indicates that PTL is a rare malignant tumor, and it is unlikely that the number of future studies will exhibit explosive exponential growth.

Figure 2 Trends in the publication of articles on PTL over the last 20 years. PTL, primary thyroid lymphoma.

Country and region analysis

Since the beginning of the 21st century, all articles on PTL have come from 48 countries/regions, of which China has published the most articles in the field of PTL with 58 (20.64%), followed by the US with 56 (19.93%), and Japan, Italy, and Turkey ranked 3rd–5th in order of the number of articles published (Table 1). Moreover, it is noteworthy that among the top 10 countries in terms of publication volume, China began its contributions to the field of PTL relatively recently, with the first article published in 2007. Despite this, China ranks first in total number of publications. As depicted in Figure 3A, the articles are primarily concentrated in Europe, East Asia, North America, and Australia. Interestingly, most countries/regions lack research establishments in the field of PTL. We employed the Top 50 algorithm to analyze the impact of national/regional contributions, thereby providing a clearer view of the international academic collaboration landscape based on the rankings. Notably, despite China having the highest number of papers, its centrality remains relatively low at 0.08. In contrast, the centrality for the United States, Italy, and Turkey are 0.28, 0.18, and 0.13, respectively, all surpassing that of China. This discrepancy suggests that despite China’s prolific output in this field, the citation frequency and the perceived significance of its research could benefit from enhancement.

Figure 3 Overview of global research on PTL. (A) The distribution of articles across various countries/regions. (B) Network diagram showing countries’ links. PTL, primary thyroid lymphoma.

Through the network of country collaborative relationships (depicted in Figure 3B), it is evident that the outermost nodes representing the United States, Italy, and Turkey are adorned with a purple ring. This typically signifies that research outcomes from these countries wield considerable influence in this field. The connecting lines between the nodes represent cooperative relationships between the countries/regions, with wider lines indicating stronger cooperative ties. Additionally, the color of the time markers in Figure 3B transitions from blue to yellow, symbolizing a progression from earlier to more recent times. It is apparent that collaborations between the United States, Italy, and several European countries predominantly occurred earlier, whereas the cooperative relationships between China, Japan, South Korea, and Turkey have mostly developed in recent years. Despite the broad spectrum of international partnerships, the level of cooperation among individual countries remains relatively limited.

Institutional analysis

We utilized the top 50 algorithm to analyze the organizations with the highest impact and the partnerships between them. To enhance clarity in displaying the links between these organizations, we employed pathfinder for pruning. The results obtained are detailed below: in Table 1, the top 3 institutions based on the number of articles published were the Chinese Academy of Medical Sciences (CAMS, n=10, 3.56%), Kuma Hospital (n=9, 3.20%), and the University of Texas System and Mayo Clinic (both n=7, 2.49%). Although CAMS had the highest number of articles, its centrality was only 0.03, which is lower than the second-ranked institution at 0.11 and the third-ranked at 0.07. As illustrated in Figure 4A, four institutional nodes are highlighted with purple outer circles, indicating their significant role in the field of PTL. These institutions are the University of Eastern Piedmont Amedeo Avogadro (n=3, centrality =0.14), Acibadem University (n=3, centrality =0.14), Kuma Hospital (n=9, centrality =0.11), and Hospital Clinic de Barcelona (n=3, centrality =0.10). These four institutions evidently exert a top-down influence on the positioning of the nodes. Furthermore, as depicted in Figure 4A, the lines of cooperation among institutions exhibit a notably greater level of complexity compared to those among countries, forming a structured network of collaboration. Typically, inter-institutional collaboration is confined within individual countries. For example, CAMS closely collaborated with universities within China, such as Zhejiang Cancer Hospital, Capital Medical University, and Fudan University. In contrast, the bottom left of Figure 4A distinctly illustrates a collaborative network of institutions within Japan.

Figure 4 Institutional collaboration and influence in PTL research. (A) Network diagram showing institutional links. (B) CiteSpace visualization map of top 10 institutions with the strongest citation bursts involved in PTL. PTL, primary thyroid lymphoma.

As shown in Figure 4B, CAMS leads with the highest citation intensity at 2.28, closely followed by Huazhong University of Science & Technology at 2.20. However, it is noteworthy that both institutions experience shorter citation outbreaks, lasting only 2 years. The institution with the longest citation burst is the University of Texas System, which has lasted for 9 years. Institutions with citation bursts extending until 2023 include Kuma Hospital and Aha Khan University, indicating that their research may set the trend for recent developments in PTL research.

Author and co-cited author analysis

We employed the G-index algorithm to identify authors who hold significance in the academic field of PTL, aiming to gain insights into academic partnerships. A total of 640 researchers have made substantial contributions to the field of PTL over the past 23 years. Notably, Hirokawa Mitsuyoshi emerges as the author with the highest number of publications, having authored 4 articles. Among these, his 2017 publication, “Preoperative diagnostic algorithm of primary thyroid lymphoma using ultrasound, aspiration cytology, and flow cytometry”, stands out as the most cited, with 21 citations. However, after calculating and correcting for centrality, all authors had a centrality of 0, indicating that they published fewer articles or did not generate enough impact to achieve centrality. Figure 5A illustrates the authors’ collaborative network, revealing that they tend to collaborate within their own ‘academic circles’.

Figure 5 Authorship patterns and key influencers in PTL research. (A) A network diagram displaying authors’ links. (B) A network diagram displaying co-cited authors’ links. PTL, primary thyroid lymphoma.

A co-citation relationship occurs between two authors when their articles are cited by the same article simultaneously, resulting in co-cited authors. When analyzing co-cited authors, we employed the Minimum Spanning Tree algorithm for pruning to create a more concise and analytically accessible visualization. Figure 5B presents the collaborative network of co-cited authors. Among the co-cited authors, the top three most cited are Derringer Ga (n=108), Thieblemont C (n=94), and Graff-Baker A (n=76). Notably, Graff-Baker A, among the top ten most cited authors, has the highest centrality (centrality =0.62). By calculating the mediated centrality of the co-cited authors, we identified the top 10 co-cited authors with high centrality (Table 2). The top three authors with the highest centrality are Tsang RW, Laing RW, and Yamaguchi M. As depicted in Figure 5B, there appears to be limited collaboration between these authors and other research teams, resulting in lower connectivity within academic networks, despite the widespread citation of their work. Alternatively, it is plausible that their research was conducted some time ago, and they may not have continued to contribute significantly to the field of PTL, leading to a decrease in their centrality.

Keyword analysis

To identify keywords with a central position in the keyword network and to examine the relationships between them, we used the G-index and Minimum Spanning Tree algorithms for analysis and pruning. Figure 6A was generated by filtering the top 30 keyword class clusters with the highest citation frequency, with the size of each node corresponding to the frequency of the keywords. Table 3 showcases the top 20 most frequently occurring keywords related to PTL. The top 10 most frequently used keywords, in descending order, were “gland”, “malignant lymphoma”, “non-Hodgkin’s lymphoma”, “primary thyroid lymphoma”, “diffuse large B-cell lymphoma”, “diagnosis”, “Hashimoto’s thyroiditis”, “prognostic factors”, “cancer”, and “thyroid lymphoma”. Among them, the frequency of “diffuse large B-cell lymphoma” was only 67 times, yet its centrality was notably high at 0.85, followed by “non-Hodgkin’s lymphoma”, with a centrality of 0.80. As shown in Figure 6A, there were additional keywords with relatively small nodes, yet their purple outer circle was more prominent, indicating higher centrality. Examples include “biopsy”, “positron emission tomography”, and “elderly patients”.

Figure 6 Keywords and emerging trends in PTL research. (A) CiteSpace visualization map of keywords clustering analysis related to PTL. (B) CiteSpace visualization map of top 20 keywords with the strongest citation bursts involved in PTL. PTL, primary thyroid lymphoma.

In addition, we constructed a keyword clustering network using the LLR algorithm and identified the largest clustering label as “0# marginal zone lymphoma”, followed by “1# chemotherapy” and “2# thyroid lymphoma” (Table 4). The highest silhouette score was associated with “7# stx11”, and the most recent keyword clustering label was “9# diffuse thyroid uptake”.

Keyword burst analysis can be utilized to observe research hotspots within a specific time period and analyze future research trends from a temporal perspective (23). Among the top 20 keywords depicted in Figure 6B, the keyword with the highest burst intensity is “primary thyroid lymphoma” (6.65), while the keyword with the longest burst duration is “features” (8 years). In terms of the starting and ending points of the burst, “tissue”, “mucosa-associated lymphoid tissue”, and “classification” emerged as hot topics at the beginning of the study. Conversely, keywords such as “features”, “primary thyroid lymphoma”, “tissue lymphoma”, “case report”, “long term”, “outcome”, and “non-Hodgkin lymphoma” have experienced recent explosive growth and have yet to reach their end. These keywords may signify the focal points of current and future research in the field of PTL.

Co-citation analysis of articles

Per the definition of co-cited authors, co-citation occurs when an article references two other articles concurrently. The greater the number of co-cited articles, the stronger the citation relationship, and the greater the significance attributed to the cited articles (24). In assessing co-cited literature, we employed both the top 50 and Pathfinder algorithms. These methodologies enable us to anticipate the ranking and citation frequency of research literature, thereby facilitating the exploration of topical interests within the field. This approach aids in identifying timely articles poised to have a significant impact on future research endeavors. By tallying the citations of co-cited articles, we identified the top 10 articles (Table 5).

The most cited among these was a review authored by Pavlidis, published in Journal of Investigative Surgery in 2019, accumulating 27 citations (25). This seminal work delineated state-of-the-art diagnostic, staging, and therapeutic strategies pertaining to PTL, alongside prognostic considerations for patients with varying pathology types. The second most cited article was authored by Graff-Baker, appearing in Current Opinion in Oncology in 2010, garnering 17 citations (16). This comprehensive review offered an exhaustive overview encompassing the diagnosis, histological subtypes, pathogenesis, and treatment modalities relevant to PTL. Of notable significance, the authors highlighted the transformative impact of rituximab on chemotherapy strategies for DLBCL, reshaping therapeutic approaches for PTL patients. Furthermore, they emphasized that surgical intervention and radiotherapy are typically reserved for patients presenting with stage I and II PTL. The third-ranking article was a review authored by Stein et al., featured in The Journal of Clinical Endocrinology & Metabolism in 2013, accruing 16 citations (26). The authors underscored the absence of sizable clinical trials evaluating the efficacy of varied treatment modalities for PTL, thereby emphasizing the importance of sourcing insights from retrospective studies and additional literature concerning the management of extranodal lymphoma. Their analysis culminated in the affirmation that radiotherapy and chemotherapy retain their pivotal roles in PTL treatment. Surgical intervention, on the other hand, was predominantly reserved for addressing specific issues such as compression symptoms and airway damage. The centrality scores of all articles were computed to be 0, suggesting that they may not have been co-cited extensively enough or did not function as bridges connecting disparate research domains or topics. Additionally, the number of citations garnered by the top 10 co-cited articles is not notably high, likely attributable to the relative rarity of PTL and the paucity of research literature in this domain. Among the top 10 co-cited articles, five were review articles and five were original research articles, predominantly comprising retrospective analyses, with only one clinical trial study. This distribution underscores the prevailing trend within the field, wherein retrospective analyses constitute the predominant research type, reflective of the challenges associated with conducting large-scale clinical trials in the context of a rare disease like PTL.

The burst of co-cited literature can unveil shifts in research focus among researchers within the same field across various time periods, offering valuable insights into potential future research trajectories (27). Figure 7 visually presents the top 20 references characterized by the highest co-citation intensity within the realm of PTL. The publication demonstrating the most substantial co-citation impact is the review by Pavlidis, which exhibits a co-citation strength of 10.39 and spans an outbreak duration of four years (25). Following closely, the review by Graff-Baker holds the second highest co-citation strength, recorded at 8.04 (16). Securing the third position is the article authored by Ansell in 1999. This seminal article in the field of PTL emerged earlier with significant impact (28). The review comprehensively addressed the management of MALT and DLBCL. It concluded that surgical resection should not be routinely employed as a treatment strategy for PTL. Treatment options for MALT may encompass radiotherapy, oral chlorambucil, or a chemotherapy regimen including cyclophosphamide, vincristine, and prednisone (CHOP). Examining the timeline, there are five articles with a total of cited outbreaks to date: a 2019 review by Pavlidis (25); a 2017 retrospective analysis by Hirokawa on the utilization of ultrasound and FC in diagnosing PTL (29); a 2019 database analysis by Noble et al., exploring PTL patient characteristics, treatment modalities, and overall survival (13); a 2019 meta-analysis by Zhang et al., assessing the sensitivity and specificity of fine-needle aspiration (FNA) for PTL diagnosis (30); and a 2018 retrospective study by Watanabe on the long-term follow-up of MALT patients post-treatment (31).

Figure 7 CiteSpace visualization map of top 20 references with the strongest citation bursts involved in PTL. PTL, primary thyroid lymphoma.

Discussion

In this study, we conducted a comprehensive search of the WoSCC database for literature pertaining to PTL spanning the years 2000 to 2023. After excluding publications that did not meet our criteria, we compiled a dataset of 281 articles. This dataset was then analyzed using CiteSpace software to visualize the study landscape and delineate research trends. Over the 23-year period, we assessed articles from various perspectives, derived empirical findings, and formulated reasoned speculations and extrapolations based on these results.

Since the onset of the 21st century, the volume of publications on PTL has demonstrated a consistent upward trend, signaling that this relatively rare disease is increasingly attracting scholarly attention. Among the nations contributing to this body of literature, China and the United States lead significantly in the number of publications, ranking first and second, respectively. Notably, the United States also exhibits the highest degree of article centrality. An analysis of citation frequencies by institutions indicates that although Chinese institutions entered the PTL research arena later, their contributions have rapidly expanded in recent years. Institutional citation burst analysis further revealed that institutions from the United States, China, and Japan are poised to remain influential in this field. Additionally, an examination of authors and co-cited authors highlights that Hirokawa Mitsuyoshi has authored the most papers, suggesting extensive research activity in this domain. The collaborative networks among authors exhibit distinct patterns, suggesting independent clusters of collaboration. Among co-cited authors, Derringer et al.’s 2000 article in The American Journal of Surgical Pathology stands out as the most cited, surpassing 200 citations (32). This seminal work concluded that PTL can manifest from MALT in the context of lymphocytic thyroiditis. Additionally, Graff-Baker emerged with the highest centrality among the top 10 co-cited authors, recorded at 0.62. Their article offers a comprehensive overview of PTL, encompassing diagnosis, histological subtypes, pathogenesis, and treatment modalities (16).

Analysis of keyword frequencies reveals ‘gland’ as the most commonly used keyword, while ‘diffuse large B-cell lymphoma’ holds the highest centrality. DLBCL represents the most prevalent and aggressive subtype of PTL. Recent advancements in IHC have facilitated the specific classification of DLBCL into germinal center B-cell (GCB) and non-GCB types, with prognostic implications (33). ‘Hashimoto’s thyroiditis’ ranks seventh among the top 10 most used keywords and is highlighted as ‘10# Hashimoto’s thyroiditis’ in keyword clustering. Both instances emphasize its importance as a recognized risk factor for PTL (34), pointing to a focus on mitigating its impact on morbidity. Keyword clustering analysis revealed the most prominent cluster labeled ‘0# marginal zone lymphoma’ (MZL), a chronic B-cell lymphoma originating from marginal zone lymphoid tissues. While MZL differs from PTL in clinical manifestations and pathological features, their treatment options may overlap in clinical practice. For instance, the R-CHOP regimen (rituximab, cyclophosphamide, adriamycin, vincristine, and prednisone), initially used in other lymphomas, has been extensively clinically validated and is now a first-line treatment for PTL approved by the United States Food and Drug Administration (FDA) (35). The second most prominent keyword cluster was labeled ‘1# chemotherapy’. Chemotherapy has been integral to PTL treatment since the 1980s, substantially limiting the role of traditional surgical interventions and markedly enhancing patient prognosis (36). Presently, the R-CHOP regimen stands as a cornerstone chemotherapy approach for PTL (2,37,38). Notably, R-CHOP administration significantly extends patient survival while concurrently reducing rates of treatment failure and tumor recurrence. Beyond rituximab, recent studies have identified other drugs effective against various lymphomas. For instance, in 2020, Hu et al. demonstrated that geniposide can dose-dependently induce apoptosis in DLBCL cells (39). Similarly, in 2021, Liu et al. confirmed through cytological experiments that AZD5991 promotes apoptosis in ibrutinib-resistant DLBCL cells (40). However, the efficacy of these drugs in treating PTL has yet to be confirmed.

Notably, the keyword clustering analysis revealed ‘7# STX11’ as having the highest silhouette. STX11 (Syntaxin 11) is a gene encoding a protein crucial for regulating intracellular membrane fusion, particularly in immune cells. It is commonly implicated in the molecular pathology and treatment of lymphomas. The clustering label ‘9# diffuse thyroid uptake’ corresponds with the latest study’s average year and is closely linked with the high centrality keyword ‘positron emission tomography’ (PET). PET imaging utilizes radiolabeled drugs to detect areas of abnormal metabolic activity in the body. TLs typically exhibit high metabolic activity, leading to abnormal thyroid function or diffuse radionuclide uptake. PET scans can aid in diagnosing the location, extent, and activity level of PTL (41). Through analysis of keyword bursts, we observed emerging trends in recent years, notably hot keywords such as ‘features’, ‘case report’, ‘long term’, and ‘outcome’. These keywords, cited in ongoing bursts, likely pertain to the pathological features and clinical manifestations of PTL. It is anticipated that future research will provide further insights into long-term outcomes and case reports of PTL patients. In 2021, Xiang et al. identified significant prognostic factors for overall survival in PTL patients, including age, marital status, histological subtype, Ann Arbor stage, surgery, chemotherapy, and radiotherapy, through multifactorial cox regression analysis (2).

By analyzing the onset of article co-citation outbreaks, we observed significant shifts in the focus of PTL research. The initial bursts between 2001 and 2003 revealed that researchers were chiefly concerned with the diagnosis, staging, and prognosis of PTL. This period also marked the introduction of radiotherapy and CHOP chemotherapy strategies for treating DLBCL. This phase represents the initial exploration into PTL treatment and establishes the groundwork for subsequent research directions (28,32,42). During the 2006–2010 period, the co-citation bursts of articles contributed potential recommendations on the optimal diagnostic approaches and treatment strategies for PTL, as well as GCB typing and prognostic analyses. During this period, researchers continued to delve deeper into treatments and validated established research concepts (5,43-46). The 2011–2017 co-citation burst of articles concentrated on various aspects including the clinicopathological features of PTL, treatment strategies for different subtypes, survival rates, the association between PTL and Hashimoto’s thyroiditis, and diagnostic techniques such as FC and IHC (16,26,35,47-49). Significantly, in 2006, the FDA approved rituximab as a first-line treatment for non-Hodgkin’s lymphoma (35). A 2010 review by Graff-Baker highlighted that the introduction of rituximab for treating DLBCL transformed the chemotherapy protocol for PTL patients, leading to the adoption of the R-CHOP treatment regimen (16). The 2019–2023 co-citation burst of articles emphasizes complementary diagnostic strategies, risk factors, and multimodal treatments—including immunological and targeted therapies—for PTL. This area represents a vibrant component of current research and is likely to remain a central focus in future investigations (12,13,25,29-31).

In the realm of gene expression and immunotherapy, a pivotal 2016 review by Swerdlow et al., published in Blood, revised the classification and diagnostic criteria for lymphoma (33). This study emphasized the necessity of differentiating DLBCL into GCB or non-GCB types to refine therapeutic strategies. Notably, the co-expression of the MYC and BCL2 genes was identified as prognostically significant and may guide the development of future targeted therapies. In 2020, Leroy L published a case report in Thyroid suggesting that genetic and molecular testing hold promise for novel treatments across various tumor types (50). This perspective aligns with Swerdlow et al.’s emphasis on gene expression, positing it as a pivotal guide for the development of future targeted therapies specifically for PTL. Through examination of articles in the field of PTL, it becomes apparent that the low prevalence of PTL hampers the feasibility of conducting large prospective clinical trials to assess the efficacy of different treatment strategies and novel drugs. Consequently, the optimal treatment approach for PTL remains a subject of debate, compounded by limited research into new pharmaceutical interventions, which may potentially draw from treatments established for other forms of lymphoma. In summary, research on PTL has progressed from initial focuses on diagnostic modalities, pathological typing, staging, and early chemotherapy strategies to more comprehensive aspects. Current research explores the clinicopathological features of PTL, varied treatment approaches for different subtypes, survival rates, risk factors, complementary diagnostic techniques, and the application of immunotherapy.

Despite challenges, researchers and clinicians generally agree on the potential for improved survival and prognosis through multimodal radiotherapy-chemotherapy combinations for aggressive DLBCL (51,52). The efficacy of such combinations was initially demonstrated by Matsuzuka et al. in 1993 (53). Subsequently, Miller et al. indicated that treating localized non-Hodgkin’s lymphoma with 3 cycles of CHOP chemotherapy plus 40–55 Gy radiotherapy yielded superior outcomes compared to CHOP chemotherapy alone (54). Onal et al. demonstrated that combination therapy yields superior overall survival compared to chemotherapy or radiotherapy alone (55). Successive studies by researchers including Doria, Mian, and Watanabe have further underscored the advantages of combination therapy strategies (47,56,57). Subsequently, the monoclonal antibody rituximab was integrated into PTL treatment, heralding the advent of the R-CHOP strategy, a targeted therapy that stands as one of the most significant recent advancements in the field (48). Rituximab’s potential synergistic effect with chemotherapy, inducing apoptosis, underscores its therapeutic value (36). Despite the absence of large prospective clinical trials demonstrating R-CHOP’s efficacy in PTL, numerous case reports and meta-analyses affirm its favorable outcomes (35,36,51,58,59). However, some studies have indicated that DLBCL patients with overexpression of BCL2 and BCL6 do not respond optimally to R-CHOP, likely due to drug resistance (60,61). It is reported that approximately 50% of DLBCL patients are BCL2 positive and 75% are BCL6 positive (44). Additionally, between 50–70% of DLBCL patients show a favorable response to R-CHOP (38). Consequently, further clinical trials are necessary to verify rituximab’s efficacy in treating PTL, although its enhanced effectiveness in certain patients cannot be denied. Beyond that, the prospects for new drugs depend on the progress of new drugs for other lymphomas. Drugs such as tafasitamab, lenalidomide, bexarotene and alemtuzumab have shown new promise in the treatment of refractory DLBCLs, follicular lymphomas and cutaneous T-cell lymphomas (62-65). It can be seen that most of the new drug research in the field of lymphoma treatment is focused on immune-targeted drugs, which is in line with the results of our hotspot and trend analysis.

In contrast, single-modality therapies are often more suitable for the MALT subtype and other less aggressive subtypes, including options like surgery or radiotherapy. However, the role of surgery in treating PTL remains contentious. While it is a primary treatment in early stages, surgery frequently falls short of achieving optimal outcomes due to challenges in performing total resection (59). Notably, as early as 1992, Pyke et al. determined from a retrospective study that surgery did not benefit patients with stage IE and IIE PTL (66), a conclusion that has since garnered widespread support among scholars (10,17,67). Skeptics of surgical treatment contend that it should be reserved mainly for patients with stage IE MALT and those who have not responded to non-surgical therapies (48,68). Indeed, surgery has transitioned from being the primary treatment for PTL (69). Nonetheless, certain researchers advocate for the incorporation of surgery into a comprehensive treatment approach. For instance, a 2019 study by Xiang et al. reported that over 50% of PTL patients had undergone surgery, identifying it as an independent prognostic factor for overall survival (2). They recommended integrating surgery as an adjunct to radiotherapy and chemotherapy to form a comprehensive treatment strategy. Similarly, Vardell et al.’s 2019 analysis using the National Cancer Database concluded that surgery enhances survival (13). Therefore, more evidence-based medical research is necessary to definitively ascertain the benefits of surgery in the treatment of PTL.

Strengths and limitations

To the best of our knowledge, this paper represents the first bibliometric analysis in the field of PTL treatment. We meticulously downloaded and analyzed a comprehensive collection of articles from the WoSCC database that fulfilled the criteria pertinent to this field, enabling us to objectively delineate research trends and hotspots. Nonetheless, we acknowledge that this study is not without its limitations. For instance, our analysis was confined to articles and reviews published in English since the 21st century, excluding publications in other languages and different types of documents. This approach may have resulted in the omission of relevant articles (70). Furthermore, some recently published articles might not have been identified as part of current research hotspots due to their lower citation rates.

Conclusions

This article employs bibliometric research methods to visualize and analyze the research trends and hotspots of PTL, offering researchers novel perspectives from various angles. Despite PTL being a rare disease with a low prevalence rate, the past two decades have witnessed a proliferation of studies that have significantly advanced the clinical diagnosis and treatment of PTL. Based on intuitive analyses, we anticipate that future research trends in the field of PTL may encompass adjunctive diagnostic techniques, long-term survival outcomes, case reports, targeted therapies, and risk factors. In conclusion, we trust that this article will offer novel perspectives and insights to researchers, fostering further advancements in the field.

Acknowledgments

The authors extend their sincere appreciation to the institutions listed in the funding section for their generous support of this research.

Funding: This work was financially supported by Science & Technology Department of Sichuan Province (No. 2021YFS0103, to A.S.), Health Commission of Sichuan Province (No. 20PJ057, to A.S.), China Health Promotion Foundation (No. HX22-228/HX-H2204083, to A.S.).

Footnote

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-317/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-24-317/coif). A.S. reports that this work was financially supported by Science & Technology Department of Sichuan Province (No. 2021YFS0103), Health Commission of Sichuan Province (No. 20PJ057), China Health Promotion Foundation (No. HX22-228/HX-H2204083). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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