A dynamic study of the postoperative management of thyroid cancer from 2003 to 2022: a bibliometric analysis

Introduction

In recent years, the global incidence of thyroid cancer has continued to increase, with age-standardized incidence rates of 3.1 and 10.1 cases per 100,000 people for men and women in 2020, respectively (1). Conversely, the thyroid cancer mortality rates for men and women have remained stable or even declined in most countries (1). The increase in the incidence of thyroid cancer is primarily due to the increased detection of indolent papillary thyroid cancer (PTC) rather than the rare but highly aggressive follicular, medullary, and anaplastic thyroid cancer (2). Thyroid surgery is one of the main treatments for thyroid cancer (3), and while technical approaches, such as the intraoperative neuromonitoring (IONM) of the recurrent laryngeal nerve, intraoperative indocyanine green fluorescence angiography, and autofluorescence of the parathyroid glands, have been introduced, permanent recurrent laryngeal nerve palsies and permanent hypoparathyroidism are still reported in 0.3–3% and in 1–4% of cases, respectively (4-8). The surgical management of thyroid cancer has shifted from a one-size-fits-all approach to an individualized, risk-tailored treatment and management strategy (9). The postoperative management of thyroid cancer, including the prevention and treatment of postoperative complications, the assessment of the postoperative risk of recurrence, adjuvant therapy, thyroid hormone replacement therapy, and the long-term monitoring of recurrence or metastasis, is an important part of any individualized treatment plan and is significant in optimizing the clinical outcome and quality of life of patients (10-12).

Bibliometrics is the study of the quantitative analysis of literature related to a specific topic using mathematical and statistical methods (13,14). A bibliometric analysis involves research content, such as countries, institutions, journals, authors, keywords, and references (15), which can clearly and visually show the research results and trends in a particular field (16,17). At present, few bibliometric analyses have been conducted on the postoperative management of thyroid cancer. Thus, this study conducted a bibliometric analysis of the literature related to the postoperative management of thyroid cancer from 2003 to 2022 to summarize the research hotspots in this field over the past 20 years, explore future development directions, and provide ideas for further exploration and innovation in this field.

Methods

Data collection

A comprehensive search was conducted through the Science Citation Index Expanded (SCI-E) database in the Web of Science Core Collection (WOSCC). The search strategy was as follows: subject: (“postoperative management” AND “thyroid cancer”); period: January 1, 2003 to December 31, 2022; language: English; and document type: Article. All the literature data that met the criteria were downloaded and exported as a text file, including data on the title, author, abstract, institution, country, journal, keywords, and references. CiteSpace 6.1.R6 was used to remove duplicate documents. Articles that did not meet the criteria or that had been published as “proceedings papers”, “editorial material”, “letters”, or “meeting abstracts” were excluded.

Data analysis

The bibliometric tool CiteSpace 6.1.R6 was selected for the bibliometric analysis and data visualization analysis, which included a country and institutional collaboration network analysis, journal co-citation and literature co-citation analysis, co-occurrence networks for keywords analysis, and keyword burst analysis. “Betweenness centrality” measures the number of times a node lies on the shortest path between other nodes. Nodes with high betweenness centrality are generally considered potential pivotal points (18). “Keyword bursts” indicate a specific period of abrupt change in keyword frequency, and burst detection algorithms for keywords are used to identify emerging research frontiers (18,19). Microsoft Office Excel 2010 was used to reflect the annual number of publications and their overall growth trends in citation counts. R studio was used to generate spatial geographic distribution maps and collaborative linkage networks.

Results

Ultimately, 1,040 publications were obtained for the visual analysis. Figure 1 shows the inclusion flow chart for the study.

Figure 1 Study inclusion flow chart. WOS, Web of Science.

Trends in the number of annual publications and citations

Over the past 20 years, despite some slight decreases in specific years, the number of publications related to the postoperative management of thyroid cancer has shown an overall upward trend, as has the number of citations in the literature (Figure 2). The year 2022 had the highest number of publications (n=129), while the year 2004 had the lowest number of publications (n=13). The volume of literature in 2022 was approximately 10 times higher than that in 2004. The year 2021 had the highest number of citations (n=3,341).

Figure 2 Numbers of publications and citations from 2003 to 2022.

National and institutional cooperation networks

In the last 20 years, a total of 64 countries and 1,400 institutions have published literature related to the postoperative management of thyroid cancer. As the collaboration network map shows, a high concentration of research on the postoperative management of thyroid cancer was conducted in North America, Asia and Europe, with frequent collaborations between North America and Europe (Figure 3). In terms of the number of publications, the United States of America (USA) had the highest number of publications (n=282), followed by China (n=245), and South Korea (n=117). The top 10 countries in terms of number of publications were mainly concentrated in North America and Asia; the two countries with the best centrality were the USA and England, of which the USA had the highest centrality (centrality =0.28) (Figure 4). Conversely, the top 10 countries in terms of centrality were mainly concentrated in North America and Europe (Table 1).

Figure 3 Cooperation network map.

Figure 4 National cooperation network.

As Figure 5 and Table 2 show, the institution with the highest number of publications was Memorial Sloan Kettering Cancer Center (n=52), which is located in the USA. The two institutions with the best centrality were Johns Hopkins University and Yonsei University, of which, Johns Hopkins University, which is located in the USA, had the best centrality (centrality =0.15). The network of national and institutional collaborations showed that the USA was the academic core of the field.

Figure 5 Institutional cooperation network.

Cited journals

In the last 20 years, a total of 307 journals have published literature related to the postoperative management of thyroid cancer. Among them (Table 3), the most cited journal was Thyroid (n=826), which has a Journal Citation Reports (JCR) division of Q1 (Journals with top 25% impact factor). Thyroid is the official journal of the American Thyroid Association and is affiliated with the European Thyroid Association and the Latin American Thyroid Society. The next most cited journals were the Journal of Clinical Endocrinology and Metabolism (n=646), and Surgery (n=610). The top 10 cited journals were related to the three areas of endocrinology and metabolism (n=4), surgery (n=4), and otolaryngology (n=2). The journal with the highest centrality (centrality =0.08) was the American Journal of Surgical Pathology, which has a JCR division of Q1 and which focuses on pathology and surgical research directions.

We further plotted the dual-map overlay of journals to show the relationship between the journals (Figure 6). The colored curves between the citation map on the left and the citation map on the right provide an understanding of the interdisciplinary relationships in the given field. Notably, publications in the medicine, medical and clinical (green track) fields were influenced by publications in the health, nursing and medicine fields (z=7.0675, f=88,426), and the molecular, biology and genetics fields (z=2.0904, f=28,291).

Figure 6 Dual-map overlay of journals.

Publications with co-citations

In the last 20 years, the top 10 cited articles in this field (Table 4) were mainly guidelines and consensus statements on thyroid cancer management (n=7), and the epidemiology of thyroid cancer (n=1), and studies related to the postoperative prognosis of thyroid cancer (n=2). The number one article on guidelines for the management of thyroid nodules and differentiated thyroid cancer in adults was written by Haugen et al. (20), and published in the Thyroid journal in 2016. The article made recommendations on the long-term management of differentiated thyroid cancer after surgery, including thyroid stimulating hormone (TSH) suppressive therapy, the monitoring of differentiated thyroid carcinoma (DTC) recurrence using ultrasound (US) and other imaging techniques [e.g., US, radioiodine-131 (RAI) single-photon emission computed tomography-computed tomography (SPECT/CT), X-ray computed tomography (CT), magnetic resonance imaging (MRI), positron emission tomography-CT (PET-CT)], serum thyroglobulin (Tg), and the comprehensive treatment and management of recurrent or metastatic DTC.

By analyzing the timeline of co-cited publications (Figure 7), an understanding was gained of the distribution of the research themes in the cited literature and their evolution over time. Before 2010, the main research topics in this field were “levothyroxine suppressive therapy”, “chyle leakage”, “thyroid carcinoma”, “sonography”, and “central neck dissection”. However, over time, in the 5 years from 2010 to 2015, the research topics in this field focused on “thyroglobulin”, and “demographic”. In recent years, the research topics have focused on “hypothyroidism”, “central compartment lymph node dissection”, and “active surveillance”.

Figure 7 Publications with co-citation timeline.

The co-occurrence and clustering of keywords

To reduce bias in the automated bibliometric analysis in Citespace, we manually merged the keywords “cancer” and “carcinoma”. Subsequently, a total of 551 keywords and 27 keyword clusters were found (Figures 8,9). The top 10 keywords were “cancer” (n=627), “management” (n=574), “surgery” (n=156), “thyroid cancer” (n=144), “nodule” (n=118), “recurrence” (n=108), “prognostic factor” (n=101), “therapy” (n=101), “follow-up” (n=88), and “papillary” (n=86). The top three keyword clusters were follow-up (#0), recurrent laryngeal nerve (#1), and medullary thyroid carcinoma (MTC) (#2).

Figure 8 Keyword co-occurrence map.

Figure 9 Keyword clustering map.

Burst detection of keywords

Through keyword burst detection, we identified the top 20 burst words about the postoperative management of thyroid cancer in the last 20 years (Figure 10). In terms of burst intensity, the top three keywords were “papillary” (strength =8.02), “management guideline” (strength =7.31), and “postoperative thyroglobulin level” (strength =6.66). In chronological order, the main early burst words were “prognostic factor”, “papillary”, “follow-up”, and “positron emission tomography”. Subsequently, the terms “preoperative ultrasonography”, “needle aspiration biopsy”, and “surgical management” emerged as keywords for preoperative assessment tools and surgical treatment. Next, words related to thyroid cancer metastasis, such as “metastasis”, “postoperative thyroglobulin level”, “lymph node dissection” and “lymph node”, emerged. In recent years, the words “management guideline”, “association guideline” and “active surveillance” have emerged, and terms related to the pathological classification of thyroid cancer, such as “microcarcinoma” and “differentiated thyroid cancer”, once again became burst words.

Figure 10 Top 20 keywords with the strongest citation bursts.

Discussion

General information

The number of publications related to the postoperative management of thyroid cancer and its citations generally showed an increasing trend over the past 20 years, indicating a gradual increase in academic focus in this area, and the possibility that more research will be conducted in the future. Johns Hopkins University showed the highest centrality (centrality =0.15) and was the academic center of the field. Collaboration between North American and European countries in this research area was frequent, while Asian countries had a high number of publications but lacked collaborations with other countries. None of the four Asian countries (i.e., China, South Korea, Japan, and Turkey) that were in the top 10 in terms of the number of publications showed close cooperation or obvious centrality with other countries. This result may be related to the differences in economic power and the medical levels of different countries. There were direct or indirect collaborations between different institutions, but these institutions tended to engage in more collaborations within their own countries. Institutions in the USA published the highest number of publications, which was consistent with the national collaboration networks. In the top 10 institutions in terms of frequency, five institutions were located in Asia, with Korean institutions accounting for 80%. Yonsei University in South Korea showed better centrality (centrality =0.14) than other institutions in Asia. This may be related to the high incidence of thyroid cancer in South Korea. A global epidemiological survey on thyroid cancer in 2020 found that the incidence rate of thyroid cancer in females in South Korea was 45 cases per 100,000 people, and that South Korea had the highest incidence-to-mortality ratio for both sexes (2). To ensure better outreach in postoperative thyroid cancer management research, we suggest that countries and institutions with close collaborative relationships continue to maintain close academic exchanges while establishing academic ties with less collaborative countries and institutions to jointly conduct high-quality multicenter-related studies and promote the globalization of postoperative thyroid cancer management research.

For the past 20 years, Thyroid has been the most cited journal for literature related to the postoperative management of thyroid cancer, and the American Journal of Surgical Pathology has been the highest centrality in publishing research related to the postoperative management of thyroid cancer. These journals cover the areas of endocrinology and metabolism, pathology, and surgery. These results suggest that cellular-level features of thyroid cancer and strategies for the perioperative management of thyroid cancer remain major areas of interest, and that future advances and breakthroughs are likely to come from these areas of research. The “2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer” were published in the Thyroid journal by Haugen et al. in 2016 (20), and this literature was the most cited article in the field for almost 20 years, but these guidelines are now outdated. We look forward to the guidelines being updated, and we note that there is a need for international guidelines on the postoperative management of patients with thyroid cancer if more optimal management is to be achieved.

The hotspots and frontiers

Our keyword co-occurrence and clustering analysis, and literature co-citation timeline graphs revealed that the research hotspots for the postoperative management of thyroid cancer in the past 20 years could be summarized into the following four topics: pathological classification, surgical strategy, postoperative complications, and postoperative follow-up. These four topics include preoperative and intraoperative issues, and thus show that preoperative and intraoperative management influence postoperative treatment.

The keyword-based clustering analysis revealed the prominence of clusters such as follow-up, recurrent laryngeal nerve, and MTC. The postoperative follow-up of thyroid cancer should be surveillance-oriented, and the proactive monitoring of thyroid cancer recurrence and metastasis is the focus of postoperative management (12). First, stratification according to the stage of thyroid cancer and risk of recurrence facilitates the selection of the most appropriate postoperative management strategy. The risk of recurrence is associated with the number and size of metastatic cumulative lymph nodes, and the presence of extranodal spread, the pathological classification of the thyroid cancer, the location and size of the tumor, and the presence of peritumoral or vascular infiltration (30). Second, current studies have shown that serum Tg levels have a high sensitivity and specificity in detecting the recurrence and metastasis of thyroid cancer (31,32). However, the optimal threshold to predict disease recurrence based on postoperative serum Tg levels has yet to be determined. A 2020 cohort study showed that an early postoperative Tg level <2 ng/mL could be used as a threshold to guide adjuvant therapy and determine the frequency of long-term monitoring (33). Other studies have shown that even with a Tg level <1 ng/mL, ¹³¹I radioiodine whole-body imaging (¹³¹I-WBS) still detects the functional remnants of thyroid tissue, suggesting the possibility of tumor recurrence, and that Tg may not be able to identify tumor metastases of smaller sizes (34,35). Serum Tg level monitoring combined with imaging techniques (e.g., US, RAI SPECT/CT, CT, MRI, and PET-CT) is an effective tool for determining the recurrence and metastasis of thyroid cancer after surgery, and it can be used to help to dynamically assess the risk of recurrence and death (36).

The recognition and management of postoperative thyroid cancer complications are an integral part of postoperative thyroid cancer management. Return laryngeal nerve (RLN) injury is a common complication after thyroidectomy (37,38). It has been reported that the incidence of permanent postoperative RLN injury is 0.3–3%, and the incidence of temporary RLN injury is 3–8.9% (4,5,39). Risk factors for postoperative RLN injury include reoperation, the type of surgery, malignancy, and tumor size, and some studies have shown a higher risk of vocal cord dyskinesia in patients who undergo central neck dissection or have larger tumors (4,5). Other studies have reported that there is no increased risk if central neck dissection is performed by high-volume surgeons (40). IONM could be used to prevent RLN injury. IONM uses vocal cord electromyography to monitor the electrophysiologic activity of the RLN, which can help identify anatomical changes in the RLN during thyroidectomy (41,42). However, several studies have shown (43-45) that IONM fails to significantly reduce the incidence of intraoperative RLN injury compared to conventional RLN visualization.

MTC is a rare and aggressive neuroendocrine carcinoma that accounts for approximately 1–2% of all thyroid cancers, and 15% of thyroid cancer-related deaths, and has a poor prognosis (26,46). Early surgery with complete tumor resection has the potential to cure MTC, and the postoperative monitoring of serum calcitonin and carcinoembryonic antigen levels is essential (47). Nevertheless, the management of advanced, progressive MTC remains challenging and is currently dominated by targeted therapies with tyrosine kinase inhibitors (TKIs) (48,49); however, further research still needs to be conducted on TKI resistance and the adverse effects of TKIs to improve patient prognosis (50,51).

The keyword burst detection analysis showed that “papillary” had the highest burst intensity. In recent years, “active surveillance” has become a burst word, and the re-emergence of burst words such as “microcarcinoma” and “differentiated thyroid cancer” indicates that the classification of thyroid cancer has again become an important area of research. PTC is the most common type of DTC, and the increase in the incidence of thyroid cancer over the past two decades primarily involved early-stage PTC (52,53). As a result of extensive screening using highly sensitive imaging equipment, an increasing number of clinically asymptomatic papillary thyroid microcarcinomas (PTMCs) are being detected, which have a low degree of malignancy and require less aggressive treatment (54,55). There is growing concern about the overdiagnosis and overtreatment of thyroid cancer, which is reflected in changes in surgical strategies and postoperative management, the controversy as to the extent of surgery, and the implementation of stricter restrictions for postoperative RAI therapy (9,11,56). Patients diagnosed with low-risk PTMC in recent years have had the following two management options: (I) surgical treatment; and (II) active surveillance (AS). Almost no other cancer has a similar management approach as that used for thyroid cancer. Currently, some consensus has been reached in relation to AS, with studies (57,58) suggesting that immediate surgery and AS have comparable oncologic outcomes, and that AS is superior to surgical treatment in terms of quality of life because of the potential of postoperative complications. However, the evidence in favor of AS is not sufficiently strong at this stage. First, there is a lack of reliable molecular markers to predict the aggressive behavior of PTMC. The 600^th amino acid in V-Raf Murine Sarcoma Viral Oncogene Homolog B (BRAF) is mutated from valine to glutamic acid (this mutation is abbreviated as V600E). BRAF V600E and telomerase reverse transcriptase (TERT) promoter mutations are considered risk factors for PTC progression (59,60). However, some studies (61,62) have shown that BRAF and TERT promoter mutations are not associated with the adverse clinical features of PTMC. Second, there are geographical differences between economic incomes. Middle-income and low-income countries may not have the necessary conditions to implement AS, which requires multidisciplinary teams of surgeons and endocrinologists, high-resolution imaging equipment, and the organized and systematic follow-up of patients (63). Third, in relation to patient anxiety, AS appears to be superior to surgical treatment in terms of quality of life, but patients who choose AS are more likely to be anxious about the progression of the disease (60,64). In the future, more research needs to be conducted to compare AS and surgical treatments over the long term. Finally, the pathologic classification of thyroid cancer remains at the academic forefront of this field. Future research hotspots will probably derive from the study of the histopathologic features of thyroid cancer, especially microcarcinoma in differentiated thyroid cancer, and its prognosis.

Limitations

This study had some limitations. First, we only searched the SCI-E database in the WOSCC. Second, all information was extracted using scientometric tools, and thus the results may be biased. Finally, the uneven quality of the data collected from the literature in the study may have reduced the credibility of the map analysis.

Conclusions

Over the past 20 years, the number of publications in this field has generally continued to increase. Among the many research directions, follow-up, recurrent laryngeal nerve, and MTC are research hotspots in the postoperative management of thyroid cancer. Future research is likely to revolve around guidelines and consensus statements on the management of thyroid cancer, AS, and microcarcinoma in differentiated thyroid cancer.

Acknowledgments

The authors would like to thank Xiyuan Hospital, China Academy of Chinese Medical Sciences for supporting this work.

Funding: The work was supported by funding from the CACMS Innovation Fund (No. CI2021A01608).

Footnote

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-23-218/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-23-218/coif). The 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.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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