Publications on ultrasound-guided thermal ablation for thyroid nodules from 2000 to 2022: a bibliometric analysis

Abstract

Background

Thyroid nodules are increasingly treated with minimally invasive surgery. Thermal ablation could efficiently treat patients with benign thyroid nodules, recurrent thyroid cancer, and low-risk papillary thyroid carcinoma. This research aims to explore the research field of thermal ablation for thyroid nodules using bibliometric analysis.

Methods

The web of science core collection (WoSCC) database was utilized from its inception to 1 October 2022, to collect research articles and reviews on ultrasound-guided thermal ablation for thyroid nodules. We applied the R package ‘bibliometrix’ to summarize the main findings, calculate the occurrences of the top keywords and visualize the international collaboration networks. The co-authorship and co-occurrence analyses were conducted with VOSviewer software. CiteSpace was used to identify the top references and keywords with the highest citation bursts.

Results

A total of 820 publications from 32 countries were retrieved. The annual number of related publications showed an increasing trend. China, Italy, and Korea were the most contributing countries. The University of Ulsan College of Medicine in Korea was the most productive institution, and Jung Hwan Baek published the maximum number of articles. The International Journal of Hyperthermia was the most productive journal. ‘Papillary thyroid micro-carcinoma (PTMC)’ and ‘association guideline’ were the most frequently used keywords in the field of thermal ablation for thyroid nodules, which indicated the potential hot research topics and frontiers in the future.

Conclusion

This bibliometric study conducts a comprehensive analysis of publications on thermal ablation for thyroid nodules, which aids investigators in discovering potential research directions.

Keywords:

• Thyroid nodules
• thermal ablation
• bibliometric
• publications

Introduction

The detection of thyroid nodules has significantly increased in recent years with the application of ultrasound examinations [1]. Nearly 85% of thyroid nodules are benign, and few are malignant [2]. Most benign thyroid nodules are asymptomatic or nonfunctioning and do not require treatment [3]. However, due to the unique location of the thyroid gland, large thyroid nodules or multiple lesions might induce compression of the esophagus and trachea, resulting in difficulty swallowing and breathing. Thyroidectomy is widely regarded as the first-line treatment for benign and malignant thyroid nodules [4]. Nevertheless, some significant morbidities, such as a scar on the neck and a high risk of hypothyroidism, might result in poor quality of life [5, 6].

To reduce surgery-related morbidity, ultrasound-guided thermal ablation for patients with benign nodules, low-risk malignant tumors, and recurrent cancer has been proposed [7–9]. Thermal ablation acts by inducing tissue necrosis through the heat, with the advantages of minimally invasiveness and few complications, comprising radiofrequency ablation (RFA), microwave ablation (MWA), laser ablation (LA), and high-focused intensity ultrasound (HIFU) [10]. In the past decades, multiple systematic reviews and meta-analyses have thoroughly analyzed the safety and efficacy of thermal ablation for thyroid disease, including benign nodules, papillary thyroid micro-carcinoma (PTMC), and recurrent thyroid cancer [11–14]. In spite of the rapid growth of published literature, accurate information, such as the number of relevant publications, countries, and journals, is lacking.

Bibliometrics is a comprehensive method using quantitative and qualitative analyses to uncover various features of publications [15, 16]. In addition to identifying highly frequently-cited publications and keywords, it also displays collaborations among countries, institutions, and authors [17, 18]. Moreover, it can provide researchers with a quick and accurate overview of a specific research field’s evolution and frontiers. Previous bibliometric analyses investigated the trends and hot topics in the field of thyroid, such as ‘thyroid nodules’ [19], ‘PTMC’ [20], and ‘anaplastic thyroid carcinoma’ [21]. In the field of thermal ablation for thyroid nodules, bibliometric analysis has not been conducted. This study aims to systematically examine the intellectual structure of research on thermal ablation for thyroid nodules using bibliometric analysis.

Methods and materials

Relevant literature was retrieved from the Web of Science Core Collection (WOSCC) database on 1 October 2022. Medical Subject Headings (MeSHs) in the National Library of Medicine were used for topic entry. The searching query was: TS = ((thyroid nodule) OR (Nodule, Thyroid) OR (Nodules, Thyroid) OR (Thyroid Nodules) OR (Thyroid Neoplasms) OR (Neoplasm, Thyroid) OR (Thyroid Neoplasm) OR (Neoplasms, Thyroid) OR (Thyroid Carcinoma) OR (Carcinoma, Thyroid) OR (Carcinomas, Thyroid) OR (Thyroid Carcinomas) OR (Cancer of Thyroid) OR (Thyroid Cancers) OR (Thyroid Cancer) OR (Cancer, Thyroid) OR (Cancers, Thyroid) OR (Cancer of the Thyroid) OR (Thyroid Adenoma) OR (Adenoma, Thyroid) OR (Adenomas, Thyroid) OR (Thyroid Adenomas)) AND TS = ((Radiofrequency Ablation) OR (Ablation, Radiofrequency) OR (Radio Frequency Ablation) OR (Ablation, Radio Frequency) OR (Radio-Frequency Ablation) OR (Ablation, Radio-Frequency) OR (Laser Ablation) OR (Ablation, Laser) OR (Microwave ablation) OR (High-Intensity Focused Ultrasound Ablation) OR (High-Intensity Focused Ultrasound Ablation) OR (thermal ablation))

The study period covered the years between 2000 and 2022. ‘All’ was selected for languages and document types. A total of 837 literature records were downloaded and exported into CiteSpace for further analysis. The file format was set as ‘Plain Text’, and the content was set as ‘Full Record with Cited References’ to obtain all the necessary details. A bibliometric analysis of 820 papers was performed after removing duplicates and selecting document types (articles and reviews). Statistical analysis and visualization of the raw data were carried out with VOSViewer 1.6.16 and CiteSpace 5.7. We visualized the number of publications in each category and the pattern of collaboration among different countries or districts. The development skeleton was outlined using reference co-citation analysis. A research landscape was created using clustered terms extracted from titles and abstracts. Future research frontiers and hotspots could be predicted using detected burst keywords.

Visual mappings of knowledge domains, such as cluster networks, were applied to present the results. Each cluster can be labeled with an extracted term from scientific literature. In some cases, the cluster network can be pruned to reduce the number of redundant links and retain the most salient links [22]. All study data were available in a public database. Therefore, approval from an institutional review board or ethics committee was not applicable and informed consent was waived.

Results

Publication characteristics

820 publications regarding thermal ablation for thyroid nodules were included, comprising 646 articles and 174 reviews. The number and trend of annual publications in this research field are presented in Figure 1. During the past 21 years, the number of articles has dramatically increased, from two in 2000 to 140 in 2021. Furthermore, the relationship between the number of articles published and the publication year was assessed using a generalized additive model. The model fitted perfectly with the annual trend of the publications (R² = 0.9809).

Figure 1. The number of publications about thermal ablation for thyroid nodules per year and the accumulative number between 2000 and 2022.

Most productive countries, institutions, and journals

The number of articles per country is shown in Figure 2. China had the greatest number of publications (n = 286), followed by Italy (n = 122), Korea (n = 121), and the USA (n = 107). The remaining countries published fewer than 100 articles. In terms of citations of each country, Korea showed the highest citations of the average article (44.11), followed by Italy (34.81), the USA (35.36), China (12.07), and France (36.52). Supplementary Figure 1 illustrates the international collaboration between countries. Korea, China, the USA, Italy, and Switzerland conducted most research collaborations. In terms of frequency of cooperation, Italy and the USA topped the list (frequency = 19), followed by Italy and Switzerland (frequency = 16), Italy and France (frequency = 13), and China and Korea (frequency = 12).

Figure 2. An overview of the contributions of each country based on the number of published articles.

It was estimated that 954 institutions contributed to research about thermal ablation for thyroid nodules. A list of the ten most productive institutions is displayed in Figure 3. China had the five most productive institutions. Italy, Korea, the USA, and Denmark had 2, 1, 1, 1 institution, respectively. Different institutions’ relationships can be estimated through a co-authorship analysis. In the overlay network, publication numbers are represented by the circles’ size, and the circles’ color indicates publication starting years. As shown in Supplementary Figure 2, researchers at Regina Apostolorum Hospital in Italy and Daerim St. Mary’s Hospital in Korea started early in the research field of thermal ablation for thyroid nodules. Comparatively, those at Chinese People’s Liberation Army General Hospital, Shanghai Jiaotong University, Sun Yat-sen University in China, and Johns Hopkins University in the USA conducted more recent research in this field.

Figure 3. The top 10 institutions with the most published articles in the research field of thermal ablation for thyroid nodules.

A total of 256 journals published research articles about thermal ablation for thyroid nodules: a list of the top 10 journals with the highest number of publications is shown in Table 1. The majority of those journals were classified into Q1 (70%), and the remaining journals were Q2 (30%). Regarding publisher location, five of the top 10 journals were in the USA, two in Korea, two in Switzerland, and one in England. The most represented journals were ‘International Journal of Hyperthermia’ ‘Thyroid’ and ‘Frontiers in Endocrinology’ with a total number of publications of 106, 40, and 38, respectively.

Table 1. The top 10 journals with most publications in the field of thermal ablation for thyroid nodules.

Rank	Journals	Publications	Country	IF	JCR category
1	International Journal of Hyperthermia	106	England	3.753	Q2
2	Thyroid	40	USA	6.506	Q1
3	Frontiers in Endocrinology	38	Switzerland	6.055	Q1
4	European Radiology	27	Switzerland	7.034	Q1
5	Korean Journal of Radiology	22	South Korea	7.109	Q1
6	Endocrine	21	USA	3.925	Q1
7	Journal of Clinical Endocrinology & Metabolism	17	USA	6.134	Q1
8	Journal of Vascular and Interventional Radiology	14	USA	3.682	Q2
9	Ultrasonography	14	South Korea	4.725	Q2
10	Radiology	12	USA	29.146	Q1

IF: impact factor; JCR category: Journal Citation Reports Category.

Most influential authors and most-cited references

In Table 2, 2602 authors contributed to publications related to thermal ablation for thyroid nodules. The most productive author was Baek, who published 102 articles in this research field (h-index = 39), followed by Lee (58 articles with h-index = 32), Luo Yukun (38 articles with h-index = 11), and Choi (37 articles with h-index = 19) and Papini (29 articles with h-index = 22).

Table 2. The top 10 authors with the most publications in the field of thermal ablation for thyroid nodules.

Rank	Authors	Publications	H-index
1	Baek JH	102	39
2	Lee JH	58	32
3	Luo Y	38	11
4	Choi YJ	37	19
5	Papini E	29	22
6	Yan L	26	7
7	Zhang Y	26	12
8	Ha EJ	24	15
9	Lang BHH	24	11
10	Pacella CM	24	21

A cluster diagram of collaborative relationships among researchers is shown in Supplementary Figure 3(a). Color denotes clusters, and circle size indicates number of publications. It appeared that cooperation between research teams was not well established in the field of thermal ablation for thyroid nodules, since the links between communities were sparse. The time-overlapping clustering network is shown in Supplementary Figure 3(b). Li Yan and Lin Weicheng, representing Chinese researchers, were establishing new research networks.

The most highly cited articles can be assessed through citation analysis. The frequency of citations could reflect the influence of articles in a particular research field. The ten most cited articles are listed in Supplementary Table 1. These articles were published between 2000 and 2016, and 80% received over 200 citations. The top two were review articles published in Endocrine Practice and Radiology. Specifically, the article entitled ‘AMERICAN ASSOCIATION OF CLINICAL ENDOCRINOLOGISTS, AMERICAN COLLEGE OF ENDOCRINOLOGY, AND ASSOCIAZIONE MEDICI ENDOCRINOLOGI MEDICAL GUIDELINES FOR CLINICAL PRACTICE FOR THE DIAGNOSIS AND MANAGEMENT OF THYROID NODULES—2016 UPDATE APPENDI’ has received 677 citations, making it the top-cited article in this research field. This guideline provided specific indications and recommendations for the clinical application of thermal ablation in treating thyroid nodules [23].

Supplementary Figure 4 presents the top 20 references with the highest citation burst. The observed interval between 2005 and 2022 is represented as a blue line. The red line indicates the burst duration, with a minimum duration of three years. One article entitled ‘Radiofrequency ablation of benign thyroid nodules: safety and imaging follow-up in 236 patients’, published in 2008, showed the most significant citation burst value (39.94) from 2008 to 2016. It was worth noting that several articles were consistently receiving citation bursts, such as ‘Ultrasound-guided radio-frequency ablation versus surgery for low risk: results of over 5 years follow-up’ from Zhang Mingbo in 2020, which suggested that such research topic would gain popularity in the future and might serve as potential frontiers in this research field.

Occurrence frequency and citation burst of keywords

Keyword networks are visualized in Figure 4(a). Keyword occurrence frequency is represented by the size of nodes, while the distance between them represents their association strength. Those keywords with a closer distance were grouped into a single cluster, roughly indicating the research theme. Cluster 1 is colored in red, with the main keywords focusing on RFA and thyroid benign nodule-related terms such as ‘RFA’, ‘thyroid nodules’, ‘benign nodules’, and ‘hypothyroidism’. Cluster 2 in green focused on different thermal ablation techniques and malignant thyroid nodules, with the main keywords ‘thermal ablation’, ‘papillary thyroid carcinoma’, ‘microwave’, and ‘laser’. Other terms, such as ‘Ultrasound’ and ‘Surgery’, also appeared in cluster 2. Cluster 3 was marked in blue color, focusing on the application of thermal ablation in PTMC with the main keywords ‘MWA’ ‘LA’, ‘PTMC’, and ‘complications’. Yellow cluster 4 concentrated on the safety and efficacy of thermal ablation for benign nodules and recurrent thyroid cancer, mainly involving ‘benign thyroid nodules’ ‘recurrent thyroid cancer’ ‘complication’ ‘safety’, and ‘efficacy’. In purple color, cluster 5 signified a special thermal ablation type including ‘ablation techniques’ and ‘HIFU’. Figure 4(b) illustrates the overlay visualization of author keywords. Keywords appearing earlier are colored blue, whereas the newly appearing keywords are highlighted in red. Keywords such as ‘thyroid nodule’ ‘RFA’ ‘MWA’ ‘LA’, and ‘ultrasound’ were the major topics in the early period. In contrast, the keywords ‘PTMC’ ‘complications’, and ‘recurrence’ have become popular in recent years and attracted much attention. Figure 4(c) displays the ten most frequent keywords, with ‘RFA’ claiming the top spot with 221 frequencies, followed by ‘thyroid’ (n = 145) and ‘thyroid nodule’ (n = 125).

Figure 4. Analysis of the research hotspots in the field of thermal ablation for thyroid nodules. (a) Keyword co-occurrence of author keywords. (b) Time-overlapping co-occurrence analysis network of author keywords. (c) A list of the top 20 most frequently used keywords. (d) Visualization map of the top 20 keywords with the strongest citation bursts.

Figure 4(d) shows the top 20 keywords with the strongest bursts of citations, with one year as the minimum burst duration. The keywords ‘experience’, ‘photocoagulation’, and ‘papillary’ have received the most prolonged attention in recent years. The keywords ‘PTMC’ and ‘association guideline’ have been used more recently, which indicates that these keywords have attracted considerable attention lately and potentially become important research topics in the future.

Discussion

This bibliometric study analyzed the development of ultrasound-guided thermal ablation for thyroid nodules from 2000 to 2022. Articles on thermal ablation for thyroid nodules showed an increasing tendency over the past two decades, with 2021 recording the highest number of published literatures. The main contributors in the thermal ablation field were almost all from China, South Korea, and Italy. This distribution was similar to the research field of PTMC, in which China, Korea, and the USA were the main contributing countries [20]. Countries with a high number of publications also have more active institutions. China had the five most productive institutions. It is noted that those productive institutions, including the Chinese People’s Liberation Army General Hospital, Shanghai Jiaotong University, and Sun Yat-sen University, conducted more recent research in this area.

The majority of the publishers of the ten most active journals are from USA and Europe. The Korean Journal of Radiology and Ultrasonography were only two journals from Asia. The International Journal of Hyperthermia was the most productive journal in the field of thermal ablation for thyroid nodules. Not surprisingly, this journal is the official journal of the Society for Thermal Medicine, the European Society for Hyperthermic Oncology, and the Japanese Society for Thermal Medicine. This journal primarily publishes research related to therapeutic thermal ablation, but it also publishes thermal ablation therapy on other organs, such as the liver and parathyroid. In addition, Thyroid was the most cited journal. Co-authorship analysis is an effective method for discovering existing partnerships and facilitating their development. In the field of thermal ablation for thyroid nodules, authors still cooperate on a national basis, with less international cooperation. The enhancement of international collaboration in the future may help to conduct higher-quality research.

Research hotspots refer to topics that have gained much attention in a specific area of research during a particular period. Analyzing citations can reveal publications’ academic influence. In the research field of thermal ablation, the highest-cited reference is the 2016 American guidelines for thyroid nodules, which first proposed a comprehensive indication of thermal ablation for thyroid nodules [23]. This study recommended LA or RFA for treating solid or complex thyroid nodules that progressively enlarge, exhibit symptoms, or cause cosmetic concerns. It also highlighted the importance of repeating fine-needle aspiration for cytologic confirmation before thermal ablation. Furthermore, it comprehensively discussed thermal ablation treatment’s efficacy, limitations, and adverse effects. This guideline remarkably confirmed the clinical value of thermal ablation in treating benign thyroid nodules. Nevertheless, this guideline did not consider thermal ablation as an alternative treatment for malignant thyroid lesions.

The visualization network was roughly divided into five clusters for each main topic through co-occurrence clustering analysis. Figure 4 shows that ‘PTMC’ has been a popular topic in recent years, indicating it is a focus point in the field of thermal ablation for thyroid nodules. Since most guidelines still regard surgery as the preferred treatment for PTMC, most recent articles have focused on comparing efficacy and safety between thermal ablation and surgery [24–27]. For solitary T1aN0M0 PTMC, even for T1bN0M0, there were no evident differences in disease progression and major complications between MWA and surgical resection [28]. It was revealed in a systematic review and meta-analysis of 1770 patients with 1882 tumors that RFA was a safe and effective treatment for low-risk PTMC. RFA could be envisioned as a step-up treatment after local tumor growth under active surveillance for PTMC. It could also serve as initial treatment in PTMC patients with severe anxiety about active surveillance [14]. Another recent meta-analysis pointed out thermal ablation had better economic benefits than surgical treatment for patients with PTMC [29]. Previous studies mainly focused on unifocal PTMC, the application of thermal ablation in multiple PTMC was rarely reported. Yan’s recent study suggested that RFA might be a promising treatment for both unifocal and multifocal PTMC in properly selected patients after sufficient preoperative evaluation [30]. One Chinese expert consensus summarized practical recommendations about standardized and improved LA treatment for PTMC, which provided a basis for applying LA in the treatment of PTMC [31].

Notably, a recent burst of keywords is indicative of new frontiers in thermal ablation. It suggests that ‘association guideline’ and ‘PTMC’ are the most recent keywords. Association guidelines about thermal ablation have been a consistent burst keyword since 2020. Since thermal ablation was proposed to apply in thyroid nodules, multiple guidelines from different nations have been published, highlighting the critical value of thermal ablation in treating thyroid nodules. Korean guidelines and consensus played a leading role. In 2009, the Korean Society of Thyroid Radiology (KSThR) primarily proposed the first set of recommendations for RFA of thyroid nodules. The Task Force Committee of the KSThR further indicated that RFA could be considered for the patient if a pathologically benign nodule’s diameter was larger than 2 cm and continued to grow; meanwhile, symptoms and clinical concerns were present [32]. According to the KSThR consensus report, RFA was a safe and well-tolerated technique, meanwhile, it was associated with few complications when performed by experienced clinicians. RFA was recommended as the first-line treatment method for solid and predominantly solid benign nodules, as well as the second approach in cases with unresolved symptoms or recurrence after ethanol ablation [33].

Guidelines in Europe and USA started late but updated rapidly. The 2015 American Thyroid Association (ATA) guidelines did not indicate that thermal ablation could be an alternative for benign thyroid nodules [4]. In contrast, the 2016 American Association of Clinical Endocrinologists (AACE) guidelines recommended LA or RFA to treat solid or complex benign thyroid nodules that consistently enlarge or cause symptomatic discomfort and cosmetic concerns [23]. In 2020 guidelines from European Thyroid Association (ETA), LA and RFA were recommended as the first-line thermal ablation modalities for benign nodules, while MWA was the second-line procedure. HIFU should be considered only for selected nodules in patients unsuitable for or declining other thermal ablation procedures due to its high cost and lower efficacy [34].

PTMC has been another ongoing burst keyword since 2020, consistent with the development of minimally-invasive treatment for PTMC. Nowadays, guidelines and consensus vary slightly between associations about the scope of application of thermal ablation for PTMC. The 2015 ATA guidelines and the 2017 South Korean Thyroid Radiofrequency Guidelines recommended that thermal ablation be employed only in patients with high surgical risk and those who refused additional surgery [4, 33]. The 2018 Austrian practice guidelines did not recommend thermal ablation in malignant thyroid nodules [35]. In 2020, Chinese experts published a consensus to standardize the application of thermal ablation for thyroid tumors [36]. The 2021 ETA practice guidelines and the 2021 international multidisciplinary consensus statement suggested that thermal ablation should be considered for PTMC in the following conditions: (1) patients are at risk of surgery; (2) have a short life expectancy (3) suffer from other diseases; (4) decline surgery; (5) hope to stop active surveillance [37]. Nevertheless, in mainstream statements, surgery has still been recommended as the primary treatment for patients with PTMC. Thermal ablation’s long-term safety and efficacy for treating PTMC require further investigation.

It is undeniable that this study has some limitations. Firstly, although the WOSCC database has been mentioned as the most reliable database for bibliometric studies, some articles might not be included. Secondly, there may be selection bias due to the majority of articles being published in English. Thirdly, inconsistencies may occur in various aspects. For instance, one institution may use different names at different stages of its history.

In conclusions, it is the first bibliometric study offering an overview of the development of research publications related to thermal ablation for thyroid nodules since 2000. We identified the most prominent references, countries, institutions, journals, and authors to indicate the most influential research. Our findings aid in determining potential directions of future research on thermal ablation for thyroid nodules. Further investigation is required to elucidate the long-term efficacy of thermal ablation in treating PTMC. Moreover, the standardized and representative guidelines immensely attract the attention of researchers, which is crucial for the broad application of thermal ablation in treating thyroid nodules.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Additional information

Funding

This study was supported by the National High Level Hospital Clinical Research Funding (No. 2023-NHLHCRF-YYPPLC-ZR-09).