Abstract

Background: Intracranial arterial stenosis (ICAS), caused by intracranial atherosclerosis, is one of the major causes of ischemic stroke. This study identified the top 100 most-cited publications on ICAS through a bibliometric analysis.

Methods: Two independent authors conducted a search in the Web of Science database for clinical articles on ICAS published between 1993 and 2022. The top 100 most-cited articles were then extracted. For each article, the analysis covered the title, author, country of origin/affiliation, journal, total number of citations, number of citations per year, and type of study.

Results: The top 100 most-cited papers in the ICAS were authored by 565 authors from 12 countries and published in 29 journals. In terms of the 5-year trend, the largest number of papers were published between 2003 and 2007 (n = 31). The median number of citations for the 100 papers was 161 (range 109–1,115). The journal with the highest proportion of the 100 most published articles was Stroke, accounting for 41% of articles and 37% of the citations. According to country of origin, the United States of America accounted for the largest number of articles, followed by China, Japan, and South Korea, with these four countries together accounting for 81% of the total number of articles and 88% of the citations. Trends in the past five years included the use of terms such as acute ischemic stroke and mechanical thrombectomy.

Conclusion: The findings of this study provide novel insight into this field and will facilitate future research endeavors.

Keywords: Bibliometric analysis, Intracranial artery stenosis, Intracranial atherosclerosis, Neurosurgery, Vascular

INTRODUCTION

Intracranial artery stenosis (ICAS), of which intracranial atherosclerosis is the predominant background, is the leading cause of ischemic stroke, and its prevalence is high in individuals of Asian, African, and Hispanic ancestry.[ 19 , 34 , 103 ] Among Asians, ICAS was found in 30–56% of all ischemic strokes.[ 47 , 114 ] The risk of recurrence of cerebral infarction in the vascular territory of symptomatic ICAS is significantly increased in patients with a severe stenosis rate ≥70% and within 17 days of onset.[ 54 ] In a randomized controlled trial (RCT) that compared the best medical treatment and stent placement for severe stenosis ≥70%, the prognosis in the endovascular treatment group was significantly poorer.[ 24 ] Therefore, further research is warranted to verify the efficacy of endovascular treatment. Epidemiological studies have indicated differences in prevalence among racial groups, and studies on genetic background have been conducted.[ 79 ]

Numerous ICAS studies have been published to date. Bibliometric analysis has been conducted in various fields and has gained immense popularity. Specifically in neurosurgery, it has been increasingly applied to investigate diseases[ 2 , 3 , 94 ] and treatment methods in the past few years.[ 22 , 93 , 106 ] The first objective was to identify the most recognized and important research topics to familiarize clinicians with important publications in the area. The second objective was to examine the results of the current stage in a specific area and maintain the academic quality of future research.

To the best of our knowledge, no published bibliometric studies have focused on ICAS and intracranial atherosclerosis. Therefore, in this study, we aim to extract the 100 most-cited articles in the field of ICAS/intracranial atherosclerosis and evaluate their influence using bibliometric methods.

MATERIALS AND METHODS

Bibliometric search strategy

On February 12, 2023, we conducted a search in the Web of Science database to identify the most-cited papers on ICAS. The search terms were used based on the title or abstract, as presented in Figure 1 . The publication period was limited to the past 30 years, 1993–2022. The results are listed in descending order according to the number of citations in the Web of Science database. In cases where the number of citations was tied, the more recent publication was defined as the top, which has less chance of being cited. Two authors (Y.H. and Y.S.) independently screened the titles and abstracts. Articles on ICAS/intracranial atherosclerosis were included in the study.

Figure 1:

Flow diagram of data extraction of 100 most-cited publications.

Meanwhile, articles that are not published or require manual search, in which ICAS/intracranial atherosclerosis was not the main topic, that do not involve humans, with acute cerebral artery occlusion with etiology other than atherosclerosis (i.e., atrial fibrillation, radiation, and moyamoya) or extracranial carotid/vertebral artery stenosis/occlusion, and listed as a systemic atherosclerosis or stroke subtype were excluded from the study. A flow diagram of the data extraction is shown in Figure 1 . A joint discussion decided the top 100 most-cited articles between two researchers under the verification of a second author (S.M.). This study did not require ethics committee approval, as it did not include data from therapeutic interventions or animal experiments.

Extraction of data and bibliometric parameters

A list of the top 100 most-cited articles selected from the database was arranged in a data table. General data such as title, author, total citations, annual citations, journal publication, and year of publication were extracted directly from the search results. Countries and institutions were determined according to the corresponding author’s affiliation. Articles were classified as original articles or reviews based on the search results and subsequent checks. Two authors (Y.H. and Y.S.) classified the research themes of each article by screening 100 paper abstracts and keywords, and finally, verification was conducted by a third author (S.M.). Journal impact factors were obtained from the 2021 Incites Journal Citation Reports by Clarivate Analytics.

Statistical analysis

For comparisons between the two groups, the Student’s t-test was used for continuous variables. Statistical analyses were performed using the JMP Pro 16 software (SAS Institute Inc., Cary, NC, United States of America [USA]). In addition, VOSviewer software, version 1.6.19 (Leiden University, Leiden, the Netherlands), for Windows, was used to plot the data of the visualization network.

RESULTS

A total of 49,799 publications were retrieved from the Web of Science database. The top 100 most-cited articles are listed in Supplemental Table S1 .

Publication year and citation

A total of 100 articles were published between 1993 and 2019. For the 5-year trends, the most published interval was 2003–2007 (n = 31), followed by 1997–2002 (n = 24) and 2008–2012 (n = 21) [ Figure 2 ]. Papers published after 2020 were not ranked among the 100 most-cited articles. The 100 articles had a total of 21,384 citations, with a median of 161 (range 109–1,115). The top 10 most-cited papers are presented in Table 1 , accounting for 29% (n = 6,183) of the total citations of the 100 articles. The median annual citation was 9 (range, 4–90), and the list of the top 10 annually cited articles is described in Table 2 . The top 10 annual citations had a median of 35 (range, 29–90). Of the papers ranked among the top 10 by annual citations, six were included in the top 10 in total citations, while the remaining four papers, including one ranked 74^th in total citations, were newly ranked. Comparing the annual citations of papers published before 2002 with those published after 2003, the latter was significantly higher (8.2 vs. 17.1; P < 0.001).

Figure 2:

Distribution of the top 100 most-cited articles by publication year between 1993 and 2022.

Table 1:

Ten most frequently cited publications on ICAS between 1993 and 2022.

Table 2:

The top 10 ICAS publications in annual citations.

Article types, keywords, and themes

Of the top 100 most-cited articles, 91 were original articles, and nine were reviews. There was no significant difference in the total number of citations (213 vs. 225; P = 0.84) or annual number of citations (13.4 vs. 20.3; P = 0.12) between the original and the review articles. Among the 100 most-cited papers, excluding reviews, the most featured themes were endovascular treatment (29%), radiological features and diagnosis (16%), risk factors (15%), and epidemiology (10%). To visualize the connection between keywords, the relationship between the words in the title and abstract was drawn using VOSviewer [ Figure 3 ]. Of the total KeyWords Plus (810 keywords in 357 types) presented by Web of Science, the most frequently occurring words that appeared ≥10 times included stroke (n = 23), percutaneous transluminal angioplasty (n = 16), middle cerebral artery (n = 14), atherosclerosis (n = 14), ischemic stroke (n = 12), prognosis (n = 12), risk factors (n = 11), race (n = 11), and angioplasty (n = 10).

Figure 3:

Network visualization of keywords in the titles and abstracts. The minimum number of keyword occurrences was fixed at 10, and the minimum cluster size was 3. The keywords that met the threshold were plotted in several clusters, with each color representing a different cluster: The red and purple clusters represent intracranial atherosclerosis and its pathophysiology; the yellow cluster represents radiological methods; the green cluster represents antithrombotic therapy for intracranial artery stenosis; and the blue cluster represents intracranial arterial stenosis and percutaneous endovascular treatment.

Recent trends

Since all but one of the papers published after 2018 were not included in the top 100 list, trends in the past few years could not be reflected in the analysis. The top 10 most-cited papers published since 2018 are listed in Supplemental Table 2 . Among these, the median number of citations and the annual number of citations for the ten papers were 58 (range, 45–122) and 14 (range, 10–31), respectively. Furthermore, five articles discussed mechanical thrombectomy for large-vessel occlusion (LVO) in the context of ICAS.

Journals, countries, authors, and institutions

In total, 100 articles were published in 27 journals. Stroke was the most common journal (n = 41), followed by Neurology (n = 13) and the American Journal of Neuroradiology (n = 9). The three journals accounted for 63% of the total publications. The journal’s impact factors are presented in Table 3 .

Table 3:

The three journals that most frequently published the top 100 most-cited publications on ICAS.

There were 565 authors involved in the 100 publications; the corresponding authors were from 12 countries [ Figure 4 ]. Most of the top 100 most-cited articles were from the USA (n = 48), followed by China (n = 17), Japan (n = 9), and South Korea (n = 7). A total of 33 articles were published from East Asia. In terms of institutional output, the Chinese University of Hong Kong yielded the highest number of articles (n = 13), followed by the Medical University of South Carolina (n = 7) and the University of Pennsylvania (n = 5) [ Supplemental Table 3 ]. As for the author, Chimowitz[ 9 , 20 , 23 - 26 , 32 , 35 , 36 , 47 , 54 , 55 , 69 , 92 , 98 , 124 ] published the largest number of articles (n = 16), with a total citation of 5988, followed by Lynn (n = 12) and Wong (n = 12) [ Supplemental Table 4 ].

Figure 4:

Distribution of the top 100 most-cited articles by countries.

DISCUSSION

Our study identified the 100 most-cited publications on ICAS/intracranial atherosclerosis and analyzed their overall characteristics, which clarified the overall progress of the research field, along with the journals, institutions, authors, and keyword levels. Bibliometric analysis is used to examine the characteristics of published articles based on specific parameters and has been applied in the field of neurosurgery.[ 2 , 3 , 22 , 94 , 106 ]

The top 100 most-cited articles are highly rated articles in a particular field, and a quantitative analysis of these articles reveals the synthesizing characteristics of key research. ICAS, the major cause of which is intracranial atherosclerosis, is the leading cause of ischemic stroke. Several hotspots regarding the epidemiology, pathophysiology, radiology/diagnosis, and medical and surgical treatments for the disease have been identified.

Terminology selection was challenging in this study since the terminology for ICAS and intracranial atherosclerosis was not standardized; multiple search terms were necessary to enable a comprehensive analysis. The search terms were elaborated such that a wide range of articles could be extracted without missing important papers. The results of the analysis of the terminology used in the titles are listed in Supplemental Table S5 . Intracranial and atherosclerosis (-tic) are more frequently used.

Regarding the year of publication, both the number of papers and citations increased after 2003; the number of annual citations also significantly increased after 2003 compared with before 2002. This may be due to the publication of the warfarin-aspirin symptomatic intracranial disease trial, a representative RCT on medical treatment with two antithrombotic agents,[ 25 ] which compared the effects of warfarin and aspirin on symptomatic ICAS and showed that the rates of adverse events were significantly higher in the warfarin group. In addition, the stenting and aggressive medical management for preventing recurrent stroke in intracranial stenosis (SAMMPRIS) study, another RCT that compared medical and endovascular treatment, is an important clinical trial published in the New England Journal of Medicine in 2011[ 24 ] which ranked second in citation and first in annual citation among the 100 papers. The authors of this study demonstrated that intracranial stents were not effective in treating symptomatic ICAS. As for the article types, >90% of the top 100 cited articles were original articles, and <10% were review articles. In addition, annual citations were higher for review than original articles; however, no significant difference was observed. Although reviews usually tend to be more cited, many novel themes, including RCTs in the original articles, may have led to narrowing the numerical differences. Considering that papers published earlier have greater opportunities for citation, the number of citations received annually should be given more weightage. Only six out of the top 10 most-cited papers remained within the top 10 when considering annual citations. The other four publications that did not rank in the top 10 most-cited papers and were newly ranked in the top 10 annual citations comprised two articles on endovascular treatment, one on epidemiology, and one review.

The top four topics in the papers were endovascular treatment, radiological features and diagnosis, risk factors, and epidemiology, accounting for approximately 70% of the total. These results indicate that the mainstream research lies in endovascular treatment, whose efficacy has not yet been proven for ICAS, as well as diagnostic imaging and pathophysiology, including radiological features. Negative data on intracranial stents have a significant impact, and many articles on intracranial stenting have been subsequently published.

Among them, the Wingspan stent system post market surveillance trial, published in 2019, is the most important study in recent years that demonstrated the potential of intracranial stents.[ 1 ] In this study, the patient selection criteria were very strict: Age 22–80 years, symptomatic ICAS 70–99%, ≥2 mm in length, modified Rankin Scale ≤3, and ≥ eight days post-onset, and the operators were limited to those with extensive experience in treating patients with Wingspan stents. In addition, blood pressure and activated clotting time during treatment were strictly monitored, and balloon size and air pressure were specified. The authors reported that the complication rate within 72 hours after the procedure decreased to 2.6%. In the future, intracranial stenting under strict indications may be firmly established.

One limitation of this research method is that except for one paper published after 2018,[ 1 ] newer publications have had fewer opportunities for citation, considering that they were recently published. Therefore, it was inferred that recent research themes were not appropriately reflected in this analysis. Among the papers published after 2018, five articles focused on mechanical thrombectomy for LVO with an ICAS background.[ 7 , 50 , 52 , 63 , 97 ] In recent years, the number of mechanical thrombectomies performed for acute LVO has increased as evidence for this procedure has become more established.[ 40 , 83 ] Accordingly, the treatment of LVO with ICAS has also been increasing; meanwhile, conventional treatment with a stent retriever tends to be refractory and causes intraoperative re-occlusion, and appropriate additional treatments such as balloon percutaneous transluminal angioplasty and intra-arterial infusion of glycoprotein IIb/IIIa inhibitors have been suggested to be useful.[ 7 , 52 , 97 ] Further studies are warranted to improve outcomes.

Analysis of keyword relevance yielded four independent clusters. The research topics differed slightly between intracranial atherosclerosis and ICAS. Since the former represents a pathological condition, it has typically been utilized in epidemiology, risk factors, pathophysiology, and diagnostic radiology studies. In the context of ICAS, secondary prevention is a primary aim, especially in symptomatic cases. Therefore, treatment measures were the focus of these studies, which can be interpreted as being closely associated with studies on the use of antithrombotic drugs and stent therapy.

Regarding journal analysis, most of the 100 articles were published in Stroke, followed by Neurology and the American Journal of Neuroradiology, which accounted for more than 60% of all publications. Two representative RCTs were published in the New England Journal of Medicine, the journal with the highest impact factor on the list. This may be explained by the high quality of articles in these journals and the fact that researchers tend to select journals with high-impact factors citing. Another factor is that neuroradiological diagnosis is very important in research on intracranial atherosclerosis. As for authors, Chimowitz, the authors of two RCTs from the USA,[ 24 , 25 ] published the largest number of papers. The number of publications from the USA was the highest by country. This trend is similar to that observed in most other fields of neurosurgical disease and treatment.[ 2 , 3 , 22 , 106 ] Meanwhile, reports from China, Japan, and South Korea accounted for 33% of the total. This is probably because ICAS is a more common cause of stroke in East Asians than in other racial groups,[ 19 , 34 , 47 , 103 , 114 ] which has led to the revitalization of research in this region. Although the prevalence of ICAS is high in other Asian countries, reports with a significant number of citations are lacking; therefore, future research in this area is anticipated.

This study has some limitations. First, although the Web of Science is a powerful tool for literature search, it does not necessarily cover all publications. Second, some authors might have been overestimated because self-citations were not excluded. Third, the analysis was mainly based on the number of citations; hence, recent papers were less likely to be cited, resulting in an underestimation of recent valuable papers. As a precaution, we have added an analysis of papers published in the most recent five years. Even though publications on the most recent topics that remain under development through research, such as genetic analyses, could not be covered. The prevalence of ICAS is higher in Asian, African, and Hispanic populations;[ 19 , 34 , 47 , 103 , 114 ] thus, the existence of genetic aspects has been suspected. An increasing number of studies have been conducted on the genetic analysis of ICAS recently.[ 33 , 78 , 101 ] Although the genetic factors underlying ICAS remain to be elucidated, current research approaches have missed our papers related to this issue. Despite these limitations, the strength of this study is its comprehensive analysis of ICAS, an important cause of ischemic stroke. The results of this study will serve as a benchmark for future studies.

CONCLUSION

This study conducted a bibliometric analysis of research on ICAS and intracranial atherosclerosis, listing important publications in this field. This analysis provides an objective view of the current state of knowledge in the clinical and research aspects within this field, providing insights into future research emphases.

Data availability

Data supporting this study’s findings are available on request from the corresponding author.

Ethical approval

Institutional review board approval is not required.

Declaration of patient consent

Patient’s consent was not required as there are no patients in this study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

SUPPLEMENTAL TABLES

Supplemental Table 1:

The 100 most frequently cited publications on ICAS between 1993 and 2022.

Supplemental Table 2:

The ten most frequently cited publications on ICAS between 2018 and 2022.

Supplemental Table 3:

Three institutions most frequently affiliated among the 100 most frequently cited publications.

Supplemental Table 4:

Three highest-ranked authors among the 100 most frequently cited publications.

Supplemental Table 5:

Number of times each term was used in the titles of the top 100 cited publications.

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