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Abstract
Introduction Endovascular interventions for intracranial aneurysms have evolved substantially over the past several decades. A citation rank list is used to measure the scientific and/or clinical impact of an article. Our objective was to identify and analyze the characteristics of the 100 most cited articles in the field of endovascular therapy for intracranial aneurysms.
Methods We performed a retrospective bibliometric analysis between July and August 2017. Articles were searched on the Science Citation Index Expanded database using Web of Science in order to identify the most cited articles in the endovascular therapy of intracranial aneurysms since 1945. Using selected key terms (‘intracranial aneurysm’, ‘aneurysm’, ‘aneurysmal subarachnoid’, ‘endovascular’, ‘coiling’, ‘stent-assisted’, ‘balloon-assisted’, ‘flow-diversion’) yielded a total of 16 314 articles. The top 100 articles were identified and analyzed to extract relevant information, including citation count, authorship, article type, subject matter, institution, country of origin, and year of publication.
Results Citations for the top 100 articles ranged from 133 to 1832. All articles were cited an average of 27 times per year. There were 45 prospective studies, including 7 level–II randomized controlled trials. Most articles were published in the 2000s (n=53), and the majority constituted level III or level IV evidence. Half of the top 100 articles arose from the USA.
Conclusion This study provides a comprehensive overview of the most cited articles in the endovascular management of intracranial aneurysms. It recognizes the contributions made by key authors and institutions, providing an important framework to an enhanced understanding of the evidence behind the endovascular treatment of aneurysms.
- Intracranial aneurysm
- endovascular
- coiling
- subarachnoid haemorrhage
- flow diversion
- stent-assisted
- balloon-assisted
Statistics from Altmetric.com
- Intracranial aneurysm
- endovascular
- coiling
- subarachnoid haemorrhage
- flow diversion
- stent-assisted
- balloon-assisted
Introduction
Intracranial aneurysms are estimated to affect between 1% and 5% of asymptomatic individuals with an estimated incidence of aneurysmal subarachnoid hemorrhage of 1 case per 10 000 persons.1 While the timing of elective treatment of unruptured aneurysms is less clear, it is accepted that ruptured intracranial aneurysms require emergent treatment to reduce the risk of catastrophic re-bleeding.2
In recent decades, endovascular therapies for intracranial pathologies have evolved into a mature subspecialty, a reflection of continued progressive research and innovative interventional techniques. While surgical clipping remained the mainstay of aneurysm treatment until the advent of the Guglielmi detachable coil in 1991,3 4 the International Subarachnoid Aneurysm Trial (ISAT) in 2002 provided contemporary evidence that endovascular coiling may provide significant improvements in survival free disability at 1 year.5
A large volume of literature is available to neuroendovascular specialists who perform endovascular aneurysm treatments. The quality of the literature varies substantially and includes low impact studies and open access journals, making it difficult to identify articles of significance. An understanding of the available literature and the most heavily cited works allows for a better understanding of the evidence base when discussing and providing these treatments.
A bibliometric analysis is a quantitative method used to examine the knowledge structure and development of a research field and its publications. A citation analysis is the most common bibliometric method which focuses on citation number and number of citations per year. It is an important way to measure and assess productivity, quality, and impact of the research of individuals, groups, and institutions.6 It provides a summary method for assessing research strength and weaknesses, identifying top journals and researchers in a subject area. Importantly, it provides a framework in developing an understanding of the available literature.7
A citation analysis evaluates the impact an article has had on a specific field of medicine by measuring the number of citations an article has received.7 A citation is the acknowledgment that one scientific article (the cited article) has been referenced by another article (the citing article). The number of citations an article has is of critical importance to the publishing journal, as the more citations that an article receives during a fixed period of time, the greater the impact factor (IF) of the journal.
The IF is the most widely known and used journal level metric. It is a measure of frequency with which the ‘average article’ in a journal has been cited in a particular year. The IF is calculated over a minimum period of 3 years from the date of publication by dividing the total number of citations received over the previous 2 years by the total citable items published during that period. Controversially, the IF is often used to both measure the importance or rank of a journal and as an approximation of the prestige of that journal. The higher the IF, the more influential and noteworthy the journal is apparently deemed.8
Since 1991 the global output of academic research into the management of intracranial aneurysms has risen.9 10 A specific quantitative analysis on the articles which have had the most significant impact on the endovascular treatment of intracranial aneurysms has not yet been performed. The aim of this study was to carry out a citation analysis on the most cited articles in the endovascular treatment of intracranial aneurysms and analyze each article individually, looking at the article type, year of publication, topic of interest, citation index, authorship, country of origin, institution, and level of evidence.
Methods
Identification of the top 100 cited articles
Between July and August 2017, we performed a retrospective bibliometric analysis, identifying articles using the Web of Science (Thomson Reuters, New York, USA) which searches the Science Citation Index Expanded database, allowing access to over 12 000 peer reviewed journals and collected citation data since 1945.
The Web of Science was utilized to identify the most cited articles in the endovascular therapy of intracranial aneurysms since 1945. Using selected key terms (‘intracranial aneurysm’, ‘aneurysm’, ‘aneurysmal subarachnoid’, ‘endovascular’, ‘coiling’, ‘stent-assisted’, ‘balloon-assisted’, ‘flow-diversion’), our search performed between July and August 2017 yielded a total of 16 314 articles. These were subsequently ranked according to the number of citations and the top 100 articles identified.
Analysis of the top 100 cited articles
A further analysis of individual articles was performed by three reviewers (JM, KP, and YR) to extract relevant information for the analysis. Individual articles were reviewed to ascertain authorship, journal title and IF, article type (eg, meta-analysis or systematic review, randomized controlled trial, prospective analysis, retrospective analysis, review article, guideline, technical note, or case report), and level of evidence, subject matter, institution and country of origin, and year of publication. There are multiple methods of grading level of evidence.11 This analysis determined the level of evidence using the Australian National Health and Medical Research Council evidence hierarchy.12 Of note, this classification defines clinical guidelines as level I evidence and randomized control trials as level II evidence.
Furthermore, the citation count and citations per year were extracted using the Web of Science. When there was disagreement or discordance between reviewers, the senior author (HA) was included to achieve consensus. Google Scholar citations were also included as a new and evolving scholarly indexing platform for comparison, which includes a wider section of the literature, including online and university repositories, theses, books, and traditional articles and abstracts.
Results
The top 100 articles regarding the endovascular treatment of intracranial aneurysms according to the most citations received are listed in table 1.
The 100 ‘citation classics’ regarding the endovascular management of intracranial aneurysms and the number of calculated annual citations
The ’ISAT of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial’, published in The Lancet in 2002, has received the most citations in the past 27 years, with a total of 1832 citations (2988 citations on Google Scholar). Of note, it also remains the most cited article per year, being cited 114.5 times on average, per year. The article with the lowest number of citations in the top 100 list, ‘Creation of saccular aneurysms in the rabbit: a model suitable for testing endovascular devices’, received 134 citations (170 on Google Scholar). Overall, the mean number of citations was 291, with the top 100 articles cited an average of 27 times per year.
The ranking of the top 10 articles using Google Scholar was concordant with the results achieved using the Web of Science, despite variation for individual articles. Overall, the number of citations was higher using Google Scholar. Despite some variation the citation trend was similar across the top 100 cited articles.
Only one of the top 100 articles was published prior to 1991 (table 2), with 64% (n=64) published since the year 2000 and 12% published within the past decade.
The decades with the most number of articles in the top 100
Two of the oldest articles were published by Guido Guglielmi in 1991. This was a two part publication in the Journal of Neurosurgery, outlining the technical basis, early experimental results (Electrothrombosis of saccular aneurysms via endovascular approach. 1. Electrochemical basis, technique, and experimental results), and preliminary clinical experience (Electrothrombosis of saccular aneurysms via endovascular approach. 2. Preliminary clinical-experience) in the detachable coil system to which he would lend his name. At the time of writing, these had been cited 653 (Google Scholar 1808) and 852 (Google Scholar 1807) times, respectively. The oldest article was published in 1974 by Fyodor Serbinenko, cited 671 times (Google Scholar 1160), describing the balloon catheterization and occlusion of major cerebral vessels in 300 patients. Of the three most recent articles published in 2013, the most recent was ‘Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial’, published in Radiology, with a total of 253 citations.
Thirty-six authors contributed two or more articles to the top 100. Eighteen authors contributed four or more articles (table 3).
The authors that contributed four or more articles to the 100 most cited articles in the endovascular management of intracranial aneurysms
Fernando Vinuela, Guido Guglielmi, and David Fiorella have contributed the most articles. David Fiorella, Andy Molyneux, and S Claiborne Johnston were the first named authors on four articles each. Fernando Vinuela is the most published author, appearing on a total of 12 articles. Andy Molyneux has contributed two of the top three cited articles of all time.
The annual number of citations was also calculated by tabulating the total number of citations over the number of years and months since the article was published (table 1). The ISAT article has the highest number of total citations but is also the article with the highest annual citations (n=114.5), despite its publication in 2002.
Sixteen journals made contributions to the top 100 with eight journals providing two or more articles (table 4).
The journals and the number of articles each journal contributed to the top 100 articles
The journals with the highest IFs included The New England Journal of Medicine (IF 72.406), The Lancet (IF 47.831), Lancet Neurology (IF 26.284), and Brain (IF 10.292). The Journal of Neurosurgery (IF 4.059) supplied 25 of the top 100 articles. Stroke (IF 5.723) contributed the second highest number (20). The Lancet provided the top three cited articles.
A total of 17 countries produced the entirety of the top 100 most cited articles (figure 1), with the majority originating in the USA (50%). France, the next highest contributor, contributed nine articles. Australia, Belgium, Switzerland, and Hungary all contributed a single article each.
The countries of origin of the top 100 articles.
Two institutions contributed the most to the top 100 (table 5).
The institutions that contributed the most articles to the 100 most cited articles in the endovascular management of intracranial aneurysms
The University of California contributed 17 articles while the Radcliffe Infirmary, Oxford contributed 7. Overall, 18 institutions contributed two or more articles each.
Topics covered in each article were grouped and are outlined in table 6.
The main topics discussed within the 100 most cited articles in the endovascular management of intracranial aneurysms
Subject matter included primary endovascular coiling (n=51), flow diversion (n=12), stent assisted (n=8) and balloon assisted approaches (n=3), novel endovascular techniques (n=8), glue embolization (n=2), miscellaneous, including review articles and guidelines (n=12), and prognostication studies (n=3).
Table 7 and figure 2 summarize the types of clinical study and level of evidence within the top 100 articles.
Levels of evidence and article type comprising the 100 most cited articles in the endovascular management of intracranial aneurysms
Graphical representation of levels of evidence comprising the 100 most cited articles in the endovascular management of intracranial aneurysm.
Most of the evidence is level III or IV, with 38 original prospective and 30 original retrospective clinical studies, respectively (68%). Overall, there were 45 prospective studies which included 7 level II randomized controlled trials. Two meta-analyses and two systematic reviews were included in the top 100 cited articles.
Discussion
Endovascular therapies for intracranial pathologies have expanded dramatically in recent decades. This bibliometric analysis emphasized the top 100 articles relating to the endovascular management of intracranial aneurysms relevant to interventional neuroradiologists, neurosurgeons, and stroke physicians. Importantly, most of the articles within the top 100 represent level III or IV evidence, with 68 original prospective and retrospective studies (figure 1). Importantly, there were seven level II randomized controlled trials and two meta-analyses comparing favorably to similar bibliometric analyses of other specialties.10 13–16 This highlights the high impact literature available to the practicing interventional neuroradiologist . Furthermore, our list of top 100 articles has been published across the spectrum of radiological, neurosurgical, and neurology journals, highlighting the multidisciplinary approach to intracranial aneurysms.
The Journal of Neurosurgery, Stroke, Neurosurgery, and the American Journal of Neuroradiology featured prominently among the top 100, highlighting their important contribution in shaping the landscape of intracranial aneurysm management. Several notable high IF journals were also included in the top 100, including The Lancet, New England Journal of Medicine, Lancet Neurology, and Brain, which supplied several important articles. The Lancet was noteworthy in contributing the top three cited articles successively in 2002, 2003, and 2005, with these three articles maintaining relatively high citations per year despite their original publication over a decade ago. Of note, these three articles represented level II randomized clinical trials while the remaining articles from other high impact journals were predominantly level V review articles.
The seminal work by Fyodor Serbinenko describing the balloon occlusion of aneurysms was published in 1974. It is the only article in the top 100 cited prior to Guglielmi’s work in 1991 and remains both highly cited (Web of Science 671, Google Scholar 1160) but also historically relevant (15.25 citations per year). This work provided the basis of balloon occlusion of intracranial aneurysms in the 1980s and an important framework for the development of subsequent endovascular treatment of aneurysms described by Guglielmi.17
Notably, this study highlights the seminal and pioneering work by Guglielmi as an important contributor to the changing landscape of intracranial aneurysm management, given the relative paucity of top 100 articles published prior to 1991 and the impact of subsequent articles following his original publications. Guglielmi and colleagues published two articles outlining the first description of the Guglielmi detachable coil, techniques for deployment, and experimental results and preliminary clinical experience in the Journal of Neurosurgery in 1991. Both articles remain within the top 10 published articles, with total citation numbers of 653 (Google Scholar 1808) and 852 (Google Scholar 1807), respectively, at the time of writing. As a comparison, the pioneering work by Sean Mullan in the Journal of Neurosurgery in 1965 describing electrically induced thrombosis in intracranial aneurysm did not even make the top 100 list, with a total of 57 citations (Google Scholar 101).18
In this study, we also calculated the number of citations per year as a surrogate marker for the contemporary influence of the listed articles. While historically relevant trials will maintain a high citation number, the number of citations per year may decline over time. The ‘ISAT of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial’ remains the most cited article over the past 27 years, with a total of 1832 citations. Of note, in the 15 years since its publication, it also remains the most cited article per year (114.5 citations per year), highlighting the importance of citations per year as a metric and the articles ongoing contemporary relevance and importance in the management of patients with ruptured intracranial aneurysms.
Additionally, the endovascular approach to unruptured aneurysms demonstrates ongoing relevance with the article, ‘Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment’ remaining the second most cited article (1489 citations), with an average 99 annual citations since its original publication.
The most common topic in a recent bibliometric analysis investigating the top 100 cited articles in neurointerventional research was the endovascular management of intracranial aneurysms (n=42).19 Among these articles, this analysis demonstrated a similar ranking trend with similar topics and level of evidence to our analysis. Similarly, the Journal of Neurosurgery featured prominently among the top 100. While the inclusion of a range of topics pertaining to neurointerventional research, including mechanical stroke thrombectomy (n=22), was less focused than our analysis, many of the top cited endovascular aneurysm papers featured prominently. In contradistinction to our analysis, their top ranking article was the PROACT II study relating to intra-arterial thrombolysis, followed closely by the ISAT trial. Key differences included the inclusion of articles dating back to 1973. Importantly, our focused analysis identified several key topic areas which did not feature prominently in their top 100 list, including nine articles on the endovascular management of unruptured intracranial aneurysms, compared with two in their analysis. This is of importance as the management of unruptured aneurysms remains a key area of research and interest within the neurointerventional literature. Additionally, our analysis included more papers on endovascular management of basilar tip aneurysms (4 vs 2), including a large case series of 150 patients, and included three articles on the management of giant and large intracranial aneurysms (vs 1). These key differences are important as many of these research topics remain contemporary and relevant.
Importantly, since their publication, many of the listed articles' citation counts have increased. For example, the ISAT trial was cited 1640 during their study period of January 2016. This had increased to 1832 during our study period of July to August 2017. This variation highlights the ongoing importance of many of these articles in contemporary endovascular aneurysm management research.
To date, no other bibliographic analysis of the literature surrounding the endovascular management of aneurysms has correlated the Web of Science results with those of Google Scholar. Using Google Scholar has many advantages over traditional approaches using Web of Science. As an emerging scientific resource, Google Scholar offers clinicians and researchers access to an expanding resource spanning multiple sources, including traditional publications and abstracts, texts, as well as expanded online repositories.
Interestingly, we demonstrated a wide disparity between citation results on Web of Science and Google Scholar. While the source and context of the citation is not immediately apparent, the inclusion of these results served to further highlight the potential impact of many of these papers. For example, the ISAT trial has a much larger Google Scholar citation count (2988 citations). Indeed, a large proportion of our listed articles had higher citation counts using Google Scholar. Studies comparing citation count profiles of articles published in general medical journals have previously demonstrated a higher citation count using Google Scholar, attributed to the coverage of non-traditional online documents, including university theses and non-peer reviewed websites.20 There are several limitations with its use, including lack of transparency in assessing the quality of these citations (which may include non-scholarly sources), while its context and applicability within the scientific literature is not qualified.
Our results compare favorably with a recent bibliometric analysis investigating the most influential publications pertaining to intracranial aneurysms and aneurysmal subarachnoid hemorrhage.9 This analysis similarly identified the three Lancet articles published in 2002, 2003, and 2005, and Guglielmi’s original description of endovascular coiling, highlighting their significance even among a broader analysis of the neurosurgical literature. Their analysis differed in the inclusion of more articles published prior to 1991, with the earliest article included published in 1951. The most frequently cited article by Hunt and colleagues in 1967 pertains to surgical risk at the time of intervention in the repair of intracranial aneurysms.21 Interestingly, and despite their inclusion of articles dating back to 1951, the Journal of Neurosurgery remains the most cited journal.
A similar but more recent article spanning the spectrum of medical and surgical specialties encompasses all elements of aneurysmal subarachnoid hemorrhage.10 Our results are unique in their focus on endovascular aneurysm management, providing a more comprehensive and focused bibliometric assessment on minimally invasive treatments.
Similar bibliometric analyses have investigated the literature surrounding urology, orthopedic, plastic, cardiac, and vascular surgery, and diagnostic radiology.10 13–16 Compared with other surgical specialties, except for one article, all of the top 100 articles from our analysis have been published since 1991, with 64% published since 2000 and 12% published since 2010, indicating the more contemporary nature of endovascular techniques. Of the top 100 urology articles, all were published between 1965 and 2003, with 54% published in the 1990s.13
Similarly, the largest proportion of highly cited articles in vascular surgery originated from the 1970–1980s.22 The top 100 cited articles in orthopedic surgery were predominantly published prior to 2000, with 42% published in the 1980s and only one article published after the year 2000. Interestingly, there were no randomized controlled trials, with 43% of articles representing case series.14 This echoed a similar trend in the plastic surgery literature where the majority of evidence was level IV and V.15
We noted a similar distribution of top 100 cited diagnostic radiology articles in radiology journals by decade of publication.16 This may indicate that the development of advanced imaging technology in diagnostic imaging may have facilitated increasing access to minimally invasive image guided approaches to aneurysm treatment. Overall, when compared with bibliometric analyses of other specialties, our list on the endovascular treatment of aneurysms contains a large volume of contemporarily pertinent articles.
Our analysis had several strengths, including the focused analysis of endovascular aneurysm management spanning a range of medical disciplines, including many topics not discussed in prior analyses. The analysis contained a high proportion of original articles, including a higher proportion of randomized controlled trials compared with other similar bibliographic analyses. Furthermore, our inclusion of the Google Scholar citation count provides a novel method in assessing the impact of many of the top 100 articles.
There are several limitations which should be considered when reviewing the results of this bibliometric analysis. While providing a literature overview, the analysis does not provide or allow for any conclusions as to the quality or merit of individual articles. Older articles are more likely to be cited regardless of their impact or relevance accumulating more citations over time. Importantly, many important discoveries do not make the top 100 list as their findings are often accepted as general knowledge by the scientific community and subsequently not heavily cited. Furthermore, there is often influence on citation patterns due to citation bias and social relations within the scientific community (including self-citations), influence by publication structures, and low rates of non-English language citations. We attempted to mitigate these limitations with the inclusion of an annual citation number as a surrogate marker for article impact.
Conclusion
This study provides an important and comprehensive overview of the most cited articles in the field of endovascular management of intracranial aneurysms over the past 27 years. It recognizes the important contributions made by key authors and institutions to the field and provides an important framework to an enhanced understanding of the evidence base behind the endovascular treatment of aneurysms. Furthermore, it highlights the seminal work by Guglielmi and how his pioneering work changed the landscape of intracranial aneurysm management as well as the significance of ISAT, which remains as relevant today as it did 15 years ago.
References
Footnotes
Contributors JM performed the literature search, preliminary article analysis, and drafted and revised the paper. KP performed the literature search and preliminary article analysis. YR performed the literature search and preliminary article analysis. HKK monitored data collection and revised the draft paper. VT revised the draft paper. JAH revised the draft paper. MJL was involved in concept design and revised the draft paper. RVC revised the draft paper. DMB revised the draft paper. HA oversaw the project, concept design, and article analysis, monitored the data collection, and revised the draft paper. All authors contributed substantially to the final article.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.