Abstract

Background: Radiosurgery is an effective, alternative treatment modality in managing patients with cerebral arteriovenous malformations (AVMs). The present study aims to highlight the scholarly impact of the top-100 most cited articles on the radiosurgical management of AVMs.

Methods: A title-specific search using the keyword “arteriovenous malformation” was conducted in the Scopus database. The outcome of the search was rearranged based on the citations count. Articles were categorized into four entities; clinical, gamma knife radiosurgery, linear accelerator (LINAC) radiosurgery, and proton beam radiosurgery. The exclusion criteria were applied to spinal or non-intracranial AVM, conference papers, non-English articles predominantly discussing the endovascular or microsurgical management.

Results: The top-100 articles on the radiosurgical management of AVM were published between 1972 and 2016. Approximately one-third of the publications were produced between 1995 and 2000. The average citations per year for all papers were seven. The most-studied entity was pertinent to the clinical application of gamma knife radiosurgery in AVM (68%). The United States was the most active country in studying the radiosurgical application in AVM. The Journal of Neurosurgery published approximately one-third of the most-cited articles in the list. The top-3 most contributing authors, publishing 80% of articles in the list, were Lunsford et al.

Conclusion: The radiosurgical management of AVMs evolved significantly throughout the years. Identifications of the publication trends facilitate the acquisition of evidence-based articles for authors investigating various radiosurgical techniques in the treatment of AVMs.

Keywords: Arteriovenous malformation, Bibliometric, Citation analysis, Stereotactic radiosurgery

INTRODUCTION

Cerebral arteriovenous malformations (AVMs) are vascular lesions characterized by a pathological connection between the venous and arterial circulation through a nidus.[ 4 ] These lesions can be diagnosed in the pediatric and adult populations, with an incidence rate of 1 person per 100,000 and a point prevalence of 18 persons per 100,000.[ 3 ]

The treatment option for accessible AVMs is usually achieved by complete surgical resection.[ 5 ] On the contrary, inaccessible deep-seated lesions and AVMs situated in eloquent cortices are commonly managed non-surgically.[ 4 , 5 ] One of the alternative and effective methods of managing patients with AVMs is radiosurgery, especially lesions of small and moderate sizes.[ 4 , 5 , 7 ]

Radiosurgery is defined as “The localized, focused, high-dose, irradiation commonly performed using Gamma knife (Leksell Gamma Knife® Perfexion, Elekta, Stockholm, Sweden), CyberKnife (Accuray Incorporated, 1310 Chesapeake Terrace, Sunnyvale, CA 94089, USA), or linear accelerator (LINAC).”[ 5 ] Radiosurgery aims to radiate the lesion by obliterating the abnormal blood vessels of the AVM nidus, without compromising the normal brain parenchyma.[ 5 ] The clinical effectiveness of radiosurgery is commonly assessed by measuring the obliteration of the pathological blood vessels on angiography.[ 5 ] However, some lesions can become angio-occult that can be apparent only on magnetic resonance imaging. Therefore, angiographic obliteration alone cannot serve to assess the effectiveness of radiosurgery in AVMs.[ 5 ] The application of radiosurgery has yielded acceptable and affordable risk-to-benefit in the management of unruptured/partially-resected AVMs, or during staged or partial embolization.[ 7 , 8 ]

Bibliometric analyses serve to address the top-cited articles in a discipline-specific scientific topic.[ 18 ] In addition, certain areas of research requiring further development can be identified and addressed accordingly.[ 18 ] Bibliometric analyses have been performed in several neurosurgical disciplines, including peripheral, traumatic, oncology, spine, and vascular-related topics.[ 1 , 2 , 6 , 12 , 16 , 18 ]

Considering the growing field of radiosurgery and its application in the management of AVMs, it is paramount to perform a bibliometric analysis of the most-influential articles in the literature. The main aim of the study is to identify, analyze, and report the current knowledge of the top-100 most-cited articles on the radiosurgical management of cerebral AVMs.

MATERIALS AND METHODS

The identification of the most-cited articles on the radiosurgical management of AVM in the Scopus database was accessed in July 2020. The title-specific search using “arteriovenous malformation” as a search keyword was conducted. The outcome of the search was rearranged based on the article’s citations count in descending order. The acquisition of the top-100 articles discussing the radiosurgical management was selected after fulfilling our inclusion and exclusion criteria. Articles discussing the radiosurgical management of cerebral AVM as a primary outcome were included. Spinal or non-intracranial AVM, conference papers, and non-English articles predominantly discussing the endovascular or microsurgical management were excluded from the study.

The examined top-100 most cited articles were categorized into the following four entities: (1) clinical, (2) gamma knife radiosurgery, (3) linear accelerator (LINAC) radiosurgery, and (4) proton beam radiosurgery. In the performance of this bibliometric review, the following citometric relevant parameters were collected; article title, authors, 1^st author’s specialty, contributing institutions, journals, country of origin, year of publication, citation count (CC), Citation per year (CY), Hirsch index (H-Index), Journal’s Source Normalized Impact Per Paper, Journal’s SCImago Journal Rank, and Journal Impact Factor.

The present study does not involve human subjects. Therefore, it is exempted from ethical approval, giving the nature of the study being non-interventional.

RESULTS

The keyword-based literature review resulted in identifying 9939 articles discussing AVM and, of which the top-100 articles according to the inclusion criteria were examined [ Table 1 ].

Table 1:

The top-100 most cited articles on the radiosurgical management of arteriovenous malformation.

The top-100 articles on the radiosurgical management of AVM were published between 1972 and 2016 [ Figure 1 ].

Figure 1:

Publication trends for the top-100 most cited articles on the radiosurgical management of arteriovenous malformation (1972–2016).

Approximately one-third of publications were produced between 1995 and 2000. The Top-100 articles have accumulated 11,456 citations and the rate of self-citation accounted for 12.12%. The average CY for all papers was seven. The most-studied entity was pertinent to the clinical application of Gamma knife radiosurgery in AVM (68%) [ Figure 2 ]. The United States was the most active country in studying the radiosurgical application in AVM [ Figure 3 ].

Figure 2:

Categorical distribution of the radiosurgical management of arteriovenous malformation in the top-100 cited articles.

Figure 3:

Countries publishing articles on the radiosurgical management of arteriovenous malformation in the top-100 cited articles.

The University of Pittsburgh was the most prolific by producing 46 articles in the list [ Figure 4 ]. The Journal of Neurosurgery (JNS) published approximately one-third of the most-cited articles in the list [ Figure 5 ]. Examination of authors showed that Lunsford et al. were the top-3 most contributing authors by being involved in 80% of articles in the list with comparable contribution volume [ Figure 6 ].

Figure 4:

Affiliated institutions contributing to the highest cited articles on the radiosurgical management of arteriovenous malformation.

Figure 5:

The top journals publishing articles on the radiosurgical management of arteriovenous malformation and their corresponding impact factor, Journal’s Source Normalized Impact per Paper, Journal’s SCImago Journal Rank.

Figure 6:

Reputable authors publishing articles on the radiosurgical management of arteriovenous malformation.

The top-most cited article based on the citation count was authored by Lunsford et al., published in 1991 by JNS as “Stereotactic radiosurgery for AVMs of the brain,” to which it collected 520 citations over the years and was ranked the 2^nd most-cited based on the citation per year.

The top most cited articles based on the citation per year was authored by Starke et al., published in 2013 by the JNS entitled “A practical grading scale for predicting outcome after radiosurgery for AVMs: analysis of 1012 treated patients” in which it had 20.6 CY and has accumulated 144 citation count over the year.

DISCUSSION

Articles addressing the radiosurgical management of AVMs evolved throughout the decades. Publications commenced by targeting the utilization of stereotactic radiosurgery using Gamma knife in the early 1970s. In the 1980s, as a result of the development and advancement of neuroimaging and proton/photon radiation technology, the publication trends shifted toward proton beam and linear accelerator (LINAC) radiosurgery. In addition, the earliest detailed reports on the utilization of proton beam radiosurgery for AVM with the longest follow-up period were published. In the top-100 list, most articles peaked in the publication in the 1990s, comprising 45% of all articles. Those articles were targeting all aspects of the radiosurgical management of AVM including the clinical outcome, Gamma knife, LINAC, and proton beam radiosurgery. In the 21^st century, the majority of publications were highlighting the dose-response and clinical outcome predictions, comprising approximately half of the articles in the top-100 list.

The article ranking first in the top-100 list was published in 1991 by Lunsford et al. titled “Stereotactic radiosurgery for arteriovenous malformations of the brain” which received a total of 520 CC and 17.9 CY.[ 15 ] The authors investigated 227 patients who underwent stereotactic radiosurgery for cerebral AVM.[ 15 ] Their 3-year experience demonstrated that radiosurgery is an important technique for AVM obliteration, especially lesions previously rendered inoperable.[ 15 ] The success rate and risks of complications were dependent on location and volume of the AVM.[ 15 ]

A year later, the second highest cited article was published by Steiner et al. titled “Clinical outcome of radiosurgery for cerebral arteriovenous malformations” to which it received 459 CC and 16.4 CY.[ 21 ] The authors described the long-term neurological outcomes for 247 consecutive patients with AVM treated with Gamma knife.[ 21 ] In their cohort, radiosurgery has proven to obliterate AVMs as evident by angiography, with few side effects. They suggested that complete protection against rebleeding in AVM occurs only after total obliteration of the lesion.[ 21 ]

Gamma knife radiosurgery

Articles predominantly discussing the application of gamma knife radiosurgery peaked in terms of publication from 1972 to 2016. Operable and non-operable AVMs, deep-seated lesions, staging, and the risk of hemorrhage were the areas of interest to authors investigating the radiosurgical aspect of AVM. Gamma knife radiosurgery populated the majority of publications in the top 100 most cited articles on the radiosurgical management of AVM, comprising around two thirds of the articles. In the category of gamma knife radiosurgery, the first utilization of radiosurgery in obliterating AVM was discussed in the literature. Gobin et al. published an article (ranked 4^th) titled “Treatment of brain AVMs by embolization and radiosurgery” to which it received 299 CC and 12.5 CY.[ 11 ] The authors investigated a cohort of 125 patients who underwent embolization before radiosurgery.[ 11 ] The patients were included in the study as they were either refusing surgery or were labeled poor surgical candidates.[ 11 ] They concluded that embolization before radiosurgery serves to facilitate irradiation of large-sized AVMs.[ 11 ] In addition, they demonstrated that the hemorrhagic risk of the residual nidus is similar to the natural history of AVMs of the same size.[ 11 ] Pollock et al. published an article (ranked 6^th) titled “Factors associated with successful arteriovenous malformation radiosurgery” to which it received 271 CC and 12.3 CY.[ 17 ] The authors proposed a new method to report the clinical outcome of radiosurgery in AVM.[ 17 ] It comprised the incorporation of the postoperative neurological deficits and angiographic obliteration results of the AVM. Their multivariate analysis proved that younger age, location, AVM volume, and the number of draining veins were associated with a better obliteration rate after radiosurgical treatment in AVMs.[ 17 ]

LINAC radiosurgery

Articles in addressing LINAC radiosurgery had a publication peak between 1989 and 2007. Around one-fifth of the articles in the top-100 most cited publications on the radiosurgical management of AVM were investigating the usage of LINAC radiosurgery. In addition, the earliest reports on the usage of LINAC radiosurgery were published in the late 80s. Around 61% of articles addressing LINAC radiosurgery peaked in publication in the 90s. In the early years of the 21^st century, articles have carried out what has been previously published in the literature, with a relatively larger number of cohorts. Colombo et al. published an article (ranked 5^th) titled “Linear accelerator radiosurgery of cerebral AVMs: an update” to which it received 281 CC and 10.8 CY.[ 14 ] The authors aimed to report the risk of bleeding and evaluate their clinical experience in 153 patients with irradiated AVMs.[ 14 ] In patients with totally-radiated AVMs, the risk of bleeding decreased from 4.8% to 0% after radiosurgery.[ 14 ] In contrast, the risk of bleeding in partially-radiated AVMs increased from 4% to 10%.[ 14 ] Friedman et al. published an article (ranked 8^th) titled “Linear accelerator radiosurgery for arteriovenous malformations: the relationship of size to outcome” to which it received 247 CC and 9.9 CY.[ 10 ] The authors investigated the association between the size of AVM and clinical outcome in a cohort of 158 patients.[ 10 ] Their study findings demonstrated that AVMs of volumes larger than 10 cc could be successfully managed using LINAC radiosurgery.[ 10 ]

Proton beam radiosurgery

In the “proton beam radiosurgery” entity, articles peaked in the publication from 1983 to 1990. During this period, the earliest, most detailed, and longest follow-up data on the application of proton beam radiosurgery were published. In addition, authors discussed the technicality of proton beam radiosurgery, treatment protocols, and the approach to the selection criteria of patients who were rendered fit to undergo such therapy. Kjellberg et al. published an article (ranked 3^rd) titled “Bragg-Peak Proton-Beam Therapy for Arteriovenous Malformations of the Brain” to which it received 388 CC ad 10.5 CY.[ 13 ] The authors investigated the outcome of such a treatment option in patients with AVM.[ 13 ] They concluded that proton beam radiosurgery appears to be a useful and alternative treatment of choice for patients harboring cranial AVMs not suitable to other treatment modalities.[ 13 ] Steinberg et al. published an article (ranked 13^th) titled “Stereotactic heavy-charged-particle bragg-peak radiation for intracranial arteriovenous malformations” to which it received 224 CC and 7.5 CY.[ 20 ] The authors presented their experience in terms of the clinical and radiological outcome in a cohort of 86 patients with inaccessible AVMs, and they concluded that heavy-charged particles proved to be effective treatment for inaccessible AVM.[ 20 ] However, they highlighted two disadvantages of that time technique; small risk of neurological complications and the long time interval of complete obliteration.[ 20 ]

Clinical articles

Articles addressing the clinical entity of the radiosurgical management of AVM were published between 1990 and 2014. During the specified period, articles predominantly investigated predictors of successful obliteration of AVM utilizing radiosurgery. Furthermore, articles comprehensively investigated and compared dose-staged versus volume-staged radiosurgical treatment of AVM in terms of outcome and complications. Friedman et al. published an article (ranked 34^th) titled “Analysis of factors predictive of success or complications in arteriovenous malformation radiosurgery” with 122 CC and 7.2 CY.[ 9 ] The authors reviewed the clinical and radiological data in 269 consecutive patients.[ 9 ] Their multivariate analysis proved that eloquent location of AVMs and 12-Gy volume was associated with radiation-induced sequelae in radiosurgery.[ 9 ] However, radiological success was associated with a lower grade (Spetzler-Martin) and steeper/ higher dose gradients.[ 9 ] Steinberg et al. published an article (ranked 49^th) titled “Surgical resection of large incompletely treated intracranial arteriovenous malformations following stereotactic radiosurgery” with 122 CC and 7.2 CY.[ 19 ] They concluded that adjunct pretreatment with radiosurgery, few years before open surgery, serves to treat large-sized AVMs.[ 19 ]

The present bibliometric analysis on the radiosurgical management of AVM highlights the following clinical key aspects to practitioners in the field: (1) radiosurgery remains an important technique in managing patients with inoperable AVMs. (2) Complete obliteration of the lesion can be achieved by radiosurgery. (3) The obliteration rate of AVM following radiosurgery can be predicted by several factors including; age, location, volume, and the number of draining veins. (4) Prior embolization of the lesion facilitates the radiosurgical management of large-sized AVMs. (5) LINAC radiosurgery can successfully treat AVMs of relatively larger volumes (>10 cc). (6) Proton beam radiosurgery, in the form of heavy-charged particles, can be utilized to treat inaccessible AVMs. (7) Radiosurgery, before microsurgical resection, may be of use to treat large-sized and complex AVMs.

Limitations

In the current bibliometric analysis, few obstacles need to be acknowledged which may limit the generalizability of the findings. First, the rate of self-citations was encountered in more than one-tenth of the articles. Therefore, self-citations might falsely increase the CC for all published articles. However, this might be caused by the small society of radiosurgery and the limited number of institutions performing such advanced technology early in the history of radiation treatment (1970s). Second, a title-based search in a keyword-fashion might miss some articles published in the literature, and hence, not included in the analysis. Third, as the CC was considered to rank the articles in a descending order, older articles were likely to accumulate a higher number of citations throughout the years. However, the CY was calculated for all articles to balance this limitation. Fourth, only one database was utilized to conduct this bibliometric analysis. Fifth, due to the time; the relatively newer technology (i.e., CyberKnife) did not appear in our list. However, we expect an increasing number of publications relevant to this topic in the near future. Although bibliometric analyses assess the intellectual scholarly work from a quantitative perspective, the present study identified key and influential articles within this relatively growing field in the management of AVM.

CONCLUSION

The radiosurgical management of AVMs evolved significantly throughout the years. Articles addressing the application of Gamma knife radiosurgery were the most frequently published category by neurosurgeons in the field. The toptwo most cited articles in the list were both published in the JNS. Identifications of the publication trends serves as a benchmark for gaining evidence-based knowledge for authors investigating various radiosurgical techniques in AVMs.

Declaration of patient consent

Patient’s consent not required as patients identity is not disclosed or compromised.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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