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REVIEW ARTICLE

THE MOST-CITED WORKS IN BRAIN ARTERIOVENOUS


MALFORMATIONS: BIBLIOMETRIC ANALYSIS OF 100
MOST CITED ARTICLES AND TREND IN CITATION
CLASSICS
Taiwo Akhigbe∗ , Adalan Zolnourian∗∗,1 and Emmanuel Tigalya∗
∗ Department of General Medicine Altnagelvin Area Hospital Northern Ireland United Kingdom., ∗∗ Department of Neurosurgery University Hospital
Southampton United Kingdom.

ABSTRACT
Background The number of times that a published article is cited is one indicator of its scientific impact. There is
an abundance of articles published on brain arteriovenous malformation [AVM]. Bibliometric analyses are useful in
determining most impactful studies within this field. This study aims to evaluate most cited works in brain AVM using
bibliometric analyses to identify most relevant research and newest trends. Methods: Brain AVM specific search using
Harzing publish or Perish publicly assessable software that indexes citations from Google Scholar were performed in
May 2017. Full length articles 100 most cited articles were reviewed base on the aim of this study. Results: After a
detailed search, 164 articles with a total number of 36776 citations over 68 year period were obtained. Further analysis
performed to obtain the 100 most cited works. The top 10 most cited article obtained further. The top 100 papers included
were cited on average of 295 times per year ranged 104 to 1827. Publication date ranged from 1981 to 2014. Sixty-six of
the 100 articles were from the United States of America, 11 from Canada, over 15 from Europe. The journal publishing
the highest number of the top 100 highly cited articles was Journal of Neurosurgery with 38 publications. The most
corresponding authors were from neurosurgical speciality. Conclusion This current report provides analysis of the most
influential works in brain AVM research describing the trend of most cited works with its comprehensive list.
KEYWORDS Brain arteriovenous malformations; bibliometric analysis; citation classics

brain malformations (BAVMs) are a complex of abnormal ar-


teries and veins that directly fistualize without an intervening
capillary bed. From a purely categorical level, BAVMs differ
Introduction from other fistulous vascular malformations, such as a vein of
Brain arteriovenous malformations (AVMs) are abnormal con- Galen malformations, dural arteriovenous fistulas, or secondary
nections between arteries and veins leading to arteriovenous malformations that arise from trauma, or neovascularization
shunting with an intervening network of vessels termed nidus that occurs after chronic cerebral venous occlusion [2]. Brain
[1]. This was first described by Steinheil in 1895, arteriovenous AVM has been recognised as a significant cause of death, long-
term morbidity due to intracranial haemorrhage and epilepsy. It
Copyright © 2018 by the Bulgarian Association of Young Surgeons is often difficult to quantify the significance of a given published
DOI: 10.5455/IJMRCR.Most-Cited-Works-Brain-Arteriovenous-Malformations work. However, one useful index of influence is the total num-
First Received: June 04, 2018
Accepted: July 02, 2018
ber of citations accrue overtime by the published article if more
Reviewers: Slavomir Kondoff (BG); Junfei Zhao (USA) than 400 citations referred to as citation classics[3]. Identifying
1
Department of Neurosurgery University Hospital Southampton United Kingdom. these highly cited works is essential to clinicians and researcher
E-mail:ardalan.zolnourian@uhs.nhs.uk

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Table 1 Top 10 Brain arteriovenous malformation-specific citations classics
Rank Citation First Author Title year Journal Country
A proposed grading system for
1 1827 R.F Speltzler 1986 Journal of Neurosurgery USA
arteriovenous malformations
The natural history of
symptomatic arteriovenous
2 1017 S.L Ondra 1990 Journal of Neurosurgery USA
malformation of the brain: 24
years follow up assessment
The pathology of vascular
3 827 W.F McCormick 1966 Journal of Neurosurgery USA
(arteriovenous) malformation
Bleeding from cerebral
4 758 C.J Graf arteriovenous malformation as a 1983 Journal of Neurosurgery USA
part of the natural history
Stereotactic radiosurgery for
5 752 L.D Lunsford 1991 Journal of Neurosurgery USA
arteriovenous malformation of the brain
Arteriovenous malformation of Journal of Neurology
6 734 P.M Crawford the brain; natural history in 1986 Neurosurgery & UK
unoperated patients Psychiatry
The natural history of unruptured
7 634 R.D Brown Jr intracranial arteriovenous 1988 Journal of Neurosurgery USA
malformations
Clinical outcome of radiosurgery
8 606 L. Steiner for cerebral arteriovenous 1992 Journal of Neurosurgery Sweden
malformation
Bragg-peak proton-beam therapy
New England
9 578 R.N Kjellberg for arteriovenous malformation of 1983 USA
Journal of Medicine
the brain
Predictors of haemorrhage in
10 469 C. Stapf patients with untreated brain 2006 Neurology USA
arteriovenous malformations

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
for evidence-based practice and current research trend and fo-
cus in brain arteriovenous malformation. Also, citation classics Table 2 Countries of origin of top-cited articles
represent the highest impact work in a specific field and offer Country Number of Articles
insights to a high area of research within this field.
Group analysis of these articles will serve to understand the United States of America 66
changing landscape and trend in this field over time. This can Canada 11
be termed bibliometric analyses, has been previously applied to
few subspecialties in neurosurgery such as epilepsy [4], pain [5] United Kingdom 3
and skull base neurosurgery [6]
Sweden 3
In spite of the rise in bibliometric analyses, currently, no such
analyses have been performed for brain AVMs research. This Australia 3
article aims to present a detailed and extensive bibliometric
Japan 3
analysis of the most highly cited works related to brain AVM
describing the changing trends and citation classics for investi- Germany 2
gators in this field.
Italy 2
Methods Search Strategy Finland 1
To identify highly cited works in brain AVM, we performed a Norway 1
generalised search using Harzing publish or perish [7], free acces-
Netherlands 1
sible software search engine easily accessible to the public, it in-
dexes raw citations from Google scholar with numerous journal Switzerland 1
articles and corresponding citation. The search was performed
in May 2017 without restriction of publication date. Search France 1
term used was “arteriovenous brain malformation”, “cerebral Greece 1
arteriovenous malformation”, “intracranial arteriovenous mal-
formation”. Also, a supplementary search was conducted using Turkey 1
most cited authors name derived from previous search terms;
authors included were Speltzler RF, SL Ondra, WF McCormick,
Graf CJ, Steiner L, Brown RD Jr, Kjellerg RN, Stapf C, Faults D. Sixty-six of the 100 articles were from the United States of
and many more. America, 11 from Canada, over 15 from Europe (Table 2). The
This search was field sensitive [4] rather than field specific, journal publishing the highest number of the top 100 highly
that is to say, articles related to Brain AVM in neurosurgery, cited articles was Journal of Neurosurgery with 38 publications.
neurosciences and other health-related publications. Inclusion Journal publishing two or more than highly cited works are
criteria were articles relevant to the field of brain AVM and pub- presented in Table 3. Christian Stapf and Bruce Pollock were
lished in peer-reviewed journal. We included clinical articles, the most prolific primary authors in the top 100 cited articles
systematic reviews, meta-analysis and non-systematic reviews with four papers each [Table 4]. The most corresponding authors
(narrative reviews). The full-length articles with citation of 100 were from neurosurgical speciality.
and above in the field of Brain AVM research were obtained and The citation classics (article cited more than 400 times) were
extensively reviewed. Articles related to aneurysmal subarach- published in seven different journals (Supplementary data) with
noid haemorrhage were excluded. The full-length articles of 100 13 identified citation classics. The journal that published the
most cited works were obtained and reviewed. greatest number of citation classics was a journal of Neuro-
surgery with seven papers
Data coding and Analysis
After rigorous collection of 100 most cited articles with specific
data collected from each article for some citations, publication Table 3 Journal (with more than two articles) in most cited
year, and the name of first author, the title of the article, speciality articles in brain arteriovenous malformation.
and country of the corresponding author at the time of publica- Journal Number of Articles
tion. The data on most cited articles are ranked in descending
order by citation numbers. Journal of Neurosurgery 38
Neurosurgery 18
Results
Stroke 13
After detailed and rigorous analyses of 164 articles with a total
number of 36776 citations over a 68-year period were obtained. Lancet 5
Further analysis performed to get the 100 most cited works. The America Journal of Neuroradiology 4
top 10 most cited article are presented in Table 1 full list of the
100 most cited articles can be found in Supplementary Table 1. New England Journal of Medicine 3
The top 100 papers included were cited on average of 295
Neurology 2
times per year ranged 104 to 1827. Publication date ranged from
1981 to 2014. Speltzer et al. published the most frequently cited Journal of America Medical
article (1827 citations). In 1986 in Journal of Neurosurgery titled 2
Association
“A proposed grading system for arteriovenous malformation”.

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Table 4 The most common primary authors with more than
one articles of the top 100 cited articles in brain arteriovenous
malformation.
First Author Number of Article Current Affiliation
Stroke and Neurological Institute, Columbia
Christian Stapf 4
University, New York, USA
Bruce E Pollock 4 Neurosurgery, Mayo Clinic, USA
William A Friedman 3 Neurosurgery, University of Florida USA
Neurological Surgery, University of
Michael T Lawton 3
Califonia San Francisco, USA
Barrows Neurological Institute, Phoenix,
Robert F Spetzler 2 Figure 1: Publication trend over the years
Arizona, USA
Interventional Neuroradiology, University
Robert A Willinsky 2
of Toronto, Canada
Neurosurgery, Macquarie University,
Discussion:
Michael K Morgan 2
Sidney Australia In this study, we identified 100 most cited articles in the field of
GM Debrum 2
Neurosurgery, University of Illinois, brain AVM research. Bibliometric analyses do not necessarily
Chicago, USA provide an evaluation of the quality of research of its impact
Alfred J Luessenhop 2
Neurosurgery Georgetown University, on clinical practice, but they portray historical account research
Washington DC [Retired 1993] publication with its changing landscapes of a scientific question
A.Hartmann 2 and significant trend of knowledge been accumulated over the
J H Choi 2 time. Trends in highly cited works allow projections and plan-
ning future foe focus of high-impact and landmark research in a
particular field.
Highly cited articles are one of the indicators of most influ-
ential work in a given field hence its imperative for clinicians
and academic community to be familiar with these articles as a
template for evidence-based practice and platform for further
research. This study identified only one randomised control trial
in the top 100 most cited articles and had been termed the first-
ever randomised controlled trial of a therapeutic intervention
to improve the prognosis of brain arteriovenous malformation
(Medical management with or without interventional therapy
for unruptured AVM). However, it was stopped early because of
Table 5 Comparison between citation classics in B-AVM, a- problems. This shows that lots of research still needed in brain
SAH, Epilepsy and Parkinson’s disease AVM.
Topic bAVM aSAH Epilepsy Parkinson disease
We compared citation classics of this study with other disci-
Year of conducting plines (Table 5), most massive citation classics was from Parkin-
2017 2015 2012 2011
citations search son disease however neurological citations from brain AVM has
Number of citations the least number of randomised controlled trial, just 1%, while
13 73 89 107
classics identified aneurysmal subarachnoid haemorrhage 7%. The rate of citation
Most cited time 1990-1999 1990-1999 1990-1999 1990-1999
varies significantly among disciplines; it may be that in brain
AVM research citations are accumulated at a slower pace than
Highest citation
1827 2763 3749 4327 other disciplines [7]
number of an article
Top journal
Randomised control Limitations
1% 7% 7% 5%
trial
There are several limitations of our studies synonymous with
Google Google Google Thomson Reuters
Database search most bibliometric studies including the possibility of missing
scholar scholar scholar web of science
highly cited work as a result of a single database search strategy.
Articles absence from the list of most cited works is not an in-
dicator of inferior impact to clinical practice. Citation provides
a global indicator of landmark publication in a specific field,
and this serves as a significant guide for essential and essential
literature for researchers

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Rank Citation First Author Title year Journal Country
A proposed grading system for Journal of
1 1827 R.F Speltzler 1986 USA
arteriovenous malformations Neurosurgery
The natural history of
symptomatic arteriovenous Journal of
2 1017 S.L Ondra 1990 USA
malformation of the brain: 24 Neurosurgery
years follow up assessment
The pathology of vascular Journal of
3 827 W.F McCormick 1966 USA
(arteriovenous) malformation Neurosurgery
Bleeding from cerebral
Journal of
4 758 C.J Graf arteriovenous malformation as a 1983 USA
Neurosurgery
part of the natural history
Stereotactic radiosurgery for
Journal of
5 752 L.D Lunsford arteriovenous malformation of the 1991 USA
Neurosurgery
brain
Journal of
Arteriovenous malformation of
Neurology
6 734 P.M Crawford the brain; natural history in 1986 UK
Neurosurgery &
unoperated patients
Psychiatry
The natural history of unruptured
Journal of
7 634 R.D Brown Jr intracranial arteriovenous 1988 USA
Neurosurgery
malformations
Clinical outcome of radiosurgery
Journal of
8 606 L. Steiner for cerebral arteriovenous 1992 Sweden
Neurosurgery
malformation
Bragg-peak proton-beam therapy New England
9 578 R.N Kjellberg for arteriovenous malformation of 1983 Journal of USA
the brain Medicine
Predictors of haemorrhage in
10 469 C. Stapf patients with untreated brain 2006 Neurology USA
arteriovenous malformations
Recommendation for the
11 457 C.S Oglivy management of intracranial 2001 Stroke USA
arteriovenous malformation
Natural history of arteriovenous
12 444 D.Fults malformation of the brain: a 1984 Neurosurgery USA
clinical study
Journal of
Artificial embolisation of cerebral
America
13 403 A.J Luessenhop arteries: report of use in case of 1960 USA
Medical
arteriovenous malformation
Association

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Treatment of brain arteriovenous
Journal of
14 388 Y. Gobin malformation by embolisation and 1996 USA
Neurology
radiosurgery
The prospective application of the
15 386 M.G Hamilton grading system of arteriovenous 1994 Neurosurgery USA
malformation
Relationship of perfusion pressure
and size to the risk of Journal of
16 385 R.F Spetzler 1992 USA
haemorrhage from an Neurosurgery
arteriovenous malformation
Arteriovenous malformation of
Journal of
17 384 D.M.C Forster the brain: a long-term clinical 1972 Sweden
Neurosurgery
study
Embolisation of arteriovenous
malformation with onyx:
18 350 R Jahan 2001 Neurosurgery USA
clinicopathological experience in
23 patients
An arterial aneurysm associated
with cerebral arteriovenous Journal of
19 348 G. Redekop 1998 Canada
malformation: classification, Neurosurgery
incidence and risk of haemorrhage
Factors associated with successful
20 344 B.E Pollock arteriovenous malformation 1998 Neurosurgery USA
radiosurgery
Linear accelerator radiosurgery
Journal of
21 341 W.A Friedman for arteriovenous malformation: 1995 USA
Neurosurgery
relationship of size to the outcome
A systematic review of the
22 331 R. Al-Shahi frequency and prognosis of 2001 Brain UK
arteriovenous malformation in adults
A heamodynamic aspect of
Journal of
23 331 H. Nornes cerebral arteriovenous 1980 Norway
Neurosurgery
malformation
24 326 I.G Fleetwood Arteriovenous malformation 2002 Lancet USA
Medical management with or
without interventional therapy for
25 318 J.P Mohr unruptured arteriovenous 2014 Lancet USA
malformation [ARUBA]; a
multicentre non-blinded RCT
Stereotactic heavy charged
particles Bragg-peak radiation for New Journal
26 318 G. K Steinberg 1990 USA
intracranial arteriovenous of England
malformation

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Haemorrhage after stereotactic
27 310 B.E Pollock radiosurgery for cerebral 1996 Neurosurgery USA
arteriovenous malformation
Natural history of brain
arteriovenous malformation: a
28 303 J.A Hernesniemi 2008 Neurosurgery Finland
long-term follow-up study of risk
of haemorrhage in 238 patients
Combined endovascular
embolisation and surgery in the
Journal of
29 302 F.Vinuela management of arteriovenous 1991 USA
Neurosurgery
malformation: an experience with
101 cases.
Demographic, morphological and
clinical characteristics of 1289
30 297 C. Hofmeister 2000 Stroke Germany
patients with brain arteriovenous
malformation
The natural history of an
Journal of
31 297 JA Jane aneurysm and arteriovenous 1985 USA
Neurosurgery
malformation
Histopathology of arteriovenous
Journal of
32 297 B.F Scheider malformation after gamma knife 1997 USA
Neurosurgery
radiosurgery
Intention-to-treat analysis of
Spetzler-Martin Grade IV and V Journal of
33 287 P.P Han 2003 USA
arteriovenous malformation: Neurosurgery
natural history and paradigm
Risk of haemorrhage after New England
34 278 K. Maruyama radiosurgery for cerebral 2005 Journal of Japan
arteriovenous malformation Medicine
Cerebral arteriovenous
malformation: indications for and Journal of
35 260 A.J Luessenhop 1984 USA
results of surgery and role of Neurosurgery
intravascular techniques
Embolization of cerebral
Journal of
36 259 G.M Debrum arteriovenous malformation with 1982 USA
Neurosurgery
bucrylate: experience in 46 cases
The risk of haemorrhage after
Journal of
37 252 W.A Friedman radiosurgery for arteriovenous 1996 USA
Neurosurgery
malformations
The effect of embolisation with
38 250 J.J Jafar N-butyl cyanoacrylate before 1993 Journal of USA
surgical resection of cerebral

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Neurosurgery
arteriovenous malformations
Endovascular treatment of
America
intracranial arteriovenous
39 250 W.Weber 2007 Journal of Germany
malformation with onyx; technical
Neuroradiology
aspects
Arteriovenous malformations;
Journal of
40 249 D. Parkinson summary of 100 consecutive 1980 Canada
Neurosurgery
supratentorial cases
Natural history and predictive
41 248 L. da Costa features of haemorrhage from 2009 Stroke Canada
brain arteriovenous malformation
Journal of
Treatment of brain arteriovenous
America
42 244 J Van Beijnum malformation: a systematic review 2011 Netherlands
Medical
and meta-analysis
Association
A proposed radiosurgery grading for Journal of
43 241 B.E Pollock 2002 USA
arteriovenous malformations Neurosurgery
Embolization of the nidus of brain
44 238 G.M Debrum arteriovenous malformation with 1997 Neurosurgery USA
butyl cyanoacrylate
Analysis of venous drainage
Journal of
45 238 Y. Miyasaka system as a factor in haemorrhage 1992 Japan
Neurosurgery
from arteriovenous malformations
New England
Arteriovenous malformations of
46 237 R.M Friedlander 2007 Journal of USA
the brain
Medicine
Correlation of the
angioarchitecture of cerebral
47 230 F. Turjman arteriovenous malformation with 1995 Neurosurgery USA
the clinical presentation of
haemorrhage
Endovascular treatment of
intracranial arteriovenous Journal of
48 225 D. Fournier 1991 Canada
malformations: experience in 49 Neurosurgery
cases
Advanced
and
Endovascular treatment of brain
49 222 A. Valavanis 1998 Technical Switzerland
arteriovenous malformation
standard in
Neurosurgery
The natural course of unoperated
intracranial arteriovenous Journal of
50 218 Y. Itoyama 1989 Japan
malformations: a study of 50 Neurosurgery
cases

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Curative embolisation of cerebral
51 218 V. Katsaridis arteriovenous malformations with 2008 Neuroradiology Greece
Onyx in 101 patients
Linear accelerator radiosurgery for Journal of
52 215 W.A Friedman 1992 Japan
arteriovenous malformations Neurosurgery
Nidal embolisation of brain America
53 212 C. Mounayer arteriovenous malformation using 2007 Journal of France
Onyx in 94 patients Neuroradiology
Posterior fossa arteriovenous Journal of
54 207 C.G Drake 1986 Canada
malformations Neurosurgery
Repeat stereotactic radiosurgery
of arteriovenous malformations:
55 201 B.E Pollock 1996 Neurosurgery USA
factors associated with incomplete
obliteration
Brain arteriovenous
56 200 J.H Choi 2005 Lancet Neurology USA
malformations in adults
Interim report of the radiological
treatment of cerebral
Journal of
57 199 Y. Yamamoto arteriovenous malformation: 1995 USA
Neurosurgery
influence of size, dose and time
on technical obliteration rate
International
Five-year results of LINAC Journal of
radiosurgery for arteriovenous Radiation
58 198 L. Miyawaki 1999 USA
malformations: outcome of large Oncology,
arteriovenous malformations Biology and
Physics
Cure, morbidity and mortality
associated with embolisation of
brain arteriovenous
59 198 R.T Frizzel 1995 Neurosurgery USA
malformations: a review of 1246
patients in 32 series over a 35-
year period
Recurrent cerebral arteriovenous
Journal of
60 189 A.Kader malformations after a negative 1996 USA
Neurosurgery
postoperative angiogram
Arteriovenous malformation Journal of
61 188 J.L Robinson 1974 UK
aneurysm and pregnancy Neurosurgery
Endovascular treatment of brain
arteriovenous malformations with
62 185 I.Saatci 2011 Journal of Turkey
prolonged intranidal onyx
injection technique: long-term

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results in 350 consecutive patients Neurosurgery
Multimodality of dep
arteriovenous malformations:
63 179 M.T Lawton 1995 Neurosurgery USA
thalamus, basal ganglia and
brainstem
Intracranial arteriovenous
Journal of
64 179 B. Guidetti malformations; consecutive and 1980 Italy
Neurosurgery
surgical treatment
A population-based study of brain
65 173 H.T ApSimon 2002 Stroke Australia
arteriovenous malformations
Risk of endovascular treatment of
66 170 A.Hartmann 2002 Stroke USA
arteriovenous brain malformations
Canadian
Arteriovenous malformation of
67 166 D. Kondziolka 1992 Journal of Canada
the brain: A forty year experience
Neurosciences
Epidemiology of brain
68 164 M.F Berman 2000 Neurosurgery USA
arteriovenous malformation
European
Management of patients with
69 164 M. Soderman 2003 Journal of Sweden
brain arteriovenous malformation
Radiology
A supplementary grading scale for
selecting patients with brain
70 163 M.T Lawton 2010 Neurosurgery USA
arteriovenous malformations for
surgery
Longitudinal risk of intracranial
haemorrhage in patients with
71 161 AX Halim 2004 Stroke USA
arteriovenous malformations of
the brain in a defined population
International
Radiosurgery and brain tolerance:
Journal of
analysis of neurodiagnostic
Radiation
72 158 J.C Flickinger imaging changes after gamma 1992 USA
Oncology,
knife radiosurgery for
Biology 7
arteriovenous malformations
Physics
The determinant of neurological
73 152 A.Hartmann outcome after surgery for brain 2000 Stroke USA
arteriovenous malformations
Arteriovenous malformations of
Archives of
74 152 B.M Stein the brain: current concepts and 1980 USA
Neurology
treatment

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Functional magnetic resonance
imaging of regional brain
Journal of
75 152 J. Maldijian activities of patients with 1996 USA
Neurosurgery
intracerebral arteriovenous
malformations
Complications of preoperative
Journal of
76 150 C.L Taylor embolization of cerebral 2004 USA
Neurosurgery
arteriovenous malformations
Results of multimodal treatment
of 141 patients with brain
77 149 B.L Hoh 2002 Neurosurgery USA
arteriovenous malformations and
seizures
Treatment of arteriovenous
America
malformation of the brain with
78 148 R.C Lawson 1990 Journal of USA
combined embolization and
Neuroradiology
stereotactic radiosurgery
Multiple cerebral arteriovenous
79 147 R.A Willinsky 1990 Neuroradiology Canada
malformations
Large and deep arteriovenous
80 145 M.A Stefani malformations are associated with 2002 Stroke Canada
risk of future haemorrhage
Cerebral arteriovenous
malformation in children: clinical Surgical
81 142 P. Celli 1984 Italy
features and outcome in children Neurology
and adults
The efficacy of particulate
embolisation combined with America
82 141 J.A Marthis stereotactic radiosurgery for the 1995 Journal of USA
treatment of large arteriovenous Neuroradiology
malformations of the brain
Clinical outcome after first and
recurrent haemorrhage in patients
83 140 J.H Choi 2006 Stroke USA
with untreated brain arteriovenous
malformations
Angioarchitectural factors present
in brain arteriovenous
84 140 M.A Stefani 2002 Stroke Canada
malformations associated with
haemorrhage presentation
Effect of presenting haemorrhage
on outcome after microsurgical
85 138 M.T Lawton 2005 Neurosurgery USA
resection of brain arteriovenous
malformations

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Complications of cerebral
86 133 C.J Ledezma arteriovenous malformations: 2006 Neurosurgery USA
multivariate analysis of predictive factors
Complications of surgery for
Journal of
87 131 M.K Morgan arteriovenous malformations of 1993 Australia
Neurosurgery
the brain
Brain arteriovenous
malformations: analysis of Journal of
88 130 R.A Willinsky 1987 Canada
angioarchitecture in relationship Neuroradiology
to haemorrhage
Ethanol endovascular
management of brain
89 129 W.F Yakes 1997 Neurosurgery USA
arteriovenous malformations:
initial results
Multimodality treatment of brain
90 129 S.K Natarajan arteriovenous malformation with 2008 Neurosurgery USA
microsurgery after embolisation
Abnormal expression of matrix
metalloproteinases and tissue
91 127 T. Hashimoto 2003 Stroke USA
inhibitors in metalloproteinases in
brain arteriovenous malformations
The association of an intracranial
aneurysm and arteriovenous Journal of
92 121 S. Hayashi 1981 USA
malformations of the brain: Neurosurgery
a case report
Complications of embolization of
Journal of
93 121 C.S Haw arteriovenous malformations of 2006 Canada
Neurosurgery
the brain
Invasive treatment of unruptured
Current Opinion
94 120 C. Stapf arteriovenous malformations is an 2006 USA
in Neurosurgery
experimental therapy
Feeding artery pedicle aneurysm
association with parenchyma Journal of
95 119 H.J Perata 1994 USA
haemorrhage and arteriovenous Neurosurgery
malformations in the brain
A concurrent arterial aneurysm in
96 117 C.Stapf brain arteriovenous malformations 2002 Neurology USA
with haemorrhagic presentations
Association of infratentorial brain
arteriovenous malformations with
97 116 A.V Khaw 2004 Stroke USA
haemorrhage at initial
presentations

Adalan Zolnourian et al./ International Journal of Medical Reviews and Case Reports (2018 2(3):36-48)
Effect of age on clinical or
morphological characteristics of
98 110 C.Stapf 2003 Stroke USA
patients with brain arteriovenous
malformations
Management of arteriovenous Journal of
99 107 R.A Solomon USA
malformations of the brain Neurosurgery
The surgical risk associated with
100 104 M.K Morgan management of Grade 1 & II 2007 Neurosurgery Australia
brain arteriovenous malformations

Conclusion
Brain AVM remains an area of tremendous but slow academic
interest and neurosurgeons interest in this field has been slow.
This is reflected in the trend and quantity of published work.
Also, there has been a significant shift in clinical practice towards
endovascular treatment due to better and improved technolo-
gies.

Authors’ Statements
Competing Interests
The authors declare no conflict of interest.

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