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Systematic Review
Revised

Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review

[version 2; peer review: 3 approved with reservations]
Suparna Das
https://orcid.org/0000-0002-2152-2719
1, Paul Kasher
https://orcid.org/0000-0002-9213-502X
1, Mueez Waqar1, Adrian Parry-Jones1, Hiren Patel1
Suparna Das
https://orcid.org/0000-0002-2152-2719
1, Paul Kasher
https://orcid.org/0000-0002-9213-502X
1, [...] Mueez Waqar1, Adrian Parry-Jones1, Hiren Patel1
PUBLISHED 07 Oct 2024
Author details Author details
OPEN PEER REVIEW
REVIEWER STATUS

Abstract

A cerebral arteriovenous malformation (cAVM) is an abnormal tangle of cerebral blood vessels. The consensus document by the Joint Writing Group (JWG) highlighted which cAVM features should be recorded. Subsequent publications have reported cAVM angioarchitecture, but it is unknown if all followed the JWG recommendations.

The aim of this systematic review was to describe use of the JWG guidelines.

A database search, using the PRISMA checklist, was performed. We describe the proportion of publications that used JWG reporting standards, which standards were used, whether the definitions used differed from the JWG, or if any additional angiographic features were reported.

Out of 4306 articles identified, 105 were selected, and a further 114 from other sources.

Thirty-three studies (33/219; 15%) specifically referred to using JWG standards.

Since the JWG publication, few studies have used their standards to report cAVMs. This implies that the angioarchitecture of cAVMs are not routinely fully described.

Keywords

cerebral arteriovenous malformation, angioarchitecture, reporting, consensus

Corresponding author: Suparna Das
Competing interests: No competing interests were disclosed.
Grant information: The authors would like to thank the Natalie Kate Moss Trust for their generous support. PK and AP-J are supported by the Stroke Association (TSA LECT 2017/02; SA L-RC 19\100000).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Copyright:  © 2024 Das S et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
How to cite: Das S, Kasher P, Waqar M et al. Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review [version 2; peer review: 3 approved with reservations]. F1000Research 2024, 12:1252 (https://doi.org/10.12688/f1000research.139256.2) First published: 29 Sep 2023, 12:1252 (https://doi.org/10.12688/f1000research.139256.1) Latest published: 25 Nov 2024, 12:1252 (https://doi.org/10.12688/f1000research.139256.3)

Revised Amendments from Version 1

The introduction was expanded to explain the clinical implications of inconsistent reporting standards, and how it impacts on patient outcomes and treatment efficacy. Also expanded to include why the JWG is significantand  the premise was clearly defined that there is unstandardised reporting and the JWG standardises the process.

The results and discussion were expanded to reflect the premise and to include the compliance with JWG guidance in 'Western' papers.

Limitations were grouped under a separate section within the discussion chapter.

Discussion was also expanded to explain why there might be variation in JWG compliance.

See the authors' detailed response to the review by Nitin Mukerji
See the authors' detailed response to the review by Johan Wikström and Maria Correia de Verdier
See the authors' detailed response to the review by Mustafa Ismail

Introduction

Cerebral arteriovenous malformations (cAVMs) cause death and disability mostly in the young.1 A cAVM anatomically consists of a nidus, that shunts blood directly from the arterial feeders to the draining veins, in the absence of capillaries.2–4 It is best described radiologically using digital subtraction angiography (DSA), with the pathognomonic features being a nidus and early venous drainage.5 The angioarchitecture of a cAVM refers to the vascular elements of a cAVM that are demonstrated on angiogram. It encompasses feeding arteries, nidus, draining veins, vascular changes resulting from high blood flow, and any accompanying abnormal vascular appearances.5

The commonest presenting feature is haemorrhage (occurring in 38-71% of cAVMs), and this contributes the most to cAVM morbidity and mortality.4 The annual rate of cAVM rupture, and consequent intracerebral haematoma (ICH), is 2-4% with the highest risk within the first five years of diagnosis.5 There are multiple ICH risk factors, including young age, prior cAVM rupture, deep and infratentorial location, large cAVM size, and deep venous drainage.4,6 Mortality rates are linked to haemorrhage from ruptured cAVMs in a high proportion of cases (10-40%).5,6

Seizures are the second most common presentation (17-30% of cAVMs) with risk factors including absence of aneurysms, temporal, frontal or cortical locations, varices, middle cerebral artery and cortical feeders, previous cAVM haemorrhage, and male gender.4,7–9

Focal neurological deficits (occurring in 5-15%) may be explained by a vascular steal phenomenon, where high shunting through the cAVM causes a reduced vascular supply in the surrounding parenchyma.4,5 It could also be due to mass effect on vulnerable white matter pathways from compressive venous dilatation.5 Risk factors for focal neurological deficits include older age, female gender, deep location, and ectasia.10

The fact that cAVM treatment is associated with significant morbidity and mortality poses additional challenges. Treatment is currently aimed at shrinking or excising the lesion, usually after it has ruptured or caused symptoms. Management decisions require a case-by-case multidisciplinary discussion balancing risks and benefits: there is no definitive algorithm for management. This is because there is little understanding of the pathophysiology underpinning cAVMs, but also there is a lack of consistency in reporting. This inconsistency poses a significant challenge to the progress of cAVM treatment.

Typically, DSA is used to classify cAVMs. cAVM presentation is believed to rely on its angioarchitecture. The latter may also be used to guide treatment. Since cAVMs have a complex morphology with each malformation being unique, reliably classifying cAVMs is challenging for clinicians managing them.

cAVMs are graded using several methods, including Spetzler-Martin (most widely used), Spetzler-Ponce, Lawton-Young or Flickinger-Pollock. They either classify using anatomical grades, or based on the likelihood of success and treatment risks. Though these grading systems incorporate certain essential information required to aid in management decisions, none of them are very detailed or sufficiently extensive. Particularly, in those cases where the grading score does not provide a definitive answer regarding best management, further detail is important. An in-depth description of cAVM angioarchitecture is also vital for cAVM clinical research, which will contribute to improved patient treatment. Furthermore, although reliability studies have shown good intra-observer agreement on the characterisation of cAVM angioarchitecture, inter-observer agreement was poor.11

In an attempt to address this, a consensus document was published by the Joint Working Group (JWG) of the Technology Assessment Committee: this provides elementary and clear definitions of terms and recommends which clinical and radiological cAVM features should be described and recorded (Table 1).12 The JWG has been very comprehensive in compiling its list of angioarchitecture definitions. This group, consisting of neuroradiologists, neurosurgeons, stroke and interventional neurologists practising in the United States of America, was created to produce guidelines for cAVM research.12 The work done by the JWG has been very significant in establishing a uniform framework for reporting. Complying with their guidance improves clarity and comparability when reporting cAVMs, and when publishing research results.

Standardising the terminology used would not only facilitate clinical trials, but also day-to-day patient management. A detailed understanding of, for instance, venous drainage would facilitate decision-making by better being able to quantify the risks and benefits of operative vs endovascular vs stereotactic radiosurgery management.

Aims

The aim of this study was to systematically review the cAVM angioarchitecture literature to describe whether and how the JWG criteria were used.

Methods

The review protocol was sent for registration to PROSPERO but not accepted due to “a perceived lack of direct impact on patient outcomes”. Reporting was in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement and checklist.13

Eligibility criteria

Peer-reviewed publications were searched from 1 Jan 2001 (when JWG standards were published) and limited to human subjects and the English language. There was no restriction on age or sex. Studies were excluded if they were reviews and/or exclusively discussed cavernous malformations, dural arteriovenous fistula, angioma, capillary telangiectasia, Vein of Galen Malformations or other angiographically occult vascular malformations.

Information sources

A database search was performed using EMBASE and Medline, on 15/07/19 by one reviewing author (SD). It was repeated on 10/9/20 to update the search by a second author (MW). There was independent assessment by a librarian and another reviewing author (HP). In addition to the electronic searches, we conducted citation tracking, checked the reference lists, and reviewed the list of similar articles.

Search strategy

To conduct searches of the Medline electronic bibliographic database, combinations of the following search terms were used.

Medical Subheadings: (Arteriovenous Malformations OR Arteriovenous Malformations, Intracranial) AND (Brain OR Intracranial)) AND (angioarchitecture OR angiogram OR angiographic OR aneurysm OR venous OR ectasia OR nidus OR angiogenesis OR varix).

Text Words: (Arteriovenous Malformations OR Arteriovenous Malformations, Intracranial) AND (Brain OR Intracranial)) AND (angioarchitecture OR angiogram OR angiographic OR aneurysm OR venous OR ectasia OR nidus).

Study selection

Studies were selected if they included any of the search strategy’s features: titles and abstracts were reviewed. Figure 1 demonstrates how articles were excluded.

Data collection process

Data extraction was performed by two independent reviewers (SD and HP) using the studies’ full text versions and by reviewing inclusion and exclusion criteria. Any disagreements were discussed between the two reviewers and an agreement reached. Pre-designed and piloted proforma were used.

Data items

All the individual data items collected from each paper are listed in Table 1.

Table 1. The cAVM angioarchitecture fields suggested by the JWG.12

Definition/categorisation (if present)
Proposed fields

  • • Location

  • • n/a

  • • Size

  • • recorded from MRI and angiography, measured in 3 dimensions (including cAVM’s largest diameter), volume calculated with ABC/2 formula

  • • Eloquence

  • • as per SMG score

  • • Border

  • • islands of normal cerebral parenchyma within cAVM nidus vs clearly outlined border with neighbouring parenchyma

Venous drainage

  • • superficial vs deep

  • • Superficial: all cAVM drainage through cortical venous system.

  • • Deep: if any/all drainage is through deep veins.

  • • periventricular

  • • drainage distinct from other deep venous drainage

  • • number of draining veins

  • • number of discrete venous channels leaving the nidus

  • • number of veins reaching sinus

  • • number of draining veins reaching any of these sinuses: superior sagittal, straight, transverse, sigmoid, cavernous, superior or inferior petrosal

  • • venous stenosis

  • • narrowing of any draining vein outflow pathway in two angiographic views

  • • venous ectasia

  • • more than double the calibre in any draining venous channel

  • • venous reflux

  • • flow reversal in any venous outflow pathway in a direction different than that to the nearest venous sinus

  • • sinus thrombosis

  • • dural venous sinus filling defect

Arterial supply

  • • feeding arteries

  • • arterial structure which displays a flow contribution to the AV shunt on DSA

  • • arterial aneurysms

  • • parent feeding vessel’s saccular dilatations

  • • Moyamoya-type changes

  • • pattern of angiographic changes indicating feeding artery occlusion

  • • Pial-to-pial collateralisation

  • • recruiting of side-by-side pial-to-pial collaterals not part of the nidus

  • • Intravascular pressure measurements

  • • n/a

Risk of bias in individual studies

Risk of bias was determined by two independent reviewers (SD and HP) using a version of a score devised to determine the methodological quality of case series and case reports,14 modified to expand its application to other study types. For each study, the quality assessment questions used were:

  • • Diagnosis: Are diagnostic criteria (as defined) for cAVM clearly identified and met?

  • • Is the method of cerebral angiography described, including the arterial injections, views taken, and what structures are included in a standard view?

  • • Is the method of calibration described?

  • • Are the cerebral angiograms reported on by two blinded neuroradiologist(s)?

  • • Were the patients reported collected over a short period of time in sufficient numbers?

  • • Is intra-rater reliability reported for each publication?

Summary measures

The principal summary measures were the number of studies following the JWG terminology and the angioarchitectural fields described.

Synthesis of results

This review aimed to assess if the description of cAVM angioarchitecture is standardised according to the JWG criteria and to explore if there are additional features that could be used to describe cAVMs and added to the JWG reporting standards. Additional features could be required to describe cAVMs as shown by some studies. Our objectives were to describe:

  • 1. which of the JWG reporting standards were used,

  • 2. adherence to definitions used in the JWG document,

  • 3. novel angiographic features not mentioned by the JWG, and

  • 4. the profession and experience of those reporting cAVMs.

We also compared the inter-observer agreement of different studies for the common criteria studied.

Risk of bias across studies

Publication and selective reporting biases were assessed.

Results

Study search

We identified 4306 publications (Figure 1) and 219 articles were selected for full-text review, reporting the angiogram findings potentially for 54, 148 individuals in total.

8d53fceb-c774-47a7-805b-7e1997eacb8a_figure1.gif

Figure 1. PRISMA flowchart demonstrates screening process for article selection.

Study designs

Most studies were retrospective (63%), with the remainder being prospective (27.9%), case reports (2.7%), studies that were both prospective and retrospective (2.7%), and educational (3.7%).

Publication trends

The studies spanned from 2001 to 2020 (the JWG report was published in 2001). The number of patients in each study ranged from 1 to 3923. The median was 120 (interquartile range: 30 to 278). The countries individually publishing the highest number of studies were China (15.5%) and the United States of America (15.1%). Studies from Western Europe, North America and Asia made up 26.5% of studies, with other countries (publishing fewer studies, i.e. one to four studies each) making up 69.9%.

Beijing Tiantan Hospital published more papers than any other centre, with data from this single centre contributing to 26 (74.3%) of the studies from China and 11.9% overall. Several studies used the same study populations, occasionally with a few more cases added due to an extension of study duration by a few years (Table 2). Out of Beijing Tiantan’s 26 studies, the commonest author groups were Lv et al and Tong et al (five studies for each author group) with the same sample population used three times for each of these two author groups (Table 2). The University of California (San Francisco) (18; 8.2%), University of Virginia (Charlottesville) (7; 3.2%), and Columbia University (New York) (6; 2.7%) were the most frequently publishing American institutions.

Table 2. Author groups with same or overlapping study populations, with the number of studies each, and the mean sample size for each group.

Author group with overlapping study populationsNumber of studies (%)Mean sample size
Beijing Tiantan Hospital
Lv, Wu, Jiang, Yang, Li, Sun, Zhang67,182,1843 (1.4)302
Ma, Kim, Chen, Wu, Ma, Su, Zhao65,662 (0.9)108
Tong, Wu, Lin, Cao, Zhao, Wang, Zhang, Zhao64,185, 773 (1.4)225
The First Affiliated Hospital of Guangzhou Medical University
Pan, Feng, Vinuela, He, Wu, Zhan69,1112 (0.9)152
University of California, San Francisco
Du, Dowd, Johnston, Young, Lawton99,1872 (0.9)304
John Hopkins University, Baltimore
Yang, Liu, Hung, Braileanu, Wang, Caplan, Colby, Coon, Huang76,902 (0.9)123
University of Virginia, Charlottesville
Ding, Starke, Quigg, Yen, Xu, Przybylowski, Dodson, Sheehan78,188–1904 (1.8)1400
University of Illinois, Urbana-Champaign
Shakur, Valyi-Nagy, Amin-Hanjani, Ya qoub, Aletich, Charbel, Alaraj71,72,152,1793 (1.4)80
Columbia University, New York
Stapf, Mohr, Pile-Spellman, Sciacca, Hartmann, Schumacher, Mast71,72,152,1794 (1.8)542
Hospital Lariboisiere, Paris
Choi, Mast, Hartmann, Marshall, Stapf177,1782 (0.9) same study population as Stapf et al735

Topics reported

Given the clinical importance of predicting haemorrhage, the aim of 65 papers (29.7%) was to test for associations between angioarchitecture and risk of bleeding (including location).1,15–78 Twelve studies tested for an association between angioarchitecture and risk of seizure.79–90

Standard imaging was compared against novel imaging techniques in four studies, and pre-operative imaging was investigated in two studies.91–96 Three studies assessed haemodynamics.37,97,98

Eleven papers studied various grading scores.91,99–108 The Spetzler-Martin Grade was the most commonly analysed, but others included the Spetzler-Ponce, Lawton-Young, and Pollock-Flickinger. Out of these 11 studies, seven assessed and proposed different grading systems.101–105,107,108

Four papers assessed the reliability of different cAVM grading scales, and two studies assessed the reliability in describing cAVM angioarchitecture.11,91,99,100,106,109 Agreement ranged from fair to excellent for both inter- and intra-rater comparisons.

Angioarchitectural characteristics were reported in association with treatments: embolisation,26,52,55,101,103,109–138 surgery,15,95,110,119,120,122,123,126,139–154 and stereotactic radiosurgery.53,83,97,60,113,119,122,123,126,129,140,145,155–161

In those studies that assessed inter-observer agreement, the commonest criteria investigated were size, SMG, venous drainage, and arterial feeders. The lowest scores were 0.62,91 0.46,91 0.56,92 and 0.695 respectively. The highest scores were 0.98,162 0.96,163 0.89,164 and 0.91164 respectively.

Quality of studies

Overall, the quality of the reporting studies was poor, with several of the study quality criteria not fulfilled (Table 3). Only 48 out of 219 studies (21.9%) used the definitions recommended by the JWG for some of the features reported (Table 3),16,19,20,23,24,26,28–30,33,35,38,47,49,55–57,61,64,66,67,71,72,75,77,90,152,156,159,165–181 with only 33 publications (15.1%) reporting and specifically mentioning using the JWG standards. Out of the ‘Western’ papers that provide a detailed angioarchitecture description, 21 publications (18.8%) used the JWG standards.

Table 3. Publications listed by authors in alphabetic order, associated with criteria assessing study quality.

The list excludes studies which do not describe angioarchitecture in detail e.g. only report location. White boxes indicate criteria fulfilled; dark grey boxes indicate criteria absent. a = JWG standard used; b = cAVM diagnostic criteria; c = DSA method: arterial injections; d = DSA method: views; e = Calibration method; f = Inter-rater reliability assessed; g = Statistics performed.

Study authorabcdefg
Abla 201474
Abecassis194
Al-Shahi11
Al-Tamimi195
Alen196
Alexander16
Anderson197
Benson88
Bharatha198
Blanc137
Braileanu199
Brunozzi 2017200
Brunozzi 2019166
Burkhardt176
Chang201
Chen202
Choi 2006177
Choi 2009178
Chowdhury168
Cuong93
D'Aliberti45
De Blasi203
de Castro-Afonso204
Guo46
Halim 200439
Halim 200247
Hernesniemi211
Hetts212
Hofmeister173
Huang32
Hung 201949
Iancu-Gontard109
Illies25
Imbesi213
Iryo214
Jayaraman 2012115
Jiang215
Jiao102
Jin24
Kakizawa216
Kandai19
Kellner17
Khaw29
Kim 200433
Kim 200750
Kim 201430
Kouznetsov217
Dinc 201942
Dinc 2018205
Ding 201736
Ding 201589
Dos Santos170
Du 2005206
Du 2016207
Ellis20
Fierstra87
Fleetwood208
Fok23
Frisoli106
Fukuda 2016209
Fukuda 2017171
Fullerton56
Galletti85
Garcin172
Gauvrit92
Geibprasert210
Griessenauer100
Kubalek63
Kurita218
Lee219
Liew220
Lin221
Liu 201582
Luo 2012183
Lv 2013182
Lv 2011a184
Lv 2011b67
Lv 2015222
Ma 2017a65
Ma 2017b66
Ma 201573
Majumdar57
Miyasaka40
Morgan 2016140
Motebejane223
Neidert104
Nishino224
Nisson 2020105
Niu22
Ognard91
Orning44
Oulasvirta225
Ozyurt162
Pan 201369
Patel226
Pawlikowska35
Pekmezci227
Reitz21
Riordan54
Robert 2014228
Robert 2017103
Robert 2015136
Sahlein61
Schmidt48
Schwartz229
Shakur 2016a41
Shakur 2016b98
Shakur 2018230
Shakur 2015231
Shankar79
Sheng232
Shotar108
Singh94
Stapf 2003179
Stapf 2002b180
Stapf 200672
Stefani 200168
Stefani 200270
Stein 2016b123
Stein 2015181
Sturiale58
Suzuki96
Tanaka144
Taschner164
Tasic59
Todaka27
Togao 2019233
Togao 2020163
Tong 2016a185
Tong 2016b64
Tong 2016c77
Tritt234
Tsuchiya95
Unlu235
Wrede236
Yamada1
Yang 2016b38
Yang 201743
Yang 2016a76
Yang 2015b90
Yang 2015a175
Ye237
Yi167
Yu31
Zwanzger238

Risk of bias within studies

Biases in the studies were because there was a small population size (less than 100 cases) in 100 studies, a second professional did not independently review angiograms in any of the studies, and there was often a re-analysis of datasets.

Number of studies reporting individual angioarchitectural features

The common angioarchitectural features are listed with the associated number of studies (Figure 2). Most studies described nidus size (175 studies; 78%), location (153; 68%), border (29; 12.9%), venous drainage (173; 76.9%), feeding arteries (88; 39.1%), and the presence of aneurysms (121; 53.8%). No studies described the angiographic features of pial to pial collaterals or Moya-Moya type changes as recommended by the JWG.

8d53fceb-c774-47a7-805b-7e1997eacb8a_figure2.gif

Figure 2. Key angiographic features listed in the Joint Writing Group’s recommendations, and the frequency with which they were reported on and defined in the studies identified.

Many studies used a variety of the recommended angiographic features, though not necessarily defining these features in the same way as the JWG (Table 4).

Table 4. Angiographic features recommended for reporting cAVMs by the JWG associated with the number of studies that record each feature.

They may have different definitions for these features compared to that stipulated by the JWG.

Angiographic feature described by the JWGNumber of studies (%)
AVM size175 (78)
AVM location153 (68)
Eloquence72 (32)
AVM border29 (12.9)
Venous drainage173 (76.9)
Number of draining veins71 (31.6)
Venous stenosis47 (20.9)
Venous ectasia42 (18.7)
Feeding artery88 (39.1)
Aneurysm121 (53.8)
Moyamoya-type changes0
Pial-to-pial collateralisation0
Intravascular pressure measurements0

Almost all the features described using the JWG guidelines were given different definitions, including, type of feeders, arterial feeders, and haemorrhagic presentation.

cAVM location was not described by the JWG, and this feature had the largest range of definitions. Some specified what constitutes deep, cortical, and/or infratentorial1,24,32,67,182,183 or dichotomised location into supratentorial and infratentorial.29,147,184,185 There were further categorisations into posterior fossa and periventricular by Ma et al.174

Venous ectasia was the feature with the second-most variations of definition. Whereas the JWG defines it as double the calibre change in any draining venous channel, others have described it as 1.5 times larger than the contralateral vessel,186 and two papers are broader in their definitions, describing venous ectasia as a markedly ectatic vein,107 or an abnormal dilatation.68,70

Aneurysms were defined as a saccular luminal dilatation of parent feeding vessels by the JWG. Most papers have essentially stated the aneurysm should be double the width of the artery, with only one definition stating the diameter is at least the same as that of the parent vessel.28

Numerous studies described angioarchitectural features which were not mentioned in the JWG report and these are described in Table 5. These features included perinidal angiogenesis, AVM nidus, deep location, and venous varix/pouch.

Table 5. The most commonly described additional angiographic features (with their associated definitions) that are not listed in the JWG standards.

Angiographic featureDefinitionNumber of studies
AVM nidus

  • • the vascular mass included in the AVM size measurement (Stapf 2003, Stapf 2006, Khaw)

  • • the junction between the feeding arteries and draining veins, without a capillary bed (Mohr)

4
Perinidal angiogenesis

  • • Vascular network within brain parenchyma between the nidus and feeding artery terminal segment, without visible arteriovenous shunts (Valavanis)

  • • Indirect supply to the AVM periphery from arterial branches other than the main arterial feeders (Shankar)

  • • The formation of a new network of arteriocapillaries in the white matter around an AVM in reaction to hypoxia. This is caused by the steal effect from a high flow nidus in the perinidal brain (Taeshineetanakul, Hu)

4
Deep location

  • • Includes basal ganglia, internal capsule, thalamus, and corpus callosum (Lin)

  • • The larger portion of the nidus is localised in deep white matter tracts, basal ganglia and thalamus, peri-ventricular regions, or posterior fossa (da Costa 2009)

  • • Includes the cerebellum, thalamus, basal ganglia, internal capsule, corpus callosum, and brainstem (Hu)

3
Venous varix/pouch/ectasia

  • • Markedly ectatic vein (Lv 2013, Luo)

  • • Focal dilatations at least twice as large as the vein diameter (Pan 2013)

  • • Focal aneurysmal dilation in the draining venous system (Daou)

  • • Proximal draining vein’s focal aneurysmal dilation (Chen 2017)

  • • Bleb that originates on the nidus venules with no defined relationship with a draining vein (D’Aliberti)

  • • Change of greater than 200% in the focal venous diameter of any drainage vein (Hu)

7

Professions conducting studies

The most common profession conducting these studies were neuroradiologists/neuro-interventionalists (101 studies) and neurosurgeons (60 studies). A neuropathologist was involved in one study.

Discussion

We have shown that only 33 studies of 219 (15.1%) included in our systematic review explicitly followed the JWG standards since their publication 20 years ago.12 Out of the ‘Western’ papers that describe angioarchitecture in detail, 21 publications (18.8%) used the JWG standards. Additionally, most studies reported venous drainage (76.9%), cAVM size (78%), and cAVM location (68%), suggesting these features are frequently considered as cAVM angioarchitecture. These parameters were the most widely used, likely due to their relation to the SMG system.

Since 219 publications were reviewed as providing data on angioarchitecture, it appears that this topic is considered important. Most commonly angioarchitectural features were used to test for associations with outcomes relevant to cAVM such as haemorrhage.

In those studies that assessed inter-observer agreement, the criteria most frequently used for comparison were size, SMG, venous drainage, and arterial feeders. It is possible that the other criteria were less used as they were more difficult to analyse on imaging.

Often, certain cAVM features are not reported as they are not present e.g. absence of venous stenosis. However, we argue that important negative findings should be mentioned in all cAVM reports. Adherence to the JWG guidelines will permit more comprehensive cAVM reporting, which will facilitate improved decision-making.

Twenty years have passed since the publication of the JWG definitions and, not unsurprisingly, several papers have reported on additional aspects of angioarchitecture which the JWG had not considered. These additional features may be helpful in understanding cAVMs and consideration should be given for their inclusion in any future update. These features are perinidal angiogenesis, deep location, venous and arterial dilatation. Angiogenesis is important for the formation and development of a cAVM and its presence may be useful in surgical planning.135 The precise location of a cAVM is crucial with well accepted definitions key for a shared understanding when discussing patient management. Venous dilatation is helpful to describe as it indicates if there may be high or low-pressure flow in the cAVM, with a larger vein reducing the pressure in a cAVM.45,69,161,174,182,183,206 This would be relevant to decide on the management approach. Equally, arterial dilatation29,86,160,186 may imply high-pressure flow in a cAVM, particularly if combined with a single vein of regular dimensions and may have clinical implications.

In this review, we also observed that pial-pial collaterals and Moya-moya changes were not recorded. This may reflect the difficulty in identifying these features, but also may suggest that they occur infrequently.

Including the JWG criteria in studies on cAVM angioarchitecture enhances the academic rigour and credibility of research publications. Few studies specifically mentioned adhering to the JWG guidelines, and in those that did not, no reasons were given for omitting them. A possible practical reason was the lack of technical equipment. Facilities will vary in different countries, including the type of biplane machine for angiograms. The widespread use of the JWG standards will have good implications for multi-centre studies and longitudinal research. It was not possible to include perspectives from various stakeholders like clinicians, researchers, and healthcare policymakers, as the few studies that made reference to the JWG, do not make any comments or provide any feedback regarding the JWG.

Limitations

Given that overall, the technical quality of publications was low, that most studies were retrospective and from small single centre series, the validity of results from these series could be questioned. Data reported from larger series also lacked the full consideration of angioarchitecture and often the same dataset was used for association studies again compromising the associations reported. In addition, as a large proportion of studies were published by single institutions, the results may not be generalisable to other cAVM populations. A similar problem was that a high proportion of publications were based on Chinese populations, particularly conducted by a specific hospital (Beijing Tiantan hospital), making results less generalisable. There was therefore potential publication bias. It may be too harsh to expect reporting by two independent neuroradiologists. There would certainly be variations in the access to technology across different health systems around the world, which would pose additional practical challenges to the universal application of the JWG standards.

Conclusion

The JWG publication did clarify that the definitions were parameters to be used in research studies.19 They have also discussed that there were no minimal criteria that should be used, emphasising that the angioarchitectural criteria were based on reasoned speculation. However, given that many of the criteria are likely to be interdependent, and studies are increasingly used to show associations with clinical presentation, this review would support the need to establish another working group to incorporate additional angiographic features and to include more specific and precise definitions for some of the features that were left open to interpretation. We would argue that these recommendations should then be widely publicised and uniformly incorporated into national and local reporting guidelines to help guide research and to ensure that clinicians can appropriately interpret this research with the understanding of the common language.

Registration and protocol

This review was not registered as described above. The review protocol can be accessed on BioStudies. The link is https://www.ebi.ac.uk/biostudies/studies/S-BSST1168. The accession number is S-BSST1168.

Data availability

BioStudies. Review of angioarchitecture literature SD. DOI: https://www.ebi.ac.uk/biostudies/studies/S-BSST1168BioStudies.

The raw data is in two files titled:

  • - ‘Review of angioarchitecture literature SD’ and

  • - ‘Review of angioarchitecture literature quality SD’.

The content is raw data from the papers used in the systematic review. The accession number is S-BSST1168.

Reporting guidelines

Biostudies. PRISMA checklist. DOI: https://www.ebi.ac.uk/biostudies/studies/S-BSST1168. The flow diagram is in Figure 1.

Acknowledgements

The authors would like to thank the Natalie Kate Moss Trust for their generous support. PK and AP-J are supported by the Stroke Association (TSA LECT 2017/02; SA L-RC 19\100000).

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Das S, Kasher P, Waqar M et al. Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review [version 2; peer review: 3 approved with reservations]. F1000Research 2024, 12:1252 (https://doi.org/10.12688/f1000research.139256.2)
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Reviewer Report 15 Nov 2024
Johan Wikström, Uppsala University, Uppsala, Sweden 
Maria Correia de Verdier, Department of Radiology, Uppsala University, Uppsala, Sweden 
Approved with Reservations
VIEWS 19
https://doi.org/10.5256/f1000research.169457.r335899
This article aims to assess the adherence to the Joint Writing Group guidelines regarding description of features in brain arteriovenous anomalies. The authors have responded to previous reviewers´ comments. I have a few additional remarks;

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Wikström J and Correia de Verdier M. Reviewer Report For: Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review [version 2; peer review: 3 approved with reservations]. F1000Research 2024, 12:1252 (https://doi.org/10.5256/f1000research.169457.r335899)
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https://f1000research.com/articles/12-1252/v2#referee-response-335899
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  • Author Response 25 Nov 2024
    Suparna Das, The University of Manchester, Manchester, UK
    25 Nov 2024
    Author Response
    Why use "cAVM" and not "BAVM" as proposed by the JWG guidelines?
    cAVM was the term used for my doctorate thesis, which this systematic review was part of.

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  • Author Response 25 Nov 2024
    Suparna Das, The University of Manchester, Manchester, UK
    25 Nov 2024
    Author Response
    Why use "cAVM" and not "BAVM" as proposed by the JWG guidelines?
    cAVM was the term used for my doctorate thesis, which this systematic review was part of.

    In ... Continue reading
    Report a concern
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Reviewer Report 08 May 2024
Mustafa Ismail, Univeristy of Baghdad, Baghdad, Iraq 
Approved with Reservations
VIEWS 40
https://doi.org/10.5256/f1000research.152519.r264835
The authors reported a systematic review about "Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review" and I congratulate them for this work. There are a few points to consider in this review:
... Continue reading
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Ismail M. Reviewer Report For: Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review [version 2; peer review: 3 approved with reservations]. F1000Research 2024, 12:1252 (https://doi.org/10.5256/f1000research.152519.r264835)
The direct URL for this report is:
https://f1000research.com/articles/12-1252/v1#referee-response-264835
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  • Author Response 07 Oct 2024
    Suparna Das, The University of Manchester, Manchester, UK
    07 Oct 2024
    Author Response
    We have addressed all the comments and we have modified mainly the introduction and discussion, but also some of the results.
    Competing Interests: No competing interests were disclosed.
    Report a concern
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  • Author Response 07 Oct 2024
    Suparna Das, The University of Manchester, Manchester, UK
    07 Oct 2024
    Author Response
    We have addressed all the comments and we have modified mainly the introduction and discussion, but also some of the results.
    Competing Interests: No competing interests were disclosed.
    Report a concern
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Reviewer Report 02 Nov 2023
Nitin Mukerji, Department of Neurosurgery, South Tees Hospitals NHS Foundation Trust, Middlesbrough, England, UK 
Approved with Reservations
VIEWS 42
https://doi.org/10.5256/f1000research.152519.r211337
The authors have picked out a standard method of reporting/describing AVMs in literature and attempted to establish compliance via a retrospective review. While the work done is commendable, well researched and drafted appropriately; there are a few criticisms:
    ... Continue reading
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    CITE
    HOW TO CITE THIS REPORT
    Mukerji N. Reviewer Report For: Reporting of angiographic studies in patients diagnosed with a cerebral arteriovenous malformation: a systematic review [version 2; peer review: 3 approved with reservations]. F1000Research 2024, 12:1252 (https://doi.org/10.5256/f1000research.152519.r211337)
    The direct URL for this report is:
    https://f1000research.com/articles/12-1252/v1#referee-response-211337
    NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
    Report a concern
    • Author Response 07 Oct 2024
      Suparna Das, The University of Manchester, Manchester, UK
      07 Oct 2024
      Author Response
      We have addressed all the comments and we have modified mainly the introduction and discussion, but also some of the results.
      Competing Interests: No competing interests were disclosed.
      Report a concern
    • Respond or Comment
    COMMENTS ON THIS REPORT
    • Author Response 07 Oct 2024
      Suparna Das, The University of Manchester, Manchester, UK
      07 Oct 2024
      Author Response
      We have addressed all the comments and we have modified mainly the introduction and discussion, but also some of the results.
      Competing Interests: No competing interests were disclosed.
      Report a concern

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    Version 3
    VERSION 3 PUBLISHED 29 Sep 2023
    Comment

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    Alongside their report, reviewers assign a status to the article:

    Approved
    The paper is scientifically sound in its current form and only minor, if any, improvements are suggested
    Approved with reservations
    A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
    Not approved
    Fundamental flaws in the paper seriously undermine the findings and conclusions

    Reviewer Reports

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    Version 3
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     25 Nov 24     		read read
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    (revision)
     07 Oct 24     		read
    Version 1
    29 Sep 23     		read read
    1. Nitin Mukerji, South Tees Hospitals NHS Foundation Trust, Middlesbrough, UK
    2. Mustafa Ismail, Univeristy of Baghdad, Baghdad, Iraq
    3. Johan Wikström, Uppsala University, Uppsala, Sweden
      Maria Correia de Verdier, Uppsala University, Uppsala, Sweden

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      Alongside their report, reviewers assign a status to the article:
      Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
      Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
      Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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