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Original Article
Carotid and vertebral injury study (CAVIS) technique for characterization of blunt traumatic aneurysms with reliability assessment
Interventional Neuroradiology 0(00) 1–8 ! The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1591019915582165 ine.sagepub.com
Christoph J Griessenauer, Paul Foreman, Mohammadali M Shoja, Kimberly P Kicielinski, John P Deveikis, Beverly C Walters and Mark R Harrigan
Abstract Traumatic aneurysms occur in up to 20% of blunt traumatic extracranial carotid artery injuries. Currently there is no standardized method for characterization of traumatic aneurysms. For the carotid and vertebral injury study (CAVIS), a prospective study of traumatic cerebrovascular injury, we established a method for aneurysm characterization and tested its reliability. Saccular aneurysm size was defined as the greatest linear distance between the expected location of the normal artery wall and the outer edge of the aneurysm lumen (‘‘depth’’). Fusiform aneurysm size was defined as the ‘‘depth’’ and longitudinal distance (‘‘length’’) paralleling the normal artery. The size of the aneurysm relative to the normal artery was also assessed. Reliability measurements were made using four raters who independently reviewed 15 computed tomographic angiograms (CTAs) and 13 digital subtraction angiograms (DSAs) demonstrating a traumatic aneurysm of the internal carotid artery. Raters categorized the aneurysms as either ‘‘saccular’’ or ‘‘fusiform’’ and made measurements. Five scans of each imaging modality were repeated to evaluate intra-rater reliability. Fleiss’s free-marginal multi-rater kappa (k), Cohen’s kappa (k), and interclass correlation coefficient (ICC) determined inter- and intra-rater reliability. Interrater agreement as to the aneurysm ‘‘shape’’ was almost perfect for CTA (k ¼ 0.82) and DSA (k ¼ 0.897). Agreements on aneurysm ‘‘depth,’’ ‘‘length,’’ ‘‘aneurysm plus parent artery,’’ and ‘‘parent artery’’ for CTA and DSA were excellent (ICC > 0.75). Intra-rater agreement as to aneurysm ‘‘shape’’ was substantial to almost perfect (k > 0.60). The CAVIS method of traumatic aneurysm characterization has remarkable inter- and intra-rater reliability and will facilitate further studies of the natural history and management of extracranial cerebrovascular traumatic aneurysms.
Keywords Carotid artery, blunt trauma, dissecting aneurysm, traumatic aneurysm, pseudoaneurysm, traumatic cerebrovascular injury
Introduction Traumatic aneurysms of the extracranial carotid and vertebral artery occur in approximately 15–20% cases of blunt traumatic cerebrovascular injury (TCVI) and have been associated with embolic ischemic stroke.1,2 The risk of a thromboembolic event associated with such traumatic aneurysms, however, is unknown and management of traumatic aneurysms associated with TCVI is controversial, ranging widely from expectant management with antithrombotic therapy to endovascular repair.3,4 Despite the absence of controlled trials and guidelines about the use of endovascular techniques for the treatment of traumatic aneurysms, endovascular treatment appears to be becoming increasingly common.4–11 In recent years, there has been an epidemic of aggressive endovascular treatment of traumatic aneurysms despite a lack of clinical data about the natural history and optimal management of these lesions.
An accurate, reproducible quantitative measurement technique for traumatic aneurysms is necessary to permit further studies to better define the natural history of these lesions and clarify the role, if any, of endovascular treatment. The carotid and vertebral injury study (CAVIS) found that anatomic features of traumatic aneurysms are important determinants of the risk of a thromboembolic event from an aneurysm;3,12 the size of the aneurysm at presentation and the likelihood of the
Division of Neurosurgery, Department of Surgery, University of Alabama at Birmingham, USA Corresponding author: Christoph Griessenauer, Division of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL 35294, USA. Email: [email protected]
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2 aneurysm to enlarge over time and are thus important indicators for treatment.12 However, there is no consensus on how to characterize traumatic aneurysms associated with TCVI, nor any reliable measurement scale or system for use in scientific studies. In this study we developed a simple, clinically applicable measurement tool to be used for CAVIS to characterize traumatic aneurysms, and assessed its reliability.
Methods Aneurysm classification and measurement technique A traumatic aneurysm was defined as a focal dilatation in the wall of the artery with a contained region of contrast material extending beyond the normal border of the artery wall following blunt trauma. The term traumatic aneurysm was used rather than the popular term pseudoaneurysm because the term pseudoaneurysm is used to describe aneurysms in which a complete disruption of the artery wall has occurred; in most aneurysms due to blunt trauma, the aneurysm is likely due to a partial disruption of the artery wall instead of complete disruption.12,13 A saccular aneurysm is a sac-like lesion in which the height of the aneurysm (i.e. the greatest distance between the normal lumen of the parent artery and the aneurysm dome) exceeds the size of the aneurysm neck (i.e. the length of the involved segment of the parent artery). Saccular aneurysm size was defined as the greatest linear distance between the expected location of the normal artery wall and the outer edge of the aneurysm lumen (‘‘depth’’). When measurements can be made in more than one plane of imaging (axial, sagittal, or coronal), the largest measurement is selected. In the sagittal and coronal plane, the measurement is made extending from a point in the middle of the aneurysm neck along the expected normal edge of the parent artery to the point on the aneurysm dome that is furthest away (Figure 1(a) to (d)). A fusiform aneurysm is a broad-based spindle-shaped or plateau-shaped aneurysm in which the height of the aneurysm is less than the size of the aneurysm neck. Fusiform aneurysms may involve the entire circumference of the artery wall or only one side of the artery wall, depending upon the nature of the trauma. Fusiform aneurysm size was defined as the ‘‘depth’’ (Figure 2(a) to (d)), in addition to the longitudinal distance (‘‘length’’) paralleling the normal artery (Figure 3). In addition, for both saccular and fusiform aneurysms, the size of the aneurysm (‘‘aneurysm plus parent artery’’) in relationship to the normal artery (‘‘parent artery’’) was also assessed (Figure 4).
Observer reliability assessment Four raters, including one vascular neurosurgeon, one neuroradiologist, and two senior neurosurgical residents independently reviewed 15 computed
Interventional Neuroradiology 0(00) tomographic angiograms (CTAs) and 13 digital subtraction angiograms (DSAs) demonstrating a traumatic aneurysm of the internal carotid artery (ICA). The images used for the study were selected from a database including patients with an aneurysm of the ICA from blunt trauma. The CTAs and DSAs did not come from the same patients. CTAs included axial, coronal, and sagittal images at a slice thickness of 6, 3, and 3 mm, respectively. DSAs included anteroposterior and lateral views of global internal carotid and vertebral injections. Five scans of each imaging modality were repeated for intra-rater reliability assessment, for a total of 38 sets of images. Scans that were repeated were randomly inserted into the dataset. Sample size was calculated using a method developed by Walter et al.,14 which showed that increasing the number of raters per subject will decrease the total number of observations required to achieve adequate sample size, a number determined to be sufficient for statistical analysis. Fleiss’s free-marginal multi-rater kappa (k) for nominal variables (‘‘shape’’) and intraclass correlation coefficient (ICC) for continuous variables (‘‘depth,’’ ‘‘length,’’ ‘‘aneurysm plus parent artery,’’ and ‘‘parent artery’’) were calculated as a measure of overall agreement (Figures 1 to 4) on aneurysm characteristics between the four raters.15,16 For intra-rater reliability analysis, Cohen’s kappa (k) and ICC were used to assess repeat measurement agreement for each rater. Agreement measured by kappa (k) was interpreted as almost perfect with k values between 0.81 and 1.00, substantial with k values between 0.61 and 0.80, moderate with k values between 0.41 and 0.60, fair with k values between 0.21 and 0.40, and poor with k values between 0 and 0.20.16 ICC greater than 0.75 was considered to have excellent inter- and intra-rater reliability, with an ICC between 0.40 and 0.75 classified as fair to good, and less than 0.40 considered poor reliability.17 The ICC was estimated using a two-way mixed effect model and an absolute agreement to assess the inter-rater concordance concerning the quantitative measurements. All statistical analysis was performed using IBM SPSS Statistics version 21.0 (SPSS, Inc., Chicago, IL) with the exception of Fleiss’s free-marginal kappa for multiple raters, which was calculated using an online program.15 This study was approved by the Institutional Review Board.
Results Inter-rater reliability CTA (n ¼ 15). Exact agreement as to the ‘‘shape’’ of the traumatic aneurysm, saccular versus fusiform, was obtained in 13 out of 15 cases (87%). Fleiss’s free-marginal multi-rater kappa (k) was 0.82, indicating an almost perfect agreement as to the ‘‘shape’’ of traumatic aneurysm between the four raters. The ICC was 0.977 (95% confidence interval (CI), 0.945–0.992) for ‘‘depth,’’ 0.974 (95% CI, 0.939–0.990) for ‘‘length,’’
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Figure 1. Saccular traumatic aneurysm. A sac-like aneurysm, with an appreciable neck, in which the height of the aneurysm (i.e. the greatest distance between the normal lumen of the parent artery and the aneurysm dome) exceeds the size of the aneurysm neck (i.e. the length of the involved segment of the parent artery). (a, b) Schematic drawing of saccular aneurysms (arrows indicate aneurysm ‘‘depth’’). (c) DSA of a left ICA saccular aneurysm with ‘‘depth’’ measurement (lateral view). (d) CTA of a left ICA saccular aneurysm with ‘‘depth’’ measurement (sagittal plane).
0.986 (95% CI, 0.970–0.995) for ‘‘aneurysm plus parent artery,’’ and 0.839 (95% CI, 0.580–0.943) for ‘‘parent artery.’’ These results implied an excellent inter-rater agreement between the four raters as to the quantitative measurements using CTA. DSA (n ¼ 13). The exact agreement between the raters as to the ‘‘shape’’ of the traumatic aneurysm, saccular versus fusiform, was obtained in 12 out of 13 cases (92%). Fleiss’s free-marginal multi-rater kappa (k) was 0.897, indicating an almost perfect agreement as to the ‘‘shape’’ between the four raters. The ICC was 0.990 (95% CI, 0.975–0.997) for ‘‘depth,’’ 0.985 (95% CI, 0.965–0.995) for ‘‘length,’’ 0.991 (95% CI, 0.979– 0.997) for ‘‘aneurysm plus parent artery,’’ and 0.860 (95% CI, 0.680–0.952) for ‘‘parent artery.’’ These results indicate excellent inter-rater agreement between
the four raters as to the quantitative measurements using DSA.
Intra-rater reliability CTA (n ¼ 5). Intra-rater reliability as to the ‘‘shape’’ was almost perfect (k > 0.80) in 3 out of 4 raters and substantial (k > 0.60) in one rater, the neuroradiologist. ICCs for ‘‘depth,’’ ‘‘length,’’ ‘‘aneurysm plus parent artery,’’ and ‘‘parent artery’’ were excellent (ICC > 0.75) in all raters (Table 1). DSA (n ¼ 5). Intra-rater observer reliability as to the ‘‘shape’’ was almost perfect (k > 0.80) in all raters. ICCs for ‘‘depth’’ and ‘‘length’’ were excellent (ICC > 0.75) in all raters while ICC for ‘‘aneurysm plus parent artery’’ was excellent (ICC > 0.75) for the
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Figure 2. Fusiform traumatic aneurysm. A broad-based spindle-shaped or plateau-shaped aneurysm in which the height of the aneurysm is less than the size of the aneurysm neck. Fusiform aneurysms may involve only one side of the parent artery wall or the entire circumference of the parent artery. (a, b) Schematic drawing of fusiform aneurysms (arrows indicate aneurysm ‘‘depth’’). (c) DSA of a right ICA fusiform aneurysm with ‘‘depth’’ measurement (lateral view). (d) CTA of a left ICA fusiform traumatic aneurysm with ‘‘depth’’ measurement (sagittal plane).
vascular neurosurgeon and neuroradiologist, and fair to good (ICC > 0.40) for the residents. ICCs for ‘‘parent artery’’ were excellent (ICC > 0.75) in one of the residents and fair to good (ICC > 0.40) in the other three raters (Table 2).
Discussion The CAVIS identified 13 trauma patients with TCVI harboring 26 traumatic aneurysms and showed that the character of traumatic aneurysms is an important determinant for a number of risk factors associated with traumatic aneurysms.3,12 These potential risks include thromboembolism,1,2 hemorrhage,18 and mass effect on adjacent structures, particularly with gradual enlargement of the aneurysm over time. Since the natural history of traumatic aneurysms is poorly understood, the point at which those factors pose a large
enough risk to justify therapeutic intervention is controversial, particularly for endovascular repair, a treatment modality that has become popular in recent years.4–11 As there currently is a need for a reliable measure of these factors in traumatic aneurysms and no consensus on how to characterize them, we developed simple, clinically applicable criteria that we used in CAVIS to characterize traumatic aneurysms and assessed their reliability.
Aneurysm shape Unlike intracranial aneurysms, which frequently have a saccular configuration, traumatic aneurysms present with a variety of different shapes. Most traumatic aneurysms have either a saccular or a fusiform shape. The agreement regarding the shape of the traumatic aneurysm, saccular versus fusiform, was almost perfect
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Figure 3. Fusiform aneurysm ‘‘length.’’ The greatest superoinferior extent of the aneurysm measured in parallel to the parent artery in the coronal or sagittal plane. (a, b) Schematic drawings of aneurysm ‘‘length’’ in fusiform aneurysms. (c) DSA of a left ICA fusiform aneurysm with ‘‘length’’ measurement (lateral view). (d) CTA of a right ICA fusiform aneurysm with ‘‘length’’ measurement (coronal plane).
between the four raters with DSA resulting in slightly superior results compared to CTA. Of the 26 traumatic aneurysms identified in CAVIS, 9 were saccular (34.6%) and 17 fusiform (65.4%).12 Saccular traumatic aneurysms may carry a greater risk of thromboembolic events because there is a potential for blood stasis and thrombosis within the aneurysm as well as exposure of subendothelial elements to circulating platelets and clotting factors from tears in the arterial wall. Fusiform traumatic aneurysms, in contrast, may result from stretching of the artery wall, rather than tearing, and carry a lower risk of thromboembolism. Two of the saccular aneurysms in
CAVIS were found in patients who had suffered an ischemic stroke and a third patient with ischemic stroke attributable to TCVI developed a saccular aneurysm after the stroke. None of the fusiform aneurysms were associated with ischemic stroke.12
Aneurysm depth Aneurysm depth is defined as the greatest linear distance between the expected location of the normal parent artery wall and the outer edge of the aneurysm lumen and represents the most frequently reported quantitative measurement for characterizing
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Figure 4. Aneurysm to parent artery ratio. Aneurysm and normal-appearing adjacent parent artery: this measurement is applicable only when the axis of the parent artery appears to be perpendicular to the plane of imaging and when there is a normal-appearing adjacent parent artery. The greatest transverse dimension of the aneurysm including the parent artery (a) in the axial plane (x) and the transverse dimension of the normal parent artery (b) above or below the aneurysm are measured (y). The aneurysm measurement ¼ x y. For spindle-shaped fusiform aneurysms, the measurement extends from the mid-point of the neck to the furthest part of the aneurysm dome on both sides, and the measurements are totaled. For plateau-shaped fusiform aneurysms, the measurement extends from the mid-point of the neck to the furthest part of the aneurysm. As conventional DSA consists of anteroposterior and lateral views only, the technique was modified. The DSA image that shows the greatest dimension of the aneurysm is selected and the greatest distance from the dome of the aneurysm to the opposite parent artery wall (x) is measured. The normal parent artery diameter is measure either proximal or distal to the aneurysm artery (y). The aneurysm measurement ¼ x y. (c) CTA of right ICA saccular aneurysm with ‘‘aneurysm plus parent artery’’ measurement (axial plane). (d) CTA of right ICA saccular aneurysm (same as in panel C) with ‘‘parent artery2 measurement (axial plane). (e) DSA of left ICA saccular ‘‘aneurysm plus parent artery’’ measurement (lateral view). (f) DSA of left ICA saccular aneurysm (same as in panel E) with ‘‘parent artery’’ measurement (lateral view).
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Table 1. Intra-rater reliability for CTAs.
Vascular neurosurgeon Neuroradiologist Neurosurgery resident 1 Neurosurgery resident 2
Cohen’s k for ‘‘shape’’
ICC for ‘‘depth’’ (95% CI)
ICC for ‘‘length’’ (95% CI)
ICC for ‘‘aneurysm plus parent artery’’ (95% CI)
ICC for ‘‘parent artery’’ (95% CI)
1.00 0.67 1.00 1.00
0.98 0.99 0.99 0.98
0.99 0.99 0.99 0.99
0.99 0.96 0.98 0.99
0.95 0.96 0.93 0.83
(0.87–0.99) (0.95–0.99) (0.93–0.99) (0.89–0.99)
(0.98–1.00) (0.96–1.00) (0.94–0.99) (0.95–0.99)
(0.99–1.00) (0.65–0.99) (0.80–0.99) (0.94–0.99)
(0.56–0.99) (0.66–0.99) (0.33–0.99) (0.17–0.98)
ICC: intraclass correlation coefficient.
Table 2. Intra-rater reliability for DSAs.
Vascular neurosurgeon Neuroradiologist Neurosurgery resident 1 Neurosurgery resident 2
Cohen’s k for ‘‘shape’’
ICC for ‘‘depth’’ (95% CI)
ICC for ‘‘length’’ (95% CI)
ICC for ‘‘aneurysm plus parent artery’’ (95% CI)
ICC for ‘‘parent artery’’ (95% CI)
1.00 1.00 1.00 1.00
0.90 0.96 0.97 0.90
0.81 0.77 0.78 0.99
0.96 0.77 0.61 0.60
0.60 0.63 0.85 0.60
(0.30–0.98) (0.73–0.99) (0.76–0.99) (0.32–0.99)
(0.39–0.98) (0.78–0.97) (0.97–0.97) (0.93–0.99)
(0.75–0.99) (3.00–0.97) (8.20–0.96) (0.54–0.95)
(0.77–0.95) (0.81–0.99) (0.20–0.98) (3.58–0.96)
ICC: intraclass correlation coefficient
aneurysms. Previous studies on measurements of the maximum diameter of intracranial aneurysm have found excellent reliability.19,20 Using a similar approach for traumatic aneurysms there was excellent agreement on aneurysm ‘‘depth’’ between the four raters yielding comparable results using DSA and CTA. ‘‘Depth’’ may be the most clinically relevant measurement for traumatic aneurysms. The average ‘‘depth’’ in CAVIS at initial diagnosis by either CTA or DSA was 6.8 mm (range 2–14 mm) for the 9 saccular aneurysms and 2.1 mm (range 1–3 mm) for the 17 fusiform aneurysms. Thus, compared to fusiform aneurysms, saccular aneurysms tend to have a greater ‘‘depth’’ upon presentation, resulting in a larger arterial radius and greater wall tension according to Laplace’s law which over time results in a greater increase in the ‘‘depth’’ of saccular aneurysms compared to fusiform aneurysms. A greater tendency of saccular aneurysms to enlarge may also reflect greater damage to the arterial wall in comparison with fusiform aneurysms, which may occur due to stretching rather than tearing of the arterial wall.12 Final follow-up imaging of the 9 saccular aneurysms in CAVIS showed that 1 (11.1%) was not visible, 4 (44.4%) were smaller, 1 (11.1%) was stable, and 3 (33%) aneurysms were larger. Final follow-up imaging of the 17 fusiform aneurysms revealed that 9 (52.9%) were not visible, 6 (35.3%) were smaller, and 2 (11.8%) were larger. Thus, saccular aneurysms were more likely to enlarge and were less likely to resolve or not visualize when compared with fusiform aneurysms. Statistically there was a trend toward behavioral differences between saccular and fusiform aneurysms as evidenced by the Fisher exact test (p ¼ 0.07). Saccular aneurysms tend to enlarge (odds ratio (OR) 3.75 (95% CI 0.49–28.4), p ¼ 0.3) over time. This difference decreased when adjusting for
aneurysm ‘‘depth’’ at diagnosis (OR 1.08 (95% CI 0.05–21.5), p ¼ 0.3); thus, while saccular aneurysms are more likely to enlarge on follow-up imaging, they are also more likely to be larger on presentation.12 Moreover, where may be an initial ‘‘depth’’ threshold above with aneurysms are more likely to grow as evidenced by the fact that 2 of 3 saccular aneurysms with an initial size larger than 6 mm were enlarged on final follow-up imaging, whereas only 1 of 6 saccular aneurysms that were 6 mm or smaller were enlarged.12 The ‘‘depth’’ measurement also has implications for the endovascular repair. Two (7.7%) of 26 traumatic aneurysms, both saccular, were treated with placement of a covered stent due to evidence of significant aneurysm growth on final follow-up imaging.12
Aneurysm length Aneurysm ‘‘length’’ was defined as the greatest extent of the aneurysm measured in parallel to the parent artery in the coronal or sagittal plane. While the perception of aneurysm length and depth may be almost identical in saccular aneurysms of whatever etiology, fusiform aneurysms with shallow depth may have a significant length as they involve and extend along the parent artery. There was excellent agreement on length between the four raters using this simple tool. In CAVIS traumatic aneurysm ‘‘length’’ was not found to be clinically significant.12
Aneurysm-to-parent-artery ratio Recent studies on intracranial aneurysms have indicated that the size ratio, i.e. the maximum diameter of the aneurysm related to the diameter of the adjacent parent artery, may predict risk of rupture, particularly in small aneurysms.21–23 A similar measurement
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8 technique employed in the present study resulted in excellent agreement on aneurysm-plus-parent-artery and parent artery measurements. The relevance of aneurysm-to-parent-artery ratio for traumatic aneurysms remains to be determined as this ratio was not found to be clinically significant in CAVIS.12
Intra-rater reliability Intra-rater reliability on aneurysm shape was almost perfect for both CTA and DSA in all raters except for the neuroradiologist who had achieved substantial agreement for CTA. Intra-rater reliability on measurements for CTA and DSA were comparable; there was no substantial difference between the rating of the vascular neurosurgeon, the neuroradiologist, and the senior residents.
Conclusions This CAVIS method of extracranial traumatic aneurysm characterization has remarkable inter- and intrarater reliability. Currently there is no standardized method for characterization of such traumatic aneurysms. The novelty of this study lies in the development of a simple, clinically relevant method to define this disease entity and introduce a common terminology that may facilitate further studies on the natural history and management of extracranial traumatic aneurysms.12 Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Conflict of interest None declared.
Acknowledgments We would like to acknowledge Kevin L Junck, PhD, Department of Radiology, University of Alabama at Birmingham for this assistance with this project.
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Original Article
Carotid and vertebral injury study (CAVIS) technique for characterization of blunt traumatic aneurysms with reliability assessment
Interventional Neuroradiology 0(00) 1–8 ! The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1591019915582165 ine.sagepub.com
Christoph J Griessenauer, Paul Foreman, Mohammadali M Shoja, Kimberly P Kicielinski, John P Deveikis, Beverly C Walters and Mark R Harrigan
Abstract Traumatic aneurysms occur in up to 20% of blunt traumatic extracranial carotid artery injuries. Currently there is no standardized method for characterization of traumatic aneurysms. For the carotid and vertebral injury study (CAVIS), a prospective study of traumatic cerebrovascular injury, we established a method for aneurysm characterization and tested its reliability. Saccular aneurysm size was defined as the greatest linear distance between the expected location of the normal artery wall and the outer edge of the aneurysm lumen (‘‘depth’’). Fusiform aneurysm size was defined as the ‘‘depth’’ and longitudinal distance (‘‘length’’) paralleling the normal artery. The size of the aneurysm relative to the normal artery was also assessed. Reliability measurements were made using four raters who independently reviewed 15 computed tomographic angiograms (CTAs) and 13 digital subtraction angiograms (DSAs) demonstrating a traumatic aneurysm of the internal carotid artery. Raters categorized the aneurysms as either ‘‘saccular’’ or ‘‘fusiform’’ and made measurements. Five scans of each imaging modality were repeated to evaluate intra-rater reliability. Fleiss’s free-marginal multi-rater kappa (k), Cohen’s kappa (k), and interclass correlation coefficient (ICC) determined inter- and intra-rater reliability. Interrater agreement as to the aneurysm ‘‘shape’’ was almost perfect for CTA (k ¼ 0.82) and DSA (k ¼ 0.897). Agreements on aneurysm ‘‘depth,’’ ‘‘length,’’ ‘‘aneurysm plus parent artery,’’ and ‘‘parent artery’’ for CTA and DSA were excellent (ICC > 0.75). Intra-rater agreement as to aneurysm ‘‘shape’’ was substantial to almost perfect (k > 0.60). The CAVIS method of traumatic aneurysm characterization has remarkable inter- and intra-rater reliability and will facilitate further studies of the natural history and management of extracranial cerebrovascular traumatic aneurysms.
Keywords Carotid artery, blunt trauma, dissecting aneurysm, traumatic aneurysm, pseudoaneurysm, traumatic cerebrovascular injury
Introduction Traumatic aneurysms of the extracranial carotid and vertebral artery occur in approximately 15–20% cases of blunt traumatic cerebrovascular injury (TCVI) and have been associated with embolic ischemic stroke.1,2 The risk of a thromboembolic event associated with such traumatic aneurysms, however, is unknown and management of traumatic aneurysms associated with TCVI is controversial, ranging widely from expectant management with antithrombotic therapy to endovascular repair.3,4 Despite the absence of controlled trials and guidelines about the use of endovascular techniques for the treatment of traumatic aneurysms, endovascular treatment appears to be becoming increasingly common.4–11 In recent years, there has been an epidemic of aggressive endovascular treatment of traumatic aneurysms despite a lack of clinical data about the natural history and optimal management of these lesions.
An accurate, reproducible quantitative measurement technique for traumatic aneurysms is necessary to permit further studies to better define the natural history of these lesions and clarify the role, if any, of endovascular treatment. The carotid and vertebral injury study (CAVIS) found that anatomic features of traumatic aneurysms are important determinants of the risk of a thromboembolic event from an aneurysm;3,12 the size of the aneurysm at presentation and the likelihood of the
Division of Neurosurgery, Department of Surgery, University of Alabama at Birmingham, USA Corresponding author: Christoph Griessenauer, Division of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL 35294, USA. Email: [email protected]
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2 aneurysm to enlarge over time and are thus important indicators for treatment.12 However, there is no consensus on how to characterize traumatic aneurysms associated with TCVI, nor any reliable measurement scale or system for use in scientific studies. In this study we developed a simple, clinically applicable measurement tool to be used for CAVIS to characterize traumatic aneurysms, and assessed its reliability.
Methods Aneurysm classification and measurement technique A traumatic aneurysm was defined as a focal dilatation in the wall of the artery with a contained region of contrast material extending beyond the normal border of the artery wall following blunt trauma. The term traumatic aneurysm was used rather than the popular term pseudoaneurysm because the term pseudoaneurysm is used to describe aneurysms in which a complete disruption of the artery wall has occurred; in most aneurysms due to blunt trauma, the aneurysm is likely due to a partial disruption of the artery wall instead of complete disruption.12,13 A saccular aneurysm is a sac-like lesion in which the height of the aneurysm (i.e. the greatest distance between the normal lumen of the parent artery and the aneurysm dome) exceeds the size of the aneurysm neck (i.e. the length of the involved segment of the parent artery). Saccular aneurysm size was defined as the greatest linear distance between the expected location of the normal artery wall and the outer edge of the aneurysm lumen (‘‘depth’’). When measurements can be made in more than one plane of imaging (axial, sagittal, or coronal), the largest measurement is selected. In the sagittal and coronal plane, the measurement is made extending from a point in the middle of the aneurysm neck along the expected normal edge of the parent artery to the point on the aneurysm dome that is furthest away (Figure 1(a) to (d)). A fusiform aneurysm is a broad-based spindle-shaped or plateau-shaped aneurysm in which the height of the aneurysm is less than the size of the aneurysm neck. Fusiform aneurysms may involve the entire circumference of the artery wall or only one side of the artery wall, depending upon the nature of the trauma. Fusiform aneurysm size was defined as the ‘‘depth’’ (Figure 2(a) to (d)), in addition to the longitudinal distance (‘‘length’’) paralleling the normal artery (Figure 3). In addition, for both saccular and fusiform aneurysms, the size of the aneurysm (‘‘aneurysm plus parent artery’’) in relationship to the normal artery (‘‘parent artery’’) was also assessed (Figure 4).
Observer reliability assessment Four raters, including one vascular neurosurgeon, one neuroradiologist, and two senior neurosurgical residents independently reviewed 15 computed
Interventional Neuroradiology 0(00) tomographic angiograms (CTAs) and 13 digital subtraction angiograms (DSAs) demonstrating a traumatic aneurysm of the internal carotid artery (ICA). The images used for the study were selected from a database including patients with an aneurysm of the ICA from blunt trauma. The CTAs and DSAs did not come from the same patients. CTAs included axial, coronal, and sagittal images at a slice thickness of 6, 3, and 3 mm, respectively. DSAs included anteroposterior and lateral views of global internal carotid and vertebral injections. Five scans of each imaging modality were repeated for intra-rater reliability assessment, for a total of 38 sets of images. Scans that were repeated were randomly inserted into the dataset. Sample size was calculated using a method developed by Walter et al.,14 which showed that increasing the number of raters per subject will decrease the total number of observations required to achieve adequate sample size, a number determined to be sufficient for statistical analysis. Fleiss’s free-marginal multi-rater kappa (k) for nominal variables (‘‘shape’’) and intraclass correlation coefficient (ICC) for continuous variables (‘‘depth,’’ ‘‘length,’’ ‘‘aneurysm plus parent artery,’’ and ‘‘parent artery’’) were calculated as a measure of overall agreement (Figures 1 to 4) on aneurysm characteristics between the four raters.15,16 For intra-rater reliability analysis, Cohen’s kappa (k) and ICC were used to assess repeat measurement agreement for each rater. Agreement measured by kappa (k) was interpreted as almost perfect with k values between 0.81 and 1.00, substantial with k values between 0.61 and 0.80, moderate with k values between 0.41 and 0.60, fair with k values between 0.21 and 0.40, and poor with k values between 0 and 0.20.16 ICC greater than 0.75 was considered to have excellent inter- and intra-rater reliability, with an ICC between 0.40 and 0.75 classified as fair to good, and less than 0.40 considered poor reliability.17 The ICC was estimated using a two-way mixed effect model and an absolute agreement to assess the inter-rater concordance concerning the quantitative measurements. All statistical analysis was performed using IBM SPSS Statistics version 21.0 (SPSS, Inc., Chicago, IL) with the exception of Fleiss’s free-marginal kappa for multiple raters, which was calculated using an online program.15 This study was approved by the Institutional Review Board.
Results Inter-rater reliability CTA (n ¼ 15). Exact agreement as to the ‘‘shape’’ of the traumatic aneurysm, saccular versus fusiform, was obtained in 13 out of 15 cases (87%). Fleiss’s free-marginal multi-rater kappa (k) was 0.82, indicating an almost perfect agreement as to the ‘‘shape’’ of traumatic aneurysm between the four raters. The ICC was 0.977 (95% confidence interval (CI), 0.945–0.992) for ‘‘depth,’’ 0.974 (95% CI, 0.939–0.990) for ‘‘length,’’
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Figure 1. Saccular traumatic aneurysm. A sac-like aneurysm, with an appreciable neck, in which the height of the aneurysm (i.e. the greatest distance between the normal lumen of the parent artery and the aneurysm dome) exceeds the size of the aneurysm neck (i.e. the length of the involved segment of the parent artery). (a, b) Schematic drawing of saccular aneurysms (arrows indicate aneurysm ‘‘depth’’). (c) DSA of a left ICA saccular aneurysm with ‘‘depth’’ measurement (lateral view). (d) CTA of a left ICA saccular aneurysm with ‘‘depth’’ measurement (sagittal plane).
0.986 (95% CI, 0.970–0.995) for ‘‘aneurysm plus parent artery,’’ and 0.839 (95% CI, 0.580–0.943) for ‘‘parent artery.’’ These results implied an excellent inter-rater agreement between the four raters as to the quantitative measurements using CTA. DSA (n ¼ 13). The exact agreement between the raters as to the ‘‘shape’’ of the traumatic aneurysm, saccular versus fusiform, was obtained in 12 out of 13 cases (92%). Fleiss’s free-marginal multi-rater kappa (k) was 0.897, indicating an almost perfect agreement as to the ‘‘shape’’ between the four raters. The ICC was 0.990 (95% CI, 0.975–0.997) for ‘‘depth,’’ 0.985 (95% CI, 0.965–0.995) for ‘‘length,’’ 0.991 (95% CI, 0.979– 0.997) for ‘‘aneurysm plus parent artery,’’ and 0.860 (95% CI, 0.680–0.952) for ‘‘parent artery.’’ These results indicate excellent inter-rater agreement between
the four raters as to the quantitative measurements using DSA.
Intra-rater reliability CTA (n ¼ 5). Intra-rater reliability as to the ‘‘shape’’ was almost perfect (k > 0.80) in 3 out of 4 raters and substantial (k > 0.60) in one rater, the neuroradiologist. ICCs for ‘‘depth,’’ ‘‘length,’’ ‘‘aneurysm plus parent artery,’’ and ‘‘parent artery’’ were excellent (ICC > 0.75) in all raters (Table 1). DSA (n ¼ 5). Intra-rater observer reliability as to the ‘‘shape’’ was almost perfect (k > 0.80) in all raters. ICCs for ‘‘depth’’ and ‘‘length’’ were excellent (ICC > 0.75) in all raters while ICC for ‘‘aneurysm plus parent artery’’ was excellent (ICC > 0.75) for the
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Figure 2. Fusiform traumatic aneurysm. A broad-based spindle-shaped or plateau-shaped aneurysm in which the height of the aneurysm is less than the size of the aneurysm neck. Fusiform aneurysms may involve only one side of the parent artery wall or the entire circumference of the parent artery. (a, b) Schematic drawing of fusiform aneurysms (arrows indicate aneurysm ‘‘depth’’). (c) DSA of a right ICA fusiform aneurysm with ‘‘depth’’ measurement (lateral view). (d) CTA of a left ICA fusiform traumatic aneurysm with ‘‘depth’’ measurement (sagittal plane).
vascular neurosurgeon and neuroradiologist, and fair to good (ICC > 0.40) for the residents. ICCs for ‘‘parent artery’’ were excellent (ICC > 0.75) in one of the residents and fair to good (ICC > 0.40) in the other three raters (Table 2).
Discussion The CAVIS identified 13 trauma patients with TCVI harboring 26 traumatic aneurysms and showed that the character of traumatic aneurysms is an important determinant for a number of risk factors associated with traumatic aneurysms.3,12 These potential risks include thromboembolism,1,2 hemorrhage,18 and mass effect on adjacent structures, particularly with gradual enlargement of the aneurysm over time. Since the natural history of traumatic aneurysms is poorly understood, the point at which those factors pose a large
enough risk to justify therapeutic intervention is controversial, particularly for endovascular repair, a treatment modality that has become popular in recent years.4–11 As there currently is a need for a reliable measure of these factors in traumatic aneurysms and no consensus on how to characterize them, we developed simple, clinically applicable criteria that we used in CAVIS to characterize traumatic aneurysms and assessed their reliability.
Aneurysm shape Unlike intracranial aneurysms, which frequently have a saccular configuration, traumatic aneurysms present with a variety of different shapes. Most traumatic aneurysms have either a saccular or a fusiform shape. The agreement regarding the shape of the traumatic aneurysm, saccular versus fusiform, was almost perfect
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Figure 3. Fusiform aneurysm ‘‘length.’’ The greatest superoinferior extent of the aneurysm measured in parallel to the parent artery in the coronal or sagittal plane. (a, b) Schematic drawings of aneurysm ‘‘length’’ in fusiform aneurysms. (c) DSA of a left ICA fusiform aneurysm with ‘‘length’’ measurement (lateral view). (d) CTA of a right ICA fusiform aneurysm with ‘‘length’’ measurement (coronal plane).
between the four raters with DSA resulting in slightly superior results compared to CTA. Of the 26 traumatic aneurysms identified in CAVIS, 9 were saccular (34.6%) and 17 fusiform (65.4%).12 Saccular traumatic aneurysms may carry a greater risk of thromboembolic events because there is a potential for blood stasis and thrombosis within the aneurysm as well as exposure of subendothelial elements to circulating platelets and clotting factors from tears in the arterial wall. Fusiform traumatic aneurysms, in contrast, may result from stretching of the artery wall, rather than tearing, and carry a lower risk of thromboembolism. Two of the saccular aneurysms in
CAVIS were found in patients who had suffered an ischemic stroke and a third patient with ischemic stroke attributable to TCVI developed a saccular aneurysm after the stroke. None of the fusiform aneurysms were associated with ischemic stroke.12
Aneurysm depth Aneurysm depth is defined as the greatest linear distance between the expected location of the normal parent artery wall and the outer edge of the aneurysm lumen and represents the most frequently reported quantitative measurement for characterizing
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Figure 4. Aneurysm to parent artery ratio. Aneurysm and normal-appearing adjacent parent artery: this measurement is applicable only when the axis of the parent artery appears to be perpendicular to the plane of imaging and when there is a normal-appearing adjacent parent artery. The greatest transverse dimension of the aneurysm including the parent artery (a) in the axial plane (x) and the transverse dimension of the normal parent artery (b) above or below the aneurysm are measured (y). The aneurysm measurement ¼ x y. For spindle-shaped fusiform aneurysms, the measurement extends from the mid-point of the neck to the furthest part of the aneurysm dome on both sides, and the measurements are totaled. For plateau-shaped fusiform aneurysms, the measurement extends from the mid-point of the neck to the furthest part of the aneurysm. As conventional DSA consists of anteroposterior and lateral views only, the technique was modified. The DSA image that shows the greatest dimension of the aneurysm is selected and the greatest distance from the dome of the aneurysm to the opposite parent artery wall (x) is measured. The normal parent artery diameter is measure either proximal or distal to the aneurysm artery (y). The aneurysm measurement ¼ x y. (c) CTA of right ICA saccular aneurysm with ‘‘aneurysm plus parent artery’’ measurement (axial plane). (d) CTA of right ICA saccular aneurysm (same as in panel C) with ‘‘parent artery2 measurement (axial plane). (e) DSA of left ICA saccular ‘‘aneurysm plus parent artery’’ measurement (lateral view). (f) DSA of left ICA saccular aneurysm (same as in panel E) with ‘‘parent artery’’ measurement (lateral view).
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Table 1. Intra-rater reliability for CTAs.
Vascular neurosurgeon Neuroradiologist Neurosurgery resident 1 Neurosurgery resident 2
Cohen’s k for ‘‘shape’’
ICC for ‘‘depth’’ (95% CI)
ICC for ‘‘length’’ (95% CI)
ICC for ‘‘aneurysm plus parent artery’’ (95% CI)
ICC for ‘‘parent artery’’ (95% CI)
1.00 0.67 1.00 1.00
0.98 0.99 0.99 0.98
0.99 0.99 0.99 0.99
0.99 0.96 0.98 0.99
0.95 0.96 0.93 0.83
(0.87–0.99) (0.95–0.99) (0.93–0.99) (0.89–0.99)
(0.98–1.00) (0.96–1.00) (0.94–0.99) (0.95–0.99)
(0.99–1.00) (0.65–0.99) (0.80–0.99) (0.94–0.99)
(0.56–0.99) (0.66–0.99) (0.33–0.99) (0.17–0.98)
ICC: intraclass correlation coefficient.
Table 2. Intra-rater reliability for DSAs.
Vascular neurosurgeon Neuroradiologist Neurosurgery resident 1 Neurosurgery resident 2
Cohen’s k for ‘‘shape’’
ICC for ‘‘depth’’ (95% CI)
ICC for ‘‘length’’ (95% CI)
ICC for ‘‘aneurysm plus parent artery’’ (95% CI)
ICC for ‘‘parent artery’’ (95% CI)
1.00 1.00 1.00 1.00
0.90 0.96 0.97 0.90
0.81 0.77 0.78 0.99
0.96 0.77 0.61 0.60
0.60 0.63 0.85 0.60
(0.30–0.98) (0.73–0.99) (0.76–0.99) (0.32–0.99)
(0.39–0.98) (0.78–0.97) (0.97–0.97) (0.93–0.99)
(0.75–0.99) (3.00–0.97) (8.20–0.96) (0.54–0.95)
(0.77–0.95) (0.81–0.99) (0.20–0.98) (3.58–0.96)
ICC: intraclass correlation coefficient
aneurysms. Previous studies on measurements of the maximum diameter of intracranial aneurysm have found excellent reliability.19,20 Using a similar approach for traumatic aneurysms there was excellent agreement on aneurysm ‘‘depth’’ between the four raters yielding comparable results using DSA and CTA. ‘‘Depth’’ may be the most clinically relevant measurement for traumatic aneurysms. The average ‘‘depth’’ in CAVIS at initial diagnosis by either CTA or DSA was 6.8 mm (range 2–14 mm) for the 9 saccular aneurysms and 2.1 mm (range 1–3 mm) for the 17 fusiform aneurysms. Thus, compared to fusiform aneurysms, saccular aneurysms tend to have a greater ‘‘depth’’ upon presentation, resulting in a larger arterial radius and greater wall tension according to Laplace’s law which over time results in a greater increase in the ‘‘depth’’ of saccular aneurysms compared to fusiform aneurysms. A greater tendency of saccular aneurysms to enlarge may also reflect greater damage to the arterial wall in comparison with fusiform aneurysms, which may occur due to stretching rather than tearing of the arterial wall.12 Final follow-up imaging of the 9 saccular aneurysms in CAVIS showed that 1 (11.1%) was not visible, 4 (44.4%) were smaller, 1 (11.1%) was stable, and 3 (33%) aneurysms were larger. Final follow-up imaging of the 17 fusiform aneurysms revealed that 9 (52.9%) were not visible, 6 (35.3%) were smaller, and 2 (11.8%) were larger. Thus, saccular aneurysms were more likely to enlarge and were less likely to resolve or not visualize when compared with fusiform aneurysms. Statistically there was a trend toward behavioral differences between saccular and fusiform aneurysms as evidenced by the Fisher exact test (p ¼ 0.07). Saccular aneurysms tend to enlarge (odds ratio (OR) 3.75 (95% CI 0.49–28.4), p ¼ 0.3) over time. This difference decreased when adjusting for
aneurysm ‘‘depth’’ at diagnosis (OR 1.08 (95% CI 0.05–21.5), p ¼ 0.3); thus, while saccular aneurysms are more likely to enlarge on follow-up imaging, they are also more likely to be larger on presentation.12 Moreover, where may be an initial ‘‘depth’’ threshold above with aneurysms are more likely to grow as evidenced by the fact that 2 of 3 saccular aneurysms with an initial size larger than 6 mm were enlarged on final follow-up imaging, whereas only 1 of 6 saccular aneurysms that were 6 mm or smaller were enlarged.12 The ‘‘depth’’ measurement also has implications for the endovascular repair. Two (7.7%) of 26 traumatic aneurysms, both saccular, were treated with placement of a covered stent due to evidence of significant aneurysm growth on final follow-up imaging.12
Aneurysm length Aneurysm ‘‘length’’ was defined as the greatest extent of the aneurysm measured in parallel to the parent artery in the coronal or sagittal plane. While the perception of aneurysm length and depth may be almost identical in saccular aneurysms of whatever etiology, fusiform aneurysms with shallow depth may have a significant length as they involve and extend along the parent artery. There was excellent agreement on length between the four raters using this simple tool. In CAVIS traumatic aneurysm ‘‘length’’ was not found to be clinically significant.12
Aneurysm-to-parent-artery ratio Recent studies on intracranial aneurysms have indicated that the size ratio, i.e. the maximum diameter of the aneurysm related to the diameter of the adjacent parent artery, may predict risk of rupture, particularly in small aneurysms.21–23 A similar measurement
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8 technique employed in the present study resulted in excellent agreement on aneurysm-plus-parent-artery and parent artery measurements. The relevance of aneurysm-to-parent-artery ratio for traumatic aneurysms remains to be determined as this ratio was not found to be clinically significant in CAVIS.12
Intra-rater reliability Intra-rater reliability on aneurysm shape was almost perfect for both CTA and DSA in all raters except for the neuroradiologist who had achieved substantial agreement for CTA. Intra-rater reliability on measurements for CTA and DSA were comparable; there was no substantial difference between the rating of the vascular neurosurgeon, the neuroradiologist, and the senior residents.
Conclusions This CAVIS method of extracranial traumatic aneurysm characterization has remarkable inter- and intrarater reliability. Currently there is no standardized method for characterization of such traumatic aneurysms. The novelty of this study lies in the development of a simple, clinically relevant method to define this disease entity and introduce a common terminology that may facilitate further studies on the natural history and management of extracranial traumatic aneurysms.12 Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Conflict of interest None declared.
Acknowledgments We would like to acknowledge Kevin L Junck, PhD, Department of Radiology, University of Alabama at Birmingham for this assistance with this project.
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