British Journal of Radiology (2006) 79, 201-207
© 2006 British Institute of Radiology
doi: 10.1259/bjr/72842752
Comparison of image quality, diagnostic confidence and interobserver variability in contrast enhanced MR angiography and 2D time of flight angiography in evaluation of carotid stenosis
D Mitra, FRCR1,
D Connolly, FRCR1,
S Jenkins, FRCR1,
P English, DCR1,
D Birchall, FRCR1,
C Mandel, FRCR1,
K Shrikanth, MD1,
B Gregson, PhD2 and
A Gholkar, FRCR1
1 Department of Neuroradiology, Regional Neurosciences Centre, Newcastle General Hospital, Westgate Road, Newcastle upon Tyne NE4 6BE, 2 Academic Department of Neurosurgery, School of Surgical and Reproductive Sciences, University of Newcastle upon Tyne NE1 7RU, UK
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Abstract
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The aim of this study was to compare image quality, level of diagnostic confidence and interobserver agreement in assessment of carotid stenosis with contrast enhanced MR angiography (CE MRA) in comparison with 2D time of flight MR angiography (2D TOF MRA). 60 carotid arteries in 30 patients were examined by three observers. Image quality and diagnostic confidence were assessed on the basis of a visual analogue scale. Interobserver variability was assessed with the help of intraclass correlation coefficient. Median values on the visual analogue scale for image quality and diagnostic confidence were higher for CE MRA compared with 2D TOF MRA for all three observers. Higher intraclass correlation values were recorded for interobserver variability for CE MRA compared with 2D TOF MRA both for visual estimation of carotid stenosis as well as for measurement of carotid stenosis on the basis of North American Symptomatic Carotid Endarterectomy Trial (NASCET) and European Carotid Surgery Trial (ECST) criteria. CE MRA provides better image quality, higher level of diagnostic confidence and more interobserver agreement compared with 2D TOF MRA.
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Introduction
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An atherosclerotic lesion at the carotid bifurcation is one of the major causes of ischaemic strokes. The North American Symptomatic Carotid Endarterectomy Trial [1] (NASCET) and European Carotid Surgery Trial [2] (ECST) have demonstrated that surgical intervention is more beneficial compared with medical management in symptomatic patients with more that 70% carotid stenosis. The value of carotid endarterectomy has been extended to include asymptomatic carotid stenosis greater than 60% after the Asymptomatic Carotid Atherosclerosis Study [3] (ACAS). Accurate pre-operative assessment of the degree of carotid stenosis is therefore of crucial importance as the benefit of surgery is not proven in lesser degrees of stenosis.
Conventional catheter angiography (CA) is accepted as the gold standard in assessment of carotid stenosis and is the modality used in the measurement of stenosis in NASCET and ECST trials. However, due to the known risks of CA (overall 1–2% risk of thromboembolic complication, risks increasing with age and presence of generalized atherosclerosis), increasing numbers of centres are using non-invasive methods for pre-operative evaluation of carotid stenosis. Doppler ultrasound (DUS) is routinely used as the screening technique in many centres. MR angiography (MRA) is another technique, which is used either to confirm or supplement DUS findings.
Time of flight MRA (TOF MRA) uses inflow of unsaturated protons in blood to generate signal within a blood vessel. However, due to dependence on flow, TOF MRA is prone to flow related artefacts such as signal dropout caused by turbulence in a severely stenosed artery. The technique is also prone to movement artefacts due to relatively long scan time.
Contrast enhanced MRA (CE MRA) uses the T1 shortening effect of intravenous paramagnetic contrast agent gadolinium to generate the signal. It is, therefore, less prone to, although not completely free of, the flow related artefacts in TOF MRA. CE MRA also requires less scan time and covers a wider field of view, which allows assessment of the aortic arch and proximal common carotid arteries.
A number of studies have been carried out to evaluate specificity and sensitivity of CE MRA using CA as the gold standard [4–12]. However, there are relatively few studies [13, 14], which have compared TOF and CE MRA directly. These latter studies have looked at the comparison of the two techniques in terms of delineation of morphological details and observer confidence but have not included interobserver variability assessment. The aim of the current study is to evaluate the image quality, diagnostic confidence of the observer and interobserver variability of the two techniques.
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Materials and methods
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30 consecutive patients with suspected carotid bifurcation disease were prospectively included in this study. A DUS study was performed in all the patients. DUS results were available in all but three patients. All patients had 2D TOF MRA of the carotid bifurcation and 3D CE MRA from the aortic arch to the skull base. All the MRA studies were performed in a Philips 1.5 Tesla scanner (Philips, Best, The Netherlands) using flexible phased array coil.
For CE MRA, an 18-gauge cannula was inserted in the ante-cubital vein. A power injector (Medrad Spectris; Medrad Inc., Maastricht, The Netherlands) was used to administer 15 ml of Magnevist (Gadopentate; Schering AG, Berlin, Germany) at a rate of 1.5 ml s–1. Bolus tracking technique was used for image acquisition, whereby a single coronal slice was acquired at a rate of 1.67 frames per second while the contrast was being injected and acquisition of CE MRA was triggered after contrast was seen in the aortic arch. A fast gradient echo sequence (3D FFE; Philips; repetition time (TR) = 5.2 ms, echo time (TE) = 1.8 ms, flip angle 40°, field of view 270 mm and matrix size 336 x 512) in the coronal plane was acquired using 50% slice interpolation giving a voxel size of 1 mm x 0.5 mm x 0.5 mm. Data in the central k-space was acquired first using an elliptocentric k-space filling technique (CENTRA; Phillips). As central k-space holds data with high amplitude and low spatial resolution, this technique allows most of the contrast information to be obtained while gadolinium was in the arterial phase. Total acquisition time for CE MRA sequence was 1 min 27 s.
An axial 2D TOF MRA (TR = 17 ms, TE = 3.4 ms, flip angle 60°, field of view 200 mm and matrix size 224 x 512) study incorporating overlapping 3 mm slices to cover the carotid bifurcation was obtained in the same session. Venous contamination was prevented by using a 15 mm "travelling" superiorly positioned pre-saturation pulse. Total acquisition time for the TOF MRA sequence was 2 min.
Apart from the different scanning parameters mentioned above, CE MRA can be visually distinguished from TOF MRA by the coronal plane of acquisition of the source images (as opposed to axial acquisition for TOF MRA), larger anatomical coverage and more background suppression.
Hard copy images were produced for both CE MRA and TOF MRA with 9 maximum intensity projection (MIP) reconstructions at 40° steps and assessment of stenosis was made from the hard copies.
In all 120 sets of images (60 carotids in 30 patients imaged with two MRA technique for each carotid) were independently assessed by 3 radiologists. Image order was completely randomized so that images of the left and the right carotids as well as the images in the two modalities (i.e. CE and TOF MRA) were scattered throughout the 120 sets of images thereby reducing the bias affecting the assessment of the degree of stenosis. It took several sittings by each radiologist to complete the assessments.
Image quality was assessed by visual analogue scale (VAS). The VAS consisted of a 5 cm long line with maximum quality at 5 and minimum quality at 0. The images were specifically assessed for slice misregistration, pulsation artefact, venous flow signal, presence of plaque ulceration, visualization of external carotid artery (ECA) branches (superior thyroid and lingual) and signal dropout.
Carotid stenosis was assessed both by visual estimation and by measurements on the basis of NASCET and ECST criteria. Stenosis was measured with the film on a horizontal viewing box. Electronic callipers (Digimax Measy 2000; Swissprecision) were used to ensure accurate measurement of stenosis. Visual estimation was graded from 1 to 6 on the basis of NASCET criteria (1, 0%; 2, <50%; 3, 50–70%; 4, 70–95%; 5, >95%; and 6, 100%). Calliper measurements were carried out at the level of maximum stenosis, distal normal internal carotid artery, common carotid artery and estimated carotid bulb. Percentage of stenosis was then calculated on the basis of NASCET and ECST criteria.
Level of observer confidence on assessment of stenosis was scored both for visual estimation and estimation on the basis of measurements described above. This was again done on a VAS described above with most confident at 5 and least confident at 0.
Statistical analysis
Data were transferred to a Microsoft Access database and statistical analysis performed with SPSS software (SPSS Inc., Chicago, IL). Differences between the two techniques in terms of image quality and observer confidence were assessed using paired t-tests. Interobserver variability between observers was calculated with the help of intraclass correlation coefficient. Mean, median, mode and standard deviation were calculated on the VAS scores and displayed in box plots.
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Results
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The study was performed on 30 patients, including 21 males and 9 females. In all 60 carotid arteries were assessed. Initial screening DUS demonstrated <50% stenosis in 24 carotids, 50–70% stenosis in 5 carotids and >70% stenosis in 25 carotids. DUS results were not available in 6 carotids (3 patients).
Image quality
The median scores of image quality for CE MRA by the three raters were 4.0, 3.5 and 2.65 and those for TOF MRA were 2.05, 2.0 and 1.05, respectively (Figure 1
). All three differences were statistically significant (p<0.00001).
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Figure 1. Box plots showing distribution of visual analogue scores for image quality from each of the three raters for contrast enhanced MR angiography(CE MRA) and time of flight MR angiography (TOF MRA).
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For further assessment of image quality, visualization of the superior thyroid and lingual branches of external carotid arteries by the two techniques were assessed (Table 1).
Observer confidence for visual assessment of stenosis
Median scores for confidence level for visual assessment of stenosis by the three raters were 4.0, 3.7 and 4.0 for CE MRA. Corresponding scores for TOF MRA were 2.8, 1.9 and 2.8 (Figure 2). All three differences were statistically significant (p<0.00001). Results of visual assessment of stenosis by three observers by both TOF MRA and CE MRA are given in Table 2.
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Figure 2. Box plots showing distribution of visual analogue scores for observer confidence(for visual estimation of stenosis) from each of the three raters for contrast enhanced MR angiography (CE MRA) and time of flight MR angiography (TOF MRA).
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Table 2. Results of assessment of carotid stenosis by three observers(A, B and C) with the three methods (NASCET, ECST and visual estimation) for both CE MRA and TOF MRA. Numbers under columns A, B and C denote number of carotids under each category of stenosis. Visual estimation was based on 6 grades depending on the severity of stenosis
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Observer confidence for assessment of stenosis by measurement
The median scores for confidence level for assessment of stenosis by measurement by the three raters were CE MRA were 4.0, 3.55 and 3.5. Corresponding scores for TOF MRA were 2.65, 1.95 and 1.7, respectively (Figure 3). Again, all the differences were highly statistically significant (p<0.00001). Results of assessment of stenosis by both NASCET and ECST methods by three observers with both TOF MRA and CE MRA are given in Table 2
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Figure 3. Box plots showing distribution of visual analogue scores for observer confidence(for stenosis estimation on the basis of measurements) from each of the three raters for contrast enhanced MR angiography (CE MRA) and time of flight MR angiography (TOF MRA).
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Image artefacts
Image artefacts observed in the two techniques were analysed (Table 3). The figures in the table are out of 60 carotid bifurcations analysed in this study.
The presence of signal dropouts were analysed separately as this particular artefact caused significant problems in the accurate assessment of the degree of stenosis (Table 4). Lower incidence of signal dropout was noted with CE MRA both at the level of stenosis (46.7% with TOF MRA, 18.3% with CE MRA) as well as beyond the level of stenosis (58.3% with TOF MRA, 15% with CE MRA).
13 patients had normal carotid bulbs. Five of these patients demonstrated signal dropout in TOF MRA but none showed signal dropout in CE MRA.
Plaque ulceration was detected more frequently with CE MRA compared with TOF MRA. An average of 18.6 plaque ulcers in 60 carotids were detected with CE MRA compared with 12.3 plaque ulcers in 60 carotids with TOF MRA by the three observers.
Interobserver variability
Interobserver agreement was measured with the help of intraclass correlation using a two way mixed effect model for absolute agreement. Measurements were made for visual evaluation of stenosis, NASCET grading of stenosis and ECST grading of stenosis (Table 5). The intraclass correlation values for CE MRA (0.893 for visual estimation, 0.890 for NASCET grading and 0.800 for ECST grading) were consistently higher compared with TOF MRA (0.730, 0.758 and 0.737, respectively).
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Discussion
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The morbidity associated with carotid endarterectomy is dependent on the complication rate of surgery as well as any complication from pre-operative investigation. Therefore, if CA is used in the pre-operative evaluation of carotid stenosis, a complication rate of 1–2% is added to the surgical complication rate of 1–2%. Reducing the risk related to CA would, therefore, improve patient outcome. Furthermore, although CA was used as a gold standard in NASCET and ECST, its position as a gold standard investigation for carotid stenosis is no longer incontrovertible. The limited projections of carotid bifurcation obtained in CA can underestimate the degree of stenosis caused by eccentric plaques. This may be one of the factors causing the reported overestimation of stenosis by MRA compared with CA [11]. Current practice is moving towards non-invasive evaluation of degree of stenosis, with CA reserved only for selected cases. In this scenario, it is of utmost importance to optimize the modality of the non-invasive investigation to prevent misclassification of patients and the resultant inappropriate treatment.
DUS has been advocated by some investigators [15] as a method of evaluating carotid stenosis prior to endarterectomy. However, DUS is limited by operator dependency, difficulty in identifying sub-total occlusion with very slow flow as well as difficulty in clearly defining the morphology of lesions in the carotid bifurcation. In many centres, therefore, DUS is used in tandem with MRA, with the latter often being the confirmatory investigation [9].
Time of flight imaging is a well-established MRA technique. This is based on the signal generated from the inflowing unsaturated protons. As this technique does not require external contrast injection, the image quality does not depend on factors such as the timing of the bolus injection, volume of contrast injected, etc. This technique also has improved sensitivity to slow flow [16] and is more accurate in defining the morphology of the proximal internal carotid artery compared with DUS. We have used 2D TOF technique as it has been validated as an accurate method [9, 17] in this context and was the standardized technique used in our department at the time of the study.
Both 2D and 3D TOF MRA, however, have limitations. The most serious limitation is the loss of signal caused by complex flow pattern in the stenotic segment of the artery causing over-estimation of the degree of stenosis. In order to produce a signal the inflowing blood should be perpendicular to the scan plane. However, severe stenosis results in turbulent flow where many of the protons in the arterial blood are no longer flowing perpendicular to the scan plane and therefore do not produce a signal. Furthermore, signal is only produced by fresh protons flowing into the scan-plane, which have not received saturation pulses. If, as in a subtotal occlusion, the flow is slow enough, these protons lose their signal due to in-plane saturation. Long scan times also result in movement artefacts (mostly due to swallowing) (Figure 4) as well as slice misregistration. In the present study, problematic slice misregistration was seen in 17 carotids with TOF MRA technique but none with CE MRA technique.
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Figure 4. (a) Time of flight MR angiography (TOF MRA) and (b) contrast enhanced MR angiography (CE MRA) showing oblique projections of the carotid arteries. Note the significant degradation of the image in TOF MRA (arrows) due to movement, which is not seen in the CE MRA image.
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CE MRA uses the T1 shortening effect of gadolinium to produce signal from a vessel. It is, therefore, not directly dependent on flow to produce a signal and has less of the flow related artefacts described above. However, as an external contrast agent is administered, the timing of the injection, volume injected and the flow rate are of crucial importance. One of the major problems in CE MRA technique is presence of venous signal, which can cause difficulty in image interpretation (Figure 5). Venous signal was seen in three carotids with TOF MRA technique compared with 23 carotids with CE MRA in this study. However, in only 1 out of the 23 carotids did the venous signal prove to be a problem in image interpretation. This is in variance with another study [14] where 27% of the contrast enhanced MRA images of the carotid bifurcation was deemed non-diagnostic due to masking of the carotid bifurcation by veins.
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Figure 5. (a) Anteroposterior (AP) and (b) oblique projections of contrast enhanced MR angiography (CE MRA) of carotid arteries showing presence of venous signal (arrows). Note that despite the presence of venous signal the visualization of the carotid arteries is not significantly impaired.
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Specific techniques have been used in order to avoid this phenomenon and to optimize signal from the arteries imaged. One such technique is called time resolved CE MRA where image is acquired repeatedly at a certain rate in a method akin to DSA (hence the technique is also known as MR DSA). In this technique the timing of the bolus injection is not critically important. In the present study, a bolus-tracking technique was used in order to optimize the timing of the injection. This technique is considered to be an improvement on the time resolved CE MRA [4]. Furthermore, the central k-space data (i.e. the high amplitude and low resolution data) was acquired first, to make sure that high contrast information was acquired while gadolinium was still in the arterial phase.
CE MRA provides a much wider field of view compared with TOF MRA (Figure 6) and allows assessment from the arch to the base of the skull and if necessary up to the circle of Willis. This allows the coverage from CE MRA to be on par with CA and helps detect any concomitant intracranial disease, which may alter the decision to proceed to end-arterectomy.
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Figure 6. (a) Time of flight MR angiography (TOF MRA) and (b) contrast enhanced MR angiography (CE MRA) showing oblique projections of the carotid arteries. Note the much larger field of view of CE MRA demonstrating vessels from the arch of the aorta to the base of the skull and the better demonstration of the external carotid branches on CE MRA (long arrows) compared with TOF MRA (short arrows).
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Quality of images in both TOF MRA and CE MRA depend on the spatial and contrast resolution as well as on the presence or absence of artefacts. Loss of signal caused by non-linear flow and in-plane saturation can result in poor resolution in TOF MRA. Signal dropouts in the stenotic and post-stenotic segments were also seen more frequently with the TOF technique than with the CE MRA technique (Table 4). Signal voids were also seen in some normal bulbs as well as a significant number of tortuous carotid arteries in TOF MRA but not seen with CE MRA (Table 4).
The higher spatial resolution of CE MRA compared with TOF MRA is also indicated by the better ability to demonstrate branches of the external carotid artery (Table 1 and Figure 6). In addition, plaque ulceration was also seen more frequently by CE MRA technique than TOF MRA. This is consistent with findings of an earlier study comparing the two techniques [13].
Slice misregistration, another known problem of 2D TOF MRA [16], resulted in difficulty in image interpretation in 17 out of 60 carotid bifurcations in this study. This problem is not encountered with CE MRA, as it is a volume acquisition technique. With all the factors described above, it is not surprising that the level of diagnostic confidence of all three raters have been consistently higher with CE MRA than TOF MRA, both for visual estimation and estimation based on measurement (Figures 2 and 3). This is in keeping with the findings of a similar study [13] where on a scale of 1 to 3 (1 being the best and 3 being the worst technique) the mean diagnostic confidence score was 1.10 for CE MRA 1.90 for pooled 2D and 3D TOF images (p<0.01).
Any imaging technique also needs to be assessed for interobserver variability, particularly a relatively new technique such as CE MRA. High observer variability in some imaging techniques such as DUS has resulted in criticism and lack of wide acceptance. Low observer variability of DSA [18] on the other hand is one of the factors favouring the use of this technique for pre-operative carotid stenosis assessment. In the present study, interobserver variability has been studied between all three observers as well as for all three methods of assessment of stenosis, i.e. visual assessment, calliper measurement by NASCET and calliper measurement by ECST criteria. Interobserver variability was measured with the help of the intraclass correlation coefficient as it is considered to be a better test than kappa statistic when there are more than two observers. Intraclass correlation values are consistently higher in CE MRA compared with TOF MRA suggesting better interobserver agreement. With CE MRA, agreement was best for visual assessment followed by NASCET grading with the lowest agreement with ECST grading. Greatest difference between CE MRA and TOF MRA with regard to intraclass correlation values was in visual assessment of stenosis with very high agreement in CE MRA and only moderate agreement in TOF MRA.
Variability between different observations by the same observer (i.e. intraobserver variability) can also be an important tool in assessing the reliability of a technique. This assessment was not included in the present study and this may be considered a shortcoming of the study.
In current radiological practice, assessment of stenosis is made by looking at the reconstructed images in a workstation. However, it is possible that each observer would use a different set of projections compared with other observers for estimation of carotid stenosis. Therefore, in this study, assessment of images was made from hard copies so that each observer saw exactly the same MIP projections and therefore eliminated any bias in the estimation of interobserver variability.
The lack of comparison of the techniques described with CA could be considered to be a weakness of the study. CA was not performed in these patients because this was not part of the normal diagnostic protocol for assessment of carotid stenosis in the centre where the study was carried out. In view of the risks associated with CA, it would have been difficult to obtain ethical approval to perform CA just for the purpose of the study.
The technique of performing CE MRA has evolved from the time of this study. The technique of CE MRA described in this paper was one that was being used at the time in the department where the study was carried out. However, the results show that even with the technique used, CE MRA method was better than TOF MRA in terms of higher image quality, higher level of diagnostic confidence and less interobserver variability.
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Conclusion
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CE MRA provides better image quality, higher level of diagnostic confidence and less interobserver variability compared with 2D TOF MRA. The CE MRA technique has now replaced TOF MRA and CA as the modality of choice in pre-surgical evaluation of extracranial carotid stenosis in the centre where this study was carried out.
Received for publication February 3, 2005.
Revision received June 14, 2005.
Accepted for publication July 15, 2005.
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Abstract
Introduction
