Three Dimensional Time-of-Flight Magnetic Resonance Angiography in Carotid Artery Surgery- A Comparison with Digital Subtraction
Angiography*
Roberto Chiesa 1, Germano Melissano 1, Renata Castellano ~, Fabio Triulzi 2, Nicoletta Anzalone 2, Fabrizio Veglia 3, Giuseppe Scotti 2 and Adalberto Grossi 1
1Institute for Cardiovascular and Respiratory Disease, 2Department of Neuroradiology and 3Unit of Epidemiology, University of Milan, Scientific Institute H. San Raffaele, Milan, Italy
Three dimensional time-of-flight magnetic resonance angiography (MRA) and intra-arterial digital subtraction angiography (DSA), considered the gold-standard technique, were compared for pre- and postoperative evaluation of the carotid bifurcation. Images of suitable quality of 194 bifurcations were available with both techniques. Percentage stenosis was graded into 5 groups: A = 0-29%, B = 30-59%, C = 60-89%, D = 90-99%, E = 100% (occlusion). Preoperative MRA (126 bifurcations) overgraded the stenosis in 14 cases and undergraded it in 11. The two techniques agreed in 101 cases and the extent of misgrading was never more than one category. Regression analysis showed a good correlation between the two methods. Severe ulceration was better identified by DSA. As far as the surgical indication was concerned, MRA had a sensitivity of 92.6 % and a specificity of 98.3 %. In 68 operated cases, postoperative MRA and intraoperative completion angiography showed a satisfactory endarterectomy with no residual stenosis in any of the cases. In conclusion, MRA seems an accurate modality for imaging of carotid bifurcations. Significant limitations still exist for an adequate demonstration of intracranial circulation.
Key Words: Magnetic resonance angiography; Carotid artery surgery; Digital subtraction angiography.
Introduction
Surgery for extracranial cerebrovascular disease requires accurate imaging of the carotid artery bifur- cation. Duplex scanning is a widely used non-inva- sive technique offering a high degree of accuracy in the screening of carotid artery occlusive disease. Some authors utilise it as the only preoperative imag- ing technique before endarterectomy. 1"2 However, most feel that intra-arterial digital subtraction angio- graphy (DSA) is a necessary preoperative test, 3 as the results from Duplex scanning are operator depen- dent 4 and in many institutions the very high sensi- tivity reported in the literature has not yet been obtained.
Mortality and morbidity produced by DSA are low, but certainly not negligible, 5-7 and shoula be
* Presented at the 6th Annual Meeting of the European Society for Vascular Surgery, Athens, September 1992.
Please address all correspondence to: Dr Roberto Chiesa, Institute for Cardiovascular and Respiratory Disease, H. San Raffaele, Via Olgettina, 60, 20132 Milan, Italy.
added to that of carotid endarterectomy when sur- gery is compared to medical therapy. A reliable non- invasive preoperative method of imaging the cerebral circulation would therefore represent a major advance in the treatment of cerebrovascular disease.
Magnetic resonance (MR) was first used to produce angiograms by Makouski 8 and Moran in 1982. 9 Wedeen et al. 1° began the clinical utilisation of this technique in 1985. High quality images of the carotid bifurcations and of the major intracranial vessels have only been obtained recently, due to im- provements in the instruments and software. Three dimensional (3D) time-of-flight magnetic resonance angiography (MRA) makes use of the characteristics of flowing blood to obtain images and does not employ contrast media or invasive techniques of any kind, nor is ionizing radiation used. As it is also less costly and time consuming than DSA it is an attract- ive technique for the vascular surgeon. 11-16
The aim of this study was to compare 3D-MRA with traditional angiography in the pre- and post- operative assessment of patients submitted to carotid endarterectomy and to establish its role in carotid artery surgery.
Between June 1991 and June 1992, 70 patients with neurologic symptoms or a carotid ar tery bruit and a positive Duplex scan were selected for preoperat ive DSA and MRA. In six pat ients it was not possible to pe r fo rm MRA: three had a pacemaker, one had cer- ebral surgical clips and two patients could not tolerate the sense of conf inement . Moreover , in one case the MRA images were of inadequate quality because of m o v e m e n t artefacts.
In 63 patients (126 bifurcations) both pre- operat ive DSA and MRA of suitable quality were available for comparison. Surgery was indicated in 60 pat ients (bilaterally in eight), who eventual ly under - wen t carotid endar te rec tomy. Intraoperat ive com- plet ion angiography and postoperat ive MR was per- fo rmed in these 60 patients (68 bifurcations).
The 63 patients of our s tudy group comprised 39 males and 24 females, wi th a mean age of 67.8 + 5.6 years (range 54-79 years), with no significant age differences be tween sexes.
of obliquity. Four s tandard projections (anteriopos- terior, ob l ique-anter ior 30 °, ob l ique-anter ior 60 ° and lateral) were recorded. Hard copy records of all the examinat ions were obtained and rev iewed blindly at the end of the s tudy by a single observer. Per cent stenosis was calculated as the ratio be tween the nar- rowes t point of the stenosis and a normal point in the distal internal carotid artery, and divided into five groups according to the degree of stenosis: A = 0- 29%, B = 30-59%, D = 60-89%, D = 90-99% and E = 100% (occlusion). A descript ion of plaque ulceration was also made where appropriate. As DSA technique is the s tandard of reference, the DSA results were cons idered representat ive of the true disease state for each pat ient (Figs 1-5).
Imaging techniques
Traditional angiography
Preoperat ive angiography of the carotid bifurcations was per fo rmed with intra-arterial DSA after selective catheterisat ion of the c o m m o n carotid arteries. Matrix size was 1024 x 1024. Two projections (oblique an- terior 30 ° and lateral) were recorded. Intraoperat ive convent ional angiography, per formed rout inely to assess the technical quality of the endar te rec tomy, was obtained by means of direct punc ture of the c o m m o n carotid artery.
Magnetic resonance angiography
MRA was per fo rmed on a 1.5T (Siemens Magne tom (63 SP) system with a Helmol tz neck coil. A 3D time- of-flight acquisition 17 with an axial vo lume of 64 m m was centred at the level of the carotid bifurcation, previously localised in the sagittal and axial plane by means of a fast gradient echo technique. Neck veins were suppressed using a superior presaturat ion slab. Acquisition t ime was less than 10 min. MRA images of the carotid bifurcation were obtained with targeted max imum intensi ty project ion (MIP) reconstruct ion, which is an au tomated postprocess ing software capable of selectively displaying vessels in any degree
'a) b)
Fig. 1 DSA (a) and MRA (b) in a case of mild stenosis of the internal carotid artery. It is notable that the branches of the external carotid artery are visualised also with MRA.
Fig. 2. DSA (a) and MRA (b) in a case of stenosis of the internal carotid artery with plaque ulceration.
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MR Carotid Angiography 173
(a)
Fig. 4. DSA (a) and MRA (b) in a case of occlusion of the internal carotid artery.
Data analysis
Cont ingency tables were analysed by means of chi- square or Spearman correlation w h e n appropriate. The relat ionship be tween per cent stenosis deter- mined by the two me thods was assessed by linear regression and the Pearson correlation coefficient. Linear regression coefficients were compared with uni ty by Student ' s t-test. All analyses were per- fo rmed with the SAS statistical package for personal computers .
Fig. 3. DSA (a) and MRA (b) internal carotid artery.
b)
in a case of critical stenosis of the
Results
Preoperative examination
126 carotid bifurcations were available for compar ison be tween preoperat ive DSA and MRA with images of adequate quality obtained wi th bo th techniques. The results wi th each technique are summar ised in Table 1. There was complete agreement be tween the two techniques in 101 cases; MRA overgraded the lesion in 14 cases and unde rg raded it in 11 cases. It is appar- ent f rom Table 1 that the extent of misgrading was never more than one category.
Regression analysis: the relat ionship be tween per cent stenosis measured by DSA and MRA is
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174 R. Chiesa et aL
Fig. 5. Int raoperat ive convent iona l ang i og raphy (a) and post- operat ive MRA (b) in a case of carotid endar t e rec tomy wi th pa tch closure.
T a b l e 1. Per c e n t s t e n o s i s i n 126 b i f u r c a t i o n s , as d i a g n o s e d w i t h D S A a n d M R A
DSA
A B C D E
MRA A
B
C
D
E
30 3
1 22
8
5
31
1
2
12 1
4 6
A = 0 -29%, B = 30-59%, C = 60-80%, D = 90-99%, E 100% occlusion. M R A overgraded the s tenos is in 14 cases and u n d e r g r a d e d it in 11. The extent of m i s g r a d i n g was neve r more than one category.
100
80
6O •
40 • •
/ 20 ~ / •
' A ' A ' A '
0 20
/ •
! , , I , , , I ,
40 60 80 100
D S A
Fig. 6. Rela t ionship be tween per cent s tenos is m e a s u r e d by DSA a n d MRA. ( - - - ) Linear regress ion and ( .) line of ident i ty (r = 0.953, y = 0.977X + 0.03).
depicted in Fig. 6 (r = 0.953; Y = 0.977X + 0.03) with no significant difference from the line of identi ty (solid line). The good correlation between the two imaging techniques in this setting is apparent.
With regard to the surgical indication, given according to the criteria of the American College of Physicians, 18 the accuracy of MRA was compared to DSA with the results reported in Table 2. MRA pro-
T a b l e 2. A c c u r a c y o f M R A c o m p a r e d w i t h D S A w i t h regard to s u r g i c a l i n d i c a t i o n , g i v e n a c c o r d i n g to the A m e r i c a n C o l l e g e o f P h y s i c i a n s TM
DSA
Positive Negat ive
MRA Positive 63 1
Negat ive 5 57
Sensi t ivi ty = 92.6%, specificity = 98.3%.
duced five false negatives. In four cases, MRA graded a 99% stenosis as an occlusion and in one case MRA graded a 70% stenosis as a 30% one. MRA also pro- duced one false positive as it graded a complete occlusion of the internal carotid artery as a 99% sten- osis. MRA sensitivity was 92.6% and specificity 98.3%.
In considering ulceration, we analysed the results of 68 operated cases: a plaque ulceration was
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MR Carotid Angiography 175
Table 3. Different kinds of plaque ulcerations seen at surgery and detected by DSA and MRA
Small Multiple discrete Large cavernous ulceration ulceration ulcerations
Gross inspection 26 15 23
DSA 15 10 19
MRA 9 5 10
DSA showed a higher accuracy than MRA in ulcers detection, however, a relevant number of plaque ulcerations were missed also by DSA.
observed in 44 cases with DSA and in 24 with MRA. A comparison between the types of plaque ulceration found at surgery and the ones observed with DSA and MRA is made in Table 3.
Postoperative examination
Sixty eight carotid artery endarterectomies were per- formed in this group of patients and patch closure was used selectively in 16 cases (23.5%). Mortality was nil and morbidity was limited to one case of transitory neurologic deficit, therefore, all cases were available for postoperative examination. Routine intraoperative completion angiography was per- formed to assess the technical quality of the endarter- ectomy and in all instances showed a patent internal carotid artery with a satisfactory endarterectomy. MRA was performed before patient discharge and also showed a patent internal carotid artery without residual stenosis in all cases. The two techniques agreed in 100% of cases.
Discussion
Intra-arterial DSA is almost universally accepted as the standard imaging method for preoperative evalu- ation of cerebrovascular disease, since it provides complete and extremely accurate imaging of the aor- tic arch and extracranial-intracranial circulation. 19-22 The advantages of this technique are well known and the spatial resolution of angiographic images cannot be obtained by any other imaging technique. How- ever, DSA is an invasive technique which employs contrast media and radiation, and is usually per- formed on in-patients. Complications arising from DSA are now much reduced when femoral catheteri- sation and non-ionic contrast media are employed, but they still occasionally occur.
MRA seems particularly attractive because it is
non-invasive, does not employ contrast media of any kind 23 and can be performed on an out-patient basis; the examination is fast and less expensive than DSA. MRA is virtually free of complications, provided that patients are accurately screened for metallic implants which preclude examination. Some patients complain of discomfort and a sense of confinement during the examination, but few patients could not tolerate this. A small number of images are inadequate due to movement artefacts. The ability of the examiner to distinguish between a very thigh stenosis and com- plete occlusion in MRA is still sometimes difficult. MRA, in fact, may overgrade the stenosis in the presence of turbulent flow, however, increasing ex- perience will certainly enhance the quality of the images and the accuracy of the interpretation.
In this series most of the patients who under- went carotid endarterectomy had an ulcerated plaque (Table 3) and MRA showed a low sensitivity in their detection, however, neither was DSA very accurate in the detection of plaque ulcers, particularly small ones. Ultrasonography is probably more accurate than both MRA and DSA in the study of plaque characteristics.
This paper focused on the evaluation of the ca- rotid bifurcation, but in our patients intracranial cir- culation is also routinely examined. MRA has been shown to demonstrate accurately the main intra- cranial vessels and their abnormalities, particularly berry aneurysms. 24-25 However, MRA assessment of the intracranial atherosclerotic occlusive disease is still unsatisfactory, especially for smaller branches, but progress is being made. Images of the aortic arch are difficult to obtain with this technique and are currently unsatisfactory.
Further improvements with MRA could be achieved with dedicated neck coils, with a larger matrix (5122 , 10242 ) and larger comparative series. Our results show that MRA is a reliable non-invasive preoperative technique for the evaluation of the ca- rotid bifurcations. It may now be considered as first choice examination when DSA is contraindicated. In the near future, MRA will be able to replace DSA in the majority of patients. As a postoperative examin- ation, MRA is accurate and useful as it provides nonoperator-dependent images which can be used to serially follow up the operated carotid artery and pro- gression of disease in the contralateral carotid artery.
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