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January2005 Vol.42 Issue:      1 Table of Contents
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The Value of 3-D Imaging Modalities in Cerebrovascular Disease Management

Adel Hassanein1, Ihab Ismail2, Mostafa Mahmoud2, Kamel Hamouda1, Shereen Fathy1, Noha Abo-Krysha1, Ahmad Abo Mousa1, Foad Abd el Monem1, Khaled Kaffas2, Osama Hassanein3
Departments of Neurology1, Radiodiagnosis2, Cairo University, Clinical Pathology, Al-Azhar University3

ABSTRACT

Stroke and stroke related disabilities secondary to extracranial carotid artery disease, remain an important public health problem. Since several clinical trials have proved the benefit of carotid intervention in patients with moderate or severe stenosis, imaging of the carotid artery has been the focus of considerable attention. Angiography has been considered the gold standard examination; however it is an invasive procedure and the frequency of strokes varies from 0.45% to 2.6%. To reduce risks related to catheter based angiography, many noninvasive imaging approaches have been advocated. The Aim of our work is to evaluate the role, diagnostic accuracy and efficacy of 3D- imaging techniques (3D power Doppler sonography and 3D CE-MR angiography) in the assessment of carotid artery lesions and their impact on the management of cerebrovascular diseases as compared to 2D Doppler ultrasound. Patients & Methods: 60 patients (39 males and 21 females) were included in this study, presenting either with  cerebrovascular stroke or transient ischemic attacks. All underwent preliminary 2D duplex scanning then 3D power Doppler and 3D contrast enhanced MR angiography. Results: A total of 63 stenosis of various degrees (range from 20 to 100%), three ulcerated plaques, one dissection, one aneurysm and two hemodynamically significant kinks were diagnosed. Our results revealed that both 3D power Doppler sonogram and 3D CE-MR angiography showed excellent agreement as regards estimation of the degree of stenosis as well as the distance of the stenosis or occlusion from the bifurcation, when compared to 2D Doppler sonography. 3D CE-MR angiographic images showed comparable lesion lengths to that estimated by 2D color duplex sonography; however 3D power Doppler scanning detected significantly shorter lesions. 3D CE-MRA appeared to be the most accurate method in detection of carotid ulcerations. Conclusion: We conclude that both 3D power Doppler sonography and 3D CE-MRA are accurate methods that have important clinical implications to assess carotid artery disease. They may provide a reliable method for observing the progression or regression of a plaque and/or change in the severity of stenosis in a segment of a carotid artery. On the other hand, they play an important role in follow up studies, especially after interventional procedures (e.g. carotid stenting) and finally all of that will be reflected on stroke management and outcome.

(Egypt J. Neurol. Psychiat. Neurosurg., 2005, 42(1): 97-113).

 




INTRODUCTION

 

                Fatty plaques can clog an artery like grease in a kitchen drain. When this happens, the reduced blood flow can cause a cerebrovascular stroke. Narrowing of the arteries, or stenosis, can be treated, but physicians must somehow look inside the affected artery to judge the severity and location of the blockage. Blockage can be caused by clogging of arteries within the brain (e.g. lacunar stroke), or hardening of the arteries leading to the brain (e.g. carotid artery atherosclerosis or occlusion)1.

                The initial lesion represents the first micro­scopically and chemically detectable lipid de­posit in the tunica intima and the cellular reac­tions associated with such deposits2. Fatty streaks are grossly visible, flat yellow patches or linear streaks deposited on the inti­mal surface of arteries. The pri­mary lipid components of fatty streaks include cholesterol esters (77%), cholesterol, and phos­pholipids3. Atheromatous plaques, also called fibrous, fibrofatty, lipid, or fibrolipid plaques, are the fun­damental lesion of atherosclerosis4.

                Calcification is a prominent feature of complicated plaques and may be extensive, involving both the su­perficial and deeper regions of the plaque. Progressive fibrosis may convert the fatty atheroma into fibrous scar4.

                Atherosclerotic plaques often develop at the origin of the CCA as it arises from the aortic arch, at the origin of the ICA in the neck, and intracranially, in the ICA siphon. Symptomatic or significant carotid atheromatosis usually involves the segment of the artery located just distal to the common carotid bifurcation, where the lesions are relatively accessible for surgical removal5.

                Plaques may become clinically symptomatic when they cause marked stenosis (more than 70% nar­rowing), if accompanied by throm­botic occlusion of the lumen, or become the source of embolism6. Ulceration or breakdown of the fibrous cap covering the atheroma may be the result of hemodynamic alterations secondary to marked stenosis because blood flow velocity and the shear stress increase as the lumen becomes narrower. High level of shear stress may pro­mote erosion of the endothelial cell lining and exposure to the circulation of the debris nor­mally covered by the fibrous cap7.

                Fragmenta­tion and release into the circulation of the ath­eromatous material may occur as the plaque undergoes central necrosis, followed by virtual liquefaction of the cholesterol esters, release of calcium-containing materials, and bleeding into the plaque. Debris resulting from the ul­ceration of fragile plaque may be released into the cerebral circulation, and these particles may occlude distal arteries and result in either transient ischemic attacks or ischemic strokes8.

                The sudden increase in plaque volume could presumably reduce blood flow to the ipsilateral hemisphere and induce either transient ischemic attacks or ischemic strokes. Such mechanism currently remains conjectural9.

                Non atheromatous carotid pathology can be caused by carotid dissection that causes less than 3% of strokes in the general population, but up to 20% of strokes in younger patients10.  Fibromuscular Dysplasia is a primary arteriopathy of an unknown cause affecting medium-sized arteries in many areas of the body and Takayasu’s Arteritis that is a chronic inflamma­tory arteriopathy primarily affecting women in the second through fourth decade of life. Although the cause of Takayasu’s arteritis is unknown, it is likely to be an autoimmune process. The aorta is affected in almost all cases, but carotid disease, although uncommon, occurs typi­cally, where there is a long-segment, sometimes severe, stenosis involving the proximal CCA begin­ning at its origin11.

2D ultrasound has proved to be reliable in some previous studies in the evaluation of carotid artery stenosis, especially when combined with Doppler imaging.         However, its feasibility and accuracy has been challenged by the physical inaccessibility of some cutting planes, which in some circumstances might be crucial for diagnosis. In addition, 2D ultrasound is technically operator dependent with variability in parameters choice and susceptibility to artifacts from calcified plaques12. Moreover, 2D images must be mentally integrated in order to form an impression of the anatomy and pathology, potentially resulting in a time-consuming, inefficient, and variable process13.

The 3D power Doppler system may enable physicians to study the region of interest in more detail, and speed up the entire patient management process14. The 3-D image provides a representation of the patent lumen through the bifurcation region, tracking the blood flow-vessel wall interface. Luminal changes can be appreciated better. Moreover, it has been shown that plaque volumes, can be used for follow-up evaluation. For this study the 3-D image was displayed with the lumen filled with the flow image information to provide a solid outline of this flow-wall interface. Movement of the ultrasound system track ball allowed rotation of the 3-D image to view the carotid bifurcation luminal contour from any angle needed to provide a clear view of the vascular anatomy. These views were then used to determine surface morphol­ogy and to measure the residual diameter at the point of maximal narrowing15.

3D power Doppler sonography can clearly demonstrate (as recon­structed 3D volume surveys) severe stenosis that could be surgically managed. Important param­eters such as the degree of the stenosis and its length and distance from the bulb can be readily demonstrated before surgery or stent implanta­tion. The 3-D ultrasound of the carotid artery has other numerous advantages as an imaging technique; first, it is noninvasive and portable and can be performed in various clinical settings. Second, it may minimize the discomfort of the patient by reducing the examination time and probe manipulation. Third, the images of the carotid artery can be reconstructed in unrestricted directions from the 3-D data set. Fourth, it provides volumetric information of not only the free lumen of the carotid artery but also the plaques, the vessel wall, and the adjacent tissue and structures, such as the jugular vein14. Much important is that 3D power Doppler Sonography can detect high grade stenosis at high position, so in ICA stenosis, 3-D image can show the stenosis precisely and can be used as a reliable tool for proper evaluation of the carotid system16.

For most applications in the extracranial ca­rotid arteries: Time of Flight [TOF] Magnetic Resonance Angiography is pre­ferred (MRA). MRA had previously been believed to routinely overestimate the de­gree of carotid stenosis when compared with catheter studies17.

MRA using two dimensional (2D) and three dimensional (3D) time of flight has shown high accuracy in diagnosing carotid stenosis greater than 70% (70-99%)18. However, on the basis of flow enhancement, MRA is limited by enhancing slow or turbulent flows. This limitation leads to overestimation of the severity of a stenosis and difficulty in distinguishing severe stenosis and total occlusions. These difficulties preclude the use of MRA alone19.

One important step towards MRA, is its capability of screening the vessels from the aortic arch to the circle of Willis without repositioning the patient by using an adequate surface coil that is able to cover a large field of view. The second step is to use a coronal contrast-enhanced (CE) MRA technique which allows visualization of these vessels in a very short examination time20.

The aim of this work is to evaluate the role, diagnostic accuracy and efficacy of 3D imaging techniques (3D power Doppler sonography and 3D CE-MR angiography) in the assessment of carotid artery lesions and their impact on stroke management as compared to 2D Doppler ultrasound.

 

PATIENTS AND METHODS

 

Patients:

This study included 60 patients (39 males and 21 females) with a mean age of 59.1years (range11-78 years).  All patients were referred from El-Kasr El Aini Hospital, Cairo University (Neurology Department, Cardiology Department, Vascular Surgery Units and  Internal Medicine Hospital).

 

Patients were divided into two groups:

1.         Group I : 14 patient (23.3%) were Asymptomatic ;with no Neurological symptoms.

2.         Group II : 46 patients (76.7%) were Symptomatic with Neurological symptoms in the form of cerebrovascular strokes or Transient ischaemic attacks.

Fifty patients (86.2%) had one or more identified risk factors for atherosclerosis, i.e. hypertension, diabetes mellitus, hypercholesterolemia, positive family history, and/or nicotine consumption.

 

Methods:

All the patients were subjected to the following assessment protocol:

I-             Thorough Clinical assessment :

Medical History and Neurological Examination: Using the standard cerebrovascular stroke assessment sheet21,22.

 

II-            Laboratory works up:

1.             Complete blood picture

2.             Erythrocyte sedimentation rate .

3.             Blood sugar tests

4.             Serum cholesterol level

5.             Serum triglyceride level

6.             Serum urea and creatinine

7.             Serum liver function testes

 

II-            Imaging :

All patients underwent preliminary 2D color duplex scanning, then 3D power Doppler and 3D contrast enhanced TOF MR angiography. Fifteen of them underwent digital subtraction angiography.

i.              Color Doppler Sonography:

Color Doppler sonography was performed by using a Sonoline Elegra Advanced ultrasound scanner (Siemens, Is-saquah, WA) and a 7.5-MHz linear-array trans­ducer. Imaging of the carotid bifurcation was done. the peak systolic velocity (PSV) was used to evaluate the degree of stenosis. When PSV was higher than 1.20 or 2.15 m/second, for example, we suspected a stenosis of the ICA greater than 50% or 70%, respectively, of the vessel diameter. We measured the respective reductions in vessel diameter in the transverse plane as well as the lengths of the respective stenosis.

ii.            3D Power Doppler Sonography:

We used in­teractive 3D imaging (3-Scape, Siemens) ul­trasound system that provides volume data acqui­sition, reconstruction, and display. 3D volume data can be acquired and displayed in B-mode, power Doppler mode, or both. Stenosis of the ICA was measured according to the NASCET criteria 23, by the ratio of the luminal diameter at the level of the greatest stenosis to that at the normal part of the artery beyond the stenosis. Distance between stenosis or occlusion and the carotid bifurcation, as well as the length of the stenosis were also calculated from 3D survey only. We used external software (Photoshop, Ver­sion 7.0; Adobe Systems Inc, San Jose, CA) for these measurements.

iii.           3D Contrast Enhanced MR Angiography:

The NASCET categories20 were arbitrarily modified to define a 98% stenosis as the presence of a signal void on MIP images at the level of the stenosis when flow was visible distal to the stenosis The image that demonstrated the most severe stenosis was used. The diameter of the most severe stenosis (A) was divided by the diameter of the distal cervical internal carotid artery beyond the stenosis (B).(Figure 1).

 

A

B

 

 

 

 

 

 

 

 

 

 

 

 

Fig. (1): North American Symptomatic Carotid Endarterectomy Trial Collaborators, 1991.

Stenosis degrees were classified into five grades:

Negative values were defined as 0% stenosis.

Grade I: stenosis less than 30%

Grade II: stenosis between 30-49.9%

Grade III: stenosis between 50-69.9%

Grade IV: stenosis between 70-99.9%

Grade V: 100 % Stenosis (occlusion)24.

 

A plaque was classified as ulcerated if fulfilling the criteria of an ulcer niche, seen in profile as a crater penetrating into a stenotic plaque. Carotid stenosis was measured at the same level on the 3D power Doppler and contrast-enhanced 3D MR angiograms. The value was subtracted from 1 and then multiplied by 100 to yield the percentage diameter stenosis.

 

Statistical Analysis:

The statistical analysis was done using an IBM compatible computer and STATISTICA 6.0 for MS Windows 98 statistical package. Descriptive statistics was presented as means ± standard deviations, median and number percentage (frequency distributions). Analytical tests used included unpaired student t test (two sided) for comparing two groups. Analysis of variance (F test) was used for comparing more than 2 groups. Post hoc test was used for comparing each group. Non parametric testing was also used to confirm significance. Paired t test was used for comparing values before and after treatment. Chi square test for contingency table analysis and Fisher's exact testing for 2 x 2 tables. Correlation and regression analysis were also performed whenever appropriate.

 

RESULTS

 

I.             Study Population:

The present work included a cohort population of 60 patients, 39 (66%) of whom were males and 21 (34%) were females .They had a mean age of 59.1 years (range of 11-78). Forty six (77%) of the included patients were symptomatic and 14 (23%) patient were asymptomatic. The most common presentation among the included patients was cerebrovascular stroke (38.8%), followed by TIA’s (26.2%). 23.1% of the patients were asymptomatic. The frequency distribution of the presenting symptoms is presented in figure (2). The indications for preliminary 2D Doppler study are reviewed in table (1). Cerebrovascular stroke was the most common indication followed by TIA.

The frequency distribution of the predisposing factors is shown in figure (3). Hypertension and diabetes mellitus were the most common risk factors met in the present study.

 

II.            Carotid disease:

Fifty patients (91%) had atherosclerotic disease and 5 patients (9%) had non atherosclerotic disease (One patient had traumatic dissection, one patient had true aneurysm, one had arteritis and two patients show hemodynamic significant arterial kinking). The distribution of the stenotic lesions in the 4 different segments (CCA, ICA, ECA and carotid bulb) are listed in table (2). While the dissection as well as the true aneurysm located in the CCA.

 

III.          Imaging:

*              Degree of stenosis in 2D duplex scanning

2D duplex scanning revealed 3 carotid segments with no stenosis(5%); (grade 0), 2 carotid stenosis (3%) of 0-30% (grade I), 20 carotid stenosis (32%) of 30-49.9%( grade II), 22 carotid stenosis (35%) of 50-69.9%(grade III), 11 carotid stenosis (17%) of 70- 99.9% (grade IV) and 5 carotid occlusions(8%) (grade V) (Figure 4).

*              Degree of stenosis in 3D power Doppler  

3D power Doppler revealed: 3  carotid segments (5%) with no stenosis (Grade 0) , 1 carotid stenosis (2%) of 0-30% (Grade I), 24 carotid stenosis (38%) of 30-49.9% (Grade II), 19 carotid stenosis (30%) of 50-69.9% (Grade III), 11 carotid stenosis (17%) of 70- 99.9% (Grade IV) and 5 carotid occlusions (8%) (Grade V) (Figure 5).

Tabulated agreement data are shown in table (3). Three-dimensional ultrasound imaging correctly categorized 57 of the 63 carotid stenosis lesions for degree of luminal narrowing, with an overall accu­racy of 90.4%. Kappa = 0.83  & p<0.001.  This indicates excellent agreement between the two methods. One case out of the 21 (4.8%)  categorized as grade II stenosis by 2D duplex scanning was overestimated to be grade III using 3D power Doppler. One case of the 23 (4.5%) diagnosed as grade III was overestimated to be grade IV while 3 (13.6%) were underestimated to be grade II. One of the 11 cases (9.1%) diagnosed as grade IV was under estimated to be grade III. All 5 total occlusions and the 3 cases with no stenosis were correctly identified by 3-D imaging with a diagnostic sensitivity and accuracy of 100% in categorizing both grades 0 and V. Hence both techniques show excellent agreement as regards estimation of the degree of stenosis (k =0.83; P<0.001).

The sensitivity, specificity and diagnostic accuracy of 3D power Doppler in estimating the degree of DR% is shown in table (4). However, this was not calculated for grade I stenosis due to the small number of cases which would adversely affect our interpretation.

A good positive correlation was observed between the percentage of stenosis measured from 2D color duplex and that measured in 3D power Doppler data set (r=0.969; P=<0.001) (Figure 6 ).

*      Degree of stenosis in 3D CE-MR Angiography:

3D CE-MR angiography revealed 3 carotid segments (5%) with no stenosis; (grade 0), 1 carotid stenosis (2%) of 0-30%; (grade I), 20 carotid stenosis (32%) of 30-49.9%; (grade II), 24 carotid stenosis (38%) of 50-69.9%; (grade III), 10 carotid stenosis (15%) of 70- 99.9%; (grade IV) and 5 (8%) carotid occlusions; (grade V) (Figure 7).

Tabulated agreement data are shown in table (5). 2D Doppler and 3D CE-MR Angiography cor­rectly categorized 58 of the 63 carotid stenosis lesions for degree of luminal narrowing, with an overall accu­racy of 92%. Kappa = 0.89 P<0.001. This indicates excellent agreement between the two methods. One case of the two diagnosed as grade I stenosis using 2D duplex scanning was overestimated to be grade II using 3D CE-MRA. Two cases out of the 21 (9.5%) categorized as grade II stenosis by 2D duplex scanning were overestimated to be grade III using 3D CE-MRA. One case of the 23 (4.3%) diagnosed as grade III and one of the 11 cases (9.1%)  diagnosed as grade IV were underestimated to be grade II and grade III respectively. All 5 total occlusions and the 3 cases with no stenosis were correctly identified by 3D CE-MRA with a diagnostic sensitivity and accuracy of 100% in diagnosing grades 0 and V. Hence both techniques show excellent agreement as regards estimation of the degree of stenosis (k =0.89; P<0.001).

The sensitivity, specificity and diagnostic accuracy of 3D CE-MRA in diagnosing the degree of DR% is shown in table (6). Again grade I stenosis cases were exempted due to their small number which would not allow accurate interpretation.

Correlation of 2D color duplex scanning and CE-MR Angiography was performed using linear regression analysis. The correlation of the 3D CE-MRA with 2Dcolor Doppler using categorical data was significantly positive (r = 0.961; P< 0.001).

Lesion lengths as determined by 3D CE-MRA showed no statistically significant differences as compared to 2D color duplex Sonography with a mean of 14.06±6.46 mm in contrast to 14.27±6.44 mm respectively (P<0.07). However, 3D power Doppler scanning detected significantly shorter lesions with a mean of 13.32±5.92 mm as compared to 2D color duplex Sonography with a (P<0.001) (Table 7).

As regards the distance of the stenosis or occlusion from the bifurcation, the results obtained from  the 3D power Doppler scanning show highly positive correlation  with those of the 2D color duplex Sonography   (r = 0.966; P < 0.001).

 

Extent of the lesion into the bifurcation

A strong positive agreement was identified between 2D color duplex and  3D power Doppler as regards the extension of the lesion into the bifurcation (k = 0.912; P < 0.001). 40 of 39 (102%) lesions were identified by 3D power Doppler scanning as focal lesions, 18 of 16 (106%) as being of moderate extent of <1 cm, and 6 of 9 (72%) as lengthy  extended lesions of > 1 cm. This indicates excellent agreement between the two methods (Table 8).

For the evaluation of the extent of the lesion into the bifurcation, the estimated extension shown by 3DCE-MRA images was as follows;  39 of 39 (100%) were correctly identified as focal lesions, 17 of 16 (106%) as being of moderate extent of <1 cm, and 8 of 9 (72%) as extended lesions of >1 cm. Hence, there is under estimation of the lengthy extent lesion by 3D CE-MRA in a single vessel. Both methods thus show excellent agreement (k = 0.912; P < 0.01).

A strong positive correlation was found between both 2D and 3D (r = 0.96; P < 0.001) and 2D and 3D CE-MRA (r = 0.997; P < 0.01 respectively in measuring the extension into the bifurcation (Table 9).

 

Ulcerations

Three well-defined ulcerations were identified by 3D CE-MRA; one of them was not identified by 2D color duplex sonography or 3D power Doppler scanning. The unidentified ulcer was located within a complex calcific lesion.

 

Angiography

The studied cases didn’t undergo angiography as part of the present work due to the known incidence of stroke (1%) may be caused by catheter angiography in patient with carotid severe stenotic lesions as stated by Davies et al.25, but 15 patients had angiography either due to the surgeon request for preoperative evaluation or during balloon dilatation and stent placement.

 

Intervention

Ten patients underwent endarterectomy. In nine patients the surgeon could confirm the 2D duplex sonography, 3D power Doppler and 3D CE-MRA findings regarding the grade of stenosis, with a diagnostic accuracy of 92.5%. In one case the imaging showed overestimation of the grade of stenosis. Three patients underwent balloon dilatation and stent placement, two of them having stenotic lesions of 70 % and 83% diameter reduction respectively were monitored after one month by 2D sonography, CE-MR angiography and 3D power Doppler for follow up.


 

 

Table 1. Indications for preliminary 2D Doppler study.

 

Asymptomatic

Number

* Bruits

4

* Pre-operative  cardiac disease

9

* Pre-operative other surgery

3

Symptomatic

 

* Visual symptoms

5

* Cerebrovascular stroke

22

* Transient ischemic attacks

15

* Vertigo

2

Total

60

 

Fig. (2): Frequency Distribution of Presenting Symptoms in Studied Cases.

 

 

Fig. (3): Frequency Distribution of Predisposing Factors.

 

Table 2. Distribution of stenotic lesions in different segments of extracranial carotid artery.

 

 

Stenotic lesions

 

Frequency

Percent (%)

CCA

28

44.5

ICA

28

44.5

ECA

5

7.9

Bulb

2

3.1

Total

63

100.0

 

 

 

Fig. (4): Frequency Distribution of Stenosis Grade by 2D color duplex   in Studied Cases.

 

 

Fig. (5): Frequency Distribution of Stenosis Grade by 3D power Doppler in studied cases.

               

Table 3. Agreement between stenosis grade by 2D color duplex  and 3D power Doppler.

 

3Dpower Doppler

2D color duplex

0

I

II

III

IV

V

0

3(100%)

 

 

 

 

 

I

 

 

1(4.8%)

 

 

 

II

 

2(100%)

20(95.2%)

3(13.6%)

 

 

III

 

 

 

18(81.8%)

1(9.1%)

 

IV

 

 

 

1(4.5%)

10(90.9%)

 

V

 

 

 

 

 

5(100%)

Total

3(100%)

2(100%)

21(100%)

22(100%)

11(100%)

5(100%)

Table 4. Sensitivity, specificity and diagnostic accuracy of 3D power Doppler  in estimating degree of DR% as diagnosed by 2D duplex.

 

 

Grade 0

Grade II

Grade III

Grade IV

Grade V

Sensitivity

100%

92.1%

93.8%

94%

100%

Specificity

100%

100%

97.9%

94.8%

100%

Accuracy

100%

95.3%

96.9%

94.8%

100%

 

r =0.969  P<0.001

 

 

Fig. (6): Scatter plot of Correlation between DR% by 2D color duplex and 3D power Doppler.

 

 

Fig. (7): Frequency Distribution of Stenosis Grade by 3D CE-MRA in Studied Cases.

Table  5. Agreement between stenosis grade by 2D color duplex  and 3D CE MRA.

 

3D CE-MRA

2D color duplex

0

I

II

III

IV

V

0

3(100%)

 

 

 

 

 

I

 

1(50.0%)

 

 

 

 

II

 

1(50.0%)

19(90.5%)

1(4.3%)

 

 

III

 

 

2(9.5%)

22(95.7%)

1(9.1%)

 

IV

 

 

 

 

10(90.9%)

 

V

 

 

 

 

 

5(100%)

Total

3(100%)

2(100%)

21(100%)

22(100%)

11(100%)

5(100%)

 

 

Table 6. Sensitivity, specificity and diagnostic accuracy of 3D CE-MRA in estimating degree of DR% in relation to 2D Duplex study.

 

 

Grade 0

Grade II

Grade III

Grade IV

Grade V

Sensitivity

100%

92.3%

93.8%

100%

100%

Specificity

100%

97.4%

100%

94%

100%

Accuracy

100%

95.4%

98.5%

98.7%

100%

 

Table 7. Comparison of Lesion length between 2D color duplex  and each of 3D power Doppler  and 3D CE-MRA.

 

 

2D color duplex

3D power Doppler

3D CE-MRA

Mean (mm)

14.27

13.32

14.06

SD (mm)

6.44

5.92

6.46

P value

 

0.001**

0.07

 

Table 8. Agreement between grade of extension into bifurcation by 2D color duplex  and 3D Doppler.

 

3D power Doppler

2D color duplex

Focal

Moderate

Lengthy

Focal

39 (100%)

 

1 (11.1%)

Moderate

 

16 (100%)

2 (22.2%)

Lengthy

 

 

6 (66.7%)

Total

39 (100%)

16 (100%)

9 (100%)

 

Table 9. Agreement between grade of extension into bifurcation by 2D color duplex  and 3D CE-MRA.

 

3D CE-MRA

2D color duplex

Focal

Moderate

Lengthy

Focal

39 (100%)

 

 

Moderate

 

16 (100%)

1 (11.1%)

Lengthy

 

 

8 (88.9%)

Total      

39 (100%)

16 (100%)

9 (100%)


DISCUSSION

 

                Among the techniques that have been used for evaluation of carotid artery stenosis, angiography is the most widely used and accepted for selection of candidates for carotid intervention. This was mentioned by the North American Symptomatic Carotid Endarterectomy Trial (NASCET) and the European Carotid Surgery Trial (ECST)22,26.

                There is considerable risk of catheter angiography in asymptomatic patients suffering from carotid stenosis; some will suffer from a stroke during the procedure. Previous publications have reported the risk of angiogram-associated infarction to be around 1% 27.

                2D ultrasound is able to overcome some of the drawbacks of the above-mentioned technique and has proved reliable in some previous studies in the evaluation of carotid artery stenosis12,13.

                3-D ultrasonographic vascular imaging shows prom­ise for the technique in its ability to quantitatively define stenosis of the carotid bifurcation region. Both a sharp delineation of the arterial wall and sufficient intraluminal signals are essential for a correct assessment of vessel diameter and classification of a stenosis. Several investigators have noted that tech­nical restrictions in measuring luminal diameters for the determination of the degree of stenosis by color Doppler sonography can be overcome by us­ing power Doppler sonography28.

MR angiography using two dimensional (2D) and three dimensional (3D) time of flight has shown high accuracy in diagnosing carotid stenosis greater than 70% (70-99%)17.

The aim of the present work was to study the role of 3D imaging (3D power Doppler sonography and 3D CE-MR Angiography) in the assessment of the carotid artery lesions. The diagnostic accuracy and over all efficacy of 2D duplex Doppler sonography were compared to both 3D modalities.

In the present study, 57 stenotic lesions were  correctly categorized by 3D power Doppler as regards their degree of stenosis out of 63 stenotic lesions identified by 2D duplex ,with an over all accuracy of 90.4%. Our diagnostic accuracy is higher than that reported by Bendick et al.15. In their study, 61 carotid bifurcations were evaluated by 3D power Doppler, 53 of these vessels showed agreement between 2D duplex sonography and the 3-D image with an overall diagnostic accuracy of 87%, similar to that reported by Hood et al.29, and Burnham et al.30. In a larger study conducted by Keberle et al.31, that included 436 stenotic lesions; 420 vessels were adequately depicted by 3D volume surveys with an overall diagnostic accuracy of 96% which is higher than that reported in our study.

Our findings confirm the value of 3D power Doppler ultrasonography as a reliable and accurate method in the diagnosis of carotid artery disease. In estimation of lesions causing more than 70% carotid artery stenosis, we report a sensitivity of 94%, a specificity of 94.8% and a diagnostic accuracy of 94.8%. Kozàkovà et al.32, reported a comparable sensitivity of 96% for estimating significant (>70%) carotid stenosis. However both specificity and diagnostic accuracy were significantly lower than that reported in the present work (77.7% and 88.3% respectively). Yao et al.33, reported a significantly lower sensitivity of 3-D ultrasound in defining severe carotid stenosis with a value of 65% despite a specificity of 100%. Hence, our present study reports significantly higher overall diagnostic accuracy as compared to the results of both Kozàkovà et al.34, and Yao et al.35.

                On the other hand, Bendick et al.15, reported that the sensitivity of 3D imaging in the detection of more than 70 % diameter reduction was 100 % and specificity of 81%. This is a comparably higher sensitivity as compared to ours (94%).

                In a study by Kozàkovà et al.32, they found that the intermediate carotid artery stenosis ranging be­tween 40% and 70% was overestimated by 3D power Doppler ultrasound to be a higher degree of stenosis. Similarly, Bendick et al.15, found that in the degree of stenosis of > 70%, 8 from 26 (31%) vessels were not correctly categorized. All were measured to be a greater degree of narrowing by 3D power Doppler imaging.

                However in our present study, a single case out of the 23 (4.5%) diagnosed as stenosis ranging between 50-69.9 % diameter reduction was overestimated to be stenosis ranging between 70- 99.9% diameter reduction. Moreover, in the 11 stenosis diagnosed to be in the range of > 70%, none was overestimated. Only one case was underestimated to be a lower degree of stenosis.

                Keberle and his colleagues31 demonstrated in their study, that in respect to the length of the stenosis and the extension of the lesion through the bifurcation into the internal carotid artery, the results assessed by the reconstructed 3D volume survey showed a significantly positive correlation to those determined by 2D duplex sonography (P< 0.01). This comes in agreement with the present work where a significant positive correlation was established between 2D duplex sonography and 3D Power Doppler as regards the length of the stenosis and the extension of the lesion through the bifurcation into the internal carotid artery (P< 0.001). Our results however showed that 3D power Doppler scanning detected significantly shorter lesions with a mean of 13.32±5.92 mm as compared to 2D color duplex with a mean of 14.27±6.44 mm (P<0.001). Hence from our results we concluded that 3D power Doppler tends to underestimate the length of the lesion and the extension of the lesion into the bifurcation.

Bendick et al.15, demonstrated in their study that 3D power Doppler imaging correctly identified 11 of 13 (85%) as focal lesions, 24 of 29 (83%) as being moderate extent of < 1 cm, and 14 of 14 (100%) as lengthy extended lesions of more than 1 cm. Hence our results show a significantly higher diagnostic accuracy in estimation of moderate and focal lesions and a significantly lower accuracy in estimating lengthy lesions than the results reported by Bendick et al.15. However, whether the diagnostic errors were made by Bendick et al.15, were over or underestimations of the extension of the lesion in the carotid bifurcation are not mentioned in their report.

                The presence of significant calcifications in the atheromatous plaque makes ultrasound visualization and quantitative evaluations unreliable .This was a limiting factor in 1.6 % of our cases. However Bendick and his contributors15, found this limiting factor in a significantly larger (5%) of the vessels evaluated.

     So problems of the 2-D ultrasound could not be entirely overcome by 3-D reconstruction. For instance, image quality of 2-D ultrasound could not be improved by 3-D reconstruction34. Sonograms contain more mottle than comparable MR images, and this is not altered by 3D reconstruction35.

                The 2D TOF MRA method is more sensitive to slower flow, while the 3D TOF method depicts a wide range of flow velocities that has shown greater accuracy in defining internal and external lumen morphology36.

                The limitation of both TOF techniques is some distortion of the carotid artery anatomy and the over estimation of the degree of stenosis in the presence of turbulent flow. The major advantages of contrast-enhanced (CE) MR angiography over 3D TOF MRA is the reduction of flow and patient-related movement artifacts, the good spatial resolution, and the large acquisition volume from the aortic arch to the circle of Willis. This allows a good estimation of the degree of carotid stenosis, a differentiation between occlusion and pseudo-occlusion, more ac­curate in diagnosing plaque ulcers and detection of tandem stenosis, which is important for clinical and therapeutic management37.

                Our results showed that the sensitivity of 3D CE-MRA imaging to 50 - 70% diameter reduction was 93.8% with a sensitivity of 100% and a diagnostic accuracy of 98.5%. These results are significantly better than that reported in the study done by Serfaty and his colleagues24, who detected sensitivity and specificity of 94% and 85% respectively for 3D gadolinium-enhanced MR angiography. They reported that all false-positive cases resulted from overestimations of intermediate stenosis (50-70%), which lower specificity. So they concluded that quantification of stenosis of 50 - 70% is inaccurate using MR angiography techniques36. This is in contrast to our results where only one case of the 23 (4.3%) diagnosed as 50-69% stenosis was underestimated to be 30-49% stenosis. From our results we hence withdrew opposite conclusions that MR angiography technique is a reliable and accurate method in estimation of carotid artery stenosis of intermediate severity (50-70%).

                Remonda et al.36, showed in their series, the presence of agreement between 3D CE-MR angiography and 2D duplex sonography in the group of severe stenosis (70–99%) was 93%. In three cases, a short severe stenosis of the extracranial internal carotid artery was underestimated with MR angiography. In six cases, a 60–67% internal carotid artery stenosis was overestimated (71–84%) with CE-MR angiography. In our study we found that one out of the 11 cases in the group of severe stenosis (70–99%) was underestimated to be a moderate stenosis (50-69%) with 100% specificity and 98.7% sensitivity.

                Kallmes et al.37, reported that the problem is to find a technique that can distinguish moderate stenosis (30-69%) from high-degree stenosis (>70%). Our study shows that such a distinction was reliably done using CE-MRA. So we concluded form our study that CE-MR angiography is accurate enough to replace conventional angiography in diagnosing severe (> 70%) stenosis.

                Depicting ulcers is of great importance and has significant applications because the North American Symptomatic Carotid Endarterectomy Trial21 showed three folds greater risk of cerebral ischemia in patients who present with a deep ulcer with a high­-grade stenosis. Saouaf and his colleagues39, found in their study that four ulcerations were detected on CE-MRA and no definite ulceration was detected by DUS. In our study three ulcerations were detected By CE-MRA, one of them was neither identified by 2D color Doppler sonography nor 3D power Doppler scanning.

                 Ulcerations have been detected with MRA but with tremendous variability between readers and a lower sensitivity (22%) when com­pared with DUS. All have lower sensitivity than ulceration found in the pathological speci­men 40.

                As regards carotid occlusions, the small number of cases diagnosed did not enable us to reach a conclusion. However, the cases we did evaluate suggest a high accuracy for 3D gadolinium-enhanced MR angiography for diagnosis of carotid occlusion which coincides with the results of Remonda et al., and Leung et al.41. 

                Further correlation of 3-D images with opera­tive specimens at the time of endarterectomy may pro­vide additional data on this aspect of stenosis assess­ment. In the present work 10 of the studied patients underwent endarterectomy and the operative data regarding the severity of stenosis reported by the surgeon concedes with both 3D power Doppler and CE-MRA imaging techniques with an over all accuracy of 90%.

                Three  Patients who  underwent intervention either endarterectomy or intraluminal balloon dilatation and stent placement were followed up by 2D duplex sonography , 3D power Doppler imaging and 3D CE-MRA and we found that the findings by 2D duplex sonography coincided with the 3D power Doppler and 3D CE-MRA  data .

                This may have important clinical implications in serial follow-up studies. For example, it may provide a reliable method for serially observing the progression or regression of a plaque and/or changes in the severity of stenosis in a segment of the carotid artery. It may also provide a reliable method in follow-up studies after interventional procedures, such as carotid endarterectomy or endoluminal stenting, to observe the local vessel change, plaque reformation, or stent dysfunction, such as inadequate expansion or recoil41.

 

Limitations of the Study

                We did not compare 3D power Doppler sonography and 3D contrast enhanced TOF MR angiography to conventional angiography. However, the results of several comparative studies have shown that color Doppler sonography is highly reliable42. Carotid angiography remains associated with a substantial number of risks and potential complications. Whereas mortality is low, the frequency of neurological events varies from 0.45% to 2.6%. In contrast, MR imaging and MR angiography have no known adverse effects and contrast-enhanced MR angiography has a low complication rate36.

                 Carotid duplex sonography is used as a first-line investigation so that most patients do not undergo conventional angiography 43&44.  In our institution a similar protocol is followed, so angiographic correlation was performed in a selected number of pa­tients (25%).

                The present study suggests the following work up for patients who are advised for carotid artery evaluation: A 2D duplex scanning should be performed and if any abnormality is detected, we can proceed in the same setting to perform 3D power Doppler reconstruction as it provides more information of the anatomical location and the lesion morphology. However if the Doppler-Duplex study shows significant stenotic lesions, suspected ulcerated plaques, heavily calcified plaques, or suspected tandem lesions  we may proceed to perform 3D CE-MR angiography. Contrast angiography is thus only reserved for the rare patients with non diagnostic CE-MRA quality.

 

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الملخــص العربـــى

 

دور التصوير - ثلاثى الأبعاد – فى تشخيص وعلاج السكتات الدماغية

 

تبينت أهمية التصوير الطبي للشرايين بعدما  تقدمت  الطرق الجراحية وغير الجراحية  لتوسيع ضيق الشرايين, وخاصة الشريان السباتى لما ينتج عن آفاته من  آثار سلبية على وظائف المخ.

ويعتبر التصوير الشرياني بحقن الصبغة معيار أساسي ووسيلة مؤثرة  لفحص الشرايين . ثم ظهرت وسائل فحص الشرايين غير التداخلية مثل الفحص بالدوبلر الملون, الأشعة المقطعية و التصوير بالرنين المغناطيسي لتلافى بعض المضاعفات التداخلية والآثار الجانبية لتصوير الشرايين بعد حقن الصبغة وقد أثبتت هذه الوسائل كفاءتها واصبح الدوبلر الملون يستخدم الآن كفحص أساسي لاختبار المرضى المحتاجين لجراحة توسيع الشرايين ومتابعتهم.

في البداية كانت الصور الناتجة عن هذه الوسائل ثنائية الأبعاد, ثم استحدثت مؤخرا الصور ثلاثية الأبعاد لمعالجة قصور الصور ثنائية الأبعاد وتهدف هذه الدراسة تقييم دور بعض وسائل التصوير الطبي ثلاثي الأبعاد الأقل تداخلا, مثل فحص الموجات الصوتية بالدوبلر المقوى والتصوير الشرياني بالرنين المغناطيسي مع حقن الصبغة في تشخيص آفات الشريان السباتى لمعرفة فوائدها وبيان مستجداتها مقارنة مع الفحص ثنائي الأبعاد.

وقد اشتملت الدراسة الحالية على 60 مريض (39 ذكر و 21 أنثى), متوسط عمرهم  59.1 عام ويعانون من أعراض قصور الشريان السباتي آو تقدموا لفحص الشرايين السباتيه لسبب آخر (فحوصات ما قبل الجراحة) كل المرضي تم فحصهم بواسطة الدوبلر الملون ثنائي الأبعاد علي الشرايين السباتيه, ثم بواسطة الدوبلر المقوي ثلاثي الأبعاد و أيضا  بواسطة التصوير الشرياني بالرنين المغناطيسي مع حقن الصبغة ثلاثي الأبعاد.

ووجد انه تتنوع إصابة الشريان السباتى بهم بين الضيق بدرجاته المختلفة وتقرحات جدار الشريان وانسلاخه و كذلك  تمدده.

ومن هذه الدراسة نستنتج إن الدوبلر المقوي ثلاثي الأبعاد و التصوير الشرياني بالرنين المغناطيسي بالصبغة ثلاثي الأبعاد يمكن استخدامهما كوسائل تكميلية مع الدوبلر الملون ثنائي الأبعاد تشخيص آفات الشريان السباتي. وإن التصوير الشرياني بالرنين المغناطيسي مع حقن الصبغة هو الطريقة التصورية الأكثر دقة في تشخيص قرح الشرايين السباتيه. 

ولهذا ينصح باستخدام الفحص بالدوبلر المقوي ثلاثي الأبعاد عندما يظهر الفحص ثنائي الأبعاد وجود علامات مرضيه بالشريان السباتي لاظهار المزيد من المعلومات. ويستخدم التصوير الشرياني بالرنين المغناطيسي مع حقن الصبغة ثلاثي الأبعاد في  الحالات آلتي بها ضيق متقدم أو اكثر من ضيق متلاحق أو اشتباه في قرح شريانيه.

 



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