Extracranial carotid doppler correlation to multidetector CT angiography in ischemic stroke patients

Received 21 August 2017 Revised 08 September 2017 Accepted 01 October 2017 Early online 31 January 2018 Print 31 January 2018 The purpose of this study was to compare the diagnostic value of Color Doppler Ultrasound (CDUS), Computed Tomographic Angiography (CTA), and advantage of their combined use in defining the degree of stenosis and morphological character of atheromatous plaque in ischemic stroke patients. This was a cross-sectional study with a total of 60 patients having 120 carotid arteries were observed. The percentage of stenosis was measured at the narrowest point by modified NASCET criteria for both CDUS and CTA. Incidence of stroke was highest in the age group 50-70years with male population commonly affected. Frequency of carotid stenosis was more in male patients aged above 60 years. Hemiparesis was most common symptoms in stroke patients. The various risk factors of carotid atherosclerosis and stenosis included hypertension, diabetes mellitus, hyperlipidemia and cardiovascular disease. Atheromatous plaques with stenosis were most commonly found on right side. Carotid bifurcation was the common site for atheromatous plaque .There was significant correlation between Color Doppler Ultrasound and Computed Tomographic Angiography for detecting 70-100% stenosis. However CTA is more accurate in comparison to duplex ultrasonography in detecting 70-99% stenosis and total occlusion. There was no significant correlation between CDUS and CTA in detecting 20-49% stenosis. Duplex ultrasonography is more sensitive in detecting these lesions. Out of 49 plaques, in this study 11 were soft plaques, 26 were non-homogenous and 13 were ulcerative plaques. Color doppler has better role in plaque characterization. Besides degree of extracranial stenosis, length of the stenosis, site of intracranial stenosis and total number of stenotic sites are better assessed by CTA. Area of effected brain parenchyma and extent of collateral circulation are better assessed by CTA which aids in prognostic value. In conclusion, the advantage of the combined use of CDUS and the CTA in the identification and quantification of ICA stenosis is higher. However ultrasound had a better role in plaque characterization. Corresponding author

The purpose of this study was to compare the diagnostic value of Color Doppler Ultrasound (CDUS), Computed Tomographic Angiography (CTA), and advantage of their combined use in defining the degree of stenosis and morphological character of atheromatous plaque in ischemic stroke patients. This was a cross-sectional study with a total of 60 patients having 120 carotid arteries were observed. The percentage of stenosis was measured at the narrowest point by modified NASCET criteria for both CDUS and CTA. Incidence of stroke was highest in the age group 50-70years with male population commonly affected. Frequency of carotid stenosis was more in male patients aged above 60 years. Hemiparesis was most common symptoms in stroke patients. The various risk factors of carotid atherosclerosis and stenosis included hypertension, diabetes mellitus, hyperlipidemia and cardiovascular disease. Atheromatous plaques with stenosis were most commonly found on right side. Carotid bifurcation was the common site for atheromatous plaque .There was significant correlation between Color Doppler Ultrasound and Computed Tomographic Angiography for detecting 70-100% stenosis. However CTA is more accurate in comparison to duplex ultrasonography in detecting 70-99% stenosis and total occlusion. There was no significant correlation between CDUS and CTA in detecting 20-49% stenosis. Duplex ultrasonography is more sensitive in detecting these lesions. Out of 49 plaques, in this study 11 were soft plaques, 26 were non-homogenous and 13 were ulcerative plaques. Color doppler has better role in plaque characterization. Besides degree of extracranial stenosis, length of the stenosis, site of intracranial stenosis and total number of stenotic sites are better assessed by CTA. Area of effected brain parenchyma and extent of collateral circulation are better assessed by CTA which aids in prognostic value. In conclusion, the advantage of the combined use of CDUS and the CTA in the identification and quantification of ICA stenosis is higher. However ultrasound had a better role in plaque characterization. troke is one of the leading causes of death more often disabling than fatal. Ultrasonography remains the most accurate noninvasive modality for evaluation of carotid artery disease. It provides information about the degree of carotid stenosis, the velocity and character of blood flow and plaque morphology 3 . However there are several pitfalls that may mislead the operator to falsely interpret the color and spectral doppler findings.
The purpose of this study was to estimate the diagnostic value of extra cranial carotid and vertebral artery doppler and Computed Tomography Angiography, to delineate the pitfalls during imaging, interpretations and limitations of Color Doppler Ultrasound, their combined use (CDUS+CTA) in the detection and quantification of severe ICA stenosis and to detect an established and preventable cause of stroke, which may subsequently help to plan future treatment modality (medical /surgical) for prevention of further cerebrovascular events.

Material and methods
This was a cross sectional study on a consecutive series of patients. A total of 60 patients (120 carotid arteries) having transient ischemic attack (TIA), reversible ischemic neurologic deficit (RIND), prolonged ischemic neurological deficit (PIND), or cerebrovascular insults (CVI) admitted to S. C. B. Medical college & Hospital, Cuttack were included in this study. The patients included were of both sexes and age above 18 years.
Patients previously operated on for carotid disease, those with already verified thrombosis in the left ventricle and/or in auricle, patients with verified brain tumors, patients with intracerebral hemorrhage, patients allergic to contrast agents, patients with abnormal renal function were excluded from this study.
The risk factors were evaluated by history, physical examination, echocardiogram and laboratory investigations during hospitalization. These included age, sex, hypertension, diabetes mellitus, hyperlipidemia, smoking and ischemic heart disease.
Ultrasonographic examination was performed with a GE pro-6 machine. Arteries were studied under grey scale, color and spectral waveform using high frequency (3-12MHz) linear probe. The percentage of stenosis was evaluated by the use of the modified NASCET (North American Symptomatic Carotid Endarterectomy Trial Collaborators, 1991) criteria (formula 100 x (A-B)/A). CTA examination was performed with GE 128 MDCTA. 70-100 ml of contrast material was injected intravenously at a flow rate of 4ml/sec with a power injector in right subclavian vein using 18 gauge needle. For optimal timing of the bolus, the bolus tracking method was used. MDCT angiography was performed using following parameters: 100kVp, 180-300mAs, 10mm collimation, 17.5mm/rotation table feed and 0.8sec rotation time. The images were reformatted with a section thickness of 0.625 mm and 3D MIP and VR images were obtained. The percentage of stenosis was evaluated by the use of both axial and coronary maximum intensity projection (MIP) and shaded-surface display (SSD) imaging.

Results
Majority of the patients in this study belonged to the age group of 50-70 years constituting about 70% of the total study population. Median age of presentation is 61 years. The highest numbers of carotid artery stenosis in our study were found in the age group of 61-70 years which was followed by 51-60 years of age group. Thus incidence of extracranial stenosis was more in age above 60 years.
In our study 41 patients (69% of total patients) having hypertension. Out of them stenosis was present in 28 cases. So 68% of hypertensive patients showed carotid stenosis. Out of 28 cases 24 were males and 4 were females. 33 patients (55% of total patients) were having diabetes, out of them stenosis was present in 22 cases. So 66% diabetic patients showed carotid stenosis. Out of 22 cases 19 were males and 3 were females (Table 1).  Carotid plaque surface ulceration is known as a strong predictor of future embolic stroke risk. Plaque ulceration is defined as an intimal defect larger than 1000µm in width, exposing thrombogenic layers of the plaque such as the necrotic core, with the possibility of a subsequent thrombus adhering to the plaque which further leads to embolization. In our study 16 ulcerative plaques were detected by doppler and 13 ulcerative plaques were detected by CTA in 37 stenotic patients. 23 plaques in USG and 18 plaques in CTA showed irregular surface which well correlate with the study. There are 9 calcified plaques noted in both types of investigation among total 49 plaques. Calcified dense plaques are more stable and there is less risk of becoming symptomatic.

Discussion
The word stroke implies brain cell death caused by infarction resulting in deficit enduring for days or longer. The deficit may be fleeting, in which case the cell death presumably does not occur. Such a brief episode is termed as Transient ischemic attack (TIA). For epidemiological reasons, focal neurological dysfunction of duration < 24 hours is termed as TIA. A longer lasting deficit with full recovery within three weeks is termed as Reversible ischemic neurological deficit (RIND). Treatment of stroke depends on reaching the earliest possible diagnosis possible through clinical and laboratory evaluation.
Though angiography is the gold standard, it is invasive and immoderate and involves significant risk to the patients. Sonography is unique among vascular imaging procedures, in that it can assess plaque composition. Sonographically detected plaque characteristics may have prognostic value and may be useful for the selection of medical and surgical therapy.
Our present study consists of evaluating extra cranial carotid artery system in 60 patients with color doppler (CDUS) and contrast enhanced computed tomographic angiography (CTA). A study by Dae Suh et al 4 considered 268 patients (219 male, 49 female; mean age 56 years) which was also consistent with our findings. The risk factors for cervical atherosclerosis was studied by Palomaki et al 5 in patients with ischemic stroke and transient ischemic attack and found that incidence of stroke increases after 60 years of age. These findings also correlate well with Thomas et al 6 and Mathiesen et al 7 results wherein prevalence of and risk factors associated with carotid artery stenosis were also consistent with our findings.
In this study 70% (42 of 60) patients were males and 30% (18 of 60) patients were females. Lemolo et al 8 in his study showed that majority of stroke victims were males. 68% of hypertensive patients show carotid stenosis and the findings correlated with Su et al 9 study who studied the trends of carotid plaque formations by the status of blood pressure. About 53% of hypertensives were observed to have plaques while the corresponding values decreased to 41% for borderline hypertensives and to 34% for normotensives 9 .
Studies 10,11 found that the carotid bifurcation was commonly involved by the atherosclerotic plaque followed by the origin of carotid. Rubba et al 12 also showed bulb as the most common site of plaque. In this study bulb was effected in 45% (22 out of 49).
The findings of study by Savic et al 13 titled 'Correlation of color doppler with multidetector CT angiography findings in carotid artery stenosis' correlated well with our study.
Out of 60 stroke patients 49 (82%) patients have thickened carotid intima medial thickness (IMT) in USG. This finding correlates with Harris study, in which 259 patients, with age ranging from 31 to 75 years old, were divided into the stroke group (n=131) and non-stroke group (n=128). The author found abnormal IMT in both age groups, with an occurrence of 130 patients in the stroke group and 46 in non-stroke group 14 .
Langsfeld et al 15 studied 419 asymptomatic patients with atherosclerotic plaques for 15-22 months and found anechoic plaques more vulnerable to be at increased risk of stroke compared with dense and echogenic plaques (p<0.02). In another study, O'Holleran et al followed 293 patients for an average of 46 months and showed that 100% of the patients with a soft lesion involving > 75% stenosis became symptomatic as compared with only 60% (p>0.05) of those with a dense plaque 16 .
Our study results were consistent with Sterpetti and colleagues, who found new neurological events occurring in 19 out of 71 carotid arteries (27%) with heterogenous plaques, where as only 6 carotid arteries out of 167 (4%) shows new events with homogenous plaques (p<0.001) 17 . Sitzer et al 18 showed that plaque ulceration and lumen thrombus are the main sources of cerebral microemboli in high-grade internal carotid artery stenosis.
In our study, 16 ulcerative plaques were detected by doppler and 13 ulcerative plaques were detected by CTA in 37 stenotic patients. 23 plaques in USG and 18 plaques in CTA showed irregular surface which correlated well with the study by Eliasziw et al 19 who studied the association between angiographically defined plaque ulceration and risk of subsequent stroke in 659 patients with severe stenosis (70-99%) enrolled in North American Symptomatic Carotid Endarterectomy trial. The study shows that in unoperated patients with 85% stenosis due to ulcerated plaque the risk of ipsilateral stroke at 24 months is high (43.9%) in comparison to non ulcerated 85% carotid stenosis, the risk of ipsilateral stroke at 24 months was 21.3%. In patients with 95% carotid stenosis the 2year risk of ipsilateral stroke was 73.2% in patients with ulcerated lesions and 21.3% in patients without evidence of ulcer (p=0.005). This was also analyzed in the ECST trial 20 which showed that stroke risk was increased among patients with irregular plaques for all degrees of stenosis, and that the association was also independent of other clinical and angiographical factors. In 1992, Steinke et al 21 reported 63 patients with higher degree of stenosis in ultrasound and that ulcerated plaques were more frequently found among symptomatic (43%) than asymptomatic patients (23%).
In Zarei et al 11 study stenosis of extracranial and intracranial arteries were detected in 38% and 29% of cases respectively. The extracranial stenosis was significantly more frequent than intracranial stenosis (p<0.01). In this study out of 60 ischemic stroke patients, 22 patients had extracranial, 13 had intracranial, 14 had both extra and intracranial stenosis and 11 patients were without stenosis. This study also showed 39 stroke patients had collateral circulation detected in CTA and the collateral status is a useful predictor for clinical outcome in acute stroke patients.

Conclusion
The results of our study suggest that the combined use of CDUS and CTA is an acceptable method for quantification of severe carotid artery stenosis. CDUS is non-invasive, affordable, safe, reproducible, less time consuming and easily available method of demonstrating extra-cranial carotid artery system. It is more accurate in evaluation of plaque morphology. However it is relatively insensitive in stenosis quantification and not reliable diagnostic method in high set carotid bifurcation, heavily calcified arterial wall, short neck, obesity, presence of edema, scar after irradiation or when changes in the distal part of the artery are not available to ultrasound review, where MDCTA is advantageous. The accuracy of the ultrasound examination is strongly dependent on the skills of the examiner.
CTA with perfusion have become a choice of modality for accurate and prompt diagnosis of cause of cerebral ischemia. The site of arterial occlusion, percentage of stenosis of extracranial as well as intracranial carotid artery, length of occlusion and pattern of poorly perfused brain tissue and extent of collateral circulation can be better assessed by CTA which is operator independent.