Long-term radiographic outcomes of microemboli following carotid interventions

Article Outline

• Abstract
• Material and methods
  • General design
  • Selection criteria for carotid interventions
  • Carotid revascularization procedures
  • MRI protocol
  • Image analysis
  • Statistical analysis
• Results
  • Clinical outcomes
  • Follow-up evaluations
• Discussion
• Author contributions
• References
• Copyright

Objective

Subclinical microemboli on diffusion-weighted magnetic resonance imaging (DWI) have been identified immediately following carotid revascularization procedures, but the clinical significance and long-term effects are largely unknown. The purpose of this study was to evaluate long-term radiographic outcomes of these DWI lesions.

Methods

Patients who underwent perioperative magnetic resonance imaging (MRI) evaluations for carotid interventions at a single institution from July 2004 to December 2008 were evaluated, particularly those who had additional follow-up MRI. DWI with apparent diffusion coefficient (ADC), fluid-attenuated inversion recovery (FLAIR), and T2-weighted MRI images were compared to determine long-term effect of microemboli.

Results

One-hundred sixty-eight consecutive patients (68 carotid artery stenting [CAS] and 100 carotid endarterectomy [CEA]) who received perioperative MRI were included. All CAS were performed with an embolic protection device. The incidence of microemboli was significantly higher in the CAS group than the CEA group (46.3% and 12%, respectively, P < .05) despite a relative low incidence of procedure-associated neurologic symptoms in both groups (2.9% vs 2%). Thirty patients (16 CAS and 14 CEA) who had follow-up MRI were further analyzed and a total of 50 postoperative DWI lesions (mean size 46.57 mm²; range 16 to 128 mm²) were identified among them. During a mean MRI follow-up of 10 months (range, 2 to 23 months), residual MRI abnormalities were only identified in DWI lesions larger than 60 mm² on postoperative MRI and on postoperative FLAIR images (n = 5, P < .001). The CEA group had fewer but larger ipsilateral distributed emboli (total 12 lesions, mean 79 mm²) compared with the CAS group (total 38 lesions, mean 27.5 mm², P < .05).

Conclusions

The majority of microemboli do not have long-term radiographic sequelae. Size and hyperintensity on postoperative FLAIR are predictive of residual brain structure abnormality, and further neurocognitive evaluations are warranted.

Stroke is the most common cause of permanent disability and remains the third leading cause of death in industrialized countries.¹ Carotid artery stenting (CAS) and carotid endarterectomy (CEA) are commonly performed revascularization procedures to prevent stroke in patients with severe carotid artery stenosis. Although distal embolization is a well-recognized procedural complication during carotid interventions, only clinically evident embolization resulting in neurologic sequelae is routinely evaluated as an outcome measure; subclinical microemboli have not been fully assessed.

Magnetic resonance imaging (MRI) offers extensive useful data by delineating the anatomy and brain pathology. A diffusion-weighted magnetic resonance image (DWI) sequence in combination with apparent diffusion coefficient (ADC) map allows visualization of ischemic regions within minutes of symptom onset (hyperacute phase) and has shown to be a reliable imaging modality with a high sensitivity (88% to 100%) and specificity (95% to 100%) detecting microembolic events associated with carotid interventions.², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹² We also showed consistent readings among experienced neuroradiologists with a low interobserver variability.¹⁰, ¹¹ Multiple studies have demonstrated that subclinical embolization detected on DWI during percutaneous carotid interventions is not uncommon despite absence of neurologic symptoms.⁶, ⁷, ⁹, ¹¹, ¹³, ¹⁴, ¹⁵ However, whether microemboli are clinically significant is largely unknown.

To determine long-term clinical manifestation of microemboli, it is important to first evaluate whether DWI lesions lead to persistent brain structure abnormality on MRI. There is very limited information evaluating long-term radiographic outcomes of microemboli. Palombo and colleagues longitudinally evaluated 30 DWI lesions in 13 patients following CAS procedures and concluded that reversibility of microemboli significantly depended on sizes and locations of the lesions.¹⁶ In this study, we examined 50 procedure-related DWI lesions to evaluate long-term radiographic outcomes of these lesions and to determine characteristics of DWI lesions that lead to residual brain structure abnormality.

In addition to DWI sequence, several other MRI sequences were utilized to determine long-term radiographic effects of microemboli. Fluid-attenuated inversion recovery (FLAIR) is thought to be more sensitive than conventional T2-weighted (T2W) MRI for detecting lesions in the brain of patients with certain ischemic diseases. For follow-up evaluation, T2W and FLAIR images, along with DWI sequence, were used in our study to identify old insults and to detect residual effects of microemboli on follow-up MRI.

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Material and methods 

General design 

All patients who underwent carotid interventions, including both CAS and CEA patients, from July 2004 to December 2008 were retrospectively reviewed. All procedures were performed by vascular surgeons at Stanford University-affiliated VA Palo Alto Health Care System (VAPAHCS). Carotid duplex scan was performed prior to the revascularization procedures and high-grade carotid stenosis was documented in all patients. Patients with symptomatic carotid stenosis 70% or greater and asymptomatic carotid stenosis 80% or greater were considered for revascularization procedures. The majority of the patients also received perioperative MRI evaluations under standard protocol that has been approved by Stanford Institutional Review Board (IRB) and VAPAHCS R&D section. In addition to standard MRI stroke protocol, the preoperative MRI protocol included three-dimensional gadolinium-enhanced MR angiographic scan of the aortic arch, carotid and vertebral arteries, and circle of Willis (COW) to delineate arterial anatomy and confirm stenosis. Patients with both pre- and postoperative MRI images were examined and only patients who had additional follow-up MRI were included in the study to determine long-term radiographic outcome of postoperative DWI abnormalities. Each DWI lesion was individually evaluated by a neuroradiologist (B.L.) and a trained rater (D.D.) to determine locations, size, and reversibility.

Selection criteria for carotid interventions 

Both symptomatic and asymptomatic patients with high-grade carotid stenoses were involved. Decision on CAS was made collaboratively among internists and vascular surgeons following the standard practice protocol. Eligibility for high-risk patients undergoing CAS was largely based on criteria established at consensus conferences including various anatomical considerations, such as high carotid bifurcation (>C2 level), presence of tracheostomy, history of ipsilateral neck irradiation, prior radical neck dissection, or carotid endarterectomy.¹⁷ The high risk criteria also included patients with one or more medical comorbidities, such as those who had myocardial infarction in the previous 3 months. High-risk pulmonary dysfunction includes patients with steroid-dependent chronic obstructive pulmonary disease, or measured forced expiratory volume in 1 second less than 30% of predicted or less than 1 L/s. The majority of the patients routinely underwent cardiac evaluation including persantine-thallium nuclear stress test or a trans-thoracic echocardiogram, and cardiology evaluation was obtained for those with abnormal cardiac studies.

Carotid revascularization procedures 

The preoperative anticoagulation regimen for all patients consisted of aspirin 81 mg. Patients who underwent CAS also received a loading dose of clopidogrel 300 mg prior to the procedure or daily dose of 75 mg for 1 week prior to CAS. Carotid endarterectomy with patch angioplasty was performed under general anesthesia using a standard protocol with routine usage of a shunt device. Type of patch and shunt were at the discretion of the individual surgeon. Patients were admitted to the surgical intensive unit for observation and postoperative MRI evaluations were performed before they were discharged home the following day on daily aspirin.

All CAS procedures were performed in an endovascular suite (GE Medical Systems, Milwaukee, Wis) with routine use of embolic protection device (EPD). An anesthesiologist was present to monitor the blood pressure as recorded by an arterial line. Oxymetry and continuous electrocardiography (ECG) were similarly monitored. The technical details of CAS have been described in our previous studies.¹⁸, ¹⁹ Briefly, a 6F, 90-cm carotid guiding sheath was secured in the distal common carotid artery, and a selective digital carotid angiogram was then performed via the sideport of the guiding sheath. An appropriate EPD and stent device were selected based on length and morphology of the lesion as well as diameter of the CCA and ICA. EPD used included FilterWire system (micropore size: 110 μ), ACCUNET (micropores size: 115 μ), Angioguard (micropore size: 100 μ), or Emboshield (micropore size: 140 μ) at the discretion of the intervening physician. Following activation of the EPD, a coaxial angioplasty balloon was used to pre-dilate the carotid lesion if necessary. Next, an appropriate self-expanding FDA-approved monorail carotid stent was deployed across the internal carotid stenosis. The stents used included ACCULINK (Guidant Inc, Sunnyvale, Calif), Precise (Cordis Corporation, Warren, NJ), and Xact (Abbott Vascular, Redwood City, Calif). Post-stenting balloon angioplasty was performed for over 20% residual stenosis. Completion carotid angiogram was performed prior to capture of the EPD to document the satisfactory result of the intervention and to exclude thromboembolism proximal to the EPD. After the EPD was captured, two-view cerebral angiograms were obtained. Lastly, the groin puncture sites were routinely closed with a closure device (Perclose or StarClose, Abbott Vascular Devices, Redwood City, Calif). Following CAS procedures, the patient was transferred to an intensive care unit with close hemodynamic monitoring. When stable, the patient underwent postoperative MRI before being discharged home the following day on life-long aspirin and 6 weeks of daily clopidogrel.

MRI protocol 

MRI studies were performed within 1 to 2 weeks prior to carotid revascularization procedures and within 48 hours after the procedure on a 1.5-T scanner (Signa Excite HD 12.0; GE Medical Systems) equipped with a head coil. The brain was scanned, utilizing multiple pulse sequences in the axial, sagittal, and coronal planes both before and after contrast administration. The MRI scans routinely included sagittal and axial spin-echo (SE) T1W, axial and coronal fast-spin echo (FSE) T2W, FLAIR, DWI, and post-contrast spin-echo T1W sequences. The intracranial vessels were imaged using three-dimensional (3D) time-of-flight (TOF) MRA techniques, and the extracranial carotid and vertebral arteries were imaged utilizing pre-contrast 2D TOF and post-contrast 2D MRA techniques.

DWI was acquired with an echo-planar sequence. An isotropic axial sequence is used: TR 12000; TE minimum 76, 128 × 128 matrix, FOV 30, 5 mm slices no gap, with b values of 0 and 1000 s/mm²). An ADC map was automatically generated. The DWI was evaluated by an experienced neuroradiologist (B.L.) who was blinded to the procedural status of the patients. Presence of new hyperintensity on DWI with corresponding decreased ADC in the brain was interpreted as a new ischemic lesion (microembolic lesion). Microemboli are recorded in terms of location, size, and number of counts for all examinations performed.

A total of 30 patients who also had follow-up MRI were further evaluated. Specifically, DWI, T2W, and FLAIR sequences were compared to determine long-term outcome of microemboli on MRI. Acquisition sequences were consistent among all MRI studies for stroke protocol. Axial T2W images were acquired with these parameters: TR 6000, effective TE (TEef) 102, echo train (ET) 12, slice thickness 3 mm, spacing 3.5 mm, total slices 45; matrix 256 × 192, FOV 24. Coronal T2W oblique, perpendicular to hippocampus: TR 5000, TEef 102, ET 10, slice thickness 3 mm @ 4 mm, matrix 256 × 192, FOV 20; FLAIR images were acquired with the following parameters: TR 9000, TE 140, inversion time (TI) 2200, slice thickness 5 mm @ 7.5 mm, matrix 256 × 192, 22 slices total, FOV 24.

Image analysis 

MRI images were evaluated by a trained rater (D.D.) and a board certified neuroradiologist (B.L.) who was the primary interpreting neuroradiologist for multiple previous studies in our institutions over the last 6 years.¹⁰, ¹¹, ²⁰ Excellent inter-rater reliability has been demonstrated (R² = 0.99 and interclass correlation [ICC] = 0.971) between the two raters. For patients with additional long-term follow-up MRI studies, DWI, FLAIR, and T2W sequences were analyzed and compared with pre- and postoperative MRI images to determine long-term radiographic effects of microemboli. Postoperative MRI images were compared with preoperative images to exclude pre-existing ischemic lesions. DWI images with ADC map were used to identify new embolic lesions associated with carotid revascularization procedures. Lesions were manually traced and the size of a lesion was calculated based on the largest cross diameter using an electronic caliper and a software package provided by GE Medical System. FLAIR and T2W were compared with preoperative/postoperative images and any new hyperintensity corresponding to the location of a postoperative new DWI lesion was defined as a residual lesion.

Statistical analysis 

Data analyses were performed by using STATA version 10.0 (Stata Corporation, College Station, Tex). Statistical analyses were performed by using the pooled Student t test and uncorrected Pearson χ² test. A Mann-Whitney U test was used when comparing characteristics of DWI lesions between CAS and CEA groups. A P value less than .05 was considered statistically significant.

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Results 

Clinical outcomes 

A total of 168 consecutive patients including 68 CAS patients and 100 CEA patients who received both pre- and postoperative MRI during a 53-month period were examined. The incidence of microemboli was significantly higher in the CAS group than the CEA group (46.3% and 12%, respectively, P < .05) despite low neurologic symptoms in both groups (2.9% in the CAS group and 2% in the CEA group). A total of 30 patients (16 CAS and 14 CEA) who also had follow-up MRI evaluations in addition to pre-and postoperative MRI images were included in the study. Among them, eleven CAS patients had 38 procedure-related DWI lesions. The average diameter of the lesions was 5 mm and the average size was 27.5 mm² (range, 15 mm² to 50.32 mm²) (Fig 1). A total of 12 new ischemic lesions were identified in five CEA patients on postoperative DWI and the average size of the lesion was 79 mm² (range, 30 mm² to 128 mm²). The CEA group had significantly fewer but larger ipsilaterally distributed embolic lesions than the CAS group based on Mann-Whitney U test (P < .001).

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• Fig 1. 

  A microembolic lesion associated with carotid revascularization procedure was demonstrated on diffusion-weighted magnetic resonance image (DWI).

Follow-up evaluations 

All 50 procedure-related lesions identified on postoperative DWI were individually analyzed. During a mean follow-up of 10 months (range, 2 months to 23 months), there was no residual hyperintensity on follow-up DWI in any lesions. No FLAIR or T2W abnormality was detected at the location of microemboli in 45 lesions, which suggested no evidence of permanent brain infarction. However, five lesions (10%), including four from the CEA group and one from the CAS group, led to hyperintense signals on FLAIR and T2W images at an average of 8 months (Range, 4 to 13 months) following revascularization procedures (Table I). Table I shows characteristics, locations, and manifestation of these five DWI lesions that had MRI evidence of residual brain infarction. They were significantly larger, with a mean area of 103.4 mm² (range, 84 mm² to 128 mm²), compared with those without residual MRI abnormality (23 mm², ranging 15 mm² to 50.3 mm²)(P < .001) (Fig 2, a). These five lesions were all located ipsilaterally to the intervened carotid arteries and distributed in both cerebellum and cerebral cortical and subcortical areas including cerebellum (n = 1), frontoparieal (n = 2), frontal lobe (n = 1), and parietal lobe (n = 1). Interestingly, all five lesions also had evidence of hyperintensity on postoperative FLAIR (Fig 2, b). Hyperintense areas on follow-up FLAIR and T2W were smaller than the area indicated on postoperative FLAIR.

Table I. Five postoperative DWI lesions associated with residual radiographic abnormalities

DWI, Diffusion-weighted magnetic resonance image; MRI, magnetic resonance imaging; CAS, carotid artery stenting; CEA, carotid endarterectomy; TIA, transient ischemic attack; HVS, hyperintense vessel sign; FLAIR, fluid-attenuated inversion recovery.

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• Fig 2. 

  A large subclinical embolic lesion with residual radiographic abnormality was shown as a hyperintense signal on postoperative diffusion-weighted magnetic resonance image (DWI) (a) and hyperintensity postoperative FLAIR image (b).

Two of the five lesions resulted in neurologic symptoms in two patients, including one patient with a 92 mm² lesion in the right frontoparietal lobe complaining of fourth digit dysfunction during rapid typing process and the other one with a 120 mm² lesion in the left frontoparietal region who presented with mild aphasia. Both patients had symptom resolution during follow-up (Table II). All five persistent MRI lesions occurred in patients with preoperative symptoms, and four patients also had additional multiple small DWI lesions, including the two with neurologic symptoms. All concomitant small DWI lesions in these patients resolved at the time of follow-up. Further analysis showed that lesions smaller than 60 mm² in our patient cohort were not associated with long-term residual FLAIR or T2W abnormality despite coexistence with large DWI lesions. Location of the lesions did not show any influence on residual radiographic effects.

Table II. Follow-up evaluation of five persistent embolic lesions

DWI, Diffusion-weighted magnetic resonance image; FLAIR, fluid-attenuated inversion recovery.

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Discussion 

Subclinical microembolization detected on postoperative DWI are common during CAS procedures despite absence of clinical symptoms.⁶, ⁷, ⁹, ¹¹, ¹³, ¹⁴, ¹⁵ However, clinical effects of microemboli are largely unknown. In this study, we examined long-term radiographic outcomes of postoperative DWI-abnormalities and identified the characteristics of the lesions that lead to residual MRI abnormalities. Our study showed that only 10% of procedure-related DWI lesions were associated with residual MRI-evident brain structure abnormality. These lesions were significantly larger and all occurred in patients with preoperative symptoms. In addition to DWI abnormality, these lesions also showed hyperintensity on postoperative FLAIR images and frequently coexisted with multiple small DWI lesions. This study provided valuable information to our limited knowledge of subclinical cerebral microemboli and highlighted a unique opportunity for improving outcome of carotid revascularization procedures.

There are only a few studies that have evaluated long-term radiographic outcome of microemboli. Palombo and colleagues evaluated 30 DWI lesions in 13 patients undergoing CAS and showed 40% of lesions persisted during follow-up.¹⁶ The author concluded that reversibility rate depended significantly on the location and size of the lesion. Wolf and associates longitudinally examined 15 CEA patients with postoperative DWI abnormalities and showed that number and volume of DWI lesions after CEA were highly predictive of brain infarction.²¹ Hauth and colleagues examined 64 DWI lesions and demonstrated that only two lesions showed manifestation at 6-month MRI and that the two persistent lesions were also visible on postoperative T2W images.²² Consistent with others, we confirmed that the majority of postoperative DWI lesions had no long-term radiographic sequelae and that the size of lesions was predictive of reversibility. Unlike Palombo et al, we did not show association between the location of lesions and radiographic outcomes. Four out of five large DWI lesions were distributed in the cerebral cortical or subcortical regions, and one in the cerebellum. However, our study did suggest that location of the lesions might contribute to clinical presentations, as two symptomatic lesions were both located in the frontoparietal region. Among the five large lesions in our cohort, four also coexisted with multiple small DWI lesions, but none of the smaller DWI lesions (<60 mm²) was associated with abnormal signal on postoperative FLAIR sequence or had residual radiographic abnormality during follow-up, which indicated that smaller DWI lesions resolved over time.

DWI sequence has shown to be sensitive and specific in diagnosing acute cerebral infarction.² Although multiple embolic sources including cardiac and proximal carotid diseases may contribute to microemboli, our postoperative MRI images were compared with the preoperative images, which were performed 1 to 2 weeks prior to revascularization procedures to determine changes in all sequences. Presence of new hyperintensity on postoperative DWI with corresponding decreased ADC in the brain was interpreted as a new ischemic lesion. Therefore, these new postoperative DWI lesions were likely procedure-related.

FLAIR imaging is more sensitive than conventional T2-weighted imaging in detecting ischemic lesions by suppressing the signal from cerebrospinal fluid while providing a heavily T2-weighted image of brain parenchyma. Brant-Zawadzki and colleagues showed that the greatest benefit from FLAIR sequence was the detection of cortical gray matter infarcts.²³ It is not a surprise that larger DWI lesions also resulted in hyperintense signals on FLAIR sequence, as these embolic events likely occurred during revascularization procedures 24 to 48 hours prior to postoperative MRI studies. Subsequently, DWI lesions with corresponding hyperintensity on postoperative FLAIR led to persistent MRI abnormalities during follow-up, which indicated permanent brain structure damage.

Admittedly, this is a retrospective analysis of our prospectively collected database and there are several limitations with this study. In this study, we only examined 30 patients who already had additional follow-up MRI studies, and time of follow-up images varied from 2 months to 23 months. Two patients who developed transient neurologic symptoms following CAS in early years did not receive follow-up MRI and were not included in this study. Due to the natural aging process, we expected longitudinal brain structure changes on MRI among older adults. Therefore, repeat MRI long after revascularization procedures would not provide valid information on radiographic outcome of postoperative DWI abnormalities. Future prospective studies will be needed to include patients who have postoperative DWI lesions to thoroughly evaluate fates of all procedure-related DWI abnormalities. Although all postoperative DWI lesions showed hyperintense signal with corresponding decreased diffusion, suggesting procedure-related hyperacute ischemia, preoperative MRI were performed 1 to 2 weeks prior to carotid revascularization procedures and all five patients with persistent MRI lesions were symptomatic prior to interventions. Therefore, it is possible that there were new embolic events that occurred after preoperative MRI but prior to intervention procedures. These preprocedural embolic events may have led to areas of the brain susceptible to ischemia and thus had a tendency to develop larger lesions. Additionally, because larger DWI lesions with residual radiographic effect were frequently coexistent with multiple small DWI lesions that resolved over time, we could not evaluate patient-related risk factors that contributed to residual radiographic abnormalities.

Although small DWI lesions were not associated with long-term brain structure damage, neurocognitive effects of these small DWI lesions remain unknown. Due to advanced age in our patient population and expected mild cognitive dysfunction at baseline, we anticipated that natural cognitive decline and change in brain structure on MRI occurred among the participants over time. Thus, retrospectively examining neurocognitive function without comparing with preoperative baseline evaluation would not accurately reflect cognitive effects of microemboli in our patient cohort. Nonetheless, understanding the neurocognitive effects of microemboli, particularly those resulting in long-term radiographic abnormalities, is essential for future public heath and for prevention of vascular-related dementia. This study suggested that subclinical embolization may prove to be a better outcome measure for carotid revascularization procedures, and prospective evaluations of neurocognitive function on patients with microemboli are warranted.

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Author contributions 

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