European Journal of Vascular & Endovascular Surgery
Volume 38, Issue 5 , Pages 546-551, November 2009

Carotid Endarterectomy Improves Cerebrovascular Reserve Capacity Preferentially in Patients with Preoperative Impairment as Indicated by Asymmetric BOLD Response to Hypercapnia

  • S.D. Goode

      Affiliations

    • Department of Academic Radiology, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK
    • Department of Vascular and Endovascular Surgery, Queens Medical Centre, Nottingham NG7 2UH, UK
    • ,
  • N. Altaf

      Affiliations

    • Department of Academic Radiology, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK
    • Department of Vascular and Endovascular Surgery, Queens Medical Centre, Nottingham NG7 2UH, UK
    • ,
  • D.P. Auer

      Affiliations

    • Department of Academic Radiology, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK
    • Corresponding Author InformationCorresponding author.
    • ,
  • S.T.R. MacSweeney

      Affiliations

    • Department of Academic Radiology, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK
    • Department of Vascular and Endovascular Surgery, Queens Medical Centre, Nottingham NG7 2UH, UK

Received 17 February 2009; accepted 14 June 2009. published online 10 September 2009.

Article Outline

Abstract 

Purpose

In patients with symptomatic carotid artery disease the predominant mechanism causing ischaemic injury is considered to be thromboembolic, however compromise of cerebral haemodynamics is considered to be a significant factor. Removal of the embolic source is accepted as the major benefit from Carotid Endarterectomy (CEA), however improvement in cerebral haemodynamics may be another beneficial outcome as suggested by Transcranial doppler (TCD). Blood Oxygen Level-Dependent (BOLD) hypercapnia functional Magnetic Resonance imaging (fMRI) can be used to map the Cerebrovascular Reserve (CVR). The aim of this study was to assess the effects of carotid surgery on cerebral haemodynamics in patients with carotid artery disease using a hypercapnia BOLD fMRI and assessment of hemispheric asymmetry.

Materials and methods

Seventeen patients with symptomatic internal carotid artery stenosis were scanned using a clinical 1.5T MR scanner. Scanning was done immediately prior to and between 4 and 8 weeks after CEA. 10% carbon dioxide was administered to achieve transient episodes of hypercapnia. The data was analyzed using FMRIB Software Library (FSL) software to derive percentage signal change (PSC) for the grey matter of the middle cerebral artery (MCA-GM) territory for both hemispheres. MCA-GM PSC was furthermore normalized to the contralateral hemisphere to derive an Hemispheric Asymmetry Index (hAI) for all patients pre- and postoperatively.

Results

Ipsilateral GM CVR improved significantly following CEA (2.47% preoperatively vs. 2.73% postoperatively, p=0.038). There was no change in CVR in the contralateral grey and white matter MCA territories (p=0.27, p=0.1). Also, the hAI was significantly more shifted to the ipsilateral hemisphere after CEA (preoperative hAI −0.56, vs. −3.90 postoperatively, p=0.02). Patients with an impaired hAI preoperatively were found to show the greatest improvement in PSC and hAI following CEA (p=0.007).

Conclusions

CEA resulted in improved CVR in patients with carotid artery disease as shown by the absolute and hemispheric asymmetry of BOLD response to hypercapnia.. These findings show that benefits from recanalisation may go beyond removal of the embolic source, by improving the cerebrovascular reserve. Moreover, hypercapnia BOLD fMRI may be a useful clinical tool in predicting this therapeutic potential in patients with severe carotid artery disease.

Keywords: Carotid artery disease, Carotid endarterectomy, Functional MRI, Hypercapnia, Cerebrovascular reserve, Haemodynamic impairment

 

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Introduction 

Carotid Endarterectomy (CEA) is performed to prevent stroke caused by a stenotic lesion in the ipsilateral internal carotid artery (ICA). A series of randomized controlled trials in the 1990s proved the benefits of CEA.1, 2 In patients with symptomatic carotid artery disease the predominant mechanism causing ischaemic injury is considered to be thromboembolic, however carotid stenosis and occlusion can also compromise cerebral haemodynamics. It is being increasingly recognized that cerebral haemodynamic impairment may convey an increased risk of stroke in these patients.3, 4, 5 Moreover, CVR (Cerebrovascular Reserve) impairment may enhance the thromboembolic risk. It has been suggested that cerebral hypoperfusion secondary to carotid disease may lead to impaired clearance of emboli and therefore increasing the risk of developing a clinical stroke as a result from carotid plaque embolization.5 The identification of patients with impairment of cerebral haemodynamics may have a significant effect on their management.

The haemodynamic effect of ICA stenosis is not only determined by the severity of stenosis, as the quality of the collateral circulation is equally important. Collateral flow capacity depends on anatomical characteristics and the presence of additional steno-occlusive disease such as contralateral ICA stenosis/occlusion. Therefore, individual assessment of the haemodynamic down stream effects of a carotid artery disease could help to identify high-risk patients, in particular those patients with bilateral disease. Removal of the embolic source is accepted as the major benefit from CEA, however improvement in cerebral haemodynamics may be another beneficial outcome in selected patients. In fact previous studies using transcranial Doppler (TCD) and (SPECT) Single photon emission computed tomography demonstrated improved CVR following CEA.6, 7, 8, 9

A parameter used to test the haemodynamic status of the cerebral circulation is the CVR capacity. CVR refers to the capacity of cerebral blood flow to increase in response to regional metabolic demand. Measuring CVR can be done by various techniques; flow velocity measurements using TCD, Cerebral Blood Flow (CBF) measurements using Positron emission tomography (PET) or Arterial Spin Labeling (ASL) or more recently Blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI). To actually assess the dynamic reserve status a vasodilatory substance is also needed such as CO2 or acetazolamide. Under normal physiological conditions, these substances induce vasodilatation, resulting in an increase in CBF. Any preexisting vasodilation will interfere with the ability of the cerebral vessels to dilate further in response to a vasodilatory stimulus. Thus, the degree of CO2 reactivity provides indirect information about the extent of the cerebral blood vessel dilatation, directly reflecting the remaining reserve capacity of the cerebral circulation.

BOLD fMRI combines the advantages of availability and high spatial resolution, without the use of radiation. This technique relies on endogenous contrast being created from changing levels in haemoglobin oxygenation saturation. BOLD fMRI can be used to produce high spatial resolution CVR maps, semiquantitative data on brain reactivity and also information on the cerebral vascular response. This technique can be used to assess CVR over any chosen region of interest (e.g. MCA territory), and furthermore limiting to tissue specific areas such as grey matter or white matter. BOLD fMRI has been used to study the CVR in healthy volunteers and patients with carotid stenosis and occlusion and has proved as good as TCD in detecting impaired CVR in addition to the above mentioned advantages.10, 11, 12, 13, 14

The aim of this study was to assess the effects of carotid surgery on haemodynamics in patients with carotid artery disease using hypercapnia BOLD fMRI as assessed by absolute signal change and the hemispheric asymmetry index (hAI). Secondly, we aimed to search for potential predictors of who may benefit most from the heamodynamic improvement following CEA by stratifying patients according to a preoperative hAI of CVR.

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Methods 

Recruitment and patients 

Patients considered for CEA were prospectively identified between March 2006 and March 2008 from the hospital transient ischemic attack (TIA) clinic. Eligibility criteria included carotid artery stenosis on Duplex scanning (60–99%), using established ultrasound criteria15 as used in the Carotid and Vertebral Artery Transluminal Angioplasty Study.16 The patients had experienced stroke, TIAs or amaurosis fugax in the previous 12 months. All participants gave written informed consent, and the study was approved by the hospital research and development department and Local Research Ethics Committee. Exclusion criteria were contraindication for MRI or when waiting for MRI would have delayed CEA. Diagnostic work-up and therapeutic management of the patients and its timing was not affected by this study.

We studied 17 patients with a mean age of 68.2 years (range, 42–81 years); there were 16 men and 1 woman, this gender distribution reflects the patients available for recruitment during the study period. All patients in this study were taking statin medications. One patient had a postoperative stroke and was therefore excluded from the final analysis. 8 patients had contralateral carotid artery disease; 4 patients with occlusion, 3 patients with 80–89% and 1 patient with 70–79% stenosis. There was no significant vertebral disease amongst these patients. All subjects were asked not to consume alcohol or caffeine for 4h before the scanning session.

MRI 

Magnetic resonance imaging (MRI) studies were performed on a clinical 1.5T scanner (Intera, Philips, Best, Netherlands). A standard 8 channel head coil was used for imaging, deploying a standard gradient echo echoplanar sequence (Repetition time (TR) ms/echo time ms 3500/60, flip angle 90 degree, matrix size 64×64, field of view 192mm with 33 slices, 3mm thick and no gap). A total of 160 volumes (approx 9min acquisition time) were acquired for each experiment. Preoperative MRI scanning was performed within 30 days of the procedure (Median 6.5 days), apart from 1 patient who had been scanned 5 months prior to CEA. Post operative MRI scanning was performed within 2 months of the carotid endarterectomy. Additionally at postoperative MRI scanning patients had DWI to assess for postoperative evidence of ischaemia.

CO2 stimulation 

ETCO2 was controlled using a standard non-rebreathing anaesthetic circuit using two one way valves to prevent rebreathing. Subjects breathed through a comfortably secure standard anaesthetic mask to ensure a closed circuit. ETCO2 was continuously monitored via a sampling tube at the mouthpiece level, with recordings being made during the whole experiment. The two periods of hypercapnia were intercalated with three periods of normocapnia. The %CO2 was varied around 10% aiming for an increase in ETCO2 between 7 and 8mmHg change. Control of CO2 gas flow was via an external source outside of the MRI scanner. We continuously monitored the subjects blood pressure, pulse and arterial oxygen saturations using a MR compatible device (Invivo, Siemens, Malvern, US).

CEA 

All CEAs were performed as per the local standard of care in conscious patients with locoregional anesthetic techniques in a tertiary referral center. Three consultant vascular surgeons performed the procedure and the center specific perioperative stroke rate is <3%17 A shunt was used if there was any loss of consciousness or focal neurological deficit in the patient. Dacron patch repairs were performed in all patients. The surgeons were not made aware of the preoperative MRI findings.

Data analysis 

The first level fMRI data analysis was carried out using FEAT v5.63 software (FMRI Expert Analysis Tool (FEAT), version 5.63, Oxford Centre for Functional Magnetic Resonance Imaging Analysis of the Brain—FMRIB – University of Oxford), part of the FMRIB software library v3.3 (FSL).18 FEAT deployed standard preprocessing with high-pass filtering, smoothing and motion correction using MCFLIRT.19 During the FSL analysis the ETCO2 data acquired during the scanning session was incorporated into the design matrix of the General Linear Model (GLM). A Gaussian model was used for modeling the haemodynamic response (HDR) function. The FSL analysis method compensated for any lags in our setup (e.g. sampling delay from patient to capnometer) by allowing for a temporal derivative of the design matrix waveform, which essentially shifts the waveform in time during the analysis to enable a better fit of the data and model. FSLs Brain Extraction Tool (BET) was used to remove non brain structures from the anatomical T1-weighted scans. Following this the T1 images were segmented into grey and white matter using FMRIB Automated Segmentation Tool (FAST) from FSL.20 A manually drawn middle cerebral artery (MCA) template territory was created in standard space. This was then combined with each patients grey matter mask resulting in individualized grey matter MCA territory masks. Absolute percent signal change (PSC) was derived from the GM MCA mask using FSL software FEAT query following conversion from standard space into functional space. This method has been previously published.21 To normalize the PSC we regressed the effect of ETCO2 change over the experiment data using a linear correction method derived from our normative set.21

To address potential problems from normalization, we additionally normalized ipsilateral PSC to the contralateral hemisphere expressed as hemispheric asymmetry index (hAI). We defined hemispheric asymmetry according to hAI=200×((PSC Contralateral hemisphere−PSC Ipsilateral operated hemisphere)/(PSC sum both hemispheres)) as reported.22, 23, 24 For the second level subgroup analysis the group was divided into those patients with CVR lateralized towards the ipsilateral hemisphere (<0) defined as preserved CVR and those lateralized to the contraleteral hemisphere (>0) defined as impaired CVR.

Statistical analysis 

Statistical calculations were performed using the Statistical Package for Social Sciences (SPSS version 15.0; SPSS, Chicago, Ill) software. Statistical significance was set as p<0.05. Data is expressed as mean percentage signal change±standard deviation (SD). T tests and U tests were performed for parametric and nonparametric variable respectively. A univariate analysis of covariance (ANCOVA) was performed to look at the effect CEA on CVR (as assessed by PSC) whilst controlling for age, MAP, contralateral carotid disease, time from symptoms to CEA and from CEA to post op scan.

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Results 

General findings 

All seventeen subjects tolerated the experiment well without adverse reaction during the course of study to inhalation of CO2. CVR maps were produced for each patient, see Fig. 1 for example of pre and post CEA CVR map. Patient 11 had to be excluded from the group analysis due to a postoperative stroke. The observed motion as estimated by FSL was within acceptable limits in all cases, i.e. less than 3mm in x, y, z axis. The mean preoperative ETCO2 change was 7.44±3.7mmHg and the mean postoperative ETCO2 change was 8.58±5mmHg (U test p=0.667). The mean preoperative MAP was 105.8±18.8 and postop MAP was 105.9±19.7 (T test p=0.984).

  • View full-size image.
  • Figure 1 

    Examples of CVR maps for pre and post CEA for patient with left sided 80–95% stenosis. Following recanalisation there is improvement in CVR on the operated side as indicated by increased BOLD signal change in the left hemisphere.

Grey matter CVR 

Ipsilateral GM CVR improved significantly following CEA (ipsilateral preoperative PSC was 2.75±0.41 and the mean postoperative PSC was 3.05±0.44, p=0.025). The mean contralateral preoperative PSC was 2.75±0.49 and the mean postoperative PSC was 2.93±0.39, this was not significant (p=0.14), (See Table 1).

Table 1. Table 1 shows results for all patients undergoing CEA for MCA grey matter territory.
Ipsilateral PSCP ValueContralateral PSCP Value
Grey matter MCA territory N=16Pre2.750.025*2.750.14
Post3.052.93

P values are given for differences between pre and post PSC.

* indicates significant difference to a level of 0.05.

hAI 

The mean preoperative hAI was −0.44±6.31 which means that the overall haemodynamic impairment was towards the operated MCA territory. Following CEA mean postoperative hAI changed to −3.9±6.18(p=0.025), indicating an increase in the ipsilateral CVR relative to the contralateral side (See Table 2).

Table 2. Results for all patients undergoing CEA.
hAIP Value
All patients N=16Pre−0.44±6.310.025*
Post−3.90±6.19

P values are given for differences between pre and post hAI.

* indicates significant difference to a level of 0.05.

Effect of preoperative impaired hAI 

To try to assess the effect of preoperative ipsilateral haemodynamic impairment our subgroup analysis looked at the effect of preoperative hAI. Our patients were split into two groups defined by their hAI – preserved CVR (hAI<0, n=7) and those with an impaired hAI (hAI>0, n=9). Those patients with an impaired CVR preoperatively showed a greater improvement following CEA (p=0.007, see Table 3).

Table 3. Table showing effect of preserved/ impaired preop hAI on CVR change following CEA.
hAIP Value
Preserved CVR N=7Pre−6.23±3.590.94
Post−6.40±5.61
Impaired CVR N=9Pre4.07±3.580.003*
Post−1.88±6.20

P values are given for differences between pre and post PSC.

* indicates significant difference to a level of 0.05.

Effect of high grade ipsilateral stenosis 

We divided our patients into two groups; those with ipsilateral low grade stenosis (60–80%) and those patients with a higher degree of stenosis (>80%). We found that those patients with a higher degree of stenosis seemed to have a greater improvement in their ipsilateral CVR following CEA.

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Discussion 

For many years, CVR has been clinically assessed using TCD, which measures blood flow velocity in the middle cerebral artery (MCA). Problems with CO2 reactivity testing using TCD include: measuring blood flow velocities rather than the more physiologically important tissue perfusion, no information on other vascular territories, no assessment of CVR due to collateral flow increase, and only 85–90% of people have a sonable temporal bone window. Currently established methods of assessing CVR include PET and SPECT, however these techniques are expensive, time consuming and due to the nonnegligable radiation exposure cannot be considered completely non-invasive. More recently MRI techniques have been used to estimate CVR non-invasively with and without vasodilatory stimulus.12, 14

Hypercapnia BOLD fMRI is a promising tool for the haemodynamic assessment of patients with carotid artery disease, due to it being non-invasive and because there is no radiation exposure. It enables not only visual qualitative assessment of CVR, like previous studies using SPECT,25 but also semiquantitative assessment of CVR. Our main findings are that patients with carotid artery disease have a significant improvement in their ipsilateral CVR as shown by increase in BOLD response to hypercapnia as absolute PSC and normalized to the contralateral hemisphere following CEA. Assessment of hAI pre and post CEA has not previously been studied, however it has been published pre and post carotid artery stenting (CAS) using 99mTc-HMPAO SPECT imaging.26 Reported data on hemispheric asymmetry pre and post CAS and did not find any significant changes in cerebral perfusion patterns. Their hAI values were similar to our data, however they had a greater variability in the values. This may be due to the SPECT method of acquiring data whereby the values are relying on very large numbers of technicium gamma rays being emitted from the patient. As opposed to our more physiological of looking at changing oxyhaemoglobin levels which may be a more accurate method.

Our findings confirm previously work.6, 7, 8, 28, 29 In particular our results correspond very closely with Haller et al.,29 who looked at CVR pre and postoperatively using a hypercapnia BOLD fMRI technique. However, they did not measure ETCO2 change following administration of a fixed amount of CO2. They were therefore unable to comment on the direct change pre and post op, instead utilising improvement in ipsilateral to contralateral carotid disease ratios. Their results showed a significant interhemispheric difference in pre procedure %SC in ipsilateral vs. contralateral whole MCA territories and no significant difference in those territories post procedure, thereby concluding that there had been improvement in the ipsilateral CVR. Our study differed in a number of ways; we used a more physiologically relevant grey matter specific MCA territory masks, we collated ETCO2 data following CO2 stimulation thus enabling us to directly quantify the degree of CO2 stimulation administered and our statistical analysis utilised further relevant demographic and physiological parameters. Using the ETCO2 data from our experiment we were able to include this into our analysis using a univariate design and thereby making a direct comparison between pre and post op PSC. Also of note in our univariate analysis is that we included age,30 gender,31, 32 and BP33 which have been shown previously to have a profound effect on CVR.

In our group of patients we had only one major complication with one patient having a postoperative stroke. This happened on the table immediately following the operation and the patient was reexplored, his symptoms had resolved the following day except for a slight numbness in his hand. Postoperative imaging revealed DWI positive lesions in his MCA territory distal to the CEA. When we analysed his post CEA CVR it had decreased markedly in contrast to the rest of our group. Haller et al. also noted patients with new DWI lesions had worsening of CVR. Our data is in agreement with this.

An important question that we tried to address relates to patient selection based on individual prediction of haemodynamic improvement. When we looked at those patients with an ipsilateral impaired CVR towards the operated side it was this group that improved most following CEA. In contrast, those patients with a preserved hAI towards the ipsilateral operated MCA territory preop did not have an improvement following CEA. This suggests that patients with a preoperative ipsilateral CVR impairment may gain a greater improvement in their overall haemodynamic status. These findings confirm previous work by Nielsen et al.34 and Hosodo et al.25 who showed that patients with preoperative hypoperfusion benefit from carotid revascularisation, whereas the haemodynamic benefit in patients with good preoperative perfusion is only limited.34 Further work is needed to assess whether this functional improvement translates into clinical benefit for patients either by future stroke reduction or improvement in cognition as suggested by previous work by Ghogawala et al.35

The main limitation of our study is the inclusion of only a relatively small number of subjects. The study size was however sufficient to demonstrate a significant improvement in CVR following CEA. With larger numbers of patients we may have been able to perform more subgroup analyses. The second limitation is the variable timings of the pre and postoperative scans, although by using a univariate analysis and including time from symptom to preoperative scan and time for CEA to postoperative scan we removed this confounding variable from the analysis. Lastly, there may have been a variable effect on CVR mediated by the use statins in our patients. Preliminary studies have shown an effect of statin treatment on CVR in healthy volunteers and patients,36, 37 whereby CVR is improved following initiation of treatment. In our study patients may have only just started their statins which may not have been acting at time of preoperative scanning session, whereas others may have been on long term treatment.

The need to be able to identify the high-risk patient undergoing carotid intervention, be it either endarterectomy or angioplasty and stenting is an important topic. Indeed in patients with high grade carotid artery disease can be further stratified into those with a high-risk carotid plaque38 or those with an obvious haemodynamic impairment. We have shown that CEA improves patients CVR, in particular in those patients with a greater ipsilateral haemodynamic impairment. This is probably mediated by improvement in patients ability to vasodilate suggesting a return of cerebral autoregulation and vasodilatory reserve capacity. We would advocate the inclusion of this simple haemodynamic assessment for patients in the diagnostic work-up for those undergoing revascularisation procedures. However, more studies are needed to establish the true clinical relevance of haemodynamic risk assessment afforded by this technique.

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Conflict of Interest/Funding 

There are no conflicts of interest.

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Acknowledgements 

Special Trustees for Nottingham University Hospitals, Peel Medical Research Trust and Royal College for Surgeons for providing 1 year Surgical Research Fellowship.

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PII: S1078-5884(09)00335-9

doi:10.1016/j.ejvs.2009.06.010

European Journal of Vascular & Endovascular Surgery
Volume 38, Issue 5 , Pages 546-551, November 2009

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