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Ann Thorac Surg 2005;79:74-79
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

White Matter Disease in Magnetic Resonance Imaging Predicts Cerebral Complications After Coronary Artery Bypass Grafting

Paulin Andréll, MDa,*, Christer Jensen, MDb, Henrik Norrsell, MD, PhDa, Olof Ekre, MD, PhDa, Sven Ekholm, MD, PhDb, Ulf Norrsell, MD, PhDc, Tore Eliasson, MD, PhDa, Clas Mannheimer, MD, PhDa, Christian Blomstrand, MD, PhDc

a Multidisciplinary Pain Center
b Department of Radiology
c Institute of Clinical Neuroscience, Stroke Research Unit, Sahlgrenska University Hospital, Göteborg, Sweden

Accepted for publication June 25, 2004.

* Address reprint requests to Dr Andréll, Multidisciplinary Pain Center, Sahlgrenska University Hospital/Östra, S-416 85 Göteborg, Sweden (E-mail: paulin.andrell{at}paincenter.se).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The aim of the present study was to assess neurologic and neuropsychologic complications in 104 patients randomized to coronary artery bypass grafting or spinal cord stimulation. An additional objective of the study was to assess whether preoperative white matter disease might predict cerebral complications, as previous studies have shown that there is a relationship between white matter disease and neuropsychologic decline after coronary artery bypass grafting.

METHODS: The patients were subjected to neurologic examination before and six months after intervention. The patients underwent a cerebral magnetic resonance imaging before intervention and the presence of white matter disease was related to development of cerebral complications.

RESULTS: More patients in the bypass group than in the spinal cord stimulation group developed focal cerebral ischemia (p < 0.05) and astheno-emotional disorder (p < 0.001). More patients with white matter disease undergoing bypass were affected by focal cerebral ischemia (p < 0.01) and astheno-emotional disorder (p < 0.001) after the intervention compared to patients with white matter disease undergoing spinal cord stimulation. In patients with no white matter disease there were no differences between the bypass group and spinal cord stimulation group with regard to cerebral complications.

CONCLUSIONS: Patients undergoing bypass had more neurologic and neuropsychologic complications than patients undergoing spinal cord stimulation. Furthermore, patients with white matter disease were affected by cerebral complications in a higher extent after bypass than after spinal cord stimulation. Thus, preoperative assessment of white matter disease before undergoing coronary artery bypass grafting might predict the patient's risk of developing cerebral injury.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
There are several reports about neurologic and neuropsychologic deficits after coronary artery bypass grafting (CABG) [1–7]. Major neurologic complications in patients undergoing CABG occur in about 2% of the patients, although there have been reports of complication rates ranging from 1% to 5% [1, 3–5]. The percentage of patients suffering from neuropsychologic dysfunctions is high at discharge, approximately 50% to 90% [2, 8]. At 8 weeks after surgery the prevalence falls to 36% and after six months to 24% [2, 6]. There have been several reports of preoperative risk factors for cerebral complications after CABG [1, 4, 5, 9, 10]. According to these studies, age is probably the strongest risk factor for focal cerebral ischemia as well as for cognitive decline [4, 9–12]. Some of the main perioperative risk factors for cerebral complications include an atherosclerotic ascending aorta, cardiopulmonary bypass time and emboli load [1, 9, 10]. Other risk factors that have been discussed are temperature, arterial and cerebral perfusion pressure. The results regarding the impact of these factors on cerebral complications are conflicting [9, 10].

Small-artery disease is often a manifestation of generalized arteriosclerosis that leads to subcortical brain ischemia (white matter disease [WMD]), and a slowly progressive decline in cognitive function [13, 14]. Ischemic WMD is visible on T2-weighted magnetic resonance images as signal hyperintensities in the brain’s white matter. Post-mortem examinations have shown that the grade of magnetic resonance imaging (MRI) hyperintensities corresponds to the severity of ischemic tissue damage. There are several reports about the relation between MRI hyperintensities in the brain’s deep white matter and neuropsychologic decline after CABG [15–19]. Magnetic resonance image hyperintensities in deep white matter are present in 47.5% of neurologically asymptomatic subjects (31 to 84 years) [20]. These signal changes progress over time, but the progression seems not to be associated with a corresponding decline in cognitive function [21, 22].

Fazekas' rating scale [18] has been developed as a simple method for classification of the hyperintensities on MRI to reflect the severity of the WMD. The MRI hyperintensities are rated as punctate, early confluent, and confluent lesions [19]. The Fazekas' rating scale is a well-known and validated method for grading WMD, but a disadvantage of the scale is that it does not differentiate between the causes of the lesions [19, 23, 24].

Spinal cord stimulation (SCS) has been used since the 1980s for treatment of angina pectoris [25]. The antianginal effect has been found to be secondary to an antiischemic effect, which in turn seems to be due to reduced myocardial oxygen consumption [26]. The treatment has been proven to be safe and favorable long-term results have been demonstrated [27, 28]. Spinal cord stimulation, which is a less invasive form of procedure, served as a therapeutic alternative to CABG in the present study.

The aim of the present study was to assess and compare cerebral complications after CABG with those following SCS. Furthermore, the study assessed whether cerebral complications after CABG and SCS, respectively, can be predicted preoperatively by the presence of WMD on MRI according to the Fazekas' rating scale.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Study Patients
The present study is a follow-up of the Electrical Stimulation versus coronary artery Bypass surgery in severe angina pectoris (ESBY) study, which was a randomized, prospective, open comparison of CABG and SCS [28]. The inclusion criteria were severe angina pectoris due to coronary artery disease, no anticipated prognostic benefit from CABG and increased surgical risk. The patients were all acceptable for CABG on a strict indication of symptom relief. Within six months after intervention, both groups experienced adequate symptom relief, without any differences between the groups [28]. There were no health-related differences between the groups, except for current smoking, renal disease, and presence of clinically significant carotid artery stenosis (ie, stenosis of greater than or equal to 70% of the vessel diameter). Baseline health characteristics for the ESBY patients are presented in Table 1 [28].


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  		Table 1. Baseline Characteristics in the ESBY Study
 
Cerebral Complications
Before primary intervention and six months post-intervention, the patients had a thorough neurologic examination by one and the same experienced neurologist. Focal cerebral ischemia was defined as stroke and/or transient ischemic attacks (TIA). The diagnoses of stroke and TIA were classified according to prevalent definitions [29]. The neurologic examination included search for symptoms indicative of astheno-emotional disorder (AED); enhanced psychic fatigability, diminished power of concentration, amnesic problems, irritability, and emotional instability [30–33]. Furthermore, the symptoms must not be secondary to a depressed mood disorder. Each symptom was judged separately and graded as "not existing in pathological extent" or "existent in moderately to severe extent." If all symptoms were present in a "moderately to severe extent," the patient was considered to have AED. Astheno-emotional disorder has many similarities to the microvascular frontal-subcortical syndrome of aging and the dysexecutive syndrome, but the diagnosis does not include motor control impairment [14, 30]. The AED diagnosis is validated and has a high interrater reliability [32, 33]. Astheno-emotional disorder implies a significant impairment for the patient that causes pronounced suffering [30]. The patients were tested preoperatively and postoperatively by a licensed neuropsychologist, with a battery of 14 neuropsychologic tests encompassing attention, memory functions, and psychomotor performance. The tests included a simple reaction time test and Trail-Making Test, parts A and B [34]. All deaths related to cerebrovascular disease were recorded in the period from inclusion up to five years later.

Magnetic Resonance Imaging
Magnetic resonance imaging examination before treatment was planned for all the patients. All examinations were performed on a 0.5 T magnet (Philips Gyroscan NT5, Eindhoven, the Netherlands). The protocol included a double spin-echo sequence. Slice thickness was 7 mm in axial projection and the in-plane pixel size was 0.9 x 0.9 mm.

White Matter Disease
To grade lesion load of MRI hyperintensities in the white matter of the brain, Fazekas' rating scale was used [18, 19]. The presence and grade of WMD according to Fazekas' rating scale were assessed before intervention by the one and the same neuroradiologist, who was blinded to the treatment allocation. White matter disease was defined as punctate foci of MRI hyperintensities, beginning confluence of foci, and large confluent areas.

The MRI changes according to Fazekas' rating scale might be due to "pure" WMD, but also to cerebral infarctions or to unspecific periventricular changes around the posterior horns, a common finding in the elderly [35]. Thus, in order to be able to relate pure WMD to cerebral complications, one and the same neuroradiologist scrutinized the white matter changes to exclude isolated periventricular areas around the posterior horns and focal solitary infarctions. In this manner a "modified" Fazekas' rating scale was used to evaluate the patients. Presence of WMD according to the ordinary and modified Fazekas' rating scale at baseline is presented in Table 2.


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  		Table 2. Presence of WMD; ie, MRI Hyperintensities, According to the Original Fazekas' Rating Scale and the "Modified" Fazekas' Rating Scale Before Intervention
 
Carotid Disease
All patients were examined with duplex Doppler sonography before the intervention in order to establish any presence and extent of carotid disease. Clinically significant carotid stenosis was judged to be present if flow velocities corresponded to a stenosis of greater than or equal to 70% of the lumen of the vessel.

Surgery
The CABG operations were performed as open-heart surgery with extracorporeal circulation according to the standard clinical practice during the study period. The cardiopulmonary bypass circuit included a membrane oxygenator and a nonpulsatile flow during bypass, typically 2.4 L/m2 of body surface area per minute (reduced to 2.0 L/m2 per minute during hypothermia). The mean arterial pressure was maintained in the range of 50 to 70 mm Hg. Hypothermia (28 to 32°C) and cardioplegia were applied. The duration of extracorporeal circulation, aorta cross-clamping, surgery, and anesthesia were monitored and related to development of cerebral complications.

During the SCS implantation the patient was awake and local anesthesia was used. The epidural space was identified at the midthoracic level, using a Touhy needle. Through this an electrode was introduced to the level of Th1-Th2 during roentgenogram monitoring. Using test stimulation the electrode position was adjusted until the paresthesia covered the distribution of the angina. The electrode was fixed and an extension wire was tunneled to below the costal arch and connected to a pulse generator [28].

Data Collection
Data on causes of death were obtained from the Center for Epidemiology at the Swedish National Board of Health and Welfare. Data concerning cerebral morbidity and surgical variables were collected from patient charts.

Statistical Analysis
Due to the small number of patients and few events, nonparametric tests were used. Categorical data were analyzed using {chi}2 tests and Fisher's exact test; relative risk and 95% confidence intervals (CI) are quoted. Continuous variables were analyzed with the Mann-Whitney U-test. All data analysis was performed using the Statistical Package for Social Sciences (SPSS 11.0.0) software (SPSS Inc, Chicago, IL) on an intention-to-treat basis. The Ethics Committee of the Göteborg University approved the study. Written informed consent was obtained from all patients.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
There were five crossovers during the study period, two from the SCS group and three from the CABG group [36]. Eight patients did not undergo any MRI due to the presence of claustrophobia, implanted devices, early crossover, or study termination.

During six months of follow-up eleven patients in the CABG group developed focal cerebral ischemia (stroke, n = 11) compared with four patients in the SCS group (stroke, n = 3; TIA, n = 1) (p < 0.05, relative risk 2.9, CI 95% 1.0 to 8.4). In the SCS group there were no events of cerebral ischemia in connection with the primary intervention, whereas nine of the eleven patients with focal ischemia in the CABG group were affected in connection with the primary intervention (p < 0.05). No patient developed more than one event of focal cerebral ischemia. There was no significant difference between the neuropsychologic consequences for the two groups with regard to formal tests. Nevertheless, more CABG patients developed AED after intervention; 14 patients compared with one patient in the SCS group (p < 0.001, relative risk 14.5, CI 95% 2.0 to 106.6). On average, these 14 patients had slower reaction times and worse Trail-Making Test results than the other subjects. The mortality data for the ESBY patients have been presented elsewhere [27, 28, 36]. The groups did not differ with regard to 5 year cerebrovascular mortality.

Patients with preoperative WMD undergoing CABG developed focal cerebral ischemia (p < 0.01) and AED (p < 0.001) after the intervention to a higher extent than patients with WMD undergoing SCS. In patients with no WMD, there were no significant differences in cerebral complications between the groups (Table 3).


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  		Table 3. Relation Between Presence of WMD According to the Original Fazekas' Rating Scale Before Intervention and Development of Cerebral Complications up to Six Months After Intervention
 
According to the modified Fazekas' rating scale, six patients who were judged to have WMD according to the original Fazekas' rating scale did not have any pure WMD. Sixteen patients had less WMD according to the modified Fazekas' rating scale (Table 2). Nevertheless, a larger number of CABG patients with WMD, according to the modified Fazekas' rating scale, had focal ischemia (p < 0.05) and AED (p < 0.01) after the intervention than SCS patients with WMD. In patients with no WMD, according to the modified Fazekas' rating scale, there were no differences with regard to development of focal cerebral ischemia between the groups. However, more CABG patients, with and without WMD, developed AED after the intervention compared with patients undergoing SCS (p < 0.05) (Table 4).


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  		Table 4. Relation Between Presence of WMD According to the "Modified" Fazekas' Rating Scale Before Intervention and Development of Cerebral Complications up to Six Months After Intervention
 
There were no differences between the groups with regard to cerebral complications related to the presence of clinically significant carotid stenosis. Development of cerebral complications after intervention was not related to the duration of extracorporal circulation, aorta cross-clamping, surgery or anesthesia, or to age. Presence or absence of WMD according to the original or to the modified Fazekas' rating scale was not related to age either.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
The patients of the ESBY study had a higher cerebrovascular morbidity in terms of stroke and TIA than reported from other studies [1, 3–5, 37]. This may be expected since one of the inclusion criteria was high surgical risk due to cerebrovascular and other concomitant diseases. The patients also had a high frequency (74%) of WMD at baseline, which may also be expected since the patients had extensive coronary artery disease [38]. Presence of cognitive dysfunction, described as AED, six months after CABG did not differ from other studies [2, 6, 37]. There were no differences between the groups with regard to performance on neuropsychologic tests, which is in line with results from previous studies [39]. A considerable number of the CABG patients (n = 7) died in connection with the primary intervention and in nine of the eleven patients with focal cerebral ischemia in the CABG group; the event was related to the surgery [28]. In contrast, SCS has no known cerebral complication risks and is implanted during local anesthesia [27, 28]. In the SCS group none of the cerebral incidents were related to the primary intervention, although one event was related to CABG. In the ESBY material there were no major complications related to the implantation, only minor perioperative complications [36].

In the present study, age was not associated with either development of cerebral complications, or with a greater presence of WMD. This might be due to selection bias; the patients may have similar risk of cerebral complications and similar extent of WMD, despite age differences, since they all were considered to be high-risk patients.

Some investigators have suggested that neurologic outcome is related to the duration of the procedure since the duration of surgery may be prolonged by several factors that may themselves contribute to cerebral injury [1, 9]. However, in the present study all patients had a high risk of perioperative complications, which may explain the minor impact of the surgery-related variables on cerebral and other events.

A novel finding in the present study is that patients with increased surgical risk of cerebral complications with WMD, in addition to other known risk factors for cerebrovascular lesions, developed more cerebral complications in connection with CABG than with SCS. Furthermore, the results imply that the Fazekas' rating scale may be too crude to grade WMD, as cerebral infarctions and periventricular changes around the posterior horn will contribute to the assessment (Fig 1). When pure WMD was estimated according to the modified Fazekas' rating scale, the results regarding the connection between WMD and the development of focal cerebral ischemia were consistent compared to the original Fazekas' rating scale (Tables 3 and 4). However, when pure WMD was related to the development of AED after surgery, the CABG patients with and without WMD developed more cases of AED than the patients in the SCS group (Tables 3 and 4). In summary, the presence of WMD seems to indicate an increased risk of focal cerebral ischemia after CABG, independent of the rating scale used to assess the MRI hyperintensities. Regarding the impact of WMD on the development of AED, the original Fazekas' rating scale indicates that WMD might be of importance, but according to the modified Fazekas' rating scale the results indicate that it is the CABG per se that increases the risk of developing AED. However, the interpretations should be cautious due to the small number of patients.



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  		Fig 1. According to the original Fazekas' rating scale this patient is considered to have confluent lesions of magnetic resonance imaging (MRI) hyperintensities. The MRI hyperintensities are, however, to a large degree due to a nonspecific periventricular change around the right posterior horn, which cannot be regarded as "pure" white matter disease. The remaining MRI hyperintensities are rated as punctate according to the "modified" Fazekas' rating scale.

 
Study limitations
The ESBY study was not blinded because the two procedures differ significantly; ie, the treatment allocation was known by the patient and the surgeon. Furthermore, the study included a limited number of patients.

Conclusions
White matter disease may be a previously unobserved surgical risk factor for cerebral complications. Patients with preoperative WMD developed cerebral complications to a higher extent following CABG than following SCS. Thus, presence of WMD might indicate an increased risk of cerebral complications for a patient after CABG. It may be valuable to perform a MRI and assess the extent of WMD before CABG and avoid surgery in patients with WMD to prevent cerebral complications. Further studies are needed to evaluate the predictive potential of WMD. The present study further supports the results from the ESBY study; that SCS might be a therapeutic alternative in patients with severe angina pectoris and surgical risk factors.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank our medical statistician, Martin Gellerstedt, for expert professional advice and for careful and precise guidance regarding the interpretation of the results. The study was supported by the Faculty of Medicine, University of Göteborg, the Swedish National Heart-Lung Foundation, and the Swedish Medical Research Council.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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