Published online before print March 6, 2008, doi: 10.1161/STROKEAHA.107.502989
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(Stroke. 2008;39:1427.)
© 2008 American Heart Association, Inc.
Original Contributions |
Cerebral Ischemic Lesions on Diffusion-Weighted Imaging Are Associated With Neurocognitive Decline After Cardiac Surgery
From the Departments of Neurology (P.A.B., L.R.) and Cardiothoracic Surgery (P.M.), Auckland City Hospital, Auckland, New Zealand; and the Departments of Medicine (P.A.B.), Psychology (S.H., L.J.T.), and Anaesthesiology (A.F.M), University of Auckland, Auckland, New Zealand.
Correspondence to Paget Milsom, FRACS, Cardiothoracic Surgery Department, Auckland City Hospital, Park Road, Grafton, Auckland, New Zealand. E-mail pmilsom{at}adhb.govt.nz
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Abstract |
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Background and Purpose— Improvements in cardiac surgery mortality and morbidity have focused interest on the neurological injury such as stroke and cognitive decline that may accompany an otherwise successful operation. We aimed to investigate (1) the rate of stroke, new ischemic change on MRI, and cognitive impairment after cardiac valve surgery; and (2) the controversial relationship between perioperative cerebral ischemia and cognitive decline.
Methods— Forty patients (26 men; mean [SD] age 62.1 [13.7] years) undergoing intracardiac surgery (7 also with coronary artery bypass grafting) were studied. Neurological, neuropsychological, and MRI examinations were performed 24 hours before surgery and 5 days (MRI and neurology) and 6 weeks (neuropsychology and neurology) after surgery. Cognitive decline from baseline was determined using the Reliable Change Index.
Results— Two of 40 (5%) patients had perioperative strokes and 22 of 35 (63%) tested had cognitive decline in at least one measure (range, 1 to 4). Sixteen of 37 participants (43%) with postoperative imaging had new ischemic lesions (range, 1 to 17 lesions) with appearances consistent with cerebral embolization. Cognitive decline was seen in all patients with, and 35% of those without, postoperative ischemic lesions (P<0.001), and there was an association between the number of abnormal cognitive tests and ischemic burden (P<0.001).
Conclusion— We have provided a reliable estimate of the rate of stroke, postoperative ischemia, and cognitive impairment at 6 weeks after cardiac valve surgery. Cognitive impairment is associated with perioperative ischemia and is more severe with greater ischemic load.
Key Words: cardiac surgery • diffusion-weighted imaging • embolism • neuropsychology
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Introduction |
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Improvements in cardiac surgery mortality and morbidity over the years have focused interest on the neurological injury that may accompany an otherwise successful operation. The spectrum of brain injury after cardiac surgery ranges from neurological death (0.21% to 2.0%), stroke (1.1% to 6.6%), and perioperative encephalopathy.1–5 Cognitive impairment is a more frequent complication and is found in a significant proportion of patients after cardiac surgery.1,6 The exact incidence of cognitive impairment varies depending on the nature of the cardiosurgical group studied, the type of surgery performed, the definition of decline, and the length of the test–retest interval. Patients with complex surgery and earlier postoperative cognitive testing are more likely to show new deficits.1
In recent years, magnetic resonance diffusion-weighted imaging (DWI) has been used to investigate the cause of neurological impairment after cardiac surgery. DWI identifies regions of cerebral ischemia with a high sensitivity and specificity and can distinguish acute from chronic infarction. Between 25% and 50% of patients undergoing cardiac surgery develop new lesions on postoperative DWI with more frequent lesions in those undergoing extensive operations.7–13 Only a minority of those with DWI lesions have had a clinical stroke.
The relationship between cognitive decline and perioperative embolization is less clear. Small case series have found an association between a dropoff in cognitive performance and new DWI lesions,14 but recent larger studies in both coronary artery bypass graft (CABG) and valve surgery have failed to find any association.11–13 This has led one group to conclude that the investigation of cerebral infarction is a potential misdirection in solving the problem of postoperative cognitive decline.13 This is an important issue because cognitive impairment after otherwise successful surgery is a serious concern for patients and their families.
In this article, we report data collected on one third of the planned patients of a larger trial of an intervention to reduce perioperative cerebral ischemia. The frequency of stroke, ischemic change seen on DWI, and cognitive decline after valve surgery has been assessed. We hypothesized that patients with cerebral ischemia after cardiac surgery would be more likely to have cognitive decline.
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Materials and Methods |
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Consecutive, neurologically independent (modified Rankin Scale <2) patients requiring elective valve replacement or repair with or without concurrent CABG at our institution were eligible for inclusion in the study. Patients undergoing valve surgery were specifically targeted because they are likely to be at higher risk for adverse cerebral outcomes than those in whom the heart is not opened and have a greater risk of embolization from vegetations, thrombi, and gaseous bubbles. These patients are all subjects of a larger ongoing trial and were randomized (1:1) to either a novel dual-vent deairing technique or conventional cardiopulmonary bypass (CPB). The dual-vent deairing technique has been designed to reduce the escape of solid and gaseous emboli into the circulation by allowing left ventricular and aortic venting from the working heart into the CPB venous line before aortic declamping.15 Exclusion criteria included preexisting neurological deficits that would hamper interpretation of clinical and radiological data, a Mini-Mental State Examination score of less than 24 out of 30, concomitant medical disorders making follow-up unlikely, overt congestive heart failure, hemodynamic instability (cardiac ejection fraction <25%, frequent arrhythmia), a hemorrhagic diathesis or hypercoagulability, concomitant carotid surgery, and contraindications to MRI scanning such as a cardiac pacemaker. All participants provided written informed consent and the study was approved by the regional ethics committee. The main trial is registered with the Australian Clinical Trials Register, number ACTRN12605000214639.
Clinical assessments consisting of a neurological examination and the National Institutes of Health Stroke Scale were performed 24 hours before surgery and were repeated at 5 days and 6 weeks postoperatively. A modified Rankin Scale was also performed at 24 hours before surgery. Assessments were performed by a neurologist trained in their administration and blinded to the results of the imaging and neuropsychological studies.
Cognitive testing was performed 24 hours before surgery and was repeated 6 weeks postoperatively. The tests used were the Trail Making Test Part A and B,16 Grooved Pegboard Test,17 and the Rey Auditory Verbal Learning Tests,18 which are tests recommended by A Statement of Consensus on Assessment of Neurobehavioural Outcome After Cardiac Surgery.19 In addition, the Letter-Number Sequencing Test,20 the Symbol Digit Modalities Test,21 a baseline National Adult Reading Test,22 and the Hospital Anxiety and Depression Scale23 were also performed. The number of neuropsychological variables used in the analyses was limited to 10 to minimize Type I error. Cognitive assessments were performed by a single trained neuropsychologist blinded to the results of the imaging and clinical studies. Cognitive impairment was determined by the calculation of Reliable Change Index (RCI) for each neuropsychological measure.24 The RCI was used because this technique has good sensitivity for detecting reliable change outside of random variability. We defined cognitive impairment as a drop in the RCI in at least one measure.
All MRI studies were obtained with a 1.5-Tesla EPI-equipped whole-body scanner (Siemens Avanto) using a standardized protocol. Scans were always performed in the same order with a T1-weighted 3-plane localizer, diffusion-weighted sequence and fluid-attenuated inversion recovery (FLAIR) sequence. Diffusion-weighted images were obtained using a multislice, single-shot spin-echo echoplanar image sequence. Slice thickness was 5 mm with a 1-mm gap with the number of slices set to include the whole brain. Matrix size was 192x192, field of view was 230 mm, and TR/TE was 4300/117 ms. Diffusion gradient strength was varied between 0 and 45 mT/m, resulting in 2 b values of increasing magnitude from 0 to 1000 seconds/mm. FLAIR images were obtained using a slice thickness of 5 mm with a 1.5-mm gap with the number of slices set to include the whole brain. Matrix size was 224x256, field of view was 230 mm, TR/TE was 8500/119 ms, and TI was 2500 ms. The total imaging time was approximately 15 minutes.
MRI studies were performed in the 24 hours before surgery after any cardiac catheterization, which in itself may result in cerebral embolism.25 MRI studies were repeated at day 5 (range, 1 to 6 days) after cardiac surgery to identify any perioperative ischemic lesions. The DWI and FLAIR images were presented to one of the investigators blinded to the results of the clinical assessments. The images were analyzed for the presence, number, and volume of DWI lesions on the postoperative scans. Lesion volume was determined using a semiautomated technique. Only lesion volumes greater than 0.2 cm3 are reported because of concerns about accuracy and lesions smaller than this are reported as "<0.2 cm3."
Anesthetic and Surgical Procedures
There were no specific alterations to standard surgical practice apart from randomization of patients to dual-vent deairing or conventional CPB to which the investigators remain blinded.15 Predicted operative mortality was calculated using the logistic form of the European System for Cardiac Operative Risk Evaluation (EuroSCORE), which takes into account a patient’s age, sex, and comorbid-, cardiac-, and operation-related factors.26 Selection of aortic cannulation sites and the crossclamp site were guided by epiaortic scanning. A single aortic clamp technique was used with clamp placement guided by transesophageal echocardiography and epiaortic scanning. Standard anesthetic techniques were used and intraoperative monitoring was in accordance with guidelines and a policy to keep the CPB perfusion pressure above 50 mm Hg.
Statistical Analysis
Statistical analyses were performed using the SPSS statistical software package with an 
value of 
0.05 considered statistically significant. Categorical data were analyzed with the 
2 statistic with Fisher’s exact test used if the expected cell size was small. The RCI was calculated using the standard error of prediction (SEp)27 with SEp=SDy
(1–r122) where SEp=SE of retest scores predicted from baseline scores; r12=test–retest coefficient; and SDy=SD of observed retest scores. The standard error of prediction was multiplied by + or –1.64 to obtain 90% CIs.
Univariate logistic regression analyses were performed to examine the association between neuropsychological outcome and age, gender, EuroSCORE, complexity of surgical procedure (dichotomized into those with valve surgery alone or valve and CABG surgery), CPB time, and postoperative DWI lesions. Univariate logistic regression analyses were also performed to examine the association between these covariates and the presence or absence of postoperative DWI lesions or cognitive decline. Missing values were set to zero. Sensitivity analyses were also performed first by dropping missing values and second by setting missing values counter to our hypothesis, ie, setting the value to the presence of new DWI lesions for patients without neuropsychological change and to the absence of new DWI lesions for patients showing neuropsychological change.
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Results |
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Forty participants (26 men; mean [SD] age 62.1 [13.7] years; range, 25 to 85 years) were enrolled in the study (Table 1). All 40 patients completed the baseline neurological and neuropsychological assessments, but 2 participants did not have a preoperative MRI due to scheduling difficulties. All 40 participants had postoperative neurological assessments performed at a mean of 5 (SD, 3) days after surgery. Four participants did not have postoperative MRI studies; Patients 7 and 33 had permanent pacemakers inserted, Patient 6 declined, and Patient 8 was discharged from the hospital before an MRI scan could be obtained. Thirty-eight participants had neurological and 35 had neuropsychological assessments at 49 (SD, 15) days; Patient 3 declined and Patient 5 had moved out of the area; Patient 2 also moved out of area but could be seen by the study neurologist; and Patients 1 and 4 missed neuropsychological testing because of scheduling difficulties.
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Two of 40 (5%) participants had perioperative strokes with the development of new focal neurological symptoms and signs, Patient 13 in whom postoperative DWI showed new cerebral infarction and Patient 33 who had a pacemaker inserted and was unable to have an MRI but had clear evidence of new large confluent cerebral infarction on CT scanning. Sixteen of 37 (43%) participants with postoperative imaging had evidence of new cerebral ischemia (range, 1 to 14 lesions) of whom only 2 (13%) had a stroke diagnosed clinically (Figure). This includes Patient 33 with a pacemaker but a perioperative infarct seen on CT scan. In 13 of 16 patients with postoperative ischemia, the lesions were small (<1 cm3) with larger confluent lesions in the remaining 3 patients. The distribution of the DWI lesions was middle cerebral artery (29%), the border zone between the middle cerebral artery and the anterior cerebral artery (23%) or the posterior cerebral artery (12%) and posterior circulation (36%), and 57% were on the left. DWI lesions occurred in more than one vascular territory in all patients with multiple lesions. Lesions were frequently cortical in location and both cortical and border zone lesions could be seen in the same patient consistent with an embolic pathogenesis (Figure). Patient 1 had 2 small (<0.2 cm3) clinically silent DWI lesions on the preoperative MRI, presumably as the complication of coronary angiography performed 24 hours earlier.
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Patients with and without postoperative DWI lesions were compared (Table 2). There were no differences in age, risk factors, EuroSCORE, CPB time, or length of stay between the 2 groups. However, patients with combined valve and CABG surgery were more likely to have postoperative ischemic change (Fisher exact, P=0.043). Logistic regression analyses also found that those with combined valve and CABG surgery were more likely to have postoperative DWI lesions (P=0.078; Table 3).
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Twenty-two of 35 (63%) patients had a decline in at least one neuropsychological measure and 12 (34%) a decline in at least 2 neuropsychological measures at 6 weeks (range, 1 to 4). In general, there were similar numbers of patients showing decline in tests of psychomotor speed, mental flexibility, and memory, whereas no patient showed a decline in working memory. Most participants had mild levels of anxiety and normal levels of depression on the Hospital Anxiety and Depression Scale at the presurgical assessment (mean [SD] anxiety: 7.3 [3.5]; depression: 4 [2.6]). Anxiety levels decreased in almost all patients after surgery (mean [SD] 5.1 [2.8], t[33]=4.442, P=0.000). Depression levels were stable compared with baseline with only one participant showing an increase to a mild level of depression (mean [SD] 3.3 [2.6], t[33]=1.666, P=0.105). Thus, any falloff in cognitive functioning was not due to an increase in anxiety or depression levels.
Thirty-two patients had both postoperative imaging and neuropsychological testing at 6 weeks. Of these 32 patients, all of those with postoperative DWI lesions (including Patient 33) had cognitive decline in at least one neuropsychological measure compared with 6 of 17 patients without postoperative ischemic change (Fisher exact test, P<0.001). Logistic regression analysis also found that cognitive decline was predicted by the presence of postoperative DWI lesions and not by age, gender, EuroSCORE, or CPB time (Table 3). These results were not materially altered with the sensitivity analysis (results not shown). Furthermore, there was an association between the number of abnormal cognitive tests and ischemic burden. A decline in 2 or more cognitive tests was seen in 6 of 8 patients with multiple DWI lesions or single lesions greater than 1 cm3 compared with 2 of 7 with a solitary DWI lesion and only 3 of 17 with no ischemic change (Fisher exact test, P<0.001).
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Discussion |
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This study has confirmed that neurological injury is common after cardiac valve surgery with approximately one in 20 patients having a stroke and 2 of 3 with cognitive decline at 6 weeks. In addition, almost half of patients have evidence of perioperative cerebral ischemia on DWI. Earlier studies have found rates of postoperative DWI lesions after valve surgery ranging from 29% to 47%9,11 with greater rates in those undergoing aortic valve surgery.8 New ischemic lesions were also more frequent in patients with combined valve and CABG surgery in keeping with the observation that these patients have a higher rate of stroke than those undergoing a single procedure.1 The DWI lesions have a distribution and appearance consistent with embolic pathogenesis, including a number in the watershed zones suggesting impaired emboli clearance due to hypoperfusion.28 In most cases, the new DWI lesions do not result in focal neurological symptoms and signs. However, they are not necessarily clinically silent, and this study has found that cognitive impairment is associated with perioperative ischemia and is more severe with greater ischemic load.
Transcranial Doppler and ultrasound studies show that high rates of embolization occur during cardiac surgery, particularly during aortic interventions.29–31 Solid emboli may arise from the CPB circuit, the surgical field, or aorta and include fibrin and platelet aggregates, silicone particles, atheroma, fat, and bone fragments. Gaseous emboli may emanate from the CPB circuit, arise from aortic cannulation and decannulation, or remain in the heart chambers and pulmonary veins after the heart is closed. Focal ischemia occurs when solid emboli or bubbles obstruct blood flow.32 Smaller bubbles may also damage the vascular endothelium and this may further reduce blood flow and disrupt the blood–brain barrier.33
Cognitive decline after otherwise successful surgery remains a major concern to patients and their families and results in increased medical costs, reduced perception of health, and lower rates of employment.2,6 Cognitive decline has been quoted as occurring in 50% to 88% of patients in the first week after cardiac surgery, falling to 30% to 70% after 6 weeks, and may persist at 1 year.1 However, this remains an area of controversy. The incidence of cognitive impairment varies depending on patient and surgical factors and is greater in those with preexisting ischemic white matter lesions and reduced cerebral reserve8,10,13,34 and when more complex surgical procedures are performed.3 The incidence of impairment is also affected by the tests used, the timing of testing, and the definitions of decline. This has led to a Statement of Consensus on Assessment of Neurobehavioural Outcomes After Cardiac Surgery in an attempt to standardize assessment,19 although it should be noted that this statement is now 12 years old and requires updating.35
The finding of an association between new ischemic lesions and cognitive impairment is in contrast to earlier studies in which no such association has been found.10–13 There are several explanations for these discrepant results. In this study, only patients with intracardiac procedures were included and these operations are more likely to result in ischemic damage. We ensured that the same neuropsychologist performed all tests in a standardized manner. Patients were screened for mood disturbance before and after surgery to ensure that testing was not affected by anxiety or depression, both of which can reduce performance. The tests used included all those recommended by consensus statements as well as 2 additional measures sensitive to functions shown to be compromised as a result of ischemic damage. This use of a standardized assessment is in contrast to some earlier studies. Knipp et al made use of a verbal learning test with fewer stimuli and recall trials compared with the measures used in this study.11,12 Bendszus et al restricted their neuropsychological examination to the use of 4 tests, only one of which is part of the recommended battery.10
The definition of change in cognitive performance after surgery is also controversial with the incidence of cognitive decline varying depending on which criteria are used.36 Most studies have used a decline of one or more SDs or a percentage change in cognitive tests from baseline to define change.37–39 We have used the RCI, which calculates the distribution of expected change around baseline performance using reliability coefficients and observed SDs of retest scores.24 This ensures the RCI is sensitive to change outside that of random variation. The categorization of retest scores into "changed" and "unchanged" is transparent, easily interpretable, and takes account of at least some of the major factors affecting test–retest performance.40,41 Some authors argue that the RCI method may not reliably identify clinically significant change.42,43 For example, a relatively small change in verbal memory may have more clinical impact than change of the same magnitude in processing speed, but this is a problem with other techniques as well. We defined cognitive impairment as a drop in performance from baseline in at least a single cognitive measure, because this takes into account the different potential etiologies, multifocal nature, and varying volumes of tissue affected and is in keeping with consensus recommendations.19 Having said this, we also found a clear relationship between abnormalities on 2 or more cognitive tests and multiple or larger ischemic lesions.
Not all patients with cognitive decline had evidence of new ischemic change for which there are a number of possible explanations. First, other nonembolic mechanisms of cognitive impairment such as hypoperfusion, microscopic air embolism, and cerebral and systemic inflammatory activation, among others, may still occur and result in cognitive impairment independent of cerebral embolization. Second, although the sensitivity of DWI is high, it is not 100% and will miss some lesions in patients with a clinical diagnosis of stroke. The spatial resolution of DWI is approximately 3 mm and is limited by pixel size and slice thickness. Cerebral damage has been demonstrated after exposure to gaseous bubbles as small as 15 µm, well below the spatial resolution of DWI.44 We speculate that the visible DWI lesions seen after surgery are likely to be the "tip of the iceberg" and may be a marker for more extensive ischemic change.
There are a number of limitations to this study. The numbers are small, and the CIs of our results are correspondingly large. We took a pragmatic approach and not all participants were able to have all of the investigations. Patients admitted to the hospital on the evening before surgery could not always have MRI scanning or cognitive testing. The use of a single neuropsychologist meant that it was not always possible to carry out testing. Two patients had cardiac pacemakers inserted perioperatively precluding follow-up MRI, and several other patients declined further MRI scans because of claustrophobia. The choice of timing of postoperative assessments was also pragmatic, with 6 weeks chosen to coincide with routine postoperative surgical follow-up, thereby limiting the number of clinic visits. A later cognitive assessment may have been more clinically relevant, but cognitive dysfunction in the postoperative period may predict further decline over the next 5 years.6 The inclusion of noncardiac surgery or age-matched, neurologically normal control subjects would also have been of interest because noncardiac surgery may also result in brain injury45,46; however, our aim was simply to investigate the relationship between cognitive impairment and embolic damage.
In summary, this study has found that in patients undergoing cardiac valve surgery, 5% will have a perioperative stroke, 43% will have new ischemic lesions on DWI in a pattern consistent with cerebral embolization, and 63% will have cognitive decline at 6 weeks. Cognitive decline is associated with perioperative ischemia and increases with greater ischemic load. The clinical significance of our results is self-evident, but there is also an important implication for research. Cardiac surgery with newer MRI techniques such as those used here may be a useful model of human stroke or vascular dementia.
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Acknowledgments |
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We thank the participants who took part in this study and the staff of the Cardiothoracic Surgery Unit and operating rooms at Auckland City Hospital and the Centre for Advanced Magnetic Resonance Imaging, University of Auckland. We also thank Varsha Parag who helped with statistical advice.
Sources of Funding
This study was funded by the Neurological Foundation and Heart Foundation of New Zealand.
Disclosures
None.
Received August 25, 2007; revision received September 15, 2007; accepted September 21, 2007.
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