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Ann Thorac Surg 2009;88:476-481. doi:10.1016/j.athoracsur.2009.04.019
© 2009 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Leukoaraiosis and Hippocampal Atrophy Predict Neurologic Outcome in Patients Who Undergo Total Aortic Arch Replacement

Naoto Morimoto, MDa,*, Kenji Okada, MDa, Kensuke Uotani, MDb, Fumio Kanda, MDc, Yutaka Okita, MDa

a Division of Cardiovascular Surgery, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan
b Division of Radiology, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan
c Division of Neurology, Kobe University Graduate School of Medicine, Kobe, Hyogo, Japan

Accepted for publication April 8, 2009.

* Address correspondence to Dr Morimoto, Division of Cardiovascular Surgery, Kobe University, 7-5-1 Kusunoki-cho, Chuuo-ku, Kobe, Hyogo, 650–0017, Japan (Email: naotofrcs{at}gmail.com).

Presented at the Poster Session of the Forty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Francisco, CA, Jan 26–28, 2009.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: This retrospective study determined whether leukoaraiosis and hippocampal atrophy seen in preoperative magnetic resonance imaging (MRI) predict neurologic outcome after total aortic arch replacement.

Methods: From August 2001 to November 2007, 131 consecutive patients (22% women) who underwent elective total arch replacement with selective cerebral perfusion were enrolled. Mean patient age was 71 ± 17 years (range, 27 to 88 years). On preoperative MRI, mean leukoaraiosis score and hippocampal atrophy score, rated according to the Scheltens scale, were 11.0 ± 9.2 and 1.5 ± 1.9, respectively. Forty-three patients (32.8%) had carotid or basilica arterial stenosis, 18 (12.6%) had a stroke, and 6 (4.2%) had a transient ischemic attack.

Results: One hospital death (0.8%) occurred. Adverse perioperative neurologic events included intraoperative stroke in 8 (6.1%), postoperative stroke in 2 (1.5%), and temporary neurologic dysfunction (TND) in 11 (8.4%). On multivariate logistic regression, significant predictors of postoperative intraoperative stroke were leukoaraiosis (odds ratio [OR], 1.1, p = 0.02) and aortic arch atheroma (OR, 2.4; p = 0.001). TND was significantly associated with leukoaraiosis (OR, 1.1, p = 0.03) and hippocampal atrophy (OR, 1.6, p = 0.01). The best cutoff value for predicting intraoperative stroke was a leukoaraiosis score exceeding 16 (sensitivity, 70%; specificity, 70%); that for predicting TND was a leukoaraiosis score exceeding 18 (sensitivity, 82%; specificity, 77%) and a hippocampal atrophy score exceeding 2 (sensitivity, 82%; specificity, 76%).

Conclusions: Leukoaraiosis and hippocampal atrophy are significant independent factors for adverse neurologic outcome after total arch replacement.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
With recent improvement in surgical technique of aortic arch reconstruction and cerebral protection, outcomes of aortic arch aneurysm operations have remarkably improved. However, perioperative brain damage resulting in stroke or transient neurologic dysfunction remains a major source of mortality and morbidity after aortic arch operations.

Chronic ischemic neuroimaging abnormalities have often been demonstrated by brain magnetic resonance imaging (MRI) of patients who anticipated cardiovascular operations. Leukoaraiosis is patchy punctuate or confluent hyperintensity in the white matter and deep gray nuclei on a T2-weighted image. This white matter hyperintensity reflects chronic ischemic damage of myelin and axon [1]. It is often associated with mild cognitive decline and vascular dementia [2], and prior studies suggest that leukoaraiosis predicts future risk of stroke and disability [3]. Hippocampal atrophy was seen in patients with vascular dementia and associated with cognitive impairment as well as leukoaraiosis [4]. These neuroradiologic abnormalities are important as a marker of neuron damage due to arteriosclerotic microangiopathy.

In this study, we aimed to identify features of leukoaraiosis and hippocampal atrophy that predict neurologic outcome after total arch replacement.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
This retrospective cohort study was approved by our local Institutional Review Board, which waived the need for patient consent because of the retrospective study nature.

Patients
This retrospective study enrolled 131 consecutive patients (99 men; mean age, 71 ± 17 years) undergoing elective total aortic arch replacement with selective cerebral perfusion (SCP) under deep hypothermia through a middle sternotomy between August 2001 and November 2007. Excluded were 30 patients who underwent emergency operations for acute aortic dissection and (impending) aortic rupture. The indication for total aortic arch replacement was a transverse or distal arch aneurysm that did not extend below the level of the carina.

Neuromagnetic Imaging
Brain MRI was performed using a 1.5-T scanner. A standardized imaging protocol was used, consisting of axial T1-weighted, T2-weighted, and fast fluid-attenuated inversion recovery (FLAIR), as well as coronal FLAIR image. The intracranial and extracranial vasculature was evaluated preoperatively using magnetic resonance angiography (MRA). All patients underwent routine 2-dimensional time of flight MRA through the neck and 3-dimensional time of flight MRA through the circle of Willis. Carotid stenosis was defined as greater than 50% stenosis.

Leukoaraiosis Rating
Leukoaraiosis were rated using the Scheltens scale [5] (Fig 1A, B). Each cerebral region was initially scored on the size of the lesions, then on their number. In accordance with this scale, the periventricular white matter hyperintensities were scored on three regions: the frontal and occipital caps, and the periventricular bands. They were rated as none, score 0; 5 mm or less, score 1; and confluent lesions and greater than 5 mm, score 2. The deep white matter hyperintensities were examined in four subcortical regions (frontal, parietal, temporal and occipital lobes). These lesions were rated as none, score 0; 3 mm and smaller and 5 or fewer lesions, score 1; 3 mm or smaller and 6 or more lesions, score 2; 4 to 10 mm and 5 or fewer lesions, score 3; 4 to 10 mm and 6 or more lesions, score 4; 10 mm or larger and 1 or more lesions, score 5; and large confluent lesions, score 6. The total leukoaraiosis score is the sum of the periventricular white matter intensities and deep white matter hyperintensities subscores for a maximum score of 30.


Figure 1
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  		Fig 1. (A) Magnetic resonance images of moderate leukoaraiosis (score = 13). (B) Magnetic resonance image of severe leukoaraiosis (score = 30). (C) Hippocampal atrophy was scored from coronal views of T1-weighted images.

 
Hippocampal Atrophy Rating
Extent of right and left hippocampal atrophy (Fig 1C) was rated using the Scheltens scale [6] from T1-weighted coronal images. This scale rates atrophy as absent, 0; minimal, 1; mild, 2; moderate, 3; and severe, 4, based on the width of the surrounding cerebrospinal spaces and the height of hippocampal formation. Left and right scores were summed to give an overall combined hippocampal atrophy score for a maximum score of 8.

Characteristics of patients by severity of leukoaraiosis and hippocampal atrophy are reported in Table 1. Figure 1 shows the MRI scans of varying leukoaraiosis and hippocampal atrophy severity and their corresponding scores, respectively. Quantitative analysis of MRI was performed by the neuroradiologist (K. U.), who was blind to patient outcomes.


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  		Table 1 Preoperative Variables
 
Grading of Aortic or Arch Vessel Atheroma
According to the appearance of the aortic arch when it was opened, severity of atheroma in the aorta and the orifice of arch vessels was scored by the surgeons (K.O. and Y.O.) as 1; normal, 2; intimal thickness, 3; atheroma less than 4 mm, 4; atheroma exceeding 4 mm, 5; mobile atheroma. Epiaortic imaging was performed by the surgeon immediately before arterial cannulation for cardiopulmonary bypass (CPB). A 5.0/7.5-MHz epiaortic probe was manipulated to obtain both transverse and longitudinal images along the entire ascending aorta and proximal aortic arch. Epiaortic ultrasound images were reviewed and graded on a 5-point scale [7]. Discrepancies between ultrasound and macroscopic findings were resolved by 3 investigators (N. M., K. O., and Y. O.), with consensus.

Surgical Technique
Standard anesthesia for total arch replacement was induced with an intravenous bolus injection of midazolam (0.3 mg/kg) and fentanyl (10 µg/kg) and was maintained with a continuous infusion of propofol (3 mg/kg/h) and continuous inhalation of sevoflurane (0.5 minimum alveolar concentration) throughout procedure. Neuromuscular block was achieved by vecuronium bromide (0.1 mg/kg).

Standard CPB technique included nonpulsatile flow, membrane oxygenator, arterial line filter, hypothermia ranging from 18° to 23°C, and alpha-stat method for acid-base management. Cardioplegic arrest was achieved by cold crystalloid cardioplegic solution (St. Thomas) and maintained with cold blood cardioplegia. The cannulation site for arterial return was selected meticulously by preoperative computed tomography (CT) scan and by an intraoperative epiaortic sonography of the ascending aorta and aortic arch. When moderate to severe atheromatous plaque or ulceration was detected in the ascending aorta or when the ascending aorta was dissected, femoral cannulation or additional cannulation into the right axillary artery with femoral cannulation was used.

The whole aortic arch was replaced using a quadrifurcated collagen or a gelatin-impregnated woven Dacron graft (DuPont, Wilmington, DE). Open distal anastomosis was performed consistently with complete transection of descending aorta. Reperfusion and rewarming were always achieved in an antegrade manner through the side branch of the graft.

Brain Protection
Our principle in SCP included arterial cannulation performed with a balloon-tipped cannula inserted directly in the brachiocephalic artery from inside the aortic arch, as well as in the left common carotid artery and left subclavian artery. Cerebral perfusion flow was maintained at 12 to 15 mL/kg/min; mean pressure in the right and left radial artery ranged from 45 to 60 mm Hg, and regional oxygen saturation of bilateral frontal cortex was maintained more than the value at the initiation of CPB. The arch vessels, the left subclavian artery, the left common carotid artery, and the brachiocephalic artery were anastomosed to side branches, respectively. Intraoperative variables were demonstrated in Table 2.


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  		Table 2 Intraoperative Variables
 
Neurologic Outcome Assessment
On extubation and removal of the monitoring lines, all patients underwent the same basic physical examination. No precise neuropsychometric testing was performed on this patient population by the neurologist (F. K.) unless an abnormality was noted by physical examination. Neurologic complications were characterized as temporary neurologic dysfunction (TND) or permanent neurologic dysfunction (that is, completed stroke). MRI or CT imaging was performed in all patients with a suspected neurologic complication. CT was examined only if MRI was contraindicated. TND was defined as a Glasgow coma scale value of less than 13. These patients typically present with transient loss of orientation, slurred language, agitation, and no clear response to commands, with no structural abnormality in the brain detectable by the imaging methods. More subtle forms of neurologic dysfunction, consisting for example of minimal disorientation and agitation that did not require sedative medication, were not recognized as TND in the current study.

Stroke was defined as a new motor or sensory deficit that was confirmed by postoperative MRI or CT of the brain. Strokes were classified by time of onset as intraoperative or postoperative. Intraoperative stroke was defined as a new neurologic deficit presented on awakening after the operation; whereas in postoperative stroke, neurologic deficits developed in the patient after normal awakening.

Statistical Analysis
Statistical analysis was done with SPSS 11.0 software (SPSS Inc, Chicago, IL). Univariate associations between potential predictors were analyzed using the Fisher exact test for categoric variables and a t test for continuous variables. Stepwise logistic regression was performed on variables with a value of p < 0.20 from the univariate analyses to determine independent predictors of postoperative stroke and temporary neurologic dysfunction. Results were reported as odds ratio (OR) with associated 95% confidence intervals (CI).

Calculation of the area under the curve (AUC) of the receiver operating characteristics (ROC), with 95% CI, was used to evaluate diagnostic accuracy by using a semiparametric method. Cutoff values for the highest sensitivity and specificity were identified. On the basis of the cutoff value, sensitivity, specificity, positive predictive value, negative predictive value, and positive and negative likelihood ratio were calculated.


   Results
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 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Hospital mortality was 0.8% (1 of 131), and 17 (13.0%) central nervous system neurologic complications were recorded. Postoperative MRI studies of the brain were performed in 15 patients who showed symptoms of neurologic complications, whereas brain CT was performed in 4 patients. Adverse neurologic events consisted of perioperative strokes in 8 patients, of whom 6 (75%) had resolved or improved to baseline at the time of hospital discharge. Neurologic dysfunctions were temporary in 11 patients (8.4%), and all were resolved at the time of hospital discharge.

Univariate analysis of risk factors revealed that leukoaraiosis score (p = 0.01), CPB time (p = 0.05), aortic arch atheroma grade (p < 0.001), episode of stroke (p = 0.04), and episode of transient ischemic attack (p = 0.03) affected the rate of intraoperative stroke (Table 3).


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  		Table 3 Univariate Analysis
 
Multivariate analysis revealed that leukoaraiosis score (p = 0.02) and arch vessel atheroma grade (p = 0.001) were predictors of intraoperative stroke and that leukoaraiosis score (p = 0.02) and hippocampal atrophy score (p = 0.001) were significantly associated with TND (Table 4). ROC analysis showed that leukoaraiosis had a good predictive value for intraoperative stroke (AUC, 0.75 ± 0.07; 95% CI, 0.61 to 0.89; p = 0.01). The best cutoff value for predicting intraoperative stroke was a leukoaraiosis score of 16 (sensitivity, 70%; specificity, 70%; Fig 2A). ROC analysis for TND showed that leukoaraiosis had a good predictive value (AUC, 0.80 ± 0.07; 95% CI, 0.67 to 0.93; p = 0.001) as well as hippocampal atrophy score (AUC, 0.84 ± 0.04; 95% CI, 0.76 to 0.93; p < 0.001). The best cutoff value for predicting watershed stroke was a leukoaraiosis score of 18 (sensitivity, 82%; specificity, 77%; Fig 2B) and a hippocampal atrophy score of 2 (sensitivity, 82%; specificity, 76%, Fig 2C).


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  		Table 4 Multivariate Analysis
 

Figure 2
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  		Fig 2. Best cutoff values obtained from receiver operating characteristic analysis. (A) Leukoaraiosis score predicting intraoperative stroke. (B) Leukoaraiosis score predicting temporary neurologic dysfunction (TND). (C) Hippocampal atrophy score predicting TND.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
In the last decades, technical improvements in CPB, myocardial protection, and intensive care have reduced the mortality and morbidity associated with operations on the thoracic aorta. The brain protection methods currently used are profound hypothermic circulatory arrest, with or without retrograde cerebral perfusion, and SCP. A prospective comparative study by Okita and associates [7] demonstrated SCP significantly reduced the prevalence of temporary neurologic dysfunction compared with retrograde cerebral perfusion. Recently Ogino and associates [8] reported that SCP with right axillary artery perfusion had a protective effect against stroke (3.3%). Even if SCP is an accepted strategy to improve brain protection during operations in the aortic arch, a recent study focusing on brain microembolization measures with transcranial Doppler showed a small amount of microemboli can be detected during SCP [9]. The reported stroke rate of retrograde cerebral perfusion in an experienced large center was 2.4% to 3% [10, 11].

Two distinct pathophysiologic mechanisms cause brain damage. Stroke after aortic arch operations usually results from brain emboli and is unlikely to be influenced by the method of brain protection, unless the operation is prolonged [12]. TND is diffuse cerebral damage caused by inadequate brain protection. Anoxic neuron injury occurs inevitably after 25 to 30 minutes of circulatory arrest at 15°C [13]. Although no supportive data have demonstrated that retrograde cerebral perfusion extended the safe period of circulatory arrest more than 30 minutes, SCP was safer for patients whose brain protection time was more than 90 minutes [14].

In recent reports, SCP successfully decreased the TND rate, but stroke rate was not decreased. Identification of risk factors for perioperative neurologic injury remains an important goal to achieve adequate brain protection during aortic arch operations.

Leukoaraiosis is patchy punctuate or confluent hyperintensity in the white matter and deep gray nuclei on T2-weighted image. This white matter hyperintensity reflects chronic ischemic damage to myelin and axons [15]. Histologically, white matter lesions shows myelin pallor, mild gliosis, and tissue rarefaction associated with loss of myelin and axons. Severe arteriosclerosis and arteriolosclerosis usually coexist with leukoaraiosis. Leukoaraiosis is incomplete infarction produced by occlusions of microvessels or chronic hypoperfusion that is undetected by clinical symptoms or by focal neuroimaging changes. The extent of leukoaraiosis may be a marker for the severity of deep brain hypoperfusion due to arteriosclerosis and arteriolosclerosis [16]. Although the clinical significance has not yet been fully elucidated, several studies demonstrated a significant relationship between increased stroke risk and leukoaraiosis. Prior study [17] demonstrated that TND was likely to develop in patients with severe leukoaraiosis. This is consistent with our findings: We found also significant correlation with leukoaraiosis and intraoperative stroke.

Our findings showed a clear relationship between the preoperative hippocampal atrophy score and the development of TND. The hippocampus has a role in emotional life, learning, and especially short-term memory, and is crucial for normal brain function. From studies using well-established models of transient global ischemia in rats, gerbils and mice, the neurons in the CA1 area of the hippocampus are most vulnerable to ischemic insult in the brain [18]. The hippocampus is also sensitive to anoxic injury because of its high metabolic demand [19]. It is quite possible that the impairment in memory function in patients with inadequate brain protection is related to neuronal injury in the hippocampus. The size of the hippocampus was correlated with the number of neuronal cells in the hippocampus. The hippocampal atrophy score might reflect the vulnerability to brain ischemia and past episodes causing apoptosis in neuronal cells in the hippocampus.

Although the clinical significance of hippocampal atrophy for predicting neurologic outcome may be equal to leukoaraiosis, hippocampal atrophy was not a predictor of stroke in this study. However, the wide use of the hippocampal atrophy score is superior to leukoaraiosis because it can be estimated by CT imaging.

The severity of atheroma in arch branches was associated with postoperative embolic stroke in this study. Recent reports indicated that most permanent neurologic injuries were due to strokes resulting from embolic phenomena and were not directly related to the method of brain protection. In an autopsy study, Amerenco and associates [20] reported that the prevalence of ulcerated plaques in the aortic arch was 28% in 183 patients with brain infarcts and 20% in 56 patients with brain hemorrhage. Blauth and associates [21] demonstrated a direct correlation among age, severe atherosclerosis of ascending aorta, and atheroemboli. The assessment of atheroma is essential to reduce the incidence of embolic stroke. An arterial cannulation site should be decided according to preoperative CT, MRI, carotid ultrasonography, and intraoperative epiaortic scanning.

We conclude that leukoaraiosis and hippocampal atrophy were significant independent predictors for neurologic outcome in patients who underwent total arch replacement.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Schmidt R, Scheltens P, Erkinjuntti T, et al. White matter lesion progression A surrogate endpoint for trials in cerebral small-vessel disease Neurology 2004;63:139-144.[Abstract/Free Full Text]
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  4. Fein G, Di Sclafani V, Tanabe J, et al. Hippocampal atrophy predict dementia in subcortical ischemic vascular disease Neurology 2000;55:1626-1635.[Abstract/Free Full Text]
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  6. Scheltens P, Leys D, Barkhof F, et al. Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates J Neurol Neurosurg Psychiatr 1992;55:967-972.[Abstract/Free Full Text]
  7. Okita Y, Minatoya K, Tagusari O, et al. Prospective comparative study of brain protection in total aortic arch replacement: deep hypothermic circulatory arrest with retrograde cerebral perfusion or selective antegrade cerebral perfusion Ann Thorac Surg 2001;72:72-79.[Abstract/Free Full Text]
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  12. Ergin MA, Griepp EB, Lansman SL, et al. Hypothermic circulatory arrest and other methods of cerebral protection during operations on the thoracic aorta J Card Surg 1994;9:525-537.[Medline]
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