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Interact CardioVasc Thorac Surg 2006;5:383-386. doi:10.1510/icvts.2005.126995
© 2006 European Association of Cardio-Thoracic Surgery

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Institutional report - Coronary

Brain magnetic resonance angiography-based strategy for stroke reduction in coronary artery bypass grafting

Yoshiyuki Takami* and Hiroshi Masumoto

Division of Cardiovascular Surgery, Kasugai Municipal Hospital, 1-1-1 Takagi-cho, Kasugai City, 486-8510, Japan

Received 18 December 2005; received in revised form 6 March 2006; accepted 3 April 2006

*Corresponding author: Tel.: +81-568-57-0057; fax: +81-568-57-0067.

E-mail address: cvs{at}hospital.kasugai.aichi.jp (Y. Takami).


    Abstract
 Top
 Abstract
 1. Introduction
 2. Subjects and methods
 3. Results
 4. Discussion
 References
 
We have been using magnetic resonance angiography (MRA) preoperatively to identify patients at increased risk of stroke in coronary artery bypass grafting (CABG). Based upon the intracranial MRA findings, either the off-pump or the on-pump procedure was selected. We report the results of our MRA-based strategy of CABG in 140 consecutive patients. Intracranial arterial lesions were found in 90 patients (64%). The most affected arteries were internal carotid (48%), followed by vertebral (18%) and middle cerebral (16%). Using the MRA score describing the severity of intracranial atherosclerosis, 35 patients with a score of ≥5 underwent off-pump, while 105 patients with a score of <5 underwent on-pump CABG. In the off-pump group, the patient age was older, the incidence of abnormal preoperative brain CT was higher, and the MRA score was higher (6.0±1.1 vs. 1.2±1.3 points) than in the on-pump groups. Even though the risk was higher in the off-pump group, the clinical outcomes were not significantly different, including the hospital mortality and the incidence of stroke and additional coronary intervention. In conclusion, the brain MRA-based selection of off-pump CABG can contribute to prevention of stroke in neurologically high-risk patients.

Key Words: Coronary artery bypass grafting; Stroke; Magnetic resonance angiography; Intracranial artery


    1. Introduction
 Top
 Abstract
 1. Introduction
 2. Subjects and methods
 3. Results
 4. Discussion
 References
 
Stroke, type 1 brain injury, after coronary artery bypass grafting (CABG) is a serious complication associated with high mortality, morbidity, and cost [1,2]. The reported rates have remained unchanged despite recent advances in surgical and anesthetic technologies. Cardiopulmonary bypass (CPB) could provide adverse neurologic effects, associated with a change in body temperature, a rapid reduction in hematocrit, and a loss of pulsatile flow. Avoiding CPB has been advocated to reduce the incidence of stroke. Recent studies revealed that off-pump CABG preserves cerebral perfusion well and reduces neurocognitive morbidity, especially in elderly patients [3,4].

Focused on the pathophysiologic cerebral perfusion, causing watershed infarction, with non-pulsatile flow during CPB [5], we hypothesize that the CABG patients with occlusive disease of intracranial arteries are at a high risk for stroke. To identify these patients, we use brain magnetic resonance angiography (MRA). Based upon the MRA findings, we have selected on-pump or off-pump CABG, using a scoring system established to describe the severity of intracranial atherosclerosis. We report our short-term results with the brain MRA-based procedural selection of CABG, on- or off-pump.


    2. Subjects and methods
 Top
 Abstract
 1. Introduction
 2. Subjects and methods
 3. Results
 4. Discussion
 References
 
2.1. Patients

A total of 156 consecutive patients undergoing elective CABG were enrolled in the present study. However, 16 patients were excluded because they underwent off-pump CABG for the following reasons; 8 patients who needed revascularization of the left anterior descending artery only, 4 patients who required an accompanying procedure for abdominal aortic aneurysm, and 4 patients who were on chronic hemodialysis. Therefore, a total of 140 patients (105 males and 35 females; mean age, 66±8 years) underwent the brain MRA-based procedural selection of CABG, on- or off-pump. For each patient, hypertension, diabetes mellitus, hyperlipidemia, smoking habit, and obesity were documented as coronary risk factors. For cerebrovascular evaluations, brain CT and intracranial MRA were performed preoperatively in all patients.

2.2. Brain MRA

Intracranial MRA examinations were performed with a 1.5-tesla magnetic resonance system (Signa Horizon LX, GE Healthcare, Buckinghamshire, UK). Images were acquired by a three-dimensional, Fourier transform time-of-flight method with a spoiled gradient-echo sequence. The repetition time was set for 30 ms, echo time for 3.2 ms, and a flip angle for 20°. The number of excitations per phase encoding was 1.0. A 259x160x140 matrix was used with a field of view of 160x1600 mm and a partition thickness of 1.0 mm, resulting in a 0.625x1.0x0.5 mm voxel. Nine projection images at 22.5° increments vertical and horizontal over a 180° range were provided.

2.3. MRA scoring system (Fig. 1)

A scoring system was developed to reflect the severity of intracranial occlusive arterial disease in the brain MRA. As shown in Fig. 1, we focused on bilateral arterial segments of internal carotid (ICA), anterior cerebral (ACA), middle cerebral (MCA), vertebral (VA), basilar (BA), and posterior cerebral (PCA) arteries. Degree of stenosis was divided into three grades depending on the narrowness of the arteries. A smooth arterial segment with <25% reduction of a diameter was graded as no lesion, and given a grading point of 0. An irregular artery with 25–49% stenosis was graded as mild, and given a grading point of 1. More than 50% stenosis, multiple lesions, or occlusion was graded as severe, and given a grading point of 3. The grading point of each arterial segment of the right and left arteries was summed to give the total MRA score. When the MRA score was ≥5 points, the patient was considered to be at high-risk for stroke and then off-pump was selected. The patients with the MRA score of <5 points were scheduled for on-pump CABG.


Figure 1
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Fig. 1. Anatomy of the focused intracranial arteries in the brain magnetic resonance angiography (MRA) and the MRA-based scoring system to select the on-pump or off-pump coronary artery bypass grafting.

ICA, internal carotid artery; ACA, anterior cerebral artery; MCA, middle cerebral artery; VA, vertebral artery; BA, basilar artery; PCA, posterior cerebral artery.

 
2.4. Surgical technique

In both on-pump and off-pump groups, median sternotomy was applied. In the on-pump patients, moderate hypothermic CPB was started with arterial cannulation on the ascending aorta, followed by aortic cross-clamping and antegrade/retrograde delivery of blood cardioplegic solution. Aortic anastomoses of the grafts were performed with a single crossclamp technique. In the off-pump patients, the target coronary artery was stabilized with the Genzyme stabilizer (Teleflex Medical, Research Triangle Park, NC, USA) or the OPVAC Synergy Stabilizer (ESTECH, Danville, CA, USA). Proximal aortic anastomosis was performed with the HEARTSTRING II Proximal Seal System (Guidant Co., Santa Clara, CA, USA).

2.5. Statistical analysis

All data were expressed as means±standard deviations. We used Fisher's exact test for analysis of discrete variables and Mann–Whitney U-test for analysis of continuous variables. A P-value of <0.05 was considered to be statistically significant.


    3. Results
 Top
 Abstract
 1. Introduction
 2. Subjects and methods
 3. Results
 4. Discussion
 References
 
3.1. Brain MRA findings

The status of intracranial arteries of patients is summarized in Table 1. Abnormal findings of the brain MRA, either stenotic or occluded, were obtained in 90 patients (64%). The most affected vessel was the ICA, observed in 67 patients (48%). The VA disease was found in 25 patients (18%), followed by MCA (22 patients, 16%), PCA (10 patients, 7%), ACA (6 patients, 4%), and BA (6 patients, 4%). The mean MRA score was 2.0±2.1 points in all patients. No patients with abnormal MRA underwent surgical interventions on the severe lesions before or during CABG, because they were neurologically asymptomatic.


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Table 1 MRA findings on a vessel basis

 
Fig. 2 shows a brain MR angiogram of a 68-year-old male patient with a left main trunk coronary disease. It reveals stenosis of the right MCA, giving an MRA score of 3, and the patient was scheduled for on-pump CABG. Fig. 3 shows a brain MR angiogram of a 70-year-old female patient with triple vessel coronary disease. It demonstrated severe stenosis of the right ICA and mild lesion of bilateral MCAs, BA, and bilateral VAs, giving an MRA score of 8, and the patient underwent off-pump CABG.


Figure 2
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Fig. 2. A brain magnetic resonance angiography (MRA) of a patient who was scheduled for on-pump coronary artery bypass grafting. The MRA-score was 3.

 

Figure 3
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Fig. 3. A brain magnetic resonance angiography (MRA) of a patient who was scheduled for off-pump coronary artery bypass grafting. The MRA-score was 8.

 
3.2. Comparison between off-pump and on-pump groups

Table 2 summarizes the comparison of the clinical characteristics, brain MRA findings, and surgical outcomes between the off-pump and on-pump patients. The mean age of the off-pump group was significantly older than that in the on-pump group (71±7 vs. 65±8 years). No significant differences were found in the prevalence of five coronary risk factors between the two groups, although the prevalence of patients on chronic hemodialysis was higher in the off-pump group. In the off-pump group, the percentage of the number of patients showing low density areas on the preoperative head CT was significantly greater than in the on-pump group (74 vs. 43%). With regard to MRA findings, the ICA was affected in all the patients in the off-pump group. The prevalences of the ICA and MCA lesions were significantly greater in the off-pump group than that in the on-pump group (ICA: 100 vs. 52%; MCA: 91 vs. 39%), while other arteries were affected similarly in both groups. The mean MRA score was significantly higher in the off-pump group than that in the on-pump group (6.0±1.1 vs. 1.2±1.3 points). Regarding the surgical outcomes, there were no significant differences in the incidences of stroke, hospital death, and additional coronary intervention between the two groups. Postoperative stroke with transient left hemiplegia occurred in one patient in the on-pump group, whose ascending aorta had proved to be extremely atheromatous when punched out for proximal anastomosis of the vein graft.


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Table 2 Comparison between off-pump and on-pump patients

 

    4. Discussion
 Top
 Abstract
 1. Introduction
 2. Subjects and methods
 3. Results
 4. Discussion
 References
 
The first finding of the present study is that the prevalence of intracranial lesions on MRA, according to our criteria, was 64% in CABG patients. Previous studies have shown a racial difference in prevalent site of atherosclerotic lesions [6, 7]. In whites, the extracranial arteries are more affected, while in Asians and blacks the intracranial arteries are more affected. In Japanese patients with ischemic heart disease, intracranial arterial stenosis coexisted in approximately 20% [7]. Also, intracranial stenosis was found in 40% of the Japanese patients scheduled for CABG [8], which seems lower than the prevalence in our study. The reasons for the high prevalence in our study include the small patient numbers, the different definition of stenosis, and the different patients' characteristics. In our study, the definition of the intracranial disease was more strict, including the mild stenosis of from 50 to 75%. In addition, our study enrolled more patients with diabetes (46%) and on chronic hemodialysis (6%), who may have more severe atherosclerotic disease.

There have been several studies to identify the predisposing factors to strokes after CABG [9, 10]. These include peripheral vascular disease, carotid artery disease, age, history of stroke, calcified aorta, duration of CPB, renal failure, smoking, diabetes mellitus, female, urgent or emergency, and ejection fraction <40%. There has been no evidence that intracranial arterial disease is a risk factor for stroke. However, the prevalence of intracranial disease was unexpectedly high, especially in Asians, as demonstrated in our study. Furthermore, hypoperfusion during CPB may be a strong risk factor associated with watershed infarction, as suggested by McKhann et al. [11]. Therefore, intracranial arterial disease should be considered as a risk factor for stroke, although we need further prospective and multicenter studies.

Second, we have established the MRA score system to quantify the severity of the intracranial artery disease. The MRA is a non-invasive neuroimaging modality with proven high sensitivity and specificity, comparable with the conventional angiography [7]. To evaluate the carotid arteries, duplex ultrasonography (DUS) is useful, however, this cannot be applied for examination of intracranial disease. The MRA has a significantly better discriminatory power than DUS for the detection of carotid artery stenosis [12, 13]. In addition, the intracranial MRA reflects the extracranial disease, although it shows so static a morphology that it is difficult to determine the intactness of the circle of Willis. Improved MRA technology provides us with detailed and precise evaluation of extra- and intracranial artery systems. Our study is the first in which an MRA scoring system is introduced into a preoperative evaluation of intracranial arteries in CABG patients. Scoring enables us to quantitatively describe the severity of the intracranial artery disease and to hold the information in common.

The third finding of our study is that the brain MRA-based strategy may be useful to prevent stroke in CABG patients. Our strategy is based on the premise that off-pump CABG reduces the incidence of stroke, as reported in the recent studies [3, 4]. In this study, we applied off-pump CABG to the patients with the MRA score of ≥5. As shown in Table 2, our procedural selection may be adequate with regards to the incidence of stroke and quality of revascularization.

Some surgeons may advocate that we should perform off-pump CABG in all patients. However, we think that on-pump CABG should be the first choice of procedure and that off-pump with more technical difficulties should be applied in selected patients. The brain MRA is useful as a non-invasive preoperative examination for the patient selection for off-pump CABG.

One limitation of this study is that it is an institutional observation study. To show the usefulness of our strategy, it is necessary to compare the on-pump and off-pump cases in only patients with the MRA score of ≥5. However, it was not possible for us to select on-pump in such high-risk patients with severe intracranial atherosclerosis. Further non-randomized studies are also necessary. Another limitation is that stroke occurred in one patients undergoing on-pump, even though the pre-operative MRA score was 2. In this patient, the ascending aorta was severely atherosclerotic when observed at the time of the proximal anastomosis. The cause of stroke was speculated to be embolization of the aortic atheroma. One of the most probable causes of stroke after CABG is cerebral embolization of atherosclerotic plaque debris from the ascending aorta [14]. To eliminate the stroke incidence, it is necessary for us to incorporate the intraoperative epiaortic echographic scanning to identify the degree of ascending aortic atherosclerosis or aorta-no-touch technique, as advocated by Hangler et al. [15], in combination with the intracranial MRA-based strategy.


    References
 Top
 Abstract
 1. Introduction
 2. Subjects and methods
 3. Results
 4. Discussion
 References
 

  1. Roach GW, Kanchuger M, Mangano CM, Newman M, Nussmeier N, Wolman R, Aggarwal A, Marschall K, Graham SH, Ley C. Adverse cerebral outcomes after coronary bypass surgery. N Engl J Med 1996; 335:1857–1863.[Abstract/Free Full Text]
  2. Puskas JD, Winston AD, Wright CE, Gott JP, Brown III WM, Craver JM, Jones EL, Guyton RA, Weintraub WS. Stroke after coronary artery operation: incidence, correlates, outcome, and cost. Ann Thorac Surg 2000; 69:1053–1056.[Abstract/Free Full Text]
  3. Lee JD, Lee SJ, Tsushima WT, Yamauchi H, Lau WT, Popper J, Stein A, Johnson D, Lee D, Petrovitch H, Dang CR. Benefits of off-pump bypass on neurologic and clinical morbidity: a prospective randomized trial. Ann Thorac Surg 2003; 76:18–26.[Abstract/Free Full Text]
  4. Athanasiou T, Al-Ruzzeh S, Kumar P, Crossman MC, Amrani M, Pepper JR, Del Stanbridge R, Casula R, Glenville B. Off-pump myocardial revascularization is associated with less incidence of stroke in elderly patients. Ann Thorac Surg 2004; 77:745–753.[Abstract/Free Full Text]
  5. In: Gravlee GP, Davis RF, Kurusz M, Utley JR. editors Cardiopulmonary bypass: principles and practice 2 2000;Philadelphia: Lippincott Williams & Wilkins.
  6. Gaplan LR, Gorelick PB, Hiler DB. Race, sex and occlusive cerebrovascular disease: a review. Stroke 1986; 17:648–655.[Free Full Text]
  7. Uehara T, Tabuchi M, Hayashi T, Kurogane H, Yamadori A. Asymptomatic occlusive lesions of carotid and intracranial arteries in Japanese patients with ischemic heart disease: evaluation by brain magnetic resonance angiography. Stroke 1996; 27:393–397.[Abstract/Free Full Text]
  8. Uehara T, Tabuchi M, Kozawa S, Mori E. MR angiographic evaluation of carotid and intracranial arteries in Japanese patients scheduled for coronary artery bypass grafting. Cerebrovasc Dis 2001; 11:341–345.[CrossRef][Medline]
  9. Mickleborough LL, Walker PM, Takagi Y, Ohasshi M, Ivanov J, Tamariz M. Risk factors for stroke in patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg 1996; 112:1250–1258.[Abstract/Free Full Text]
  10. Charlesworth DC, Likosky DS, Marrin CAS, Maloney CT, Quinton HB, Morton JR, Leavitt BJ, Clough RA, O'Connor GT. Northern New England Cardiovascular Disease Study Group. Development and validation of a prediction model for strokes after coronary artery bypass grafting. Ann Thorac Surg 2003; 76:436–443.[Abstract/Free Full Text]
  11. McKhann GM, Goldsborough MA, Borowicz Jr LM, Mellits ED, Brookmeyer R, Quaskey SA, Baumgartner WA, Cameron DE, Stuart RS, Gardner TJ. Predictors of stroke risk in coronary atery bypass patients. Ann Thorac Surg 1997; 63:516–521.[Abstract/Free Full Text]
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  14. Kapentanakis EI, Stamou SC, Dullum MKC, Hill PC, Haile E, Boyce SW, Bafi AS, Petro KR, Corso PJ. The impact of aortic manipulation on neurologic outcome after coronary artery bypass surgery: a risk-adjusted study. Ann Thorac Surg 2004; 78:1564–1571.[Abstract/Free Full Text]
  15. Hangler HB, Nagele G, Danzmayr M, Mueller L, Ruttmann E, Laufer G, Bonatti J. Modification of surgical technique for ascending aortic atherosclerosis: impact on stroke reduction in coronary artery bypass grafting. J Thorac Cardiovasc Surg 2003; 126:391–400.[Abstract/Free Full Text]




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