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Ann Thorac Surg 2001;71:1905-1912
© 2001 The Society of Thoracic Surgeons
a Center for Aortic Surgery, Lahey Clinic, Burlington, USA
b Department of Surgery, Tufts University, Boston, MA, USA
c Department of Neurology, Tufts University, Boston, MA, USA
d Department of Biostatistics, Tufts University, Boston, MA, USA
e Department of Anesthesia, Tufts University, Boston, MA, USA
Accepted for publication January 3, 2001.
Address reprint requests to Dr Svensson, Lahey Clinic, 41 Mall Road, Burlington, MA 01805
e-mail: lars_g_svensson{at}lahey.org
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Abstract |
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 Top Abstract IntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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Methods. Of 139 potential aortic arch repairs (denominator), we randomized 30 patients to either DHCA alone (n = 10), DHCA plus retrograde brain perfusion (RBP) (n = 10), or antegrade perfusion (ANTE) (n = 10); a further 5 coronary bypass (CAB) patients were controls. Fifty-one neurocognitive subscores were obtained for each patient at each of four intervals: preoperatively, 3 to 6 days postoperatively, 2 to 3 weeks postoperatively, and 6 months postoperatively. Intraoperative and postoperative S-100 blood levels and electroencephalograms were also obtained.
Results. For the denominator, the 30-day and hospital survival rate was 97.8% (136 of 139) and the stroke rate 2.8% (4 of 139). For the randomized patients, the survival rate was 100% and no patient suffered a stroke or seizure. Circulatory arrest (CA) times were not different (DHCA:RBP:ANTE) for 11 total arch repairs (including 6 elephant trunk; mean, 41.4 minutes; standard deviation, 15). Hemi-arch repairs (n = 17) were quickest with DHCA (mean 10.0 minutes; standard deviation, 3.6; p = 0.011) and longest with ANTE (mean 23.8 minutes; standard deviation, 10.28; p = 0.004). Of the patients, 96% had clinical neurocognitive impairment at 3 to 6 days, but by 2 to 3 weeks only 9% had a residual new deficit (1 DHCA, 1 RBP, 1 ANTE), and by 6 months these 3 patients had recovered. Comparison of postoperative mean scores showed the DHCA group did better than RBP patients in 5 of 7 significantly different (p < 0.05) scores and versus 9 of 9 ANTE patients. There were no S-100 level differences between CA groups, but levels were significantly higher versus the CAB controls, particularly at the end of bypass (p < 0.0001); however, these may have been influenced by other variables such as greater pump time, cardiotomy use, and postoperative autotransfusion. Circulatory arrest (p = 0.01) and pump time (p = 0.057) correlated with peak S-100 levels.
Conclusions. The results of hypothermic arrest have improved; however, there is no neurocognitive advantage with RBP or ANTE. Nevertheless, retrograde brain perfusion may, in a larger study, potentially reduce the risk of strokes related to embolic material. S-100 levels may be artificial. In patients with severe atheroma or high risk for embolic strokes, we use a combination of retrograde and antegrade perfusion on a selective basis.
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Introduction |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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Between July 31, 1996 and May 18, 1999 (the date of the operation of the last randomized patient), 139 denominator patients were to undergo repairs (30 of which were included in this prospective randomized study). Five elective CAB patients served as controls. Three CAB patients had peripheral vascular disease, 2 patients had diabetes, 1 patient had a carotid stenosis, and 1 patient had a history of congestive heart failure. The 30 patients who were to have DHCA for aortic arch operations, were randomly assigned by opaque envelopes to three equal groups for DHCA, ANTE, and RBP. Exclusion criteria were patients more than 75 years (n = 27), patients undergoing emergency operations (n = 30) or urgent operations (n = 48), or patients who had residual deficits from previous strokes. Also excluded were left thoracotomy, deep hypothermic arrest patients. More than one exclusion factor may have applied. The nonrandomized denominator patients were older, as expected (65.2 years versus 59.0 years, p = 0.033), but had no significant difference for incidence of dissection, reoperation, creatinine levels, forced expiratory volume in 1 second, pump time, circulatory arrest (for arrested patients, 22.7 minutes versus 26.7 minutes), day of extubation (2.6 days versus 1.3 days), or postoperative discharge (7.5 days versus 7.8 days).
Antegrade perfusion was performed by cannulation or attaching an end-to-side graft to the right subclavian artery and occluding the right innominate artery by using a balloon catheter with pressure transduction. The left common carotid artery was perfused by using an occluding balloon catheter also with pressure transduction (Table 1) [25]. Pressures were maintained at 40 to 60 mm Hg. Retrograde brain perfusion was performed by perfusing the superior vena cava at 300 to 500 mL/min with the superior vena cava snared and by keeping pressure measured with the central line in the superior vena cava between 25 and 35 mm Hg, as previously described in our first 50 patients [6, 11]. The patients were cooled using the 
-stat method of pH control [6] until all measured temperatures (tympanic, rectal, bladder, esophageal, and blood) were below 20°C and electroencephalogram silence was achieved at a sensitivity of 2 µV for 5 minutes. The patient’s head was packed in ice at the start of cooling. The electroencephalogram was repeated the morning after the operation. Sodium thiopental at 5 mg/kg and 200 mg lidocaine were given before circulatory arrest, and carbon dioxide gas was used to flood the operative field at 10 L/minute before opening the aorta and until the chest was closed. Magnesium sulfate (2 g) was given before clamp removal. The cardiopulmonary bypass circuit was primed with 25 g of mannitol and a further 12.5 g was given after circulatory arrest. A Leuko Guard LG-6 40 micron filter (Pall Biomedical, Portsmouth, UK) was used in the arterial line circuit. Anesthetics were managed with a balanced technique using narcotics, benzodiazepines, and isoflurane.
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Comparisons of the mean neurocognitive scores for the three circulatory arrest groups and also of the coronary artery bypass group were done by the independent t test at each of the four time intervals for the neurocognitive tests. Since our a priori intention was to compare treatment effects to determine differences between the groups, this comparison of means was the simplest and most accurate method without having to decide if deficits were present or not. We did not use change of scores because they are also not optimal. Initially, we intended to use double-multivariate repeated measures of analysis of variance (with fixed effects as well as group-time interactions). However, both a priori and post hoc power analyses revealed that such an analysis was inappropriate with the small sample size. For the longitudinal repeated measures of analysis of variance, we had 9% power to detect a 0.10 effect size in groups by time interaction, 22% power to detect a 0.10 between group difference, and 20% power to detect an effect of 0.10 within the groups over time. Therefore, linear and nonlinear trends were thus calculated using linear and polynomial contrasts and compared with each other. The results of trends did not reveal a consistent difference or advantage between groups. A priori power calculations are not reported here; the incidence of deficits after circulatory arrests were not known, and lack of a true population estimate compromised the integrity of these calculations. Coronary artery bypass studies had shown a wide incidence of postoperative deficits. The S-100 levels were compared at the 12 intervals as previously described using the t test.
In our previous report [25], we attempted to use the definitions of neurocognitive deficit, such as 20% decline in 20% of the tests, or one standard deviation decline in individual tests. These definitions are arbitrary and have not been correlated with clinical patient function. In this study, our neuropsychologist, however, made blinded clinical diagnoses of neuropsychological deficits based on overall assessments of the scores and the patient’s function, including the effect that the patient’s learning had to do with the tests. No patient required assessment by a neurologist. We believe this blinded analysis for our study was a better method of deciding when a neurocognitive deficit was present, although, clearly a different blinded neuropsychologist may have made a different determination. Thus, while this allowed for a blinded comparison of our groups, comparison with other studies should be done with caution. Ideally, a panel of neuropsychologists would evaluate a patient and reach a consensus, however, this method was not possible for this study. The coronary artery bypass group was used for the comparison with the CA patients to try to negate some of the influence of learning on test scores, anesthesia, and a short period of cardiopulmonary bypass. Clearly, we are also interested in whether the CA patients would do significantly worse than CAB patients. Nevertheless, because we did not have a group of nonoperated patients who underwent serial neurocognitive testing, we cannot correct for the effects of learning and repetition of testing on scores or negate the effects of anesthesia alone on scores.
Preoperatively, 13 randomized patients had chronic pulmonary disease (DHCA = 3, RBP = 5, ANTE = 5), 7 patients had peripheral vascular disease (DHCA = 3, RBP = 3, ANTE = 1), 4 patients had previously known neurologic deficits that they had recovered from (DHC A = 0, RBP = 3, ANTE = 1), and 1 RBP patient had diabetes. The operations performed on these patients, other than the repair of aortic arch aneurysms, included insertion of composite valve grafts in 16 patients (DHCA = 7, RBP = 4, ANTE = 5), coronary artery bypass surgery in 7 patients (DHCA = 3, RBP = 2, ANTE = 2), endarterectomy of the aorta or branch arteries in 5 patients (DHCA = 1, RBP = 3, ANTE = 1), repair of aortic dissection in 9 patients (DHCA = 3, RBP = 5, ANTE = 1), insertion of elephant trunk procedure in 6 patients (DHCA = 1, RBP = 4, ANTE = 1) [26], minimal access exposure in 5 patients (DHCA = 2, RBP = 1, ANTE = 2), and operations on 3 Marfan syndrome patients (DHCA = 0, RBP = 3, ANTE = 0). There were no statistically significant (p < 0.05) different patient variables between the groups. Of the 28 patients who underwent arch repairs, 24 donated autologous blood before operation, and 6 of these patients (25%) required an intraoperative homologous blood transfusion.
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Results |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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For the 11 patients who had the entire aortic arch replaced, including six elephant trunk procedures, the mean period of circulatory arrest time was 41.4 minutes (standard deviation ± 15 minutes) with no difference between DHCA (n = 3), RBP (n = 5), or ANTE (n = 3) (p = not significant). Hemi-arch repairs (n = 17), however, were most quickly performed with DHCA (7 beveled hemi-arches) (10.0 minutes, standard deviation ± 0.36 minutes, p = 0.011) while ANTE (1 open distal ascending, 4 beveled arches, 1 tongue replacement of the entire arch) took the longest (23.8 minutes, standard deviation ± 10.28 minutes, p = 0.004) reflecting the time required to insert and also remove the innominate and common carotid balloon catheters, in addition to working around the catheters. The mean, range, and number of patients with circulatory arrest times greater than 60 minutes for each group were: DHCA, –21.05 minutes, 7 to 57 minutes, and 0; RBP, –27.6 minutes, 15 to 48 minutes, and 0; and ANTE, –32.1 minutes, 15 to 66, and 1. The mean time to extubation after operation was 1.33 days (minimum = 0.5 days, maximum = 3.5 days, standard deviation ± 0.74 days). By blinded clinical assessment of neurocognitive function during testing of the 28 circulatory arrest patients, 38% of patients had a preoperative deficit and 96% of patients had a neurocognitive deficit 3 to 6 days after operation, although most of the patients still required narcotic pain medication at this stage. After discharge from the hospital and testing 2 to 3 weeks after the operation, 9% of patients (3 of 28) still showed a persistent new deficit as determined by our neuropsychologist: 1 patient in each group (1 DHCA, 1 RBP, 1 ANTE). Approximately 6 months after operation, however, all 3 of these patients had recovered. Similarly, none of the CAB patients had acquired a new deficit at 2 to 3 weeks, or at 6 months after operation.
Comparison of the 51 mean preoperative subscores obtained showed no statistically significant differences between the groups across the preoperative subscores. However, postoperative comparison of all patients revealed DHCA patients performed better than RBP patients on five of seven subscores at the p less than 0.05 level of significance (Table 2). In addition, the DHCA patients performed better than the ANTE patients in 9 of 9 postoperative subscores at the p less than 0.05 level of significance. Thus, DHCA patients performed better than either RBP or ANTE patients postoperatively. Polynomial contrast analysis of trends failed to show a distinct advantage for any circulatory arrest group or CAB group.
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Postoperative complications in this series of patients included atrial fibrillation in 10 patients, temporary hoarseness in 1 patient, temporary reintubations in 2 patients, with 1 patient requiring stapling of apical blebs associated with severe chronic obstructive pulmonary disease, transient ventricular arrhythmias in 2 patients, and no perioperative myocardial infarcts. Preoperatively 1 RBP patient had two 30-second episodes of blurred vision and visual field loss with left-sided paresis that resolved; magnetic resonance imaging showed a small hemispheric stroke, and postoperatively the patient reported having another 15-second episode of blurred vision and field loss without any associated paresis or neurologic findings.
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Comment |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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While it was initially hoped that RBP would be more effective in protecting the brain during periods of CA, as reported by other authors and also in our initial experience with 50 patients, subsequent studies have shown that the brain is incompletely perfused by the RBP method [5, 8, 11–16, 19]. These vagaries in brain microcapillary perfusion notwithstanding, the question remains whether RBP could reduce the risk of stroke by virtue of retrograde great vessel flushing of particulate or gaseous emboli. A study would require a larger number of patients to settle that question. Based on the stroke rate of 2.8% (4 of 139) during this study period, we would have required 650 patients or more to have had enough power ( = 0.05; effect size, 0.20; 80% power; 95% confidence level) to evaluate any benefits in reducing strokes. Of note in this study, no randomized patients developed a stroke in any of the groups; therefore, this could not be evaluated. In one of the larger studies of retrograde brain perfusion by Coselli [15], the incidence of stroke did appear to be reduced by retrograde perfusion when compared with historical controls.
In the present study, antegrade brain perfusion also had no additive protective effect. In the initial studies of antegrade brain perfusion reported by Crawford and Saleh [3], there was a high incidence of stroke, presumably related to the catheter induced great vessel damage and resultant embolization. In the present study, to try to reduce the risk of stroke, we chose to use the right subclavian artery for antegrade perfusion with occlusion of the innominate artery as this allowed for retrograde flushing of any embolic material that might accumulate in the great vessels. With perfusion of only the right subclavian artery and occlusion of the origin of the innominate artery, the left common carotid artery is also flushed of any potential embolic material as one completes the aortic arch repair. In this study, we found that the use of antegrade perfusion for hemi-arch repairs prolonged the period of CA and, therefore, any potential benefits may be negated by a longer CA time for the hemi-arch repairs. For replacement of the entire arch, however, antegrade perfusion may still be of value, particularly if the CA times exceed 60 minutes or more. In our study, however, the average time for replacement of the entire aortic arch was 41 minutes. If CA times are expected to exceed 60 minutes, except for unforeseen problems, then we believe a different operative technique for repairing the entire aortic arch should be considered. While there has been increasing popularity for ANTE, particularly in Japan, the results have been variable and the recent study by Ueda and colleagues [20] would suggest that this does not significantly reduce the risk of stroke or neurocognitive deficits. While profound hypothermia and CA were used in this study together with ANTE, it is doubtful that patients would have done better if moderate hypothermia had been used, as espoused by some authors, since the risk of ischemic injury could have been greater at a higher temperature.
Based on the findings in the present study, we recommend the use of circulatory arrest alone for brief CA periods. However, if we anticipate extensive atheroma in the aortic arch or we need to perform an endarterectomy of the aortic arch, we add RBP for its retrograde flushing effect. Antegrade brain perfusion can be used for complex aortic arch repairs, and for left-sided thoracotomies with ascending or arch repairs combined with descending thoracic or thoracoabdominal aortic repairs.
We used a broad range of extensive neurocognitive testing in this study. Based on the correlations between tests and CA period, cardiopulmonary bypass time and discrimination between groups, we would recommend that the Wechsler memory and intelligence tests, Beck depression inventory, Shipley institute of living scale, trail making tests, California verbal learning tests, finger oscillation test, and controlled word association test (FAS), or similar tests be among core neurocognitive tests. The use of percentage decline or changes in standard deviation for diagnosis of binary dichotomous neurocognitive deficits is arbitrary, reduces statistical power, and has little correlation with clinical functional ability of patients. Rather, we recommend that future randomized studies comparing intervention utilize comparison of means or more sophisticated methods of analyzing change of scores. In addition, ideally there should be a nonoperated control group to compensate for the effect of learning on test scores. Based on this study and the findings of tests correlating with the period of CA in some tests only at 6 months postoperatively, studies should include a neurocognitive evaluation at 6 months postoperatively.
The S-100 protein has been used for trying to determine whether brain injury has occurred, including with the use of cardiopulmonary bypass [24]. While the marker may detect subtle degrees of brain injury, there is evidence that other factors may raise the levels of S-100 in the blood, such as not using line filters, use of a cardiotomy suction during the period of cardiopulmonary bypass, or postoperative autotransfusion [27]. In this study, the circulatory arrest time and cardiopulmonary bypass time correlated with peak S-100 levels. Whether the higher elevations of S-100 in the CA patients compared with the coronary artery bypass patients reflects neurologic injury or the effects of prolonged cardiopulmonary bypass time and greater usage of the pump sucker, or whether it is an artifact, is unclear. Since there were no strokes in this series, we did not see the delayed return of S-100 levels to base line that is seen with postoperative strokes. Thus, the levels had returned to base line within 1 day of the operation, in keeping with the patients being awake and following commands the morning after the operation.
Not evaluated in this study were our standard ancillary procedures of -stat pH control, administering mannitol, magnesium sulfate, thiopental or lidocaine, packing the patient’s head in ice, 40 micron leuko-filtration, and CO2 operative field flooding. Nevertheless, we believe these measures contribute to the incremental improved results in our overall series with a 97.8% survival and 2.8% incidence of stroke.
One of the weaknesses of this study is that patients are not matched on relevant covariates before randomization since it was not possible with this group of patients. Also, the number of patients in each group is not large. Nevertheless, because we are dealing with quantitative data and each CA group had 10 patients assigned to it, we felt this was adequate to evaluate any changes in neurocognitive function or S-100 levels postoperatively and to prevent a Type I error. Because of the exorbitant cost per patient of performing this study, we thought it best to start with a pilot study of this magnitude because no published data were available on scored neurocognitive testing and S-100 levels after CA. We did not do routine preoperative brain magnetic resonance imaging or computed tomographic scans which may have explained some of the preoperative neurocognitive deficits. Ueda and colleagues [20] did preoperative brain scans in a study of 113 patients who were to undergo arch repairs and found 65% of patients (24 of 65) who had a computed tomography had evidence of infarction and 49% of 42 patients by magnetic resonance imaging.
In conclusion, we would recommend that surgeons continue to use DHCA by the well established techniques, and RBP or ANTE be added on a selective basis according to the expected operative procedure, namely, RBP in patients when a lot of potential embolic material is expected and ANTE when prolonged CA times may occur. Although this study has failed to show added neurocognitive protective benefits with these techniques, in a larger series of patients and with a greater number of strokes there could potentially be some benefit in stroke reduction. We would also encourage further prospective randomized studies of brain protection methods to include DHCA and CA alone as the control group. While the best method of determining when a neurocognitive deficit has occurred continues to be debated, we believe that a blinded neuropsychologist’s clinical evaluation of the patient based on neurocognitive testing and diagnosis of new neurocognitive deficit is an accurate intrastudy method for determining an end point for analysis in prospective studies. Ideally the study should be replicated with a larger sample, so that a longitudinal, mixed-model analysis of variance can be performed. Whereas the value of S-100 levels in detecting subtle brain injury is questionable based on this study and recent reports [27], it would be optimal if S-100 levels were controlled in a multivariate framework.
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Acknowledgments |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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TopAbstractIntroductionMaterial and methodsResultsCommentAcknowledgmentsReferences |
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