This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (1) Citing Articles via Google Scholar Google Scholar Articles by Djaiani, G. Articles by Rakowski, H. Search for Related Content PubMed PubMed Citation Articles by Djaiani, G. Articles by Rakowski, H.

---

CARDIOVASCULAR ANESTHESIOLOGY

Epiaortic Scanning Modifies Planned Intraoperative Surgical Management But Not Cerebral Embolic Load During Coronary Artery Bypass Surgery

George Djaiani, MD, FRCA^*, Mohamed Ali, MD^*, Michael A. Borger, MD, PhD, Anna Woo, MD, SM, Jo Carroll, RN^*, Christopher Feindel, MD, Ludwik Fedorko, MD, PhD^*, Jacek Karski, MD^*, and Harry Rakowski, MD

From the *Department of Anesthesiology, and Divisions of Cardiovascular Surgery and Cardiology, Toronto General Hospital, University Health Network, University of Toronto, Toronto, Canada.

Address correspondence and reprint requests to George Djaiani, MD, FRCA, Department of Anesthesiology, Toronto General Hospital, Eaton North 3-410, 200 Elizabeth Street, Toronto, ON M5G 2C4, Canada. Address e-mail to george.djaiani{at}uhn.on.ca.

Abstract

BACKGROUND: Patients with aortic atheroma are at increased risk for neurological injury after coronary artery bypass graft (CABG) surgery. We sought to determine the role of epiaortic ultrasound scanning for reducing cerebral embolic load, and whether its use leads to changes of planned intraoperative surgical management in patients undergoing CABG surgery.

METHODS: Patients >70-yr-of-age scheduled for CABG surgery were prospectively randomized to either an epiaortic scanning (EAS) group (aortic manipulation guided by epiaortic ultrasound) or a control group (manual aortic palpation without EAS). All patients received a comprehensive transesophageal echocardiographic examination. Transcranial Doppler (TCD) was used to monitor the middle cerebral arteries for emboli continuously from 2 min before aortic cannulation to 2 min after aortic decannulation. Neurological assessment was performed with the National Institute of Health stroke scale before surgery and at hospital discharge. The NEECHAM confusion scale was used for assessment and monitoring of patient global cognitive function on each day after surgery until hospital discharge.

RESULTS: Intraoperative surgical management was changed in 16 of 55 (29%) patients in the EAS group and in 7 of 58 (12%) patients in the control group (P = 0.025). These changes included adjustments of the ascending aorta cannulation site for cardiopulmonary bypass (CPB), the avoidance of aortic cross-clamping by using ventricular fibrillatory arrest during surgery, or by conversion to off-pump surgery. During surgery, 7 of 58 (12%) patients in the control group crossed over to the EAS group based on the results of manual aortic palpation. The median [range] TCD detected cerebral embolic count did not differ between the EAS and control groups during aortic manipulations (EAS, 11.5 [1–516] vs control, 22.0 [1–160], P = 0.91) or during CPB (EAS, 42.0 [4–516] vs control, 63.0 [5–758], P = 0.46). The NEECHAM confusion scores and National Institute of Health stroke scale scores were similar between the two groups.

CONCLUSIONS: These results show that the use of EAS led to modifications in intraoperative surgical management in almost one-third of patients undergoing CABG surgery. The use of EAS did not lead to a reduced number of TCD-detected cerebral emboli before or during CPB.

A considerable number of patients undergoing cardiac surgery develop neurological complications postoperatively ranging from subtle cognitive changes to clinically evident confusion, delirium, and stroke.1–3 Atherosclerosis of the ascending aorta and the aortic arch are important risk factors for perioperative stroke.4,5 We reported that even patients with mild-to-moderate atheroma of the ascending aorta undergoing coronary artery bypass graft (CABG) surgery with cardiopulmonary bypass (CPB) developed ischemic brain injury that was associated with an increased cerebral embolic load during CPB.6

Epiaortic ultrasound scanning (EAS) is superior to manual palpation of the ascending aorta and to transesophageal echocardiography (TEE) for the detection of atherosclerosis of the ascending aorta, particularly of noncalcified plaques.7–10 EAS may reduce the frequency of neurological injury after surgery due to cerebral embolism by allowing for the identification and, thus, avoidance of atheroma at the sites of ascending aortic manipulations (e.g., cannulation for CPB, aortic cross-clamping, and proximal CABG anastomosis).11–13

The primary objective of this study was to determine whether the use of EAS leads to a reduction in cerebral embolic load as detected with transcranial Doppler (TCD) monitoring of the middle cerebral arteries in patients undergoing CABG surgery. The secondary objective was to examine whether EAS use leads to changes in the planned surgical management compared with manual palpation and TEE.

METHODS

Study Population
After IRB approval, informed consent was obtained from 126 patients older than 70-yr-of-age, who were scheduled for elective CABG surgery with CPB. Patients were excluded for the following: surgical procedure in addition to CABG surgery, reoperative surgery, emergent surgery, presence of >50% carotid stenosis, preexisting atrial fibrillation, when TEE was contraindicated, or when TEE revealed an intracardiac source of potential emboli (see below).

Anesthetic Management
All patients received premedication with lorazepam 2 mg 1–2 h before surgery. Anesthetic technique was standardized and included fentanyl 10–20 µg/kg, midazolam 0.1 mg/kg, pancuronium 0.15–0.20 mg/kg, and isoflurane 0.5%–1.5%. All patients received tranexamic acid 50 mg/kg IV after induction of anesthesia. After surgery, patients were transferred to intensive care unit where they were sedated with propofol 0.5–4 mg · kg^–1 · h^–1 and intermittent IV morphine. The patients’ tracheas were extubated when the following criteria were met: patient responsive and cooperative, SaO₂ 94% with Fio₂ 60%, complete reversal of neuromuscular blockade, Paco₂ 35–55 mm Hg, stable hemodynamics, absence of uncontrolled arrhythmia, and nasopharyngeal temperature >36°C.

Operative Technique and Management of CPB
After median sternotomy, saphenous vein harvesting, and mobilization of the internal mammary artery, the patients were given heparin to achieve an activated clotting time >400 s. Cannulation was performed with a 24 F arterial cannula (model 6672, Sarns/3M Health Care, Ann Arbor, MI) in an atheromatous-free segment in the ascending aorta. If distal aortic arch cannulation was chosen, a 24 F flexible aortic arch cannula (model 4335, Sarns) was used. In the latter instance, the aortotomy was located on the inferolateral aspect of the aortic arch, just proximal to the origin of the left subclavian artery. Management of CPB included systemic temperature "drift" to 33°C–34°C, -stat pH management, mean perfusion pressure between 60 and 80 mm Hg, pump flow rates of 2.0–2.4 L · min^–1 · m^–2, and hematocrit >20%. Myocardial protection was achieved with intermittent antegrade and occasionally retrograde cold blood cardioplegia. Cardiotomy suction was used in a standard closed venous reservoir where cardiotomy blood was collected and reinfused through the arterial circuit back to the patient. A 32-µm filter (Avecor Affinity, Minneapolis, MN) was used in the arterial perfusion line. Before separation from CPB, patients were rewarmed to 36°C–37°C. During rewarming, the maximal inflow temperature was limited to 37°C. After separation from CPB, heparin was neutralized with protamine 1 mg for every 100 U of heparin.

Echocardiographic Assessment and Randomization
After induction of general anesthesia and endotracheal intubation, a comprehensive TEE examination was performed obtaining all standard views using a multiplane 4–7 MHz probe connected to a Sonos 5500 ^TM echocardiography machine (Philips Medical Systems, Andover, MA). This examination included careful exclusion of an intracardiac source of potential emboli such as atrial septal defect, left atrial/ventricular thrombus, and significant mitral or aortic valve calcification. The proximal thoracic aorta was further evaluated with TEE for presence of atheromatous disease of the ascending aorta and aortic arch.

A computer-generated randomization code in blocks of four was used to assign patients to either the EAS or control groups. In the control group, the aortic arch and the ascending aorta were evaluated with manual palpation by the surgeon at the sites for aortic cannulation, proximal bypass graft anastamosis, and aortic cross-clamp application. In the EAS group, epiaortic ultrasound was used to evaluate the aortic arch and the ascending aorta for atherosclerosis at the sites of aortic manipulation. For this examination, the pericardial cradle was first filled with warm normal saline. A 6–15 MHz linear ultrasound probe (Philips Medical Systems) covered with ultrasound gel and wrapped in sterile transducer cover (CIVCO Medical Instruments, Kalona, IA) was used by the surgeon to scan the ascending aorta from the aortic valve to midaortic arch in transverse and longitudinal planes. Both, TEE and EAS images were recorded and saved digitally.

The ascending aorta was imaged by TEE from the midesophageal view of the aortic valve in the longitudinal plane. The ascending aorta was divided into proximal (visualized by TEE) and distal (not seen by TEE due to the blind spot) segments. The proximal segment was assessed by TEE and manual palpation in the control group and by TEE and epiaortic scanning in the EAS group. The distal part was assessed by manual palpation in the control group and by EAS in the EAS group. The aortic arch was imaged by rotating the TEE probe posteriorly to initially image the descending aorta and then slowly withdrawing the probe until the left subclavian artery was identified. Based on anatomical landmarks, the aortic arch was defined as the aortic segment between the innominate artery and left subclavian artery. The aortic arch was examined in both transverse and longitudinal planes. The ascending aorta and aortic arch were graded in real time for the severity of atherosclerosis on a four-point scale as previously described: normal (grade 0), mild (grade 1), moderate (grade 2), or severe atheroma (grade 3).6 Briefly, a normal aorta was defined as maximum intimal thickness 2 mm with no irregularities; mild atherosclerosis defined as aortic thickness >2 but 4 mm without irregularities; moderate atherosclerosis when there was >4 mm intimal thickening without irregularities; and severe atherosclerosis was defined as intimal thickness >4 mm with diffuse calcification, mobile plaques, and/or ulcerated lesions. All assessments were done by an experienced echocardiographer who was blinded to the primary outcome. The grading of the aorta was based on strict numerical criteria to reduce the interobserver variability and was performed in real time during surgery. The echocardiographic findings were communicated to the operating surgeon who was free to modify the operating technique and apply ultrasound guidance for any intended aortic manipulation to minimize potential embolization.

TCD Measurements
TCD (MultiDop X4; DWL Electronic Systems, Sipplingen, Germany) monitoring of the right and left middle cerebral arteries was performed continuously from 2 min before aortic cannulation until 2 min after aortic decannulation. The Doppler sound was turned off and visual displays were not available to anesthesiologists, surgeons, or perfusionists involved in patient care. A 2 MHz pulsed-wave transducer (diameter, 1.7 cm) was used to simultaneously monitor two depths spaced 4.97 mm apart at a mean (± the standard error) insonation depth of 48.7 ± 1.7 mm and 53.7 ± 1.7 mm, respectively. A high-pass filter set at 100 Hz and a low-pass filter at 80 kHz were used.

In addition to the total number of TCD-detected emboli during CPB, the number of emboli 1 min before and 2 min after each of the following surgical interventions was quantitated: aortic cannulation and decannulation, cross-clamp application and removal, CPB start and end, and the start of cardiac ejection. Since the injection of medications and blood sampling by the perfusionists are also associated with embolic events, the number of perfusionists’ interventions was also recorded.14

Failure to acquire adequate acoustic windows bilaterally resulted in unilateral recordings in some patients. Consequently, when only single-sided embolic counts were obtained, these data were multiplied by the factor of 2 to approximate bilateral recording analysis.

We have previously described our technique of detection and analysis of cerebral embolic signals.14 In brief, automated software (TCD-8 for MultiDop X4, version 8.00q) was used to discriminate between emboli and artifact according to the bigate method. High-intensity signals were considered artifact if they occurred in both depths simultaneously. They were considered emboli if they appeared sequentially in a manner that was consistent with flow velocity and distance between the two sample volumes. Automated embolic counts were verified by a manual off-line review of the records of each event by an observer blinded to patient group assignment.

Neurological Assessment
The patients underwent neurological assessment with the National Institute of Health (NIH) stroke scale (NIHSS)15 at baseline and before hospital discharge. The NIHSS is a 42-point validated neurologic examination that quantifies neurologic deficits in 11 categories with an increasing score indicating worse neurological function. The NIHSS was performed at all sessions by the same trained research personnel.

The patients’ global cognitive function was evaluated with the NEECHAM confusion scale16 on each day after surgery until hospital discharge. The NEECHAM confusion scale contains 9 items organized in 3 domains with a total possible score ranging from 0 to 30. Subscale 1 (0–14 points) grades the primary components of cognitive function: attention/alertness (0–4 points), verbal and motor command of information (0–5 points), and memory and orientation (0–5 points). Subscale 2 (0–10 points) measures behavioral manifestations associated with more physical performance functions: appearance/posture control (0–2 points), sensorimotor performance (0–4 points), and verbal manifestations accompanying or heralding delirium-like syndromes (0–4 points). Subscale 3 (0–6 points) assesses physiological and autonomic stability, vital signs (0–2 points), oxygen saturation measurement (0–2 points), and urinary continence (0–2 points). Total score indicates the different degrees of confusion and are weighted as follows: 0–19, moderate to severe confusion; 20–24, mild or early development of confusion; 25–26, "not confused" but at high risk; 27–30, normal function.

Sample Size Justification and Statistical Analysis
On the basis of our previous investigations,14,17 we estimated that the mean TCD cerebral embolic count during CPB would be 2.4 ± 1.9 (sd) emboli per minute. Based on an = 0.05 and study power 1-β = 0.8, 80 patients (40 in each group) were required to detect 50% reduction in cerebral embolic rate in the EAS group compared with the control group. We estimated an inability to obtain adequate TCD signal in 10% of patients, and the attrition rate of 10%. The final sample size thus was estimated to be 104 patients (52 patients in each arm).

Demographic data and surgical characteristics were compared between groups with the ² test dichotomous variables, and the t-test for continuous variables. Embolic counts were analyzed with Mann–Whitney U-test. One-way ANOVA was used to compare the NEECHAM scores. A P value <0.05 was considered significant. Statistical analysis was conducted with the MINITAB computer software (MINITAB Inc., State College, PA).

All analyses were performed on an intention-to-treat basis.

RESULTS

Demographic Data and Surgical Characteristics
Thirteen patients were found to have a potential intracardiac source of emboli based on the initial TEE examination: 10 patients had a patent foramen ovale and three patients had moderate aortic stenosis. These patients were excluded from the analysis. A total of 113 patients were randomized to either EAS (n = 55) or control group (n = 58) groups. There were no differences in baseline demographic data or surgical characteristics between the two groups (Table 1).

Aortic Atheroma Characteristics
The grading and distribution of atheroma in the proximal and distal (TEE "blind" spot) ascending aorta and the aortic arch are presented in Table 2 and Figure 1. In two of the seven patients who crossed-over from the control group, EAS demonstrated grade 2 atheroma in the distal portion of the ascending aorta (not identified with manual palpation or TEE). Both of these patients had mobile atheroma in the aortic arch, which was already identified by TEE before EAS. Another patient that crossed-over to EAS had grade 1 atheroma in the proximal ascending aorta and the aortic arch. More detailed EAS examination revealed grade 1 atheroma in the distal part of the ascending aorta. The remaining four patients who crossed-over to EAS were confirmed to have grade 1 atheroma in the proximal ascending aorta and grade 2 atheroma in the aortic arch.

View larger version (9K): [in this window] [in a new window]   Figure 1. Distribution of severity of atheromatous disease in the ascending aorta and aortic arch. Data are expressed as the percentage of patients. Grade 0, normal aorta (maximum intimal thickness 2mm); grade 1, mild atheroma (maximum intimal thickness >2–4 mm); grade 2, moderate atheroma (maximum intimal thickness >4 mm); and grade 3, severe atheroma (diffuse calcification of the ascending aorta, or mobile plaques determined during intraoperative).

TCD Findings
Adequate TCD signals were acquired in 43(78%) patients from the EAS group and in 42 (72%) patients from the control group (P = 0.48). Unilateral only recordings were available in four patients in the EAS group (two right sided and two left sided) and in five patients in the control group (three right side and two left side). There was no significant difference between groups in the TCD embolic counts obtained from the left and right-sided recordings. There was no significant difference in the total number of cerebral embolic events during CPB or during each surgical intervention between the two groups (Table 3). The number of perfusionists’ interventions during CPB was not different between groups (EAS, 7.0 ± 4.4 vs control, 7.7 ± 3.8, P = 0.25).

Surgical Modifications
Modification in surgical management occurred more often in the EAS group compared with the control group (EAS, 16% or 29% of patients vs controls, 7% or 12% of patients, P = 0.025) as listed in Table 4. Changes in the surgical plan occurred in three of the seven control group patients who crossed-over to the EAS group. These modifications included conversion to off-pump coronary artery bypass (OPCAB) surgery, ventricular fibrillatory arrest with no cross-clamp application, and distal aortic arch cannulation in an area free of atheroma.

Neurological Assessment
Compared with the baseline values, the NEECHAM scores were considerably lower during the first three postoperative days in both groups of patients; however, there was no difference between the groups (Fig. 2). There was no significant difference in the NIHSS between the two groups (Table 5). Postoperative morbidity and mortality were comparable between the two groups (Table 6).

View larger version (10K): [in this window] [in a new window]   Figure 2. Perioperative trends in the NEECHAM scores in the EAS and control groups.

DISCUSSION

In this prospectively randomized, controlled trial in patients undergoing CABG surgery, we failed to demonstrate a difference in the number of TCD-detected cerebral embolic counts (primary end-point) in patients undergoing EAS compared with the control group. Assessing for atherosclerosis of the ascending aorta with EAS led to modification in surgical management in 29% of patients compared with just 12% of the control group. However, these modifications did not translate into significant differences between the two groups in either neurological or global cognitive function.

Our results are similar to the findings of Murkin18 who evaluated EAS versus standard care in a randomized trial of 191 patients undergoing CABG surgery. In that study, EAS resulted in modifications in the site of aortic cannulation, the type of aortic cannula used, the site of aortic cross-clamp application, or the site of partial aortic clamping in 23.5% of patients. In contrast to our results, Murkin18 found that the use of EAS resulted in a significant reduction in the number of TCD-detected cerebral emboli during aortic interventions. In our study, TEE was used in addition to direct palpation to assess for atherosclerosis of the ascending aorta in the control group. In the study by Murkin,18 only direct manual palpation of the aorta was used in the control group. Furthermore, we allowed for crossover of patients from the control group to the EAS group based on clinical assessments. These maneuvers might have resulted in a lower intervention-related embolic count in the control group. When patients crossing-over to the EAS group were excluded from the analysis, the median cerebral embolic count decreased in the control group and increased when crossovers were added to the EAS group (Table 3); however, this change in the TCD count did not reach statistical significance. A post hoc analysis identified that, based on the current embolic count, the required sample size would have to be increased to 660 patients to show the superiority of EAS.

The current study identified that all grade atheroma was detected in 12.7% of patients in the EAS group and 5.2% patients in the control group; however, this difference did not reach statistical significance, P = 0.16. These findings were attributed to the scan findings in the distal ascending aorta, the segment that is difficult to image with TEE. The identification of atheromatous disease in the distal ascending aorta with EAS influenced surgical decision regarding approach to aortic cannulation. Although TEE has poor positive-predictive value for detection of ascending aorta atheromas compared with EAS, its high negative-predictive value (100%) supports its usefulness in screening for aortic atherosclerosis.9 In fact, TEE played an important role in identifying atheroma in the aortic arch that were present in more than one-third of patients in both groups. A new diagnostic device (the A-View ® balloon catheter) for visualizing the distal part of the ascending aorta (the TEE blind spot) might further enhance the effectiveness of TEE for detecting atherosclerosis of the ascending aorta.19

Atherosclerosis of the ascending aorta is a recognized risk factor for perioperative stroke due to cerebral embolization.8,20 An autopsy report involving 262 patients who had undergone cardiac surgery revealed that macro- and microhemorrhages, brain infarction, subarachnoid hemorrhages, and hypoxemic brain damage were present in 49% of patients. The brain infarcts resulted from atheroemboli, fat or foreign body emboli, or from emboli originating from localized cerebral artery atherosclerosis.21

The rate of cerebral embolization during cardiac surgery appears to be related to degree of the atheromatous burden of the ascending aorta and aortic arch.6,22 However, the link between cerebral embolization and neurocognitive dysfunction is controversial. More than a decade ago, Pugsley et al. reported that 43% of patients undergoing CABG surgery had >1000 cerebral microemboli detected with TCD and that the development of neurocognitive dysfunction 8 weeks after surgery was related to embolic count.23 Hammon et al. showed that cognitive impairment was more common in patients with more than 100 emboli whereas a reduction in the number of emboli by modifications of surgical technique decreased the incidence of this impairment.24 On the contrary, Bar-Yosef et al.25 showed that severity of atheromatous disease of the ascending aorta and aortic arch was not predictive of neurocognitive dysfunction after CABG surgery. Furthermore, Neville et al.26 showed a similar degree of cognitive decline in patients undergoing valve versus coronary surgery even though cerebral embolic count was four-fold higher in the valve group. These findings are supported by the studies demonstrating similar rates of cognitive decline in patients undergoing either on-pump CABG or OPCAB surgery, despite a significant reduction in the number of TCD-detected embolic signals with OPCAB surgery.27–29 However, one of the major shortcomings of these studies includes lack of routine use of EAS in identifying location and severity of the atheromatous disease in the ascending aorta and aortic arch. Our recent report emphasized that the quality, rather than quantity, of the cerebral embolic load may play a primary role in the pathogenesis of central nervous system injury associated with cardiac surgery.30

Abu-Omar et al.31 reported that 72%–88% of the total cerebral embolic load detected with TCD in both open or closed chamber cardiac surgeries are gaseous in composition. Avoidance of aortic atheroma by using EAS to guide surgical interventions would likely primarily reduce TCD embolic signals due to solid emboli containing atheromatous debris. Further, positioning of the aortic cannula away from an atherosclerotic portion of the aorta might reduce solid emboli that result from the effects of CPB inflow or the "sand blasting" effect.32 As a result, the lack of discrimination in the type of emboli detected by TCD in our study might account for our failure to detect a difference in TCD embolic counts between the two groups.

Constant improvement in the surgical and CPB management techniques as well as an increased awareness of cerebral embolization with implementation of TCD monitoring have resulted in a reduction of the number of embolic events in most of the patients undergoing cardiac surgery.33 Cerebral embolic count could be considerably reduced by thorough surgical and perfusionist management, including placement of an airtight purse-string suture around the venous cannula, distal aortic arch cannulation, and prevention of air entrapment into the CPB circuit by meticulous perfusionist interventions.34 Consequently, the total cerebral embolic count in the current study was considerably lower than previously reported.14,17

The introduction of EAS into clinical practice was associated with a reduction in the prevalence of stroke from 1.2% to 0.7% in retrospective review of 8547 patients undergoing CABG surgery.12 Hammon et al.13 further showed that a surgical strategy designed to minimize aortic manipulation guided by EAS significantly reduced the incidence of cognitive deficits in CABG patients compared with traditional techniques. Others have reported that alterations of surgical techniques based on assessments for atherosclerosis of the ascending aorta reduces the prevalence of TCD-detected cerebral emboli and clinically reported stroke.35–37 Zingone et al.11 reported that EAS was associated with a several-fold reduction in early postoperative stroke in high-risk patients with atherosclerosis of the ascending aorta. These data together support the notion that EAS-guided surgery to avoid atherosclerosis of the ascending aorta and aortic arch reduces the frequency of brain injury, regardless of its impact on TCD-detected cerebral emboli counts.

Several limitations with the current study are acknowledged. Since EAS was performed by the operating surgeon, "blinding" was not possible because of ethical considerations of potentially allowing aortic manipulations at a site of known atherosclerosis. Although the surgeons were not "blinded" to the EAS findings, they were blinded to the TCD findings. A second limitation was our allowance of crossover to EAS based on surgical assessments. In our practice, we feel that it would be unethical to not allow this crossover design. In fact, all seven patients who crossed over to EAS had their planned surgical management altered after the EAS assessment.

In conclusion, the use of EAS to guide surgical manipulations of the aorta did not reduce the number of TCD-detected cerebral embolic count compared with the control group. Information provided by EAS, however, did result in modifications in the surgical management in almost one-third of patients. These results support that EAS should be considered particularly for elderly and high-risk patients undergoing CABG surgery.

Footnotes

Accepted for publication February 4, 2008.

Supported by grants from the American Society of Echocardiography and the Canadian Anesthesiologists’ Society.

REFERENCES

1. Selnes OA, Goldsborough MA, Borowicz LM, McKhann GM. Neurobehavioural sequelae of cardiopulmonary bypass. Lancet 1999;353:1601–16[Web of Science][Medline]
2. Newman MF, Kirchner JL, Phillips-Bute B, Gaver V, Grocott H, Jones RH, Mark DB, Reves JG, Blumenthal JA. Longitudinal assessment of neurocognitive function after coronary-artery bypass surgery. N Engl J Med 2001;344:395–402[Abstract/Free Full Text]
3. Borger MA, Ivanov J, Weisel RD, Rao V, Peniston CM. Stroke during coronary bypass surgery: principal role of cerebral macroemboli. Eur J Cardiothorac Surg 2001;19:627–32[Abstract/Free Full Text]
4. Davila-Roman VG, Barzilai B, Wareing TH, Murphy SF, Schechtman KB, Kouchoukos NT. Atherosclerosis of the ascending aorta: Prevalence and role as an independent predictor of cerebrovascular events in cardiac patients. Stroke 1994;25:2010–6[Abstract]
5. van der Linden J, Hadjinikolaou L, Bergman P, Lindblom D. Postoperative stroke in cardiac surgery is related to the location and extent of atherosclerotic disease in the ascending aorta. J Am Coll Cardiol 2001;38:131–5[Abstract/Free Full Text]
6. Djaiani G, Fedorko L, Borger M, Mikulis D, Carroll J, Cheng D, Karkouti K, Beattie S, Karski J. Mild to moderate atheromatous disease of the thoracic aorta and new ischemic brain lesions after conventional coronary artery bypass graft surgery. Stroke 2004;35:e356–8[Abstract/Free Full Text]
7. Wareing TH, Davila-Roman VG, Barzilai B, Murphy SF, Kouchoukos NT. Management of the severely atherosclerotic ascending aorta during cardiac operations. A strategy for detection and treatment. J Thorac Cardiovasc Surg 1992;103:453–62[Abstract]
8. Wareing TH, Davila-Roman VG, Daily BB, Murphy SF, Schechtman KB, Barzilai B, Kouchoukos NT. Strategy for the reduction of stroke incidence in cardiac surgical patients. Ann Thorac Surg 1993;55:1400–7[Abstract]
9. Konstadt SN, Reich DL, Kahn RS, Viggiani RF. Transesophageal echocardiography can be used to screen for ascending aortic atherosclerosis. Anesth Analg 1995;81:225–8[Abstract]
10. Das S, Dunning J. Can epiaortic ultrasound reduce the incidence of intraoperative stroke during cardiac surgery? Interact Cardiovasc Thorac Surg 2004;3:71–5[Abstract/Free Full Text]
11. Zingone B, Rauber E, Gatti G, Pappalardo A, Benussi B, Dreas L, Lattuada L. The impact of epiaortic ultrasonographic scanning on the risk of perioperative stroke. Eur J Cardiothorac Surg 2006;29:720–8[Abstract/Free Full Text]
12. Ozatik MA, Gol MK, Fansa I, Uncu H, Kucuker SA, Kucukaksu S, Bayazit M, Sener E, Tasdemir O. Risk factors for stroke following coronary artery bypass operations. J Card Surg 2005;20:52–7[Web of Science][Medline]
13. Hammon JW, Stump DA, Butterworth JF, Moody DM, Rorie K, Deal DD, Kincaid EH, Oaks TE, Kon ND. Single crossclamp improves 6-month cognitive outcome in high-risk coronary bypass patients: the effect of reduced aortic manipulation. J Thorac Cardiovasc Surg 2006;131:114–21[Abstract/Free Full Text]
14. Taylor RL, Borger MA, Weisel RD, Fedorko L, Feindel CM. Cerebral microemboli during cardiopulmonary bypass: increased emboli during perfusionist interventions. Ann Thorac Surg 1999;68:89–93[Abstract/Free Full Text]
15. Muir KW, Grosset DG, Lees KR. Interconversion of stroke scales. Implications for therapeutic trials. Stroke 1994;25:1366–70[Abstract]
16. Neelon VJ, Champagne MT, Carlson JR, Funk SG. The NEECHAM confusion scale: construction, validation and clinical testing. Nurs Res 1996;45:324–30[Web of Science][Medline]
17. Borger MA, Taylor RL, Weisel RD, Kulkarni G, Benaroia M, Rao V, Cohen G, Fedorko L, Feindel CM. Decreased cerebral emboli during distal aortic arch cannulation: a randomized clinical trial. J Thorac Cardiovasc Surg 1999;118:740–5[Abstract/Free Full Text]
18. Murkin JM. Pathophysiological basis of CNS injury in cardiac surgical patients: detection and prevention. Perfusion 2006;21:203–8[Abstract/Free Full Text]
19. van Zaane B, Nierich AP, Buhre WF, Brandon Bravo Bruinsma GJ, Moons KG. Resolving the blind spot of transoesophageal echocardiography: a new diagnostic device for visualizing the ascending aorta in cardiac surgery. Br J Anaesth 2007;98:434–41[Abstract/Free Full Text]
20. Blauth CI, Cosgrove DM, Webb BW, Ratliff NB, Boylan M, Piedmonte MR, Lytle BW, Loop FD. Atheroembolism from the ascending aorta. An emerging problem in cardiac surgery. J Thorac Cardiovasc Surg 1992;103:1104–11[Abstract]
21. Emmrich P, Hahn J, Ogunlade V, Geiger K, Schober R, Mohr FW. Neuropathological findings after cardiac surgery-retrospective study over 6 years. Z Kardiol 2003;92:925–37[Web of Science][Medline]
22. Mackensen GB, Ti LK, Phillips-Bute BG, Mathew JP, Newman MF, Grocott HP. Cerebral embolization during cardiac surgery: impact of aortic atheroma burden. Br J Anaesth 2003;91:656–61[Abstract/Free Full Text]
23. Pugsley W, Klinger L, Paschalis C, Treasure T, Harrison M, Newman S. The impact of microemboli during cardiopulmonary bypass on neuropsychological functioning. Stroke 1994;25:1393–9[Abstract]
24. Hammon JW Jr, Stump DA, Kon ND, Cordell AR, Hudspeth AS, Oaks TE, Brooker RF, Rogers AT, Hilbawi R, Coker LH, Troost BT. Risk factors and solutions for the development of neurobehavioral changes after coronary artery bypass grafting. Ann Thorac Surg 1997;63:1613–8[Abstract/Free Full Text]
25. Bar-Yosef S, Anders M, Mackensen GB, Ti LK, Mathew JP, Phillips-Bute B, Messier RH, Grocott HP. Aortic atheroma burden and cognitive dysfunction after coronary artery bypass graft surgery. Ann Thorac Surg 2004;78:1556–62[Abstract/Free Full Text]
26. Neville MJ, Butterworth J, James RL, Hammon JW, Stump DA. Similar neurobehavioral outcome after valve or coronary artery operations despite differing carotid embolic counts. J Thorac Cardiovasc Surg 2001;121:125–36[Web of Science][Medline]
27. Van Dijk D, Jansen EW, Hijman R, Nierich AP, Diephuis JC, Moons KG, Lahpor JR, Borst C, Keizer AM, Nathoe HM, Grobbee DE, De Jaegere PP, Kalkman CJ. Cognitive outcome after off-pump and on-pump coronary artery bypass graft surgery: a randomized trial. JAMA 2002;287:1405–12[Abstract/Free Full Text]
28. Lund C, Hol PK, Lundblad R, Fosse E, Sundet K, Tennoe B, Brucher R, Russell D. Comparison of cerebral embolization during off-pump and on-pump coronary artery bypass surgery. Ann Thorac Surg 2003;76:765–70[Abstract/Free Full Text]
29. Motallebzadeh R, Bland JM, Markus HS, Kaski JC, Jahangiri M. Neurocognitive function and cerebral emboli: Randomized study of on-pump versus off-pump coronary artery bypass surgery. Ann Thorac Surg 2007;83:475–82[Abstract/Free Full Text]
30. Djaiani G, Fedorko L, Borger MA, Green R, Carroll J, Marcon M, Karski J. Continuous-flow cell saver reduces cognitive decline in elderly patients after coronary bypass surgery. Circulation 2007;116:1888–95[Abstract/Free Full Text]
31. Abu-Omar Y, Balacumaraswami L, Pigott DW, Matthews PM, Taggart DP. Solid and gaseous cerebral microembolization during off-pump, on-pump, and open cardiac surgery procedures. J Thorac Cardiovasc Surg 2004;127:1759–65[Abstract/Free Full Text]
32. Swaminathan M, Grocott HP, Mackensen GB, Podgoreanu M, Glower D, Mathew JP. The "Sandblasting" effect of aortic cannula on arch atheroma during cardiopulmonary bypass. Anesth Analg 2007;104:1350–1[Free Full Text]
33. Borger MA, Djaiani G, Fedorko L, Carroll J, Carson SM. Reduction of cerebral emboli during cardiac surgery: influence of surgeon and perfusionist feedback. Heart Surg Forum 2003;6:204–5
34. Prasongsukarn K, Borger M. Reducing cerebral emboli during cardiopulmonary bypass. Semin Cardiothorac Vasc Anesth 2005;9:153–8[Abstract/Free Full Text]
35. Ribakove GH, Katz ES, Galloway AC, Grossi EA, Esposito RA, Baumann FG, Kronzon I, Spencer FC. Surgical implications of transesophageal echocardiography to grade the atheromatous aortic arch. Ann Thorac Surg 1992;53:758–63[Abstract]
36. Mills NL, Everson CT. Atherosclerosis of the ascending aorta and coronary artery bypass. J Thorac Cardiovasc Surg 1991;102:546–53[Abstract]
37. Trehan N, Mishra M, Sharma OP, Mishra A, Kasliwal RR. Further reduction in stroke after off-pump coronary artery bypass grafting: a 10-year experience. Ann Thorac Surg 2001;72:S1026–32[Abstract/Free Full Text]

This article has been cited by other articles:

				W. S. Whitley and K. E. Glas An Argument for Routine Ultrasound Screening of the Thoracic Aorta in the Cardiac Surgery Population Seminars in Cardiothoracic and Vascular Anesthesia, December 1, 2008; 12(4): 290 - 297. [Abstract] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (1) Citing Articles via Google Scholar Google Scholar Articles by Djaiani, G. Articles by Rakowski, H. Search for Related Content PubMed PubMed Citation Articles by Djaiani, G. Articles by Rakowski, H.