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Ann Thorac Surg 1999;67:478-483
© 1999 The Society of Thoracic Surgeons


Original Articles

Extracorporeal circulation before and after ultrasonographic evaluation of the ascending aorta

Masashi Ura, MDa, Ryuzo Sakata, MDa, Yoshihiro Nakayama, MDa, Tadaomi-Alfonso Miyamoto, MDa,b, Tomoko Goto, MDb

a Cardiovascular Surgery, Kumamoto Central Hospital, Kumamoto, Japan
b Anesthesiology, Kumamoto Central Hospital, Kumamoto, Japan

Accepted for publication July 24, 1998.

Address reprint requests to Dr Sakata, 96 Tainoshima, Tamukaemachi, Kumamotoshi, Japan, 862-0965


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Comment
 References
 
Background. To further gain insight into atheroembolization mechanisms epiaortic two-dimensional echocardiographic evaluation before extracorporeal circulation and after decannulation may be helpful.

Methods. Epiaortic two-dimensional echocardiography was performed before cannulation and after decannulation in 188 (124 men) patients (mean age, 67.7 years; range, 43 to 86 years) undergoing operation with extracorporeal circulation for ischemic heart disease during 1996.

Results. After decannulation, a new intimal lesion was recognized in 10 of 188 patients (5.3%): mobile type in 5 patients (3 ending with a stroke [60%], 2 having brain computed tomographic scans compatible with embolism), intimal tear in 2, and intimal irregularity in 3 patients. Stroke occurred in a significantly smaller number of patients (2 of 178 [1.1%]; p < 0.001) without new lesions.

Conclusions. Clamp- or cannula-induced new lesions, especially of mobile type, are often complicated by postoperative stroke. Aggressive surgical technique modifications may need to be considered to avoid creating new lesions, particularly of the mobile type.


    Introduction
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 Abstract
 Introduction
 Methods
 Results
 Comment
 References
 
Because the morbidity and mortality of stroke complicating cardiac operations are high, need to prevent this complication is mandatory. The reported incidence of perioperative stroke varies from institution to institution between 1.0% to 4.5% [18]. Possible causes include embolism of air or particulate matter from the heart-lung machine, associated ascending aorta, carotid artery, aortic arch disease, or the heart, but by far the most important cause is emboli from atherosclerotic ascending aorta, which has been identified as one of the major risk factors for stroke after heart operations [911].

Epiaortic ultrasonographic examination before cannulation has provided valuable information to implement changes of the surgical technique on the spot to minimize atheroembolization. Imaging after decannulation was thought to be helpful in adding understanding as to when or why the embolization occurs.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Comment
 References
 
Of 194 patients undergoing operation for ischemic heart disease at Kumamoto Central Hospital during 1996, 6 patients had revascularization without manipulating the ascending aorta, and 188 had some type of ascending aorta manipulation to establish extracorporeal circulation (ECC). To identify the changes induced by the manipulation the same sonographic probe was used for two-dimensional epiaortic ultrasonography of the ascending aorta before cannulation and after decannulation. There were 124 men and 64 women, with the mean age of 67.7 years (range, 43 to 86 years). The operative procedures are summarized in Table 1 ; 171 patients underwent isolated coronary artery bypass grafting, 16 coronary artery bypass grafting in conjunction with various other procedures, and 1 isolated ventricular aneurysmectomy. This study was approved by the institutional ethics committee and the internal review board; all patients gave informed consent and all procedures followed established institutional guidelines.


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Table 1. Operative procedures

 
Technique
After median sternotomy and pericardiotomy the ascending aorta was evaluated by palpation to determine clinical location and extent of the thickening or calcification. The pericardial cavity was filled with saline, transverse and longitudinal two-dimensional images of the ascending aorta and the proximal aortic arch were obtained with a 7.5-MHZ linear transducer (IOE-702V, Toshiba-Medical, Tokyo, Japan) equipped with a 4-cm sonolucent spacer wrapped in a sterile plastic sheath. We graded the severity of atherosclerosis taking into account the thickness of the lesion and its longitudinal extent; the atherosclerotic lesion per se was assessed as mild if the intima had no thickening or was minimal (<3 mm), moderate if the intimal thickening was >3 but <4 mm, and severe if the thickening was protruding >4 mm, often mobile or the calcification involved more than one-half of the quadrant on the transverse image. The severity of the atherosclerosis was graded as: grade 1 = only mild lesions; grade 2 = moderate or severe intimal lesions involving only one-third of the length of the ascending aorta; grade 3 = moderate or severe intimal lesions involving less than two-thirds of the length of the ascending aorta; grade 4 = severe intimal lesions involving two-thirds or more of the ascending aorta. All operations were performed under standard cardiopulmonary bypass and moderate hypothermia (28° to 32°C). Arterial cannulations were performed in the ascending aorta (THI angled type aortic 21F or 24F perfusion cannula; Argyle Co, St. Louis, MO), femoral or subclavian artery (William Harvey arterial perfusion cannulae, type 1858; Bard, Inc, Billerica, MA) depending on the severity of atherosclerosis. When the ascending aorta was cannulated, double purse-string sutures and a stab wound with no-clamp technique was used. Except for 1 patient, all anastomoses including the proximals were performed during a single period of aortic cross-clamping (Fogarty soft-jaw clamp, 86 mm; Baxter Co, Irvine, CA). Because palpation of the ascending aorta underestimates the severity of atherosclerosis, the decision to implement some modifications of the operative technique was made mostly based on the qualitative sonographic information and secondarily on the surgeon’s evaluation. Epiaortic ultrasonographic imaging was repeated after decannulation for comparison to data obtained before ECC using the cannulation site and pulmonary artery as reference points.

Postoperative neurologic events
Patients were examined preoperatively by the physician in charge. If a neurologic deficit was suspected, consultation with the neurologist was sought but no neuropsychologic studies were made before or after operation. Two independent neurologists assessed the development of perioperative stroke. Only permanent or reversible focal complications such as reversible ischemic neurologic deficit or transient ischemic attacks, were considered neurologic events. Confusion, agitation, dementia, disorientation, or psychosis were considered neurologic events only if new focal neurologic signs were also present. When clinical conditions permitted computed tomographic scans of brain were performed in patients with postoperative neurologic events, and in some, brain magnetic resonance plain or angiographic imaging, carotid duplex scanning, or scintigraphy were performed in an effort to seek the cause (embolic or hypoperfusion) of the stroke.

Statistical analysis
The association of aortic atheromatous disease with history-related variables was assessed with multivariate regression analysis. Statistical comparison between groups was performed using the Fisher’s exact probability test. All analysis were performed using the SAS Institute version 6.12 (Cary, NC) software.


    Results
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 Introduction
 Methods
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Grade 1 severity of the atherosclerosis was present in 133 patients, grade 2 in 25, grade 3 in 20, and grade 4 in 10 patients. Figure 1 illustrates their schematic distribution. The intimal lesions were more prevalent and more severe in the distal two-thirds of the ascending aorta, which happens to be the area closest to the clamp and cannulation sites.



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Fig 1. Schematic distribution of the atheromatous lesions in the ascending aorta. Lesions are more often encountered in the middle and distal thirds of the ascending aorta. In parentheses are the percentage of all lesions.

 
Multivariate regression analysis to assess the association of aortic atheromatous disease with history-related variables (gender, age, hypertension, diabetes, hyperlipidemia, cerebral vascular events, chronic renal failure, arteriosclerosis obliterans of lower extremities, and abdominal aortic aneurysm) identified abdominal aortic aneurysm (p < 0.001), arteriosclerosis obliterans (p < 0.04), and male gender (p < 0.03) to be significant independent predictors of the severity of atherosclerosis in the ascending aorta.

A typical ultrasonographic image after ECC is shown in Figure 2. Both cannulation sites of the arterial and cardioplegic cannulas usually projected into the aortic lumen but was considered as abnormal only if it had a mobile component. A new lesion in the ascending aorta intima was identified in 10 (5.3%) of 188 patients after decannulation (Table 2 ). New lesions were of the mobile type (5 patients, 4 with grading 3 or 4 before ECC), intimal tear (2 patients), and intimal irregularity (3 patients). Three of the new mobile-type lesions were related to the aortic clamp (2 to the cross-clamp, and 1 to the tangential clamp), and the other 2 to the aortic cannula jet, which typically is located opposite to the cannulation side (Figs 3 to 5 ).



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Fig 2. Typical image after extracorporeal circulation (post) after decannulation. Arrow 1: aortic cannulation site; arrow 2: cardioplegic cannulation site.

 

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Table 2. New lesions

 


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Fig 3. A new irregularity (arrow) appearing on the echographic image after decannulation that was not present before extracorporeal circulation (pre). (post = after extracorporeal circulation.)

 


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Fig 4. A new tear (arrow) has appeared on the posterior wall of the aorta. (post = after extracorporeal circulation; pre = before extracorporeal circulation.)

 


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Fig 5. Intimal tear (arrow 1) and subsequent new mobile lesion (arrow 2) are apparent on the image after decannulation but not present before extracorporeal circulation (arrow; pre). (post = after extracorporeal circulation.)

 
No stroke occurred in patients with only new intimal irregularity or intimal tears but no mobile component.

Five patients (2.7%) sustained a neurologic complication. Three of the 10 patients (3 of 10 [30%] with new lesions or 3 of 5 [60%] with a new mobile type lesion) had a stroke, whereas only 2 of 178 (1.1%) of the patients with no apparent intimal changes after surgical manipulation had a stroke; the incidence of stroke in patients with a new mobile-type lesion being significantly higher (p < 0.001) than in patients without new intimal changes.

The clinical profiles of these patients with postoperative stroke are summarized in Table 3. All patients were in sinus rhythm and none had evidence of intracardiac thrombus. Embolism was thought to be the cause of stroke in 3 of the 5 patients and hypoperfusion during ECC or postoperative period in the other 2 patients. Three of the 5 patients with new mobile-type lesions developed stroke, 2 being embolic (1 related to the cross-clamp and the other was the only patient on whom a side-biting clamp was used to perform the proximal anastomosis) by all standards, and likely to be embolic in the third one. Patients 3 and 4 had a mobile atheroma before ECC as well as new mobile lesions after ECC and both developed stroke but the stroke was believed by the neurologists to have been caused by hypoperfusion.


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Table 3. Postoperative neurologic complications

 
The mortality in patients developing permanent neurologic deficit is high; in fact 2 of the 5 patients with stroke died from infection on the 34th and 60th postoperative day, respectively. The only other death in this series was from gastrointestinal bleeding, thus stroke constituted the cause of death in two thirds of the deaths.


    Comment
 Top
 Abstract
 Introduction
 Methods
 Results
 Comment
 References
 
Stroke from atheroembolism has been recognized as the gravest complication after cardiac operation. Blauth and colleagues [12] identified atheroemboli and abnormalities consistent with atheroemboli in 48 of 221 patients (21.7%) that had undergone cardiac operations and who eventually came to autopsy; 46 of them (95.8%) had atherosclerosis of the ascending aorta and there was a high correlation of atheroemboli with the severity of the atherosclerotic changes.

Identifying the diseased ascending aorta before manipulation to be able to implement surgical technique deviations from the routinely used methods should intuitively help to avoid dislodging atherosclerotic debris, and ultrasonography has proved to be valuable to prevent strokes during cardiac surgical procedures [15, 811].

Epiaortic and transesophageal ultrasound have proved to be superior to palpation to recognize ascending aortic atherosclerosis; epiaortic ultrasound being more accurate than transesophageal echocardiography in evaluating atherosclerotic changes in the ascending aorta [13]. Ten percent of 100 consecutive patients undergoing cardiac operation reported by Davila-Roman and colleagues [1] had severe atherosclerosis by epiaortic echocardiography; age and diabetes being significant independent predictors of the presence of severe atherosclerosis in the ascending aorta. Our study identified abdominal aortic aneurysm and arteriosclerosis obliterans to be independent significant predictors, and at least in patients with these other risk factors epiaortic echocardiographic evaluation should precede cannulation regardless of the palpatory findings.

Although all strokes may not be prevented, epiaortic echocardiographic evaluation provides valuable information to warrant some sort of a major modification in the operative technique or procedure with rewarding results [15]. Wareing and associates [2] reported no strokes among 27 patients with moderate or severe atherosclerosis who had graft replacement of the aorta using hypothermic circulatory arrest, whereas the stroke rate was 6.3% in patients on whom only minor modifications had been implemented.

Of the 10 new lesions probable causes could be ascribed to aortic clamp in 7 patients (cross-clamp in 6, partial-clamp in 1), aortic cannulation in 1 patient, and the high-pressure jet from the arterial cannula tip in 2 patients. In these 2 patients new mobile-type lesions appeared opposite to the cannula in spite of having cannulated the ascending aorta in a relatively soft site without echocardiographic evidence of atherosclerotic changes, and not cross-clamping the aorta, compatible with the so-called sandblast effect [10, 11]. Whether the new mobile-type lesions represent ruptured atheroma plaque or thrombus forming at the site of intimal injury is uncertain because no postmortem studies were performed, but given the early postoperative timing of the two-dimensional echocardiographic study makes atheroma as the most likely structure.

The association between neurobehavioral changes after coronary artery bypass grafting and cerebral microembolization detected by carotid Doppler transducer has been recognized by Hammon and colleagues [14] and has served to implement strategy changes designed to reduce manipulation of the ascending aorta to minimize the number of microemboli [15].

The stroke complicating a number of operative procedures has been linked to dislodgement of material from an atherosclerotic aorta. Katz and associates [11] observed a mobile atheroma disappear after aortic cannulation during transesophageal monitoring and the patient had a stroke postoperatively, concluding that patients with mobile atheromatous disease are at higher risk for embolic strokes during cardiopulmonary bypass. Similar association between protruding aortic atheromas and spontaneously occurring embolic disease have been noted by other investigators [1619]. Tunick and colleagues [16] found protruding atheromas to independently predict vascular events: 14 of 42 patients with atheromas had 19 vascular events and only 3 of 42 control patients had events during a 2-year follow-up. Embolic events were more likely to occur if the debris was pedunculated and highly mobile, rather than when it was sessile and immobile [19]. Three of our 5 patients with a new mobile-type lesion had postoperative stroke; in 2 patients computed tomographic scans and neurologic findings were compatible with embolization (multiple infarction), whereas stroke occurred only in 2 of 183 patients without abnormality after decannulation. Therefore, prevention is the most effective and important measure to be taken, but at times difficult to accomplish [2, 3, 11].

Although our study failed to demonstrate an unequivocal relation between all new lesions caused by surgical manipulation and postoperative neurologic events, the incidence of neurologic events and cerebral embolism was significantly higher in those patients with a new mobile-type lesion (p < 0.001). Further observations in a larger number of patients may determine the role of the other new lesions in the genesis of postoperative neurologic deficits. Because new mobile lesions are caused either by the clamp (cross-clamp or the tangential side-biting clamp), the aortic cannulation, or the cannula jet, their use should be avoided in patients with predisposing atherosclerotic changes of the ascending aorta.

In our series, various degrees of modification of surgical procedures had been undertaken in all 5 patients with postoperative neurologic events. It is speculated that a more aggressive modification might have prevented, if not all, at least the embolic strokes. Further refinements in the ultrasonic imaging itself or in our assessment of the severity of atherosclerotic changes may offer a specific guide to decide the extent of the surgical modifications to effectively prevent postoperative strokes. In fact preliminary efforts at echographic quantification of the severity of the atherosclerosis have evolved into a scoring system that seems to be useful to determine the extent of the surgical technique modification to be undertaken.

In summary, this study corroborates the well-known usefulness of intraoperative epiaortic ultrasonographic imaging to identify before cannulation the atherosclerotic changes in the ascending aorta. Epiaortic evaluation should be performed at least in patients who have other stigmata of atherosclerotic disease (arteriosclerosis obliterans and abdominal aortic aneurysm). Reevaluation of the ascending aorta after surgical manipulation revealed intimal changes going from intimal irregularities, intimal tear to new mobile lesions; the causes could be ascribed mainly to the aortic clamp, the aortic cannulation, and the cannula jet. A significant number of patients with a new mobile lesion developed postoperative stroke. Reevaluation of ascending aorta after decannulation provided evidence of what had been theorized to be mechanisms of the embolization.


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Comment
 References
 

  1. Davila-Roman V.G., Barzilai B., Wareing T.H., Murphy S.F., Kouchoukos N.T. Intraoperative ultrasonographic evaluation of the ascending aorta in 100 consecutive patients undergoing cardiac surgery. Circulation 1991;84(suppl 3):47-53.
  2. Wareing T.H., Davila-Roman V.G., Daily B.B., et al. Strategy for the reduction of stroke incidence in cardiac surgical patients. Ann Thorac Surg 1993;55:1400-1408.[Abstract]
  3. Wareing T.H., Davila-Roman V.G., Barzilai B., Murphy S.F., Kouchoukos N.T. Management of the severely atherosclerotic ascending aorta during cardiac operations. J Thorac Cardiovasc Surg 1992;103:453-462.[Abstract]
  4. Marshall W.G.J., Barzilai B., Kouchoukos N.T., Saffitz J. Intraoperative ultrasonic imaging of the ascending aorta. Ann Thorac Surg 1989;48:339-344.[Abstract]
  5. Barzilai B., Marshall W.G., Jr, Saffitz J.E., Kouchoukos N.T. Avoidance of embolic complications by ultrasonic characterization of the ascending aorta. Circulation 1989;80(suppl 1):275-279.
  6. Mills N.L., Everson C.T. Atherosclerosis of the ascending aorta and coronary artery bypass. J Thorac Cardiovasc Surg 1991;102:546-553.[Abstract]
  7. Aranki S.F., Rizzo R.J., Adams D.H., et al. Single-clamp technique, an important adjunct to myocardial and cerebral protection in coronary operations. Ann Thorac Surg 1994;58:296-303.[Abstract]
  8. Ribakove G.H., Katz E.S., Galloway A.C., et al. Surgical implications of transesophageal echocardiography to grade the atheromatous aortic arch. Ann Thorac Surg 1992;53:758-763.[Abstract]
  9. Lynn G.M., Stefanko K., Reed J.F., III, Gee W., Nicholas G. Risk factors for stroke after coronary artery bypass. J Thorac Cardiovasc Surg 1992;104:1518-1523.[Abstract]
  10. Grossi E.A., Kanchuger M.S., Schwartz D.S., et al. Effect of cannula length on aortic arch flow, protection of the atheromatous aortic arch. Ann Thorac Surg 1995;59:710-712.[Abstract/Free Full Text]
  11. Katz E.S., Tunick P.A., Rusinek H., Ribakove G., Spencer F.C., Kronzon I. Protruding aortic atheromas predict stroke in elderly patients undergoing cardiopulmonary bypass. Experience with intraoperative transesophageal echocardiography. J Am Coll Cardiol 1992;20:70-77.[Abstract]
  12. Blauth C.I., Cosgrove D.M., Webb B.W., et al. Atheroembolism from the ascending aorta. An emerging problem in cardiac surgery. J Thorac Cardiovasc Surg 1992;103:1104-1112.[Abstract]
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