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J Thorac Cardiovasc Surg 1995;110:1745-1755
© 1995 Mosby, Inc.

SURGERY FOR ACQUIRED HEART DISEASE

SURGICAL MANAGEMENT OF INFECTIVE ENDOCARDITIS ASSOCIATED WITH CEREBRAL COMPLICATIONSMulti-center retrospective study in Japan

Osaka, Japan, for the 174 centers of the Japanese Association of Thoracic Surgery

From the Division of Cardiovascular Surgery, Division of Neurology, National Cardiovascular Center of Japan, Osaka, Japan. Supported in part by a grant for research on cardiovascular diseases from the Ministry of Health and Welfare, Japan.

Received for publication Dec. 23, 1994. Accepted for publication April 19, 1995. Address for reprints: Kiyoyuki Eishi, MD, Division of Cardiovascular Surgery, National Cardiovascular Center of Japan, 5-7-1 Fujishiro-dai, Suita, Osaka 565, Japan.

Abstract

To establish guidelines for the surgical treatment of patients with infective endocarditis who have cerebrovascular complications, we conducted a detailed retrospective study of 181 of 244 patients with cerebral complications among 2523 surgical cases of infective endocarditis of the Japanese Association of Thoracic Surgery. The results showed that 9.7% of all patients with infective endocarditis had associated cerebral complications: 108 (44.3%) had active native valve endocarditis, 96 (39.3%) had healed native valve endocarditis, and 40 (16.4%) had prosthetic valve endocarditis. The hospital mortality of the patients with cerebral complications was 11.0% in the group as a whole: 13.9% in active native valve endocarditis, 3.1% in healed native valve endocarditis, and 37.5% in prosthetic valve endocarditis. Diseased valves included the following: aortic valve in 55.5%, mitral valve in 49.8%, tricuspid valve in 1.3%, and pulmonary valve in 1.3%. In 181 patients with cerebral complications, organisms were detected as follows: gram-positive cocci in 133 (73.5% [Streptococcus in 85, Staphylococcus in 32]), gram-negative in 18 (9.9%), fungus in 11 (6.1%), and unknown in 19 (10.5%). Types of cerebral complications included cerebral infarction in 64.6%, cerebral bleeding in 31.5%, cerebral abscess in 2.8%, and meningitis in 1.1%. Hospital mortality rate and an exacerbation rate of cerebral complications, including related death, according to the interval from onset of cerebral infarction to cardiac surgery, were as follows: 66.3% and 45.5% within 24 hours, 31.3% and 43.8% between 2 and 7 days, 16.7% and 16.7% between 8 and 14 days, 10.0% and 10.0% between 15 and 21 days, 26.3% and 10.5% between 22 and 28 days, and 7.0% and 2.3% over 4 weeks later, respectively. A significant correlation existed between the interval and the exacerbation of cerebral complications (tied p = 0.008). Preoperative risk factors affecting exacerbation of cerebral complications were as follows: (1) severity of cerebral complication (p = 0.006), (2) intervals (p = 0.012), and (3) uncontrolled congestive heart failure as indications for cardiac surgery (p = 0.014). One patient underwent a cardiac operation within 24 hours of the onset of cerebral hemorrhage and died of cerebral damage. No exacerbations occurred in 10 patients who underwent their operation between 2 and 28 days. Nevertheless, exacerbations occurred in 19.0% of patients whose operation was done more than 4 weeks later. These data suggest that cardiac operations can be done safely 4 weeks after cerebral infarction, and if the delay is more than 2 weeks, the exacerbation rate will be around 10%. The risk of progression of cerebral damage is still significant 15 days and even 4 weeks after cerebral hemorrhage. (J THORAC CARDIOVASC SURG 1995;110:1745-55)

The best means of treating patients with infective endocarditis who have various complications such as severe congestive heart failure, intramyocardial abscesses, sepsis, major embolization, or cerebral aneurysm is the subject of controversy. In the past decade, early surgical treatment has been recommended even during the active stage before progression of the lesions. ^1-3 In patients with cerebrovascular complications, however, a surgical approach to the cardiac lesion still involves several unsolved problems. ^4-11 A major concern is the timing of cardiac surgery in these patients, because cardiopulmonary bypass with unusual hypotension and total heparinization would amplify the cerebral ischemic damage and hemorrhage. ⁸ Several groups, ours included, have tried to clarify the safety period between the cerebrovascular event and the cardiac operation, instead of limiting the number of patients with cerebral complications in each group. ^5,8-10 To establish the surgical treatment of patients with infective endocarditis associated with cerebrovascular complications, we conducted a detailed, retrospective analysis of 181 of 244 patients with cerebral complications among 2523 surgical cases of infective endocarditis of the Japanese Association of Thoracic Surgery (JATS).

PATIENTS AND METHODS

We sent a questionnaire to 600 centers belonging to the JATS and received replies from 261 centers, including 174 departments with 2523 patients having cardiac operations for infective endocarditis. A total of 244 patients had associated cerebral complications, and 181 of them were analyzed in detail. The questionnaire consisted of two parts: (1) Each center was asked for a summary of the number and outcome of patients with infective endocarditis according to the types of infective endocarditis ¹ (active/healed and native valve/prosthetic valve) and the presence of cerebral complications; (2) the other portion inquired about each patient with cerebral complications, asking for details such as age, gender, atrial fibrillation, anticoagulant therapy, diseased valve, organism, effectiveness of antimicrobial therapy, reason for early cardiac operation, interval between the onset of symptoms and the cardiac operation, type of cerebral complication, cerebral aneurysm, prior cerebral surgery, severity, influence of operation on cerebral damage, and outcome.

Analyses and statistics
The difference in mortality between the group without cerebral complications and the group with cerebral complications was tested for significance by ² analysis. A diseased valve and an organism were summarized as characteristics of the patients having associated cerebral complications. The type and timing of cerebral disease were documented. To study the influence of cardiac surgery on preoperative cerebral complications, we analyzed the interval between the onset of cerebral complications and performance of the cardiac operation, as well as other preoperative variables. The effectiveness of antimicrobial therapy was ranked in three grades (1 = ineffective, 2 = effective, and 3 = well controlled). Also, the severity of cerebral complications was ranked (1 = mild, 2 = moderate, and 3 = severe). Indications for early cardiac surgery included ineffectiveness of antimicrobial therapy, vegetations, and uncontrolled congestive heart failure. Cerebral angiographic examination was done in 58.8% of the patients with cerebral hemorrhage. A correlation between the interval and the exacerbation of cerebral complications was evaluated by means of the Spearman rank correlation coefficient. The intervals were then classified in several groups, and a variability between the groups for the exacerbation was estimated by Scheffe's F procedure for post-hoc comparisons, according to the Kruskal-Wallis test. To analyze the risk factors affecting exacerbation of cerebral complications, we expressed preoperative variables as mean ± standard error. The difference between the groups with and without exacerbation was tested for significance by the unpaired t test, and incidence was expressed as percentage of patients having the variable compared with the entire group of patients and then compared by ² analysis. Moreover, all variables and incidence (transformed to continuous variables) were estimated by stepwise regression analysis. Statistical significance was accepted at a p level of <0.05. These analyses were done with the Stat View system (Abacus Concepts, Inc., Berkeley, Calif.).

RESULTS

Summary of all patients with infective endocarditis
In total, 2523 patients having infective endocarditis were treated surgically in 174 centers of JATS. Of all the patients, 893 (35.4%) had active native valve endocarditis, 1317 (52.2%) had healed native valve endocarditis, and 315 (12.5%) had prosthetic valve endocarditis. Operative mortality rate was 13.5% in those with active endocarditis, 4.0% in those with healed endocarditis, and 33.3% in those with prosthetic valve endocarditis. On the other hand, 244 patients, 9.7% of all patients with infective endocarditis, had associated cerebral complications. A total of 1080 (44.3%) had active endocarditis, 96 (39.3%) had healed endocarditis, and 40 (16.4%) had prosthetic valve endocarditis. The mortality rates of the patients with cerebral complications were 13.9% (active endocarditis), 3.1% (healed endocarditis), and 37.5% (prosthetic valve endocarditis). No differences in mortality were detected between the group without cerebral complications and the group with cerebral complications (Table I).

Influence of cardiac surgery on preoperative cerebral infarction
In 11 patients, the cardiac operation was performed within 24 hours after the onset of cerebral infarction (mortality rate 66.3%) (Figs. 1 and 2). The operation was performed between 2 and 7 days later in 16 patients (mortality rate 31.3%), between 8 and 14 days later in 12 patients (mortality rate 16.7%), between 15 and 21 days later in 10 patients (mortality rate 10.0%), between 22 and 28 days later in 19 patients (mortality rate 26.3%), and more than 4 weeks later in 43 patients (mortality rate 7.0%). The rates of exacerbation of cerebral complications, including related death, were as follows: 45.5% in patients who were operated on within 24 hours, 43.8% in those operated on within 2 to 7 days, 16.7% for those operated on within 8 to 14 days, 10.0% for those operated on within 15 to 21 days, 10.5% for those operated on within 22 to 28 days, and 2.3% for those operated on more than 4 weeks later (Fig. 3). A significant correlation existed between the interval and the exacerbation of cerebral complications by the Spearman rank correlation coefficient (tied p = 0.008). When the intervals were classified in three groups (within 7 days, 8 to 14 days, and 15 to 28 days), a significant difference for the exacerbation was confirmed by post-hoc comparisons (p = 0.022) between the group within 7 days and the group treated at 15 to 28 days (Fig. 4).

View larger version (133K): [in this window] [in a new window]   Fig. 1. Computed tomographic scans of a patient with right middle cerebral artery infarction resulting from infective endocarditis. This patient underwent a Bentall-type operation for graft infection on the same day, resulting in massive brain swelling, and died 3 days later. Top row, Preoperative computed tomographic scans; bottom row, postoperative scans.

View larger version (34K): [in this window] [in a new window]   Fig. 2. Distribution of the patients and hospital mortality according to intervals from the onset of cerebral infarction until the cardiac operation.

View larger version (49K): [in this window] [in a new window]   Fig. 3. Exacerbation rate of cerebral damage including death related to cerebral injury according to the intervals from the onset of cerebral infarction (CI) until the cardiac operation.

View larger version (39K): [in this window] [in a new window]   Fig. 4. Correlation between the interval from the onset of cerebral infarction (CI) until the cardiac operation and the exacerbation of cerebral complications. When the intervals were classified into three groups, a significant difference in exacerbations was confirmed by post-hoc comparisons between the group operated on within 7 days and the group operated on within 15 to 28 days. ns, Not significant.

View larger version (124K): [in this window] [in a new window]   Fig. 5. Computed tomographic scans of a patient with cerebral hemorrhage resulting from infective endocarditis. This patient underwent mitral valve rereplacement 15 days after cerebral hemorrhage without any complications. Left, Preoperative computed tomographic scan; right, postoperative scan.

View larger version (27K): [in this window] [in a new window]   Fig. 6. Distribution of the patients and hospital mortality according to the intervals from the onset of cerebral hemorrhage until the cardiac operation.

View larger version (39K): [in this window] [in a new window]   Fig. 7. Exacerbation rate of cerebral damage including death related to cerebral injury (CB) according to the intervals from the onset of cerebral hemorrhage until the cardiac operation.

This study consisted of a questionnaire to the centers belonging to the JATS. The 181 patients gleaned from 244 patients with cerebral complications undergoing surgical treatment for infective endocarditis were able to be analyzed in detail. Several groups have tried to assess the effect of the timing of surgical therapy on patients with recent neurologic injuries. ^5,8-10 However, because of the limited number of cases, the appropriate timing of surgical intervention has not been addressed adequately. This study was based on a sufficient number for discussion of the effect of cardiac operations on patients with cerebral complications.

Characteristics of patients with cerebral complications
It has been reported that 20% to 30% of patients with infective endocarditis may have cerebrovascular complications. ^6,8,12-17 In this review of 2523 surgical cases of infective endocarditis, 9.7% of the total (12.1% of patients having active native valve endocarditis, 7.3% of those having healed native valve endocarditis, and 12.7% of those having prosthetic valve endocarditis) had associated cerebral complications. Cerebral ischemia was present in 64.6% and hemorrhage in 31.5%. ^6,18 Staphylococcus aureus was the most virulent organism involved in the central nervous system. ^1,6,7,18-20 However, in this study of cerebral complications, Streptococcus was the most common organism followed by Staphylococcus. This trend mirrors findings in the whole population of patients with infective endocarditis. ¹ In 42% of the patients with cerebral complications, antibiotics were ineffective.

Mortality of cardiac surgery in patients having infective endocarditis with cerebral complications compared with that of patients without cerebral complications
The operative outcome would be influenced by the organism, the intensity of cardiac dysfunction, the presence of annular abscess, and so forth. Irrespective of these factors, the mortality rate in patients with cerebral complications was no higher than that in patients without cerebral complications in this study (13.5% versus 11.0%). Also, the mortality rate in the patients with cerebral hemorrhage was no higher than that in patients with cerebral infarction (20.0% versus 20.7%). Pruitt and associates ²¹ reported that the mortality rate for 84 patients with neurologic complications was 58%, in contrast to the 20% mortality rate among the 134 patients without neurologic involvement. Operative mortality for early valve replacement ranges from 10% to 37%. ^2,7,20,22-26 The preoperative condition of the patients with cerebral complications, especially of those requiring early operation, would be more severe. Our results showed that preoperative cerebral complications caused a substantial number of deaths. It is clear that the timing of the cardiac operation affects the outcome in patients with cerebral infarction.

Influence of cardiac surgery on preoperative cerebral infarction
The major purpose of this study is to clarify how long to wait before performing a cardiac operation after the onset of cerebral complications in patients in whom early cardiac repair would be advisable. In 43.8% of the patients requiring a cardiac operation within 7 days after cerebral infarction, cerebral damage was exacerbated. The exacerbation rate decreased gradually with the timing of the operation and, in the group operated on after 28 days, it was 2.3%.

According to these data, a cardiac operation can be done safely after 4 weeks; after a delay of more than 2 weeks, the exacerbation rate will be around 10%. If the natural history of the patient receiving medication is expected to be very bad, surgical repair might be appropriate even in a week. Moreover, if the patient requires an early operation because of uncontrolled heart failure or if the preoperative cerebral infarction is severe, the risk of surgical treatment would be higher than expected according to timing of the operation. Ineffectiveness of antimicrobial therapy may affect cerebral damage, although such an effect was not verified statistically.

Influence of cardiac surgery on preoperative cerebral hemorrhage
The number of patients who underwent a cardiac operation within 4 weeks after cerebral infarction was large, whereas the number having the operation within 4 weeks after hemorrhage might be too small (13 patients) to allow us to evaluate the influence of the passage of time before heart surgery. However, heart surgery within 24 hours after cerebral hemorrhage has a high risk of causing fatal cerebral damage. Although no one of the 11 patients who underwent cardiac surgery between 15 days and 28 days after cerebral hemorrhage had exacerbation of cerebral damage during the operation, 19.0% of 21 patients operated on more than 4 weeks later had an exacerbation. These data suggest that there is some risk of progression of cerebral damage 15 days and even 4 weeks after the hemorrhage, regardless of the timing of the operation. The severity of cerebral complications and the ineffectiveness of antimicrobial therapy may affect cerebral damage, although this effect was not verified statistically. The incidence of clinically apparent mycotic aneurysm in patients with bacterial endocarditis was reported as 2% to 10%. ^{13-16,19,27,28} In our study, a cerebral aneurysm was noticed in about 80% of the patients with cerebral hemorrhage who received cerebral angiograms, and surgical treatment for cerebral aneurysm or hemorrhage would be expected to reduce the risk of cerebral damage during cardiac operations. To decrease the tendency toward hemorrhage, reduced heparinization in conjunction with a heparin-coated pump system would be useful during cardiac operations.

CONCLUSION

From a multi-center retrospective study, 181 patients with infective endocarditis and cerebral complications were analyzed in detail. The rate of exacerbation of cerebral complications decreased to 10% in patients who underwent surgical treatment more than 15 days after cerebral infarction and to 2.3% in those operated on more than 4 weeks later. Preoperative risk factors were severity of cerebral complications, interval from onset of symptoms to operation, and uncontrolled heart failure as the indication for cardiac surgery. More than 15 days after cerebral hemorrhage, the risk of the progression of cerebral damage is still significant, and this risk persists even 4 weeks later.

Acknowledgments

We are grateful to all the institutions belonging to the JATS for providing data for this manuscript.

Footnotes

J THORAC CARDIOVASC SURG 1995;110:1745-55

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