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Ann Thorac Surg 2002;74:650-659
© 2002 The Society of Thoracic Surgeons
a Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
b Department of Biostatistics and Epidemiology, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
* Address reprint requests to Dr Sabik, Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, 9500 Euclid Ave/F25, Cleveland, OH—44195 USA
e-mail: sabik{at}ccf.org
Presented at the Forty-eighth Annual Meeting of the Southern Thoracic Surgical Association, San Antonio, TX, Nov 8–10, 2001.
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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Methods. From 1988 through 2000, 103 patients with aortic PVE underwent root replacement with a cryopreserved aortic allograft. Abscesses were present in 78%, and aortoventricular discontinuity was present in 40%. Thirty-two patients had at least one previous operation for endocarditis. In 23 patients with a history of native valve endocarditis, the allograft was implanted after one episode (17 patients), two episodes (5 patients), or three episodes of PVE (1 patient). In the 80 patients without a history of native valve endocarditis, the allograft was placed after one previous aortic valve replacement (57 patients), two (19), or three (4) previous aortic valve replacements. Among the 92 patients with positive cultures, 52 had staphylococcal organisms, 20 had streptococcal, 6 had fungal, 4 had gram-negative, and 6 had enterococcal organisms. Mean follow-up was 4.3 ± 2.9 years.
Results. Hospital mortality was 3.9%. Permanent pacemakers were required in 31 patients. Survival at 1 year, 2 years, 5 years, and 10 years was 90%, 86%, 73%, and 56%, respectively, with a risk of 5.3% per year after 6 months. Four patients underwent reoperation for recurrent PVE of the allograft (95% freedom from recurrent PVE at 
2 years). Risk of recurrent PVE peaked at 9 months and then declined to a low level by 18 months.
Conclusions. A strategy of radical debridement and aortic root replacement with a cryopreserved aortic allograft for aortic PVE is safe, effective, and recommended.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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Mean age of the patients was 57 ± 15 years (range, 24 to 84 years). Eighty-two percent were men. Seventy-four patients had one previous aortic valve replacement, 24 had two, and 5 had three replacements. The sequence of aortic valve replacements and previous infections is presented in Table 1. Among the 23 patients with a history of native valve endocarditis, the allograft was implanted after one episode (17 patients), two episodes (5 patients), or three episodes of PVE (1 patient). In the remaining 80 patients, a cryopreserved aortic allograft was placed after one previous aortic valve operation (57 patients), two (19), or three previous aortic valve operations (4 patients).
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Fistulas were present in 15 patients (15%), and complete aortoventricular discontinuity was found in 41 (40%). Older patients were at higher risk for the latter (59 ± 16 years versus 55 ± 14 years, p = 0.003), as were those presenting with hypotension (41% versus 13%; p = 0.003) and those with staphylococcal infections (68% versus 39%; p = 0.009).
The interval from aortic valve replacement to operation for PVE was 3 months or less in 18 patients (17.5%), 6 months or less in 36 (35%), 1 year or less in 55 (53%), 2 years or less in 64 (62%), 5 years or less in 76 (74%), and 10 years or less in 95 patients (92%). See Appendix 1 for details.
Operative technique
All operations were performed through a median sternotomy. Cardiopulmonary bypass was performed with aortic cannulation in most patients, but not uncommonly using other routes (Table 5).
Right atrial or bicaval cannulation was used for venous drainage.
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In many cases, infection had destroyed the usual landmarks of the aortic root. To orient the allograft, the two fibrous trigones and anterior mitral valve leaflet on the allograft were aligned with the patient’s fibrous trigones and anterior mitral valve leaflet.
The coronary ostia were mobilized as buttons and sewn to the allograft with running 5-0 polypropylene monofilament suture. The distal anastomosis of the allograft to the ascending aorta was constructed in end-to-end fashion with running 4-0 polypropylene monofilament suture.
If the ascending aorta needed to be replaced, either an aortic valve allograft long enough to do this or an allograft aorta was used. Nonbiological material was avoided in reconstructing the aortic root or replacing the ascending aorta.
In reconstructing aortic roots with allografts, infected areas of myocardium were excluded from the systemic circulation. Allografts were sutured to the heart proximal to the infection. The most common site of abscess formation was the mitral-aortic intervalvular fibrosa (see Fig 1A). To exclude this abscess cavity from the circulation, the attached anterior leaflet of the mitral valve on the aortic allograft was sutured to the native anterior leaflet of the mitral valve (Fig 1B). The abscess cavity was not closed but allowed to "drain" into the mediastinum. The mediastinum was routinely drained with chest tubes for 48 to 72 hours.
Antibiotics were begun as soon as a diagnosis of PVE was made and continued for at least 8 weeks after operation. Patients with fungal infections were placed on a lifelong regimen of oral antifungal agents.
Follow-up
Follow-up was complete for all patients. Mean follow-up was 4.3 ± 2.9 years for survivors (maximum follow-up, 12.6 years), and 397 patient-years of total follow-up were available for analysis. Of the survivors, 77% were followed for 2 years, 30% for 5 years, and 7% for 10 or more years. Therefore, time-related depictions were truncated at 10 years.
Data analysis
Variables and end points analyzed
To characterize the endocarditis, descriptive statistics and multivariable logistic regression were used to identify factors associated with a single abscess, multiple abscesses, and aortoventricular discontinuity. To investigate hospital outcomes, multivariable logistic regression was used to identify predictors of respiratory failure, renal failure, and need for permanent pacemakers. To determine the rate of recurrent endocarditis and to identify risk factors for deathafter operation, multivariable analysis was performed in the hazard function domain [1].
Descriptive statistics
Descriptive statistics included the mean and standard deviation for continuous variables, and frequencies and percentages for categorical variables. Nonparametric estimates of time-related events were obtained using the Kaplan-Meier method. A parametric method was used to resolve the number of phases of instantaneous risk for each time-related end point (hazard function) and to estimate shaping parameters [1].
Multivariable analyses
Screening of variables for possible relation to findings of interest or end points employed contingency table methods, t testing, Cox proportional univariable analysis, and stratified life-table analysis using the log-rank test. Potential correlates and risk factors were organized for analysis as in Appendix 2. Continuous and ordinal variables were assessed univariably by decile risk analysis to suggest possible transformations of scale that best calibrated the variable with respect to model assumptions. For the small number of missing values, noninformative imputation of the mean value was used.
The primary variable selection method for all multivariable analyses was bootstrap bagging using 1,000 resampled data sets, a forward stepwise procedure, and a p value criterion for retention of variables of 0.05 [2]. Variables appearing in at least 50% of the bootstrap analyses were considered reliably identified.
Presentation
Confidence limits of proportions and time-related depictions are accompanied by confidence limits equivalent to one standard error (68%). Tables of risk factors identified in the hazard function domain are presented with regression coefficients rather than hazard ratios because the model is not one of proportional hazards and because many of the continuous factors were transformed to meet model assumptions. The latter reason also accounts for presentation of logistic regression coefficients rather than estimated odds ratios.
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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Complete heart block requiring a permanent pacemaker occurred in 31 patients (30%). It was more common in patients who had more than one previous operation (51% versus 18%), in those with multiple abscesses (45% versus 22%), and in those with an aortic bioprosthesis in place at the time of operation for PVE (65% versus 43%) (Table 6).
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Renal failure occurred in 24 patients (23%). Risk factors were older age (65 ± 12 years versus 54 ± 15 years) and higher preoperative creatinine level (1.9 ± 1.2 mg/dL versus 1.3 ± 0.84 mg/dL) (see Table 6).
Recurrent aortic prosthetic valve endocarditis
Four patients developed recurrent endocarditis. At the time of allograft insertion, 3 of the 4 had abscesses (multiple in 2), and 1 had aortoventricular discontinuity. All had active gram-positive infections, 1 had Staphylococcus aureus and a gram-negative organism, 1 had Staphylococcus epidermidis, and 1 had Enterococcus. All required reoperation. (Only 1 other patient underwent allograft explantation, and it was for subvalvular stenosis 2 years postoperatively.)
Freedom from recurrent endocarditis at 1 year, 2 years, 5 years, and 10 years was 96%, 95%, 95%, and 95%, respectively (Fig 2A). Instantaneous risk (hazard function) of recurrent aortic PVE peaked at 9 months (Fig 2B). Risk of recurrent endocarditis at 6 months, 1 year, and 2 years was 0.25% per year, 0.44% per year, and 0.08% per year, respectively. Of the 4 patients with recurrent endocarditis, 1 died 4 months after reoperation and 1, 10 years after reoperation.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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The goals of surgical therapy for aortic PVE include removal of all infected and necrotic material, repair of any resultant cardiac defects, and placement of a competent valve. However, severe destruction of the aortic root occurring with aortic PVE, including abscesses, aortoventricular discontinuity, fistulas, and ventricular septal defects, makes its reconstruction difficult.
A number of different operations to treat aortic PVE have been described. These include patch closure of annular and aortic defects and suturing of the prosthetic valve directly to the patch [14], supracoronary placement of the prosthetic valve with closure of coronary ostia and coronary artery bypass grafting [15], composite prosthetic valve conduit replacement and reimplantation of coronary ostia [16], the Ross procedure [17], and aortic root replacement with an allograft [11].
Principal findings
The strategy of treating aortic PVE with radical debridement and replacement of the aortic root and valve with a cryopreserved aortic allograft was effective. Hospital mortality was low, morbidity was related to aggressive infection, freedom from recurrent endocarditis was high, and long-term survival was good.
Hospital mortality
Hospital mortality was lower in our series (3.9%) than in other series (10% to 20%), [9, 10, 13, 14, 18] where mechanical or xenograft valves were used to treat PVE. We believe the improvement was due both to our strategy of radical debridement of infected tissue and to some features of allografts that make them especially beneficial in treating PVE. These features include (1) their flexibility, which allows allografts to be tailored to conform to aortic roots distorted by infection and debridement, (2) their attached anterior mitral valve leaflet, which can be used to repair defects such as fistulas, ventricular septal defects, and abscesses, and (3) their biological nature, which appears to make them relatively resistant to early recurrent infection [19–21].
Early survival after operation was indirectly related to the aggressiveness of the infection. All four hospital deaths occurred in patients with early, active, destructive staphylococcal infections. Fistulas and early-onset PVE were risk factors for early death; aortoventricular discontinuity was a risk factor for early operation for PVE.
Postoperative morbidity
Postoperative morbidity was related to the aggressiveness and destructiveness of the infection. Patients with multiple abscesses were more likely to experience respiratory failure postoperatively and to require permanent pacemakers. Almost one third of our patients, developed heart block requiring a permanent pacemaker after operation. This complication was due both to the aggressiveness of the aortic root infection and to the radical debridement necessary to eradicate it.
Recurrent endocarditis
Risk of recurrent endocarditis was also lower in our series compared with others. At 10 years, freedom from recurrent endocarditis was 95%, whereas others have reported 82% [10]. We believe our lower risk was due to both aggressive debridement of infected tissue and resistance of allografts to infection [19–21].
In our series, the pattern of risk of recurrent endocarditis also differed from that of other studies. We found that risk peaked about 9 months after operation and then declined slowly. In previous reports in which aortic allografts were used to treat both native valve endocarditis and PVE [19–21], risk did not peak but rather remained at a constant low level. Why our pattern was different is unclear, but it may have been due to the severe invasiveness of infections observed in our series and the fact that all the patients in our series had PVE. All 4 patients in whom recurrent endocarditis developed had deeply invasive and destructive infections. Despite radical debridement, not all infected material may have been excised. Postoperative antibiotic therapy may have quieted the infection but not completely eradicated it, thus accounting for the relatively late recurrence of endocarditis in a small number of patients.
Long-term survival
We believe this strategy for treating aortic PVE improves survival. Comparing the outcomes in this series with previous reports on endocarditis is difficult because most series contain heterogeneous patient populations; ie, patients with both native valve endocarditis and PVE, both mitral and aortic valve endocarditis, and both healed and active endocarditis. In our study, the patient population was fairly homogeneous; all patients had aortic PVE, and 92 had active culture-positive endocarditis.
Despite these difficulties in comparison, late survival in this report appears to be better than that in previous reports where mechanical or xenograft valves were used to treat PVE. If hospital mortality is included in determining late survival (not simply survival after discharge), long-term survival for patients with standard prostheses has been only about 50% to 60% at 5 years and 30% to 40% at 10 years [9, 10, 14, 18, 22, 23]. In a previous study of PVE from our institution [8], survival including hospital mortality was similar to that of this report—71% and 52% at 5 and 10 years, respectively. However, a substantial number of those patients underwent operation for healed PVE. We believe the improvement in survival in the present study is attributable in part to both the low hospital mortality and the low incidence of recurrent endocarditis (4 patients), which is itself important for long-term survival.
For additional perspective, we compared time-related survival of patients in this series with survival of patients who had the same characteristics undergoing reoperative aortic valve replacement for noninfectious indications (see Appendix 2 & 3). They were nearly identical (see Fig 3). This suggests that when patients with aortic PVE are treated with aggressive debridement and allograft aortic root replacement, the survival penalty paid for the presence of active endocarditis is neutralized. These patients appear to have a "normal" survival comparable to that of patients undergoing reoperative aortic valve replacement.
Limitations
Although this is the largest series reported to date of patients treated surgically for aortic PVE, in absolute numbers there were only 103 patients, and few had postoperative events. Therefore, it is not possible to determine predictors of hospital death or recurrence of endocarditis. Also, because half the patients had had previous aortic valve replacement at other institutions, referral patterns may have skewed the apparently long intervals between that operation and treatment of PVE or may have increased the prevalence of invasive PVE. It is also important to note that follow-up is too short to allow late allograft structural failure to affect outcomes and to assess whether endocarditis will have an adverse influence on allograft durability.
Conclusions
A strategy of radical debridement of infected and necrotic material and aortic root replacement with a cryopreserved aortic allograft was effective for aortic PVE. Hospital mortality was low, freedom from recurrent endocarditis was high, and long-term survival was good. Postoperative morbidity and early mortality were directly related to the aggressiveness of the infection. Heart block requiring a permanent pacemaker was a common complication of this aggressive therapy. On the basis of this study, we recommend this treatment strategy for aortic PVE.
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Acknowledgments |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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Appendix |
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Appendix 1. Timing of infection |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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To obtain probability density functions for subgroups of patients, the multivariable equation was solved for each patient across time, with each patient’s individual values for variables in the model. Estimates of the subgroup cumulative frequency distribution and probability density functions were then found by averaging these individual curves [24]. Factors associated with earlier and later time to operation for PVE were identified by multivariable analysis in the hazard function domain [1].
Results
The overall distribution of intervals between immediately preceding aortic valve replacement and operation for PVE exhibited an early peak 2 months after aortic valve replacement that fell to a persistent, but low level (Fig A1).
Factors associated with a short interval to operation for PVE included aortoventricular discontinuity, a more symptomatic patient, type of infective organism, and type of prosthesis before onset of PVE (Appendix Table 1). The shortest intervals to operation were observed in Staphylococcus epidermidis PVE (Fig A2).
Staphylococcus aureus infections exhibited somewhat longer intervals and streptococcal infections, the longest intervals, rather evenly distributed across time.
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Timing for this study was based on hard data on dates of operation. We did not have secure information about the date of onset of the infections.
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Appendix 2 |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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Symptoms and signs
New York Heart Association functional class, emergent operation, dyspnea, progressive heart failure, hypotension, syncope, preoperative neurologic event, persistent leukocytosis, persistent pyrexia, systemic embolization, progressive aortic regurgitation, interval between previous operation and operation for prosthetic valve endocarditis
Characteristics of endocarditis
Culture positive or negative, gram-positive or negative, specific infecting organism, presence of single abscess or multiple abscesses, fistulas, aortoventricular discontinuity
Preoperative medical management of endocarditis
Complete course of antibiotics, incomplete course, no antibiotics
Previous endocarditis
Native valve endocarditis, sequence of infection with respect to each operation, total number of occurrences of endocarditis
Prosthesis in place at time of prosthetic valve endocarditis
Type of prosthesis (mechanical, biological, allograft), device manufacturer, group of porcine xenograft devices, previous aortic replacement (ascending or arch)
Cardiac-related comorbidity
Family history of coronary artery disease, rhythm mechanism, total number of cardiac operations, presence of mitral regurgitation
Noncardiac comorbidity
Smoking history, renal disease, preoperative creatinine level, preoperative blood urea nitrogen level, preoperative bilirubin level
Procedure
Use of patch extension to allograft, replacement of ascending aorta or arch, concomitant operations, date of procedure
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Appendix 3. Expected survival |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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The multivariable equation was solved for time-related survival for each of the 103 patients using patient-specific values for model variables. The 103 curves were then averaged across time to yield expected survival [24].
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Discussion |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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DR SABIK: Five patients in this series have had the allograft removed. Recurrent endocarditis developed in 4 of them, and all 4 required reoperation and allograft replacement. Subvalvular stenosis developed in the other patient, and reoperation was necessary to relieve the obstruction. At the time of reoperation in that patient, the allograft valve leaflets appeared normal and pliable.
We have been unable to accurately determine all the causes of late death, and consequently I do not know how many of the late deaths were valve related. However, it does not appear to us that during the 10-year follow-up, allograft failure has been an important cause of late morbidity and mortality.
DR RANDALL B. GRIEPP (New York, NY): Dr Sabik, this is, I think, the lowest hospital mortality ever reported for acute prosthetic valve endocarditis, and you and your colleagues at The Cleveland Clinic are to be congratulated. I will discuss a slightly different approach.
For a number of reasons my associates and I have used prosthetic material in this situation. Over the same interval, we have operated on 28 patients with prosthetic valve endocarditis, either after previous aortic valve replacements or previous composite replacements. The adverse outcome was 11%; in other words, 89% of the patients were discharged from the hospital without neurological deficit. In that group, we had 1 patient who had recurrent endocarditis while still in the hospital and 1, within the first year, but there were no other instances of recurrent endocarditis in these patients, in all of whom a prosthetic conduit was used.
We agree with the first two of your three principles, beginning with the need for radical debridement of infected tissue. We also think it is important to remove a good part of the ascending aorta so that the conduit lies in vascularized tissue in the posterior pericardium. However, we have been amazed to see that prosthetic material seems to be very resistant to infection and to recurrent endocarditis.
One point I consider important is the durability of the repair. I wonder if the 5% ongoing mortality risk for your patients had anything to do with the aortic homograft per se, for example, in terms of the integrity of the valve.
DR SABIK: Prosthetic valve endocarditis clearly compromises the long-term outcome of patients after aortic valve replacement. Previously published series where mechanical or xenograft valves have been used to treat prosthetic valve endocarditis and where hospital mortality has been included in the long-term survival calculation have demonstrated 5 and 10-year survival of only 50% to 60% and 30% to 40%, respectively. It also appears that even when patients survive reoperation for prosthetic valve endocarditis, the long-term outcome is still compromised. These less than desirable results are possibly due to the complications of recurrent endocarditis, such as risk of reoperation and paraprosthetic leak. In our series, survival, including hospital mortality, was 73% at 5 years and 56% at 10 years. This improved long-term survival is due to our low hospital mortality and possibly to the low occurrence of recurrent infection. Allografts have been shown to have a low relative risk of infection, and in our series, freedom from recurrent endocarditis was 95% at 10 years.
As I stated earlier, we do not believe homograft failure has been a significant cause of late mortality and morbidity. However, the time period of this study is only 10 years, and I would not expect much allograft failure during that interval.
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsAppendix 1. Timing of...Appendix 2Appendix 3. Expected survivalDiscussion References |
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B. Mahesh, G. Angelini, M. Caputo, X. Y. Jin, and A. Bryan Prosthetic Valve Endocarditis Ann. Thorac. Surg., September 1, 2005; 80(3): 1151 - 1158. [Abstract] [Full Text] [PDF]
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L. M. Baddour, W. R. Wilson, A. S. Bayer, V. G. Fowler Jr, A. F. Bolger, M. E. Levison, P. Ferrieri, M. A. Gerber, L. Y. Tani, M. H. Gewitz, et al. Infective Endocarditis: Diagnosis, Antimicrobial Therapy, and Management of Complications: A Statement for Healthcare Professionals From the Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease, Council on Cardiovascular Disease in the Young, and the Councils on Clinical Cardiology, Stroke, and Cardiovascular Surgery and Anesthesia, American Heart Association: Endorsed by the Infectious Diseases Society of America Circulation, June 14, 2005; 111(23): e394 - e434. [Abstract] [Full Text] [PDF]
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N. Kucher, B. Kipfer, C. Seiler, and Y. Allemann Giant anastomotic pseudoaneurysm complicating aortic xenograft replacement Ann. Thorac. Surg., June 1, 2004; 77(6): 2197 - 2199. [Abstract] [Full Text] [PDF]
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R. G. Leyh, K. Knobloch, C. Hagl, A. Ruhparwar, S. Fischer, T. Kofidis, and A. Haverich Replacement of the aortic root for acute prosthetic valve endocarditis: Prosthetic composite versus aortic allograft root replacement J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1416 - 1420. [Abstract] [Full Text] [PDF]
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B. W. Lytle, J. F. Sabik, E. H. Blackstone, L. G. Svensson, G. B. Pettersson, and D. M. Cosgrove III Reoperative cryopreserved root and ascending aorta replacement for acute aortic prosthetic valve endocarditis Ann. Thorac. Surg., November 1, 2002; 74(5): S1754 - 1757. [Abstract] [Full Text] [PDF]
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