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Ann Thorac Surg 1995;60:538-543
© 1995 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Surgical and Long-Term Antifungal Therapy for Fungal Prosthetic Valve Endocarditis

Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Background. Fungal prosthetic valve endocarditis is an uncommon but serious disease. We have developed a strategy of treatment that includes perioperative amphotericin B, radical debridement of infected tissue, reconstruction using biologic tissue when possible, and prolonged oral suppressive antifungal therapy.

Methods. We retrospectively reviewed the charts of 12 patients reoperated on for fungal prosthetic valve endocarditis involving the aortic valve (10 patients: six porcine valves, two mechanical valves, two homografts) and the mitral valve (2 patients, both porcine valves). Prosthetic valve endocarditis developed in 7 within 12 months after the first valve procedure. The organisms included Candidaspecies (9 patients), Scopulariopsis brevicaulis (1), Saccharomyces cervisiae (1), and histoplasmosis (1).

Results. At operation, all patients had prosthetic vegetations, 8 had abscesses, and 4 had sinus tracts. Seven received aortic homografts, 4 received porcine valves (two mitral), and 1 received a mechanical prosthesis. Two patients died in the hospital after prolonged illnesses (83% hospital survival). Four patients had recurrence an average of 25 months later and 3 underwent further surgical intervention. One patient had recurrence and died 17 months postoperatively. One other late death occurred 96 months after operation, and there was no evidence of recurrence. Eight patients (67%) are alive and well 51.5 +/- 61.0 months (range, 1 to 189 months) after the first redo procedure for fungal prosthetic valve endocarditis.

Conclusions. We conclude that preoperative treatment with amphotericin B, radical resection of all infected tissue, cardiac reconstruction using biologic tissue when possible, and life-long oral antifungal therapy is effective for fungal prosthetic valve endocarditis.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Fungal prosthetic valve endocarditis (PVE) is an uncommon but serious disease with historically high fatality rates [1, 2]. Traditional therapy for this disorder has consisted of intravenous amphotericin B with or without flucytosine and surgical replacement of the infected prosthesis [1, 2]. Although all reported series are small, hospital survival rates have been only 20% to 45% [2–6], and late survival has also been unfavorable because of the difficulty of eradicating the infection.

This report examines the results in 12 patients with fungal PVE treated surgically during the years 1978 through 1994. Since 1988, we have combined radical excision of infected tissue and valve replacement with indefinite treatment with oral azole agents in addition to perioperative amphotericin.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Patient Population
From November 1978 through December 1994, 184 patients were operated on for PVE at The Cleveland Clinic. Twelve had fungal PVE, and their charts were retrospectively reviewed. Six were men. The average age was 51.3 +/- 16.9 years (range, 23 to 71 years); 4 patients were older than 65 years. Fungal infection involved an aortic prosthesis in 10 patients and a mitral prosthesis in 2. In the aortic position, five infected valves were porcine, two were mechanical, two were homografts, and one was pericardial. In the mitral position, both infected valves were porcine bioprostheses.

Initial operative procedures included aortic valve replacement in 7 patients, composite aortic root replacement in 1 patient, aortic valve replacement and coronary artery bypass grafting in 1, aortic valve replacement and mitral valve repair in 1, aortic and mitral valve replacements in 1, and mitral valve replacement in 1. Porcine valves were inserted at the initial operation in 7 patients, mechanical valves in 2, aortic homografts in 2, and a pericardial valve in 1 patient.

Prosthetic valve endocarditis was termed early when it appeared within 12 months of valve insertion and late when it occurred after 1 year. Fungal PVE developed early in 7 patients and late, in 5 (Fig 1). The time to infection did not correlate with the valve position.

View larger version (30K): [in this window] [in a new window]   Fig 1. . Time interval between valve replacement and development of fungal prosthetic valve endocarditis.

Cultures from each patient at operation grew fungus. Candida albicans infected 5 patients; Candida parapsilosis, 3; and Scopulariopsis brevicaulis, Candida chaetamion, histoplasmosis, and Saccharomyces cervisiae, 1 patient each. Amphotericin B was begun preoperatively in 11 patients in whom a diagnosis was made before operation. In 1 patient, the diagnosis was reached at the time of operation, and a regimen of amphotericin B was begun postoperatively. Only patients demonstrating congestive heart failure underwent emergent operation; the others were given a variable course of amphotericin B preoperatively to ensure adequate tissue levels. In general, operation was approached in an urgent fashion as opposed to an emergent fashion.

All patients had preoperative transthoracic echocardiograms, and vegetations were detected on all. Eight patients had paraprosthetic abscesses, 3 had intracardiac sinus tracts, and 1 had an aorta–right ventricular fistula. Nine patients had normal left ventricular function, 1 patient had mild dysfunction, and 2 had moderate dysfunction.

Surgical Technique
All patients had reoperation through a repeat median sternotomy. Standard cardiopulmonary bypass at hypothermia with antegrade and retrograde cardioplegia was used. After explantation of the prosthetic valve, infected tissue was radically debrided. Seven patients with infected aortic prostheses and 1 patient with an involved mitral prosthesis had paraannular abscesses. Abscess cavities and sinus tracts were also extensively debrided. Autologous pericardium was used to repair the aorta–right ventricular fistula. In general, an attempt was made to avoid closing off paraprosthetic abscess cavities with bioprosthetic material (for fear of future abscess formation).

In 7 patients with infected aortic valve prostheses, reconstruction was accomplished using an aortic root homograft with reimplantation of the coronary arteries. The 3 others, operated on prior to the availability of homografts at The Cleveland Clinic, had prosthetic valves reinserted into the aortic position. Two were porcine valves, and one was a mechanical valve. Only 1 patient with mitral PVE had an annular abscess requiring aggressive debridement and bovine pericardial reconstruction of the mitral annulus. The other patient with mitral prosthetic endocarditis had an infection involving only the bioprosthetic leaflets, and annular debridement was not required. Both patients received porcine bioprostheses.

One patient sustained two further episodes of fungal PVE. She underwent a redo valve operation for each episode. At each reoperation, only the bioprosthetic leaflets were involved, and therefore only valve replacement was performed.

The entire group of 12 patients received an average of 1.8 +/- 0.7 g (range, 1 to 3 g) of amphotericin B perioperatively. Renal function deterioration limited higher doses in the majority of patients. Four patients were given flucytosine in addition to amphotericin to take advantage of the synergy of the two drugs against certain species of Candida, thus permitting the use of smaller doses of the latter drug.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Two patients died in the hospital or within 30 days of operation, an 83% hospital survival rate. One patient was seen 4 months and the other, 21 months after the initial valve replacement. Both had infected aortic prostheses. At the original valve replacement, 1 received a mechanical valve and the other, an aortic root homograft. Each died of multiorgan failure and uncontrolled sepsis after a prolonged hospital illness. The two fungi involved were C albicans and C parapsilosis.

There were two late hospital deaths at 17 and 96 months postoperatively. One of these patients was never truly cured of fungal PVE. He had severe chronic fungal toenail infection (S brevicaulis), which eventually infected the aortic homograft valve. The fungus was resistant in vitro to amphotericin B as well as all oral azoles. Despite treatment with a 2.5-g total dose of amphotericin B and long-term suppressive antifungal therapy (fluconazole), he was seen again with recurrent lower extremity emboli and died of uncontrolled fungal sepsis 17 months after the first redo operation. He was the only patient with a fungus resistant to all antifungal therapy and whose infection therefore could not be controlled. The other late death occurred as a result of an automobile accident.

Nine of the 10 hospital survivors were discharged home on a regimen of long-term oral suppressive antifungal therapy. One patient developed an allergy to Itraconazole and therefore was not maintained on suppressive therapy. Five were discharged on a regimen of fluconazole (200 to 400 mg/d); 3, ketoconazole (200 mg/d), and 1, Itraconazole (220 mg/d). The only complication to long-term oral therapy was anorexia, noted in 1 patient, which subsided after the dose was reduced. Otherwise, patients tolerated oral suppressive therapy well.

Late follow-up information was available on all patients. Eight patients are currently alive and well without evidence of recurrent disease an average of 51.5 +/- 61.0 months postoperatively (range, 1 to 189 months). Long-term survival is depicted in Figure 2. Four of the 8 patients are alive and well 5 years or more after initial operation for fungal PVE. The patient who has survived longest underwent the initial mitral valve replacement 15 years ago. She has required three reoperations for recurrent fungal PVE, as already noted. All surviving patients are in New York Heart Association functional class I. Two of the 4 patients are more than 65 years old and are alive and well 10 and 15 months after operation.

View larger version (15K): [in this window] [in a new window]   Fig 2. . Long-term survival after prosthetic replacement for fungal prosthetic valve endocarditis. Figure includes hospital mortality and represents the duration of survival after prosthesis replacement.

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Fungal PVE is not a common disease. During the 16-year period of our study, 10,780 heart valve replacements were performed at The Cleveland Clinic Foundation. There were 184 cases of PVE (1.7%), and 12 (6.5%) of them were due to fungus (0.1% of all heart valve replacements). This is not a true incidence, as some patients were referred to us from outside institutions. Nonetheless, it is an uncommon complication of valve replacement surgery and important because of its grave prognosis.

Untreated fungal PVE is uniformly fatal [3]. Initial attempts to treat fungal prosthetic endocarditis with amphotericin B and flucytosine were also uniformly unsuccessful [1, 2]. Treatment results improve greatly with surgical replacement of the infected prosthetic valves combined with perioperative antifungal therapy [2]. However, hospital survival rates remain lower than 40% [1, 2], and late recurrences are frequent [4–6]. Our strategy represents another improvement in the management of this devastating problem. By employing aggressive amphotericin B therapy perioperatively, radical surgical debridement of all infected tissue, valve replacement using biologic tissue when possible, and indefinite oral suppressive antifungal therapy, we have been able to record a greater than 50% 5-year survival rate that includes hospital deaths and survival after reoperation for this disease.

Our ability to accurately diagnose fungal PVE may also have influenced our results. The widespread use of echocardiography has been a major advancement to this end [8]. Two-dimensional echocardiography has improved the detection rate of valvar vegetations to 85% [8, 9]. However, a negative study does not rule out the presence of valvar endocarditis [10–12]. The use of transesophageal echocardiography has further improved the detection rate of prosthetic endocarditis, specifically in patients with prosthetic mitral valve endocarditis [13]. Imaging the mitral prosthesis through the left atrium provides an unobstructed view of the mitral orifice, and vegetations can be seen more accurately [14].

Moreover, we experienced a high incidence of positive fungal blood cultures in our series, and this helped secure an earlier diagnosis. Most historical series report positive fungal cultures in only 50% of patients affected [3]. This may be due to use of the lysis centrifugation technique [7], but we also did not have a case of Aspergillus PVE. Patients with Aspergillus endocarditis rarely have positive blood cultures [15]. Fungal endocarditis characteristically produces bulky vegetations, and systemic embolization is now known to be characteristic of this disease. These findings should increase one's suspicion that the disease is present. Indeed 58% of our patients were seen with bulky emboli, one of the most frequent findings when patients are first seen [8, 11]. The difficulty of establishing a correct diagnosis before death and therefore of initiating appropriate therapy early in the disease process likely has contributed to the historically poor results associated with this disease.

Surgical removal of the infected prosthesis remains the most important aspect of treating patients with fungal PVE. We aggressively debride all necrotic infected tissue and reconstruct the heart with biologic tissue when possible. The use of homografts to reconstruct the left ventricular outflow tract may also help in the treatment of endocarditis. Homografts facilitate the surgical management of paraannular abscesses and may be more resistant to recurrent infections. Paraannular abscesses are frequently associated with fungal PVE [6]. In our series, 67% of the patients had paraprosthetic abscesses. Homograft aortic root replacement provides an excellent method of excluding abscesses and reconstructing the left ventricular outflow tract. Abscess cavities in the left ventricular outflow tract can be managed by suturing the leading edge of the homograft annulus to the inferior border of the abscessed cavity. The abscessed cavity is not covered over, thus leaving a packet of infected tissue that can lead to recurrent infection, paraprosthetic leak, and dehiscence of the prosthetic valve.

Homografts have been shown to reduce the risks of early bacterial infection [16, 17]. This may also be true for fungal endocarditis. Further, the aortic root homograft has been shown to be very durable with excellent long-term results when used to reconstruct the left ventricular outflow tract complicated by paraprosthetic valve abscesses [18]. Of the 7 patients treated for fungal PVE using a homograft, only 1 had a recurrence. This fungus (S brevicaulis) was resistant to all tested antifungal agents, and the infection was never truly eradicated. Although the use of homograft material in patients with fungal PVE does not completely prevent reinfection, the majority of our patients were adequately treated with use of a homograft. This was universally true in patients who had fungal organisms sensitive to antifungal agents. Homografts remain our prosthesis of choice for these reasons.

Antifungal drug therapy remains an important part of the management of patients with fungal PVE. Amphotericin B, traditionally the drug of choice, is nephrotoxic and cumbersome to administer [4], which limits the extent to which it can be used. Nonetheless, perioperative administration of amphotericin B achieves excellent blood and tissue levels prior to operation and may help to reduce the incidence of early recurrence. In an effort to better control the fungal process, we prefer to treat all patients with amphotericin B perioperatively.

Despite amphotericin therapy and surgical prosthetic replacement, it is doubtful that the patient is ever truly cured of fungal PVE. Johnston and associates [4] in a review of the surgical literature demonstrated the propensity for Candida fungal PVE treated with amphotericin B and surgical valve replacement to recur months after treatment. Thirty-three percent of our patients experienced recurrent fungal PVE an average of about 2 years after the first valve replacement for the disease. The high incidence of recurrence in our patients as well as our experience with patients who were apparently cured only to sustain recurrence soon after stopping oral suppressive therapy has led us to conclude that all patients should be maintained on lifelong suppressive antifungal therapy.

Others [4, 6] have come to similar conclusions. Johnston and coauthors [4] suggested the use of fluconazole for long-term suppression of presumed residual foci of Candida after a course of amphotericin B (>2 g total dose over 6 to 8 weeks) and valve replacement. Miller [6] came to a similar conclusion after reviewing the Stanford experience. Fluconazole, a potent antifungal compound, can be taken orally once a day. The drug is relatively safe to use. Moreover, in a 1985 report [19], fluconazole appeared to have none of the adverse effects of amphotericin B or flucytosine. Animal studies have demonstrated the efficacy of azole agents used to treat fungal native valve endocarditis. In a rabbit model of endocarditis [20], valve leaflets were cleared of vegetations by fluconazole (20 mg/kg) but were not reliably cleared by amphotericin (3 mg/kg) or flucytosine (35 mg/kg), either alone or in combination.

There is evidence that azole agents can successfully treat fungal PVE even when used alone in highly select cases. Czwerwiec and colleagues [21] reported one case of their own and reviewed two other case reports in which fluconazole was used successfully as the only therapy in patients with Candida PVE. In 2 of these patients, long-term resolution was obtained with long-term oral fluconazole therapy. The third patient had a recurrence of endocarditis and died 10 days after discontinuing fluconazole. Surgical therapy was contraindicated in each patient because of compounding medical problems, and the patients could not take amphotericin. None of the patients had congestive heart failure. Even more impressive was that each of these patients demonstrated resolution of the prosthetic vegetations on echocardiographic monitoring while on a regimen of fluconazole therapy. It is important to understand, however, that a tissue diagnosis was not obtained in any of these patients; therefore the diagnosis of fungal PVE was not substantiated, and the diagnosis is somewhat in doubt.

Despite the use of long-term suppressive antifungal therapy, long-term cure may not be possible. Our patient with S brevicaulis, which was resistant in vitro to both amphotericin and fluconazole, had recurrence postoperatively while on a regimen of fluconazole. This fungus may be especially difficult, if not impossible, to eradicate. In vitro sensitivity of antifungal agents is fraught with problems of irreproducibility and typically corresponds poorly to the high activity of these agents in vivo [22]. Therefore, on the basis of drug-sensitivity testing, it is difficult to predict which patients will be resistant to all forms of therapy. The low toxicity of azole agents and their ease of administration have led some researchers to expand their use to all patients undergoing a valve operation.

Longman and associates [20] suggested the use of fluconazole as prophylaxis in all patients undergoing valve replacement. However, the low incidence of fungal PVE (0.1% in our series) does not seem to justify this. Its use in patients in whom transient fungemias develop after initial valve replacement may be beneficial after a course of intravenous amphotericin B. Fang and co-workers [23] demonstrated the high risk of fungal PVE in patients who experience transient fungemias. In their report on 9 patients who had undergone prior valve replacement and had sustained transient fungemias, 3 (33%) had evidence of fungal PVE, and on further evaluation, 2 (22%) went on to develop PVE later. Presumably the high in vivo activity of oral azole antifungal agents may have prevented some of these patients from progressing to fungal PVE as suggested by Longman and associates [20]. The efficacy of prophylactic oral antifungal agents has not been proved clinically. We do not advocate the use of oral azole therapy alone to treat known cases of endocarditis but bring up these examples as a potential new use of oral antifungal agents in patients who experience transient fungemia after heart valve replacement.

Using the described approach to fungal PVE, we believe that we have improved on the historically poor results of fungal PVE. Lifelong antifungal suppression and follow-up are needed in these extremely difficult patients. Recurrent fungal PVE is common, especially if antifungal therapy is discontinued. A combined medical and surgical approach that includes early diagnosis, aggressive surgical debridement of all infected tissue, removal of the infected prosthesis, intensive amphotericin B therapy, and lifelong oral suppressive therapy can improve the historically poor treatment results of this devastating disease.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Presented at the Poster Session of the Thirty-first Annual Meeting of The Society of Thoracic Surgeons, Palm Springs, CA, Jan 30-Feb 1, 1995.

Address reprint requests to Dr Muehrcke, Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195.

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Derek D. Muehrcke Bruce W. Lytle Delos M. Cosgrove, III Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Muehrcke, D. D. Articles by Cosgrove, D. M. Search for Related Content PubMed PubMed Citation Articles by Muehrcke, D. D. Articles by Cosgrove, D. M., III