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Ann Thorac Surg 2007;83:1295-1302
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Predictors of Death and Impact of Surgery in Staphylococcus aureus Infective Endocarditis

Jean Paul Remadi, MDa, Gilbert Habib, MDb, Georges Nadji, MDa, Amel Brahim, MDa, Franck Thuny, MDb, Jean Paul Casalta, MDb, Marcel Peltier, MDa, Christophe Tribouilloy, MD, PhDa,*

a Department of Cardiovascular Disease, INSERM, ERI-12 CHU, Amiens, France
b Department of Cardiology, La Timone Hospital, Marseille, France

Accepted for publication September 28, 2006.

* Address correspondence to Dr Tribouilloy, INSERM, ERI-12 CHU, Hôpital Sud, Avenue René Laënnec, 80054 Amiens, Cédex 1, France (Email: tribouilloy.christophe{at}chuamiens.fr).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: We studied a large cohort of adults with Staphylococcus aureus infective endocarditis to evaluate the predictors of outcome and to establish whether early surgery is associated with reduced mortality.

Methods: The study prospectively enrolled 116 consecutive patients with definite S aureus infective endocarditis, according to Duke criteria and examined by transthoracic and transesophageal echocardiography.

Results: The in-hospital mortality rate was 26%, and the 36-month survival rate was 57% ± 5%. Multivariate analyses identified comorbidity index, congestive heart failure, severe sepsis, prosthetic valve infective endocarditis, and major neurologic events as predictors of in-hospital mortality; severe sepsis and comorbidity index as predictors of overall mortality; and the comorbidity index as a predictor of late mortality. In unadjusted analyses, early surgery performed in 47% of patients was associated with lower in-hospital mortality (16% versus 34%; p = 0.034) and with better 36-month survival (77% ± 6% versus 39% ± 7%; p < 0.001). After adjustment of baseline variables related to mortality, early surgery remained associated with reduced overall mortality.

Conclusions: Prognosis of S aureus infective endocarditis remains poor, related to the comorbidities, presence of congestive heart failure, severe sepsis, major neurologic events, and prosthetic valve. Early surgery is independently associated with reduced overall mortality and should be considered in selected cases to improve the outcome.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Staphylococcus aureus is the leading cause of infective endocarditis (IE) in many regions of the world [1–3]. The frequency of S aureus IE increases constantly and was recently estimated at between 25% and 50% of cases [1–5]. S aureus IE is associated with a poor prognosis. It is more severe than the IE prognosis of other pathogens (excluding fungal pathogens), with a high in-hospital mortality of 30% to 46%, according to various authors [2, 6–8], and even reaching 71% in a study published in 1986 [9]. Prognostic factors in S aureus IE have not been clearly identified, however, because only a few recent studies have been specifically devoted to S aureus IE [1, 10–15].

We focused this study solely on early surgery results for S aureus IE, to the exclusion of other pathogens. We analyzed and compared the results of medical treatment alone with those of combined medical and surgical treatment to try to optimize the management of these patients. This two-center study was performed with the objectives of (1) identifying the determinants of outcome in a large population of consecutive patients with definite S aureus IE according to Duke criteria, and (2) determining whether early surgery was associated with reduced mortality.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patients
From January 1991 to January 2001, 116 consecutive patients (76 men and 40 women, mean age 55.8 ± 16.8 years) from two French centers (Amiens, 61 patients; Marseille, 55 patients) with definite S aureus IE according to Duke criteria [15, 16] (Table 1) were prospectively enrolled and formed our study population. The Duke criteria were applied retrospectively to patients hospitalized before publication of Duke criteria. This study was approved by each center’s Ethics Committee, and patient consent was not necessary.


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  		Table 1 Association Between Patient’s Characteristics and In-Hospital Mortality
 
Early surgical intervention was defined as surgery performed during hospitalization for management of IE [17, 18]. All patients had blood cultures that were positive for S aureus and underwent systematic transthoracic (TTE) and transesophageal echocardiographic (TEE) studies. All patients were scheduled for 4 to 6 weeks of antibiotic treatment. During the same period, 498 patients with definite IE (streptococcus predominantly), according to Duke criteria, were admitted.

Clinical Indicators
Age, gender, presence of comorbidities, valvular heart disease, valve prosthesis, a cardiac surgical procedure, presence of an intravascular device (venous catheter, pacemaker, and dialysis device), and the portal of entry were analyzed. A validated comorbidity index (Charlson index) taking into account the patient’s age, and other specific comorbid states was calculated [19].

The following acute clinical events present on admission or occurring during hospitalization were recorded: moderate-to-severe congestive heart failure, neurologic events, peripheral embolism, and severe sepsis. The duration of symptoms before admission (interval between the presumed onset of symptoms and the date of admission for IE) and the portal of entry of the infection were investigated. The diagnosis of embolic events was determined by clinical signs and data derived from noninvasive procedures. Cerebral and thoracoabdominal computed tomography (CT) scans were performed in 65% of patients. A major neurologic event was defined by the development of an ischemic stroke with hemiplegia, a hemorrhagic stroke, a cerebral abscess, features of encephalopathy, or coma [20]. A minor neurologic event was defined by a transient ischemic attack or cerebral embolic accident with no serious clinical signs [20]. Severe sepsis was defined as a systemic inflammatory syndrome secondary to an infectious process, leading to organ dysfunction, signs of hypoperfusion, or hypotension [21].

Echocardiography
Echocardiography was performed on a Hewlett-Packard Sonos phased-array ultrasound system (HP 1000, HP 2500, or HP 5500; Palo Alto, CA) using a 2.5-MHz transthoracic transducer and a 5-MHz transesophageal transducer. TTE was systematically completed by TEE. All echocardiographic studies were performed by standard techniques and by experienced echocardiographers without any complications during the acute phase of IE. Standard definitions were used for vegetations, abscesses, and other cardiac infective lesions [15, 22–24]. All TEE recordings were reviewed by an experienced echocardiographer to measure the maximum length of vegetations in various planes [25]. The mobility of vegetation was graded on a scale of 1 to 4, with severe mobility corresponding to grade 4 [26]. Valvular regurgitation was quantified by Doppler echocardiography using the standard methods [27].

Baseline Characteristics
Table 1 summarizes clinical and echocardiographic findings in the 116 cases of S aureus IE. IE affected the valve prosthesis in 17% of patients (mechanical prosthesis in 9%, biologic prosthesis in 8%). Vegetations were visualized in 93% of patients and perivalvular abscesses in 21%. The main portal of entry was cutaneous in 49%. Right side IE represented 26% of S aureus IE cases. Seven patients (6%) had a history of intravenous drug abuse.

Surgical Management
Early surgery (during the initial hospitalization) was performed in 55 patients (47%; Table 2). The indications for early surgery included severe heart failure in 12 patients (22%), large persistent vegetation after systemic embolism in 9 (16%), uncontrolled infection in 9 (16%), severe regurgitation in 4 (7%), pacemaker line infection in 8 (14.5%), abscess or perivalvular involvement in 2 (3.6%), and multiple indications in 7 (13%). Among these 55 patients, 9 had mechanical valves (6 aortic valves, 3 mitral valves), 13 had biologic valves (7 aortic valves, 6 mitral valves), 14 had mitral or tricuspid valve repair, 10 had pacemaker line extraction, and 9 had an aortic homograft valve. The mean length of antibiotic therapy before surgery was 12 ± 9 days.


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  		Table 2 Comparison of Characteristics of Medical Group and of Early Surgical Group
 
Thirty-seven (67.2%) of these 55 patients underwent surgery within the first 15 days after being diagnosed with IE. Three patients were treated medically and underwent surgery after the initial hospitalization for persistent valvular regurgitation (no operative death).

Follow-Up
Follow-up data included surgical treatment and death occurring during initial hospitalization or follow-up. In-hospital mortality was defined as death occurring during the initial hospitalization for IE [17, 18]. Overall mortality included death occurring during initial hospitalization and follow-up. Late mortality excluded death occurring during initial hospitalization. The follow-up was completed in 100% of patients, with a mean patient follow-up of 23 ± 11 months.

Statistical Analysis
Statistical analysis was performed with SPSS 9.0 (SPSS Inc., Chicago, IL). Quantitative variables were expressed as the mean ± standard deviation. Comparisons between groups were calculated using the Student t test or the {chi}2 test. The cumulative probability of survival was estimated using the Kaplan-Meier actuarial method at 1-month intervals and reported as a mean estimated survival ± standard error. The log-rank test was used to determine any significant differences. Multivariate analyzes were performed incorporating as potential predictors of mortality the comorbidity index and variables related to mortality in univariate analysis with p ≤ 0.10. A multivariate logistic regression model was used for in-hospital mortality and a Cox multivariate model for overall mortality and for late mortality. A probability of p < 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
In-Hospital Mortality
Thirty patients died, for an in-hospital mortality rate of 26% for the entire group. The main causes of death included multiorgan failure in 12 patients, neurologic events in 4, sudden death in 4, heart failure in 7, intraoperative death in 2, and tamponade in 1. Univariate analysis revealed that factors related to in-hospital mortality were the comorbidity index, history of renal failure, valvular prosthetic IE, congestive heart failure, severe sepsis, major neurologic events, and early surgery (Table 1). Multivariate analysis identified congestive heart failure, severe sepsis, prosthetic IE, major neurologic events, and the comorbidity index as independent predictors of in-hospital mortality (Table 2).

Overall Mortality and Late Mortality
The overall survival at 36 months was 57% ± 5% (Fig 1). Twenty of the 86 patients that survived hospitalization died during the follow-up after discharge. The causes of late death included heart failure in 5, neurologic events in 2, cancers in 3, sudden death in 1, myocardial infarction in 1, and was unknown in 8. Three patients underwent surgery after the initial hospitalization for management of IE (no operative death).


Figure 1
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  		Fig 1. Kaplan-Meier overall survival curves of patients with Staphylococcus aureus endocarditis in the global population (diamonds), in the medical group (squares), and in the early surgical group (triangles). The overall survival was significantly lower in the medical group compared with the early surgical group (p = 0.001).

 
Univariate analysis revealed that factors related to overall mortality were age, the comorbidity index, history of renal failure, right-sided IE, congestive heart failure, severe sepsis, and early surgery (Table 3). Multivariate analysis identified the comorbidity index, severe sepsis, and early surgery as predictors of overall mortality (Table 4). Univariate analysis revealed that factors associated with late mortality (excluding in-hospital mortality) were age (p = 0.05), the comorbidity index (p < 0.0001), and neoplasia (p = 0.009). Multivariate analysis identified a comorbidity index >2 (hazard ratio [HR], 3.4; 95% confidence interval [CI], 1.1 to 10; p < 0.03) as the only variable associated with late mortality.


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  		Table 3 Association Between Patient’s Characteristics and Overall Mortality
 

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  		Table 4 Multivariate Analysis: Predictors of In-Hospital and of Overall Mortality
 
Early Surgery
Fifty-five patients (47%) underwent early surgical therapy (Table 2) and were compared with patients who received medical therapy alone during the hospitalization for IE. In-hospital mortality was significantly lower in the early surgical group, at 9 deaths (16.4%), than in the group that received medical therapy alone, where 21 died (34%; p = 0.034). The operative mortality rate of the surgery group was lower during the second week after the diagnosis.

The 36-month rates for actuarial overall survival (Fig 1) and late survival (Fig 2) were significantly higher in the early surgical therapy group (77% ± 6% and 92% ± 6%), than in the medical group (39% ± 7% and 71% ± 8%), respectively. After adjustment of baseline variables related to mortality, early surgery was associated with reduced overall mortality, with a trend (p = 0.1) toward reduction of in-hospital mortality (Table 4). When patients with right-sided IE were excluded, the results of these multivariate analyses were similar, with early surgery associated with lower overall mortality (HR, 0.4l; 95% CI, 0.37 to 0.8; p = 0.02).


Figure 2
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  		Fig 2. Kaplan Meier late survival curves of patients with Staphylococcus aureus endocarditis in the medical group (squares) and in the early surgical group (diamonds). Late survival was significantly lower in the medical group compared with the surgical group (p = 0.03).

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
S aureus is a malignant disease known to be responsible for severe sepsis [7, 8], which has now emerged as a dominant cause of IE [1, 3, 7]. In our studies, it accounted for more than 30% of all endocarditis cases treated over the same period. S aureus IE occurs in a more debilitated clinical setting, including chronic renal failure, hemodialysis, diabetes mellitus, alcoholism, cancer, hematologic malignancy, immunodepression, and drug addiction [1, 28, 29]. Comorbidities were related to mortality in our study. S aureus has been associated with both a higher rate of complications and mortality in IE [5, 22, 30–32]. In-hospital mortality is between 30% and 71% according to various authors [2, 6, 7, 9, 14, 33]. The in-hospital mortality rate of 26% in our studies was related to comorbidities, severe sepsis, congestive heart failure, major neurologic events, and prosthesis IE.

Previous studies have noted a high incidence of neurologic events in patients with S aureus IE [15, 34, 35], and in accordance with this was the high rate of 19% for major neurologic events observed in our studies. Because a cerebral and thoracoabdominal CT scan was not performed in all patients, the true incidence of embolic events in the current study may have been underestimated.

Early congestive heart failure was present in 28% of patients in our cohort. As previously reported in left-sided IE [31, 32, 36], heart failure in our cohort of S aureus IE was found to be a strong prognostic factor associated with higher mortality rates. However, Roder and colleagues [14] reported that late congestive heart failure in S aureus IE was associated with a lower survival rate in the subset of patients who received medical therapy only, whereas early heart failure in the disease process was not related to higher mortality.

We observed a high frequency of severe sepsis, present in 27% of cases. Severe sepsis was the most common factor independently associated with in-hospital mortality and overall mortality in our patients. Sepsis represents a powerful marker of poor prognosis, because severe cases progress to multiorgan dysfunction, disseminated intravascular coagulation, lactic acidosis, and death [7, 8, 37].

Patients with S aureus prosthetic IE are a very high-risk subgroup as confirmed by our study. S aureus infection in prosthetic IE is associated with an increased mortality, as high as 40% and 47.5%, respectively, in two studies including only patients with S aureus prosthetic IE [11, 12].

By using systematic TEE, we were able to visualize vegetation in more than 90% of patients. Vegetation size or mobility assessed early in the course of IE were not indicative of mortality in our study as in two recent studies that included all types of IE [5, 31].

Recent uncontrolled observational studies have suggested that early surgery is more beneficial for patients with IE compared with medical therapy alone [2, 31, 36, 38]. Thus, surgery is currently performed in at least 25% of patients with active IE [2, 5], and in 45% and 50% of patients, respectively, in 2 recent studies [2, 39]. In our study, including only S aureus IE, cardiac surgery was performed in 47% of patients during their initial hospitalization, with an operative mortality of 16.4% (Table 5). Our results suggest that the optimal timing for the surgery is before the 15th day after the diagnosis.


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  		Table 5 Surgical Indications and Timing for Procedures
 
Hoen and colleagues [2] suggested that the decrease in the rate of in-hospital mortality observed in a 10-year interval may have been related to a higher rate of cardiac surgery. In a recent large prospective study including 267 patients with left-sided IE [5], as in other previous series [40–43], early cardiac surgery was not associated with lower in-hospital mortality. However, Vikram and colleagues [39] found that for patients with left-sided complicated IE, surgery was an independent predictor of 6-month survival. Reduced mortality related to surgery was particularly significant among patients with congestive heart failure [39]. In the current study, early surgery in S aureus IE was associated with reduced in hospital mortality in a univariate model with a trend in multivariate analysis toward reduction of in-hospital mortality (p = 0.1). Moreover, early surgery was independently related to reduce overall mortality.

Our study used a validated comorbidity index to analyze the impact of comorbidity on risk of death [20, 31, 39]. This index is related in our cohort independently to in-hospital mortality, overall mortality, and late mortality. Because a poor general condition may constitute a contraindication for cardiac surgery, we found that the comorbidity index was significantly higher in the patients treated medically. However, after adjustment by the comorbidity index and other predictors of outcome, early surgery remained associated with a better outcome. We also performed multivariate analyses excluding patients with right-sided IE. We obtained similar results with early surgery independently related in S aureus left-sided IE to lower overall mortality.

Decisions about surgery are often problematic owing to the lack of evidence from randomized controlled studies. In most cases, thorough consultation between the medical and the surgical teams is necessary to analyze the best strategy. Surgery in our cohort was performed according to conventional guidelines, predominantly in the presence of complications. We cannot rule out the possibility that our patients may have represented a selected cohort from referral centers with more severe illness than the average population with S aureus. Significant differences in baseline characteristics between the surgical group and the medical group were observed. However, these results are important, especially because to date, a randomized trial comparing the surgical and medical strategies has not been performed, and to do seems ethically unacceptable [44]. Therefore, an acceptable method of comparison of the two strategies is to allow for baseline outcome predictors and comorbidities in multivariate analyses, as we performed in the present study.

Prognosis of S aureus IE remains poor, related to the comorbidities, presence of congestive heart failure, severe sepsis, major neurologic events, and prosthetic valve IE. Early surgery is independently associated with reduced hospital and overall mortality compared with nonsurgical therapy and should be considered in selected cases to improve the outcome.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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