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Ann Thorac Surg 2007;83:2081-2086
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Epidemiology and Clinical Outcomes of Infective Endocarditis in Hemodialysis Patients

Desikan Kamalakannan, MBBS, MRCP*, Rama Manohara Pai, MBBS, Leonard B. Johnson, MD, FACP, Julius M. Gardin, MD, FACC, Louis D. Saravolatz, MD, FIDSA

St. John Hospital and Medical Center, Wayne State University School of Medicine, Detroit, Michigan

Accepted for publication February 14, 2007.

* Address correspondence to Dr Kamalakannan, Clinical Cardiology, St. John Hospital and Medical Center, 22151 Moross Rd, Suite 126, Detroit, MI 48236 (Email: desikan.kamalakannan{at}stjohn.org).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Infective endocarditis is one of the most serious complications of bacteremia in patients undergoing chronic hemodialysis and is more frequent than previously recognized. The aim of our study was to describe the clinical characteristics, outcome, and factors predicting mortality of infective endocarditis in hemodialysis patients.

Methods: In this retrospective review, all patients on chronic hemodialysis admitted to a 600-bed urban teaching hospital with infective endocarditis over a 15-year period (1990 to 2004), were identified using discharge codes. Modified Duke criteria were retrospectively applied, and patients fulfilling the criteria for definite endocarditis were included in the study.

Results: Sixty-nine patients on hemodialysis with definite endocarditis were identified. The predominant type of vascular access was double-lumen catheter (66.7%). The mean duration of dialysis was 37 ± 32 months. The predominant organism was Staphylococcus aureus (57.9%), of which 57.5% were methicillin susceptible. The most frequently infected valve was mitral (49.3%), followed by aortic (21.7%) and tricuspid (10.1%) valves. The cardiac and neurologic complication rates were 40.6% and 37.7%, respectively. Fifteen patients underwent valvular heart surgery. The overall in-hospital mortality was 49.3% (34 of 69). More patients who had surgery survived than patients who did not (12 of 15 versus 23 of 54; p = 0.018, odds ratio = 5.39, 95% confidence interval: 1.3 to 17.6). On logistic regression, valve surgery was the only independent factor predicting survival (p = 0.023).

Conclusions: The prognosis of infective endocarditis in hemodialysis patients is poor, with surgery serving as an independent predictor of survival.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Infections are the second leading cause of death in the dialysis population, next only to cardiovascular disease [1]. This patient population is predisposed to infection secondary to transient bacteremia due to repetitive vascular access for hemodialysis through an arteriovenous fistula or indwelling catheter [2–4]. Furthermore, these patients have relatively poor immune function secondary to uremia [5]. The incidence of bacteremia is dependent on the type of vascular access and ranges from 1.6 to 7.7 per 1,000 catheter-days for indwelling catheters and from 0.2 to 0.5 per 1,000 catheter-days for native ateriovenous fistulas [6]. One of the catastrophic complications of blood stream infections is infective endocarditis.

The incidence of infective endocarditis in hemodialysis patients is estimated to be 308/100,000 patient-years [7], which is 50- to 180-fold higher than the 1.7 to 6.2 cases per 100,000 patient-years [8] reported for the general population. The mortality rate among these patients ranges from 30% to 56% at 1 year [7]. A recent study reported 52% in-hospital mortality [9], which is more than twice the mortality for infective endocarditis in the general population. Much of the literature on infective endocarditis in the hemodialysis population comes from case reports and a few retrospective series. We reviewed the risk factors, clinical features, and outcomes of patients on hemodialysis admitted to our institution over 15 years to provide additional information on features that are predictive of improved outcome.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
All patients admitted to St. John Hospital and Medical Center, a 600-bed urban teaching hospital in Detroit, Michigan, with a diagnosis of infective endocarditis who were on chronic hemodialysis were identified from the hospital database for the period January 1, 1990, to December 31, 2004. The medical records were reviewed, and data were collected on underlying conditions, infecting organism, clinical data (including relevant laboratory and echocardiographic information), treatment, and outcomes (survival versus death). Modified Duke criteria were used to confirm the diagnosis of definite infective endocarditis. Patients who did not fulfill the criteria for definite infective endocarditis were excluded. Patients who had acute renal failure requiring hemodialysis after the diagnosis of infective endocarditis were also excluded.

Demographic, clinical, and in-hospital outcome data were extracted from charts of the selected patients. For analyzing the factors predicting survival, the patients were divided into two groups: survivors and nonsurvivors. Statistical analysis was performed using the Statistical Package for Social Services (SPSS) software, version 11.5 (SPSS, Chicago, Illinois). Fisher’s exact test was used for categorical variables, and analysis of variance (ANOVA) was used for continuous variables to identify differences between survivors and nonsurvivors. Logistic regression was used to identify factors predicting survival. A p value of less than 0.05 was considered statistically significant. The retrospective study was approved by the Institutional Review Board and was exempted from individual consent.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Sixty-nine patients on chronic hemodialysis who fulfilled the definite diagnostic criteria for infective endocarditis were identified during the 15-year period. Of these, 31 patients (45%) were male, 19 (27.5%) Caucasian, 48 (69.6%) African American, and 2 (2.9%) were of other ethnicity. The mean age of the cohort was 56 ± 13 years (mean ± SD). The dialysis access was an ateriovenous fistula in 8 patients (11.6%), ateriovenous graft in 15 (21.7%), and percutaneous tunneled catheter in 46 (66.7%). The access sites were internal jugular 20 (29%), subclavian 22 (31.9%), femoral 3 (4.3%), upper limb 23 (33.3%), and lumbar 1 (1.4%). The mean duration of dialysis was 37 ± 32 months. The mean access duration was 10 ± 2 months. A history of hypertension was present in 62 patients (89.9%), diabetes mellitus in 26 (37.7%), coronary artery disease in 17 (24.6%), and congestive heart failure (CHF) in 13 (18.8%). One patient (1.4%) had human immunodeficiency virus infection, and 2 patients (2.9%) were on immunosuppressive medications.

The frequency of intravenous drug abuse, valvular heart disease, and metal prosthetic valves were 8 (11.6%), 7 (10.1%), and 3 (4.3%), respectively. History of invasive procedure within 3 months before admission was recorded only in 6 patients (8.7%), of which 5 (7.2%) were access manipulations and 1 (1.4%) was a dental procedure. The most common presenting symptom was fever, which occurred in 35 patients (50.7%), followed by malaise in 27 (39.1%) and altered mental status in 25 (36.2%). The frequencies of common presenting symptoms are summarized in Table 1. Blood cultures were positive in 68 patients (98.6%). The causative organisms for episodes of infective endocarditis are listed in Table 2. The mean bacteremia duration was 6.6 ± 4.3 days. The mean white blood cell count on admission was 13.5 ± 6 thousand/mm3.


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  		Table 1 Presenting Symptoms of Infective Endocarditis in Hemodialysis Patients
 

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  		Table 2 Causative Organism for Infective Endocarditis in Hemodialysis Patients
 
Transthoracic echocardiogram was performed in 65 patients (94.2%); 36 (55.3%) of these were positive for vegetation. Transesophageal echocardiography was done in 53 patients (76.8%), of whom 49 (92.5%) were positive for vegetation. Among the 29 cases of infective endocarditis with transthoracic echocardiography that failed to reveal vegetations, 25 had transesophageal echocardiography that demonstrated vegetations. The most frequently affected valve was the mitral valve, in 34 patients (49.3%), followed by aortic valve in 15 (21.7%) and tricuspid valve in 7 (10.1%). Multiple valves were affected in 9 patients (13%). No vegetations were identified in 4 patients (5.8%). Of these 4 patients, all had positive blood cultures (Staphylococcus aureus, 2; Streptococcus viridans, 1; and persistent coagulase negative staphylococci, 1) that fulfilled the major criteria, 3 had new valvular regurgitation (major criteria), and 1 had fever, septic emboli, and an Osier’s node (3 minor criteria) to fulfill the diagnostic criteria for infective endocarditis. The mean vegetation size was 1.7 ± 1.1 cm. Valvular regurgitation was reported by echocardiogram in 62 patients (89%). Of these, the regurgitation was mild, moderate, and severe in 23 (33%), 23 (33%), and 16 (23%), respectively.

As for complications of infective endocarditis, septic emboli occurred in 35 patients (50.7%), followed by neurologic complication in 26 (37.7%) and congestive heart failure in 21 (30.4%). The sites of emboli were brain, 24 (34.8%); extremity, 4 (5.8%); lung, 3 (4.3%); vertebra, 3 (4.3%); spleen, 3 (4.3%); joints, 1 (1.4%); and eye, 1 (1.4%). Other complications were heart block in 6 (8.7%), ventricular tachyarrhythmia in 1 (1.4%), valvular abscess in 5 (7.2%), and intracranial hemorrhage in 5 (7.2%). None of the patients in this series had a mycotic aneurysm.

Of the 61 patients (88.4%) who had an indwelling ateriovenous graft or percutaneous tunneled catheter, these were removed in 50 (72.5%). Of the 69 patients in the study, 24 patients had an indication for surgical treatment. Nine of these patients did not undergo surgical treatment. The reasons for not performing surgery were acute embolic stroke with severe neurologic deficit (2 patients), nonrevascularizable ischemic cardiomyopathy with severe left ventricular dysfunction (1 patient), multiorgan failure from overwhelming sepsis (1 patient), severe thrombocytopenia (1 patient, platelet count of 15,000), two prior sternotomies for coronary artery bypass surgery (1 patient), severe baseline dementia (1 patient), meningoencephalitis from sepsis (1 patient), and death from ventricular arrhythmia on the night before planned surgery (1 patient).

Fifteen patients (21.7%) underwent valvular heart surgery (8 mitral, 4 aortic, and 3 mitral and aortic). Of these, 8 patients had metal prosthetic valve, 5 patients had bioprosthetic valves, and 2 patients had valve repair. The indications for surgery in these patients were refractory heart failure (7 of 15), recurrent emboli (4 of 15), root abscess (2 of 15), and persistent infection despite appropriate antibiotics (2 of 15). Postsurgical complications included atrial fibrillation (3 of 15), and junctional bradycardia requiring permanent pacemaker (2 of 15). Three patients died after valvular surgery. The terminal events leading to death in these patients were progressive sepsis with multiorgan failure (2 patients) and bleeding (1 patient, who was a Jehovah’s Witness and hence refused blood transfusion). The mean duration of antibiotic treatment in the 12 of 15 these patients who survived after surgery was 4 ± 1 week (range-2 to 6 weeks, depending on the type of organism). In the medically treated group, 31 patients died. The terminal events leading to death in these patients were progressive sepsis with multiorgan failure (17 patients), stroke (10 patients), heart failure (2 patients), bleeding (1 patient, who had sudden rupture of ateriovenous fistula leading to torrential bleed), and ventricular tachyarrhythmia (1 patient). Overall in-hospital mortality was 49.3% (34 of 69). The average length of stay in the hospital was 21.7 ± 16.5 days.

The data were further analyzed by dividing the patients into two groups, survivors and nonsurvivors. There were no baseline differences between the two groups in demographics, comorbid and predisposing conditions, valve affected, causative organism, and incidence of complication. There were no significant differences in white blood cell count, baseline hemoglobin, duration of bacteremia, or vegetation size. The only significantly different factor between the two groups was in-patient valvular surgery, which was performed in 12 patients (34.3%) in the survivor group compared with 3 patients (8.8%) in the nonsurvivor group (p = 0.018). The data by groups are summarized in Tables 3 and 4. Go


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  		Table 3 Demographic Data of Survivors and Nonsurvivors
 

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  		Table 4 Clinical Characteristics of Survivors and Nonsurvivors
 
On logistic regression analysis, in-patient valvular surgery was the only independent factor predicting in-patient outcome (survival). The variables included for the analysis were low albumin, low ejection fraction, severe valvular regurgitation, age, hypertension, diabetes mellitus, white blood cell count, hemoglobin, vegetation site, organism, coronary artery disease, intracranial hemorrhage, valvular abscess, septic emboli, heart failure, neurologic complication, and whether access was removed.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
This report outlines our retrospective 15-year institutional experience with infective endocarditis in patients receiving long-term hemodialysis. This is the largest series describing the clinical characteristics and outcomes of infective endocarditis in the hemodialysis population. The true incidence of infective endocarditis in hemodialysis patients is at best an underestimate from retrospective studies. It is reported to occur in 6% of patients receiving hemodialysis [10]. The frequency of documented bacteremia is about 0.7 to 1.2 episodes per 100 patient-months among patients on chronic hemodialysis [3, 11, 12]. Of these bacteremic patients, infective endocarditis has been reported to develop in 1% to 12% (3, 4, 11, 13). The relatively low incidence of infective endocarditis in bacteremic patients is probably due to prompt antibiotic treatment and removal of apparently infected vascular catheters in these patients.

The Duke criteria have been well validated for the diagnosis of infective endocarditis, and they have undergone several refinements recently. The modified Duke criteria [14] requires typical micro-organisms from two separate blood cultures, in the absence of a primary focus for the blood culture to be a major criteria. That may pose difficulties in applying the criteria to the hemodialysis population, as most of them will have indwelling vascular access catheters, which serve as a primary focus [9]. However, a microorganism consistent with infective endocarditis from persistently positive blood cultures, defined as at least two positive cultures of blood samples drawn 12 hours apart, or all of three, or the majority of four or more separate cultures of blood (with first and last samples drawn at least 1 hour apart), is also stated as a major criterion; and this was fulfilled in 68 of 69 patients in this study. One patient was culture negative but fulfilled other criteria to be included as definite infective endocarditis.

The incidence of hemodialysis access-related bacteremia exists on a hierarchical continuum from higher to lower as follows: temporary catheter, greater than permanent central venous catheter, greater than ateriovenous grafts, greater than native ateriovenous fistula [15]. This hierarchy is clearly reflected in the frequencies of different access types in our study population (permanent catheter, 66.7%; ateriovenous graft, 21.7%; ateriovenous fistula, 11.6%). Although National Kidney Foundation clinical guidelines recommend native ateriovenous fistula as the preferred vascular access [16], this is not always possible, and it is reported that 28% of patients have catheters as the primary vascular access for hemodialysis [17], exposing them to a higher risk of bacteremia.

Staphylococcus aureus has surpassed Streptococcus viridans as the most common cause of infective endocarditis in the general population, accounting for 32% and 18%, respectivley, of the 1,779 patients from the International Collaboration on Endocarditis Perspective Cohort Study [18]. Coagulase negative staphylococci and enterococci accounted for 11% each in the same study. Previous studies on infective endocarditis on hemodialysis patients have reported S aureus as the most common causative organism, with frequencies ranging from 40% to 80%, of which 5% to 23% were methicillin-resistant S aureus (MRSA) [9, 10, 19, 20]. This study confirms S aureus as the major causative organism accounting for 57.9% of cases (40 of 69) in this population. Of these, methicillin-susceptible S aureus (MSSA) accounted for 33.3% and MRSA for 24.6%. The higher rates of methicillin resistance in this population likely reflect increasing national trends of resistance in isolates of S aureus, both in the community and hospital settings [21]. Furthermore, increased healthcare contact of this population, due to comorbid conditions, predisposes them to MRSA infection. It has been reported that 30% of S aureus blood stream isolates in the United States are methicillin resistant [22], and there is increasing frequency of MRSA among both nosocomial and dialysis-associated S aureus bacteremias [23, 24].

Our data are consistent with previous reports in that left-sided endocarditis is about twice as common as right-sided endocarditis in this population, and the mitral valve more frequently affected than the aortic valve [9, 10, 19, 20]. It is believed that thickening of the aortic and mitral valves, which are common in end-stage renal disease, may lead to increased susceptibility to infective endocarditis due to alterations in laminar flow [25]. Mitral annular calcification, which is also common in end-stage renal disease patients, has been shown to increase susceptibility to infective endocarditis [26].

The cardiac (40.6%) and neurologic (37.7%) complication rates in our study population are similar to that of the general population, which is reported to be one third to one half and 25% to 35%, respectively [27–29]. The high incidence of emboli (50.7%), especially cerebral (34.8%), in our study population is likely due to predominant left-sided endocarditis, especially mitral valve, which has been shown to be associated with increased risk of embolization [30, 31].

All patients were started on empiric antibiotic therapy initially, which was then changed according to in-vitro susceptibility testing. Vancomycin was used as the empiric antibiotic in 68 of 69 patients along with an aminoglycoside in 38 of 69 patients. Fifteen patients (21.7%) underwent valvular heart surgery during the hospitalization. This is consistent with reports from the general population suggesting that 25% to 30% of patients with infective endocarditis require surgery during the acute phase of infection [32–35].

The in-hospital mortality rate was 49.3% in our study, which is comparable with the 52% in a recent study [9]. Another study reported a 47% 60-day mortality [10]. This is twice that of the overall mortality of 20% to 25% reported in the general population in the antibiotic era [36]. This may be because of the higher incidence of S aureus infection and the presence of comorbid conditions. In our study, the patients who underwent surgery had a higher survival rate than those who did not have surgery (12 of 15 versus 23 of 54, p = 0.018, odds ratio = 5.39, 95% confidence interval: 1.3 to 17.6). Vikram and colleagues [37] have previously shown that valve surgery is independently associated with reduced mortality in left-sided native valve endocarditis even after adjustment for baseline variables. On logistic regression, valve surgery was the only independent predictor for survival (p = 0.023). Given that most of the patients in our series had left-sided endocarditis, this result is not entirely surprising.

The main limitation of our study was its retrospective nature. Hence, selection bias for valvular surgery cannot be excluded, although there were no differences in the demographic and clinical variables between survivors and nonsurvivor. Another limitation is the lack of long-term follow-up of in-hospital survivors.

In conclusion, our study suggests that the prognosis for infective endocarditis in hemodialysis patients is poor, with a high mortality rate, and it provides further data to support the role of valve surgery in select patients with infective endocarditis.[13]


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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