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Contemporary Epidemiology and Prognosis of Health Care–Associated Infective Endocarditis

  1. Nuria Fernández-Hidalgo1,
  2. Benito Almirante1,
  3. Pilar Tornos2,
  4. Carles Pigrau1,
  5. Antonia Sambola2,
  6. Albert Igual3, and
  7. Albert Pahissa1
  1. 1Departments of Infectious Diseases, Hospital Universitari Vall d'Hebron, Universitat Autonòma de Barcelona, Barcelona, Spain
  2. 2Departments of Cardiology, Hospital Universitari Vall d'Hebron, Universitat Autonòma de Barcelona, Barcelona, Spain
  3. 3Cardiac Surgery, Hospital Universitari Vall d'Hebron, Universitat Autonòma de Barcelona, Barcelona, Spain
  1. Reprints or correspondence: Dr. Nuria Fernández-Hidalgo, Infectious Diseases Dept., Hospital Universitari Vall d'Hebron, Passeig de la Vall d'Hebron 119–129, 08035 Barcelona, Spain (nufernan{at}gmail.com).
 
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Abstract

Background. The aim of this study was to describe the characteristics of health care-associated infective endocarditis (HAIE) and to establish the risk factors for mortality.

Methods. We conducted a prospective, observational cohort study. HAIE was defined according to the following conditions: (1) symptom onset >48 h after hospitalization or within 6 months after hospital discharge; or (2) ambulatory manipulations causing endocarditis.

Results. Eighty-three episodes of HAIE (accounting for 28.4% of all cases of endocarditis) were diagnosed. Compared with patients with community-acquired endocarditis, patients with HAIE were older (median age ± standard deviation, 65.3±16.4 years vs. 57.8±17.0 years; P=.001), were in poorer health before disease onset (Charlson index, 2.5±2.3 vs. 1.7±2.1; P=.006), had more staphylococcal (55.4% vs. 28.3% of cases) and enterococcal infections (22.9% vs. 7.7% of cases; P<.005), underwent fewer surgeries (22.9% vs. 45.9% of cases; P<.005), and experienced a higher rate of in-hospital (45.8% vs. 22.0%) and 1-year mortality (59.5% vs. 29.6%; P<.005). In the HAIE cohort, independent predictors of in-hospital death were stroke (odds ratio [OR], 8.95; 95% confidence interval [CI], 2.04–39.31; P=.004), congestive heart failure (OR, 5.48; 95% CI, 1.77–17.03; P=.003), surgery indicated but not performed (OR, 3.74; 95% CI, 1.22–11.45; P=.021), and enterococcal infection (OR, 0.18; 95% CI, 0.04–0.78; P=.022). Independent predictors of 1-year mortality were surgery indicated but not performed (OR, 7.81; 95% CI, 2.06–29.67; P=.003), acute renal failure (OR, 7.18; 95% CI, 1.32–39.18; P=.023), and enterococcal infection (OR, 0.18; 95% CI, 0.04–0.81; P=.026). For the series overall (292 episodes), HAIE was an independent predictor of in-hospital (OR, 2.83; 95% CI, 1.34–5.98; P=.007) and 1-year mortality (OR, 2.59; 95% CI, 1.25–5.39; P=.011).

Conclusions. HAIE is an important health problem associated with considerable mortality. New strategies to prevent HAIE should be assessed.

Despite improvements in the diagnosis and surgical treatment of infective endocarditis (IE), this disease continues to be associated with high rates of morbidity and mortality [1–3]. This is a consequence of changes in the epidemiology of IE that have been observed during the past few years [4]. The classic concept of viridans group streptococcal IE involving a rheumatic valve resulting from a dental infection or manipulation has now almost disappeared in developed countries [5, 6]. At the same time, the increasing number of patients with a prosthetic valve or long-term central venous catheter, both of which are well-recognized risk factors for the development of IE, has led to an increasing rate of health care-associated IE (HAIE) [4]. In this scenario, most of the microorganisms isolated are Staphylococcus species [7].

The few existing studies that describe the characteristics of nosocomial IE have reported rates of 7.7%–21.5% of all IE cases [8–10]. However, these studies underestimate the true magnitude of the problem. Patients who are highly dependent on the health care system, such as those who are receiving ambulatory hemodialysis treatment, and who acquire IE secondary to catheter-related bacteremia are often erroneously classified as having community-acquired IE (CAIE), rather than nosohusial IE (i.e., HAIE).

The aims of this study were as follows: (1) to describe the epidemiology, clinical characteristics, and prognosis of HAIE; (2) to compare the characteristics of HAIE with those CAIE; and (3) to establish the independent risk factors for HAIE-related in-hospital and 1-year mortality.

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Patients and Methods

Patients and settings. This prospective, observational cohort study was performed at Vall d'Hebron Hospital, which is a 1000-bed teaching hospital in Barcelona, Spain, that includes all major medical and surgical departments and a referral center for cardiac surgery. All consecutive adult patients (⩾18 years of age) with a diagnosis of definite or possible IE [11] who were treated at our center from January 2000 through December 2007 were enrolled in the study. Patients were identified from our Infectious Diseases Department database, the Microbiology Department blood culture registry, and the echocardiography laboratory. All interventions were performed by the same medical staff team during the entire study period.

Patients who were referred for surgery from another center at completion of antimicrobial treatment, patients with noninvasive endocarditis, and patients with pacemaker infection and no evidence of endocardial involvement were excluded from the study.

Data collection. Demographic, clinical, diagnostic, treatment, and follow-up data were obtained by detailed chart abstraction with use of standardized reporting forms and were entered into a Microsoft Access 2000 database created specifically for the purpose of this study.

Definitions. IE was defined as HAIE according to the following criteria: (1) onset of symptoms >48 h after hospitalization with no evidence of IE at the time of hospital admission or within 6 months after hospital discharge [9] (designated nosocomial IE) or (2) diagnostic or therapeutic manipulations in the ambulatory setting within 6 months before symptom onset (designated nosohusial IE), including long-term central venous catheter use; autologous or prosthetic arteriovenous fistula for hemodialysis; invasive intravascular techniques (cardiac catheterization, pacemaker insertion, and other intravascular devices); urologic, gynecologic, or digestive procedures; and acupuncture.

Catheter-related bacteremia is defined elsewhere [12]. Long-term central venous catheter-related bacteremia was diagnosed by means of simultaneous quantitative blood cultures.

The Charlson index [13] at hospital admission was used to stratify patients with respect to overall comorbidity. The presence of diabetes mellitus, hemodialysis, neoplasm, or any heart disease at hospital admission was recorded.

The EuroSCORE [14] was calculated for all patients with an indication for surgery. Cardiac surgery was indicated according to the American Heart Association guidelines [15]. For patients with an indication for surgery but for whom surgery was not performed, the main reason for this decision was recorded. Only cardiac surgery performed during hospitalization was taken into consideration.

IE complications were defined as the development of any of the following conditions: (1) persistent fever (present 7 days after the start of treatment), (2) congestive heart failure (new condition or worsening of a known previous condition), (3) intracardiac abscess (diagnosed by echocardiography or during surgery), (4) new conduction abnormality, (5) stroke, (6) systemic embolism other than stroke, and (7) acute renal failure (defined as a 50% increase in the baseline creatinine concentration).

In-hospital mortality was defined as death from any cause during hospitalization. Related mortality was defined as death secondary to sepsis or complications of IE, as described above. The 1-year cumulative mortality was defined as death from any cause within 1 year after hospital discharge.

Patients were evaluated in the outpatient clinic on days 30, 90, and 365 after hospital discharge. Blood samples were obtained for culture 2 days after completion of antimicrobial treatment and 30 and 90 days after hospital discharge. Echocardiographic examination was performed at the end of treatment and at least once again during the first year of follow-up.

Statistical analysis. Quantitative variables are reported as means and standard deviations, median values and ranges, or median values and interquartile ranges. The χ2 test (or Fisher's exact test, when appropriate) was used to compare the distribution of categorical variables, and the Student's t test was used for continuous variables. Differences were considered to be statistically significant at a P value of <.05. For the multivariate analysis, the effects on in-hospital and 1-year mortality of variables that were determined to be clinically and statistically significant in the univariate analysis (P<.1) were analyzed by logistic regression. Only patients with at least 1 year of follow-up were included in the 1-year mortality analysis. Statistical analyses were performed with Microsoft SPSS-PC+, version 12.0 (SPSS).

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Results

Two hundred ninety-two episodes of IE in 289 patients were treated at our hospital during the study period. Eighty-three cases in 83 patients (28.4% of all cases of IE) were classified as HAIE. Sixty-seven cases (80.7%) were nosocomial infections, and 16 cases (19.3%) were nosohusial infections. Seventy-one patients (85.5%) were classified as presenting with definite IE according to the modified Duke criteria [11].

Source of infection. It was possible to establish the source of infection (other than hospital admission within the previous 6 months) in 63 (75.9%) of the 83 cases of HAIE. The most important sources of infection were catheter-related bacteremia (33 cases; 39.8%), cardiac surgery (10 cases; 12.0%), and arteriovenous fistula for hemodialysis (8 cases; 9.6%) (table 1). In detail, patients who underwent urologic and colonoscopic manipulations (most of whom had enterococcal IE) developed bacteremia <12 h after the procedure. For patients with cardiac catheterization and pacemaker implantation (most of whom had IE due to coagulase-negative staphylococci), the onset of symptoms was <1 month after the procedure (which was always described as difficult). In the case that was associated with acupuncture, the patient developed local signs of infection on the skin 3 weeks before the onset of other symptoms. Finally, 1 patient presented with early infection of the ostium of the gastrostomy tube and cultures that were persistently positive for Candida albicans; this patient developed IE due to the same microorganism 2 weeks later.

Table 1
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Table 1

Source of infection in 83 cases of health care—associated infective endocarditis.

In table 2, the characteristics of patients with HAIE who had a known source of infection are compared with those of patients for whom a hospital admission within the previous 6 months was the only risk factor for IE. Detailed data on cases of nosohusial HAIE are shown in table 3.

Table 2
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Table 2

Comparison between 63 patients with health care—associated infective endocarditis (HAIE) with a known source of infection and 20 patients with HAIE whose only risk factor for infective endocarditis was hospital admission within the previous 6 months.

Table 3
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Table 3

Characteristics of 16 patients with cases of nosohusial infective endocarditis.

Predisposing cardiac factors. Forty (48.2%) of the patients with HAIE had a cardiac factor that predisposed them for IE. Of these 40 patients, 24 (28.9% of all patients with HAIE) had a prosthetic valve; 2 of these 24 patients had IE episodes that involved both native and prosthetic valves. Sixteen (19.3%) of 83 patients had a predisposing factor other than a prosthetic valve, including 14 patients with valvular disease and 2 patients with congenital heart disease.

Etiology. Staphylococcus aureus was the most frequently isolated microorganism (28 cases; 33.7%), followed by Enterococcus species (19 cases; 22.9%) and coagulase-negative staphylococci (18 cases; 21.7%) (table 4).

Table 4
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Table 4

Microorganisms causing health care—associated infective endocarditis.

Cardiac involvement. The mitral valve alone was affected in 36 (43.4%) of 83 cases, the aortic valve alone was affected in 26 (31.3%), 2 valves were affected in 10 (12.0%), an unknown number of valves were affected in 5 (6.0%), the tricuspid valve alone was affected in 3 (3.6%), a pacemaker lead and the endocardial wall in 2 (2.4%), and the pulmonary valve and pacemaker lead in 1 (1.2%).

Surgery. Nineteen (22.9%) of 83 patients underwent surgery during the active phase of infection. However, 29 patients with an indication for surgery did not undergo valve replacement. Four of these patients died before surgery could be performed, and in the 25 remaining patients, surgery was rejected because of the high associated risk. The median EuroSCORE for these high-risk patients was 13 points (interquartile range, 9.5–15.5; range, 5–21). Overall, 20 of 29 patients died during hospitalization (69.0%); the 1-year cumulative mortality was 85.2%.

Outcome. Seventy-one patients (85.5%) experienced at least 1 complication during hospitalization. Of these patients, 39 (47.0% of all patients with HAIE) experienced congestive heart failure, 23 (27.7%) experienced systemic embolism other than stroke, 19 (22.9%) experienced acute renal failure, 16 (19.3%) experienced stroke, 13 (15.7%) experienced persistent fever, 9 (10.8%) experienced a new conduction abnormality episode, and 8 (9.6%) experienced intracardiac abscess. Thirty-nine patients (47.0%) experienced >1 complication.

Thirty-eight patients (45.8%) died during hospitalization. Of these, 32 (84.2%) experienced HAIE-related in-hospital deaths, including 15 deaths from congestive heart failure, 7 from stroke, 4 from septic shock (all in patients with episodes of HAIE due to S. aureus), 2 immediately after surgery, 1 from multiorgan failure, 1 during valve replacement surgery, 1 from pulmonary thromboembolism, and 1 sudden death (table 5). The 1-year mortality among patients with 1 year of follow-up was 59.5% (44 patients died). In addition, there were 6 in-hospital deaths that were not related to HAIE.

Table 5
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Table 5

Characteristics of 32 patients with health care—associated infective endocarditis (HAIE) who died during hospitalization.

Patients who died during hospitalization included 16 (57.1%) of 28 patients with HAIE due to S. aureus (7 [87.5%] of 8 patients with infection due to methicillin-resistant S. aureus and 9 [45%] of 20 patients with infection due to methicillin-susceptible S. aureus), 5 (55.6%) of 9 patients with HAIE due to Streptococcus viridans, 8 (44.4%) of 18 patients with HAIE due to coagulase-negative staphylococci, and 5 (26.3%) of 19 with HAIE due to Enterococcus species.

Comparison between HAIE and CAIE. In table 6, the characteristics of patients with HAIE are compared with the characteristics of patients with IE that was not health care related. Most cases of HAIE involved mitral valves and occurred among elderly individuals in poor general condition; men and women were equally affected. Compared with patients who had CAIE, patients with HAIE were transferred less often from another facility; had more infections that were due to S. aureus, Enterococcus species, and coagulase-negative staphylococci; underwent surgery during hospitalization less often (although with a higher median presurgery risk, as determined by EuroSCORE); and had higher in-hospital and 1-year mortality.

Table 6
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Table 6

Univariate comparison between patients with health care—associated infective endocarditis (HAIE) and patients with community-acquired infective endocarditis (CAIE) episodes.

Predictors of outcome. In the univariate analysis, the factors associated with in-hospital death in patients with HAIE were diabetes mellitus, enterococcal infection, vegetation diameter, pulmonary arterial blood pressure, indication for surgery, surgery indicated but not performed (SINP), development of any complication, congestive heart failure, stroke, acute renal failure, and duration of intensive care unit stay (table 7). For the multivariate logistic regression analysis, we included only stroke, congestive heart failure, SINP, and enterococcal infection, which were the most clinically significant variables in the analysis. These variables remained independently associated with in-hospital mortality.

Table 7
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Table 7

Association between characteristics of patients with health care—associated infective endocarditis (HAIE) and in-hospital death.

Similarly, factors associated with death at 1 year in patients with HAIE were Charlson index, enterococcal infection, moderate-to-severe aortic regurgitation, elevated pulmonary arterial blood pressure, indication for surgery, SINP, development of any complication, congestive heart failure, stroke, and acute renal failure (table 8). Enterococcal infection, SINP, congestive heart failure, stroke, and acute renal failure were included in the multivariate logistic regression analysis, in which SINP, acute renal failure, and enterococal infection remained independently associated with 1-year mortality. Finally, when the whole series was examined with use of multivariate analysis, HAIE was an independent risk factor for both in-hospital (OR, 2.83; 95% CI, 1.34–5.98; P=.007) and 1-year mortality (OR, 2.59; 95% CI, 1.25–5.39; P=.011).

Table 8
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Table 8

Association between characteristics of patients with health care—associated infective endocarditis (HAIE) and 1-year mortality.

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Discussion

Previous studies have reported that nosocomial IE accounts for up to 21.5% of all IE cases [8–10]. However, these studies have some limitations, including the use of retrospective, rather than contemporary, series [8,9] and the failure to include nosohusial episodes [8–10]. Our study describes the epidemiology and prognosis of HAIE (including cases of nosohusial IE) in a contemporary, prospective cohort of patients. With use of this broader definition, we found that HAIE represented almost 30% of all episodes of IE, reflecting current changes in the epidemiology of this disease in developed countries. The fact that this study was conducted in a single hospital by the same team of medical personnel throughout the study period conferred homogeneity on the medical decisions and interventions and, therefore, conferred homgeneity on the results.

Advances in diagnostic and therapeutic techniques have improved the quality of life of many patients, particularly by avoiding hospitalization for certain procedures. However, patients who are not hospitalized are exposed to the same risk of bacteremia as patients who are hospitalized, as was well demonstrated in most of the nosohusial episodes in our series. We did not classify cases of IE that occurred after oral manipulations as cases of nosohusial infection, because although we treated 5 episodes of IE that began within 2 weeks after dental extraction, it is difficult to know whether these cases were, in fact, attributable to the dental extraction or were secondary to routine daily activities. Moreover, the characteristics of this small subgroup of patients were similar to the characteristics of those in the CAIE group, with whom they were classified.

On the basis of incidence and etiology data from patients with IE that manifested during the 6-month period after hospital discharge, Ben-Ami et al. [9] suggested that the definition of HAIE should be broadened to include these episodes. Previous analyses of our series showed that patients with HAIE defined according to this broadened definition were similar to patients with HAIE defined according to the most conservative definition (i.e., only including cases of IE that occurred 1–2 months after hospital discharge), even with respect to etiology and mortality, and were significantly different from patients with CAIE (data not shown). On the basis of these results, we decided to adopt the classification proposed by Ben-Ami et al. [9], although the link between some cases of viridans group IE and health care could be questioned. Thus, further studies should validate our definition of HAIE.

The source of infection was attributed to manipulation of a vascular access in 41 cases. This illustrates that catheterization is an important cause of HAIE and explains the high rate of infection due to staphylococci and enterococci. These findings are not surprising, because the risk of endocarditis associated with catheter-related bacteremia due to S. aureus and Enterococcus species is well recognized [16, 17]. Nevertheless, these data are a cause for concern and indicate the need to improve the care provided to patients with all types of vascular accesses, because HAIE is potentially avoidable and has considerable associated mortality [18].

There were 4 episodes of HAIE secondary to persistent bacteremia in mediastinitis after cardiac surgery (3 due to S. aureus and 1 due to Staphylococcus epidermidis). Early debridement of any deep wound infection would potentially avoid persistent bacteremia and, therefore, decrease the risk of endocarditis [19].

There were fewer patients who were transferred from another center in the HAIE group than there were in the CAIE group. This could be explained by the fact that a tertiary teaching center performs a great number of ambulatory procedures (e.g., hemodialysis and chemotherapy infusion) that place patients at risk for bacteremia.

The microorganism that was isolated most often in both the HAIE group and the CAIE group was Staphylococcus species, as has been described by other authors [7], which indicates the changing epidemiology of this disease. There was a higher rate of MRSA infection in the HAIE group than in the CAIE group, as expected. Moreover, most patients with HAIE due to MRSA died, a fact that indicates the difficulty of treating these cases. In our study, enterococcal IE was associated with a lower rate of in-hospital and 1-year mortality. This is not surprising, because a previous study has demonstrated that enterococcal IE is associated with a lower risk of embolism and lower mortality than staphylococcal IE [20].

HAIE affects elderly men and women in poor general condition. This comorbid status leads to close contact with the health system and a subsequent increased risk of acquiring bacteremia and IE; it also influences the attitude of physicians attending these patients. It is worth mentioning that 29 (60.4%) of 48 patients with HAIE who had an indication for surgery did not undergo valve replacement during hospitalization because of a high surgical risk, and this was an independent risk factor for in-hospital and 1-year mortality. Moreover, mortality was higher in the HAIE group than in the CAIE group. Although there were no differences between the HAIE and CAIE groups with respect to the incidence or type of complications (indicating that IE is a severe disease regardless of the source of acquisition), in the multivariate analysis of the whole series (292 episodes), HAIE was an independent risk factor for in-hospital and 1-year mortality.

Only 26 (31.3%) of our 83 patients with HAIE were potential candidates for antimicrobial prophylaxis (24 patients with prosthetic valve endocarditis and 2 patients with congenital heart disease). Nevertheless, only a small or negligible percentage of IE episodes could have been prevented by administration of antimicrobial prophylaxis. Therefore, routine antimicrobial prophylaxis administered before most invasive procedures is no longer considered to be appropriate [21]. The maintenance of proper aseptic measures before and during invasive procedures is probably much more important than a generalized use of prophylactic antimicrobials.

This study has several limitations. It is subject to the referral bias of a large tertiary teaching center. The high rate of HAIE in the series implied a high rate of S. aureus infection. Extrapolation of the results to other community hospitals should be done with caution. Detection of IE in hospitalized patients requires a high index of suspicion and routine practice of transesophageal echocardiography in patients with bacteremia (in particular, in patients with infections caused by gram-positive microorganisms) [16,22]. Taking into account the high mortality associated with HAIE, it is possible that some HAIE episodes that occurred during the study period may not have been diagnosed. Finally, some episodes of viridans group IE could have been unintentionally misclassified.

In conclusion, this study reveals that HAIE is an important health problem that affects elderly men and women in poor general condition equally. The infection is mainly caused by staphylococci and enterococci and is associated with considerable in-hospital and 1-year mortality. Maximizing prophylactic measures during the insertion and manipulation of venous catheters and, in general, maintaining aseptic measures before and during any invasive procedures could reduce the rate of this devastating infection.

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Acknowledgments

We thank Celine Cavallo.

Financial support. The Spanish Network for Research in Infectious Diseases (REIPI RD06/0008, to B.A., C.P., and A.P.).

Potential conflicts of interest. All authors: no conflicts.

  • Received April 16, 2008.
  • Accepted July 23, 2008.
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  1. Clin Infect Dis. (2008) 47 (10): 1287-1297. doi: 10.1086/592576
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