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Ann Thorac Surg 2006;81:1284-1290
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Risk Factors of Prosthetic Valve Endocarditis: A Case-Control Study

M. Carmen Fariñas, MD, PhD a , * , Alberto Pérez-Vázquez, MD, PhD d , Concepción Fariñas-Álvarez, MD, PhD c , J. Daniel García-Palomo, MD, PhD a , José M. Bernal, MD, PhD b , José M. Revuelta, MD, PhD b , Jesús González-Macías, MD, PhD a

a Infectious Diseases Unit, Department of Internal Medicine, Hospital Universitario Marqués de Valdecilla, Universidad de Cantabria, Santander, Spain
b Infectious Diseases Unit, Department of Cardiovascular Surgery, Hospital Universitario Marqués de Valdecilla, Universidad de Cantabria, Santander, Spain
c Division of Preventive Medicine, Hospital Sierrallana, Torrelavega, Cantabria, Spain
d Medicina Familiar y Comunitaria, Centro de Salud Caldas de Reyes, Pontevedra, Spain

Accepted for publication August 15, 2005.

* Address correspondence to Dr Fariñas, Infectious Diseases Unit, Department of Internal Medicine, Hospital Universitario Marqués de Valdecilla, Avda. Valdecilla s/n, 39008 Santander, Spain (Email: mirfac{at}humv.es; farinasc{at}unican.es).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Prosthetic valve endocarditis is an important cause of the morbidity and mortality associated with heart valve replacement surgery. The objective of this study was to assess risk factors of prosthetic valve endocarditis related to patients, perioperative events, and postoperative complications.

METHODS: This was a retrospective case-control study conducted in a tertiary care hospital in Santander, Spain, from January 1986 to January 1998. Cases were patients with "definite" and "possible" infective endocarditis defined according to the Durack criteria. Controls were patients undergoing prosthetic valve replacement who at the time of the study had not developed infective endocarditis. Information was abstracted from medical records. Cases and controls (1:2) were matched by sex, age at operation (± 5 years), surgery of one or more valves in the same anatomic position, and date of operation (± 6 months).

RESULTS: There were 81 cases and 162 controls. In the multivariate analysis, risk factors significantly associated with prosthetic valve endocarditis were functional class III or IV (New York Heart Association), alcohol consumption, prior history of endocarditis, fever in the intensive care unit, and gastrointestinal bleeding. Functional class III or IV and complications of the surgical wound were independent predictors of early infective endocarditis, whereas fever in the intensive care unit and gastrointestinal bleeding were predictors of prosthetic valve endocarditis late after operation.

CONCLUSIONS: Patients with prosthetic valve endocarditis differ from people without infective endocarditis with regard to intrinsic and postoperative risk factors but not regarding perioperative-related variables.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Prosthetic valve endocarditis (PVE) is a serious complication of cardiac valve replacement. The risk of infection of the prosthetic material shows a bimodal distribution pattern, with an early peak during the first 6 weeks after operation [1] and a likelihood of approximately 3% during the first postoperative year. The incidence of late PVE ranges between 0.1 and 2.3 per 100 patient-years [1–3]. The only treatment of established PVE infection is intravenous antimicrobial therapy, although most patients require surgical removal and replacement of the infected prosthesis in addition to antibiotic therapy. Many patients with "cured" PVE infection will eventually required reoperation. In-hospital mortality rates of reoperations for PVE have been 22% to 46% even at centers with extensive experience in valve surgery [4, 5]. Thus, there is a need to identify patients at risk of PVE and institute appropriate preventive measures.

Since the early 1970s, cardiac valve replacement operations have been performed at our institution. To assess the current status of determinants of the occurrence of PVE, we reviewed the case histories of patients who underwent cardiac valve replacement operations from 1986 to 1998. Intrinsic and extrinsic risk factors of PVE were evaluated by univariate and multivariate analyses.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
The study was conducted at a 1,200-bed community and teaching hospital. The hospital has a department of cardiovascular surgery, a service of cardiology, and a unit of infectious diseases, and has been a reference center of cardiovascular surgery for other hospitals in the country.

A retrospective case-control study was designed. The study was approved by the Institutional Review Board. Given the retrospective design of the study and that information was gathered from medical records, informed consent was not obtained. During the chart review phase, we considered the "definite" and "possible" diagnostic categories of infective endocarditis defined by Durack and colleagues [6] when establishing a diagnosis of PVE. All patients with PVE admitted from January 1986 to January 1998 were included. Because of the large latency period between surgical procedure and development of PVE, all patients undergoing cardiac valve replacement operations since 1974 were eligible. Although some patients had more than one episode of PVE, each infectious episode was considered a new case owing to potential modification of risk factors. Early infections were defined as those in which clinical symptoms or signs were recorded during the first 60 days after surgery. Patients who did not meet Durack criteria [6] were excluded, as were patients undergoing heart valve surgery at other institutions but admitted to our hospital for the treatment of PVE. Controls were patients undergoing prosthetic valve replacement who at the time of the study had not developed PVE. Patients who died during hospitalization for valve replacement surgery were excluded to rule out the possibility of undiagnosed infection of the prosthetic material as the cause of death.

Cases and controls (1:2) were matched by sex, age at operation (± 5 years), surgery of one or more valves in the same anatomic position, and date of operation (± 6 months selecting the closest date).

Medical records of patients were reviewed for intrinsic and extrinsic risk factors. Categorical intrinsic and extrinsic variables were categorized as present vs absent. Patient's related factors included the following: age; sex; place of origin (our community or reference from other communities); preoperative functional class according to the New York Heart Association (NYHA) classification; hemodynamic examination results; atrial fibrillation; previous endocarditis with native or prosthetic valves; previous valve surgery; history of diabetes mellitus, chronic obstructive pulmonary disease (COPD), neoplasm, acute cerebrovascular events, liver disease, immunosuppression, prostatic syndrome, gastrectomy, and sternotomy; obesity; alcohol consumption (>80 g daily in men and >30 g daily in women); current smoking; intravenous drug use; and preoperative analytic data. Extrinsic risk factors were as follows: date of hospital admission; date of surgery; type of operation (urgent or elective); prostheses characteristics (size, position, and type); duration of anesthesia; time of cardiopulmonary bypass; time of cold ischemia; intraoperative events; antibiotic prophylaxis; length of stay in the intensive care unit (ICU); need of mechanical ventilation; packed red blood cell transfusion; fever during ICU stay (temperature ≥ 38°C for 48 hours or more); parenteral nutrition; reoperation; gastrointestinal bleeding; wound complications; and invasive diagnostic and therapeutic maneuvers, in particular insertion of a nasogastric tube, urinary catheter, and arterial and venous lines.

The sample size was estimated according to an average frequency of exposure to the risk factors of 30% to obtain an odds ratio (OR) of 2.3 with an alpha level of 0.05 and a beta value of 0.2 (for 80% power). The sample size needed for the study was 75 cases. Matched odds ratios (ORs) estimates and their 95 percent confidence intervals (CIs) were calculated. Univariate and multivariate statistical analysis was carried out using EGRET statistical software package [7] and logXact for Windows (logistic regression analysis program with exact inference). Variables were entered into a stepwise backward multiple conditional logistic regression model. The level of significance to remain in the model was 0.25. The model was manually corrected with those variables identified as risk factors for PVE, which introduced substantial changes in weight of the logistic parameters [8]. Statistical significance was set at p less than 0.05. Results are expressed as matched crude and adjusted ORs with 95% CIs.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
During the study period, 93 episodes of PVE were diagnosed (76 patients had one episode, 7 patients had two episodes, and only 1 patient had three episodes). Twelve of these episodes occurred in patients who had undergone prosthetic valve replacement operations at other centers, and given that information regarding perioperative risk factors was not available, these 12 cases were excluded. The study population consisted of 81 cases and 162 controls. The classification of cases according to Durack criteria [6] is shown in Figure 1. In the group of patients with PVE, there were 61 men and 20 women with a mean age of 49 years (95% CI: 46 to 52). The mean age of controls was 50 years (95% CI: 48 to 52). Location of infected prosthesis included aortic in 45 cases, mitral in 20, and mitroaortic in 16. Of the 81 cases of an infected prosthetic valve, there were 17 cases (21%) of early PVE and 64 cases (79%) of late PVE.


Figure 1
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  		Fig 1. Classification of cases according to confirmation by surgical findings and Durack criteria. (PVE = prosthetic valve endocarditis.)

 
In relation to qualitative intrinsic risk factors, independent variables significantly associated with an increased risk of PVE were preoperative NYHA functional class III or IV (adjusted OR = 3.01; 95% CI: 1.37 to 6.60), alcohol consumption (adjusted OR = 2.62; 95% CI: 1.22 to 5.59), and previous endocarditis (adjusted OR = 2.95; 95% CI: 1.07 to 8.15; Table 1). None of the perioperative variables was selected as a significant predictor in the logistic regression model. However, development of fever during stay in the ICU (OR = 19.21; adjusted 95% CI: 5.18 to 71.21) and postoperative gastrointestinal bleeding (OR = 12.28; adjusted 95% CI: 1.45 to 103.9) were significantly associated with an increased risk for PVE (Table 2). On the other hand, functional class III or IV (OR = 12.29) and complications of the surgical wound (OR = 7.60) were significant risk factors for early PVE (Table 3). Finally, fever during ICU stay (OR = 6.13; 95% CI: 1.89 to 18.98) and gastrointestinal bleeding (OR = 5.31; 95% CI: 1.28 to 21.97) were significantly associated with an increased risk of late PVE (Table 4).


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  		Table 1. Qualitative Intrinsic Risk Factors for the Development of Prosthetic Valve Endocarditis
 

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  		Table 2. Perioperative and Postoperative Extrinsic Risk Factors of Prosthetic Valve Endocarditis
 

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  		Table 3. Risk Factors of Early (< 6 Weeks) Prosthetic Valve Endocarditis
 

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  		Table 4. Risk Factors of Late Prosthetic Valve Endocarditis
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
In the emerging years of heart valve replacement surgery, the incidence of bacterial endocarditis after cardiac operations was as high as 10% [9]. Although during the past 40 years, improvements in the characteristics of the prostheses, surgical technique, knowledge of the mechanisms of infection and antibiotic prophylaxis, among others, have been associated with a decrease in infective endocarditis, PVE continues to be a serious complication of cardiac valve replacement with a high mortality rate.

In a review of our experience in the last 12 years [10], it was found that preoperative NYHA functional class was associated with a greater risk of PVE in general as well as early PVE. Although these findings are not in agreement with previous reports [1, 4, 11], they may indicate that patients should undergo surgery sooner.

Diabetes mellitus has been studied as a risk factor for surgical wound infection [12] and PVE with discordant results [4, 13]. In different studies designed to assess risk factors of PVE, diabetes has not been included [1, 11, 14]. In the present series, the prevalence of diabetes among PVE cases (1 of 81 patients) is lower than the expected 4% to 6% in our reference population [15], probably owing to the sample size, and for this reason an association between diabetes and PVE was not observed.

It is generally considered that patients who have had an episode of endocarditis before valve replacement surgery have a fourfold to sixfold increased the risk of infection of the prosthetic material [1, 4, 16, 17]. Although the magnitude of the odds ratio found in our patients was lower, previous endocarditis was significantly associated with an increased risk of PVE especially and probably in patients with early PVE. The effect of alcohol consumption as a risk factor for infective endocarditis has not been previously examined. Alcohol consumption was a significant determinant of PVE in the present series. This association may be explained by different mechanisms, including a higher risk of periodontal disease [18, 19], a higher rate of postoperative complications, and a longer postoperative hospitalization related to subclinical impairment of cardiac function, immune status, and homeostasis [20].

In agreement with the study of Grover and associates [4], urgent surgery showed a nonsignificant statistical trend to appear as a risk factor, mostly in case of early PVE.

With regard to the type of prostheses (mechanical or bioprosthesis) as a risk factor for PVE, results of different series are controversial [1, 11, 21, 22]. Mechanical prostheses appear to be associated with a higher risk for early PVE compared with a higher risk for late PVE in case of bioprosthesis [14, 17]. In our patients, a statistically not significant trend of the type of prosthesis (biologic material) as risk factor for late PVE was observed.

It has been shown that patients in whom heart valve replacement operations were associated with coronary artery bypass grafting have a higher risk of endocarditis [14], although in our study, like others [1, 4], an increased risk was not observed. On the other hand, the duration of anesthesia and the time of cardiopulmonary and cold ischemia did not reached statistical significance in our patients. This finding is consistent with the study of Grover and colleagues [4]. However, in the series of Ivert and coworkers [1] and Calderwood and colleagues [14], longer cardiopulmonary bypass time was an incremental risk factor for developing PVE.

Unexplained postoperative fever has been reported in as many as 70% of patients who had undergone a cardiac operation [23]. This sign, however, has a low specificity (15%) for the diagnosis of infection [24]. In our patients, fever during the immediate postoperative period was a significant risk factor of PVE in general and late PVE. The small sample size may probably account for the lack of statistical significance of this factor as a predictor of early PVE.

Gastrointestinal complications frequently occur in patients admitted to the intensive care unit. Of these, ulceration and bleeding in association with stress-related mucosal disease may contribute to increase mortality and to prolong duration of hospitalization [25]. A significantly increased risk of PVE was found in our patients with gastrointestinal bleeding. This factor was independently associated with PVE in the whole series of patients, as well as in patients with late PVE. This finding has not been previously reported. It is known that gastrointestinal bleeding may favor bacteremia due to breakdown of the mucosal barrier. Patients with cirrhosis and a high risk for bleeding due to gastroesophageal varices do not show a higher risk for infective endocarditis; however, history of gastrointestinal bleeding is frequent among cirrhotic patients with endocarditis [26]. Moreover, added risks associated with diagnostic and therapeutic procedures should be considered (eg, gastrointestinal endoscopies are associated with 0% to 8% (2% to 5%) episodes of bacteremia, particularly in case of breakdown of the mucosa [27]. Although this risk factor has not been previously reported, the effect of emergency gastroscopy for upper gastrointestinal bleeding could not be evaluated in our study due to the small number of patients undergoing this procedure. Our observation of gastrointestinal bleeding is based on 10 patients but the implications of further confirmation of these findings could be that for patients with postoperative gastrointestinal bleeding blood cultures should be drawn and aggressive antibiotic therapy sould be started.

Complications related to wound healing after thoracotomy occur in 0.57% to 6.8% of patients [28]. Moreover, about 3% of operated patients develop bacteremia after cardiac operations [29], and in 60% of these cases the source of bloodstream infection is the surgical wound. In our patients, wound complications were a significant risk factor of early PVE. Other perioperative and postoperative factors analyzed were not significant.

The present findings should be interpreted according to some limitations of the study. Firstly, the retrospective design of the study, with the consequent risk of bias classification regarding exposure to risk factors both in cases and controls. This feature invalidated the statistical analysis of some variables with a high number of missing values and limited the power of the study for other variables. Secondly, the criteria of Durack and colleagues [6] was accepted for the diagnosis of PVE. Although these criteria have a high diagnostic sensitivity and specificity, two different categories ("definite" and "possible") were accepted for each suspected case of endocarditis. However, because only 6 (7%) of the 81 cases of PVE were included in the "possible" diagnostic category, important bias in the estimations of the odds ratios of the risk factors seems improbable. Finally, case-control studies provide a level of evidence lower than cohort studies, but given the relatively low incidence of PVE, the prolonged latency period between operation and infection, and the coexistence of exposure to multiple risk factors, a case-control design was considered as the most efficient for the evaluation of these risks [8].

In summary, risk factors significantly associated with prosthetic valve endocarditis were NYHA functional class III or IV, alcohol consumption, previous endocarditis, fever in the ICU, and gastrointestinal bleeding. Functional class III or IV and complications of the surgical wound were independent predictors of early PVE, whereas postoperative fever and gastrointestinal bleeding were predictors of late PVE. Patients with prosthetic valve endocarditis differ from patients without infective endocarditis with regard to intrinsic and postoperative risk factors but not regarding perioperative-related variables.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Marta Pulido, MD, for editing the manuscript and editorial assistance, and Prof Llorca for advice in the statistical revision.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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