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European Heart Journal Advance Access originally published online on October 10, 2006
European Heart Journal 2007 28(1):65-71; doi:10.1093/eurheartj/ehl315
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© The European Society of Cardiology 2006. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Clinical and prognostic profile of patients with infective endocarditis who need urgent surgery

Ana Revilla1,*, Javier López1, Isidre Vilacosta2, Eduardo Villacorta1, María J. Rollán3, José R. Echevarría1, Yolanda Carrascal1, Salvatore Di Stefano1, Enrique Fulquet1, Enrique Rodríguez2, Luis Fiz1 and José A. San Román1

1 Department of Cardiology and Cardiac Surgery, Institute of Heart Sciences (ICICOR), Hospital Clínico Universitario, Ramón y Cajal 3-5, 47005 Valladolid, Spain
2 Department of Cardiology and Cardiac Surgery, Hospital Clínico San Carlos, Madrid, Spain
3 Department of Cardiology, Hospital Río Hortega, Valladolid, Spain

Received 26 May 2006; revised 20 September 2006; accepted 28 September 2006; online publish-ahead-of-print 10 October 2006.

* Corresponding author. Tel: +34 983420026; fax: +34 983255305. E-mail address: arevillaorodea{at}gmail.com


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Appendix
 Acknowledgements
 References
 
Aims Surgery in patients with infective endocarditis (IE) can be elective (upon completion of antibiotic treatment) or urgent (before antibiotic treatment has ended) when the clinical course is unfavourable. However, urgent surgery for left-sided endocarditis is associated with high mortality. The aims of this study were to describe the profile of patients with left-sided endocarditis who underwent urgent surgery and to analyse the factors that predicted mortality.

Methods and results Among 508 consecutive episodes of IE, 391 were left-sided and 89 required urgent surgery. The main reasons for urgent surgery were heart failure that did not respond to medication (72%) and persistent infection despite appropriate antibiotic treatment (31%). Thirty-two patients (36%) died during their hospital stay. Univariate analysis identified renal failure, septic shock, Gram-negative bacteria, persistent infection, and surgery for persistent infection as factors associated with mortality. Multivariate analysis confirmed only persistent infection and renal insufficiency as factors independently associated with a poor prognosis.

Conclusion Patients with IE who need urgent surgery have a poor clinical course. Heart failure, the main cause of urgent surgery, was not associated with higher mortality. However, persistent infection and renal failure were factors associated with higher post-surgical mortality.

Key Words: Endocarditis • Cardiac surgical procedures • Prognosis • Renal insufficiency • Congestive heart failure • Hospital mortality


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Appendix
 Acknowledgements
 References
 
Infective endocarditis (IE), an inflammatory disease characterized by endocardial proliferation usually involving the valves and caused by a variety of microorganisms, bears a poor prognostic profile. Before the use of antibiotics, nearly all patients died from uncontrolled infection. The prognosis improved in relation to advances in its diagnosis and that of its complications, and particularly as a result of antibiotic treatment.1 The restrictive attitude towards surgical intervention in acute endocarditis has changed during the last decade and early operation for IE is more common today.2 Surgical treatment, a substantial advance in improving the prognosis for this disease, can be elective (to be performed upon completion of antibiotic treatment) or urgent (needed because of an unfavourable clinical course before antibiotic treatment has been completed). The mortality rate of 9% for patients who undergo elective surgery3 can rise to as high as 25–35% for patients who need urgent surgery.3–8 This increased risk emphasizes the need to identify those factors that may worsen the prognosis of patients who need urgent surgery. The aims of this study were to describe the profile of patients with left-sided endocarditis who underwent urgent surgery and to analyse the factors that predicted mortality in this group.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Appendix
 Acknowledgements
 References
 
Study group
We prospectively collected 508 episodes of IE diagnosed consecutively at three tertiary centres between 1996 and 2004 according to the Duke criteria (until 2002) or the modified Duke criteria9 (2003 and 2004). Of these 508 episodes, 391 were located in the left side of the heart, 132 (34%) were electively operated on, and 89 patients required urgent surgery. These 89 patients were studied for the present report.

We analysed a total of 90 variables (appendix): 19 epidemiological, 8 clinical, 10 laboratory, 4 radiological, 6 electrocardiographic, 13 microbiological, 16 echocardiographic, and 14 outcome-related. All patients underwent at least one physical examination, one electrocardiogram, one chest X-ray, one urinalysis, three blood cultures upon hospital admission, three additional blood cultures 48 h after admission, and one transthoracic or transoesophageal echocardiogram. Empiric antibiotic treatment was started if needed and specific antibiotic treatment was initiated after the results of blood culture were available. If blood cultures were negative after 72 h, specific serological tests were done for Chlamydia, Brucella, Q fever, Legionella, and Mycoplasma.

To ensure consecutive enrolment, all patients who underwent echocardiography in whom endocarditis was suspected were observed until a diagnosis was established. Patients with a final diagnosis of endocarditis were included in the study. A standardized case report form was used by all participant centres and all patients were registered on an on-going database with all variables recorded at the time of entry.

Definition of terms
The only event considered in this study was in-hospital death regardless of its cause. We considered cases as early-onset prosthetic valve endocarditis when the disease occurred within the first year after surgery. Acute onset was considered to exist when the time between the appearance of symptoms and hospital admission was less than 15 days. Renal insufficiency was defined as the presence of a serum creatinine concentration higher than 2 mg/dL. Atrioventricular block included first, second, or third degree block of atrioventricular conduction. Heart failure was diagnosed on the basis of established criteria.10 Perivalvular complications were defined as follows: abscess, a closed cavity with no signs of flow, and with lower echographic density than the adjacent structures; pseudoaneurysm, echolucent cavities communicating with the vascular lumen, with evidence of flow; fistula, a narrow communication between two adjacent cavities, with flow through the tract.1,11–12

Indications for urgent surgery
Urgent surgery was defined as surgery done before antibiotic treatment was completed. The indications for urgent surgery in our group were predefined by consensus and are as follows: mild heart failure unresponsive to medication, pulmonary oedema, persistent infection (persistent fever and/or positive blood cultures after 7 days of appropriate antibiotic treatment, once other possible foci of infection were ruled out) and repeat embolism despite appropriate antibiotic treatment, with persistence of vegetations on echocardiogram. The initial presence of perivalvular complications in patients with a favourable clinical course was not considered an indication for urgent surgery, although enlargement of pseudoaneurysms and abscesses or progression to a fistula were considered indications.

Statistical analysis
Categorical variables are reported as absolute values and percentages and continuous variables are reported as mean ± standard deviation unless stated otherwise. Normality assumption was determined by Shapiro–Wilk's test. Continuous variables were compared with Student's t-test and Mann–Whitney U-test for non-normal variables, and categorical variables were compared with the {chi}2 test and Fisher's exact test when appropriate.

Univariate logistic regression analysis was performed to estimate the odds ratio. Log-transformed continuous variables were introduced in the model to assess the linearity.

Multivariable logistic regression analysis was performed to determine the independent predictors of in-hospital mortality. Variables introduced in the multivariable analysis were persistent infection, renal failure, and heart failure. Renal failure and persistent infection were significant in the univariate analysis and heart failure was introduced for its clinical relevance.3,8,13 On the other hand, septic shock was not introduced in the model because of its direct association with persistent infection (94% patients with septic shock had persistent infection). We have calculated adjusted odds ratios with 95% confidence intervals for each variable. We performed Hosmer–Lemershow test. To assess the goodness of classification rule, we have made cross-validation.

All tests were two-sided and differences were considered statistically significant at P-values ≤ 0.05. Statistical analysis was performed with SPSS software V 12.0 (SPSS Inc., Chicago, IL, USA) and SAS software V 8.2 (SAS Institute Inc., Cary, NC, USA).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Appendix
 Acknowledgements
 References
 
Mean age of the patients in our study group (n = 89) was 56 ± 14 years. About two-thirds of the cases (67%) originated in the community, and 10 patients had a history of a previous episode of IE. The presence of previous heart disease, diseases that predisposed patients to IE, and the port of entry of the infection are summarized in Table 1.


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  		Table 1 Presence of previous heart disease, predisposing diseases, and port of entry of the infection

 
Blood cultures were negative in 18 patients (20%), five of whom had received antibiotic treatment for febrile syndrome before hospitalization. In five cases, the causal microorganism was identified in other cultures. The remaining patients had positive blood cultures. Thus, the causal microorganism could be identified in 76 cases (85%). The microbiological profile for our group of patients is shown in Table 2.


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  		Table 2 Causal microorganisms

 
Clinical, radiographic, and electrocardiographic manifestations upon admission are shown in Table 3. Of note is that most patients had fever and 48 patients (54%) had symptoms and signs of heart failure, with 39 patients in NYHA functional class III or IV.


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  		Table 3 Clinical, radiographic, and electrocardiographic manifestations at admission

 
The findings on transoesophageal echocardiography are shown in Table 4. Endocarditis was multivalvular in 19 patients (21%) and involved a prosthetic valve in 29 (33%); in the latter group, 14 patients had early-onset prosthetic endocarditis. In most patients (83%), vegetations could be observed on transoesophageal echocardiogram, and 35 patients had at least one perivalvular complication: 20 had abscesses, 16 had pseudoaneurysms, and 7 had fistulas. Seven patients had more than one type of perivalvular complication. Moderate or severe valve regurgitation was detected in 72 patients.


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  		Table 4 Findings on transoesophageal echocardiography

 
During hospitalization, 15 patients developed heart failure, 15 renal failure, 12 septic shock, 3 ischaemic stroke, 1 intracranial bleeding, and 13 peripheral embolisms. In this latter group, nine embolisms were splenic, one hepatic, one in the lower limbs, and two in other locations.

Median time from onset of antibiotic therapy to surgery was 10 days (IQR 4–20 days). The main reason for urgent surgery was heart failure that did not respond to medication or pulmonary oedema in 53 patients (60%), persistent infection despite appropriate antibiotic treatment in 17 (19%), both causes in 11 patients (12%), perivalvular complications in 5 (6%), and repeat embolisms despite antibiotic treatment in 3 (3%). Type of surgery was as follows: 76 mechanical prosthesis (85%), 7 bioprosthesis (9%), 5 homografts (6%), and 1 composite aortic graft.

During their hospital stay 32 patients died (36%). Nine patients died during surgery and the remaining 23 in the post-operative period: 11 died from septic shock, 5 from multiorganic failure, 3 from ventricular arrhythmia, 2 from heart failure, 1 from haemorrhagic shock, and 1 from heart tamponade. There were no statistically significance difference between mortality of patients urgently and electively operated on (36 vs. 24%; P = 0.10). Mortality rates in patients with different types of endocarditis are shown in Table 5.


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  		Table 5 Mortality rates in patients with different types of endocarditis

 
The univariate analysis is specified in Table 6. Of note, prosthetic involvement did not increase mortality. The multivariate analysis (Table 7) confirmed only persistent infection (OR 3.50, 95% CI 1.24–9.93) and renal failure (OR 2.91, 95% CI 1.05–8.07) as factors independently associated with poor prognosis. These odds ratios were similar to the odds we obtained in the univariate analysis. Hosmer–Lemershow test was not significant (P = 0.79). Cross-validation analysis revealed classification rules based on independent variables which allow us to obtain a sensitivity of 78% and a specificity of 58%.


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  		Table 6 Univariate analysis for in-hospital mortality

 

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  		Table 7 Multivariate analysis for the event (in-hospital death)

 
We also analysed the clinical, echocardiographic, and outcome-related variables recorded during the first 72 h after admission in patients who developed persistent infection and renal failure. The variables associated with the appearance of persistent infection are shown in Table 8. None of the echocardiographic variables was predictive of persistent infection. In patients with persistent infection, Staphylococcus aureus or Gram-negative bacteria were the organisms detected most often in blood cultures, and Streptococcus viridans was detected less frequently. None of the clinical, echocardiographic, or microbiological variables recorded prospectively upon admission were associated with the development of renal failure.


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  		Table 8 Univariate analysis for persistent infection

 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Appendix
 Acknowledgements
 References
 
Before the age of antibiotics, IE was a fatal disease. With the introduction of antibiotics, it became a curable disease in some cases. Mortality nevertheless remains high, mainly because of heart failure secondary to valvular destruction.14 Surgery has improved the prognosis, although it was initially used only once the infection had been eradicated with antibiotic treatment. In 1965, the first case involving surgery during the active disease was published.15 Since then, a number of observational studies have noted the effectiveness of surgery in patients with active endocarditis complicated by heart failure or uncontrolled infection.3,15–16

Several earlier studies have investigated the factors that predicted the prognosis for IE,3,8,17–20 but all have limitations: they were retrospective; transoesophageal echocardiography was not done in all patients; the analyses omitted variables of importance (echocardiographic and outcome-related); or the population described was heterogeneous (right-sided and left-sided endocarditis, cases that required urgent surgery and that were cured with medication). The present study is the first to analyse a prospective, homogeneous cohort to identify which factors were predictive of a poor prognosis in patients who needed urgent surgery.

None of the clinical factors, previous history of heart disease or predisposing factors, influenced the prognosis in our patients. In an earlier series of patients,8,18–20 the importance of these factors in the prognosis was generally limited. In another relatively recent series, diabetes mellitus was found to be an independent predictor of mortality.21 According to our results, however, the influence of diabetes on the prognosis was not maintained in patients who needed urgent surgery. Despite the general idea that prosthetic endocarditis bears a worse prognosis than native endocarditis, infection of a prosthesis was not found to be a predictor of mortality in our series. It has to be taken into account that ours is a selected high-risk population, since all are patients who underwent urgent surgery due to their clinical status. Therefore, variables associated to the poor clinical profile are expected to be more strongly related to mortality than the type of valve affected.

Persistent infection indicates failure of conservative management22 and is associated with high mortality.22–24 Surgery is advised for these patients, and completion of a course of appropriate antibiotic treatment should not delay the operation.11 According to our results, persistent infection is an independent predictive factor of mortality. Patients with endocarditis and persistent infection who require urgent surgery are four-fold as likely to die after surgery as patients who do not have persistent infection. Why persistent infection is a predictor of death after urgent surgery is far from clear. Theoretically, persistent infection implies a higher degree of valvular destruction and surrounding tissues, but this relationship is not supported by our data. In fact, patients with persistent infection had neither more regurgitant valves nor more periannular complications in our series. Conceptually, heart failure in endocarditis is caused by a localized problem at the valve and thus can be successfully treated with surgery which is no more than a local therapeutic tool. In contrast, uncontrolled infection despite optimal antibiotic treatment represents a systemic dissemination of the disease which, therefore, is expected not to be solved by a local therapeutic approach.

Renal failure was also an independent factor associated with an unfavourable prognosis in our patients with endocarditis who needed urgent surgery. Several elements contribute to renal dysfunction in IE, for example, immunocomplex glomerulonephritis, renal artery embolism, toxicity of the antibiotic treatment, and haemodynamic alterations.25 Renal failure was previously shown to be a factor associated with post-operative mortality after heart surgery26 and after surgery in general.27 Moreover, renal failure is a systemic manifestation related with the severity of IE, a connection which probably explains why it is also associated with a worse prognosis.

An important difference between our results and those of earlier series is the significance of the causative microorganism as a prognostic factor: we did not identify any causal agent as directly related with mortality. Only Gram-negative bacteria were associated with higher mortality, as noted in earlier studies,19,28 although the number of cases of endocarditis caused by these organisms in our series was too small to allow us to draw firm conclusions. In our experience, the predominant infective organism was Staphylococcus species, similar to previously reported on by others.2,29 Some authors have documented a relationship between Staphylococcus aureus and a worse prognosis for endocarditis.3,8,19–21,29 Staphylococcus aureus is a highly destructive microorganism frequently associated with perivalvular complications and embolisms.30 Our data suggest that the prognosis after urgent surgery depends mainly on whether the infection was controlled or not, rather than on the germ that caused endocarditis. However, Staphylococcus aureus was associated with the development of persistent infection. In other words, the presence of this microorganism predicted a higher likelihood of developing persistent infection, and thus a more unfavourable clinical course.

Some laboratory parameters have been suggested to be associated with a worse prognosis. A number of studies reported that leukopenia or leukocytosis implies a worse prognosis for endocarditis.18,19 The magnitude of the inflammation reflects a systemic response to infection and suggests that IE can be considered a whole-organism infection.18 Several scores have been developed to measure the severity of sepsis, and many include leukocytosis, thrombopenia, anaemia, and transaminase alterations. Thus, the importance of these variables for the prognosis lies in their capacity to express the severity and extent of the infection. In our statistical model, persistent infection and renal failure expressed these characteristics most clearly.

The importance of heart failure as a prognostic factor in endocarditis varies in different studies. Some series found this to be a fundamental prognostic factor,3,8,17,19,20 whereas others reported no influence on the prognosis.18,21 Chu et al.21 explained these discrepancies as the result of difference in the criteria used to define and diagnose heart failure. Studies based on validated diagnostic criteria found no relation between heart failure and prognosis.10,20 Heart failure in endocarditis is always secondary to valvular dysfunction, generally due to valve failure. Valve replacement or repair would therefore resolve the problem without being expected to worsen the prognosis for urgent surgery. By no means, it can be inferred from our results that heart failure does not adversely affect prognosis in patients with IE. What our data suggest is that heart failure, unlike persistent infection and renal failure, does not worsen prognosis in patients who need urgent surgery according to the indications followed by our group.

In practical terms, when a patient with IE shows a poor clinical course because of heart failure that does not respond to medication, urgent surgery is advisable, since concerns that this will increase mortality are unfounded. However, if the reason for the patient's poor clinical course is infection that does not respond to medication or persistent infection, urgent surgery, if performed, should be assumed to involve a greater likelihood of death. An earlier surgical approach might be advocated in this context. Given that surgery in infected patients after 7 days of appropriate treatment (a not evidence based cut-off) carries a high-mortality risk, we can speculate that surgery within 3–5 days of persistent fever or positive blood cultures unrelated to other conditions could improve prognosis. Further studies will be needed to gather evidence on this issue.

The low use of homografts in our series (only 6%) is explained by the unavailability to obtain them on an urgent basis. Although the definition for urgent surgery used in our protocol was that performed before the end of the antibiotic treatment, most of the 89 patients of our study were operated within 24 h after the indication was established and that homografts were not available.

We are aware of potential weaknesses of the present study. First, this is an observational study and allocation of therapies was not randomized. Thus, bias in the selection of therapies was present. Secondly, ours are large reference centres that obviously introduce a bias in the patients included in our database. Thus, our conclusions are pertinent to tertiary care centres with surgical facilities and cannot be generalized. Finally, due to the low number of patients included in the study, some risk factors may not have emerged from the current analysis. However, this statistical shortcoming might have been counterbalanced because there were a lot of events.

In conclusion, patients with IE who need urgent surgery have an unfavourable clinical presentation and a poor clinical course. The main cause for urgent surgery is heart failure, which was not associated with higher mortality in our patients. In contrast, persistent infection and renal failure were associated with higher post-operative mortality.


   Appendix
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Appendix
Acknowledgements
 References
 
Variables included in the case report form:

  1. Epidemiological: gender, age, referred, nosocomial acquisition, comorbid conditions (diabetes mellitus, immunocompromised state, immunodepressor therapy, chronic anaemia, renal insufficiency, cancer, chronic bronchitis, skin disease, collagen disease, HIV, drug addiction), factors predisposing to IE (prosthesis, rheumatic fever, degenerative valvular disease, previous endocarditis).
  2. Clinical: time between initial symptoms and hospitalization, clinical manifestations at hospitalization (heart failure, NYHA functional class, dyspnoea, fever, renal insufficiency, abnormal skin findings, splenomegaly).
  3. Laboratory: haematological findings (serum creatinine, blood urea nitrogen, haemoglobin, haematocrit, white blood cell count mean, white blood cell count > 10 000 x 103 µL, platelets, sedimentation globular rate), urine findings (haematuria, proteinuria).
  4. Radiographic: cardiac enlargement, septic emboli, pleural effusion, pulmonary congestion.
  5. Electrocardiographic: atrioventricular block, right bundle branch block, left bundle branch block, atrial fibrillation, acute myocardial infarction, supraventricular tachycardia.
  6. Microbiological: Viridans Streptococci, Bovis Streptococci, other Streptococci, Aureus Staphylococci, Coagulase-negative Staphylococci, HACEK, Enterococci, polymicrobial, fungi, anaerobes, Gram-negative bacilli, negative cultures, and others.
  7. Echocardiographic: multivalvular, prosthetic, valve involved (mitral, aortic, aortic mechanical prosthesis, mitral mechanical prosthesis, aortic bioprosthetic, mitral bioprosthetic), vegetations, mayor diameter, area > 0.85 cm2, periannular complications (abscess, pseudoaneurysm, fistula), valve perforation, ejection fraction.
  8. Outcome-related: clinical manifestations along hospitalization (fever, heart failure, renal failure, septic shock, ischaemic stroke, intracranial bleeding, peripheral embolisms, pulmonary embolism, abnormal skin findings), persistent infection, type of surgery, main reason for surgery, death, cause of death.


   Acknowledgements
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Appendix
 Acknowledgements
References
 
We thank Itziar Gómez and Agustín Mayo for their statistical advice and Karen Shashok for her technical support in the English version of the original manuscript. This study was financed in part by the Cooperative Network for Cardiovascular Research (Red Cooperativa de Investigación Cardiovascular, RECAVA) of the Spanish National Institute of Health (Instituto de Salud Carlos III) and by a grant from the Sociedad Castellano-Leonesa de Cardiología (SOCALEC).

Conflict of interest: none declared.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Appendix
 Acknowledgements
 References
 

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