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Archives of cardiovascular diseases
Volume 109, n° 10
pages 542-549 (octobre 2016)
Doi : 10.1016/j.acvd.2016.02.010
Received : 11 October 2015 ;  accepted : 9 February 2016
Comparison of prognoses of Staphylococcus aureus left-sided prosthetic endocarditis and prosthetic endocarditis caused by other pathogens
Comparaison du pronostic des l’endocardites sur prothèse valvulaire à staphylocoque doré et à un autre germe
 

Layal Abdallah a, Gilbert Habib b, Jean-Paul Remadi a, Erwan Salaun b, Jean-Paul Casalta b, Christophe Tribouilloy a,
a Département de cardiologie, CHU d’Amiens–Picardie, 80054 Amiens, France 
b Département de cardiologie, hôpital de la Timone, Aix-Marseille université, CHU de Marseille, 13385 Marseille, France 

Corresponding author. Département de cardiologie, CHU d’Amiens–Picardie, avenue René Laënnec, 80054 Amiens cedex 1, France.
Summary
Background

Staphylococcus aureus prosthetic valve endocarditis (SAPIE) is a serious disease.

Aims

Our objective was to study the clinical, echocardiographic and prognostic characteristics of left-sided SAPIE, and to compare these characteristics with those of left-sided non-Saureus prosthetic infective endocarditis (NSAPIE) (i.e. left-sided prosthetic infective endocarditis caused by another germ).

Methods

This was a retrospective analysis of 35 cases of SAPIE among 247 cases of left-sided prosthetic valve endocarditis hospitalized at two university hospitals (Amiens and Marseille, France).

Results

SAPIE accounted for 14.1% of the cases of left-sided prosthetic valve endocarditis. SAPIE complications included heart failure (in 42.8% of cases), acute renal failure (in 51.4%), sepsis (in 51.4%), neurological events (in 31.4%), systemic embolic event (in 34.2%) and abscess (in 60.0%). In-hospital mortality occurred in 48.5% of SAPIE cases compared with 16% of NSAPIE cases. A comparison of the SAPIE and NSAPIE groups showed a significant difference in terms of 4-year survival (31.8±7.3% vs 60.1±4.1%; P =0.001). Severe sepsis was the only prognostic factor associated with in-hospital mortality (odds ratio 5.7; P =0.03) and long-term mortality (odds ratio 3.7; P =0.01) in cases of SAPIE. Sepsis-induced multiple organ dysfunction syndrome was the main cause of in-hospital mortality (70.5%).

Conclusions

SAPIE is a very serious disease, with elevated in-hospital mortality resulting from sepsis-induced multiple organ dysfunction syndrome. Emergency surgery is recommended in these cases, when possible, before the occurrence of complications, especially severe sepsis.

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Résumé
Introduction

L’endocardite infectieuse sur prothèse à Staphylococcus aureus (EIPSA) reste une maladie grave.

Objectifs

L’objectif est d’étudier les caractéristiques cliniques, échographiques et pronostiques des EIPSA du cœur gauche et de comparer ces caractéristiques aux autres endocardites sur prothèse.

Méthodes

Il s’agit d’une étude rétrospective analysant les données de 35 EIPSA hospitalisées aux CHU d’Amiens et de Marseille.

Résultats

EIPSA représente 14,1 % des endocardites sur prothèse. EIPSA se complique dans 42,8 % des cas d’insuffisance cardiaque, 51,4 % d’insuffisance rénale aiguë, 51,4 % de sepsis, 31,4 % d’évènement neurologique, 34,2 % d’embolie systémique et 60,0 % d’abcès périannulaires. La mortalité hospitalière est de 48,5 %, plus élevée que celle des EI sur prothèse non liées au Saureus . La comparaison de survie globale actuarielle à 4ans montre une différence significative entre le groupe de SAPIE et le groupe des autres endocardites sur prothèse (31,8±7,3 % vs 60,1±4,1 % ; p =0,001). Le sepsis sévère est le seul facteur pronostique associé à la mortalité hospitalière (OR à 5,7 ; p =0,03) et à la mortalité à long cours (OR 3,7 ; p =0,01). La défaillance multiviscérale induite par le sepsis est la principale cause de mortalité hospitalière (70,5 %).

Conclusions

EIPSA est une maladie grave avec une mortalité hospitalière très élevée due dans la majorité des cas à une défaillance multiviscérale induite par le sepsis. Les recommandations européennes conseillent pour ce type d’EI, la réalisation d’une chirurgie urgente sans attendre, si possible, l’apparition des complications.

The full text of this article is available in PDF format.

Keywords : Infective endocarditis, Staphylococcus aureus , Left-sided prosthetic valve, Prognosis, Sepsis

Mots clés : Endocardite infectieuse, Staphylococcus aureus , Prothèse du cœur gauche, Pronostic, Sepsis

Abbreviations : CI, IE, MRSA, NSAPIE, OR, SAPIE, TOE, TTE


Background

Infective endocarditis (IE) is a severe disease, with diagnostic difficulties, changing epidemiology in recent decades and high mortality rates. The incidence of IE ranges from 3 to 10 episodes per 100,000 people per year [1]. The epidemiology of IE has changed significantly in recent years, with the advent of new predisposing factors [2], such as the presence of prosthetic valves or intracardiac materials, haemodialysis, nosocomial infections, immunodeficiency, increased use of injectable treatment and, especially, the aging population with increasing degenerative diseases. These changes have been associated with an increase in infection rates by Staphylococcus aureus [1]. In the past, Saureus infective endocarditis was infrequent, accounting for 6.9% of IE in 1931 [3]; these rates have increased steadily from 16% in 1941–1961 [3] to 19–38% currently [2, 3, 4]. Despite the progress in antimicrobial therapy, mortality remains high, especially in cases of prosthetic infection [2].

The management of prosthetic IE is complicated, especially in cases of left-sided Saureus prosthetic infective endocarditis (SAPIE). Current guidelines [1, 5] on SAPIE are based on only a few studies [6, 7, 8], and the indication for surgical treatment is level of proof C. New guidelines from the USA [5] recommend surgery during initial hospitalization for left-sided SAPIE (class IB).

The aims of our work were to determine the clinical and echocardiographic characteristics and prognostic factors of left-sided SAPIE, and to compare these characteristics with those of left-sided non-Saureus prosthetic infective endocarditis (NSAPIE) (i.e. left-sided prosthetic infective endocarditis caused by another germ).

Methods

Between January 1990 and December 2010, 1254 consecutive patients from two French centres (Amiens and Marseille) with definite IE according to the Duke criteria [9, 10] were referred to our echocardiographic laboratory. All patients were examined by transthoracic echocardiography (TTE) and transoesophageal echocardiography (TOE). A total of 247 patients (19.6%) had acute left-sided prosthetic valve IE (mitral and aortic valves), including 35 (14.1%) with blood or valve cultures that were positive for Saureus ; all 247 patients were included in this study (Figure 1). In our series, Streptococcus viridans was found in 17.8% of cases (n =35), Saureus in 14.1% (n =35), coagulase-negative staphylococci in 10.2% (n =25), Streptococcus bovis in 10.1% (n =25), Enterococcus foecalis in 17% (n =42) and other germs in 4% (n =10). The microorganism was not identified in 26.8% of cases (n =66). Clinical, biological and echocardiographic data were collected prospectively, whereas follow-up data were obtained retrospectively.



Figure 1


Figure 1. 

Study population: flow chart. IE: infective endocarditis; NSAPIE: non-Staphylococcus aureus prosthetic infective endocarditis; SAPIE: S. aureus prosthetic infective endocarditis.

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Clinical variables

Age, sex, presence of co-morbidity (history of diabetes, cancer, haematological malignancy, cirrhosis, renal failure, dialysis, heart failure or coronary artery disease) and presence of an intravascular device (venous catheter, pacemaker or dialysis device) were analysed. The Charlson co-morbidity index, taking into account the patient's age and history, was calculated [11].

The following acute clinical events present on admission or occurring during hospitalization were recorded: heart failure, neurological event, embolism and severe sepsis. The portal of entry of the infection was investigated. Embolic events were diagnosed based on clinical signs and data derived from a non-invasive procedure (brain, chest and abdomen computed tomography); 74% of patients (n =183) had a computed tomography scan. A neurological event was defined as the development of ischaemic stroke with hemiplegia, haemorrhagic stroke, transient ischaemic attack, brain abscess and features of encephalopathy or coma. Severe sepsis was defined as a systemic inflammatory syndrome secondary to an infectious process, leading to organ dysfunction, signs of hypoperfusion or hypotension [12, 13].

Echocardiography

All patients were systematically assessed by TTE completed by TOE. All echocardiographic studies were performed according to standard techniques and by experienced physicians during the acute phase of IE. Standard definitions were used for vegetations, abscesses and other cardiac infective lesions [14]. All TOE recordings were reviewed by an experienced physician to measure the maximum length of vegetations in various planes. Valvular regurgitation was quantified by Doppler echocardiography using standard methods [15].

Follow-up

Follow-up data included surgical treatment and death during hospitalization or follow-up. In-hospital mortality was defined as death during the initial hospitalization for IE. Long-term mortality included death during hospitalization and during follow-up. Data on deaths during follow-up were obtained retrospectively. Follow-up was complete in 100% of cases, with a mean follow-up of 25.5±37.7months.

Statistical analysis

Statistical analyses were performed with SPSS 21.0 software (IBM, Armonk, NY, USA). Quantitative variables are expressed as means±standard deviations. Comparisons between groups were carried out using Student's t -test or the χ 2 test. The cumulative probability of survival was estimated using the Kaplan–Meier actuarial method at 1-month intervals, and reported as mean estimated survival±standard error. The log-rank test was used to determine any significant differences. Multivariable analyses were performed, incorporating, as potential predictors of mortality, variables correlated with mortality on univariate analysis with P -values0.10. A multivariable logistic regression model was used for in-hospital mortality and a Cox multivariable model was used for long-term mortality.

Results
Baseline characteristics

Of the 247 patients with left prosthetic IE (155 men/92 women, mean age 65.1±14.2), 15.8% had diabetes and 11.7% had neoplasia, with a mean co-morbidity index of 2.92±2.1 (Table 1). IE involved the aortic prosthesis in 57.4% of cases, the mitral prosthesis in 29.1% of cases and both the mitral and aortic valves in 13.3% of cases. The portal of entry was identified in 46.5% of cases with a homogeneous distribution (12.5% of cutaneous origin, 12.1% of nasopharyngeal origin and 18.6% of digestive origin). The main complications were heart failure (32.7%), acute renal failure (19.0%), severe sepsis (19.4%), neurological events (21.4%), systemic embolism (25.1%) and abscess (41.2%).

In our series, SAPIE accounted for 14.1% (35/247) of the cases of left-sided prosthetic IE. SAPIE was late (occurring more than 1year after implantation of the prosthesis) in most cases (89%). The mean delay between surgery and prosthetic valve endocarditis in the 247 patients with prosthetic IE was 91months (range, 74–108months); for the SAPIE group, the mean delay was 85months (range, 53–118months). SAPIE involved the aortic prosthesis in 62.8% of cases, the mitral prosthesis in 22.8% of cases and both the mitral and aortic valves in 14.2% of cases. The main complications of SAPIE (Table 1) were heart failure (42.8%), acute renal failure (51.4%), severe sepsis (51.4%), neurological events (31.4%), systemic embolism (34.2%) and abscess (60.0%).

Comparison of the SAPIE and NSAPIE groups (Table 1) showed that the two populations were similar in terms of age (P =0.6), sex (P =0.34) and co-morbidity index (P =0.78). There were no significant differences in terms of rates of heart failure (42.8% vs 31.1%; P =0.18), neurological events (31.4% vs 19.8%; P =0.12) and systemic embolism (34.2 vs 23.5%; P =0.8). However, higher rates of acute renal failure (51.4% vs 13.6%; P =0.0001), abscess (60.0% vs 38.2%; P =0.025) and severe sepsis (51.4% vs 16.9%; P =0.0001) were observed in the SAPIE group.

Surgery

Early surgery was performed for 136 patients (55.0%) in the total left-sided prosthetic IE population: 15 patients (42.8%) in the SAPIE group; 121 patients (56.6%) in the NSAPIE group. Comparison of the SAPIE and NSAPIE groups (Table 1) showed a significant difference between the two groups in terms of operative mortality (46.6% vs 20.8%; P =0.048). In case of SAPIE, in-hospital mortality was 46.6% in patients treated surgically (n =7/15 patients) and 50.0% among non-operated patients (n =10/20 patients; P =0.82).

In-hospital mortality

The in-hospital mortality rate in the total left-sided prosthetic IE population was 20.6%. Multivariable analysis showed that infection by Saureus (odds ratio [OR] 4.4, 95% CI 1.8–11; P =0.0001) was strongly associated with in-hospital mortality.

In-hospital mortality (Table 1) was very high in case of SAPIE (48.5% vs 16.0% in case of NSAPIE; P =0.0001). Univariate (Table 2) and multivariable (Table 3) analyses showed that severe sepsis was the only predictive factor for in-hospital mortality (OR 5.7, 95% CI 1.61–29.2; P =0.03) in case of SAPIE. Univariate analysis of in-hospital mortality showed that there was a trend toward significance for acute renal failure (P =0.1). The analysis of the causes of in-hospital mortality in the SAPIE group (Figure 2) showed that death was essentially caused by multiple organ dysfunction syndrome induced by severe sepsis (n =12, 70.5%). The other causes of death were respiratory infection (n =2, 11.76%), intestinal obstruction (n =1, 5.9%), myocardial infarction (n =1, 5.9%) and stroke (n =1, 5.9%).



Figure 2


Figure 2. 

Histogram of the causes of in-hospital mortality in cases of SAPIE. SAPIE: Staphylococcus aureus prosthetic infective endocarditis.

Zoom

Among the 17 patients who died during hospitalization in the SAPIE group, eight patients were operated on. The causes of death were: multiple organ dysfunction syndrome induced by severe sepsis in 62.5% of cases (n =5); stroke in 12.5% (n =1); myocardial infarction in 12.5% (n =1); and intestinal obstruction in 12.5% (n =1). The remaining nine patients who died during hospitalization had not been operated on. Multiple organ dysfunction syndrome induced by severe sepsis was also the main cause of death in this subgroup of nine patients (77.8% of cases, n =7); the other cause of death was respiratory infection (22.2%, n =2).

Long-term mortality

Long-term 4-year survival was 56.2±6.2 in the total population (Figure 3). For left-sided prosthetic IE (Figure 3), infection by Saureus was strongly associated with long-term mortality. Comparison of the SAPIE and NSAPIE groups (Figure 3) showed a significant difference in terms of long-term 4-year survival (31.8±7.3% vs 60.1±4.1%; P =0.001); this difference was mainly related to the high in-hospital mortality rate in the SAPIE group. On univariate analysis, the factors associated with long-term mortality, in case of SAPIE, were severe sepsis (P =0.015) and acute renal failure (P =0.08) (Table 4). On multivariable analysis, severe sepsis was the only predictive factor associated with long-term mortality (OR 3.7, 95% CI 1.3–10.6; P =0.01) (Table 3).



Figure 3


Figure 3. 

Actuarial survival curves at 4years: long-term mortality. The red curve represents the Staphylococcus aureus prosthetic infective endocarditis (SAPIE) group; the blue curve represents the non-Saureus prosthetic infective endocarditis (NSAPIE) group; the green curve represents the overall study population. *P corresponds to a statistically significant P -value<0.05 between NSAPIE and SAPIE.

Zoom

Discussion

SAPIE is an extremely serious disease, with a high rate of in-hospital mortality [6, 7, 8]. However, only a few studies have been specifically devoted to SAPIE, with a limited number of patients [6, 7, 8]. Our study showed a very high in-hospital mortality rate in case of left-sided SAPIE (48.5%), despite improved diagnostic techniques and therapeutic approaches. Severe sepsis is the only prognostic factor independently associated with in-hospital mortality and long-term mortality in case of SAPIE.

The left-sided prosthetic IE present in our series accounted for 19.7% of all cases of IE. This rate is similar to those published previously, which range from 16% to 31% [6, 16, 17]. In our series, Streptococcus viridans was the germ found most frequently (in 17.8% of cases). In the literature, the rate of SAPIE among cases of left-sided prosthetic IE ranges between 23% and 29% [3, 17]. Left-sided prosthetic IE often occurs in patients with poor clinical status and major co-morbidities [16]; accordingly, a high co-morbidity index was observed in our series.

Compared with NSAPIE, SAPIE has been associated with higher complication rates and in-hospital mortality rates ranging between 36% and 47.5% in published series [6, 8]. In our study, the in-hospital mortality rate was 48.5% and the long-term 4-year survival rate was 31.8±7.3%. In our series, SAPIE was complicated by heart failure in 42.8% of cases; previous studies have also reported a similarly high incidence of heart failure [6, 8]. The heart failure was not a significant predictor factor of in-hospital mortality [6, 8]. Neurological complications were observed in 31.4% of cases, which is a higher rate than those reported in the literature [6, 8]. Infection by Saureus is known for its embolic risk, which is well illustrated by the 34.2% rate of systemic embolic complications in our series (rates in the literature range from 27% to 41% [6, 8]). Chirouze et al. [6] showed that stroke was a prognostic factor for hospital mortality, and Sohail et al. [8] reported that in a medically treated SAPIE group, mortality was about 100% for neurological complications; such findings were not observed in our series.

In our series, SAPIE was complicated by severe sepsis in 51.4% of cases, with multiple organ dysfunction syndrome explaining the high in-hospital mortality rate. Sepsis was found to be the main predictor of in-hospital and long-term mortality; such a finding has not been described in previous studies of SAPIE [6, 8]. It seems logical that severe sepsis was the main determinant of hospital mortality because of the known virulence of these bacteria. Annular abscess is very common in cases of SAPIE (60% in our series and 42% in the series of Sohail et al. [8]). As previously reported [6, 8], abscess was not a factor significantly associated with in-hospital and long-term mortality in our series. However, in 1998, John et al. [7] reported that abscess was a major prognostic factor determining mortality at 3months. Indeed, abscess will make the control of infection by antibiotics more difficult, will aggravate the sepsis and will lead to prosthetic desinsertion.

Comparison of the SAPIE and NSAPIE groups showed a significant difference in-hospital mortality rates (P =0.0001) and 4-year survival rates (P =0.001). Moreover, we identified that Saureus infection was a powerful pejorative prognostic factor in left-sided prosthetic IE. SAPIE is associated with higher complication rates, including acute renal failure, severe sepsis, abscesses, and neurological events, although the difference was not significant.

SAPIE management difficulties explain the current recommendation for urgent surgical treatment, even though series have not demonstrated the superiority of early surgery over medical treatment in terms of mortality [8]. However, demonstrating the value of surgery is difficult, mainly because the groups of patients who are or are not operated on are not comparable. Moreover, in our series, the number of operated patients was small, which induced a lack of statistical power. Only a randomized study can answer this question, but its realization is unethical. European guidelines [1] advocate (class IIaC) urgent early surgical treatment (within the first 7days of antibiotics) or elective surgery (after 7days of antibiotic treatment) in case of SAPIE, whereas the new guidelines from the USA [5] strongly advise surgical treatment during hospitalization and before the end of antibiotic therapy in case of SAPIE (class IB). Given the very high in-hospital mortality rate and despite the significant operative mortality risk, these guidelines are logical. Our opinion is that surgery should be systematically discussed urgently, and considered, if possible, before the onset of severe sepsis. Further studies on this topic, including many more patients, are necessary.

Study limitations

Our study has a number of limitations. The follow-up data were obtained retrospectively. This study of left-sided SAPIE needs to be completed by studies in prospective cohorts, to evaluate the influence of surgical treatment on mortality and to better define its indications. However, it would be ethically and practically impossible to conduct a randomized study to determine the treatment of IE, as these patients need to be managed case by case. Our study was performed in two tertiary care centres, with possibly more severe patients than in other centres, which could in part explain the high mortality rate. Moreover, the limited number of patients included could explain the lack of statistical significance of certain results.

Conclusions

SAPIE is a very serious disease, with very high rates of in-hospital and long-term mortality. This infection is often complicated by severe sepsis, renal failure, abscess and neurological complications. The main prognostic factor associated with long-term and in-hospital mortality was severe sepsis, leading to a risk of multiple organ dysfunction syndrome. Because of the aggressive nature of the microorganism, surgery should be considered very early, when possible, before the onset of complications, especially severe sepsis.

Sources of funding

None.

Disclosure of interest

The authors declare that they have no competing interest.

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