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Changing Profile of Infective Endocarditis
Results of a 1-Year Survey in France
Bruno Hoen, MD;
François Alla, MD;
Christine Selton-Suty, MD;
Isabelle Béguinot, MD;
Anne Bouvet, MD;
Serge Briançon, MD;
Jean-Paul Casalta, MD;
Nicolas Danchin, MD;
François Delahaye, MD;
Jerome Etienne, MD;
Vincent Le Moing, MD;
Catherine Leport, MD;
Jean-Luc Mainardi, MD;
Raymond Ruimy, MD;
François Vandenesch, MD;
for the Association pour l'Etude et la Prévention de l'Endocardite
Infectieuse (AEPEI) Study Group
JAMA. 2002;288:75-81.
ABSTRACT
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Context Since the first modern clinical description of infective endocarditis
(IE) at the end of the 19th century, the profile of the disease has evolved
continuously, as highlighted in epidemiological studies including a French
survey performed in 1991.
Objective To update information gained from the 1991 study on the epidemiology
of IE in France.
Design and Setting Population-based survey conducted from January through December 1999
in all hospitals in 6 French regions representing 26% of the population (16
million inhabitants).
Patients Three hundred ninety adult inpatients diagnosed with IE according to
Duke criteria.
Main Outcome Measures Incidence of IE; proportion of patients with underlying heart disease;
clinical characteristics; causative microorganisms; surgical and mortality
outcomes.
Results The annual age- and sex-standardized incidence was 31 (95% confidence
interval [CI], 28-35) cases per million, not including the region of New Caledonia,
which had 161 (95% CI, 117-216) cases per million. There was no previously
known heart disease in 47% of the cases. The proportion of prosthetic-valve
IE was 16%. Causative microorganisms were: streptococci, 48% (group D streptococci,
25%; oral streptococci, 17%, pyogenic streptococci, 6%); enterococci, 8%; Abiotrophia species, 2%; staphylococci, 29%; and other
or multiple pathogens, 8%. Blood cultures were negative in 9% and no microorganism
was identified in 5% of the cases. Early valve surgery was performed in 49%
of the patients. In-hospital mortality was 16%. Compared with 1991, this study
showed a decreased incidence of IE in patients with previously known underlying
heart disease (20.6 cases per million vs 15.1 cases per million; P<.001); a smaller incidence of oral streptococcal IE (7.8 cases
per million vs 5.1 cases per million; P<.001),
compensated by a larger proportion of IE due to group D streptococci (5.3
cases per million vs 6.2 cases per million; P = .67)
and staphylococci (4.9 cases per million vs 5.7 cases per million; P = .97); an increased rate of early valve surgery (31.2% vs 49.7%; P<.001); and a decreased in-hospital mortality rate
(21.6% vs 16.6%; P = .08).
Conclusion Although the incidence of IE has not changed, important changes in disease
characteristics, treatment, and outcomes were noted.
INTRODUCTION
Recent studies have shown that the annual incidence of infective endocarditis
(IE) is stable between 15 and 60 cases per million.1-4
However, since the first modern clinical description of IE by Osler,5 the profile of the disease has continuously evolved.
This fact was highlighted in different epidemiological studies,6-7
including a French survey of IE performed in 1991, in which the main results,
compared with a similar study conducted in 1983,8
showed (1) stable annual incidence at 24 cases per million; (2) increased
age of onset; (3) decreasing proportion of IE on abnormal native valve, compensated
by an increased proportion of prosthetic valve IE and native valve IE in patients
with previously unrecognized predisposing conditions; and (4) a changing microbiologic
profile, with an increased proportion of group D streptococci and staphylococci.1, 9
To update the description of epidemiological, clinical, microbiologic,
and outcome characteristics of IE in France, the same group who had conducted
the 1991 survey carried out a new survey.
METHODS
This population-based study was conducted prospectively in 1999 in 6
French regions: Ile de France, Lorraine, Rhône-Alpes, Franche-Comté,
Marne, and New Caledonia. The first 3 had taken part in the previous study.
The population of the 6 regions (16 million inhabitants) comprises 26% of
the French population. Only those patients with a first hospitalization between
January 1, 1999, and December 31, 1999, were included in this analysis.
The study was distributed by mail to all physicians working in hospitals
of these regions who were either likely to take care of patients with IE (ie,
specialists in infectious diseases, intensive care, internal medicine, cardiology,
and cardiac surgery) or were echocardiographers or microbiologists. Physicians
were asked to fax a notification form to the study coordinating center for
each suspected case of IE. They were reminded of this study on a regular basis
by mail. For each patient older than 18 years and living in one of the study
regions, specific case report forms were sent to both the attending physician
and the microbiologist.
On the clinical report form, the following information was collected:
sex, date of birth, place of residence, date of first hospitalization, transfer
from or to another facility, history of heart disease, procedures and situations
at risk for IE, comorbidities, clinical signs and symptoms, laboratory and
imaging examinations, echocardiographic data, microbiological data, medical
and surgical treatment, and outcome. Investigators were provided with standard
definitions of all variables. For quantitative parameters, the physicians
were asked to provide the maximal or highest value recorded during the course
of the disease. Location of IE was determined according to echocardiographic
and/or surgical findings. Patients were informed of the study but did not
need to give consent.
Microbiologists were asked to fill out a form that included information
on the identification and susceptibility of causative microorganism (total
number and number of positive blood cultures, results of valve cultures, and
serological tests) and to send the isolated strains to a single centralized
core laboratory (Laboratoire de Bactériologie, Centre Hospitalier Universitaire
Bichat-Claude Bernard, Paris). Identification of streptococci and staphylococci
was subsequently confirmed by the Centre National de Référence
des Streptocoques (Paris) and the Centre National de Référence
des Toxémies à Staphylocoques (Lyon), respectively. In addition,
for patients whose first blood cultures remained negative, attending physicians
were asked to complete specific analyses including additional sets of blood
cultures on enriched media and serological tests for Coxiella
burnetii, Bartonella species, chlamydiae,
and Legionella, which were performed in national
reference laboratories (Centre National de Référence des Rickettsies
[Marseilles] and the Centre National de Référence des Legionella
[Lyon]), and for Brucella, Mycoplasma
pneumoniae, Candida, and Aspergillus. Results of all serological tests were validated by an
expert microbiologist (F.V.) according to previously published recommendations.10
Once completed, all case report forms were checked and validated by
2 expert investigators who had not been involved in the care of the corresponding
case. These investigators were responsible for validating the diagnosis according
to the Duke criteria.11 Only definite cases
of IE were included in the study. This study was approved by the institutional
review board of the Centre Hospitalier Universitaire de Besançon.
Incidence rates, expressed as number of cases per million inhabitants,
were calculated by dividing the number of cases recorded within the study
year by the number of persons residing in the study regions and aged 15 years
or older. Population references were obtained for France and New Caledonia
from the 199912 and 199613
censuses, respectively. Results of this survey were compared with those of
the 1991 survey within the 3 areas that were common to both studies in terms
of crude and standardized incidences, group-specific incidences (underlying
heart disease, causative microorganism), surgical treatment, and mortality
rates. Comparison was restricted to patients older than 18 years and fulfilling
the Beth Israel criteria modified with echocardiography for definite, probable,
or possible endocarditis.1 The latter were
used because the Duke criteria were not available in 1991 and could not be
applied retrospectively. In both periods, incidence was standardized to the
sex-by-age distribution of the 1990 French population.14
The method described by Fay and Feuer15 was
used for calculation and comparison of 95% confidence intervals (CIs) of standardized
incidence rates.
Quantitative variables are expressed as their mean (SD) with 95% CIs
or median (interquartile range). Qualitative variables are expressed as percentages.
For intergroup comparison, we used ad hoc methods (1-way analysis of variance,
Pearson  2 test). All statistical analyses were performed using
SAS version 8.02 software (SAS Institute Inc, Cary, NC) and .05 was the level
of significance.
RESULTS
A total of 925 notifications led to the identification of 819 patients
with a putative diagnosis of IE. Among these, 429 were excluded for the following
reasons: hospitalization outside the study period (n = 178); living outside
the study regions (n = 131); failure to fulfill Duke criteria (n = 106); case
report form not returned (n = 11); and younger than 18 years (n = 3). The
present report is based on the remaining 390 eligible cases of definite IE.
There were 277 men and 113 women with a mean (SD) age of 59.5 (17.2) years
(range, 16-95 years).
Incidence
The crude annual incidence of IE was 30 (95% CI, 27-33) cases per million
population. The age- and sex-standardized annual incidence was 31 (95% CI,
28-35) cases per million for France not including New Caledonia, and 161 (95%
CI, 117-216) for New Caledonia (mean, 44; 95% CI, 39-50 in men and mean, 17;
95% CI, 14-20 in women). Incidence increased dramatically in patients older
than 50 years and peaked at 145 cases per million in men between 70 and 80
years (Figure 1).
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Figure. Incidence of Infective Endocarditis
by Age and Sex in the Study Population
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Underlying Heart Disease
The distribution of underlying heart disease is summarized in Table 1. Of note, 185 patients (47%) had
no previously known heart disease. Thirty-five patients (9%) had a history
of prior IE (mean [SD] time interval between the 2 episodes, 7.5 [4.0] years;
range, 0-60 years). Twenty-eight patients (7%) had a pacemaker; 12 of these
also had valvular disease, 10 of whom developed left-sided IE without pacemaker
involvement. Among the 63 patients who had prosthetic valves, 10 had 2 prostheses.
Of the 73 prosthetic valves, 33 were mechanical and 40 were biological.
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Table 1. Distribution of Underlying Heart
Disease in Patients (N = 390) With Infective Endocarditis
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Characteristics of IE
Location and Echocardiographic Data
Table 2 summarizes the distribution
of the different IE locations. A major echocardiographic criterion was present
in 355 cases (91%), including 336 cases with vegetations (86%), 66 cases with
an abscess (17%), and 15 cases of prosthesis dehiscence (24% of the patients
with valvular prosthesis). Ninety percent of the patients underwent both transthoracic
and transesophageal echocardiography. The remaining 10% had only transthoracic
echocardiography.
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Table 2. Location of Infective Endocarditis
(IE) in Patients (N = 390)
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Clinical and Laboratory Findings
Fever was nearly universal (355/387, 92%) (missing data for 3 cases)
while septic shock was reported in 9% of patients (32/371, missing data for
19 cases). Severe congestive heart failure was quite common (34%), with only
over one third requiring diuretic therapy (36%). Ten of 355 patients (3%)
had a Glasgow Coma Scale score of 8 or lower during the course of the disease.
Serum creatinine level was greater than 2.04 mg/dL (>180 µmol/L) at
least once in 102 patients (27%).
At least 1 vascular phenomenon (systemic arterial embolism, 126; septic
pulmonary infarct, 43; intracranial hemorrhage, 9; mycotic aneurysm, 12; or
Janeway lesion, 9) occurred in 172 patients (44%). Distribution of systemic
arterial emboli was as follows: central nervous system, 60 (48%); limbs, 38
(30%); liver, 4 (3%); spleen, 40 (32%); kidney, 8 (6%); coronary, 8 (6%);
and others not specified, 16 (13%). Central nervous system emboli were recorded
in 24 (21%) of mitral valve IE, 20 (15%) of aortic valve IE, and 10 (18%)
of combined aortic and mitral IE cases. Immunologic manifestations were observed
in 104 patients (27%) and included glomerulonephritis, 43 (41%); Osler nodes,
17 (16%); Roth spots, 5 (5%); and rheumatoid factor, 53 (51%). At least 1
extracardiac phenomenon was present in 78% of the right-sided IE cases (mainly
pulmonary embolism, 68%) and in 52% of left-sided IE cases.
Procedures and Situations at Risk
A total of 143 patients (37%) had experienced a medical or surgical
procedure (n = 49) and/or a situation at risk of bacteremia (n = 107) within
the month prior to hospitalization. Portals of entry were dental (poor dental
condition or dental procedure, n = 34), cutaneous (n = 76), and miscellaneous
other conditions (n = 46). Cutaneous portals of entry included traumatic or
chronic wounds (n = 23), intravenous drug use (n = 22), and percutaneous iatrogenic
procedure (n = 31). The latter were distributed as follows: chronic hemodialysis,
13; indwelling catheters, 11; pacemakers, 5; and percutaneous balloon valvuloplasty,
2.
Causative Microorganisms
The median (interquartile range) number of blood cultures drawn was
5 (3-7); positive blood cultures was 4 (3-6) and the mean proportion of positive
blood cultures was 78%. Blood cultures remained negative in 9% of the cases.
Overall, streptococci remained the most common causative agent of IE. The
distribution of causative microorganisms is displayed in Table 3. Group D streptococci and Staphylococcus
aureus accounted for a quarter of the cases each, whereas oral streptococci
were responsible for less than 20% of the cases. Nosocomial and/or iatrogenic
IE were more often due to staphylococci than were community-acquired IE (17/49
[35%] vs 73/341 [21%]; P = .04).
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Table 3. Distribution of Causative Microorganisms
in Patients (N = 390) With Infective Endocarditis
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Table 4 shows a comparison
of patient characteristics across the 3 main groups of microorganisms. Ages
were significantly different within the 3 groups, group D streptococci IE
patients being older and IE patients with S aureus
being younger. Patients with group D streptococci and S
aureus IE had less known underlying valve disease. Patients with S aureus IE had a higher mortality rate and a lower surgery
rate.
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Table 4. Comparison of Main Characteristics
of Infective Endocarditis (IE) Across the 3 Main Groups of Causative Microorganisms*
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The causative microorganisms were identified by blood culture in 356
patients (91%) and by other methods in 15 additional patients (4%) (6 cultures
of valve or pacemaker leads, 8 serological tests, 1 16S ribosomal RNA gene
amplification that led to the identification of Staphylococcus
cohnii in a peripheral embolus). No microorganism could be identified
in 19 patients (5%), 12 of whom received antibiotic treatment prior to blood
samplings. Two or more microorganisms were identified concomitantly in 13
patients.
Outcome
Mean (SD) duration of hospital stay was 47 (33) days (range, 0-268;
median [interquartile range], 42 [28-59] days). During this period, 191 patients
(49%) underwent valve surgery after a median (interquartile range) 21 (9-37)
days after admission. The diagnosis of IE was confirmed by macroscopic, histological,
or bacteriologic findings in 179 of the 191 operated patients (94%). In the
remaining 12 patients, gross anatomic examination was not conclusive, histological
examination was not performed in 11 cases, and bacteriologic examination was
negative in 9. Sixteen patients (4%) underwent pacemaker lead removal (thoracotomy,
12; percutaneous removal, 4). Sixty-two patients died, which accounted for
a 16% in-hospital mortality rate. The surgery and mortality rates according
to various conditions are displayed in Table 5.
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Table 5. Surgery and Mortality During the
Initial Hospital Stay as a Function of Different Variables in Patients (N
= 390) With Infective Endocarditis*
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Comparison With the 1991 Study
Compared characteristics of IE in the 2 study periods are displayed
in Table 6.15-16
The overall crude incidence of IE has not changed over time. However, the
standardized incidence of IE has decreased in patients with previously known
heart disease and in patients with prosthetic valves. The incidence of IE
due to oral streptococci has decreased while it has remained stable for group
D streptococci and S aureus. The rate of surgical
treatment has significantly increased and the mortality rate tended to decrease.
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Table 6. Comparison Between the Results of
1991 and 1999 Surveys for Characteristics of Infective Endocarditis (IE) in
Patients With Definite or Possible IE According to Modified Beth Israel Criteria
and Who Were Living in 1 of the 3 Regions That Were Common to Both Studies*
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COMMENT
The annual IE incidence rate of 31 cases per million found in this study
is in the range of those from other recent studies (ie, comprised between
15 and 60 cases per million).1-4
Only 1 recent study has shown a dramatically higher annual incidence rate
of 116 per million,17 which was partially explained
by a high proportion associated with intravenous drug use. By contrast, only
6% of patients in our population were intravenous drug users. The high incidence
of IE observed in New Caledonia can be explained by the persistence of rheumatic
fever and the low socioeconomic status.18
One major strength of our study is the low influence of referral bias,
compared with most previous studies, which are mainly based on series collected
in a single tertiary-care center. It is well known that the clinical features
of IE substantially differ between patients from referral centers and those
seen in primary-care centers.19 In the present
study, the 390 cases were reported by 193 physicians from 91 unselected medical
facilities.
Underreporting is a potential limitation that relies on physicians reporting
and not on active search of cases by investigators. In our study, underreporting
was minimized in that we relied on 3 separate sources of notification (physicians,
echocardiographists, and microbiologists) that were relatively independent,
though not completely, of one another. In addition, the proportion of case
report forms that were not returned was as low as 1.3% (11 of 819). Finally,
the proportion of patients living within 1 of the study regions and treated
for IE in hospitals outside these regions was lower than 5% by analysis of
the 1999 French national database file of diagnosis related groups at hospitalization
discharge.20
Some of our findings depict "classic" features of IE including predominance
of men and prevalence in the elderly. In contrast, we recorded several new
trends: (1) an increasing percentage of IE in patients with no previously
known heart disease; (2) important changes in the distribution of causative
microorganisms; (3) an increase of performance valve surgery during the initial
hospitalization; and (4) a trend toward decreased in-hospital mortality.
The proportion of IE patients without previously known cardiac disease
increased from 34% in 1991 to 47% in 1999. This resulted mainly from a significantly
decreased incidence of IE in patients with previously known valve disease,
especially those with prosthetic valves. This trend was also evidenced by
Tornos et al.21 In their study of native valve
IE in nonaddicts, the proportion of patients with no previously known heart
disease significantly increased from 22% in the 1975-1983 period to 46% in
the 1984-1992 period. These figures can be interpreted in several ways, including
the dramatic decrease of postrheumatic fever valvular complications, the improved
practice of antibiotic prophylaxis in patients with valve disease, and an
underrecognition of degenerative valve lesions in elderly patients.22
We observed major changes in the distribution of causative microorganisms.
The proportion of group D streptococci markedly increased from 14% in 1991
to 25% in 1999. However, this almost 2-fold increase of group D streptococcal
IE is explained less by an increased incidence of group D streptococcal IE
than by a sharp decrease in the incidence of oral streptococcal IE (Table 6). Altogether, the decreased incidence
of IE in patients with known valvular disease as well as the decreased incidence
of IE due to oral streptococci may have resulted from improved dental hygiene
and prophylaxis in at-risk patients, although our study was not equipped to
determine the veracity of this.
Another trend observed in this study as well as in others21, 23
was the increased proportion of staphylococci, both S aureus and coagulase-negative staphylococci. This can neither be attributed
to an overrepresentation of intravenous drug users nor to prosthetic valve
endocarditis since only 13% of S aureus IE occurred
in patients with prosthetic valves, whereas this percentage was 18% in IE
caused by oral streptococci (Table 4).
By contrast, 15% of all cases of staphylococcal IE had a nosocomial or iatrogenic
origin. We also showed that nosocomial or iatrogenic IE were more often due
to staphylococci than were community-acquired IE. In a recent study, hospital-acquired
IE not related to cardiac surgery represented about 10% of a series of 248
cases of IE.24 In 2 recent series of nosocomial
IE, staphylococci were responsible for about 80% of the cases, with a S aureus coagulase-negative staphylococci ratio of about
3:1.25-26
Compared with the 1991 survey, this study also showed important changes
in terms of outcome and prognosis. Overall in-hospital mortality rate decreased
from 21.6% to 16.6%, although the percentage of early surgical treatment increased
from 31.2% to 49.7%. As expected, patients with aortic valve IE were operated
on more often than patients with IE in other locations. By contrast, staphylococcal
IE, which is usually regarded as more destructive and requiring more aggressive
and earlier surgical treatment, was found to be operated on less frequently
than enterococcal and streptococcal IE. Although not fully understood, this
trend has also been found in other recent studies.27-28
Improvement of outcome may result to a large extent from improved surgical
management, as emphasized by Tornos et al21
who showed a decreased overall mortality rate from 19% in 1975-1983 to 12%
in 1984-1992 concurrently with a significantly decreased surgical mortality
rate from 43% to 18%. They attributed this reduction in surgical mortality
rate to better timing of surgery in cases of IE complicated with congestive
heart failure. We also showed a significantly lower mortality rate in operated
patients compared with those treated only medically. Even if some of the most
severely ill patients may have been denied surgery, these results do support
early surgical treatment of IE, especially in patients who do not improve
satisfactorily under medical treatment alone, as previously advocated.29
Infective endocarditis has long been described as a disease with polymorphic
manifestations.30 This study contributes to
reminding physicians that while its incidence has not decreased, its clinical
and microbiologic profile is changing continuously and rapidly. This emphasizes
the need for close epidemiological surveillance of this disease.
AUTHOR INFORMATION
Author Contributions: Study
concept and design: Hoen, Alla, Béguinot, Bouvet, Selton-Suty,
Briançon, Danchin, Delahaye, Etienne, Le Moing, Leport, Mainardi, Vandenesch.
Acquisition of data: Hoen, Alla, Selton-Suty,
Béguinot, Bouvet, Casalta, Delahaye, Le Moing, Leport, Mainardi, Ruimy.
Analysis and interpretation of data: Hoen,
Alla, Selton-Suty, Béguinot, Bouvet, Briançon, Delahaye, Le
Moing, Leport, Mainardi, Vandenesch.
Drafting of the manuscript: Hoen, Alla, Selton-Suty,
Béguinot, Delahaye, Ruimy.
Critical revision of the manuscript for important
intellectual content: Hoen, Alla, Selton-Suty, Béguinot, Bouvet,
Briançon, Casalta, Danchin, Delahaye, Etienne, Le Moing, Leport, Mainardi,
Vandenesch.
Statistical expertise: Alla, Briançon.
Obtained funding: Hoen, Leport, Ruimy.
Administrative, technical, or material support:
Hoen, Alla, Briançon, Casalta, Danchin, Delahaye, Le Moing, Mainardi.
Study supervision: Hoen, Briançon, Danchin,
Delahaye, Etienne, Leport.
The Association pour l'Etude et la Prévention
de l'Endocardite Infectieuse (AEPEI) Study Group: Steering committee: B. Hoen and C. Leport (principal investigators),
S. Briançon, N. Danchin, F. Delahaye, and J. Etienne (co-investigators). Writing committee: F. Alla, I. Béguinot, F. Delahaye,
B. Hoen (coordinating author), R. Ruimy, and C. Selton-Suty. Region study coordinating investigators: Y. Bernard, F. Duchêne,
and P. Plésiat (Franche-Comté); F. Alla, T. Doco-Lecompte, and
M. Weber (Lorraine); I. Béguinot, P. Nazeyrollas, and V. Vernet (Marne);
B. Garin, F. Lacassin, and J. Robert (New Caledonia); A. Andremont, E. Garbarz,
V. Le Moing, J.L. Mainardi, and R. Ruimy (Paris and Ile-de-France); C. Chidiac
and F. Vandenesch (Rhône-Alpes). Other members:
A. Bouvet, P. Bruneval, X. Duval, V. Goulet, R. Roudaut, R. Salamon, and J.
Texier-Maugein. Clinical research assistants: S.
Boucherit, Y. Bourezane, W. Nouioua, and D. Renaud. Centre
National de Référence des Streptocoques: A. Bouvet, G.
Collobert, B. Merad, and L. Schlegel. Centre National de
Référence des Toxémies à Staphylocoques:
M. Bes, J. Etienne, and F. Vandenesch. Centre National de
Référence des Legionella: J. Etienne, S. Jarraud, and
M. Reyrolle. Centre National de Référence
des Rickettsies: J.P. Casalta and D. Raoult.
Funding/Support: This work was funded by the
Programme Hospitalier de Recherche Clinique (grant PHRC 1997 – RC30),
the Fédération Française de Cardiologie, and the Aventis
and GlaxoSmithKline Laboratories, France. This work was supported by the following
professional organizations: Association des Professeurs de Pathologie Infectieuse
et Tropicale, Société de Pathologie Infectieuse de Langue Française,
Société Française de Microbiologie, Société
Nationale Française de Médecine Interne, Société
de Réanimation de Langue Française, Société Française
de Gérontologie, Société Française de Cardiologie,
Société Française de Chirurgie Thoracique et Cardiovasculaire,
Société Française d'Anesthésie-Réanimation,
Ligue Française pour la Prévention des Maladies Infectieuses,
and the Fédération Française de Cardiologie.
Acknowledgment: We are fully indebted to the
physicians and microbiologists who participated in this survey. We acknowledge
the contribution of Flore Lacassin, MD, who coordinated the study in New Caledonia.
We also thank Sandrine Cordier and Charline Audren for their secretarial assistance,
and Alaine Perrott and Jacqueline Zevnick for reviewing the manuscript.
Corresponding Author and Reprints: Bruno
Hoen, MD, Service de Maladies Infectieuses et Tropicales, University of Besançon
Medical Center, F-25030 Besançon Cedex, France (e-mail: bruno.hoen{at}ufc-chu.univ-fcomte.fr).
Author Affiliations: Centre Hospitalier Universitaire
de Besançon, Besançon (Dr Hoen), Centre Hospitalier Universitaire
de Nancy, Nancy (Drs Alla, Selton-Suty, and Briançon), Centre Hospitalier
Universitaire de Reims, Reims (Dr Béguinot), Centre National de Référence
des Streptocoques, Hôtel Dieu, Université Paris VI (Dr Bouvet),
Centre National de Référence des Rickettsies, Marseille (Dr
Casalta), Hôpital Européen Georges Pompidou, Paris (Drs Danchin
and Mainardi), Hôpital Louis Pradel, Lyon (Drs Delahaye and Vandenesch),
Centre National de Référence des Staphylocoques, Lyon (Drs Etienne
and Vandenesch), Centre Hospitalier Universitaire Bichat-Claude Bernard, Paris
(Drs Le Moing, Leport, and Ruimy), France.
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