EPIBACDIAL: A Multicenter Prospective Study of Risk Factors for Bacteremia in Chronic Hemodialysis Patients’ BRUNO HOEN,* AGNES PAUL-DAUPHIN,t DOMINIQUE HESTIN, and MICHELE KESSLER *Se?1,ice de Maladies Infectieuses et Tropicales, #Sen,ice d ‘inforinatique M#{233}dicale, Epidemiologic et Statistiques, and Sen’ice de N#{233}phrologie, University of Nancy Medical Center, Vandoeut’re, France. Abstract. Baeteremic infections are a major cause of mortality and morbidity in chronic hemodialysis patients. New develop- ments in managing these patients (erythropoietin therapy. nasal mupirocin, long-term implanted catheters, and synthetic mem- branes) may have altered the epidemiologic patterns of bacte- remia in dialysis patients. This multicenter prospective cross- sectional study was carried out to determine the current incidence of and risk factors for baeteremia in chronic hemo- dialysis patients in France. A total of 988 adults on chronic hemodialysis for I mo or longer was followed up prospectively for 6 mo in 19 French dialysis units. The factors associated with the development of at least one bacteremic episode over 6 mo were determined using the multivariate Cox proportional hazards model. Staphylococcus aureus (ii = 20) and coagu- lase-negative staphylococci (ii = 15) were responsible for most of the 51 bacteremic episodes recorded. The incidence of bacteremia was 0.93 episode per 100 patient-months. Four risk factors for bacteremia were identified: (I) vascular access (catheter versus fistula: RR = 7.6: 95% CI, 3.7 to 15.6); (2) history of bacteremia (2 versus no previous episode: RR 7.3: 95% CI. 3.2 to 16.4); (3) immunosuppressive therapy (current versus no: RR = 3.0; 95% CI, I .0 to 6. 1); and (4) corpuscular hemoglobin (per 1 g/dl increment: RR 0.7: 95% CI. 0.6 to 0.9). Catheters, especially long-term implanted cath- eters, were found to be the leading risk factor of bacteremia in chronic hemodialysis patients. There was a trend toward re- currenee of bacteremia that was not associated with chronic staphylococcal nasal carriage. Synthetic membranes were not associated with a lower risk of bacteremia in this population of well dialyzed patients. but anemia linked to resistance to eryth- ropoietin appeared to be a possible risk factor for bacteremia. (J Am Soc Nephrol 9: 869-876, 1998) Bacterial infections are still a major cause of morbidity and mortality in chronic hemodialysis patients. Bacteremie infec- tions have an incidence of approximately one episode per 100 patient-months (I) and may be life-threatening in these pa- tients. Several risk factors for bacterial infections in chronic hemodialysis have been identified or suggested, including Staphylococcus aureus nasal carriage (2,3), a history of bacte- rial infection (4), the use of a central venous dialysis catheter rather than an arteriovenous fistula ( 1 .5,6), iron overload (I ,7,8), hypoalbuminemia (9). and the use of bioincompatible membranes ( 10. 11 ). A previous multivariate analysis identified three parameters as significant and independent risk factors for bacterial infection in chronic hemodialysis (4). These were a history of bacterial infection (at least one previous bacterial infection), the type of vascular access (catheter versus native fistula), and elevated serum ferritin (>500 p.g/L). Since that study was conducted, new developments in the management of dialysis patients have included the widespread use of recom- Received July 9. 1997. Accepted October 8. 1997. “See Appendix for participating centers and laboratories. Correspondence to Dr. Bruno Hoen. Service de Maladies lnfectieuses et Tropicales. University of Besan#{231}on Medical Center. F-25030 Besancon Cedex. France. b046-6673/0905-0869$03.0()/() Journal of the American Society of Nephrology Copyright iD 1998 by the American Society of Nephrology binant erythropoietin and nasal mupirocin ointments. New dialysis techniques also have been implemented. such as the use of long-term dialysis catheters and synthetic-presumably more biocompatible-membranes. This investigation was con- dueted to assess the influence of these changes on the epide- miobogie patterns of bacteremia in chronic hemodialysis pa- tients. Materials and Methods Study Design A prospective survey of all patients undergoing chronic hemodial- ysis in hospital dialysis centers or in self-care dialysis units was conducted in 19 French dialysis units. Patients undergoing dialysis at home were excluded. All adult patients who were on a regular hemodialysis program for more than 30 d on September 1 , I 994, were included in the study. All patients were followed for 6 mo. unless follow-up was censored by renal transplantation. the patient’s moving to a dialysis center not participating in the study, switch to peritoneal dialysis. or death. The patients physicians were asked not to change the patient’s dialyzer throughout the study period. and to do only minimal changes in other dialysis procedures. such as number and duration of dialysis sessions. They also were asked to take at least two blood cultures. to swab the vascular access (either the needle puncture site of fistulas or the exit site of catheters. over a I -cm2 skin area) and the patient’s nostrils for Staphylococcus aureu.s in anyone suspected of developing a bacteremic infection (fever, signs of inflammation at the vascular access site). The coordinating investigators were notified of all confirmed diagnoses of bacterensia. The microbiobogists from
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EPIBACDIAL: A Multicenter Prospective Study of Risk
Factors for Bacteremia in Chronic Hemodialysis Patients�’
BRUNO HOEN,* AGNES PAUL-DAUPHIN,t DOMINIQUE HESTIN,� and
MICHELE KESSLER�*Se?1,ice de Maladies Infectieuses et Tropicales, #Sen,ice d ‘inforinatique M#{233}dicale, Epidemiologic et
Statistiques, and �Sen’ice de N#{233}phrologie, University of Nancy Medical Center, Vandoeut’re, France.
Abstract. Baeteremic infections are a major cause of mortality
and morbidity in chronic hemodialysis patients. New develop-
ments in managing these patients (erythropoietin therapy. nasal
mupirocin, long-term implanted catheters, and synthetic mem-
branes) may have altered the epidemiologic patterns of bacte-
remia in dialysis patients. This multicenter prospective cross-
sectional study was carried out to determine the current
incidence of and risk factors for baeteremia in chronic hemo-
dialysis patients in France. A total of 988 adults on chronic
hemodialysis for I mo or longer was followed up prospectively
for 6 mo in 19 French dialysis units. The factors associated
with the development of at least one bacteremic episode over
6 mo were determined using the multivariate Cox proportional
hazards model. Staphylococcus aureus (ii = 20) and coagu-
lase-negative staphylococci (ii = 15) were responsible for most
of the 5 1 bacteremic episodes recorded. The incidence of
bacteremia was 0.93 episode per 100 patient-months. Four risk
factors for bacteremia were identified: (I) vascular access
(catheter versus fistula: RR = 7.6: 95% CI, 3.7 to 15.6); (2)
history of bacteremia (�2 versus no previous episode: RR
7.3: 95% CI. 3.2 to 16.4); (3) immunosuppressive therapy
(current versus no: RR = 3.0; 95% CI, I .0 to 6. 1); and (4)
three parameters as significant and independent risk factors for
bacterial infection in chronic hemodialysis (4). These were a
history of bacterial infection (at least one previous bacterial
infection), the type of vascular access (catheter versus native
fistula), and elevated serum ferritin (>500 p.g/L). Since that
study was conducted, new developments in the management of
dialysis patients have included the widespread use of recom-
Received July 9. 1997. Accepted October 8. 1997.
“See Appendix for participating centers and laboratories.Correspondence to Dr. Bruno Hoen. Service de Maladies lnfectieuses et
Tropicales. University of Besan#{231}onMedical Center. F-25030 Besancon Cedex.France.
b046-6673/0905-0869$03.0()/()
Journal of the American Society of Nephrology
Copyright iD 1998 by the American Society of Nephrology
binant erythropoietin and nasal mupirocin ointments. New
dialysis techniques also have been implemented. such as the
use of long-term dialysis catheters and synthetic-presumably
more biocompatible-membranes. This investigation was con-
dueted to assess the influence of these changes on the epide-
miobogie patterns of bacteremia in chronic hemodialysis pa-
tients.
Materials and MethodsStudy Design
A prospective survey of all patients undergoing chronic hemodial-
ysis in hospital dialysis centers or in self-care dialysis units was
conducted in 19 French dialysis units. Patients undergoing dialysis at
home were excluded. All adult patients who were on a regular
hemodialysis program for more than 30 d on September 1 , I994, wereincluded in the study. All patients were followed for 6 mo. unless
follow-up was censored by renal transplantation. the patient’s moving
to a dialysis center not participating in the study, switch to peritoneal
dialysis. or death. The patients� physicians were asked not to change
the patient’s dialyzer throughout the study period. and to do only
minimal changes in other dialysis procedures. such as number and
duration of dialysis sessions. They also were asked to take at least two
blood cultures. to swab the vascular access (either the needle puncture
site of fistulas or the exit site of catheters. over a I -cm2 skin area) and
the patient’s nostrils for Staphylococcus aureu.s in anyone suspected
of developing a bacteremic infection (fever, signs of inflammation at
the vascular access site). The coordinating investigators were notified
of all confirmed diagnoses of bacterensia. The microbiobogists from
870 Journal of the American Society of Nephrology
the laboratory affiliated with each dialysis unit were also asked to
notify the coordinators of all positive blood cultures originating from
the dialysis unit. All notification forms were examined by the coor-
dinating investigators, who classified each ease according to the
following definitions.
Case Definitions
Only bacteremie episodes were considered. If a single blood culturewas positive for coagulase-negative staphylococci, Corvnebacteria, or
Bacillus sp., the culture was considered contaminated or representa-
tive of a transient bacteremia but not of a bacteremie episode. All
other situations in patients in whom at least one blood culture was
positive were defined as bacteremie episodes. Patients who developed
such a bacteremie episode within I mo before the start of the study
were not considered for incidence calculation and risk factor analysis.
Data Collection
The following data were recorded for each patient enrolled in the
study, at the time of inclusion, in September 1994: birth date: gender;
cause of renal failure; comorbid factors: date of start of dialysis;
history of bacteremia, kidney transplantation or peritoneal dialysis;previous and current erythropoietin treatment; current immunosup-pressive therapy; any iron supplementation, desfemoxamine treat-
ment, or nasal mupirocin ointments within the past 6 mo; results of
nasal swab culture; surgical procedures within the past month; and
history of blood transfusions and dialysis procedures (number ofdialysis sessions per week, duration of each session, dialysis mem-
brane, vascular access). Dialysis membrane types were listed assynthetic (polysulfone. AN69#{174},and pobymethylmethacrylate) or eel-
lubosic (hemophane, Cuprophane, and cellulose acetate). Baseline
laboratory data included serum protein, albumin, ferritin, and C-reac-tive protein levels, corpuscular hemoglobin. and blood urea nitrogen
concentrations before and after dialysis. Samples for blood ureanitrogen were taken immediately before the start of dialysis and at the
end of the session, after reducing the blood pump rate to 50 ml/min.
The post/predialysis plasma urea nitrogen ratio (R) was used to
calculate the urea reduction rate (URR = I - R) and to estimate KtIV,
from the formula: KtJV = - 1.18 X ln(R) ( I 2).
When a bacteremie episode was diagnosed, the patient’s attending
physician filled out a case record form that included: the date of firstpositive blood culture; the number of blood cultures performed and
number of positive blood cultures; identification of the micro-organ-
isms recovered from blood cultures; vascular access and nasal swabs;
possible administrations of nasal mupiroein ointments; and changes in
dialysis procedures between the beginning of the study and the onset
of the baeteremic episode.
The data collected at the end of the study period included the
number of bacteremic episodes, the number and type of any surgical
procedures, changes in vascular access and dialysis procedures. and
any changes in supportive therapy (erythropoietin, iron supplementa-
tion, desferrioxamine, blood transfusion, nasal mupirocin) since the
beginning of the study. The same laboratory data as those recorded atinclusion were also checked. The date of patient death, renal trans-
plantation, or moving was also recorded.All of the data were entered into a computerized database (Dbase
IV#{174})by two independent operators. The two database files were then
automatically compared, and all discrepancies were checked andcorrected.
Bacteriologic Techniques
The swab samples taken from the patients’ nostrils were inoculated
onto Columbia and Chapman agar plates and incubated for 48 h.
Plates were then evaluated for the presence of Staphylococcus aureus.
The plates inoculated with the swabs taken from the patients’ vascular
access sites were evaluated for the presence of any bacteria. Blood
cultures were performed using each center’s standard techniques.
Patients
A total of 988 adult patients (597 men and 391 women; mean age,
60 yr; range, 16 to 88 yr) was enrolled. Most patients (is = 839. 85%)
attended hospital dialysis centers, and 149 (15%) were treated inself-care units. The causes of renal failure were chronic gbomerubo-
nephritis (n = 223), angioselerosis (a = 176), chronic interstitial
Bellasea JP, Revert L, Gatell JM: Infection of hemodialysis
catheters: Incidence and mechanisms. Am J Nephrol 9: 454-459,
I 989
7. Boelaert JR. Daneels RF, Sehurgers ML, Matthys EG. GordtsBZ, Van Landuyt HW: Iron overload in haemodialysis patientsincreases the risk of baeteraemia: A prospective study. Nephrol