Full text of DOI:10.1016/S0272-6386(00)70044-8

Hospital-Acquired Infections Among Chronic Hemodialysis Patients
Erika M.C. D’Agata, MD, David B. Mount, MD, Valerie Thayer, RN, and William Schaffner, MD
● The epidemiological characteristics of nosocomial infections among patients requiring chronic hemodialysis, a
high-risk and rapidly growing population, have not been fully elucidated. During a 30-month cohort study, rates of
bloodstream infections (BSIs), urinary tract infections (UTIs), pneumonia, and diarrhea caused by Clostridium
difficile and the distribution of pathogens among hospitalized chronic hemodialysis patients were compared with
hospitalized patients not requiring chronic hemodialysis. To identify risk factors for developing a nosocomial
infection among chronic hemodialysis patients, a matched case-control study was performed. A total of 1,557
nosocomial infections were detected during 1,317 of 68,361 admissions (2%). Of these, 47 nosocomial infections
occurred in chronic hemodialysis patients during 31 of 578 admissions (5%). Nosocomial infections were signifi-
cantly more frequent among the chronic hemodialysis group (9.1/1,000 patient-days) compared with the non–
chronic hemodialysis group (3.8/1,000 patient-days; relative risk [RR], 2.4; 95% confidence interval [CI], 1.8 to 3.2;
P F 0.001). UTIs were the most common nosocomial infections among chronic hemodialysis patients, accounting
for 47% of all infections in this population. UTIs were significantly more common among chronic hemodialysis
patients (4.2/1,000 patient-days) compared with non–chronic hemodialysis patients (0.7/1,000 patient-days; RR, 6.2;
95% CI, 3.8 to 9.5; P F 0.001). Among chronic hemodialysis patients, Candida spp and enterococci were the most
common pathogens in contrast to coagulase-negative staphylococci and Staphylococcus aureus among patients
not requiring hemodialysis. Using conditional logistic regression, a greater index of comorbidity was significantly
associated with nosocomial infections among the chronic hemodialysis population (odds ratio, 3.6; 95% CI, 1.2 to
10.7; P ؍ 0.02). Chronic hemodialysis patients are at a substantially greater risk for developing a nosocomial
infection compared with other hospitalized patients.
ꢀ 2000 by the National Kidney Foundation, Inc.
INDEX WORDS: Infection; hemodialysis (HD); risk factors; hospitals; cross-infection; urinary tract infections (UTIs).
HE NUMBER OF patients with end-stage
renal disease is increasing by 9% per year.1
were compared with those of patients not under-
going hemodialysis who were hospitalized dur-
ing the same time. In addition, to identify risk
factors for nosocomial infections among chronic
hemodialysis patients, a matched case-control
study was performed.
T
Among those undergoing hemodialysis, the ma-
jority will require at least one hospitalization
every year.2 Once hospitalized, these patients
have an intrinsic susceptibility to developing an
infection as a result of numerous comorbid con-
ditions, uremic toxicity, and anemia of chronic
renal failure, all of which contribute to an immu-
nocompromised state.3-6 In addition, chronic he-
modialysis patients depend on vascular access,
which increases the risk for developing bacter-
emia, the nosocomial infection with the greatest
mortality rate.7
Nosocomial infections contribute directly to a
substantial number of hospital deaths and extra
hospital days.7 These infections have not been
extensively investigated in chronic hemodialysis
patients, even though they are a high-risk popula-
tion. To develop effective and customized preven-
tion strategies, the epidemiological characteris-
tics of nosocomial infections need to be fully
elucidated in this population.
METHODS
Patient Population
The Vanderbilt University Medical Center (Nashville,
TN) is a 663-bed tertiary-care hospital with an average of
28,000 patient discharges per year. During July 1, 1995,
through December 31, 1997, hospital-wide surveillance for
nosocomial infections was performed. Patients undergoing
hemodialysis during their hospitalization were identified by
reviewing billing records with specific Current Procedural
Terminology codes for hemodialysis (codes 90935 and
From the Department of Medicine, Division of Infectious
Diseases; and Division of Nephrology, Vanderbilt University
Medical Center, Nashville, TN.
Received September 13, 1999; accepted in revised form
January 7, 2000.
Address reprint requests to Erika M.C. D’Agata, MD,
Vanderbilt University Medical Center, Division of Infectious
Diseases, Medical Center North A-3310, 21st Ave and Gar-
land St, Nashville, TN 37232-2605. E-mail: erika.
d’agata@mcmail.vanderbilt.edu
To determine the incidence of nosocomial
infections and survey the causative pathogens, a
30-month prospective surveillance study was per-
formed on all hospitalized chronic hemodialysis
patients admitted to a tertiary-care medical cen-
ter. Results among chronic hemodialysis patients
ꢀ 2000 by the National Kidney Foundation, Inc.
0272-6386/00/3506-0010$3.00/0
doi:10.1053/ajkd.2000.7469
American Journal of Kidney Diseases, Vol 35, No 6 (June), 2000: pp 1083-1088
1083

1084
D’AGATA ET AL
90937). Demographic and clinical data were obtained by
reviewing computerized medical records. Chronic renal fail-
ure was defined as hemodialysis initiated before the current
hospital admission. Comorbid conditions were assessed by
the Charlson index.8 Patients were classified as immunocom-
promised if they were administered immunosuppressive
medications or had human immunodeficiency virus infec-
tion or a malignancy.
and controls. A P value of 0.05 or less was considered
statistically significant. All analyses were performed using
Stata 6.0 (Stata Corporation, College Station, TX).
RESULTS
Hospital-Acquired Infections
During the 30-month study period, there were
68,361 patient admissions to the hospital. Of
these, 365 patients required chronic hemodialy-
sis during 578 admissions. These chronic hemo-
dialysis patients had a mean age of 55 Ϯ 8 (SD)
years. Fifty-two percent were men, 56% were
Caucasian, and 43% had diabetes mellitus. The
most common underlying causes of kidney dis-
ease were diabetes mellitus (41%) and hyperten-
sion (31%).
A total of 1,557 nosocomial infections (pneu-
monia, BSIs, UTIs, and CD) were detected
throughout the hospital. These nosocomial infec-
tions occurred during 1,317 (2%) patient admis-
sions. Among these, 47 nosocomial infections
occurred during 31 admissions (5%) requiring
chronic hemodialysis. Thus, nosocomial infec-
tions occurred significantly more frequently dur-
ing admissions that required chronic hemodialy-
sis (31 of 578 admissions) than during admissions
that did not require hemodialysis (1,286 of 67,783
admissions; relative risk [RR] 2.9; 95% confi-
dence interval [CI], 2 to 4; P Ͻ 0.001).
Among patients undergoing chronic hemodi-
alysis, the median length of stay was 25 days
(range, 9 to 96 days) for those patients who
developed a nosocomial infection compared with
a median of 4 days (range, 1 to 76 days) for those
chronic hemodialysis patients who did not de-
velop a nosocomial infection (P Ͻ 0.001). Hospi-
tal wide, the median length of stay for all patients
was 5 days. Even after adjusting for total length
of hospital stay, nosocomial infections were sig-
nificantly more frequent among patients undergo-
ing chronic hemodialysis (9.1/1,000 patient-
days) than among patients who did not require
chronic hemodialysis (3.8/1,000 patient-days; RR,
2.4; 95% CI, 1.8 to 3.2; P Ͻ 0.001).
Surveillance of Hospital-Acquired Infections
During the study period, trained, experienced infection
control nurses performed prospective hospital-wide nosoco-
mial infection surveillance according to the standard proto-
col of the National Nosocomial Infection Surveillance (NNIS)
system of the Centers for Disease Control and Prevention
(CDC).9 Daily lists of patients with positive culture results
from any site were obtained from the clinical microbiology
laboratory. Medical charts of these patients were reviewed to
determine if a positive culture result represented contamina-
tion, colonization, or an infection. A nosocomial infection
was defined as an infection not present or incubating at the
time of hospital admission. Definitions established by the
NNIS system for site-specific nosocomial infections were
used.9
The four most common nosocomial infections occurring
among nonsurgical patients were evaluated in this study:
pneumonia, primary bloodstream infections (BSIs), urinary
tract infections (UTIs), and diarrhea caused by Clostridium
diffıcile (CD). According to the NNIS criteria, primary BSIs
included those infections related to an intravascular device.
For each documented UTI, urinary catheterization or other
instrumentation of the urinary tract during the prior 7 days
was recorded. Nosocomial infection rates among patients
undergoing chronic hemodialysis were compared with rates
among patients hospitalized during the same study period
who were not undergoing hemodialysis. Identification of
pathogens was performed by the clinical microbiology labo-
ratory, following the guidelines of the National Committee
for Clinical Laboratory Standards.10
Case-Control Study
To define the risk factors for developing a nosocomial
infection among the cohort of chronic hemodialysis patients,
a matched case-control study was performed. Cases were
defined as all chronic hemodialysis patients who developed
a nosocomial infection during the study period; controls
were selected from chronic hemodialysis patients who did
not develop a nosocomial infection. For those patients admit-
ted more than once during the study period, only the earliest
admission was included in the analysis. One control was
selected for each case. Matching criteria included year of
hospital admission and duration of hospitalization.
The specific types of nosocomial infections
according to chronic hemodialysis exposure are
listed in Table 1. Nosocomial UTIs were the
most common nosocomial infection among the
chronic hemodialysis population, accounting for
nearly half the nosocomial infections (47%).
Notably, all 22 nosocomial UTIs in the chronic
Statistical Analysis
Categorical variables were compared using chi-square or
Fischer’s exact test. Continuous variables were compared
using Student’s t-test or Wilcoxon’s rank-sum test for nonpar-
ametric distributions. Conditional logistic regression was
used to estimate the odds ratio of potential risk factors for
developing a nosocomial infection among the matched cases

NOSOCOMIAL INFECTIONS IN DIALYSIS PATIENTS
Table 1. Nosocomial Infection Rates According to Chronic Hemodialysis Exposure
No. of Infections (%) Per 1,000 Patient-Days
1085
CHD
Non-CHD
CHD
Non-CHD
Type
(n ϭ 47)
(n ϭ 1,510)
(n ϭ 5,182)
(n ϭ 398,983)
RR (95% CI)
P
Urinary tract infection
Bloodstream infection
Pneumonia
22 (47)
13 (28)
9 (19)
3 (6)
275 (18)
558 (37)
612 (41)
65 (4)
4.2
2.5
1.7
0.6
0.7
1.4
1.5
0.2
6.2 (3.8-9.5)
1.8 (1.1-3.1)
1.1 (0.5-2.2)
3.6 (0.7-11)
Ͻ0.001
0.05
0.7
Clostridium difficile diarrhea
0.07
Abbreviation: CHD, chronic hemodialysis.
hemodialysis patients were symptomatic with
fever and urinary tract symptoms. Instrumenta-
tion of the urinary tract occurred among 20
chronic hemodialysis patients with UTI (91%),
of whom 17 patients had an indwelling urinary
catheter during the prior 7 days. There was no
significant difference in the frequency of instru-
mentation of the urinary tract among the chronic
hemodialysis patients with UTIs (20 of 22 pa-
tients) compared with nonhemodialysis patients
with UTIs (237 of 275 patients; P ϭ 0.5).
Among the non–chronic hemodialysis popula-
tion, pneumonia was the most common nosoco-
mial infection (41%). BSIs were the second most
frequent nosocomial infection in both the chronic
hemodialysis and non–chronic hemodialysis
groups. Of the 13 BSIs among chronic hemodi-
alysis patients, 1 BSI was associated with an
arteriovenous fistula infection and 4 BSIs were
associated with temporary central catheter infec-
tions. CD was the least frequent nosocomial
infection in both groups.
sis. Among patients undergoing chronic hemodi-
alysis, enterococci and Candida spp were the
most common pathogens compared with coagu-
lase-negative staphylococci and Staphylococcus
aureus among patients not requiring hemodialysis.
Infections Occurring in the Intensive Care Unit
The proportion of nosocomial infections occur-
ring while patients were in the intensive care unit
(ICU) was significantly less among patients un-
dergoing chronic hemodialysis (22 of 47 pa-
tients) compared with patients not requiring he-
modialysis (1,020 of 1,510 patients; RR, 0.4;
95% CI, 0.2 to 0.7; P ϭ 0.003). BSIs and CD
occurred in the ICU significantly more often
among the nonhemodialysis group compared with
the chronic hemodialysis group (P ϭ 0.03; Fig 1).
The frequency of pathogens implicated in ICU
infections was analyzed for the four most com-
mon pathogens isolated from the chronic he-
modialysis group. Infections caused by Entero-
bacter spp occurred more frequently and
Pseudomonas aeruginosa infections less fre-
quently in the ICU among the chronic hemodialy-
sis group compared with the nonhemodialysis
group (P Ͻ 0.05). There was no statistically
significant difference in the frequency of entero-
coccal or candidal infections occurring in the
ICU between the two groups (Fig 2).
After adjusting for length of hospital stay,
UTIs and BSIs were significantly more frequent
among the chronic hemodialysis group com-
pared with the nonhemodialysis group. There
was a trend toward a greater rate of CD diarrhea
among chronic hemodialysis patients compared
with nonhemodialysis patients after adjusting for
length of hospital stay (P ϭ 0.07; Table 1).
Distribution of Nosocomial Pathogens
Case-Control Study
The most frequent bacterial pathogens recov-
ered from nosocomial infections (UTIs, BSIs,
pneumonia) according to hemodialysis exposure
are listed in Table 2. Chronic hemodialysis pa-
tients had a different distribution of bacterial
pathogens implicated in nosocomial infections
compared with patients not requiring hemodialy-
Twenty-nine patients during 31 admissions
requiring chronic hemodialysis developed at least
one nosocomial infection. These patients were
matched to 29 chronic hemodialysis patients
who did not develop a nosocomial infection. All
cases were matched to controls by year of admis-
sion. Cases were also matched to controls by

1086
D’AGATA ET AL
Table 2. Distribution of Most Common Bacterial Pathogens Isolated From Nosocomial Infections
According to Hemodialysis Exposure
Type of Infection (%)
No. of
Pathogens (%)*
Urinary Tract
Infections
Bloodstream
Infections
Pneumonia†
CHD
Non-CHD
CHD
Non-CHD
CHD
Non-CHD
CHD
Non-CHD
Pathogen
(n ϭ 48)
(n ϭ 1,702)
(n ϭ 22)
(n ϭ 314)
(n ϭ 13)
(n ϭ 661)
(n ϭ 5)
(n ϭ 412)
Enterococcus spp
Candida spp
Enterobacter spp
Pseudomonas aeru-
ginosa
6 (13)
8 (17)
6 (13)
144 (8)
90 (5)
79 (5)
2 (9)
6 (27)
3 (14)
46 (15)
42 (13)
15 (5)
4 (31)
2 (15)
2 (15)
98 (15)
48 (7)
18 (3)
0 (0)
0 (0)
1 (20)
0 (0)
59 (14)
46 (8)
5 (10)
174 (10)
4 (18)
43 (14)
1 (8)
15 (2)
0 (0)
116 (19)
Staphylococcus
aureus
Escherichia coli
Coagulase-negative
staphylococci
Other‡
3 (6)
3 (6)
201 (12)
107 (6)
0 (0)
3 (14)
8 (3)
69 (22)
1 (8)
0 (0)
65 (10)
17 (3)
2 (40)
0 (0)
128 (21)
21 (3)
1 (2)
16 (33)
245 (14)
662 (39)
0 (0)
4 (18)
4 (1)
87 (28)
1 (8)
2 (15)
241 (36)
159 (24)
0 (0)
2 (40)
0 (0)
42 (10)
Abbreviation: CHD, chronic hemodialysis.
*More than one pathogen isolated per infection.
†Pathogen not identified in all cases.
‡Two organisms or less per species in the CHD group, including Morganella spp, Klebsiella spp, Stenotrophomonas spp,
Acinetobacter spp, Citrobacter spp, Proteus spp, Aeromonas spp, Streptococcus spp, and Aspergillus spp.
DISCUSSION
total duration of hospitalization: 26 cases within
1 day and 3 cases, who remained in the hospital
greater than 40 days, within 6 days.
A 30-month prospective cohort study was per-
formed to describe the epidemiological character-
istics of four of the most common nosocomial
infections, pneumonia, BSIs, UTIs, and CD,
among chronic hemodialysis patients. The re-
sults of this study show that patients undergoing
chronic hemodialysis were at a significantly
greater risk for developing a nosocomial infec-
tion compared with patients not requiring chronic
hemodialysis and that these infections occurred
more commonly outside of the ICU setting among
Using conditional logistic regression, chronic
hemodialysis patients who developed a nosoco-
mial infection had a significantly greater index of
comorbidity, as defined by the Charlson score
(Table 3). There were no differences in patient
demographic characteristics, presence of diabe-
tes mellitus, or an immunocompromised state.
Five patients (17%) among the cases died and
one patient (3%) among the controls died (odds
ratio, 5.0; 95% CI, 0.6 to 43; P ϭ 0.1).
Fig 1. Proportion of noso-
comial infections occurring
in the ICU according to chronic
hemodialysis exposure. (N)
Chronic hemodialysis; (S)
non-chronic hemodialysis.

NOSOCOMIAL INFECTIONS IN DIALYSIS PATIENTS
1087
Fig 2. Proportion of bac-
terial pathogens implicated
in nosocomial ICU infections
according to chronic hemodi-
alyss exposure. (N) Chronic
hemodialysis; (S) non-chronic
hemodialysis.
chronic hemodialysis patients. A greater index of
comorbidity among the chronic hemodialysis
population was associated with a 3.6-fold in-
creased risk for developing a nosocomial infec-
tion, even after matching for the confounding
effects of year of hospital admission and duration
of hospitalization.
Chronic hemodialysis patients had a distinc-
tive distribution of nosocomial pathogens. The
NNIS system of the CDC has consistently re-
ported coagulase-negative staphylococci and
Escherichia coli as the major pathogens impli-
cated in BSIs and UTIs, respectively. These
findings are in agreement with the nosocomial
infections detected among the nonhemodialysis
population in this study. In contrast, among the
chronic hemodialysis population in this study,
enterococci and Candida spp were the pathogens
most commonly associated with BSIs and UTIs,
respectively. With the rapidly increasing rates of
vancomycin-resistant enterococci in the dialysis
population and the limited therapeutic options
for the treatment of these infections,11 the pre-
dominance of enterococci implicated in nosoco-
mial BSIs in this population is concerning. Fur-
thermore, among all types of nosocomial
infections, bacteremias are associated with the
greatest mortality.7 Thus, the potential for greater
mortality rates from nosocomial bacteremias in
the dialysis population needs to be considered.
Likewise, the predominance of Candida spp as
the causative pathogens for nosocomial UTIs
suggests that these infections may be associated
with greater morbidity and mortality among he-
modialysis patients compared with other hospital-
ized patients in whom gram-negative pathogens
predominate.7,12,13 The outcome of nosocomial
infections among chronic hemodialysis patients
warrants further elucidation.
The urinary tract may not be recognized as an
important source of infection among the chronic
hemodialysis population in view of the minimal
urine output in these patients. The results of this
study imply otherwise. Symptomatic UTIs were
the most common nosocomial infections among
the chronic hemodialysis patients. The diagnosis
of UTI was based on strict CDC criteria, includ-
ing the recovery of a single pathogen in concen-
trations greater than 105 colonies per milliliter
from a urine specimen, in addition to urinary
tract symptoms or fever without another source.
Therefore, positive urine culture results were
unlikely to represent bacterial overgrowth in
residual bladder urine.
Table 3. Risk Factors for Nosocomial Infections
Among Hospitalized Patients Requiring Chronic
Hemodialysis
Cases
Controls
OR
Characteristic
(n ϭ 29) (n ϭ 29)
(95% CI)
P
Mean Charlson
score
4.2
2.8
3.6 (1.2-10.7) 0.02
Age* (y)
55 Ϯ 4 52 Ϯ 3 1.0 (0.9-1.1) 0.3
Sex (men/
women)
Diabetes mel-
litus
Immunocompro-
mised state
11/18
10
7/22
6
1.4 (0.4-4.4) 0.6
2.0 (0.6-6.4) 0.2
0.4 (0.1-1.7) 0.2
These results suggest that the urinary tract is
an important source of fever and infection among
hospitalized chronic hemodialysis patients with
urine output. In this study, the majority of hemo-
5
9
Abbreviation: OR, odds ratio.
*Mean Ϯ SD.

1088
D’AGATA ET AL
4. Miller T, Ormrod D, Collins J: Host defense and
infection in dialysis patients, in Nissenson AR, Fine RN,
Gentiel DE (eds): Clinical Dialysis. East Norwalk, CT,
Appleton & Lange, 1990, pp 559-578
5. Goldblum SE, Reed WP: Host defenses and immuno-
logic alterations associated with chronic hemodialysis. Ann
Intern Med 93:597-613, 1980
dialysis patients who developed a UTI under-
went prior urinary catheterization, the major risk
factor for UTI.14 Thus, to decrease the rate of
nosocomial UTIs and ultimately improve patient
outcome, urinary catheterization in this popula-
tion should be minimized.
6. VanHolder R, Ringoir S: Polymorphonuclear cell func-
tion and infection in dialysis. Kidney Int 38:S91-S95, 1992
7. Emori TG, Ganynes RP: An overview of nosocomial
infections, including the role of the microbiology laboratory.
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8. Charlson M, Pompei P, Ales K, MacKenzie CR: A new
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9. National Nosocomial Infections Surveillance System:
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Atlanta, GA, Centers for Disease Control and Prevention,
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Yolken RH: Manual of Clinical Microbiology (ed 6). Wash-
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Effective surveillance efforts for nosocomial
infections require stratification by severity of
underlying illness and exposure to invasive de-
vices. By risk-adjusting rates of nosocomial in-
fections, valid interhospital and intrahospital com-
parisons can be performed.15-17 The optimal
method for stratification for severity of underly-
ing illness, especially in patients outside of the
ICU, is not clear. In this study, the Charlson
index was used as a measure of comorbidity.
This simple scoring system generates a compos-
ite value for age and preexisting medical condi-
tions and has been validated in the population of
end-stage renal disease.18 Among chronic hemo-
dialysis patients, those with a high score were at
significantly greater risk for acquiring a nosoco-
mial infection. Thus, future surveillance efforts
of nosocomial infections among the dialysis popu-
lation should consider using the Charlson score,
in addition to device exposure, to obtain risk-
adjusted rates of nosocomial infections.
This study underscores the importance of noso-
comial infections in the chronic hemodialysis
population. The distinctive distribution of patho-
gens suggests that nosocomial infections in this
population may be associated with greater rates
of morbidity and mortality compared with hospi-
talized patients not requiring chronic hemodialy-
sis. Because more than one third of nosocomial
infections are preventable, intense surveillance
efforts and prevention measures should focus on
this high-risk and rapidly growing population.1,19
13. Hughes WT: Systemic candidiasis: A study of 109
fatal cases. Pediatr Infect Dis 1:11-18, 1982
14. Burke JP, Riley K: Nosocomial urinary tract infec-
tions, in Mayhall G (ed): Hospital Epidemiology and Infec-
tion Control. Baltimore, MD, Williams & Wilkins, 1996, pp
139-153
15. National Nosocomial Infections Surveillance Sys-
tem: National Nosocomial Infections Surveillance System
(NNIS) report: Data summary from October 1986-April
1997. Am J Infect Control 25:477-487, 1997
16. Britt MR, Schleupner CJ, Matsumiya S: Severity of
underlying disease as a predictor of nosocomial infection.
Utility in the control of nosocomial infections. JAMA 239:
1047-1051, 1978
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