MAJOR ARTICLE

Burden of Infection in Patients with End-Stage

Renal Disease Requiring Long-Term Dialysis
Steven J. Berman,1,2 E. William Johnson,2 Curtis Nakatsu,2 Michael Alkan,3 Randi Chen,1 and Jean LeDuc1
1
Department of Infection Control and Epidemiology and Renal Institute of the Pacific, St. Francis Health Care Systems of Hawaii,
and 2Department of Medicine, John A. Burns School of Medicine, Honolulu, Hawaii; and 3Ben-Gurion University Center for Health Sciences,
Beersheba, Israel

Background. This study examines the spectrum of infections in a selected population of patients requiring
long-term dialysis, enlarging the focus beyond infections associated with the dialysis process.
Methods. Infection data were reviewed from complete archived inpatient and outpatient dialysis records of
433 patients who were treated at a single hospital-based dialysis program and its dialysis satellites over a 9-year
period, from 1 January 1992 to 31 December 2000.
Results. The study period included 424,700 days of dialysis experience. A total of 2412 episodes of bacterial
or fungal infections were treated in 433 patients. The infection rate was 5.7 episodes per 1000 days of dialysis.
Patients received 5111 courses of antibiotics over 42,627 days of treatment, which cumulatively accounted for 10%
of the total days of the study. Infections associated with hemodialysis vascular access devices comprised 20.5% of
the total episodes. Infections below the knee (19.3% of infection episodes), pneumonia (13%), and other skin
and soft-tissue infections (9%) were also important types and sources of infection, accounting for 142% of the
total episodes. Eighty-two percent of the infections (1971 episodes) were acquired in the community. Of these,
868 (44%) required hospitalization. An additional 441 episodes were nosocomial. The profile of bacteria isolated
from patients with community-acquired infections mirrored that of bacteria recovered from patients with noso-
comial infections.
Conclusion. Patients with end-stage renal disease have an enormous burden of infection. The majority of the
infections are unrelated to dialysis. Frequent and long-term antibiotic use and cohorting of patients in the dialysis
unit have altered the microbiological flora of such individuals, with clinical and epidemiological implications.

When long-term dialysis became a federal entitlement
in 1972, the program was envisioned as a way station
before transplantation [1]. Over the ensuing 30 years,
the size and demographic composition of the dialysis
population has shifted dramatically to become much
older and much sicker. For many patients undergoing
long-term dialysis, there is little hope of receiving a new
kidney. In 1999, Medicare spent more than $15 billion
on the End-Stage Renal Disease (ESRD) program. The
resources required for this care have outstripped all
projections. Because of the formula for reimbursement
under the federally mandated ESRD program, dialysis
Received 26 February 2004; accepted 2 June 2004; electronically published 18
November 2004.
Reprints or correspondence: Dr. Steven J. Berman, 1380 Lusitana St., Honolulu,
Hawaii 96813 (sberman@aloha.net).
Clinical Infectious Diseases 2004; 39:1747–53
 2004 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2004/3912-0001$15.00
centers have scant resources to deal with the chronic
problems of individual patients [2, 3].
Since the insertion of the first vascular-access devices
(VADs) that made chronic hemodialysis practical (i.e.,
hemodialysis VADs [HVADs]), VAD-associated infec-
tion has been a major issue [4–6]. Infection-control
programs in dialysis units have, with great success, min-
imized the opportunity for infectious complications
from viruses and bacteria acquired through contami-
nation of dialysis fluids and equipment [7]. Infections
of HVADs continue to be a problem; patients average
3.5 episodes of HVAD infections per 100 months of
hemodialysis [6]. Many of these infections are caused
by gram-positive methicillin-resistant Staphylococcus
aureus (MRSA) [8], and widespread vancomycin use
[9] has contributed to the appearance in this population
of vancomycin-resistant S. aureus (VRSA) [10] and
vancomycin-resistant enterococci (VRE) [11]. Preven-
tion of these infections and of acquisition of multidrug-
resistant gram-positive bacteria are, understandably, an

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 obvious focus of and priority for infection control in all dialysis
programs [12]. Nephrologists and infectious diseases specialists
familiar with patients receiving long-term dialysis recognize
that dialysis-related infections are only part of the problem.
This article calls attention to the remaining bacterial infections
in the dialysis population, the pervasive exposure to antibiotics,
and the bacterial flora that colonize and infect these patients.
MATERIALS AND METHODS
Patient population and source documents. This is a retro-
spective review of the medical records of 433 patients who had
undergone dialysis between 1 January 1992 and 31 December
2000. A total of 341 patients started dialysis for the first time
after 1 January 1992. The inpatient hospital and outpatient
dialysis records were the source documents. Patients received
dialysis at 1 of 4 neighborhood hemodialysis centers and were
hospitalized at a single facility under the umbrella of the St.
Francis Renal Institute of the Pacific (SFRIP), a not-for-profit
hospital-based program in Honolulu, Hawaii. For patients who
are currently undergoing dialysis, the outpatient medical re-
cords are kept at the neighborhood dialysis units and are col-
lated with the inpatient records after the patient leaves the
program. Thus, the review was limited to patients who were
not undergoing dialysis at the time of data collection. Of the
patients in the study, 417 patients died, and 16 patients left the
SFRIP dialysis program. Patients were excluded from the anal-
ysis if they underwent successful kidney transplantation or were
alive and undergoing dialysis at the end of the study period, if
they received hemodialysis for !90 days, or if they were hos-
pitalized elsewhere (unless there was sufficient documentation
for the reason for hospitalization and complete information on
antibiotic therapy and culture results).
Statistical analysis. Personnel who are experienced with
dialysis reviewed the inpatient and outpatient records for all
study patients. One of the investigators (C.N.) performed a
second review. The data were entered into a relational database
(4th Dimension) and were analyzed using a statistical package
(SPSS). The x2 test was used to compare the proportion of
gram-positive and gram-negative bacterial isolates recovered
during episodes of community-acquired infection with the pro-
portion recovered during nosocomial infections, as well as to
compare the infection-related mortality rate in the study cohort
with that reported in the US Renal Data System (USRDS) [14].
Fisher’s z test was used to test the differences between the study
population at SFRIP and data from the USRDS 1999 and 2002
reports. The infection rate was defined for each patient as the
number of infections per 1000 days of life during the study
period. Student’s t test was used to compare the infection rates
for patients whose primary cause of ESRD was diabetes mellitus
with infection rates for patients with ESRD due to other causes.
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All P values are based on results of the 2-sided test. R.C. was
responsible for the statistical analysis.
Definition of infection. An episode of infection was defined
as the use of antibiotic treatment for ⭓3 days in the context
of criteria of signs and symptoms, as outlined in the Centers
for Disease Control and Prevention guidelines for the definition
of nosocomial infections [13]. The half-life of some antibiotics
is prolonged in patients with severe renal failure. Some pro-
tocols call for the administration of antibiotics only at the end
of each hemodialysis session. A course of treatment was ac-
ceptable if at least 2 antibiotic doses, separated by a nonhe-
modialysis day, were administered. Treatment with 1 dose of
vancomycin was included as an episode of infection if sup-
porting clinical signs or microbiological data were present by
the third day of treatment, because 1 dose of vancomycin may
sustain adequate serum concentration for at least 7 days in
patients who are dialyzed with low-flux dialyzers. Because fever
during hemodialysis is common and may arise from a variety
of causes, including bacteremia and use of an HVAD, nephrol-
ogists may order blood cultures and an empirical dose of an-
tibiotics when notified about the fever. There is usually no
continuation of treatment at the next dialysis session, unless
there is additional evidence of infection. Thus, patients who
received a single dose of antibiotics or treatment courses for a
duration 13 days without microbiological or clinical evidence
of infection at the time of the next dialysis were excluded from
the analysis. Infection at a previous site was counted as a new
episode if no antibiotics were given for a minimum of 120 days
before the current course of treatment. All below-the-knee in-
fections (BKIs), with the exception of postoperative wound
infection, were grouped together. All other skin and soft-tissue
infections (SSTIs) were similarly grouped. Sepsis syndrome was
diagnosed if a patient had fever, tachycardia, and leukocytosis
without localizing signs of infection and received antibiotics
for at least 3 days. The diagnosis of septicemia required bac-
teremia in the presence of fever, no local signs of infection that
suggested the source of the bacteremia, and no relapse of bac-
teremia for 120 days after completion of the antibiotic course.
Patients who had received prophylactic courses of antibiotics,
treatment for tuberculosis and leprosy, and treatment for viral
infections were not included in the analysis. Infection leading
to death required not only the clinical diagnosis of infection
noted above, but also documentation by the attending physician
or the infectious diseases consultant that the infection was re-
sponsible for the patient’s death.
Nosocomial versus community-acquired infection. Nos-
ocomial infections were defined according to standard criteria
[13]. Infections in patients who were directly admitted from a
skilled nursing or long-term care facility were also considered
to be nosocomial. If the onset of signs and symptoms of in-
 Table 1. Characteristics of study patients with end-stage renal disease
(ESRD) from the St. Francis Renal Institute of the Pacific (SFRIP; Honolulu, HI)
and the 2002 US Renal Data Survey (USRDS).

SFRIP USRDS
Characteristic (n p 433) (n p 92,635)a P
Age at onset of dialysis, years 62.3 61.1 .0021
One-year survival rate 80.2 79.5 NS
Raceb
White 19 66
African American 1 30
Asian 54 3
Pacific Islander 30 …
Female sex 50 47 NS
Cause of ESRD
Diabetes mellitus 56 43 .0001
Hypertension 11 26 .0001
Chronic glomerulonephritis 18 8 .0001
Comorbidity
Congestive heart failure 36 29 .0016
Coronary artery disease 32 22 .0001
Peripheral vascular disease 17 14 .069
Chronic obstructive pulmonary disease 3.23 5.8 .022
Death due to infection 17.7 14.8c NS
Hospitalization
Duration, days per patient-year 12.9 14.3 .009
No. of admissions per patient-year 2.1 2.0 NS
Reason
Vascular-access procedure 13.2 13.2 NS
Pneumonia 5.9 2.5 .0001
Septicemia 1.7 3.5 .042
No. of VAD infections per 100 months 3.5 3.5d NS
Kt/V ratio 11.2e 82

NOTE. Data are percentage of patients, unless otherwise indicated. NS, not significant.
a
Data are from USRDS 2002 [2], unless otherwise indicated. All patients were new re-
cipients of dialysis in 2000.
b
Hawaii is a multiethnic society.
c
1999 USRDS report [14], by x2 analysis.
d
As reported by Tokars et al. [7].
e
Adequacy of urea removal, where K is the urea clearance rate, t is the treatment duration,
and V is the volume of water in the patient’s body.

fection and the first treatment occurred in the outpatient setting
or within 48 h after hospital admission, the infection was con-
sidered to be community acquired.
Microbiological analysis. Bacterial isolates were included
if cultures were performed within 2 days after starting antibiotic
therapy and if culture specimens were obtained from sites com-
patible with the clinical diagnosis. All isolates recovered from
cultures of blood and other normally sterile body fluids were
included, except for coagulase-negative staphylococci (CONS),
which required isolation from 11 blood culture. Specimens
from central catheters, including those providing access for
hemodialysis, were cultured by the roll plate technique and
were included in the analysis if 115 colonies were present [14].
RESULTS
Patient characteristics. The archived medical records of 433
patients requiring long-term dialysis between 1 January 1992
and 31 December 2000 were reviewed. There were 424,700
dialysis days reported for these patients. The mean age at the
onset of dialysis was 62.3 years, and the mean duration (SD)
of dialysis before death was 980  650 days. Diabetes mellitus
was the most common cause of ESRD (56% of patients), and
80% of patients were of Asian or Pacific Islander race. Other
than these differences, the demographic and clinical profiles of
patients in the study population were similar to those of Med-
icare patients undergoing dialysis, as reported by the USRDS

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 Figure 1. Number and types of community-acquired and nosocomial infections diagnosed in patients with end-stage renal disease. BKI, below-
the-knee infection; DIARRHEA, enteric bacterial infection; ENT, ears/nose/throat; G/U, genital/urinary tract; HVAD, hemodialysis vascular-access device;
MISC, miscellaneous; NHVAD, non–hemodialysis vascular-access device; PD, peritoneal dialysis–related infection; POSTOP WOUND, postoperative
wound; SSTI, skin/soft-tissue infection.
[15]. Similar profile findings included the percentage of patients
who were alive after 1 year of dialysis, the rate of HVAD in-
fection, the rate of death due to infection, and/or the rate of
hospitalization for any reason (table 1).
Clinical infection. A total of 2412 episodes of infection
were identified, with a rate of 5.7 episodes per 1000 days of
dialysis. Community-acquired infections accounted for 1971
episodes (82%); of these, 868 (44%) required hospitalization.
There were an additional 441 nosocomial infections treated in
the hospital. Dialysis-related infections were responsible for
24% of the episodes, including 495 HVAD infections and 90
peritoneal dialysis–related infections. Three other types of in-
fections caused 50% of the total episodes: BKIs (468 episodes),
pneumonia (315 episodes), and SSTIs at other sites (214 epi-
sodes) (figure 1). The infection rate in patients with ESRD due
to diabetes mellitus was higher than that for the rest of the
study cohort (6.72 vs. 4.79 episodes per 1000 dialysis-days).
Almost all of the difference in the infection rate (94%) between
the 2 study populations was due to BKIs and SSTIs. Indepen-
dent of the cause of ESRD, the final year of life was especially
burdensome: 1201 (50%) of the total episodes occurred during
this period.
Antibiotics. Patients received at least 1 antibiotic for the
treatment of infection on 42,627 days—a cumulative total of
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10% of the study days. Antibiotics with favorable pharmaco-
kinetic characteristics in patients with renal failure were used
in both the hospital and outpatient dialysis settings (figure 2).
Ten antibiotics accounted for 80% of the 5111 courses of
treatment: cefazolin (1013 courses), vancomycin (939), tobra-
mycin (939), gentamicin (606), ceftazidime (347), ciprofloxacin
(289), ceftriaxone (263), metronidazole (185), ampicillin (120),
and piperacillin/tazobactam (88).
Microbiological findings. In 1134 episodes of infection,
1440 organisms were isolated (table 2). Cultures were not per-
formed (905 episodes) or were sterile (373 episodes) for the
remainder. A total of 48% of the organisms were gram-positive
cocci, and 35% were aerobic gram-negative rods. S. aureus (328
isolates), CONS (206), Pseudomonas aeruginosa (148), Esche-
richia coli (102), Klebsiella species (77), and Enterobacter species
(64) were the most frequent isolates recovered. S. aureus and
CONS were the most commonly isolated bacteria from patients
with an HVAD. There was no significant difference between
the relative proportion of gram-positive cocci and aerobic
gram-negative rods associated with either nosocomial or com-
munity-acquired infections of the VAD, with pneumonia, or
with BKI. Gram-negative bacteria were isolated from the pri-
mary cultures at similar rates for each of these types of infection.
Most striking was the frequency of isolation of gram-negative
 Figure 2. Courses of antibiotics administered to outpatients in the dialysis unit and to inpatients in the hospital. PIP-TAZO, piperacillin-tazobactam.
bacilli from patients with community-acquired pneumonia.
These bacteria were present in 55% of the 113 episodes asso-
ciated with positive sputum culture results, including 23 epi-
sodes in which P. aeruginosa was isolated.
DISCUSSION
This study reviews the inpatient and outpatient infection ex-
perience in a cohort of patients with ESRD requiring long-term
dialysis. Infection was common, averaging 5.7 events per 1000
dialysis-days, and antibiotic use was extensive, occurring on
∼10% of the study days. Although infections at the dialysis
access site were responsible for 24% of the total episodes, the
rest of the infection burden was unrelated to dialysis. BKIs,
other SSTIs, and pneumonia accounted for 42% of the total
number of infections.
The cohort was selected retrospectively on the basis of avail-
able medical records from a 9-year period, compiling data from
1425,000 days after the initiation of long-term dialysis. It was
not designed to show the relationship between the natural his-
tory of infection and the vintage of dialysis, because 95% of
the 433 study patients died during the study period, and pa-
tients who were alive at the end of the study were excluded
from the analysis. Despite this limitation, the cohort experi-
enced rates of 1-year survival, HVAD infection, and hospital-
ization and numbers of hospital-days per year that were similar
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to those of patients described in the national database of ESRD
(USRDS) and in other published studies [6, 16]. The demo-
graphic characteristics of this cohort differed from those of
patients in the USRDS database with respect to race and the
primary cause of ESRD.
Diabetes mellitus was the cause of ESRD in 56% of the
patients in our cohort, compared with 43% in patients de-
scribed in the 2002 USRDS. Significantly more infections oc-
curred in our diabetic patient group, especially infections of
the lower extremity (BKIs) and other SSTIs. We predict that,
by 2007, diabetes mellitus will be the cause of ESRD for 142%
of new dialysis patients in the United States and anticipate that
the number of infections will increase accordingly.
Bacteria isolated from cultures of samples obtained from
patients with nosocomial or community-acquired infections
were similar. Thirty-five percent of the primary isolates were
aerobic gram-negative rods. This is of interest because gram-
negative bacilli comprise a small percentage of the normal flora
of the skin and respiratory tracts of healthy individuals [17].
Historically, colonization and infection with these organisms
have been associated with the hospital setting, bedridden pa-
tients, indwelling Foley catheters, or patients requiring me-
chanical ventilation [18–20]. Though patients with ESRD are
ambulatory and live at home, they share the 3 characteristics
that support the presence of organisms associated with noso-
 Table 2. Microbiological data on infections in patients with end-stage renal disease undergoing dialysis.

All sites Pneumonia HVAD Below-knee infection

Nosocomial CA Nosocomial CA Nosocomial CA Nosocomial CA

Bacterial isolate (n p 370) (n p 1070) (n p 73) (n p 113) (n p 36) (n p 201) (n p 32) (n p 275)

Gram-positive cocci
Total 158 (43) 539 (50) 16 (22) 29 (26) 30 (83) 149 (74) 23 (72) 147 (54)
a
Coagulase-negative staphylococci 53 (14) 153 (14) 0 1 (1) 16 (44) 46 (23) 7 (22) 42 (15)
Methicillin-susceptible Staphylococcus aureus 19 (5) 194 (18) 0 12 (11) 7 (19) 70 (35) 3 (9) 49 (18)
Methicillin-resistant S. aureus 45 (6) 70 (7) 16 (22) 13 (12) 4 (11) 20 (10) 4 (13) 13 (5)
a
Enterococcus species 23 (5) 70 (7) 0 1 (1) 2 (6) 9 (5) 6 (19) 27 (10)
Vancomycin-resistant enterococci 12 (8) 1 (0) 0 0 0 0 2 (6) 0
Other 59 (16) 6 (1) 0 0 17 (47) 1 (1) 1 (3) 16 (6)
Aerobic gram-negative rods 126 (34) 384 (36) 47 (64) 62 (55) 5 (14) 37 (18) 9 (28) 92 (34)
Pseudomonas aeruginosa 31 (8) 117 (11) 16 (2) 24 (21) 0 9 (5) 5 (16) 25 (9)
Escherichia coli 25 (3) 77 (7) 2 (3) 4 (4) 1 (3) 5 (3) 2 (6) 20 (7)
Klebsiella species 20 (3) 57 (5) 10 (14) 12 (11) 0 7 (4) 0 9 (3)
Enterobacter species 22 (3) 42 (4) 9 (12) 5 (4) 0 10 (5) 0 0
Other 28 (3) 91 (9) 10 (14) 17 (15) 3 (9) 6 (4) 2 (6) 38 (14)
Respiratory pathogens
Moraxella species 4 (1) 5 (1) 4 (6) 2 (2) 0 0 0 0
Haemophilus influenzae 5 (1) 18 (2) 2 (3) 11 (12) 0 0 0 0
Pneumococcus species 2 (1) 9 (1) 2 (3) 7 (6) 0 0 0 0
Miscellaneous 75 (20) 115 (11) 2 (3) 2 (2) 1 (3) 15 (8) 0 36 (13)

NOTE. Data are no. (%) of bacterial isolates and represent a total of 1440 isolates from 1134 episodes in 433 patients. CA, community acquired; HVAD,
hemodialysis vascular-access device.
a
Isolated from an empyema.

comial infections: antibiotic use [21], clustering in a common
environment (hemodialysis units), and the presence of in-
dwelling medical devices [22].
Cefazolin, with its favorable pharmacokinetic profile in pa-
tients undergoing hemodialysis, was the most frequently pre-
scribed antibiotic. Consistent with the medical literature, S.
aureus and CONS were the most common bacteria isolated
from HVAD infections [23]. Vancomycin use was less than that
reported in other centers [24], because of a lower percentage
of methicillin resistant isolates from cultures yielding S. aureus
[9, 12] and antibiotic policy. SFRIP made a 20-year effort to
use cefazolin for all suspected VAD infections and reserved
vancomycin for verified MRSA or MRSE infection or for initial
empirical treatment for sepsis syndrome due to a suspected
VAD source. The policy has become Hobson’s choice, because
the extensive use of cefazolin, more than likely, was a major
reason for the unusually high frequency of isolation of gram-
negative bacteria, such as P. aeruginosa in cultures of sputum
specimens obtained from patients with pneumonia, in cases of
community-acquired infection.
Although it may be difficult to distinguish between patho-
genicity and colonization in a retrospective study, the recovery
of these organisms from the initial cultures performed for pa-
tients with infection is relevant. In the future, guidelines for
empirical therapy for many community-acquired infections in
patients undergoing dialysis may recommend broad-spectrum
antibiotics, which will further contribute to the problem of
antibiotic pressure. Because 80% of all infectious episodes oc-
curred at home, the risk of spreading these and other antibiotic-
resistant bacteria to members of the patient’s household, al-
though not yet quantified, is real.
The infection burden associated with patients undergoing
dialysis and its impact on society will only increase with the
increasing number of such patients, which estimated to double
to 600,000 by 2010. What can be done to alter this paradigm?
In our cohort, two-thirds of the episodes of infection were in
the catheter-access device, the skin and soft tissues (including
the ischemic and insensitive foot), or the lung. Many of these
infections are preventable with standard treatment programs
and protocols.
With an HVAD infection rate of 3.5 cases per 1000 days of
use, the federally mandated ESRD program has made the pre-
vention of access-site infections a priority. One of the factors
that determine the HVAD infection rate is the type of vascular
access. The highest rate occurs with the temporary noncuffed
dialysis catheter, which is usually placed in the internal jugular
vein, and the lowest rate occurs with the simple fistula, which
is generally placed in the forearm. Dialysis programs have a
comprehensive infrastructure for monitoring dialysis devices.
They are required to report the prevalence of each type of access

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 and are mandated to use simple fistulas first to decrease the
infection rate (Jared Sugihara, personal communication). Stan-
dard protocols are followed to prepare the access site before
the initiation of dialysis. The staff is trained to inspect the VAD
for problems that may lead to infection-associated thrombosis,
aneurysm, hematoma, or nonhealing puncture sites.
There is no similar required structure in the dialysis unit for
the prevention of infections unrelated to dialysis. Patients in
frail health frequently delay seeking early medical attention—
the cornerstone of the personal physician’s approach to pre-
ventive medical care. High-risk, infection-prone patients con-
stitute the following groups: those with multisystem disease
(including peripheral vascular disease or an insensitive foot),
those with severe functional limitations [25], and those who
are malnourished [26]. There are evidence-based programs to
improve the health and prevent complications of these con-
ditions [27–29]. We hope that this article will encourage the
implementation of such programs, which can help the patient
reduce their infection burden and limit the appearance and
spread of multidrug-resistant bacteria.
Acknowledgments
We wish to thank Joann Tsark and Kathryn Braun for advice on study
design, Michael McNiel (Tsunami Dataworks) for developing the database,
Julie D. Benedetto and Jane Doll for supervising data extraction, Daniel F.
Brandt and Sarah K. Kemble for conducting a pilot test of the database,
and Jared Sugihara for review of the manuscript.
Financial support. Centers for Disease Control and Prevention (grant
H75/CCH922284-01), the Hawaii Medical Services Association Founda-
tion, and the Velin and Julia Kung Foundation.
Potential conflicts of interest. All authors: no conflicts.
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