ORIGINAL ARTICLE

10.1111/j.1469-0691.2006.01435.x

Investigation of the possible association between nosocomial candiduria

and candidaemia
C. A. Binelli1, M. L. Moretti2, R. S. Assis1, N. Sauaia1, P. R. Menezes1, E. Ribeiro2, D. C. P. Geiger2,
Y. Mikami3, M. Miyaji3, M. S. Oliveira2, A. A. Barone1 and A. S. Levin1
1

Faculty of Medicine of the University of Sao Paulo, Sao Paulo, 2Faculty of Medical Sciences, State
University of Campinas, Campinas, Brazil, and 3Chiba University, Chiba, Japan

ABSTRACT
This study aimed to determine whether candiduria is associated with the occurrence of nosocomial
candidaemia. In the case-control part of the study, 115 cases (nosocomial candidaemia) and 115 controls
(nosocomial bacteraemia) were similar in age, severity of condition and time of hospitalisation. There
was a significant association of candidaemia with candiduria (OR 9.79; 95% CI 2.1444.76). In the
microbiology part of the study, 23 pairs of Candida-positive urine and blood cultures were obtained from
23 patients. In ten (43%) cases, the urine and blood culture isolates belonged to different species, and
molecular typing showed a difference in two of the 13 cases yielding the same species from both
specimens. Overall, there was a significant association between candiduria and candidaemia, but the
Candida isolates from urine and blood were different for 52% of the patients. Thus, the data indicated
that the urinary tract was probably not a source for the candidaemia.
Keywords

Bacteraemia, Candida spp., candidaemia, candidurea, nosocomial infection

Original Submission: 9 June 2005;

Revised Submission: 22 September 2005;

Accepted: 10 November 2005

Clin Microbiol Infect 2006; 12: 538543

INTRODUCTION
Candida spp. frequently colonise the digestive and
genital tracts, as well as the mucosal surfaces, of
237% of healthy individuals, but colonisation of
80% of hospitalised patients can occur [1,2].
Colonisation usually precedes candidaemia, and
is considered to be an important risk-factor as
most infections are endogenous [17]. Candidaemia is a severe infection and has a high risk of
death (4680%) when compared with bacteraemia
[1,810], with an attributable mortality of 38% [8].
The natural history of candiduria is not clearly
established. Urinary tract colonisation deserves
consideration, as it is a common event in hospitalised patients [1114], affecting 6.520% of
patients [5]. Candiduria, which is asymptomatic
or with only slight symptoms, is considered
benign, even in patients with underlying disease

Corresponding author and reprint requests: A. S. Levin, Rua

Harmonia 564 52, Sao Paulo, SP 05435000, Brazil
E-mail: gcih@hcnet.usp.br

Deceased

such as diabetes mellitus [15,16]. Patients with

urological disease and candiduria who undergo
surgery or manipulation of the urinary tract are at
risk of candidaemia [17], considered to be ascendant and not haematogenic [18]. However, some
studies emphasise that candiduria should never
be ignored in septic patients, as it may be the first
sign of a systemic Candida infection [1921].
However, it seems to be difficult to differentiate
between colonisation and infection, and to establish the role of Candida colonisation in the occurrence of candidaemia. In a multicentre study with
4276 intensive care patients [22], rectal and urinary colonisation had a low positive predictive
value for candidaemia, with only 1% of colonised
patients developing Candida bloodstream infections. Molecular typing demonstrated that the
colonising isolate and that from the blood were
identical for 17 of 18 Candida infections. In a
prospective multicentre study of 861 patients with
documented funguria, only 1.3% presented with
proven candidaemia [16]. The aim of the present
study was to determine whether there is an
independent association between candiduria and
candidaemia.

2006 Copyright by the European Society of Clinical Microbiology and Infectious Diseases

Binelli et al.

METHODS AND MATERIALS

This study comprised two parts: an epidemiological casecontrol study performed between 1996 and 2000 to evaluate
the association between candiduria and candidaemia, and a
microbiological study involving specimens obtained between
1999 and 2001 to evaluate whether Candida spp. isolated from
the blood and urine of each patient were identical.
Epidemiological study design
Individually matched cases and controls were patients from the
Hospital das Clnicas of the University of Sao Paulo, Brazil, a
tertiary-care teaching hospital associated with the university
with c.2000 beds in five buildings and 15 intensive care units.
This institution is the main reference hospital in Sao Paulo, a city
with c.11 million inhabitants. Cases and controls were obtained
from the database of the hospitals infection control department.
A case was defined as a patient aged 5 years, with at least
one blood culture positive for Candida spp., a Candida-positive
urine culture collected in the period between 2 weeks before
and 2 days after the positive blood culture was taken, and who
was hospitalised for 48 h before the positive blood culture
was taken.
A control was defined as a patient aged 5 years from the
same unit of the hospital as the case, who had a positive blood
culture for bacteria within 9 months of the case, a positive
urine culture collected in the period between 2 weeks before
and 2 days after the positive blood culture was taken, and who
was hospitalised for 48 h before the positive blood culture
was taken. When there were several potential controls for a
case, the age and date of hospitalisation were selected to be as
close as possible to those of the case.
Assessment of disease and exposure. The following data were
collected from the medical records for cases and controls:
gender, age, hospital unit, days of hospitalisation before the
positive blood culture, use of an endotracheal tube during the
previous 30 days, use of central venous and urinary catheters
during the previous 30 days, use of antimicrobial drugs during
hospitalisation, use of steroids (defined as a daily dose of
15 mg of prednisone or equivalent for 1 week), chemotherapy or antifungal drugs, dialysis, parenteral nutrition within
the 30-day period before the positive blood culture, cancer,
surgical procedures, care at a day-hospital within 30 days of
the positive culture, the presence of neutropenia (defined as a
neutrophil count < 1000 mm3) within the previous 2 weeks,
and the severity of each patients condition on admission and
on the day of the positive blood culture according to the
APACHE II score [23]. The isolation of fungi at other sites
(defined as any positive cultures other than from blood) was
also recorded. Underlying diseases were those reported by the
attending physician and stated clearly in the patient records.
Candidaemia was defined as a blood culture positive for
Candida; candiduria was defined as a urine culture positive for
Candida with 10 000 CFU mL [24].
Statistical analysis. The sample size was calculated considering
one control for each case, using Stata 7.0 software (Stata Corp.,
College Station, TX, USA). The OR to be detected was 3.5 and,
based on data from the same hospital in 1997, the prevalence of
candiduria in patients with bacteraemia was predicted to be

Nosocomial candiduria and candidaemia 539

7%. A sample of 115 cases and 115 controls would then have a
power of 82% to detect an OR of 3.5 with p 0.05. A database
was constructed using Epi Info 6 v.6.02 (CDC, Atlanta, GA,
USA). In the univariate analysis, ORs for individually matched
case-control studies and 95% CIs were estimated for each of
the categorical variables, and were analysed using McNemar
chi-square tests. For continuous variables, the mean, median
and standard deviation were calculated for cases and controls,
and the Wilcoxon matched pairs signed-rank test was used for
analysis. Significance was set at p 0.05.
In the multivariate analysis, conditional multiple logistic
regression was used. Exposure variables were tested if p
was 0.25 in the univariate analysis, using a stepwise
forward method. To stay in the final model, exposure
variables required p values 0.05 according to the likelihood
ratio test.
Microbiological study
Between 1999 and 2001, all urine cultures positive for Candida
spp. from patients aged 5 years were stored for 3 weeks. If,
within this period, there was a positive blood culture for
Candida spp., a matched pair was formed. Isolates from blood
and urine were identified by colony morphology, cell morphology, the germ tube test [25], the automated Vitek system
(bioMerieux, Marcy lEtoile, France), CHROMagar [26], carbon
assimilation tests (ID32 C; bioMerieux) [27,28], and specific
antisera for Candida (Candida check; Iatron, Tokyo, Japan) [29].
Molecular typing was performed when the same species of
Candida was isolated from the blood and the urine of a single
patient.
DNA extraction for randomly amplified polymorphic DNA
(RAPD) typing was performed as described previously [30,31],
with minor modifications. Four primers were used: Oligo 2
primer (5-TCACGATGCA) for Candida albicans, Candida tropicalis and Candida glabrata; Oligo 3 primer (5-ATCGATCSSC)
for C. albicans and C. glabrata; P5 primer (5-AACGCGCAAC)
for C. tropicalis; and Oligo 1 primer (5-ATTGCGTCCA) for C.
glabrata. Isolates were considered to be different if the banding
patterns differed by one, or more than one, readily detectable
band.
Pulsed-field gel electrophoresis (PFGE) was performed as
described previously [32]. The electrophoretic karyotype (EK)
was determined for C. albicans, C. tropicalis and C. glabrata. In
addition, C. albicans and C. tropicalis were analysed by
restriction endonuclease analysis using SfiI 10 U mL and
BssHII 4 U mL, respectively, followed by PFGE. Isolates were
considered to be identical if all readily detectable bands of one
isolate matched those of another. If not, the coefficients of
similarity were determined.

RESULTS
Epidemiological study
Between 1996 and 2000, there were 117 cases of
candidaemia, but controls were found for only
115; therefore, two cases were not included in the
analysis. Forty percent of the patients were from
intensive care units. The median time from the

2006 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 12, 538543

540 Clinical Microbiology and Infection, Volume 12 Number 6, June 2006

urine culture to the first positive blood culture

was 1 day (range )223 days) for cases and 1 day
(range )218 days) for controls. The Candida spp.
causing candidaemia and candiduria are summarised in Table 1. Variables associated statistically
with candidaemia were candiduria and the presence of fungi at other sites (Table 2). Both groups
were similar in terms of age, severity of clinical
condition and days of hospitalisation (Table 3).
The variables included in the multivariate
analysis were candiduria, the presence of fungi
at other sites, the use of antimicrobial drugs,
neutropenia and cancer. The multivariate analysis
only showed an association of candidaemia with
candiduria and with previous antimicrobial use
(Table 4). Deaths during hospitalisation and with-

Table 1. Causes of candidaemia and candiduria

Organism

Candidaemia
n (%)

Candiduria
in cases
n

Candiduria
in controls
n

Candida
Candida
Candida
Candida
Candida
Candida
Candida
Candida
Candida
Total

43
26
21
7
5
3
2
1
7
115

12
10

1
24

6
2

1
9

albicans
tropicalis
parapsilosis
glabrata
guillermondii
krusei
famata
kefyr
spp.

(37)
(23)
(18)
(6)
(4)
(3)
(23)
(1)
(6)

Table 3. Factors associated with candidaemia: univariate

analysis of continuous variables
Variable

Median

Range

p value

Age (years)
Cases
46
789
Controls
42
387
APACHE II score at hospitalisation
Cases
13
034
Controls
12
052
APACHE II score on day of positive blood culture
Cases
16
247
Controls
16
139
Days of hospitalisation before positive blood culture
Cases
19
0127
Controls
16
0138

0.18

0.09

0.87

0.33

SD, standard deviation.

Table 4. Factors associated with candidaemia: results of

multivariate analysis
Variable

OR

95% CI

p value

Candiduria
Antimicrobial use

9.79
3.79

2.1444.76
1.0613.56

0.003
0.041

in 30 days of discharge were significantly higher

for cases (51%) than for controls (37%) (p 0.02).
Microbiological study

Table 2. Factors associated with candidaemia: univariate

analysis of categorical variables

There were 23 pairs of urine and blood isolates

from 23 patients; in ten (43%) cases, the species
isolated from blood was different to that isolated
from urine (Table 5). The urine of one patient
yielded two different species, namely C. glabrata
(in the blood) and C. tropicalis. Molecular typing
was performed for 14 pairs of isolates.
Table 5. Identification of pairs of Candida isolates from
blood and urine cultures

n (%) of

Variable

Cases
n = 115

Controls
n = 115

OR

95% CI

p value

Patient number

Blood culture

Urine culture

Male gender
Candiduria
Haematuriaa
Proteinuriaa
Care at day hospital
Use of antimicrobial drugs
Use of antifungal drugs
Urinary catheter
Central venous catheter
Endotracheal tube
Haemodialysis
Peritoneal dialysis
Total parenteral nutrition
Surgical procedure
Steroid use
Chemotherapy
Presence of underlying disease
Cancer
Diabetes mellitus
Neutropenia
Other diseases
Fungi at other sites

68
24
63
51
15
111
23
71
97
43
12
3
21
50
44
26
113
41
9
32
114
25

70
9
59
48
18
103
28
71
99
36
12
1
19
57
40
31
114
31
10
25
114
10

0.89
8.50
1.07
1.06
0.63
3.00
0.75
1.00
0.87
1.31
1.00
3.00
1.17
0.72
1.19
0.50
0.50
2.00
0.89
1.88
1.00
2.67

0.451.74
1.9636.79
0.522.22
0.542.10
0.201.91
0.979.3
0.381.46
0.541.86
0.411.82
0.732.36
0.323.10
0.3128.84
0.542.52
0.391.32
0.672.13
0.171.46
0.055.51
0.944.27
0.342.30
0.794.42
0.0615.99
1.245.74

0.86
0.001
1.00
1.00
0.58
0.08
0.50
0.87
0.85
0.33
0.77
0.62
0.84
0.36
0.66
0.30
1.00
0.10
1.00
0.21
0.48
0.01

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23

C. albicans
C. tropicalis
C. glabrata
C. glabrata
C. parapsilosis
C. tropicalis
C. albicans
C. albicans
C. albicans
C. parapsilosis
C. tropicalis
C. tropicalis
C tropicalis
C. tropicalis
C. tropicalis
C. albicans
C. tropicalis
C. albicans
C. albicans
C. albicans
C. tropicalis
C. albicans
C. tropicalis

C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.
C.

(59)
(21)
(70)
(57)
(13)
(97)
(20)
(62)
(84)
(37)
(10)
(3)
(18)
(43)
(38)
(23)
(98)
(36)
(8)
(28)
(99)
(22)

(61)
(8)
(66)
(53)
(16)
(90)
(24)
(62)
(86)
(31)
(10)
(1)
(17)
(50)
(35)
(27)
(99)
(27)
(9)
(22)
(99)
(9)

glabrata
tropicalis
albicans
tropicalis C. glabrata
tropicalis
tropicalis
albicans
albicans
tropicalis
tropicalis
tropicalis
krusei
glabrata
albicans
tropicalis
albicans
tropicalis
albicans
albicans
albicans
tropicalis
tropicalis
tropicalis

Information available for 90 cases and 90 controls only.

2006 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 12, 538543

Binelli et al.

C. albicans
Twelve isolates, comprising six pairs from urine
and blood, generated four different DNA profiles
when analysed by RAPD using oligo 2, and three
profiles when analysed by oligo 3. The pairs of C.
albicans isolates were identical for each patient,
regardless of which primer was used. EK analysis
yielded three DNA profiles. The blood and urine
isolates of each patient were also identical following restriction endonuclease analysis.
C. tropicalis
Seven pairs of blood and urine isolates were
studied by RAPD and PFGE. Primer P5 generated
five different profiles; the profiles of the urine and
blood samples were different in one pair. Four
different profiles were produced using oligo 2; the
blood and urine isolates were different for
another pair. The isolates could not be differentiated by EK analysis. In patients 15 and 23, the
similarity coefficients for the blood and urine
isolates were 71.5% and 76.5%, respectively,
following restriction endonuclease analysis with
BssHII, suggesting that the isolates might be
different.
C. glabrata
Patient 4 yielded C. glabrata isolates from blood
and urine; the isolates were identical following
RAPD and PFGE analysis.
DISCUSSION
The significance of Candida isolated from urine is
still unclear. Candidaemia is a rare occurrence in
hospitalised patients, and therefore a cohort study
to evaluate candiduria as a risk-factor for candidaemia was not considered practical. Thus, a casecontrol study was chosen. In the present study,
univariate analysis indicated a significant association of candidaemia with candiduria and the
isolation of fungi at other sites. Multivariate
analysis showed an association between candidaemia and candiduria and previous use of antimicrobial drugs. The OR for candiduria was 9.79.
These findings suggest that patients with candiduria have an increased risk for presenting with
candidaemia. It was not possible to define whether candiduria was the source of candidaemia.
Mortality was significantly higher among cases,
but death can be associated with a number of
other factors, such as site of infection, underlying

Nosocomial candiduria and candidaemia 541

conditions and adequate treatment, that were not

evaluated in the present study. Thus, this result
should be viewed with caution.
There are probably many factors involved in the
genesis of candidaemia, including extensive use of
antimicrobial agents and translocation from the
digestive tract [7]. Thus, the treatment of candiduria as a measure to prevent candidaemia [33,34]
may not be an effective strategy. It is important to
define whether there is a causative association
between candidaemia and candiduria before
recommending such extensive antifungal use.
In ten of 23 cases, the species of Candida isolated
from the blood and urine were different. Molecular typing demonstrated that the paired isolates
from blood and urine were identical for each of
the six patients with C. albicans. Among the seven
patients with C. tropicalis, the paired isolates were
different for two patients. The blood and urine
isolates of C. glabrata from one patient had
identical profiles. In the present study, restriction
endonuclease analysis was more discriminatory
than RAPD, in accordance with previous findings
[35,36]. Overall, among the 23 pairs of blood and
urine isolates from 23 patients, the isolate in the
blood was different from that in the urine for 52%
of the patients. Therefore, the microbiological
data do not support the epidemiological association, which suggests that candiduria has the
same risk-factors as Candida bloodstream infection, and that candidaemia may not be a direct
consequence of candiduria. Thus the use of
empirical antifungal treatment in patients with
candiduria [33,34] could lead to unnecessary
antifungal prescription.
One of the limitations of the present study was
the lack of routine surveillance for Candida at
other sites, and this could explain why the
presence of fungi at other sites variable was
not significant by multivariate analysis. It was not
possible to ascertain whether patients without
cultures were not colonised by fungi. Another
limitation was that there may have been mixed
Candida urine infections that were not detected,
although in one patient, two species of Candida
were isolated from the urine.
In studying nosocomial infections, the choice of
controls is often difficult. Using controls that
represented the source population was considered, but it was felt that such individuals could be
younger and less ill than the cases. This could
result in significant associations between candid-

2006 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 12, 538543

542 Clinical Microbiology and Infection, Volume 12 Number 6, June 2006

aemia and previously well-studied factors, such

as age, days of hospitalisation, invasive devices
and severity of clinical condition [37], that might
overshadow the primary hypothesis (i.e., the
presence of candiduria as an independent riskfactor for candidaemia). Thus, control patients
with nosocomial bloodstream infections, who
would present a high prevalence of well-studied
risk-factors for candidaemia, were chosen. For the
same reason, cases and controls were matched
based on age. McCarthy and Giesecke [38] have
discussed the difficulty in choosing controls for
studies in infectious diseases, emphasising that
bias could occur because of differences in surveillance methods used to obtain cases and
controls, and suggested that both groups should
be selected using the same method of surveillance
and the same infectious diagnosis, albeit caused
by different microorganisms.
Established factors associated with systemic
infections, such as age, severity of condition
(APACHE II score), previous days of hospitalisation and the use of invasive devices, were similar
in cases and controls. The choice of severely-ill
controls may have led to over-matching, and
therefore an underestimation of the ORs, but it
was considered that this was an adequate strategy
to evaluate the association of candidaemia with
candiduria, since it suggests that the actual OR
may be > 9.8.
In conclusion, although candidaemia was associated strongly with candiduria in an epidemiological study, the microbiological study indicated
that urine was not the main source of Candida
bloodstream infection.

5.

6.

7.
8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

ACKNOWLEDGEMENTS
This study was supported by a doctoral grant from FAPESP
(Fundacao de Amparo a` Pesquisa do Estado de Sao Paulo),
grant 98 134011.

18.
19.

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