Predictive value of oral colonization by Candida yeasts for the onset of a nosocomial infection in elderly hospitalized patients

Journal of Medical Microbiology (2006), 55, 223–228
DOI 10.1099/jmm.0.46155-0
Predictive value of oral colonization by Candida
yeasts for the onset of a nosocomial infection in
elderly hospitalized patients
S. Fanello,1 J. P. Bouchara,2 M. Sauteron,1 V. Delbos,1 E. Parot,1
A. Marot-Leblond,2 E. Moalic,3 A. M. Le Flohicc3 and B. Brangerd4
1
Correspondence
Department of Public Health, Faculty of Medicine, 49045 Angers Cedex 01, France
S. Fanello
2Host–parasite Interactions Study Group (UPRES-EA 3142), Laboratory of Parasitology and
sefanello@chu-angers.fr
Mycology, Angers University Hospital, 49933 Angers Cedex 9, France
3Department of Microbiology, Morvan University Hospital, 29609 Brest Cedex, France
4CCLIN OUEST, Pontchaillou University Hospital, 35033 Rennes Cedex, France
The incidence of nosocomial yeast infections has increased markedly in recent decades, especially
among the elderly. The present study was therefore initiated not only to determine the predictive
value of oral colonization by yeasts for the onset of a nosocomial Candida infection in elderly
hospitalized patients (>65 years), but also to clarify the factors that promote infection and to
establish a relationship between the intensity of oral carriage and the onset of yeast infection. During
this prospective cohort study, 256 patients (156 women and 100 men with a mean age of
83±8 years) were surveyed for yeast colonization or infection. Samples were collected every
4 days from day 0 to day 16 from four sites in the mouth, and intrinsic and extrinsic factors that might
promote infection were recorded for each patient. Pulsed ?eld gel electrophoresis was performed
on Candida albicans isolates from all infected patients. Poor nutritional status was observed in
81 % of the patients and hyposalivation in 41 %. The colonization level was 67 % on day 0 (59 %
C. albicans) and a heavy carriage of yeasts (>50 c.f.u.) was observed for 51 % of the patients.
The incidence of nosocomial colonization reached 6?9 % on day 4 (6?1 % on day 8 and 2?7 % on
day 12), and that of nosocomial infection was 3?7 % on day 4 (6?8 % on day 8, 11?3 % on day
12 and 19?2 % on day 16). Of the 35 patients infected, 57 % were suffering from oral candidiasis.
The principal risk factors for colonization were a dental prosthesis, poor oral hygiene and the use of
antibiotics. The risk factors for infection, in addition to those already mentioned for colonization,
were endocrine disease, poor nutritional status, prolonged hospitalization and high colony counts.
Genotyping revealed person-to-person transmission in two patients. Thus, this study demonstrates
a signi?cant association between oral colonization and the onset of yeast infections in elderly
hospitalized patients. Therefore, oral samples should be collected at admission and antifungal
treatment should be administered in cases of colonization, especially in patients presenting a heavy
Received 12 May 2005
carriage of yeasts. Genotyping of the strains con?rmed the possibility of person-to-person
Accepted 29 September 2005
transmission.
INTRODUCTION
from patient to patient or from healthcare staff to patient
(Fanello et al., 2001). Many scienti?c investigations have
Candidiasis, which accounts for 66–80 % of fungal infec-
dealt with nosocomial yeast infections, the frequency of
tions, is a super?cial or deep-seated infection caused by
which has increased steadily in recent decades from 6 %
opportunistic yeasts belonging to the genus Candida (Jarvis,
to more than 10 % (Beck-Sague & Jarvis, 1993). Moreover,
1995; Fridkin & Jarvis, 1996). Among all Candida species,
community-acquired infections have also been described in
Candida albicans is by far the most common in all clinical
hospitalized patients, where similar colonization levels of
forms of candidiasis, representing 70–80 % of all yeast iso-
about 35 % have been reported in two studies, regardless of
lates (Taylor et al., 1994; Jarvis, 1995; Wenzel, 1995). Since
the hospital department (Aly et al., 1991; Vazquez et al., 1993).
Candida is usually a commensal of the digestive tract, candi-
diasis mainly originates endogenously, but exogenous con-
Despite this extensive literature, little is known about
tamination may also occur, for example due to transmission
candidiasis in the elderly. In our geriatric department, we
46155 G 2006 SGM
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S. Fanello and others
found that Candida yeasts were responsible for a third of
the presence of diarrhoea, the exclusive detection of yeasts in the
nosocomial infections with an exclusively oral localization
microbiological examination of faeces samples and a cure resulting
(Boussarie et al., 1996). Further studies con?rmed these
from antifungal treatment.
data, showing colonization in 64 % of patients and a level of
All patient characteristics considered as risk factors for Candida
nosocomial contamination of 40 %, with oral infections
infection were recorded. Nutritional status was evaluated on the basis
predominating (Fanello et al., 2001). Oral candidiasis is
of anthropometric criteria, such as body mass index, triceps skin fold
therefore a frequent disease in the elderly (Vazquez et al.,
and brachial perimeter, and from biological data, i.e. serum albumin,
1993; Odds, 1979; Fanello et al., 2001) and may exacerbate
serum pre-albumin and C-reactive protein (Fanello et al., 2000).
an already precarious nutritional status in hospitalized
Physiological factors, such as the age of the patient, the presence of a
dental prosthesis and its ef?ciency, maceration and salivary ?ow
patients (Fanello et al., 2000).
(assessed as satisfactory, poor or uncertain), as well as underlying
diseases including diabetes, hypothyroidism, hypoparathyroidism,
However, whether these high levels re?ect only colonization
adrenal insuf?ciency and malignant disorders, were noted. Iatrogenic
or whether they also predict the onset of a super?cial or
factors were also recorded: systemic antibiotic therapy, atropine
disseminated infection is still a matter of debate. The present
therapy (responsible for oral dryness), psychotropic agents (neuro-
study was therefore conducted in order to determine the
leptics) and, in particular, chlorpromazine, phenothiazine and
predictive value of oral colonization by Candida yeasts for
imipramine, catheters and peripheral or central venous lines, urinary
the onset of candidiasis in elderly hospitalized patients.
catheters, radiotherapy of the ear, nose and throat area and cortico-
steroid therapy.
Given the possibility of exogenous contamination and
person-to-person transmission, it was necessary to check the
Statistical analysis of the data. Univariate analysis was per-
genotype homology of the isolates recovered from the same
formed in the ?rst instance using Pearson’s x2 test and odds ratio
patient, both during infection and before the onset of the
(OR) for qualitative variables, Fisher’s exact test when theoretical
infection. The secondary objectives were to determine the
populations were less than ?ve, Student’s t-test for quantitative vari-
intrinsic or extrinsic promoting factors and to establish a
ables and the Mann–Whitney test if the distribution of variables did
relationship between the intensity of yeast carriage and the
not follow a normal law or if the populations were less than 30.
onset of infection.
Multivariate analysis was performed in the second instance. The
logistic regression model was used as a variable to explain the presence
of an oral Candida infection. Variables statistically signi?cant at a 20 %
METHODS
threshold in the univariate analysis were introduced into the model to
select predictive factors independent of Candida infection.
Study design. This was a prospective cohort study, which received
the approval of the Ethical Committee of our University Hospital,
Considering a percentage of passage from colonization to infection of
conducted over a 16 month period (from November 2001 to
about 20 % (OR=2) and a colonization level of 60 %, the recruitment
February 2003) in 330 elderly patients hospitalized in an internal
of about 180 colonized patients was necessary and therefore 256
medicine ward orientated towards geriatrics.
patients were included in this study, with an 80 % probability
(a=0?005; bilateral test).
All patients over the age of 65 years hospitalized during the study
period, who were free of any clinical signs of fungal infection at
Biological study. Clinical samples were cultured on CHROMagar
admission and who agreed to the collection of samples, were included
Candida agar plates (Becton Dickinson), which facilitate the detec-
in this study.
tion of mixed populations of yeasts. For green colonies, which corre-
spond to C. albicans or Candida dubliniensis, differentiation between
The patients were informed about the methods for sample collection
these two species was performed using a Bichro-Dubli latex kit
and signed an informed consent form. Oral samples were taken on day
(Fumouze Laboratory). This latex co-agglutination card test, avail-
0 and then every 4 days until day 12, after which they were collected
able for the direct identi?cation of C. dubliniensis from colonies, is
once a week. In order to avoid swallowing dysfunctions due to oral
based on the agglutination of blastospores with coloured latex parti-
rinses, samples were obtained by swabbing the anterior and exterior
cles coated with a monoclonal antibody speci?c to the cell-surface
surfaces of the tongue, the gingivolingual groove and the palate. In
antigen of C. dubliniensis. For colonies of another colour, biochemi-
addition, a fourth sample was acquired from the dental prosthesis of
cal identi?cation was performed using ID32C strips (bioMe´rieux).
denture wearers. A heavy carriage of yeasts was de?ned by the detection
of more than 50 c.f.u. from these samples, as described previously
Isolates from patients infected by C. albicans were compared with those
(Fanello et al., 2001).
obtained from the same patient before the onset of the infection. To do
this, isolates were typed by pulsed ?eld gel electrophoresis with the
In the case of a clinical suspicion of candidiasis, additional samples
transverse alternating ?eld electrophoresis technique, which has shown
were examined: swabbing of inguinal folds, urine (spontaneous speci-
its validity and discriminatory power for various yeast species
men collected after local cleansing, sampling from urinary catheter if
(Defontaine et al., 1996).
present or sterile minute specimen when required for medical reasons),
stools (fresh stools or anal swabbing), bronchial aspirations and blood
in the case of fever.
RESULTS AND DISCUSSION
The criteria for exclusion were: patients aged less than 65 years, clinical
signs of candidiasis at admission, patient refusal or the impossibility of
Study population
systematic sampling.
This study involved 256 patients over a period of 16 months.
The diagnosis of oral or urinary infection was based on the criteria
Of these, 195 patients were colonized, representing 97?5 %
proposed by Bodey (1993). A digestive candidiasis was suspected from
of the expected number of colonized patients. Twenty
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Oral colonization by yeasts in the elderly
dossiers could not be analysed because of the lack of some
clinical samples.
The cohort comprised 100 men and 156 women. Of these,
99 % were admitted via the Emergency Room. Two-thirds
came from their homes, whilst 31 % came from an institu-
tion. The body mass index was signi?cantly lower among the
women. The level of malnutrition or poor nutritional status,
mainly due to exogenous undernourishment (85 %), was
identical in the two sexes (about 80 %). All social and
anthropometric data are summarized in Table 1.
The dominant pathologies encountered were cardiac, pneu-
monological and neurological diseases, which accounted
for more than 60 % of diagnoses. Antibiotic therapy was
being received by 35?2 % of patients (70 % amoxicillin alone
or associated with clavulanic acid, and 20 % quinolones).
Their medical histories revealed cancer (21?5 %) or diabetes
Fig. 1. Risk of oral colonization by yeast (open circles) and
(12 %), and 15 % of patients were being treated with
yeast infection (closed circles) according to the duration of
psychotropic agents. Invasive procedures included periph-
hospitalization.
eral lines (36 % of patients), central lines (2 %) and urinary
catheters (5?5 %).
isolates, was by far the most common yeast isolated, whilst
Frequency of oral colonization or infection by
C. dubliniensis was recovered from only four patients.
Candida yeasts
During the study period, 35 patients presented with a noso-
Because of the variable duration of hospitalization, second
comial yeast infection. Twenty of these had an oral infection
samples were obtained from 178 of the original 256 patients
diagnosed from the following clinical signs: perleche (60 %),
(69?5 %), third samples from 45 % of patients and fourth
smooth glossal atrophy (30 %) and thrush (10 %). Two of
samples from 24 % of patients. A colonization level of 67 %
them also presented an inguinal skin fold infection or
was observed at admission and analysis of the subsequent
pressure sores. Seventy-?ve per cent of the patients were
samples revealed similar colonization levels of 71–72 %.
treated orally with amphotericin B, whilst ?uconazole was
Thus, the incidence of nosocomial colonization (newly
used for the other patients. There was no systemic com-
colonized cases) reached 6?9 % for days 0–4, 6?14 % for days
plication. The time to the onset of the infection was
4–8 and 2?7 % for days 8–12 (Fig. 1). The distribution of
8±5 days (Fig. 1).
Candida isolates as a function of species is shown in Table 2.
Candida albicans, which accounted for 59 % of all yeast
Other infected patients (15) mainly presented an inguinal
(six patients) or digestive (two patients) yeast infection.
These patients were treated with ?uconazole and a cure was
Table 1. Anthropometric data
achieved in 76?5 % of cases. Two deaths occurred in the
cohort, due to a Candida lung infection and to Candida
Percentages are expressed relative to the total number of patients
pyelonephritis. The time to the onset of the infection was
examined.
9±5 days. The incidence level of nosocomial infection was
3?7 % for the ?rst period, 6?8 % for the second period,
Parameter
Value
11?3 % for the third period and 19?2 % for the fourth period.
Total number of patients
256
Age (years)
82±8
Of the 35 infected patients, 23 were infected by C. albicans
Weight (kg)
66±16
(66 %) and no C. dubliniensis was recovered from these
Height (cm)
162±9
patients. Genotype analysis of these isolates revealed homo-
Body mass index (height weight22)
25±5
logies between two patients, demonstrating person-to-
Well nourished (%)
18
person transmission. For all patients but one, the same
Poor nutritional status (%)
68
genotype was found from clinical samples obtained during
Hyposalivation (<1 ml min21) (%)
42
the infection and before the onset of the infection, thus
Dental prosthesis (%)
51
attesting the endogenous origin of the infection.
Oral hygiene: (%)
Two previous studies carried out in our University Hospital
Satisfactory
41
Poor
17
revealed the importance of yeasts in nosocomial infections
Uncertain
42
(Boussarie et al., 1996; Fanello et al., 2001). The level of
nosocomial infections reached about 20 %, with an oral
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S. Fanello and others
Table 2. Characteristics of oral colonization observed from the four samples
Characteristic
Day 0
Day 4
Day 8
Day 12
(n=256)
(n=178)
(n=115)
(n=62)
Colonization (%)a*
67
72
71
71
Nosocomial colonization (%)a
–
6?9
6?1
2?7
Heavy carriage of yeasts (%)b
51
51
49
45
Association of at least two yeast species: (%)b
Palate
23
27?4
28
26
Tongue
26
27?7
27
28
Gums
27
28?4
29
37
Dental prosthesis
42
39?6
44
41
Candida species: (%)c
C. albicans
59
54?5
52
53
C. glabrata
15
17?5
14?5
24
C. tropicalis
13?5
14
14?5
9
Others
12?5
14
19
14
*Results correspond to percentages of the total number of patients examined (a), positive patients (b) and
yeasts isolated (c).
localization in 80 % of the cases, as also noticed in other
signi?cant link between the intensity of carriage and the
studies (Eggimann et al., 2003; Grimoud et al., 2003; Lizioli
onset of yeast infections. The predominance of C. albicans
et al., 2003). Moreover, in agreement with other studies
was regular (54–60 %), as in most previous studies per-
(Boccia et al., 2002; Khan et al., 2003; Vazquez et al., 1993),
formed on hospitalized patients (Ellis et al., 2000) or on
we con?rmed the possibility of person-to-person transmis-
healthcare workers (Bonassoli & Svidzinski, 2002).
sion of C. albicans and the high level (64 %) of oral coloni-
zation by yeasts at admission of the patients. Here, we have
Risk factors
provided additional information, since we not only estab-
lished a link between oral colonization and the onset of
Table 3 shows the different links observed in colonized
candidiasis, but also speci?ed the risk factors for coloniza-
patients. Nutritional status, salivation or underlying disease
tion and for infection.
was not linked to colonization by yeasts. After logistic
regression, three factors were still statistically linked to
During the present study, we found that colonization
colonization: poor oral hygiene, the wearing of a dental
affected two-thirds of the patients, as previously reported in
prosthesis and the presence of a peripheral line, as previously
long-term geriatric care units (Grimoud et al., 2003). As for
reported (Shay et al., 1997). However, although the presence
the incidence of yeast infections, this exceeded that found in
of a peripheral line could not alone explain colonization,
an intensive care unit (7?7 %) by Lupetti et al. (2002).
it is conceivable that patients requiring a line presented with
However, this survey focused on deep-seated infections.
an acute pathology at admission and required antibiotic
More importantly, half of the colonized patients were heavy
therapy (a factor that disappeared after regression). Simi-
carriers (higher than 50 c.f.u.), thus con?rming the previous
larly, there was a signi?cant link between colonization of the
?ndings of Akpan & Morgan (2002), and we found a
palate and the wearing of a dental prosthesis.
Table 3. Risk factors linked statistically to yeast colonization
CI, Con?dence interval; ND, not determined; NS, not signi?cant.
Risk factor
x2 test
Logistic regression
Signi?cance
OR
95 % CI
Signi?cance
OR adjusted
Dental prosthesis
0?008
1?2
1?0<OR<1?3
0?03
2
Peripheral line
0?015
1?2
1?0<OR<1?3
0?014
2?3
Antibiotic therapy
0?048
1?15
1?0<OR<1?3
NS
ND
Poor oral hygiene
0?0001
ND
ND
0?002
ND
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Oral colonization by yeasts in the elderly
Table 4. Risk factors linked statistically to the onset of a nosocomial yeast infection
See Table 3 for abbreviations.
Risk factor
x2 test
Logistic regression
Signi?cance
OR
95 % CI
Signi?cance
OR adjusted
De?cient pre-albumin
0?006
3?6
1?3<OR<9?8
NS
ND
De?cient albumin
0?006
2?8
1?3<OR<6?2
NS
ND
Underlying endocrine disease
0?027
2?4
1?2<OR<5?2
0?03
11?1
Antibiotic therapy
0?011
2?2
1?2<OR<4?1
NS
ND
Prolonged hospitalization
0?008
2?1
1?3<OR<3?5
NS
ND
Underlying lung disease
0?004
1?8
1?1<OR<3?1
NS
ND
Heavy carriage of yeasts
0?0001
1?6
1?4<OR<2
0?004
9?44
Colonization
0?0004
1?4
1?3<OR<1?5
NS
ND
Poor oral hygiene
0?014
ND
ND
NS
ND
Poor nutritional status
0?014
ND
ND
NS
ND
Among the main variables statistically linked to the onset
made up of elderly patients hospitalized for a community-
of nosocomial yeast infection (Table 4), only two factors
acquired infection and receiving probabilistic antibiotic
remained statistically linked to nosocomial yeast infections
therapy. They also often wear dental prostheses. Faced with
after logistic regression: the existence of endocrine disease
these elements, swabbing of the mouth should be performed
and a heavy carriage of yeasts. As for diabetes, this factor
to detect any yeast colonization. If the results are positive,
appeared at the limit of signi?cance retained.
and particularly in the case of a heavy oral carriage of yeasts
(>50 c.f.u.), such elderly patients could bene?t from anti-
In patients harbouring at least two yeast species, the main
fungal therapy. Some therapeutic regimens have been pro-
risk factors were, after logistic regression, the presence of a
posed, depending on the identi?ed yeast (Shay et al., 1997)
dental prosthesis and a heavy carriage of yeasts. In addition,
and on the endogenous or exogenous origin of colonization
the risk factors statistically linked to a heavy carriage of
(Pfaller, 1996). A clinical study showed that prophylactic
yeasts are shown in Table 5. After logistic regression, these
treatment with ?uconazole reduced the risk of nosocomial
were found to be the use of psychotropic agents and a
infection by 55 % in a surgical intensive care unit (Pelz et al.,
hospitalization time longer than 3 weeks.
2001). However, the risks and bene?ts of prophylactic
treatment in elderly patients remain to be determined and
In conclusion, the results of the present study con?rmed the
the possibility of the development of resistance to antifungal
high prevalence of oral colonization by yeasts in patients
agents among yeasts in the genus Candida needs to be
hospitalized for an acute pathology in an internal medicine
considered.
ward. The levels of nosocomial yeast infections rose steadily
during hospitalization. A link was established between
colonization and fungal infection, as well as with the inten-
ACKNOWLEDGEMENTS
sity of carriage. In addition, this study enabled the de?nition
This work was supported by a grant from the Programme Hospitalier
of an elderly population at high risk of colonization and of
de Recherche Clinique du Ministe`re des Solidarite´s de la Sante´ et de la
subsequent nosocomial yeast infection. This population is
Famille (PHRC 2001) and from CCLIN Ouest.
Table 5. Risk factors linked statistically to a heavy carriage
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