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Digestive and Liver Disease 46 (2014) 1086–1092
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Digestive and Liver Disease
journal homepage: www.elsevier.com/locate/dld
Alimentary Tract
Prevalence and risk factors of Clostridium difficile infection in patients
hospitalized for flare of inflammatory bowel disease: A retrospective
assessment
Helene Regnault a,∗ , Anne Bourrier a , Valerie Lalande b , Isabelle Nion-Larmurier a ,
Harry Sokol a , Philippe Seksik a , Frederic Barbut c , Jacques Cosnes a , Laurent Beaugerie a
a
Department of Gastroenterology, APHP, Saint-Antoine Hospital, Paris, France
Department of Microbiology, APHP, Saint-Antoine Hospital, Paris, France
c
National Reference Laboratory for C. difficile, Paris, France
b
a r t i c l e
i n f o
Article history:
Received 14 March 2014
Accepted 4 September 2014
Available online 5 October 2014
Keywords:
Clostridium difficile infection
Inflammatory bowel disease
Nonsteroidal anti-inflammatory drugs
a b s t r a c t
Background: Recent studies have identified a high frequency of Clostridium difficile infections in patients
with active inflammatory bowel disease.
Aims: To retrospectively assess the determinants and results of Clostridium difficile testing upon the admission of patients hospitalized with active inflammatory bowel disease in a tertiary care centre and to
determine the predicting factors of Clostridium difficile infections.
Methods: We reviewed all admissions from January 2008 and December 2010 for inflammatory bowel
disease flare-ups. A toxigenic culture and a stool cytotoxicity assay were performed for all patients tested
for Clostridium difficile.
Results: Out of 813 consecutive stays, Clostridium difficile diagnostic assays have been performed in 59% of
inpatients. The independent predictive factors for the testing were IBD (ulcerative colitis: OR 2.0, 95% CI
1.5–2.9; p < 0.0001) and colonic involvement at admission (OR 2.2, 95% CI 1.5–3.1, p < 0.0001). Clostridium
difficile infection was present in 7.0% of the inpatients who underwent testing. In a multivariate analysis,
the only independent predictor was the intake of nonsteroidal anti-inflammatory drugs within the two
months before admission (OR 3.8, 95% CI 1.2–12.3; p = 0.02).
Conclusions: Clostridium difficile infection is frequently associated with active inflammatory bowel disease. Our study suggests that a recent intake of nonsteroidal anti-inflammatory drugs is a risk factor for
inflammatory bowel disease -associated Clostridium difficile infection.
© 2014 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.
1. Introduction
Clostridium difficile (C. difficile) is a Gram-positive anaerobic
spore-forming bacterium that produces toxins. It is responsible for
a spectrum of clinical presentations, ranging from asymptomatic
carriage to clinically significant diarrhoea, fulminant colitis, sepsis
and death [1,2]. Risk factors for C. difficile infections (CDI) traditionally include antibiotic use, age, severe comorbidities or contact
with healthcare facilities. An alarming trend of increased incidence
and severity of CDI over the past several years has been reported
worldwide, along with an increased duration of hospitalization and
costs [3,4]. As an example, the estimated costs attributed to CDI
∗ Corresponding author at: Service de Hépatogastroentérologie, Groupe Hospitalier Pitié-Salpétrière, 47-83 boulevard de l’hôpital, 75651 Paris Cedex, France.
Tel.: +33 1 42 16 10 34; fax: +33 1 42 16 14 25.
E-mail address: [email protected] (H. Regnault).
alone are approximately 3.2 billion dollars per year in the United
States [5].
It is particularly difficult to diagnose CDI in patients with inflammatory bowel disease (IBD; Crohn’s disease (CD), ulcerative colitis
(UC)), because the presentation is similar and consists of abdominal
pain and diarrhoea. Indeed, CDI can mimic a flare of the disease, but
can also trigger a relapse that could evolve on its own, regardless of
the treatment of the infection [6,7]. The relationship between CDI
and IBD flares has been recognized as an emerging problem. Several
retrospective studies on large populations have suggested a rise in
the rate of CDI among patients with IBD along with an increase in
disease severity. For example, the incidence of CDI among hospitalized patients with IBD increased from 1.8% in 2004 to 4.6% in
2005 [8]. CDI appeared to be three times more frequent in patients
with UC than in patients with CD, but the percentage of patients
who were tested for C. difficile was not specified [9–12]. CDI was
associated with an increased severity of relapse, an increase in the
number and length of hospital stays, higher rates of colectomy, and
http://dx.doi.org/10.1016/j.dld.2014.09.003
1590-8658/© 2014 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.
H. Regnault et al. / Digestive and Liver Disease 46 (2014) 1086–1092
1087
IBD patients hospitalized with the associate stay codes:
Crohn’s disease (K50) or ulcerative colitis (K51)
(n= 833)
Verification of inclusion criteria in
medical records or reports of
hospitalization
Non IBD patients
(n= 2)
IBD patients without IBD flare
(n= 18)
IBD patients hospitalized for flare
(n= 813)
Fusion with the microbiological
requests
Clostridium difficile
(CD) testing
(n= 480)
CD infection (CDI)
(n= 34)
IBD relapse without
CDI
(n= 443)
No CD testing
(n= 333)
Non toxinogenic CD
(stool culture +, toxine -)
(n=3)
Fig. 1. Flow chart of case definitions in all hospitalized patients for inflammatory bowel disease flares from 2008 to 2010. IBD, inflammatory bowel disease; CD, Clostridium
difficile; CDI, clostridium difficile infection.
a four-fold increase in mortality [9,10]. In these studies, infection
in patients with IBD was predominantly community-acquired, in
contrast to the general inpatient population where CDI is primarily
acquired within the healthcare setting itself [8,12].
To date, the risk factors for CDI in patients with IBD are not firmly
established. Some authors have tried to identify them in cohorts
that may not necessarily be representative of the study population because they have included all hospitalized patients, whereas
they should have included only patients who were tested for C.
difficile. In our tertiary center, C. difficile testing upon the admission of a patient for an IBD flare has been gradually introduced as a
routine procedure. This allowed us to conduct this study with two
objectives: first, to assess the frequency and the determinants of
C. difficile testing upon the admission of patients hospitalized for a
flare of IBD, and second, to identify risk factors for CDI in patients
hospitalized for a flare of IBD.
2. Methods
2.1. Study population and variables
Our study population consisted of all patients hospitalized for
IBD flares in the Gastroenterology Department of the Saint-Antoine
IBD center from 1 January 2008 to 31 December 2010. We used
data from the department of medical information and established
a list of all the consecutive stays with the following WHO codes: K
50 (CD) and K 51 (UC). In parallel, using hospitalization reports,
we identified all patients with an established diagnosis of IBD
and symptoms of active IBD (diarrhoea with possible presence of
blood/mucus and/or abdominal cramps) and who were tested for
C. difficile between 1 January 2008 and 31 December 2010. Those
two lists were merged to identify patients who were both hospitalized with a flare of IBD and tested for C. difficile. A systematic
verification of inclusion criteria was made from reports of hospitalization and/or from medical records. Patients without active IBD
at admission were excluded (Fig. 1).
Demographic characteristics included gender, age and body
mass index (BMI) classified into three groups (BMI <18.5: underweight, BMI between 18.5 and 25: normal weight, BMI >25:
overweight and obesity). Comorbidity was adjusted using the
Charlson index, a well-validated mortality prognosis index [13].
Other considered risk factors were current smoking status at admission, history of appendectomy or ICD. Medication use included
chronic use of proton pump inhibitors (PPIs), anti-inflammatory
drugs (NSAIDs) or antibiotics within the two months prior to hospitalization. We recorded disease characteristics including the type
of IBD (i.e., CD or UC), anatomic distribution of the disease (isolated small bowel vs. colonic involvement < or >50%, perianal
lesions), the duration of disease from diagnosis and any history of a
previous surgical resection (segmental or total colectomy, ileocecal
resection). We also recorded the type of therapy, including corticosteroid use within the two months prior to hospitalization, which
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H. Regnault et al. / Digestive and Liver Disease 46 (2014) 1086–1092
allowed us to classify patients into 3 groups: group 1 = no steroids,
group 2 = between 20 and 40 milligrams of prednisolone or budesonide equivalent, group 3 = 40 milligrams or more of prednisolone
equivalent. Other therapies included immunomodulators (azathioprine, 6-mercaptopurine), methotrexate and anti-TNF (infliximab,
adalimumab, certolizumab). Data on the IBD flare-ups included
the date of admission, length of stay, and white blood cell
count.
2.2. C. difficile testing
In our tertiary-care center, the diagnosis of CDI systematically
involved a stool culture on selective medium and a stool cytotoxicity assay. In the case of a positive culture and a negative
stool cytotoxicity assay, a toxigenic culture (in vitro determination of the ability of the isolate to produce toxins) was performed.
CDI was defined either by a positive stool toxigenic culture and a
positive stool cytotoxicity assay or, in cases of negative stool cytotoxicity assays, a positive toxigenic culture [14,15]. In accordance
with the definition generally admitted in the literature, CDI was
defined as community-acquired if the patient had a positive C. difficile test within 48 h following admission and no hospitalization
in the two months prior to the current admission. CDI was considered hospital-acquired if patients were hospitalized in the two
months prior to the current admission or if their test results were
positive during their hospital stay after a negative result from the
initial test performed at admission. Finally, if CDI testing had been
conducted after three days in the absence of available data at the
time of hospital admission, the origin of the CDI was defined as
indeterminate.
For patients with CDI, complementary data were recorded,
including clinical data (existence of fever, diarrhoea, rectal bleeding), biological data (serum levels of C-reactive protein, albumin),
severity of endoscopic criteria (false membranes, ulcerations covering more than half of the circumference, mucosal detachment),
and the index of activity (for CD, a Harvey-Bradshaw score
higher than 12 defines severe CD [16], while for UC, a Lichtiger
score greater than 10 defined severe acute UC [17]). We also
recorded the following types of therapy and treatments: empiric
antibiotics (e.g., fluoroquinolone or metronidazole), CDI treatment (e.g., metronidazole or vancomycin), corticosteroids and
maintenance or intensification of immunosuppressive therapy
(including methotrexate, azathioprine, 6-mercaptopurine, antiTNF␣). Finally, we recorded any surgical treatment or death.
2.3. Statistical analysis
The data were processed using Statview®
software (version 5.0,
SAS Institute Inc., Cary, NC). The results of the quantitative variables are expressed as a median and an interquartile range. The
qualitative variables are expressed as numbers and percentages.
To identify the predicting factors of CDI testing, a univariate analysis was performed using the 2 test and Fisher’s exact test, when
necessary. The variables were as follows: age, gender, BMI, Charlson
index, type of IBD, colonic involvement upon hospital admission,
duration of disease, current smoking status, CDI therapy (e.g., corticosteroid equivalent dose equal to or greater than 20 milligrams of
prednisolone, immunosuppressants), antibiotics, PPIs and NSAIDs
used in the previous two months prior to admission and white
blood cell count. For the purpose of the analysis, quantitative variables were dichotomized around the median. A p value less than
0.05 was considered statistically significant. The variables with p
values <0.35 in the univariate analysis were entered in a multivariate logistic regression analysis using a backward stepwise
procedure. To assess the predictors of CDI among the patients who
were tested, univariate and multivariate analyses were made from
the above variables using the same statistical procedure.
3. Results
3.1. Characteristics of the study population
A total of 813 hospital stays from 1 January 2008 to 31 December
2010 corresponding to 584 patients were analyzed. In all, 104,
23, 16, 3, 3 and 1 patients completed 1, 2, 3, 4, 5, 6 and 7 stays,
respectively. Table 1 shows the demographic characteristics of the
patients. There were more women than men hospitalized for IBD
flares in this study, both in the group with CD and in the group with
UC. Approximately two thirds of the patients had CD (n = 538) and
one third had UC (n = 77). A majority of the patients had extensive
colitis, which was observed in patients with both CD (50, 5%) and
in those with UC (72, 4%). Tobacco use was noted in 229 patients
with CD (43%) and in 50 with UC (18%). Approximately two thirds
of the patients were receiving immunosuppressive treatment at
the time of admission, either corticosteroids, immunomodulators
or anti-TNF drugs. NSAIDs use, including only non-selective Cox
inhibitors, was noted in 27 patients.
3.2. C. difficile testing rate and predictors for CDI testing
C. difficile testing within 48 h of admission for patients hospitalized for an IBD flare was performed in 483 (59%) of the 813
patients. By univariate analysis, C. difficile testing did not vary significantly according to gender or age (Table 2). Predictive factors for
C. difficile testing within 48 h of admission were UC (p < 0.0001) and
colonic involvement attributed to IBD on admission (p < 0.0001). By
multivariate analysis, the two independent predictors for C. difficile
testing on admission in patients hospitalized for an IBD flare were
UC (OR 2, 95% CI 1.5–2.9, p < 0.0001) and colonic involvement (OR
2.2, 95% CI 1.5–3.1, p < 0.0001).
Table 1
Characteristics of patients admitted for a flare-up of inflammatory bowel disease.
Gender, n (%)
Male
Age (years)
Median (range)
Number of patients, n
2008
2009
2010
Body mass index
Median (range)
Duration of disease (years)
Median (range)
Crohn’s disease
(n = 534)
Ulcerative
colitis (n = 279)
236 (44.2)
125 (44.8)
31 (25–43)
180
199
155
33 (24–46)
88
94
97
20 (18–22)
21 (19–24)
7 (2–14)
5 (2–10)
Extent of disease, n (%)
Ileal
Colonic <50%
Colonic >50%
Anoperineal
424 (79)
20 (3.7)
270 (50.5)
238 (44.5)
24 (8.6)
63 (22.5)
202 (72.4)
45 (16)
Charlson comorbidity index
Median (range)
Smoking, n (%)
2 (1–3)
229 (43)
2 (1–3)
50 (18)
Inflammatory bowel disease –related medication, n (%)
90 (16.8)
1. Corticosteroids >20 mg
152 (28.4)
2. Immunomodulators
129 (24.1)
3. Anti-TNF 1 or 2 or 3
371 (69.4)
94 (33.7)
44 (15.7)
67 (24.0)
205 (72.4)
H. Regnault et al. / Digestive and Liver Disease 46 (2014) 1086–1092
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Table 2
Characteristics of patients with or without Clostridium difficile testing at admission (univariate analysis).
Clostridium difficile testing (n = 483)
Age (years)
Median (range)
32 (25–43)
No Clostridium difficile testing (n = 330)
31 (24–44)
p
0.74
Gender, n (%)
Male
220 (45.5)
142 (43)
0.69
Body mass index, n (%)
<18.5
18.5–25
>25
114 (23.6)
289 (59.8)
80 (16.5)
84 (25.4)
192 (58.1)
54 (16.3)
0.72
2 (1–3)
0.63
Charlson index
Median (range)
2 (1–3.25)
Inflammatory bowel disease type, n (%)
Crohn’s disease
Ulcerative colitis
277 (57.3)
206 (42.7)
259 (78.4)
71 (21.6)
< 0.0001
Colonic involvement, n (%)
364 (75.3)
191 (57.8)
< 0.0001
Smoking, n (%)
155 (32.1)
123 (37.3)
0.12
History of Clostridium difficile infection, n (%)
14 (3.4)
4 (0.9)
0.11
Community context, n (%)
439 (90.7)
301 (91.5)
0.36
Maintenance therapy, n (%)
Corticosteroidsa
Immunosuppressants
111 (22.9)
244 (49.8)
73 (22.1)
168 (50.9)
0.71
0.94
Antibiotics, n (%)b
122 (25.2)
69 (20.9)
0.34
Proton pump inhibitors, n (%)
54 (11.2)
47 (14.2)
0.21
Nonsteroidal anti-inflammatory drugs, n (%)b
19 (3.9)
8 (2.4)
0.18
White blood cell count
Median (range)
8340 (6100–11,270)
8295 (6205–11,580)
0.9
p is significant if <0.05.
a
>20 milligrams prednisolone equivalent.
b
In the two months prior to the admission.
3.3. Characteristics of CDI and predictors for CDI
CDI was detected in 34 patients, representing 4.1% of all stays
over the three years that were included in our study and 7% of stays
in which C. difficile testing was performed (Table 3). In a univariate
analysis, the predictors of CDI for patients who were tested were
a BMI <18.5 or >25, NSAID intake within the two months prior to
admission, and a high white blood cell count. In a multivariate analysis, the only independent risk factor was NSAID intake within 2
months prior to admission (OR 3.8, 95% CI 1.2–12.3, p = 0.02).
Of the 34 cases of CDI, 19 were community-acquired, 8 were
healthcare-associated, and 7 were undetermined infections. Characteristics of patients who developed one of the three types of
CDI are detailed in Table 4. IBD was active by definition in the
three groups. Of the 19 community-acquired infections, 11 patients
had an endoscopy, three of which revealed pseudomembranes
along with three additional endoscopic severity criteria. All patients
had been treated for CDI with either oral metronidazole or oral
vancomycin. Approximately half of them had received corticosteroids in addition to antibiotics. Background therapy was changed
in 6 of 19 patients. In the case of healthcare-associated infections,
the activity of IBD met the criteria for severity in the majority of
cases. The majority of patients had been diagnosed with UC, and no
pseudomembranes were reported on endoscopic examination.
4. Discussion
Our study shows that CDI occurs in 7% of patients with IBD who
are hospitalized for flares and tested for C. difficile. We also found
that recent intake of NSAIDS is an independent predictor for CDI.
Presently, there is no consensus methodology for the diagnosis
of CDI in a population of patients with IBD. In the general population, the definition encompasses clinical criteria (acute diarrhoea
for more than two days), bacteriological criteria (positive detection of toxins in the stool or isolation of a toxigenic strain) and/or
endoscopic pseudomembranes [18]. Clinical criteria are difficult to
interpret in patients with IBD because diarrhoea is also a symptom
of a flare. In addition, colonization with C. difficile was demonstrated more frequently in patients with quiescent IBD compared
to healthy subjects (7% CD, 9% UC, 1% controls) [19]. Various experts
claim that there is an association between toxin detection in stool
and toxigenic culture in the general population. In our study, we
applied this strategy using both complementary techniques to confirm the diagnosis in symptomatic patients. We believe that these
methodological conditions were optimal to assess the frequency,
impact and risk factors for CDI in patients hospitalized for IBD flares
and who were tested for CDI.
In this retrospective study that ended in December 2010, just
before generalization of CDI testing in our centre, we found that
testing for CDI was performed primarily in patients with UC and in
those with colonic involvement at admission; this was most likely
influenced by several studies that designated these two characteristics as risk factors for CDI [8,12]. In fact, the results of these
initial studies were biased because the statistical analysis was not
restricted to those patients in whom C. difficile testing was performed. A review of more recent literature that assessed 42 studies
is in agreement with our findings: the incidence of CDI was the
same for patients with UC and for those with CD and was the same
in patients hospitalized for a flare of the disease and among those
who were asymptomatic [20]. In another study, the increase in
the prevalence of CDI was similar in patients with UC compared
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H. Regnault et al. / Digestive and Liver Disease 46 (2014) 1086–1092
Table 3
Characteristics of patients with or without Clostridium difficile infection (univariate analysis).
Clostridium difficile infection (n = 34)
No Clostridium difficile infection (n = 449)
p
Age (years)
Median (range)
33 (22–46)
Gender, n (%)
Male
17 (50)
246 (55.1)
0.58
Body mass index, n (%)
<18.5
18.5–25
>25
11 (32.3)
14 (41.2)
8 (23.5)
103 (23)
275 (61.6)
57 (12.7)
0.04
Charlson index
Median (range)
32 (25–44)
0.85
3 (2–5)
2 (1–3)
0.85
Inflammatory bowel disease type, n (%)
Crohn’s disease
Ulcerative colitis
20 (58.8)
14 (41.2)
258 (57.8)
191 (42.2)
0.85
Colonic involvement, n (%)
27 (79.4)
337 (75.5)
0.58
Duration of disease
Median (range)
Smoking, n (%)
4 (2–6)
6 (2–13)
0.26
11 (32.3)
144 (32.2)
0.97
2 (5.8)
16 (3.5)
0.37
Maintenance therapy
Corticosteroidsa
Immunomodulatorsb
Anti-TNF
Total (%)
8
8
9
25 (73.5)
103
121
108
332 (73.9)
0.93
Antibiotics, n (%)
History of Clostridium difficile infection, n (%)
12 (35.3)
110 (24.5)
0.16
Proton pump inhibitors, n (%)
3 (8.8)
51 (11.3)
0.64
Nonsteroidal anti-inflammatory drugs, n (%)
4 (11.7)
15 (3.3)
0.01
White blood cell count
Median (range)
9900 (7200–12,320)
8235 (6088–11,315)
0.0037
p is significant if <0.05.
a
>20 milligrams prednisolone equivalent.
b
In the two months prior to the admission, immunomodulators include azathioprine, methotrexate and purinethol.
to those with CD and colonic involvement [21]. In our study, UC
and colonic involvement were not risk factors for CDI.
We acknowledge that in our retrospective study, only 59% of
the patients admitted for active IBD were tested for CDI, which
introduced a selection bias of the population tested. Due to this
selection bias, our study population cannot be considered as
representative of the patients admitted for IBD flare. However,
our multivariate analysis for identifying risk factors of CDI was
restricted to patients tested for CDI and well-phenotyped. This
‘denominator’ was accurate, in contrast to most of the studies published to date that considered together in the search for risk factors
of CDI patients tested and not tested for CDI.
We found that recent use of NSAIDs was an independent predictor for CDI even we remain cautious with this result because
of the small number of patients. NSAIDs operate by inhibiting
cyclooxygenase (COX), which is an enzyme capable of producing
anti-inflammatory prostaglandins [22]. They alter the intestinal
barrier, especially by modifying the microcirculation and increasing its permeability [23]. NSAIDs can promote acute diarrhoea in
the general population [24] but can also trigger severe acute colitis
that may be fatal [25,26]. In most cases, NSAIDs trigger or aggravate infectious or inflammatory colitis. Several studies have shown
that the use of NSAIDs can also trigger or exacerbate a flare-up of
IBD [27–29]. Conflicting results have been published that emphasize that NSAID use is not associated with an increased likelihood of
active disease in an outpatient population with IBD [30]. However,
a prospective trial showed that NSAIDs triggered a flare in approximately 20% of patients with quiescent disease [31]. In accordance
with these data, some American scientific societies have considered
that the evidence of the deleterious effects of NSAIDs was obvious
enough to recommend that patients with CD avoid these drugs [32].
In our study, antibiotic use within the eight weeks before admission to the hospital was not recognized as an independent risk
factor for CDI, contrary to the findings in the general population
[33]. Only 35% of patients with CDI had received antibiotic treatment within the two months before admission, which is similar
to findings in previous publications [34]. Similarly, a recent study
showed that 61% of patients who developed community-acquired
CDI had not been exposed to antibiotic treatment within the three
months prior to the infection [35]. The difference with the general population is most likely because patients with IBD usually
acquire CDI outside of the hospital and are less exposed to antibiotic
treatment.
Healthcare-associated CDI were not uncommon in our study
population. They mostly involved patients who suffered from UC
that was complicated by severe acute colitis in the majority of cases
and who were previously treated with corticosteroids. The diagnosis was sometimes made after repetitive C. difficile testing, usually
if clinical deterioration occurred.
Our study shows that CDI is frequently associated with flare-ups
of IBD that require hospitalization. This justifies systematic testing
patients with IBD for CDI upon their admission to the hospital. Furthermore, we found that CDI was diagnosed after several previous
negative test results during a hospitalization. A change in practice
should logically move towards a systematic way to detect CDI upon
admission of patients with IBD flares and be repeated in cases of
worsening digestive symptoms during the hospital stay. We also
show that the use of NSAIDs in the two months prior to admission
H. Regnault et al. / Digestive and Liver Disease 46 (2014) 1086–1092
1091
Table 4
Characteristics of patients hospitalized for inflammatory bowel disease flare with Clostridium difficile infection.
Community- acquired Clostridium
difficile infection* (n = 19)
Crohn’s disease, n (%)
Healthcare- associated Clostridium
difficile infection ** (n = 8)
Indeterminate Clostridium
difficile infection*** (n = 7)
13 (68.4)
3 (37.5)
3 (43)
Ulcerative colitis, n (%)
6 (31.5)
5 (62.5)
4 (57)
Duration of disease (years)
Median (range)
Severe flare of Crohn’s disease**** , n (%)
4.58
5 (38.4)
3.70
2 (66.7)
3.95
1 (33.3)
Severe flare of Ulcerative colitis***** , n (%)
4 (67)
3 (60)
1 (25)
Charlson index
Median (range)
0.5
3
11 (57.9)
3 (15.8)
3 (15.8)
7 (87.5)
0
1 (12.5)
4 (57)
0
1 (14.3)
Probabilistic antibiotherapy, n (%)
• Metronidazole
• Fluoroquinolones
Corticosteroids, n (%)
7 (37)
6
5
9 (47)
1 (12.5)
1
1
4 (50)
1 (14)
1
0
3 (43)
Intensification or maintenance of
immunosuppressive drugs, n (%)
• Immunomodulatorsa
• Anti-TNF
6 (31.5)
6 (75)
1 (14)
4
3
3
5
0
1
Endoscopic features, n (%)
• Pseudomembranes
• Severity criteria
2.5
Length of stay (days)
Median (range)
8 (11.75–29.25)
Smoking, n (%)
7 (37)
3 (37.5)
1 (14)
13 (68.4)
6 (31.6)
7 (87.5)
2 (25)
4 (57.1)
0
Clostridium difficile infection treatment, n (%)
• Metronidazole
•Vancomycin
32.5 (25.25–49.75)
8 (4.75–10.25)
*
Clostridium difficile testing conducted within the first forty-eight hours after hospitalization where the patient was not hospitalized in the two months prior to the
admission.
**
Patient hospitalized in the two months prior to the admission or Clostridium difficile testing was positive during the stay after a negative first test on admission.
***
Clostridium difficile testing conducted after three days without available data on admission.
****
Defined as a Harvey-Bradshaw score > 12.
*****
Defined as a Lichtiger score >10.
a
Immunomodulators (azathioprine, purinethol, methotrexate).
appears to be the only independent predictor of a combination of
CDI and a flare-up of IBD that requires hospitalization; this is an
additional reason to recommend that patients with IBD avoid this
particular therapy. It is obvious that it is a preliminary result that
needs to be validated in a large cohort of patients. Nevertheless,
these results suggest that an exploration of how NSAIDs promote
the emergence of C. difficile during chronic inflammation might be
worthwhile.
Conflict of interest
None declared.
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