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infection
Harry Sokol, Sarah Jegou, Claire Mcquitty, Marjolene Straub, Valentin
Leducq, Cecilia Landman, Julien Kirchgesner, Guillaume Le Gall, Anne
Bourrier, Isabelle Nion-Larmurier, et al.
To cite this version:
Harry Sokol, Sarah Jegou, Claire Mcquitty, Marjolene Straub, Valentin Leducq, et al.. Specificities of the intestinal microbiota in patients with inflammatory bowel disease and Clostridium difficile infection. Gut microbes, Taylor & Francis, 2017, 9 (1), pp.1-6. �10.1080/19490976.2017.1361092�. �hal-01582584�
Specificities of the intestinal microbiota in patients with inflammatory bowel disease and
1
Clostridium difficile infection
2 3
Harry Sokol1,2,3,4*, Sarah Jegou1,4, Claire McQuitty1,4, Marjolene Straub1,4, Valentin Leducq1,4,
4
Cecilia Landman3,4, Julien Kirchgesner3,4, Guillaume Le Gall3,4, Anne Bourrier3,4, Isabelle
Nion-5
Larmurier3,4, Jacques Cosnes3,4, Philippe Seksik3,4, Mathias L. Richard2,4 and Laurent
6
Beaugerie3,4
7 8
1 Sorbonne University - UPMC Univ Paris 06, INSERM ERL 1157, Avenir Team Gut Microbiota
9
and Immunity, UMR 7203, Saint-Antoine Hospital, Paris, France
10
2 INRA, UMR1319 Micalis & AgroParisTech, Jouy en Josas, France
11
3 Department of Gastroenterology, Saint Antoine Hospital, AP-HP, UPMC Univ Paris 06, Paris,
12
France
13
4 Inflammation-Immunopathology-Biotherapy Department (DHU i2B), Paris, France
14 15
*Corresponding author: Harry Sokol, Service de Gastroentérologie et Nutrition, Hôpital
Saint-16
Antoine, 184 rue du faubourg St Antoine, 75571 Paris cedex 12, France.
E-17
mail: harry.sokol@aphp.fr Phone: +33 149 283 162. Fax: +33 149 283 188
18 19
Short title: Microbiota in IBD with CDI
20 21
Abbreviations: inflammatory bowel diseases (IBD), healthy subjects (HS), Crohn’s disease (CD),
22
ulcerative colitis (UC)
23 24
Abstract
25
Background and Aims: Clostridium difficile infection (CDI) is a common complication in
26
inflammatory bowel disease (IBD) and has been associated with poor IBD outcome. Intestinal
27
microbiota composition in IBD patients with CDI has not been specifically evaluated to date.
28
Methods: The fecal microbiota of 56 IBD patients, including 8 in flare with concomitant CDI,
29
24 in flare without CDI, and 24 in remission, as well as 24 healthy subjects, was studied using
30
16S sequencing. Analysis was performed using the Qiime pipeline.
31
Results: Compared to IBD patients without CDI, IBD patients with CDI had more pronounced
32
dysbiosis with higher levels of Ruminococcus gnavus and Enterococcus operational taxonomic
33
units (OTUs) and lower levels of Blautia and Dorea OTUs. Correlation network analysis
34
suggested a disrupted ecosystem in IBD patients in flare, particularly in those with CDI.
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Conclusions: In patients with IBD, CDI is associated with a more pronounced intestinal
36
dysbiosis with specific alterations in intestinal microorganisms.
37 38
Keywords: IBD, Clostridium difficile
39 40
Introduction
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Clostridium difficile infection (CDI) is a common complication of inflammatory bowel disease
42
(IBD) and has been associated with a poor IBD outcome1. CDI typically occurs after a transient
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microbiota perturbation in the gut. Thus, antibiotic intake is a major risk factor in the general
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population. In IBD, as the gut microbiota is basally perturbed (i.e., dysbiosis)2, CDI can occur
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even without an antibiotic trigger.
46
Microbiota composition in patients with CDI is imbalanced and characterized by decreased
47
biodiversity3,4, as well as notable increases and decreases in several taxa that are known to be
48
increased and decreased in IBD4, respectively. For example, Bifidobacterium and members of
49
Clostridium clusters IV and XIVa (such as Faecalibacterium prausnitzii or Roseburia intestinalis)
50
were decreased, while Enterobacteriaceae and Enterococcus were increased5. However,
51
intestinal microbiota composition in IBD patients with CDI has not been specifically evaluated
52 to date. 53 54
Results
55Population, microbiota composition and diversity
56
Our study population was composed of 56 IBD patients, including 8 in flare with concomitant
57
CDI, 24 in flare without CDI, and 24 patients in remission, as well as 24 healthy subjects (HS)
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(Table 1). IBD patients in flare without CDI and patients in remission were matched to patients
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in flare with CDI (3:1) based on IBD subtype and topography. None of the study participants
60
reported having taken antibiotics or using colon-cleansing products for at least 2 months prior
61
to enrollment.
Beta diversity analysis showed a clustering of samples by disease phenotype and a progressive
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microbiota shift from HS to IBD in remission, to IBD in flare and finally to IBD in flare with CDI
64
(Figure 1A-B). Compared with the HS samples, the alpha diversity (assessed by four different
65
indexes) was significantly decreased in IBD patients, particularly in samples from patients in
66
flare (Figure 1C, Suppl Figure 1A-B). There was no significant difference between patients with
67
and without CDI.
68
As expected, most of the bacteria from both the IBD and HS samples belonged to the phyla
69
Firmicutes, Bacteroidetes, Proteobacteria and Actinobacteria (Figure 1D), and the distribution
70
of these phyla in the patients was in agreement with published data6. Firmicutes and
71
Bacteroidetes were the most abundant in HS. In IBD patients, particularly those in flare, there
72
was a decrease in Firmicutes (mostly from the Ruminococcaceae family) associated with an
73
increase of Proteobacteria (mostly from the Enterobacteriaceae family ; Figure 1D, Suppl
74
Figure 1C).
75 76
Differential bacterial composition and altered microbial network in CDI
77
To identify more precisely the impact of CDI on IBD microbiota, we directly compared the
78
bacterial composition of IBD patients in flare, both with and without CDI, using LEfSe (Linear
79
discriminant analysis Effect Size)7. We identified several OTU that differentiated patients with
80
and without CDI (Figure 1E, Suppl Table 1). Several Blautia and Dorea OTUs were decreased
81
in patients with CDI, whereas several Clostridium, Ruminococcus gnavus and Enterococcus
82
OTUs were increased in patients with CDI.
To evaluate globally the microbial gut ecosystem and its alterations in IBD and CDI, we built a
84
microbial correlation network by phenotype (Figure 2). In HS, we observed a highly connected
85
network between many bacterial OTUs, suggesting the presence of a balanced and
86
cooperative ecosystem. Although smaller than that of HS, the correlation network was also
87
well-connected in IBD patients in remission. In contrast, the correlation network was
88
disrupted in IBD patients in flare, with separated bacterial clusters being detected. For IBD
89
patients in flare who also had CDI, the alterations were even more pronounced with a lower
90
relative connectedness (2.1 vs 5.4 in IBD patients in flare without CDI, p<10-8) and no
91
interaction between several groups of bacteria, suggesting a loss of cooperation in the
92 ecosystem. 93 94
Discussion
95To the best of our knowledge, this report presents the first detailed analysis of the intestinal
96
microbiota of IBD patients both with and without CDI. In accordance with previous studies,
97
we confirmed that the intestinal microbiota of IBD patients is dysbiotic. The current study
98
showed that CDI in patients with IBD flare is associated with a more severe dysbiosis than in
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an IBD flare without CDI. This infection is characterized by specific alterations in intestinal
100
microorganisms with an impaired microbial ecosystem. Interestingly, among the decreased
101
bacterial OTUs in patients with CDI, we identified many genera known to be deficient in IBD
102
compared to HS, such as Blautia and Dorea6. In addition, the Ruminococcus gnavus and
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Enterococcus OTUs that were increased in the patients with CDI have also been shown to be
104
overrepresented in IBD patients compared to HS8,9. This finding indicates a deeper dysbiosis
in IBD patients with CDI. Moreover, several CDI features in non-IBD patients, such as increased
106
numbers of Enterococcus5, were also found in the IBD patients.
107
In conclusion, this study showed that in patients with IBD, CDI is associated with a more
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pronounced intestinal dysbiosis. Whether this feature is a cause or a consequence of CDI is
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not established. Therefore, the next step will be to investigate microbiota factors associated
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with the risk of developing CDI in IBD as a prerequisite for preventive intervention.
111 112
Materials and Methods
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Patients and sample collection
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All patients were recruited at the Gastroenterology Department of the Saint Antoine Hospital
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(Paris, France) and provided informed consent. Approval was obtained from the local ethics
116
committee (Comite de Protection des Personnes Ile-de-France IV, Suivitheque study). A
117
diagnosis of IBD was defined by clinical, radiological, endoscopic and histological criteria. A
118
flare was determined by the physician in charge of the patient based on clinical and biological
119
data. None of the study participants reported having taken antibiotics or using colon-cleansing
120
products for at least 2 months prior to enrollment. Patient characteristics are presented in
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Table 1. Samples from healthy subjects (HS) and from IBD patients without a Clostridium
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difficile infection were described previously 2. Whole stools were collected in sterile boxes and
123
immediately homogenized, and 0.2 g aliquots were frozen at −80°C for further analysis.
124 125
Fecal DNA extraction
Genomic DNA was extracted from 200 mg of feces as previously described 1. Following
127
microbial lysis with both mechanical and chemical steps, nucleic acids were precipitated in
128
isopropanol for 10 minutes at room temperature, incubated for 15 minutes on ice and
129
centrifuged for 30 minutes at 15,000 g and 4°C. Pellets were suspended in 112 µL of phosphate
130
buffer and 12 µL of potassium acetate. After RNase treatment and DNA precipitation, nucleic
131
acids were recovered via centrifugation at 15,000 g and 4°C for 30 minutes. The DNA pellet
132
was suspended in 100 µL of TE buffer.
133 134
16S rRNA gene sequencing
135
After extraction, total DNA concentration was measured using PicoGreen (Invitrogen), and
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global 16S gene DNA copy numbers were measured using a qPCR method adapted from
137
Maeda et al. 10, enabling inhibition effect estimation and DNA concentration adjustment. The
138
sequence region of the 16S rRNA gene spanning the variable region V3-V5 was amplified using
139
the broad-range forward primer, For16S_519 (CAGCMGCCGCGGTAATAC), and reverse primer,
140
Rev16S_926 (CCGTCAATTCMTTTGAGTTT). The amplification reaction (initial activation step at
141
94°C for 1 min, followed by 30 cycles of 94°C for 15 s, 43°C for 15 s, 68°C for 45 s and a final
142
incubation step at 68°C for 1 min) was performed in a total volume of 100 µL containing 1X
143
PCR buffer, 2 mM MgSO4, 1 U of DNA High Fidelity Taq Polymerase (Invitrogen, Carlsbad, CA),
144
625 nM of each barcoded primer (IDT), 250 µM of each dNTP (Invitrogen) and the
145
concentration-adjusted DNA sample. A bidirectional library was prepared using the One
146
Touch2 Template Kit and sequenced on PGM Ion Torrent using the Ion PGM Sequencing 400
147
Kit (Life Technologies, Carlsbad, CA).
148 149
16S rRNA gene sequence analysis
The sequences were demultiplexed and quality filtered using the Quantitative Insights Into
151
Microbial Ecology (QIIME, version 1.8.0) software package11. The sequences were trimmed for
152
barcodes and PCR primers and were binned for a minimal sequence length of 200 bp. The
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sequences were then assigned to (OTUs) using the UCLUST algorithm 12 with a 97% threshold
154
pairwise identity and taxonomically classified using the Greengenes reference database13.
155
Rarefaction was performed (10,000 sequences per sample) and used to compare OTU
156
abundances across samples. Principal component analyses (PCA) of the Bray Curtis distance,
157
with each sample colored according to disease phenotype, were built and used to assess the
158
variation between experimental groups. The number of observed species, as well as the
159
Shannon, Simpson and Chao1 diversity indexes, were calculated using rarefied data (depth =
160
10,000 sequences/sample) and used to characterize species diversity in a community.
161 162
Clostridium difficile testing
163
Diagnosis of CDI was performed using a stool culture on selective medium (TCCA, taurocholate
164
cycloserine cefoxitine medium) and a stool cytotoxicity assay on MRC-5 cells. In cases in which
165
a positive culture and negative stool cytotoxicity assay were obtained, a toxigenic culture
166
(determination of the isolate’s ability to produce toxins in vitro) was performed. 167
168
Statistical analysis
169
GraphPad Prism version 6.0 (San Diego, CA) was used for all analyses and graph preparation.
170
For all graphical data, the results are expressed as the mean ± SEM, and statistical analyses
171
were performed using the 2-tailed nonparametric Mann–Whitney U-test or the Kruskal-Wallis
172
test with Dunn’s multiple comparison test. Statistical significance of the sample grouping for
the beta diversity analysis was performed using the Permanova method (9999 permutations).
174
Differences with a P value less than 0.05 were considered to be significant.
175
Comparisons between IBD patients with and without CDI was performed using the linear
176
discriminant analysis (LDA) effect size (LEfSe) pipeline 7.
177
A correlation network was built using an OTU table and the Spearman correlation. Only OTUs
178
present in >50% of the samples were used. The p values were corrected using the Benjamini
179
and Hochberg procedure to control for the false discovery rate (FDR). Correlation network
180
figures were built using Cytoscape 3.1.1. The relative connectedness of the networks was
181
calculated by dividing the number of significant interactions (edges) by the number of taxa
182
(nodes) in the network. Statistical significance was assessed by a chi-square test.
183 184
Authors’ Contributions
185
HS designed and supervised the study. VL, SJ and CM provided technical help. HS, CL, JK, GL,
186
AB, INL, JC, PS, LB, recruited the patients, HS performed the analysis and interpreted the
187
data. HS wrote the manuscript.
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The authors state that the manuscript, including related data, figures and tables, has not
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been previously published and that the manuscript is not under consideration elsewhere.
190 191
Funding
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This study was supported by an unrestricted Biocodex grant.
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Conflicts of interest
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The authors disclose no conflicts of interest.
197 198
References
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Figure Legends
248
Figure 1: Bacterial microbiota biodiversity and composition. (A) Beta diversity. Principal
249
coordinate analysis of the Bray Curtis distance with each sample colored by the disease
250
phenotype. PC1, PC2, and PC3 represent the top three principal coordinates that captured the
251
most diversity, with the fraction of diversity captured by that coordinate shown as a
252
percentage. (B) PC1 value according disease phenotype (t test, ** = p< 0.01; *** = p< 0.001).
253
(C) OTU number describing the diversity of the bacterial microbiota in the different groups
254
studied (t test,* = p< 0.05; ** = p< 0.01; *** = p< 0.001). (D) Global composition of bacteria at
255
the phyla level. HS and patient sub-groups are labeled on the X-axis and expressed as the
256
relative OTU abundance per group. (E) Bacterial taxa differentially enriched in IBD patients in
257
flare both with and without CDI (generated using LeFSE analysis, LDA score >2).
258
Figure 2: Bacterial microbiota correlation network. Correlation network for the HS, IBD in
259
remission, and IBD in flare both without and with CDI was generated using Cytoscape. Each
260
circle (node) represents an OTU, the color represents its bacterial phylum (blue: Firmicutes;
261
green: Bacteroidetes; orange: Proteobacteria), and its size represents the number of direct
262
edges that it has. The edge color indicates the magnitude of the distance correlation; green
263
indicates a positive correlation and red indicates a negative correlation (determined using the
264
Spearman test). Statistical significance was determined for all pairwise comparisons; only
265
significant correlations (p value < 0.05 after FDR correction) are displayed.
266 267 268 269
Supplementary Materials and Methods
270 271 272
Supplementary Figure Legend
274
Supplementary Figure 1: Bacterial microbiota biodiversity and composition. (A) Chao1
275
diversity index of the bacterial microbiota in the different groups studied. (B) Shannon
276
diversity index of the bacterial microbiota in the different groups studied (t test,* = p< 0.05;
277
** = p< 0.01; *** = p< 0.001). (C) Global composition of bacteria at the family level. HS and
278
patient sub-groups are labeled on the X-axis and expressed as the relative OTU abundances
279
per group.
280 281
OTU591671 OTU523542 OTU180661 OTU349431 OTU353791 OTU191355 OTU583398 OTU221784 OTU198967 OTU182656 OTU197091 OTU199501 OTU333580 OTU290281 OTU1110312 OTU919158 OTU332317 OTU336830 NR_OTU38 OTU188001 OTU228061 OTU_208790 OTU_179137 OTU_344804 OTU551902 OTU346720 OTU292228 OTU357261 OTU194223 OTU537886 OTU562376 OTU210647 OTU804526 OTU196087 OTU363064 OTU363232 OTU355154 OTU181059 OTU831922 OTU337403 OTU593733 OTU353214 OTU192741 OTU546876 OTU333166 OTU591439 OTU197329 OTU322258 OTU361811 OTU355307 OTU2065341 OTU199036 OTU192308 OTU1040889 OTU659361 OTU909065 OTU1085832 OTU579608 OTU_323135 OTU941096 OTU276561OTU179961 OTU1015154 OTU1046408 OTU349882 OTU198941 OTU318190 OTU180702 OTU573189 NR_OTU12 OTU358333 OTU1106362 OTU357168 OTU1082539 OTU193528 OTU320120 OTU357529 OTU1105343 OTU368318 OTU199543 OTU772282 OTU198190 OTU560336 OTU544859 OTU350277 OTU343353 OTU531722 OTU180754 OTU575041 OTU353149 OTU364926 OTU197603 OTU577170 OTU359538 OTU365484 OTU344154 OTU291090OTU362997 OTU589071 OTU199716 OTU3426658 OTU361845 OTU199228 OTU292242 OTU369429 OTU561171 OTU1111191 OTU4374204 OTU190620 OTU196893 OTU194258 OTU312707 OTU368950 OTU216710 OTU354461 OTU584541 OTU572476 OTU188918 OTU535375 OTU195941 OTU347226 OTU198824OTU529531 OTU548836 OTU953855 OTU360553 OTU198127 OTU199147OTU198636 OTU366641 OTU364109OTU336375 OTU366771 OTU1078587OTU357582OTU589277 OTU523934 OTU366195 OTU341953 OTU337729 OTU365118 OTU583656 OTU513935 OTU196942 OTU194758 OTU4345821 OTU361619 OTU367688 OTU194236 OTU509416 OTU182545 OTU552528 OTU514272 OTU197505 OTU173996 OTU327298 OTU348642 OTU338987 OTU578016 OTU366633 OTU328098 OTU366846 OTU357389 OTU351231 OTU547913 OTU366352 OTU178629 OTU619919 OTU838544 OTU1062061 OTU_355334 OTU369109 OTU348406 OTU553080 OTU571642 OTU198270 OTU353155 OTU193452 OTU541602 OTU194584 OTU525401 OTU197364 OTU583746 OTU360329 OTU346302 OTU361556 OTU352747 OTU359563 OTU342666 OTU182799 OTU353292 OTU360392 OTU701221 OTU528362 OTU193887 OTU198945 OTU198542 OTU192282 OTU508968 OTU531436 OTU563572 OTU547906 NR_OTU43 OTU350121 OTU592139 OTU330578
OTU178238 OTU848615 OTU1111294 OTU558420 OTU339494 OTU579293 OTU199344 OTU364092 OTU359978 OTU571178 OTU195115 OTU192983 OTU198584 OTU198626 OTU178012 OTU851323 OTU193213 OTU180082 OTU183855 OTU210965 OTU360985 OTU696563 OTU184770 OTU198555 OTU188333 OTU196787 OTU358798 OTU199753 OTU302746 OTU309433 OTU198866 OTU370357 OTU178627 OTU368261 OTU345111 OTU352304 OTU196898 OTU366584 OTU514523 OTU851865 OTU358104 OTU585480 OTU367213 OTU363017 OTU738351 OTU520643 OTU296298 OTU526773 OTU198184 OTU173863 OTU196599 OTU975306 OTU708680OTU180523 OTU357412 OTU359149 OTU187505 OTU518438 OTU367909 OTU175741 OTU197761 OTU1848900 OTU195465 OTU298942 OTU359650 OTU1719314 NR_OTU9 OTU196713 OTU370287 OTU327218 OTU340219OTU367433 OTU368698 OTU329597 OTU191687 OTU563086 OTU183781 OTU190577OTU314582 OTU336205 OTU199218 OTU181437 OTU190711 OTU346738 OTU189152 OTU369182 OTU189816 OTU178420 OTU365574 OTU370183 OTU336133 OTU193592 OTU357449 OTU182864 OTU364048 OTU542934 OTU197426 OTU332732 OTU362767 OTU548503 OTU348751 OTU766113 OTU1016598 OTU291512 OTU368203 OTU470382 OTU185667 OTU180771 OTU369635 OTU196314 OTU184991 OTU359120 OTU189630 OTU363646 OTU191874 OTU351388 OTU529789 OTU588315 OTU347382 OTU184803 OTU189916 OTU516022 OTU529979 OTU456774 OTU3579707 OTU360147 OTU622256 OTU580008 OTU197324 OTU184990 OTU188079 OTU372348 OTU807046 OTU523140 OTU823634 OTU269531 OTU177623 OTU315846 OTU369027 OTU1076587 OTU180509 OTU623471 OTU369227OTU564941 OTU194001
OTU369027 OTU562376 OTU199753 OTU696563 OTU985239 OTU369227 OTU191687 OTU529531 OTU564806 OTU360015 OTU1111191 OTU909065 OTU554338 OTU659361 OTU210965OTU348642 OTU183781 OTU198190 OTU145801 OTU336133 OTU537886 OTU366641 OTU363064 OTU1078587 OTU364048 OTU366846 OTU1076587 OTU551902 OTU318190 OTU628226 OTU509416 OTU708680 OTU547913 OTU366771 OTU470382 OTU555945 OTU365118 OTU551822 OTU546876 OTU368318 OTU541602 OTU591635 OTU370183 OTU851865 OTU291090 OTU581079 OTU701221 OTU364926 OTU178629 OTU359538 OTU350277 OTU4345821 OTU3426658 OTU197505 OTU351231 OTU362997 OTU584541 OTU354850 OTU199716 OTU589277 OTU577170 OTU953855 OTU513445 OTU560336 OTU332317 OTU1046408 OTU1015154 OTU1111294 OTU348751 OTU583398 OTU984572 OTU1073276 OTU579608 OTU1083194 OTU1085832 OTU797229 OTU782953 OTU941096 OTU967427 OTU4384044 OTU1060104 OTU1068499 OTU1082539 OTU627071 OTU1088134 OTU968954 OTU1111582 OTU4309764 OTU1000273 OTU1059729 OTU531722 OTU535375 OTU583656 OTU357582 OTU196990 OTU187470 OTU628226 OTU189403 OTU2762219 OTU1111191 OTU554303 OTU562376 OTU563572 OTU564806 OTU354850 OTU589277 NR_OTU26 OTU323231 OTU301578OTU2624257 OTU197072 OTU199716 OTU59 OTU1078587 OTU1904686 OTU366771 OTU366641 OTU548587 OTU180082 OTU198866 OTU659361 OTU583656 OTU350277 OTU851323 OTU360238 OTU584541 OTU1076587 OTU589071 OTU4008675 OTU4462436 OTU572476 OTU344154 OTU577170 OTU3426658 OTU560336 OTU797229 OTU345303 OTU696563 OTU587269 OTU194416 OTU114821 OTU968954 OTU1060104OTU1046054 OTU1085832 OTU1015154 OTU941096 OTU1000273 OTU1088134 OTU1059729 OTU196370 OTU1860112 OTU1839271 OTU183495 OTU198251 OTU198423 OTU1068499 OTU1083194 OTU1046408 OTU1092300 OTU529180 OTU592160 OTU701221 OTU579608 NR_OTU1 OTU587530 OTU810399 OTU342427 OTU585419 OTU_359750 OTU_828483 OTU_354798 OTU_396697 OTU878104 OTU1019878 OTU145801 OTU2549971 OTU300297 OTU360015 OTU342397 OTU335701 OTU563086 OTU1082539 OTU1111582 OTU354905 OTU259772 OTU606927 OTU367688 OTU561607 OTU353149 OTU580521 OTU529180 OTU514272 OTU291512 OTU322580 OTU509416 OTU338987 OTU547913 OTU198270 OTU194236 OTU182545 OTU347639 OTU194758 OTU181853 OTU292228 OTU361619 OTU341953 OTU523934 OTU328098 OTU187569 OTU196942 OTU772384 OTU178629 OTU366846 OTU197022 OTU180037 OTU1076587 OTU197761 OTU752354 OTU369429 OTU1105343 OTU622256 OTU372348 OTU4374204 OTU523140 OTU175978 OTU208927 OTU198941 OTU195757 OTU738351 OTU221784 OTU312707 OTU561171 OTU529531 OTU355307 OTU330469 OTU360553 OTU318190 OTU985239 OTU183855 OTU288442 OTU348751 OTU210965 OTU369027 OTU196087 OTU360985 OTU365222 OTU823634 OTU180702OTU363646 OTU523542 OTU369017 OTU363232OTU591671 OTU189916 OTU357529 OTU348642 OTU804526 OTU198555 OTU583398 OTU1106362 OTU846141 OTU623471 OTU199753 OTU369227 OTU555945 OTU563086 OTU194001 OTU199228 OTU196572 OTU358333 OTU531675 OTU363064 OTU368318 OTU551902 OTU546876 OTU198824 OTU329597 OTU368203 OTU183781 OTU191687 OTU350091 OTU357168 OTU3768338 OTU843454 OTU526773 OTU324163 OTU296298 OTU189895 OTU1060104 OTU191355 OTU580008 OTU542934 OTU573189 OTU363348 OTU185667 OTU456774 OTU529979 OTU359493 OTU336205 OTU192834 OTU365118 OTU366641 OTU1078587 OTU198636 OTU370183 OTU368950 OTU366237 OTU346738 OTU365574 OTU331850 OTU336133 OTU513935 OTU193592 OTU364109 OTU336375 OTU308544 OTU185861 OTU365484 OTU364048 OTU516022 OTU696563 OTU198626 OTU366771 OTU198127 OTU1085832 OTU941096 OTU579608 OTU1015154 OTU1046408 OTU360392 OTU532203 OTU189152 OTU470382 OTU360147 OTU188918 OTU357389 NR_OTU36 OTU583656 OTU584541 OTU589071 OTU199147 OTU572476 OTU362997 OTU589277 OTU350277 OTU3426658 OTU344154 OTU357412 OTU518438 OTU531436 NR_OTU61 OTU351388 OTU541602 OTU198945 OTU196787 OTU513445 OTU571178 OTU354850 OTU199716 OTU352304OTU359978 OTU347382 OTU585480 OTU4281639 OTU514523 OTU851865 OTU188333 OTU352747 OTU192983 OTU332929 OTU369182 OTU353791 OTU588315 OTU909065 OTU180661 OTU562376 NR_OTU7 OTU198067
OTU1111191 OTU524575 OTU975306 OTU528362 OTU363400 OTU659361 OTU508968 OTU370287 OTU362767 OTU701221 OTU370357 OTU302746 OTU364092 OTU759751 OTU360015 OTU508984 OTU355154 OTU1040889 OTU173863 OTU4396888 OTU525401 OTU359650 OTU197364 OTU180523 OTU193887 OTU198584 OTU196893 OTU529789 OTU290281 OTU193213 OTU190711 OTU182065 OTU367909 OTU368261 OTU351231 OTU563572 OTU535375 OTU560336 OTU332317 OTU4345821 OTU531722 NR_OTU29 OTU198190 OTU1719314 OTU199344 OTU708680 OTU359149 OTU188099
Healthy subjects
IBD remission
IBD flare (no CDI)
OTU Increased in LDA pvalue k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__New_ReferenceOTU12 no_ICD 2,709772134 0,042547194 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU368950 no_ICD 2,126381739 0,042417294 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU523934 no_ICD 2,298329146 0,042612179 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU292228 no_ICD 2,334277874 0,042547194 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU365574 no_ICD 2,395775029 0,042547194 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU364109 no_ICD 2,464763391 0,042514711 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU346738 no_ICD 2,478248177 0,04264468 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU336133 no_ICD 2,652839773 0,013516916 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__OTU370183 no_ICD 3,497785175 0,006901304 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales_OTU312882 no_ICD 2,138634014 0,029440095 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Coprococcus.s__OTU509416 no_ICD 2,764876219 0,009538398 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Dorea.s__OTU350091 no_ICD 2,222337607 0,042514711 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Dorea.s__OTU523542 no_ICD 2,354482673 0,029463885 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Dorea.s__OTU363232 no_ICD 2,506881192 0,029535294 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Dorea.s__OTU363064 no_ICD 3,048426578 0,034512032 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_OTU333166 no_ICD 2,568375203 0,042547194 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Mogibacteriaceae.g__.s__OTU197505 no_ICD 2,197417666 0,01343149 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Mogibacteriaceae.g__.s__OTU197329 no_ICD 2,229470457 0,042612179 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Mogibacteriaceae.g__.s__OTU591439 no_ICD 2,312112231 0,029630589 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Peptostreptococcaceae.g__.s__OTU547714 no_ICD 2,07927405 0,041764625 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU348406 no_ICD 2,351951641 0,0291788 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU330578 no_ICD 2,545676932 0,042482233 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU571642 no_ICD 2,548597635 0,042547194 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU355307 no_ICD 2,593950091 0,042514711 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU363017 no_ICD 2,896417034 0,042612179 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU561607 no_ICD 2,963892372 0,042612179 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__.s__OTU1062061 no_ICD 3,13030404 0,020237338 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia.s__New_ReferenceOTU26 ICD 3,159333048 0,020836678 k__Bacteria.p__Bacteroidetes.c__Bacteroidia.o__Bacteroidales.f__Bacteroidaceae.g__Bacteroides.s__uniformis_OTU197072 ICD 2,105371372 0,039902891 k__Bacteria.p__Bacteroidetes.c__Bacteroidia.o__Bacteroidales.f__Barnesiellaceae.g__.s__OTU3090117 ICD 2,280992361 0,014787029
k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Blautia_362958 ICD 2,798873291 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__.s__306259 ICD 2,151239488 0,017782486 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__.s__OTU190003 ICD 2,153583951 0,024479083 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae_828483 ICD 3,047627085 0,005981652 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae_359750 ICD 3,44732167 0,000365284 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__.s__OTU606927 ICD 3,612199191 0,008833481 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__.g__.s__534957 ICD 2,017894414 0,022198769 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales_1846390 ICD 2,072160288 0,00240333 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales_New_CleanUp_ReferenceOTU22805 ICD 2,086165919 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__.g__.s__OTU198251 ICD 2,147435522 0,021612188 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__.g__.s__New_CleanUp_ReferenceOTU23027 ICD 2,176783737 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__.g__.s__OTU529180 ICD 2,25867102 0,027619597 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales_New_CleanUp_ReferenceOTU36592 ICD 2,344953413 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__.g__.s__OTU342397 ICD 2,865633643 0,0291519 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__.g__.s__354798 ICD 3,27040575 0,00597103 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales_OTU628226 ICD 3,654128818 0,002459037 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__Clostridium.s__perfringens_650343 ICD 2,262257751 0,00240333 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__Clostridium.s__724298 ICD 2,488412305 0,00240333 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__Clostridium.s__perfringens_396697 ICD 2,780555912 0,000365284 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__Clostridium.s__butyricum_OTU541328 ICD 3,091233772 0,044571347 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__Clostridium.s__4352349 ICD 3,582042637 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Clostridiaceae.g__Clostridium.s__2670715 ICD 4,231520538 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Coprococcus.s__OTU300297 ICD 2,39102753 0,041918675 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Coprococcus.s__OTU259772 ICD 2,868751036 0,013633486 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Dorea.s__OTU196176 ICD 2,073798121 0,044719844 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Dorea.s__New_CleanUp_ReferenceOTU33563 ICD 2,236455645 0,014787029 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Enterococcaceae_OTU225919 ICD 2,031815342 0,020070872 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Enterococcaceae.g__Enterococcus.s__OTU777667 ICD 2,231527429 0,001438634 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Enterococcaceae.g__Enterococcus.s__OTU810399 ICD 2,960440267 0,001510648 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Enterococcaceae.g__Enterococcus.s__OTU1111582 ICD 3,316570625 0,041876848 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Epulopiscium.s__1658639 ICD 2,619604976 0,014787029 k__Bacteria.p__Firmicutes.c__Erysipelotrichi.o__Erysipelotrichales.f__Erysipelotrichaceae.g__.s__OTU262095 ICD 2,014896732 0,048335369
k__Bacteria.p__Proteobacteria.c__Gammaproteobacteria.o__Pasteurellales.f__Pasteurellaceae.g__Haemophilus.s__parainfluenzae_OTU1016422 ICD 2,175725828 0,01836869 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__New_CleanUp_ReferenceOTU29281 ICD 2,014500266 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__New_CleanUp_ReferenceOTU1777 ICD 2,033502038 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU186955 ICD 2,058689631 0,016187289 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_OTU191999 ICD 2,10430887 0,013054349 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_OTU2714942 ICD 2,112447997 0,020744402 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU4426877 ICD 2,144346253 0,028308724 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_OTU515387 ICD 2,222776486 0,020529372 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU196990 ICD 2,278921856 0,012400722 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU186521 ICD 2,285395169 0,00240333 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU525142 ICD 2,307560565 0,022351007 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU554303 ICD 2,393225748 0,000249348 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_OTU196370 ICD 2,961263016 0,013515946 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_New_CleanUp_ReferenceOTU41303 ICD 2,973537047 0,01460627 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__.s__OTU564806 ICD 3,059346739 0,009969624 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae_OTU198423 ICD 3,13442702 0,012613888 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__zeae_679245 ICD 2,219688181 0,014635653 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__794205 ICD 2,222146634 0,00240333 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__692823 ICD 2,275755931 0,020107819 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__OTU91147 ICD 2,372015581 0,016187289 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__New_ReferenceOTU28 ICD 2,565255835 0,008021195 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Lactobacillaceae.g__Lactobacillus.s__manihotivorans_OTU518033 ICD 2,649528161 0,00240333 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU2575651 ICD 2,057219895 0,033823367 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU183495 ICD 2,122071431 0,043954718 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU4338803 ICD 2,144541001 0,020486998 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU1551841 ICD 2,153436752 0,020738111 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Ruminococcaceae.g__Ruminococcus.s__New_CleanUp_ReferenceOTU24360 ICD 2,233794941 0,014787029 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU1839271 ICD 2,250891702 0,011241596 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU416341 ICD 2,603989613 0,028308724 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Ruminococcus.s__gnavus_OTU360015 ICD 3,948864961 0,044232625 k__Bacteria.p__Firmicutes.c__Bacilli.o__Lactobacillales.f__Streptococcaceae.g__Streptococcus.s__4348151 ICD 2,011583756 0,002410416
k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Epulopiscium.s__295029 ICD 3,028901583 0,014635653 k__Bacteria.p__Firmicutes.c__Clostridia.o__Clostridiales.f__Lachnospiraceae.g__Epulopiscium.s__298247 ICD 3,26744118 0,013164598
Age : Year (mean +/- SD) 33.4 +/- 10.5 36.5 +/- 11.6 36.5 +/- 11.6 33.0 +/- 10.2 Male : n (%) 5 (62.6%) 14 (58.3%) 14 (58.3%) 15 (62.5%) Active smoking : n(%) 2 (25.0%) 9 (37.5%) 9 (37.5%) 1 (4.2%) CD/UC : n(%) CD UC CD UC CD UC NA n (%) 6 (75%) 2 (25%) 18 (75%) 6 (25%) 18 (75%) 6 (25%) NA Montreal classification A1 / A2 / A3 (n) 6 / 0 / 0 NA 4 / 12 / 2 NA 3 / 15 / 0 NA NA L1 / L2 / L3 (n) 2 / 2 / 2 NA 6 / 6 / 6 NA 6 / 6 / 6 NA NA B1 / B2 / B3 (n) 4 / 0 / 2 NA 9 / 2 / 7 NA 6 / 2 / 10 NA NA E1 / E2 / E3 (n) NA 0 / 1 / 1 NA 0 / 3 / 3 NA 0 / 3 / 3 NA Treatment: n(%) NA 5-ASA 3 (37.5%) 10 (41.7%) 6 (25.9%) 0 Coticosteroids 1 (12.5%) 10 (41.7%) 1 (4.2%) 0 Thiopurine or MTX 1 (12.5%) 10 (41.7%) 10 (41.7%) 0 anti-TNFa 2 (25.0%) 13 (54.2%) 19 (79.2%) 0 Antibiotics 0 0 0 0
