The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease: the BISCUIT study

Richard Hansen, Susan H Berry, Indrani Mukhopadhya, John M Thomson, Karin A Saunders, Charlotte E Nicholl, W Michael Bisset, Sabarinathan Loganathan, Gamal Mahdi, Dagmar Kastner-Cole, Andy R Barclay, Jon Bishop, Diana M Flynn, Paraic McGrogan, Richard K Russell, Emad M El-Omar, Georgina L Hold

Research output: Contribution to journalArticle

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Abstract

Introduction

Children presenting for the first time with inflammatory bowel disease (IBD) offer a unique opportunity to study aetiological agents before the confounders of treatment. Microaerophilic bacteria can exploit the ecological niche of the intestinal epithelium; Helicobacter and Campylobacter are previously implicated in IBD pathogenesis. We set out to study these and other microaerophilic bacteria in de-novo paediatric IBD.

Patients and Methods

100 children undergoing colonoscopy were recruited including 44 treatment naïve de-novo IBD patients and 42 with normal colons. Colonic biopsies were subjected to microaerophilic culture with Gram-negative isolates then identified by sequencing. Biopsies were also PCR screened for the specific microaerophilic bacterial groups: Helicobacteraceae, Campylobacteraceae and Sutterella wadsworthensis.

Results

129 Gram-negative microaerophilic bacterial isolates were identified from 10 genera. The most frequently cultured was S. wadsworthensis (32 distinct isolates). Unusual Campylobacter were isolated from 8 subjects (including 3 C. concisus, 1 C. curvus, 1 C. lari, 1 C. rectus, 3 C. showae). No Helicobacter were cultured. When comparing IBD vs. normal colon control by PCR the prevalence figures were not significantly different (Helicobacter 11% vs. 12%, p = 1.00; Campylobacter 75% vs. 76%, p = 1.00; S. wadsworthensis 82% vs. 71%, p = 0.312).

Conclusions

This study offers a comprehensive overview of the microaerophilic microbiota of the paediatric colon including at IBD onset. Campylobacter appear to be surprisingly common, are not more strongly associated with IBD and can be isolated from around 8% of paediatric colonic biopsies. S. wadsworthensis appears to be a common commensal. Helicobacter species are relatively rare in the paediatric colon.
Original languageEnglish
Article numbere58825
Number of pages10
JournalPloS ONE
Volume8
Issue number3
DOIs
Publication statusPublished - 12 Mar 2013

Fingerprint

Pediatrics
inflammatory bowel disease
Microbiota
Sutterella wadsworthensis
Inflammatory Bowel Diseases
Helicobacter
Campylobacter
colon
Biopsy
Colon
biopsy
Campylobacter showae
Campylobacter curvus
Campylobacter rectus
Helicobacteraceae
Campylobacter concisus
Campylobacteraceae
Bacteria
Campylobacter lari
colonoscopy

Keywords

  • adolescent
  • campylobacter
  • child
  • child, preschool
  • female
  • Helicobacter pylori
  • humans
  • inflammatory bowel diseases
  • intestinal mucosa
  • male
  • metagenome
  • RNA, ribosomal, 16S

Cite this

Hansen, R., Berry, S. H., Mukhopadhya, I., Thomson, J. M., Saunders, K. A., Nicholl, C. E., ... Hold, G. L. (2013). The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease: the BISCUIT study. PloS ONE, 8(3), [e58825]. https://doi.org/10.1371/journal.pone.0058825

The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease : the BISCUIT study. / Hansen, Richard; Berry, Susan H; Mukhopadhya, Indrani; Thomson, John M; Saunders, Karin A; Nicholl, Charlotte E; Bisset, W Michael; Loganathan, Sabarinathan; Mahdi, Gamal; Kastner-Cole, Dagmar; Barclay, Andy R; Bishop, Jon; Flynn, Diana M; McGrogan, Paraic; Russell, Richard K; El-Omar, Emad M; Hold, Georgina L.

In: PloS ONE, Vol. 8, No. 3, e58825, 12.03.2013.

Research output: Contribution to journalArticle

Hansen, R, Berry, SH, Mukhopadhya, I, Thomson, JM, Saunders, KA, Nicholl, CE, Bisset, WM, Loganathan, S, Mahdi, G, Kastner-Cole, D, Barclay, AR, Bishop, J, Flynn, DM, McGrogan, P, Russell, RK, El-Omar, EM & Hold, GL 2013, 'The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease: the BISCUIT study', PloS ONE, vol. 8, no. 3, e58825. https://doi.org/10.1371/journal.pone.0058825
Hansen, Richard ; Berry, Susan H ; Mukhopadhya, Indrani ; Thomson, John M ; Saunders, Karin A ; Nicholl, Charlotte E ; Bisset, W Michael ; Loganathan, Sabarinathan ; Mahdi, Gamal ; Kastner-Cole, Dagmar ; Barclay, Andy R ; Bishop, Jon ; Flynn, Diana M ; McGrogan, Paraic ; Russell, Richard K ; El-Omar, Emad M ; Hold, Georgina L. / The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease : the BISCUIT study. In: PloS ONE. 2013 ; Vol. 8, No. 3.
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abstract = "IntroductionChildren presenting for the first time with inflammatory bowel disease (IBD) offer a unique opportunity to study aetiological agents before the confounders of treatment. Microaerophilic bacteria can exploit the ecological niche of the intestinal epithelium; Helicobacter and Campylobacter are previously implicated in IBD pathogenesis. We set out to study these and other microaerophilic bacteria in de-novo paediatric IBD.Patients and Methods100 children undergoing colonoscopy were recruited including 44 treatment na{\"i}ve de-novo IBD patients and 42 with normal colons. Colonic biopsies were subjected to microaerophilic culture with Gram-negative isolates then identified by sequencing. Biopsies were also PCR screened for the specific microaerophilic bacterial groups: Helicobacteraceae, Campylobacteraceae and Sutterella wadsworthensis.Results129 Gram-negative microaerophilic bacterial isolates were identified from 10 genera. The most frequently cultured was S. wadsworthensis (32 distinct isolates). Unusual Campylobacter were isolated from 8 subjects (including 3 C. concisus, 1 C. curvus, 1 C. lari, 1 C. rectus, 3 C. showae). No Helicobacter were cultured. When comparing IBD vs. normal colon control by PCR the prevalence figures were not significantly different (Helicobacter 11{\%} vs. 12{\%}, p = 1.00; Campylobacter 75{\%} vs. 76{\%}, p = 1.00; S. wadsworthensis 82{\%} vs. 71{\%}, p = 0.312).ConclusionsThis study offers a comprehensive overview of the microaerophilic microbiota of the paediatric colon including at IBD onset. Campylobacter appear to be surprisingly common, are not more strongly associated with IBD and can be isolated from around 8{\%} of paediatric colonic biopsies. S. wadsworthensis appears to be a common commensal. Helicobacter species are relatively rare in the paediatric colon.",
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AU - Hansen, Richard

AU - Berry, Susan H

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AU - Thomson, John M

AU - Saunders, Karin A

AU - Nicholl, Charlotte E

AU - Bisset, W Michael

AU - Loganathan, Sabarinathan

AU - Mahdi, Gamal

AU - Kastner-Cole, Dagmar

AU - Barclay, Andy R

AU - Bishop, Jon

AU - Flynn, Diana M

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N2 - IntroductionChildren presenting for the first time with inflammatory bowel disease (IBD) offer a unique opportunity to study aetiological agents before the confounders of treatment. Microaerophilic bacteria can exploit the ecological niche of the intestinal epithelium; Helicobacter and Campylobacter are previously implicated in IBD pathogenesis. We set out to study these and other microaerophilic bacteria in de-novo paediatric IBD.Patients and Methods100 children undergoing colonoscopy were recruited including 44 treatment naïve de-novo IBD patients and 42 with normal colons. Colonic biopsies were subjected to microaerophilic culture with Gram-negative isolates then identified by sequencing. Biopsies were also PCR screened for the specific microaerophilic bacterial groups: Helicobacteraceae, Campylobacteraceae and Sutterella wadsworthensis.Results129 Gram-negative microaerophilic bacterial isolates were identified from 10 genera. The most frequently cultured was S. wadsworthensis (32 distinct isolates). Unusual Campylobacter were isolated from 8 subjects (including 3 C. concisus, 1 C. curvus, 1 C. lari, 1 C. rectus, 3 C. showae). No Helicobacter were cultured. When comparing IBD vs. normal colon control by PCR the prevalence figures were not significantly different (Helicobacter 11% vs. 12%, p = 1.00; Campylobacter 75% vs. 76%, p = 1.00; S. wadsworthensis 82% vs. 71%, p = 0.312).ConclusionsThis study offers a comprehensive overview of the microaerophilic microbiota of the paediatric colon including at IBD onset. Campylobacter appear to be surprisingly common, are not more strongly associated with IBD and can be isolated from around 8% of paediatric colonic biopsies. S. wadsworthensis appears to be a common commensal. Helicobacter species are relatively rare in the paediatric colon.

AB - IntroductionChildren presenting for the first time with inflammatory bowel disease (IBD) offer a unique opportunity to study aetiological agents before the confounders of treatment. Microaerophilic bacteria can exploit the ecological niche of the intestinal epithelium; Helicobacter and Campylobacter are previously implicated in IBD pathogenesis. We set out to study these and other microaerophilic bacteria in de-novo paediatric IBD.Patients and Methods100 children undergoing colonoscopy were recruited including 44 treatment naïve de-novo IBD patients and 42 with normal colons. Colonic biopsies were subjected to microaerophilic culture with Gram-negative isolates then identified by sequencing. Biopsies were also PCR screened for the specific microaerophilic bacterial groups: Helicobacteraceae, Campylobacteraceae and Sutterella wadsworthensis.Results129 Gram-negative microaerophilic bacterial isolates were identified from 10 genera. The most frequently cultured was S. wadsworthensis (32 distinct isolates). Unusual Campylobacter were isolated from 8 subjects (including 3 C. concisus, 1 C. curvus, 1 C. lari, 1 C. rectus, 3 C. showae). No Helicobacter were cultured. When comparing IBD vs. normal colon control by PCR the prevalence figures were not significantly different (Helicobacter 11% vs. 12%, p = 1.00; Campylobacter 75% vs. 76%, p = 1.00; S. wadsworthensis 82% vs. 71%, p = 0.312).ConclusionsThis study offers a comprehensive overview of the microaerophilic microbiota of the paediatric colon including at IBD onset. Campylobacter appear to be surprisingly common, are not more strongly associated with IBD and can be isolated from around 8% of paediatric colonic biopsies. S. wadsworthensis appears to be a common commensal. Helicobacter species are relatively rare in the paediatric colon.

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KW - female

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KW - intestinal mucosa

KW - male

KW - metagenome

KW - RNA, ribosomal, 16S

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