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Inflammatory bowel disease
Original research
Role of adherent and invasive Escherichia coli in Crohn’s disease: lessons from the postoperative recurrence model
  1. Anthony Buisson1,2,
  2. Harry Sokol3,4,5,
  3. Nassim Hammoudi6,7,
  4. Stéphane nancey8,
  5. Xavier Treton9,
  6. Maria Nachury10,
  7. Mathurin Fumery11,
  8. Xavier Hébuterne12,
  9. Michael Rodrigues1,
  10. Jean-Pierre Hugot13,
  11. Gilles Boschetti8,
  12. Carmen Stefanescu9,
  13. Pauline Wils10,
  14. Philippe Seksik3,4,
  15. Lionel Le Bourhis7,
  16. Madeleine Bezault14,
  17. Pierre Sauvanet1,15,
  18. Bruno Pereira16,
  19. Matthieu Allez6,7,
  20. Nicolas Barnich1
  21. on behalf of the Remind study group
    1. 1 Microbes, Intestin, Inflammation et Susceptibilité de l’Hôte (M2iSH), UMR 1071, USC INRAE 2018, Clermont-Ferrand, France
    2. 2 Université Clermont Auvergne, Inserm, 3iHP, CHU Clermont-Ferrand, Service d’Hépato-Gastroentérologie, Clermont-Ferrand, France
    3. 3 Sorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Saint Antoine Hospital, Gastroenterology department, F-75012 Paris, France
    4. 4 Paris Center for Microbiome Medicine (PaCeMM) FHU, Paris, France
    5. 5 INRAE, UMR1319 Micalis, AgroParisTech, Jouy-en-Josas, France
    6. 6 Gastroenterology Department, Hôpital Saint-Louis hospital, Assitance Publique-Hôpitaux de Paris (AP-HP), Paris, France
    7. 7 Université De Paris, Institut de Recherche Saint-Louis, EMily, INSERM U1160, F-75010, Paris, France
    8. 8 Gastroenterology Department, Centre Hospitalier Lyon-Sud, Pierre-Benite, France
    9. 9 Gastroenterology Department, Hôpital Beaujon, MICI et Assistance Nutritive, APHP, Paris, France
    10. 10 Univ. Lille, Inserm, CHU Lille, U1286 - INFINITE - Institute for Translational Research in Inflammation, F-59000 Lille, France
    11. 11 Hepatogastroenterology department, Amiens University Hospital, an Peritox, UMR-I 01, University Amiens, Amiens, France
    12. 12 Gastroenterology and Clinical Nutrition, CHU of Nice and University Côte d’Azur Nice, Nice, France
    13. 13 Centre de recherche sur l’inflammation; INSERM UMR 1149; Assistance Publique-Hôpitaux de Paris; Université de Paris, F-75018 Paris, France
    14. 14 Remind study group, Paris, France
    15. 15 Chirurgie digestive, CHU Clermont-Ferrand, Clermont-Ferrand, France
    16. 16 Biostatistics Unit, University Hospital, DRCI, Clermont-Ferrand, France
    1. Correspondence to Pr Anthony Buisson, Gastroenterology Department, CHU Clermont-Ferrand, Clermont-Ferrand, France; a_buisson{at}hotmail.fr

    Abstract

    Objective We used the postoperative recurrence model to better understand the role of adherent and invasive Escherichia coli (AIEC) bacteria in Crohn’s disease (CD), taking advantage of a well-characterised postoperative cohort.

    Design From a prospective, multicentre cohort of operated patients with CD, AIEC identification was performed within the surgical specimen (M0) (N=181 patients) and the neoterminal ileum (n=119 patients/181) during colonoscopy performed 6 months after surgery (M6). Endoscopic postoperative recurrence was graded using Rutgeerts’ index. The mucosa-associated microbiota was analysed by 16S sequencing at M0 and M6. Relative risks or ORs were adjusted on potential confounders.

    Results AIEC prevalence was twofold higher within the neoterminal ileum at M6 (30.3%) than within the surgical specimen (14.9%) (p<0.001). AIEC within the neoterminal ileum at M6 was associated with higher rate of early ileal lesions (i1) (41.6% vs 17.1%; aRR 3.49 (95% CI 1.01 to 12.04), p=0.048) or ileal lesions (i2b+i3) (38.2% vs 17.1%; aRR 3.45 (95% CI 1.06 to 11.30), p=0.040) compared with no lesion (i0). AIEC within the surgical specimen was predictive of higher risk of i2b-endoscopic postoperative recurrence (POR) (aOR 2.54 (95% CI 1.01 to 6.44), p=0.049) and severe endoscopic POR (aOR 3.36 (95% CI 1.25 to 9.06), p=0.017). While only 5.0% (6/119) of the patients were AIEC-positive at both M0 and M6, 43.7% (52/119), patients with history of positive test for AIEC (M0 or M6) had higher risk of ileal endoscopic POR (aOR 2.32 (95% CI 1.01 to 5.39), p=0.048)), i2b-endoscopic postoperative recurrence (aOR 2.41 (95% CI 1.01 to 5.74); p=0.048) and severe endoscopic postoperative (aOR=3.84 (95% CI 1.32 to 11.18), p=0.013). AIEC colonisation was associated with a specific microbiota signature including increased abundance of Ruminococcus gnavus.

    Conclusion Based on the postoperative recurrence model, our data support the idea that AIEC are involved in the early steps of ileal CD.

    Trial registration number NCT03458195.

    • BACTERIAL INTERACTIONS
    • BACTERIAL PATHOGENESIS
    • CROHN'S DISEASE
    • E. COLI

    Data availability statement

    Data are available on reasonable request.

    https://doi.org/10.1136/gutjnl-2021-325971

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      Data availability statement

      Data are available on reasonable request.

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      Footnotes

      • Twitter @h_sokol, @Matfum

      • Collaborators REMIND Study Group Investigators: Saint-Louis, Paris: Pierre Cattan, Mircea Chirica, Nicolas Munoz-Bongrand, Hélène Corte, Jean-Marc Gornet, Clotilde Baudry, Nelson Lourenco, Mariane Maillet, My-Linh Tran-Minh, Andrée Nisard; Saint-Antoine, Paris: Laurent Beaugerie, Anne Bourrier, Isabelle Nion-Larmurier, Cecilia Landman, Julien Kirchgesner, Xavier Dray, Ulrika Chaput, Marine Camus, Philippe Marteau, Loic Brot, Najim Chafai, Jeremie H. Lefevre, Clotilde Debove, Yann Parc, Magali Svreck, Nadia Hoyau-Idrissi; Beaujon, Clichy: Nathalie Guedj, Yves Panis, Leon Maggiorri, Mariane Ferron, Yoram Bouhnik, Olivier Corcos; Clermont-Ferrand: Gilles Bommelaer, Marion Goutte, Anne Dubois, Caroline Chevarin, Marie Dodel, Dilek Coban; Lille: Pierre Desreumaux, Philippe Zerbib, Coralie Sommeville, Virginie Suffys; Amiens: Jean-Louis Dupas, Franck Brazier, Clara Yzet, Denis Chatelain, Christophe Attencourt, Charles Sabbagh, Martine Leconte; Lyon: Bernard Flourié, Yves François, Eddy Cotte, Anne-Laure Charlois, Peggy Falgon, Driffa Moussata, Marion Chauvenet, Sarah Boyer; Nice: Jérome Filippi, Paul Hofmann; REMIND: Carole Margalef, Patricia Detre.

      • Contributors Guarantor of the article: AB.

        AB, HS, MA and NB designed the study, obtained funding and wrote the manuscript. AB, HS, BP and NB contributed to bioinformatics data analysis. All REMIND investigators contributed to the recruitment and follow-up of patients. MR and PS performed microbiological experiments and AIEC characterisation. All authors read and approved the final manuscript.

      • Funding This REMIND study has been supported by grants from MSD France, Association François Aupetit and the Helmsley Charitable Trust. This study was also supported by the Ministère de la Recherche et de la Technologie; Inserm (UMR 1071); INRAE (USC-2018), the French government’s IDEX-I-SITE initiative 16-IDEX-0001 (CAP 20-25) of the University of Clermont Auvergne; and the Inserm National Programme 'Microbiote'.

      • Disclaimer The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

      • Competing interests None declared.

      • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

      • Provenance and peer review Not commissioned; externally peer reviewed.

      • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

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