Adherent-invasive Escherichia coli in Crohn's disease: the 25th anniversary

Nicolas Barnich¹, Janelle C Arthur^{2

3}, Anthony Buisson^{1

4}, Barry J Campbell^{5

6}, Franck Carbonnel^{7

8}, Benoit Chassaing^{9

10}, Brian K Coombes^{11

12}, Jérémy Denizot¹, Belgin Dogan¹³, Jeremiah Faith¹⁴, Nobuhiko Kamada^{15

16}, Randy S Longman¹⁷, Margarita Martinez-Medina¹⁸, Claire L O'Brien^{19

20}, R Balfour Sartor^{3

21}, Shiying Zhang¹³; AIEC Research Group; Jean-Frederic Colombel²², Kenneth W Simpson²³; AIEC Research group

Collaborators, Affiliations

Collaborators

AIEC Research group:
Manasi Agrawal, Ju-Hyun Ahn, Souwelimatou Amani, Janelle Arthur, Candice Aurrand, Nicolas Barnich, Elisabeth Billard, Queralt Bonet-Rossinyol, Hélène Botchorichvilli, Anthony Buisson, Paula Bustamante, Barry Campbell, Franck Carbonnel, Emre Cardakli, Benoit Chassaing, Caroline Chevarin, Brian Coombes, Jean-Frederic Colombel, Alison Da Silva, Flavie Dambrine, Lena Darwish, Charlene Dauriat, Fanny De Clercq, Jérémy Denizot, Belgin Dogan, Bethan Evans, Jeremiah Faith, Marion Falabregue, Margot Fargeas, Frédéric Faure, Llorenc Fernandez-Coll, Aline Fiebig, Kerry Hernandez, Kendall Hupp, Katie Lacobucci, Nobuhiko Kamada, Saori Kashiwagi, Kaj Kreutzfeldt, Chuang Li, Valerie Livrelli, Randy Longman, Elena Lucchetta, Margarita Martinez-Medina, Derek McKay, Armaan Mohan, Manabu Nagayama, Hang Nguyen, Claire O'Brien, Inga Peter, Carole Peyssonnaux, Silvia Pires, Corominas Maria Nuria Ramos I, Nathalie Rolhion, Heloise Rytter, Nancy Saad, Balfour Sartor, Ellen Scherl, Paul Scholl, Stephanie Schuller, Jennifer Schwartz, Kenneth Simpson, Adeline Sivignon, Carola Venturini, Wei Yang, Megan Zangara, Shiying Zhang

Affiliations

¹ Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte (M2iSH), Université Clermont Auvergne, Inserm U1071, USC-INRAE 1382, Clermont-Ferrand, France.
² Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina, USA.
³ Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, North Carolina, USA.
⁴ Service d'Hépato-Gastro Entérologie, CHU Clermont-Ferrand, 3iHP, Clermont-Ferrand, France.
⁵ Department of Infection Biology & Microbiomes, Institute of Infection, Veterinary & Ecological Sciences, University of Liverpool, Liverpool, UK.
⁶ Microbiome Innovation Centre, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK.
⁷ Department of Gastroenterology, Hôpitaux Universitaires Bicêtre, AP-HP, Université Paris Saclay, Le Kremlin Bicêtre, Gif-sur-Yvette, France.
⁸ Centre for Epidemiology and Population Health, INSERM, Universite Paris-Saclay, Villejuif, France.
⁹ Microbiome-Host Interactions, INSERM U1306, CNRS UMR6047, Institut Pasteur, Université Paris Cité, Paris, France.
¹⁰ IHU Infiny, CHRU de Nancy, Vandoeuvre-les-Nancy, France.
¹¹ Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada.
¹² Institute for Infectious Disease Research, McMaster University Michael G DeGroote, Hamilton, Ontario, Canada.
¹³ Department of Clinical Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York, USA.
¹⁴ Department of Genetics and Genomics Sciences, Icahn School of Medicine, New York, New York, USA.
¹⁵ Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan, USA.
¹⁶ WPI Immunology Frontier Research Center, The University of Osaka, Osaka, Japan.
¹⁷ Division of Gastroenterology and Hepatology, Jill Roberts Center and Institute for Research in IBD, Weill Cornell Medicine, New York, New York, USA.
¹⁸ Microbiology of Intestinal Diseases, Biology Department, Universitat de Girona, Girona, Spain.
¹⁹ IBD Research Laboratory, Canberra Hospital, Canberra, Australian Capital Territory, Australia.
²⁰ Biomedical Science, Faculty of Science and Technology, University of Canberra, Canberra, Australian Capital Territory, Australia.
²¹ Division of Gastroenterology and Hepatology, The University of North Carolina, Chapel Hill, North Carolina, USA.
²² The Henry D. Janowitz Division of Gastroenterology, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA Jean-frederic.colombel@mssm.edu kws5@cornell.edu.
²³ Department of Clinical Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York, USA Jean-frederic.colombel@mssm.edu kws5@cornell.edu.

PMID: 40473402
DOI: 10.1136/gutjnl-2025-335331

Review

Adherent-invasive Escherichia coli in Crohn's disease: the 25th anniversary

Nicolas Barnich et al. Gut. 2025.

. 2025 Jun 5:gutjnl-2025-335331.

doi: 10.1136/gutjnl-2025-335331. Online ahead of print.

Authors

Collaborators

AIEC Research group:
Manasi Agrawal, Ju-Hyun Ahn, Souwelimatou Amani, Janelle Arthur, Candice Aurrand, Nicolas Barnich, Elisabeth Billard, Queralt Bonet-Rossinyol, Hélène Botchorichvilli, Anthony Buisson, Paula Bustamante, Barry Campbell, Franck Carbonnel, Emre Cardakli, Benoit Chassaing, Caroline Chevarin, Brian Coombes, Jean-Frederic Colombel, Alison Da Silva, Flavie Dambrine, Lena Darwish, Charlene Dauriat, Fanny De Clercq, Jérémy Denizot, Belgin Dogan, Bethan Evans, Jeremiah Faith, Marion Falabregue, Margot Fargeas, Frédéric Faure, Llorenc Fernandez-Coll, Aline Fiebig, Kerry Hernandez, Kendall Hupp, Katie Lacobucci, Nobuhiko Kamada, Saori Kashiwagi, Kaj Kreutzfeldt, Chuang Li, Valerie Livrelli, Randy Longman, Elena Lucchetta, Margarita Martinez-Medina, Derek McKay, Armaan Mohan, Manabu Nagayama, Hang Nguyen, Claire O'Brien, Inga Peter, Carole Peyssonnaux, Silvia Pires, Corominas Maria Nuria Ramos I, Nathalie Rolhion, Heloise Rytter, Nancy Saad, Balfour Sartor, Ellen Scherl, Paul Scholl, Stephanie Schuller, Jennifer Schwartz, Kenneth Simpson, Adeline Sivignon, Carola Venturini, Wei Yang, Megan Zangara, Shiying Zhang

Affiliations

¹ Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte (M2iSH), Université Clermont Auvergne, Inserm U1071, USC-INRAE 1382, Clermont-Ferrand, France.
² Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina, USA.
³ Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, North Carolina, USA.
⁴ Service d'Hépato-Gastro Entérologie, CHU Clermont-Ferrand, 3iHP, Clermont-Ferrand, France.
⁵ Department of Infection Biology & Microbiomes, Institute of Infection, Veterinary & Ecological Sciences, University of Liverpool, Liverpool, UK.
⁶ Microbiome Innovation Centre, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK.
⁷ Department of Gastroenterology, Hôpitaux Universitaires Bicêtre, AP-HP, Université Paris Saclay, Le Kremlin Bicêtre, Gif-sur-Yvette, France.
⁸ Centre for Epidemiology and Population Health, INSERM, Universite Paris-Saclay, Villejuif, France.
⁹ Microbiome-Host Interactions, INSERM U1306, CNRS UMR6047, Institut Pasteur, Université Paris Cité, Paris, France.
¹⁰ IHU Infiny, CHRU de Nancy, Vandoeuvre-les-Nancy, France.
¹¹ Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada.
¹² Institute for Infectious Disease Research, McMaster University Michael G DeGroote, Hamilton, Ontario, Canada.
¹³ Department of Clinical Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York, USA.
¹⁴ Department of Genetics and Genomics Sciences, Icahn School of Medicine, New York, New York, USA.
¹⁵ Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan, USA.
¹⁶ WPI Immunology Frontier Research Center, The University of Osaka, Osaka, Japan.
¹⁷ Division of Gastroenterology and Hepatology, Jill Roberts Center and Institute for Research in IBD, Weill Cornell Medicine, New York, New York, USA.
¹⁸ Microbiology of Intestinal Diseases, Biology Department, Universitat de Girona, Girona, Spain.
¹⁹ IBD Research Laboratory, Canberra Hospital, Canberra, Australian Capital Territory, Australia.
²⁰ Biomedical Science, Faculty of Science and Technology, University of Canberra, Canberra, Australian Capital Territory, Australia.
²¹ Division of Gastroenterology and Hepatology, The University of North Carolina, Chapel Hill, North Carolina, USA.
²² The Henry D. Janowitz Division of Gastroenterology, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA Jean-frederic.colombel@mssm.edu kws5@cornell.edu.
²³ Department of Clinical Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York, USA Jean-frederic.colombel@mssm.edu kws5@cornell.edu.

PMID: 40473402
DOI: 10.1136/gutjnl-2025-335331

Abstract

In 1998, Arlette Darfeuille-Michaud, Christel Neut and Jean-Frederic Colombel discovered a novel pathovar of Escherichia coli, adherent and invasive Escherichia coli (AIEC), in the ileum of patients with Crohn's disease (CD), that was genetically distinct from diarrheagenic E. coli, could adhere to and invade intestinal epithelial cells and survive in macrophages. The consistent association between AIEC and CD (approximately 30% across the world), their ability to exploit CD-associated genetic traits, and virulence in preclinical colitis models but not healthy hosts spurred global research to elucidate their pathogenicity. Research focused on integrating AIEC with the microbiome, metabolome, metagenome, host response and the impact of diet and antimicrobials has linked the luminal microenvironment and AIEC metabolism to health and disease. This deeper understanding has led to therapeutic trials and precision medicine targeting AIEC-colonised patients. In November 2023, prominent members of the AIEC research community met to present and discuss the many facets of basic, translational and clinical AIEC fields at 'AIEC: past, present and future' in NYC. This review is a summary of this international meeting highlighting the history of AIEC, knowledge accumulated over the past 25 years about its pathogenic properties and proposes a standardised approach for screening patients for AIEC.

Keywords: CROHN'S DISEASE; E. COLI; GASTROINTESTINAL MICROBIOME.

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Conflict of interest statement

Competing interests: AB: Consulting fees from Abbvie, Amgen, Arena, Biogen, Biocon, Celltrion, CTMA, Galapagos/AlfaSigma, GutyCare/Resilience, Fresenius-Kabi, Janssen, Lilly, MSD, Nexbiome, Pfizer, Roche, Sandoz, Takeda and Tillotts. Lecture fees from Abbvie, Amgen, Biogen, Celltrion, Galapagos/AlfaSigma, Janssen, Lilly, Mayoli-Spindler, MSD, Nordic Pharma, Norgine, Pfizer, Roche, Takeda, Tillotts and Vifor Pharma. Research grant from Abbvie, Celltrion, Janssen, Lessaffre, Lilly, Pfizer, Sandoz and Takeda. FC: reports receiving research grants from Alpha Wassermann, MaaT pharma, Mayoly Spindler, Medtronic, Nestlé; receiving payment for lectures from AbbVie, AlphaSigma, Ferring, Janssen, Eli Lilly, Nestlé Health Sciences, Pierre Fabre, Pileje, Takeda, Tillots, Viatris ; receiving consulting fees from AbbVie, Janssen, MaaT pharma, Tillots. JF: Scientific Advisory Board: Seed Health and Vedanta Biosciences. Consultant: Genfit. J-FC: reports receiving research grants from AbbVie, Janssen Pharmaceuticals, Takeda, Prometheus and Bristol Myers Squibb; receiving payment for lectures from AbbVie, Celltrion, Roche and Takeda; receiving consulting fees from AbbVie, Amgen, AnaptysBio, Allergan, Apini, Arena Pharmaceuticals, Astellas, Boehringer Ingelheim, Bristol Myers Squibb, Celgene, Celltrion, Clearview, Eli Lilly, Envision Pharma Ferring Pharmaceuticals, Galmed Research, Glaxo Smith Kline, Roche, Janssen Pharmaceuticals, Kaleido Biosciences, Immunic, Iterative Scopes, Landos, Microba Life Science, Merck, Mirador, Novartis, Otsuka Pharmaceutical, Pfizer, Protagonist Therapeutics, Sanofi, Sun Pharma, Takeda, Teva, TiGenix and is holding stock options in Intestinal Biotech Development. RL: Consultant for Sanofi and Xencor. Scientific Advisory Board for CJ Biosciences. Grant support from Boehringer Ingelheim. KWS: Member of the Scientific Advisory for Farmina Pet Foods, The Kerry Health and Scientific Advisory Council Nutrition Institute (KHNI) and Bactana. Grant support from Farmina Per Foods and Kerry. RBS: reports serving on the Scientific Advisory Board of Locus Bioscience and currently receives preclinical grant support from Ferring, Locus, ImmunyX and COSMOS. Previous grant support from Janssen, Gusto Global, Vendata, Biomica and BiomX.

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Adherent-invasive Escherichia coli in Crohn's disease: the 25th anniversary

Collaborators

Affiliations

Adherent-invasive Escherichia coli in Crohn's disease: the 25th anniversary

Authors

Collaborators

Affiliations

Abstract

Conflict of interest statement

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