Abstract

OBJECTIVES:

The Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) program was initiated by the International Organization for the Study of Inflammatory Bowel Diseases (IOIBD). It examined potential treatment targets for inflammatory bowel disease (IBD) to be used for a “treat-to-target” clinical management strategy using an evidence-based expert consensus process.

METHODS:

A Steering Committee of 28 IBD specialists developed recommendations based on a systematic literature review and expert opinion. Consensus was gained if ≥75% of participants scored the recommendation as 7–10 on a 10-point rating scale (where 10=agree completely).

RESULTS:

The group agreed upon 12 recommendations for ulcerative colitis (UC) and Crohn’s disease (CD). The agreed target for UC was clinical/patient-reported outcome (PRO) remission (defined as resolution of rectal bleeding and diarrhea/altered bowel habit) and endoscopic remission (defined as a Mayo endoscopic subscore of 0–1). Histological remission was considered as an adjunctive goal. Clinical/PRO remission was also agreed upon as a target for CD and defined as resolution of abdominal pain and diarrhea/altered bowel habit; and endoscopic remission, defined as resolution of ulceration at ileocolonoscopy, or resolution of findings of inflammation on cross-sectional imaging in patients who cannot be adequately assessed with ileocolonoscopy. Biomarker remission (normal C-reactive protein (CRP) and calprotectin) was considered as an adjunctive target.

CONCLUSIONS:

Evidence- and consensus-based recommendations for selecting the goals for treat-to-target strategies in patients with IBD are made available. Prospective studies are needed to determine how these targets will change disease course and patients’ quality of life.

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Acknowledgements

Writing assistance was provided by Helena Williams of Leading Edge Medical Education, part of the Lucid Group, UK, who received funding assistance from IOIBD. AbbVie and Ferring were not involved in the development of this manuscript and the authors maintained complete control over its content. We thank Severine Vermeire, Siew Ng, Marco Greco, Edouard Louis, and Marion O’Connor for their assistance.

Author information

Affiliations

  1. INSERM Unité 954 and Department of Hepato-Gastroenterology, University Hospital of Nancy, University of Lorraine, Houdemont, France

    • L Peyrin-Biroulet
  2. Division of Gastroenterology, University of California San Diego, La Jolla, California, USA

    • W Sandborn
  3. Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai, New York, New York, USA

    • B E Sands
    •  & J -F Colombel
  4. McMaster University, Hamilton, Ontario, Canada

    • W Reinisch
  5. Medical University of Vienna, Vienna, Austria

    • W Reinisch
  6. Department of Surgery, Academic Medical Center, Amsterdam, The Netherlands

    • W Bemelman
  7. Translational Gastroenterology Unit, John Radcliffe Hospital, Oxford, UK

    • R V Bryant
  8. Department of Gastroenterology, Academic Medical Centre, Amsterdam, The Netherlands

    • G D'Haens
    •  & M Samaan
  9. Inflammatory Bowel Disease Center, Department of Gastroenterology and Liver Diseases, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

    • I Dotan
  10. Division of Pediatric Gastroenterology and Hepatology, Icahn School of Medicine at Mount Sinai, New York, New York, USA

    • M Dubinsky
  11. University of Western Ontario, London, Ontario, Canada

    • B Feagan
  12. Inflammatory Bowel Disease Center, Department of Gastroenterology, Humanitas Research Hospital, Rozzano, Milan, Italy

    • G Fiorino
    •  & S Danese
  13. Department of Medicine, University of Otago, Christchurch, New Zealand

    • R Gearry
  14. Columbia University Division of Digestive and Liver Diseases, New York, New York, USA

    • S Krishnareddy
  15. First Department of Medicine, Semmelweis University, Budapest, Hungary

    • P L Lakatos
  16. Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota, USA

    • E V Loftus Jr
  17. AP-HP, Department of Digestive Diseases, Hôpital Lariboisière Medicosurgical and University Denis Diderot, Paris, France

    • P Marteau
  18. North Zealand Hospital, Capital Region, University of Copenhagen, Copenhagen, Denmark

    • P Munkholm
  19. Inflammatory Bowel Disease Group, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada

    • T B Murdoch
  20. Department of Gastroenterology, Hospital Clinic of Barcelona, IDIBAPS, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Barcelona, Spain

    • I Ordás
    •  & J Panes
  21. Inflammatory Bowel Disease Clinic University of Calgary, Calgary, Alberta, Canada

    • R Panaccione
  22. Department of Pathology and Laboratory Medicine, Mount Sinai Hospital, Toronto, Ontario, Canada

    • R H Riddell
  23. Division of Gastroenterology, CHU Sherbrooke, Sherbrooke, Quebec, Canada

    • J Ruel
  24. Section of Gastroenterology, Hepatology and Nutrition, University of Chicago Medicine, Chicago, Illinois, USA

    • D T Rubin
  25. Dartmouth-Hitchcock Inflammatory Bowel Disease Center, Hanover, New Hampshire, USA

    • C A Siegel
  26. Zane Cohen Centre for Digestive Diseases, Division of Gastroenterology, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada

    • M S Silverberg
    •  & S O'Donnell
  27. Department of Radiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands

    • J Stoker
  28. Department of General Internal Medicine, Christian-Albrechts-University, University Hospital Schleswig Holstein, Kiel, Germany

    • S Schreiber
  29. Translational Gastroenterology Unit, John Radcliffe Hospital, Oxford, UK

    • S Travis
  30. Division of Gastroenterology, University of Leuven, Leuven, Belgium

    • G Van Assche
  31. University of Toronto, Toronto, Ontario, Canada

    • G Van Assche
  32. Service des Maladies de l’Appareil Digestif et INSERM U991, CHU Pontchaillou et Université de Rennes 1, Rennes, France

    • G Bouguen
  33. Department of Hepato-Gastroenterology, Claude Huriez Hospital, Université Lille Nord de France, Lille, France

    • B Pariente
  34. Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada

    • S Winer
  35. Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA

    • S Hanauer

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Competing interests

Guarantor of the article: Jean-Frederic Colombel, MD.

Specific author contributions: Members of the Executive Steering Committee who lead the overall process of generating and agreeing the targets: L. Peyrin-Biroulet, W. Sandborn, B.E. Sands, J.F. Colombel, and S. Hanauer; attended the voting meeting: L. Peyrin-Biroulet, W. Sandborn, B.E. Sands, W. Reinisch, R.V. Bryant, I. Dotan, M. Dubinsky, B. Feagan, G. Fiorino, R. Gearry, S. Krishnareddy, P.L. Lakatos, E.V. Loftus, P. Marteau, T.B. Murdoch, I. Ordás, R.H. Riddell, J. Ruel, D.T. Rubin, M. Samaan, C.A. Siegel, J. Stoker, S. Schreiber, S. Travis, J. Panes, S. Hanauer, and J.F. Colombel; were workshop leaders for the ‘Clinical targets’ section: G. Van Assche and P.L. Lakatos; workshop leaders for endoscopic targets: G. D’Haens and P. Marteau; workshop leaders for histological targets: S. Travis and R.H. Riddell; workshop leaders for imaging targets, with S. Danese as a key contributor to this workgroup: J. Panes and W. Bemelman; workshop leaders for biomarkers: R. Panaccione and M. Samaan; workshop leaders for patient-reported outcomes: B.E. Sands and P. Munkholm; contributed to the systematic literature reviews: R.V. Bryant, G. Fiorino, S. Krishnareddy, T.B Murdoch, I. Ordás, J. Ruel, M. Samaan, G. Bouguen, S. O’Donnell, B. Pariente, and S. Winer. All authors contributed to the critical review and revision of each draft of the manuscript and all authors approved the final version for submission.

Financial support: The STRIDE program was initiated by the IOIBD and received a multi-sponsored educational grant from AbbVie and Ferring; it is driven by an independent Steering Committee.

Potential competing interests: LPB: consulting fees from Merck, Abbott, Janssen, Genentech, Mitsubishi, Ferring, Norgine, Tillots, Vifor, Shire, Therakos, Pharmacosmos, Pilège, BMS, UCB-pharma, Hospira, Celltrion, Takeda, Boehringer-Ingelheim, Lilly, and Pfizer. Lecture fees from Merck, Abbott, Janssen, Ferring, Norgine, Tillots, Vifor, Therakos, and HAC-pharma. WS: consulting fees and research support from Abbott Laboratories, Janssen Biotech, UCB Pharma, and Takeda, as well as consulting fees from Merck/Schering-Plough. BES: honoraria for service on an advisory board for AbbVie, Millennium Pharmaceuticals, Takeda, Shire, Pfizer, Luitpold Pharmaceuticals, Janssen Research and Development, Prometheus Laboratories, Forest Research Institute, Salix, and Vedanta Biosciences. WR: speaker, consultant, and/or advisory board member for Abbott Laboratories, Abbvie, Aesca, Amgen, AM Pharma, Aptalis, Astellas, Astra Zeneca, Avaxia, Bioclinica, Biogen IDEC, Bristol-Myers Squibb, Cellerix, Chemocentryx, Celgene, Centocor, Celltrion, Danone Austria, Elan, Falk Pharma GmbH, Ferring, Galapagos, Genentech, Grìnenthal, Inova, Janssen, Johnson & Johnson, Kyowa Hakko Kirin Pharma, Lipid Therapeutics, MedImmune, Millenium, Mitsubishi Tanabe Pharma Corporation, MSD, Novartis, Ocera, Otsuka, PDL, Pharmacosmos, Pfizer, Procter & Gamble, Prometheus, Robarts Clinical Trial, Schering-Plough, Setpointmedical, Shire, Takeda, Therakos, Tigenix, UCB, Vifor, Yakult, Zyngenia, and 4SC. GD’H: Advisor for Abbvie, Ablynx, Actogenix, Amgen, AM Pharma, Astra Zeneca, Avaxia, Bristol-Myerss Squibb, Boehringer-Ingelheim, Celgene, Celltrion, Cosmo, Covidien, Elan, Ferring, Falk Pharma, Centocor/Janssen Biologics, Engene, Galapagos, Gilead, GlaxoSmithKline, Hospira, Medimetrics, Millenium/Takeda, Mitsubishi Pharma, MSD, Mundipharma, NovoNordisk, Otsuka, Pfizer, Protein Design Laboratories, Prometheus Laboratories/Nestle, Receptos, Robarts Clinical Trials, Salix, Sandoz, Setpoint, Shire, Teva, Tigenix, Tillotts, UCB, Versant and Vifor and received speaker fees from Abbvie, Ferring, Janssen Biologics, MSD, Mundipharma, Norgine, Shire, Takeda, Tillotts, UCB, and Vifor. ID: Consultant for Janssen, AbbVie, Takeda, Genentech, and Pfizer; speaker’s fees from Ferring, Falk Pharma, Janssen, AbbVie, and MSD. MCD: consultancy for Abbvie, Janssen, Takeda, UCB, Genentech, Pfizer, Shire, Salix, and Prometheus Labs, research support from Janssen and Prometheus Labs. BF: consultant for Abbott/AbbVie, Actogenix, Albireo Pharma, Amgen, Astra Zeneca, Avaxia Biologics Inc., Avir Pharma, Axcan, Baxter Healthcare Corp., Boehringer-Ingelheim, Bristol-Myers Squibb, Calypso Biotech, Celgene, Elan/Biogen, EnGene, Ferring Pharma, Roche/Genentech, GiCare Pharma, Gilead, Given Imaging Inc., GSK, Ironwood Pharma, Janssen Biotech (Centocor), JnJ/Janssen, Kyowa Kakko Kirin Co Ltd., Lexicon, Lilly, Merck, Millennium, Nektar, Novonordisk, Pfizer, Prometheus Therapeutics and Diagnostics, Protagonist, Receptos, Salix Pharma, Serono, Shire, Sigmoid Pharma, Synergy Pharma Inc., Takeda, Teva Pharma, TiGenix, Tillotts, UCB Pharma, Vertex Pharma, Warner-Chilcott, Wyeth, Zealand, and Zyngenia; speaker’s bureau for Abbott/AbbVie, JnJ/Janssen, Takeda, Warner-Chilcott, UCB Pharma; advisory board member for Abbott/AbbVie, Amgen, Astra Zeneca, Avaxia Biologics Inc., Bristol-Myers Squibb, Celgene, Centocor Inc., Elan/Biogen, Ferring, JnJ/Janssen, Merck, Novartis, Novonordisk, Pfizer, Prometheus Laboratories, Protagonist, Salix Pharma, Takeda, Teva, TiGenix, Tillotts Pharma AG, UCB Pharma; grant/research support from Abbott/AbbVie, Amgen, Astra Zeneca, Bristol-Myers Squibb (BMS), Janssen Biotech (Centocor), JnJ/Janssen, Roche/Genentech, Millennium, Pfizer, Receptos, Santarus, Sanofi, Tillotts, and UCB Pharma. GF: consultant and advisory board member for MSD, Takeda, AbbVie, and Janssen. RG: speaker’s fees, consultancies, ad boards, travel support from AbbVie, Janssen, Hospira, and Baxter. PLL: speaker for AbbVie, Egis, Ferring, and MSD. In the past 2 years he has consulted for AbbVie, Celltrion, Egis, Hospira, Ferring, MSD, and Takeda and has received unrestricted research grants from AbbVie and MSD. EVL: consultancy honoraria from AbbVie, Janssen, UCB, Takeda, MedImmune, and Immune Pharmaceuticals; research support from AbbVie, Janssen, UCB, Takeda, Genentech, Pfizer, Bristol-Myers Squibb, GlaxoSmithKline, Amgen, Santarus, and Robarts Clinical Trials. PM: honoraria for consultancy, and lecture and travel fees from AbbVie, Biocodex, Danone, Dr Falk, Ferring, Ipsen, Merck Médication Familiale, MSD, Nestlé, and Vifor Pharma. P Munkholm: Consultant and speaker for Tillotts, AbbVie, MSD, Takeda, Dr Falk, Shire, AstraZeneca, Swedish Orphan, Ferring, and Pharmacosmos. IO: speaker’s fees from Abbvie and MSD. RP: consultant and/or lecture fees from AbbVie, Amgen, AstraZeneca, Axcan Pharma, Biogen Idec, Bristol-Myers Squibb, Centocor, ChemoCentryx, Eisai Medical Research, ELAN, Ferring, Genentech, GlaxoSmithKline, Janssen, MSD, Millennium, Ocera Therapeutics, Otsuka America Pharmaceuticals, Pfizer, Shire Pharmaceuticals, Prometheus, Schering Plough, Synta Pharmaceuticals, Teva, UCB Pharma, and Warner Chilcott. JR: consultant for Janssen, AbbVie, and Takeda. DTR: Consultant for Promethus Pharmaceuticals, AbbVie, UCB, Janssen, and Takeda, grant support from Promethus Pharmaceuticals and UCB. CAS: consultant/advisory board member for Abbvie, Lilly, Janssen, Salix, Pfizer, Prometheus, Takeda, and UCB; speaker for CME activities for Abbvie, Janssen, and Takeda. MSS: consulting fees, research support, and speaker fees received from Janssen, Abbvie, Takeda, and Prometheus. JS: consultant for Robarts Clinical Trials. SS: consultancy honoraria from AbbVie, Celltrion, Celgene, Ferring, Genentech, Hospira, Janssen, Robarts, UCB, and Takeda; speaker’s fees from MSD and Falk Pharma. ST: former President of ECCO and conducted no industry consulting during his time as President, but since that time has acted as advisor to, lecturer for, or been in receipt of research support from AbbVie, AstraZeneca, Boerrhinger, Celgene, Cosmo, Ferring, Genentech, GSK, Novo Nordisk, NPS, Pfizer, Takeda, and Vifor. GvA: consultant for Abbvie, Takeda, Janssen, MSD, and Ferring; speaker’s fees from Abbvie, MSD, Janssen, Warner-Chillcot, Ferring, Takeda, and Celltrion. SD: consultancy honoraria from Abbvie, Astra Zeneca, Danone, MSD, Novo Nordisk, Takeda Millennium, Salix Pharmaceuticals, and Pfizer. JP: consultancy honoraria from AbbVie, Boehringer Ingelheim, Bristol-Myers Squibb, Galapagos, Janssen, MSD, Novo-Nordisk, Pfizer, Takeda, Topivert, and Tigenix. GB: speaker’s fee from Abbvie, MSD, Ferring, and Norgine France. BP: lecture and travel fees from AbbVie and Ferring MSD. SH: consultant for AbbVie, Janssen, Shire, Salix, Takeda, UCB, Actavis, Ferring, and Prometheus, and on the speaker’s bureau for AbbVie, Janssen, Salix, and Takeda. J-FC: consultant, advisory board member, or speaker for AbbVie, Bristol Meyers Squibb, Ferring, Genentech, Giuliani SPA, Given Imaging, Merck, Millenium Pharmaceuticals, Pfizer, Prometheus Laboratories, Sanofi, Schering Plough Corporation, Takeda, Teva Pharmaceuticals, and UCB Pharma.

Corresponding authors

Correspondence to S Hanauer or J -F Colombel.

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DOI

https://doi.org/10.1038/ajg.2015.233

SUPPLEMENTARY MATERIAL is linked to the online version of the paper at http://www.nature.com/ajg

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