The Pathogenesis of Extraintestinal Manifestations: Implications for IBD Research, Diagnosis, and Therapy

Journal of Crohn's and Colitis - Tập 13 Số 5 - Trang 541-554 - 2019
Charlotte Hedin1, Stephan R. Vavricka2, Andrew J. Stagg3, Alain Schoepfer4, Tim Raine5, L. Puig6, Uwe Pleyer7, Alexander A. Navarini8, Andrea E. van der Meulen‐de Jong9, Jochen Maul10,11, K. Katsanos12, A Kagramanova13, Thomas Greuter14,15, Yago González-Lama16, F. van Gaalen17, Pierre Ellul18, Johan Burisch19,20, Dominik Bettenworth21, Markus Becker22, Giorgos Bamias23, Florian Rieder24,25
1Gastroenterology unit, Patient Area Gastroenterology, Dermatovenereology and Rheumatology, Karolinska University Hospital, Stockholm, Sweden
2Department of Gastroenterology and Hepatology, University Hospital Zurich, Zurich, Switzerland
3Centre for Immunobiology, Bart’s and The London Medical School, Queen Mary University of London, London, UK
4Division of Gastroenterology and Hepatology, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
5Department of Gastroenterology, Addenbrooke’s Hospital, Cambridge University Teaching Hospitals NHS Foundation Trust, Cambridge, UK
6Department of Dermatology, Hospital de la Santa Creu i Sant Pau. Universitat Autònoma de Barcelona, Barcelona, Catalonia, Spain
7University Eye Clinic, Uveitis Center, Charité – Universitätsmedizin Berlin, Berlin, Germany
8Department of Dermatology, University Hospital Zurich, Zurich, Switzerland
9Department of Gastroenterology Leiden University Medical Center Leiden The Netherlands
10Department of Medicine (Gastroenterology, Infectious Diseases, Rheumatology), Campus Benjamin Franklin, Charité - Universitätsmedizin Berlin, Berlin, Germany
11Gastroenterologie am Bayerischen Platz, Berlin, Germany
12Division of Gastroenterology, Department of Internal Medicine, Medical School, University of Ioannina School of Medical Sciences, Ioannina, Greece
13IBD Department, The Loginov Moscow Clinical Scientific Centre, Moscow, Russia
14Division of Gastroenterology and Hepatology, University Hospital Zurich, Zurich, Switzerland
15Gastroenterology Research Unit, Mayo Clinic, Rochester, MN, USA
16IBD Unit, Gastroenterology and Hepatology Department, Puerta de Hierro University Hospital, Majadahonda, Madrid, Spain
17Department of Rheumatology, Leiden University Medical Center [LUMC], Leiden, Netherlands
18Department of Medicine, Division of Gastroenterology, Mater Dei Hospital, Msida, Malta
19Abdominal Center K, Medical Section, Bispebjerg and Frederiksberg Hospital, University of Copenhagen, Copenhagen, Denmark
20Center for Clinical Research and Prevention, Bispebjerg and Frederiksberg Hospital, University of Copenhagen, Copenhagen, Denmark
21Department of Medicine B, Gastroenterology and Hepatology, University Hospital Münster, Münster, Germany
22Department of Ophthalmology, Triemli Hospital, Zurich, Switzerland & Department of Ophthalmology, University of Heidelberg, Heidelberg, Germany
23National and Kapodistrian University of Athens, GI Unit, 3rd Academic Department of Internal Medicine, Sotiria Hospital, Athens, Greece
24Department of Gastroenterology, Hepatology, and Nutrition
25Department of Gastroenterology, Hepatology and Nutrition, Digestive Diseases and Surgery Institute, Cleveland Clinic Foundation, Cleveland, OH, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Vavricka, 2015, Chronological order of appearance of extraintestinal manifestations relative to the time of IBD diagnosis in the Swiss inflammatory bowel disease cohort, Inflamm Bowel Dis, 21, 1794, 10.1097/MIB.0000000000000429

Harbord, 2016, The first European evidence-based consensus on extra-intestinal manifestations in inflammatory bowel disease, J Crohns Colitis, 10, 239, 10.1093/ecco-jcc/jjv213

Adams, 2006, Aberrant homing of mucosal T cells and extra-intestinal manifestations of inflammatory bowel disease, Nat Rev Immunol, 6, 244, 10.1038/nri1784

Trivedi, 2016, Intestinal CCL25 expression is increased in colitis and correlates with inflammatory activity, J Autoimmun, 68, 98, 10.1016/j.jaut.2016.01.001

Grant, 2001, MAdCAM-1 expressed in chronic inflammatory liver disease supports mucosal lymphocyte adhesion to hepatic endothelium [MAdCAM-1 in chronic inflammatory liver disease], Hepatology, 33, 1065, 10.1053/jhep.2001.24231

Eksteen, 2004, Hepatic endothelial CCL25 mediates the recruitment of CCR9+ gut-homing lymphocytes to the liver in primary sclerosing cholangitis, J Exp Med, 200, 1511, 10.1084/jem.20041035

Mann, 2012, Skin- and gut-homing molecules on human circulating γδ T cells and their dysregulation in inflammatory bowel disease, Clin Exp Immunol, 170, 122, 10.1111/j.1365-2249.2012.04649.x

Salmi, 1995, Dual binding capacity of mucosal immunoblasts to mucosal and synovial endothelium in humans: dissection of the molecular mechanisms, J Exp Med, 181, 137, 10.1084/jem.181.1.137

Salmi, 2001, Human leukocyte subpopulations from inflamed gut bind to joint vasculature using distinct sets of adhesion molecules, J Immunol, 166, 4650, 10.4049/jimmunol.166.7.4650

McNab, 1996, Vascular adhesion protein 1 mediates binding of T cells to human hepatic endothelium, Gastroenterology, 110, 522, 10.1053/gast.1996.v110.pm8566600

Lalor, 2002, Vascular adhesion protein-1 mediates adhesion and transmigration of lymphocytes on human hepatic endothelial cells, J Immunol, 169, 983, 10.4049/jimmunol.169.2.983

Agace, 2000, Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation, Eur J Immunol, 30, 819, 10.1002/1521-4141(200003)30:3<819::AID-IMMU819>3.0.CO;2-Y

Yuan, 2001, Chemokine receptor CXCR3 expression in inflammatory bowel disease, Inflamm Bowel Dis, 7, 281, 10.1097/00054725-200111000-00001

Jacques, 2014, The role of mechanical stress in the pathogenesis of spondyloarthritis and how to combat it, Best Pract Res Clin Rheumatol, 28, 703, 10.1016/j.berh.2014.10.009

Kummen, 2017, The gut microbial profile in patients with primary sclerosing cholangitis is distinct from patients with ulcerative colitis without biliary disease and healthy controls, Gut, 66, 611, 10.1136/gutjnl-2015-310500

Torres, 2016, The features of mucosa-associated microbiota in primary sclerosing cholangitis, Aliment Pharmacol Ther, 43, 790, 10.1111/apt.13552

Kevans, 2016, Characterization of intestinal microbiota in ulcerative colitis patients with and without primary sclerosing cholangitis, J Crohns Colitis, 10, 330, 10.1093/ecco-jcc/jjv204

Scofield, 1995, HLA-B27 binding of peptide from its own sequence and similar peptides from bacteria: Implications for spondyloarthropathies, Lancet, 345, 1542, 10.1016/S0140-6736(95)91089-1

Ramos, 2002, Molecular mimicry of an HLA-B27–derived ligand of arthritis-linked subtypes with chlamydial proteins, J Biol Chem, 277, 37573, 10.1074/jbc.M205470200

Horai, 2015, Microbiota-dependent activation of an autoreactive T cell receptor provokes autoimmunity in an immunologically privileged site, Immunity, 43, 343, 10.1016/j.immuni.2015.07.014

Nakamura, 2017, Short chain fatty acids ameliorate immune-mediated uveitis partially by altering migration of lymphocytes from the intestine, Sci Rep, 7, 11745, 10.1038/s41598-017-12163-3

Bodenheimer, 1983, Elevated circulating immune complexes in primary sclerosing cholangitis, Hepatology, 3, 150, 10.1002/hep.1840030203

Biancone, 1995, Production of immunoglobulin G and G1 antibodies to cytoskeletal protein by lamina propria cells in ulcerative colitis, Gastroenterology, 109, 3, 10.1016/0016-5085(95)90263-5

Geng, 1998, Tropomyosin isoforms in intestinal mucosa: Production of autoantibodies to tropomyosin isoforms in ulcerative colitis, Gastroenterology, 114, 912, 10.1016/S0016-5085(98)70310-5

Das, 1987, The production and characterization of monoclonal antibodies to a human colonic antigen associated with ulcerative colitis: Cellular localization of the antigen by using the monoclonal antibody, J Immunol, 139, 77, 10.4049/jimmunol.139.1.77

Das, 1990, A shared and unique epitope[s] on human colon, skin, and biliary epithelium detected by a monoclonal antibody, Gastroenterology, 98, 464, 10.1016/0016-5085(90)90839-S

Bhagat, 1994, A shared and unique peptide in the human colon, eye, and joint detected by a monoclonal antibody, Gastroenterology, 107, 103, 10.1016/0016-5085(94)90066-3

Parkes, 2013, Genetic insights into common pathways and complex relationships among immune-mediated diseases, Nat Rev Genet, 14, 661, 10.1038/nrg3502

Severs, 2016, Smoking is associated with extra-intestinal manifestations in inflammatory bowel disease, J Crohns Colitis, 10, 455, 10.1093/ecco-jcc/jjv238

Park, 2017, IBD immunopathogenesis: A comprehensive review of inflammatory molecules, Autoimmun Rev, 16, 416, 10.1016/j.autrev.2017.02.013

Pastor Rojo, 2007, Serum lipopolysaccharide-binding protein in endotoxemic patients with inflammatory bowel disease, Inflamm Bowel Dis, 13, 269, 10.1002/ibd.20019

Adenis, 1992, Increased pulmonary and intestinal permeability in Crohn’s disease, Gut, 33, 678, 10.1136/gut.33.5.678

Sherlock, 2012, IL-23 induces spondyloarthropathy by acting on ROR-γt+ CD3+CD4–CD8– entheseal resident T cells, Nat Med, 18, 1069, 10.1038/nm.2817

Condliffe, 1998, Neutrophil priming: Pathophysiological consequences and underlying mechanisms, Clin Sci [Lond], 94, 461, 10.1042/cs0940461

McCarthy, 1991, Peripheral blood neutrophils in inflammatory bowel disease: Morphological evidence of in vivo activation in active disease, Clin Exp Immunol, 86, 489, 10.1111/j.1365-2249.1991.tb02958.x

Nikolaus, 1998, Increased secretion of pro-inflammatory cytokines by circulating polymorphonuclear neutrophils and regulation by interleukin 10 during intestinal inflammation, Gut, 42, 470, 10.1136/gut.42.4.470

Smith, 2009, Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn’s disease, J Exp Med, 206, 1883, 10.1084/jem.20091233

Sanders, 2014, Increased production of retinoic acid by intestinal macrophages contributes to their inflammatory phenotype in patients with Crohn’s disease, Gastroenterology, 146, 1278, 10.1053/j.gastro.2014.01.057

Clarke, 2010, Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity, Nat Med, 16, 228, 10.1038/nm.2087

Balmer, 2014, Microbiota-derived compounds drive steady-state granulopoiesis via MyD88/TICAM signaling, J Immunol, 193, 5273, 10.4049/jimmunol.1400762

Iwamura, 2017, Sensing of the microbiota by NOD1 in mesenchymal stromal cells regulates murine hematopoiesis, Blood, 129, 171, 10.1182/blood-2016-06-723742

Khosravi, 2014, Gut microbiota promote hematopoiesis to control bacterial infection, Cell Host Microbe, 15, 374, 10.1016/j.chom.2014.02.006

Shi, 2011, Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands, Immunity, 34, 590, 10.1016/j.immuni.2011.02.016

Griseri, 2012, Dysregulated hematopoietic stem and progenitor cell activity promotes interleukin-23–driven chronic intestinal inflammation, Immunity, 37, 1116, 10.1016/j.immuni.2012.08.025

Askenase, 2015, Bone-marrow–resident NK cells prime monocytes for regulatory function during infection, Immunity, 42, 1130, 10.1016/j.immuni.2015.05.011

Trompette, 2014, Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis, Nat Med, 20, 159, 10.1038/nm.3444

Kim, 2014, Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE₂, Cell Host Microbe, 15, 95, 10.1016/j.chom.2013.12.010

Breban, 2017, Faecal microbiota study reveals specific dysbiosis in spondyloarthritis, Ann Rheum Dis, 76, 1614, 10.1136/annrheumdis-2016-211064

Tito, 2017, Brief report: Dialister as a microbial marker of disease activity in spondyloarthritis, Arthritis Rheumatol, 69, 114, 10.1002/art.39802

Scher, 2015, Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease, Arthritis Rheumatol, 67, 128, 10.1002/art.38892

Eppinga, 2017, Depletion of Saccharomyces cerevisiae in psoriasis patients, restored by dimethylfumarate therapy [DMF], PLoS One, 12, e0176955, 10.1371/journal.pone.0176955

Sabino, 2016, Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD, Gut, 65, 1681, 10.1136/gutjnl-2015-311004

Bajer, 2017, Distinct gut microbiota profiles in patients with primary sclerosing cholangitis and ulcerative colitis, World J Gastroenterol, 23, 4548, 10.3748/wjg.v23.i25.4548

Zinkernagel, 2017, Association of the intestinal microbiome with the development of neovascular age-related macular degeneration, Sci Rep, 7, 40826, 10.1038/srep40826

Wen, 2018, Epigenetics, microbiota, and intraocular inflammation: new paradigms of immune regulation in the eye, Prog Retin Eye Res, 64, 84, 10.1016/j.preteyeres.2018.01.001

Crost, 2016, The mucin-degradation strategy of Ruminococcus gnavus: The importance of intramolecular trans-sialidases, Gut Microbes, 7, 302, 10.1080/19490976.2016.1186334

Swann, 2011, Systemic gut microbial modulation of bile acid metabolism in host tissue compartments, Proc Natl Acad Sci U S A, 108, 4523, 10.1073/pnas.1006734107

Hedin, 2017, The gut microbiota of siblings offers insights into microbial pathogenesis of inflammatory bowel disease, Gut Microbes, 8, 359, 10.1080/19490976.2017.1284733

Hansen, 2012, Patterns of early gut colonization shape future immune responses of the host, PLoS One, 7, e34043, 10.1371/journal.pone.0034043

Montoya, 2016, Patients with ankylosing spondylitis have been breast fed less often than healthy controls: A case–control retrospective study, Ann Rheum Dis, 75, 879, 10.1136/annrheumdis-2015-208187

van Sommeren, 2014, Extraintestinal manifestations and complications in inflammatory bowel disease: From shared genetics to shared biological pathways, Inflamm Bowel Dis, 20, 987

Satsangi, 1996, Clinical patterns of familial inflammatory bowel disease, Gut, 38, 738, 10.1136/gut.38.5.738

Taleban, 2016, Ocular manifestations in inflammatory bowel disease are associated with other extra-intestinal manifestations, gender, and genes implicated in other immune-related traits, J Crohns Colitis, 10, 43, 10.1093/ecco-jcc/jjv178

Peeters, 2004, Radiological sacroiliitis, a hallmark of spondylitis, is linked with CARD15 gene polymorphisms in patients with Crohn’s disease, Ann Rheum Dis, 63, 1131, 10.1136/ard.2004.021774

Martin, 2002, Anterior uveitis: Current concepts of pathogenesis and interactions with the spondyloarthropathies, Curr Opin Rheumatol, 14, 337, 10.1097/00002281-200207000-00001

Kontoyiannis, 1999, Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: Implications for joint and gut-associated immunopathologies, Immunity, 10, 387, 10.1016/S1074-7613(00)80038-2

Bamias, 2013, Intestinal-specific TNFα overexpression induces Crohn’s-like ileitis in mice, PLoS One, 8, e72594, 10.1371/journal.pone.0072594

Roulis, 2016, Host and microbiota interactions are critical for development of murine Crohn’s-like ileitis, Mucosal Immunol, 9, 787, 10.1038/mi.2015.102

Apostolaki, 2008, Role of beta7 integrin and the chemokine/chemokine receptor pair CCL25/CCR9 in modeled TNF-dependent Crohn’s disease, Gastroenterology, 134, 2025, 10.1053/j.gastro.2008.02.085

Hammer, 1990, Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human β2m: An animal model of HLA-B27–associated human disorders, Cell, 63, 1099, 10.1016/0092-8674(90)90512-D

DeLay, 2009, HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats, Arthritis Rheum, 60, 2633, 10.1002/art.24763

Turner, 2005, HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response, J Immunol, 175, 2438, 10.4049/jimmunol.175.4.2438

Rath, 1996, Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats, J Clin Invest, 98, 945, 10.1172/JCI118878

Ruutu, 2012, β-glucan triggers spondylarthritis and Crohn’s disease–like ileitis in SKG mice, Arthritis Rheum, 64, 2211, 10.1002/art.34423

Benham, 2014, Interleukin-23 mediates the intestinal response to microbial β-1,3-glucan and the development of spondyloarthritis pathology in SKG mice, Arthritis Rheumatol, 66, 1755, 10.1002/art.38638

Milia, 2009, HLA-B27 transgenic rat: An animal model mimicking gut and joint involvement in human spondyloarthritides, Ann N Y Acad Sci, 1173, 570, 10.1111/j.1749-6632.2009.04757.x

Fiorino, 2009, Review article: Anti TNF-α induced psoriasis in patients with inflammatory bowel disease, Aliment Pharmacol Ther, 29, 921, 10.1111/j.1365-2036.2009.03955.x

Fiorino, 2014, Paradoxical immune-mediated inflammation in inflammatory bowel disease patients receiving anti-TNF-α agents, Autoimmun Rev, 13, 15, 10.1016/j.autrev.2013.06.005

Palucka, 2005, Cross-regulation of TNF and IFN-alpha in autoimmune diseases, Proc Natl Acad Sci U S A, 102, 3372, 10.1073/pnas.0408506102

de Gannes, 2007, Psoriasis and pustular dermatitis triggered by TNF-α inhibitors in patients with rheumatologic conditions, Arch Dermatol, 143, 223, 10.1001/archderm.143.2.223

Nestle, 2005, Defining upstream elements of psoriasis pathogenesis: An emerging role for interferon alpha, J Invest Dermatol, 125, xiv, 10.1111/j.0022-202X.2005.23923.x

Greuter, 2017, Skin manifestations of inflammatory bowel disease, Clin Rev Allergy Immunol, 53, 413, 10.1007/s12016-017-8617-4

Rahier, 2010, Severe skin lesions cause patients with inflammatory bowel disease to discontinue anti-tumor necrosis factor therapy, Clin Gastroenterol Hepatol, 8, 1048, 10.1016/j.cgh.2010.07.022

Vavricka, 2018, Expression patterns of TNFα, MAdCAM1, and STAT3 in intestinal and skin manifestations of inflammatory bowel disease, J Crohns Colitis, 12, 347, 10.1093/ecco-jcc/jjx158

Varkas, 2017, An induction or flare of arthritis and/or sacroiliitis by vedolizumab in inflammatory bowel disease: A case series, Ann Rheum Dis, 76, 878, 10.1136/annrheumdis-2016-210233

Tadbiri, 2018, Impact of vedolizumab therapy on extra-intestinal manifestations in patients with inflammatory bowel disease: A multicentre cohort study nested in the OBSERV-IBD cohort, Aliment Pharmacol Ther, 47, 485, 10.1111/apt.14419

Hadis, 2011, Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria, Immunity, 34, 237, 10.1016/j.immuni.2011.01.016

Cassani, 2011, Gut-tropic T cells that express integrin α4β7 and CCR9 are required for induction of oral immune tolerance in mice, Gastroenterology, 141, 2109, 10.1053/j.gastro.2011.09.015

Tillack, 2014, Anti-TNF antibody–induced psoriasiform skin lesions in patients with inflammatory bowel disease are characterised by interferon-γ–expressing Th1 cells and IL-17A/IL-22–expressing Th17 cells and respond to anti-IL-12/IL-23 antibody treatment, Gut, 63, 567, 10.1136/gutjnl-2012-302853

Andrisani, 2013, Development of psoriasis scalp with alopecia during treatment of Crohn’s disease with infliximab and rapid response to both diseases to ustekinumab, Eur Rev Med Pharmacol Sci, 17, 2831

Gregoriou, 2011, Pustular psoriasis development after initial ustekinumab administration in chronic plaque psoriasis, Eur J Dermatol, 21, 104, 10.1684/ejd.2011.1164

Hueber, 2012, Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn’s disease: Unexpected results of a randomised, double-blind placebo-controlled trial, Gut, 61, 1693, 10.1136/gutjnl-2011-301668

Hohenberger, 2018, Interleukin-17 inhibition: Role in psoriasis and inflammatory bowel disease, J Dermatolog Treat, 29, 13, 10.1080/09546634.2017.1329511

Brooklyn, 2006, Infliximab for the treatment of pyoderma gangrenosum: A randomised, double blind, placebo controlled trial, Gut, 55, 505, 10.1136/gut.2005.074815

Karreman, 2017, The prevalence and incidence of axial and peripheral spondyloarthritis in inflammatory bowel disease: A systematic review and meta-analysis, J Crohns Colitis, 11, 631

Dougados, 2011, Spondyloarthritis, Lancet, 377, 2127, 10.1016/S0140-6736(11)60071-8

Queiro, 2000, Subclinical sacroiliitis in inflammatory bowel disease: A clinical and follow-up study, Clin Rheumatol, 19, 445, 10.1007/s100670070003

Peeters, 2008, Clinical and genetic factors associated with sacroiliitis in Crohn’s disease, J Gastroenterol Hepatol, 23, 132, 10.1111/j.1440-1746.2007.05108.x

de Vlam, 2000, Spondyloarthropathy is underestimated in inflammatory bowel disease: Prevalence and HLA association, J Rheumatol, 27, 2860

Salvarani, 2001, Musculoskeletal manifestations in a population-based cohort of inflammatory bowel disease patients, Scand J Gastroenterol, 36, 1307, 10.1080/003655201317097173

Bourikas, 2009, Musculoskeletal manifestations of inflammatory bowel disease, Inflamm Bowel Dis, 15, 1915, 10.1002/ibd.20942

Rudwaleit, 2009, The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis [part II]: Validation and final selection, Ann Rheum Dis, 68, 777, 10.1136/ard.2009.108233

Rudwaleit, 2011, The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general, Ann Rheum Dis, 70, 25, 10.1136/ard.2010.133645

Sepriano, 2017, Performance of the ASAS classification criteria for axial and peripheral spondyloarthritis: A systematic literature review and meta-analysis, Ann Rheum Dis, 76, 886, 10.1136/annrheumdis-2016-210747

Amor, 1990, Criteria of the classification of spondylarthropathies, Rev Rhum Mal Osteoartic, 57, 85

Dougados, 1991, The European Spondylarthropathy Study Group preliminary criteria for the classification of spondylarthropathy, Arthritis Rheum, 34, 1218, 10.1002/art.1780341003

van der Linden, 1984, Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria, Arthritis Rheum, 27, 361, 10.1002/art.1780270401

van der Heijde, 2009, ASDAS, a highly discriminatory ASAS-endorsed disease activity score in patients with ankylosing spondylitis, Ann Rheum Dis, 68, 1811, 10.1136/ard.2008.100826

Mease, 2015, Randomized controlled trial of adalimumab in patients with nonpsoriatic peripheral spondyloarthritis, Arthritis Rheumatol, 67, 914, 10.1002/art.39008

Trusko, 2013, The Standardization of Uveitis Nomenclature [SUN] Project. Development of a clinical evidence base utilizing informatics tools and techniques, Methods Inf Med, 52, 259, 10.3414/ME12-01-0063

Jabs, 2005, Standardization of uveitis nomenclature for reporting clinical data. Results of the First International Workshop, Am J Ophthalmol, 140, 509, 10.1016/j.ajo.2005.03.057

Vavricka, 2011, Frequency and risk factors for extraintestinal manifestations in the Swiss inflammatory bowel disease cohort, Am J Gastroenterol, 106, 110, 10.1038/ajg.2010.343

Vavricka, 2015, Extraintestinal manifestations of inflammatory bowel disease, Inflamm Bowel Dis, 21, 1982, 10.1097/MIB.0000000000000392

Fredriksson, 1978, Severe psoriasis—oral therapy with a new retinoid, Dermatologica, 157, 238, 10.1159/000250839

Marks, 1989, Assessment of disease progress in psoriasis, Arch Dermatol, 125, 235, 10.1001/archderm.1989.01670140087017

Ramsay, 1991, Measurement of involved surface area in patients with psoriasis, Br J Dermatol, 124, 565, 10.1111/j.1365-2133.1991.tb04952.x

Hanifin, 2001, The eczema area and severity index [EASI]: assessment of reliability in atopic dermatitis. EASI Evaluator Group, Exp Dermatol, 10, 11, 10.1034/j.1600-0625.2001.100102.x

Weizman, 2014, Clinical, serologic, and genetic factors associated with pyoderma gangrenosum and erythema nodosum in inflammatory bowel disease patients, Inflamm Bowel Dis, 20, 525, 10.1097/01.MIB.0000442011.60285.68

Alonso, 2015, Identification of risk loci for Crohn’s disease phenotypes using a genome-wide association study, Gastroenterology, 148, 794, 10.1053/j.gastro.2014.12.030

Cortes, 2013, Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci, Nat Genet, 45, 730, 10.1038/ng.2667

Reveille, 2015, Biomarkers for diagnosis, monitoring of progression, and treatment responses in ankylosing spondylitis and axial spondyloarthritis, Clin Rheumatol, 34, 1009, 10.1007/s10067-015-2949-3

Prajzlerová, 2016, An update on biomarkers in axial spondyloarthritis, Autoimmun Rev, 15, 501, 10.1016/j.autrev.2016.02.002

Menti, 2016, Bayesian machine learning techniques for revealing complex interactions among genetic and clinical factors in association with extra-intestinal manifestations in IBD patients, AMIA Annu Symp Proc, 2016, 884

van Gaalen, 2014, Assessment of sacroiliitis by radiographs and MRI: Where are we now?, Curr Opin Rheumatol, 26, 384, 10.1097/BOR.0000000000000066

Atzeni, 2014, Rheumatic manifestations in inflammatory bowel disease, Autoimmun Rev, 13, 20, 10.1016/j.autrev.2013.06.006

Hermann, 2012, Descriptions of spinal MRI lesions and definition of a positive MRI of the spine in axial spondyloarthritis: a consensual approach by the ASAS/OMERACT MRI study group, Ann Rheum Dis, 71, 1278, 10.1136/ard.2011.150680

Sudoł-Szopińska, 2016, Diagnostic imaging of psoriatic arthritis. Part II: magnetic resonance imaging and ultrasonography, J Ultrason, 16, 163, 10.15557/JoU.2016.0018

D’Agostino, 2011, How to diagnose spondyloarthritis early? Accuracy of peripheral enthesitis detection by power Doppler ultrasonography, Ann Rheum Dis, 70, 1433, 10.1136/ard.2010.138701

Maksymowych, 2009, Progress in spondylarthritis. Spondyloarthritis: Lessons from imaging, Arthritis Res Ther, 11, 222, 10.1186/ar2665

van der Heijde, 2005, How should treatment effect on spinal radiographic progression in patients with ankylosing spondylitis be measured?, Arthritis Rheum, 52, 1979, 10.1002/art.21133

Spoorenberg, 2004, Radiological scoring methods in ankylosing spondylitis. Reliability and change over 1 and 2 years, J Rheumatol, 31, 125

Baraliakos, 2005, Inflammation in ankylosing spondylitis: A systematic description of the extent and frequency of acute spinal changes using magnetic resonance imaging, Ann Rheum Dis, 64, 730, 10.1136/ard.2004.029298

Braun, 2003, Magnetic resonance imaging examinations of the spine in patients with ankylosing spondylitis, before and after successful therapy with infliximab: Evaluation of a new scoring system, Arthritis Rheum, 48, 1126, 10.1002/art.10883

MacKay, 1998, The bath ankylosing spondylitis radiology index [BASRI]: A new, validated approach to disease assessment, Arthritis Rheum, 41, 2263, 10.1002/1529-0131(199812)41:12<2263::AID-ART23>3.0.CO;2-I

Van Praet, 2013, Microscopic gut inflammation in axial spondyloarthritis: A multiparametric predictive model, Ann Rheum Dis, 72, 414, 10.1136/annrheumdis-2012-202135

Mundwiler, 2009, Inflammatory bowel disease serologies in ankylosing spondylitis patients: A pilot study, Arthritis Res Ther, 11, R177, 10.1186/ar2866

Wallis, 2013, Elevated serum anti-flagellin antibodies implicate subclinical bowel inflammation in ankylosing spondylitis: An observational study, Arthritis Res Ther, 15, R166, 10.1186/ar4350

Jiang, 2006, Retrospective survey of 452 patients with inflammatory bowel disease in Wuhan city, central China, Inflamm Bowel Dis, 12, 212, 10.1097/01.MIB.0000201098.26450.ae

Burisch, 2014, East–West gradient in the incidence of inflammatory bowel disease in Europe: The ECCO-EpiCom inception cohort, Gut, 63, 588, 10.1136/gutjnl-2013-304636

Ng, 2016, Early course of inflammatory bowel disease in a population-based inception cohort study from 8 countries in Asia and Australia, Gastroenterology, 150, 86, 10.1053/j.gastro.2015.09.005

Lakatos, 2003, Association of extraintestinal manifestations of inflammatory bowel disease in a province of western Hungary with disease phenotype: Results of a 25-year follow-up study, World J Gastroenterol, 9, 2300, 10.3748/wjg.v9.i10.2300

Roberts, 2014, Extraintestinal manifestations of inflammatory bowel disease and the influence of smoking, Digestion, 90, 122, 10.1159/000363228

Karmiris, 2016, Prevalence and characteristics of extra-intestinal manifestations in a large cohort of Greek patients with inflammatory bowel disease, J Crohns Colitis, 10, 429, 10.1093/ecco-jcc/jjv232

Orchard, 1998, Peripheral arthropathies in inflammatory bowel disease: Their articular distribution and natural history, Gut, 42, 387, 10.1136/gut.42.3.387

Vegh, 2016, Association of extraintestinal manifestations and anaemia with disease outcomes in patients with inflammatory bowel disease, Scand J Gastroenterol, 51, 848, 10.3109/00365521.2016.1140807

Isene, 2015, Extraintestinal manifestations in Crohn’s disease and ulcerative colitis: Results from a prospective, population-based European inception cohort, Scand J Gastroenterol, 50, 300, 10.3109/00365521.2014.991752

Ott, 2014, Smoking increases the risk of extraintestinal manifestations in Crohn’s disease, World J Gastroenterol, 20, 12269, 10.3748/wjg.v20.i34.12269

Bernstein, 2001, The prevalence of extraintestinal diseases in inflammatory bowel disease: A population-based study, Am J Gastroenterol, 96, 1116, 10.1111/j.1572-0241.2001.03756.x

Manguso, 2004, Cigarette smoking and appendectomy are risk factors for extraintestinal manifestations in ulcerative colitis, Am J Gastroenterol, 99, 327, 10.1111/j.1572-0241.2004.04039.x

Orchard, 2009, The prevalence, clinical features and association of HLA-B27 in sacroiliitis associated with established Crohn’s disease, Aliment Pharmacol Ther, 29, 193, 10.1111/j.1365-2036.2008.03868.x

Orchard, 2002, Uveitis and erythema nodosum in inflammatory bowel disease: Clinical features and the role of HLA genes, Gastroenterology, 123, 714, 10.1053/gast.2002.35396

Orchard, 2000, Clinical phenotype is related to HLA genotype in the peripheral arthropathies of inflammatory bowel disease, Gastroenterology, 118, 274, 10.1016/S0016-5085(00)70209-5

Klingberg, 2017, A longitudinal study of fecal calprotectin and the development of inflammatory bowel disease in ankylosing spondylitis, Arthritis Res Ther, 19, 21, 10.1186/s13075-017-1223-2

Peyrin-Biroulet, 2017, Systematic review of tumor necrosis factor antagonists in extraintestinal manifestations in inflammatory bowel disease, Clin Gastroenterol Hepatol, 15, 25, 10.1016/j.cgh.2016.06.025

Hirten, 2015, Vedolizumab and infliximab combination therapy in the treatment of Crohn’s disease, Am J Gastroenterol, 110, 1737, 10.1038/ajg.2015.355

Vande Casteele, 2017, American Gastroenterological Association Institute technical review on the role of therapeutic drug monitoring in the management of inflammatory bowel diseases, Gastroenterology, 153, 835, 10.1053/j.gastro.2017.07.031

Peyrin-Biroulet, 2016, Defining disease severity in inflammatory bowel diseases: Current and future directions, Clin Gastroenterol Hepatol, 14, 348, 10.1016/j.cgh.2015.06.001

Pincus, 2002, Urgent care and tight control of rheumatoid arthritis as in diabetes and hypertension: Better treatments but a shortage of rheumatologists, Arthritis Rheum, 46, 851, 10.1002/art.10202

Rachmani, 2005, Treatment of high-risk patients with diabetes: Motivation and teaching intervention: A randomized, prospective 8-year follow-up study, J Am Soc Nephrol, 16, S22, 10.1681/ASN.2004110965

Eeg-Olofsson, 2007, Glycemic and risk factor control in type 1 diabetes: Results from 13,612 patients in a national diabetes register, Diabetes Care, 30, 496, 10.2337/dc06-1406

Patel, 2007, Effects of a fixed combination of perindopril and indapamide on macrovascular and microvascular outcomes in patients with type 2 diabetes mellitus [the ADVANCE trial]: A randomised controlled trial, Lancet, 370, 829, 10.1016/S0140-6736(07)61303-8

Peyrin-Biroulet, 2015, Selecting therapeutic targets in inflammatory bowel disease [STRIDE]: Determining therapeutic goals for treat-to-target, Am J Gastroenterol, 110, 1324, 10.1038/ajg.2015.233

Office of Communications, Division of Drug Information, Center for Drug Evaluation and Research, Food and Drug Administration, 10903 New Hampshire Ave., Silver Spring, Maryland, USA

Guyatt, 1989, A new measure of health status for clinical trials in inflammatory bowel disease, Gastroenterology, 96, 804, 10.1016/0016-5085(89)90905-0

Love, 1992, Quality of life in inflammatory bowel disease, J Clin Gastroenterol, 14, 15, 10.1097/00004836-199201000-00005

Reilly, 1993, The validity and reproducibility of a work productivity and activity impairment instrument, Pharmacoeconomics, 4, 353, 10.2165/00019053-199304050-00006

Ware, 1996, A 12-item short-form health survey: Construction of scales and preliminary tests of reliability and validity, Med Care, 34, 220, 10.1097/00005650-199603000-00003

Cheung, 2009, EQ-5D User Guide: Basic Information on how to use the EQ-5D Version 2.0