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Contents

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Preface

Inflammatory bowel disease research is changing. Progress in defining and treating these diseases is advancing in lock step with the furious pace of technological advances that continue to refine the tools of discovery. With sequencing of the entire genome completed, genetics research is providing direction for molecular and immunological in vivo and in vitro investigation, which in turn directs the development of targeted therapeutics. As translational investigation evolves, what is learned in clinical research is combined with what is learned in basic science research and is leading to a “personalized medicine” approach for managing inflammatory bowel diseases and is bringing the potential of prevention into view.

As Editors, our intention is that this book will provide insight along the entire continuum from basic science to clinical practice. The basic science chapters present findings in the context of what has already been established about the clinicopathological nature of the diseases. The clinical chapters describe the most effective applications of all available diagnostic and therapeutic approaches. This book reflects today’s trends toward globalism and is a truly international effort. We encouraged our contributors to editorialize and provide thought-provoking, progress-stimulating content in their manuscripts. Now, more than ever, is the combination of all disciplines working in concert with the pharmaceutical industry key to the development of better treatments, with fewer side effects, and for predicting patient responses. As drugs become more specialized, it is vitally important to describe carefully patient populations both for study and for treatment. With ever increasing evidence that the inflammatory bowel diseases are heterogeneous disorders, drugs will likely only be effective in certain subpopulations of patients.

Above all, we hope that this book will stimulate future research to the point that achieving a diagnosis and development of a treatment plan will be directed by genetic, immunological and clinical markers of phenotypic distinctions.

We would like to express our sincere gratitude to each of the authors, our colleagues and partners, for nearly three decades of commitment to inflammatory bowel disease, and for their insightful, field-leading contributions. We would also like to acknowledge the commitment, patience and support of our publishers, Wiley-Blackwell, particularly Alison Brown, Adam Gilbert, Gill Whitley, Elisabeth Dodds and Oliver Walter.

Stephan R. Targan
Los Angeles
Fergus Shanahan
Cork
Loren C. Karp
Los Angeles

List of Contributors

Faten N. Aberra

Assistant Professor of Medicine
Division of Gastroenterology
University of Pennsylvania Philadelphia, PA, USA

Maria T. Abreu

Chief, Division of Gastroenterology
Department of Medicine
University of Miami Miller School of Medicine
Miami, FL, USA

David H. Alpers

William B. Kountz Professor of Medicine
Department of Internal Medicine
Division of Gastroenterology
Washington University School of Medicine
St Louis, MO, USA

Raja Atreya

Laboratory of Immunology
Department of Medicine
University of Mainz
Mainz, Germany

Mohammad Azam

Gastroenterology Research Registrar
Department of Gastroenterology
Connolly Hospital
Dublin,Ireland

Charles N. Bernstein

Professor of Medicine
Head, Section of Gastroenterology
Director, University of Manitoba IBD Clinical and
Research Centre
Bingham Chair in Gastroenterology
University of Manitoba
Winnipeg, Manitoba, Canada

David G. Binion

Co-Director, Inflammatory Bowel Disease Center
Director, Translational IBD Research;
Visiting Professor of Medicine
Division of Gastroenterology, Hepatology and Nutrition
University of Pittsburgh School of Medicine
Pittsburgh, PA, USA

Richard S. Blumberg

Chief, Division of Gastroenterology, Hepatology and Endoscopy
Brigham and Women’s Hospital
Professor of Medicine, Harvard Medical School
Boston, MA USA

Leonidas A. Bourikas

Fellow in Gastroenterology
University Hospital of Heraklion
University of Crete Medical School
Heraklion, Crete, Greece

Keith Breglio

Inflammatory Bowel Disease Center
Division of Gastroenterology
Department of Pediatrics
Mount Sinai School of Medicine
New York, NY, USA

Roger Chapman

Gastroenterology Unit
John Radcliffe Hospital
Oxford, UK

Lea Ann Chen

Mount Sinai School of Medicine
New York, NY, USA

Stephen M. Collins

Professor of Medicine
The Farncombe Family Digestive Health Institute
McMaster University Medical Centre
Hamilton, ON, Canada

William Connell

Director, IBD Clinic
Department of Gastroenterology
St Vincent’s Hospital Melbourne
Fitzroy, Victoria, Australia

Ross D. Cranston

Assistant Professor
Division of Infectious Diseases
Department of Medicine
University of Pittsburgh
Pittsburgh, PA, USA

Kenneth Croitoru

Professor of Medicine
Mount Sinai Hospital;
Department of Medicine
University of Toronto
Toronto, ON, Canada

Sue Cullen

Consultant Gastroenterologist
Department of Gastroenterology
Wycombe General Hospital
High Wycombe, Bucks, UK

Sun-Chuan Dai

Department of Medicine
Cedars-Sinai Medical Center
Los Angeles, CA, USA

Lee A. Denson

Division of Gastroenterology, Hepatology, and Nutrition
Cincinnati Children’s Hospital Medical Center
Cincinnati, OH, USA

Shane M. Devlin

Clinical Assistant Professor
Inflammatory Bowel Disease Clinic
Division of Gastroenterology
The University of Calgary
Calgary, Alberta, Canada

Marla C. Dubinsky

Associate Professor of Pediatrics
Director of Pediatric IBD Center
Cedars-Sinai Medical Center
Los Angeles, CA, USA

Laurence J. Egan

Professor of Clinical Pharmacology
Clinical Science Institute
National University of Ireland
Galway, Ireland

Charles O. Elson

Division of Gastroenterology and Hepatology
Department of Medicine
University of Alabama at Birmingham
Birmingham,AL, USA

Sue C. Eng

Clinical Gastroenterologist
Eastside Gastroenterology
Kirkland, WA, USA

Richard J. Farrell

Consultant Gastroenterologist
Department of Gastroenterology
Connolly Hospital
Dublin, Ireland

Michael J.G. Farthing

Vice-Chancellor and Professor of Medicine
University of Sussex
Sussex House
Brighton, Sussex, UK

Victor W. Fazio

Chairman, Digestive Disease Institute
Cleveland Clinic
Cleveland, OH, USA

Masayuki Fukata

Division of Gastroenterology
Department of Medicine
University of Miami Miller School of Medicine
Miami, FL, USA

Marc Girardin

Research Fellow
Division of Gastroenterology
Montreal General Hospital
McGill University
Montreal, QC, Canada

D. Neil Granger

Boyd Professor and Head
Department of Molecular and Cellular Physiology
Louisiana State University Health Sciences Center
Shreveport, LA, USA

Matthew B. Grisham

Boyd Professor
Department of Molecular and Cellular Physiology
Louisiana State University Health Sciences Center
Shreveport, LA, USA

Norman R. Harris

Professor
Department of Molecular and Cellular Physiology
Louisiana State University Health Sciences Center
Shreveport, LA, USA

Steven Itzkowitz

Professor of Medicine
Mount Sinai School of Medicine
New York, NY, USA

Derek P. Jewell

Professor of Gastroenterology
John Radcliffe Hospital
Oxford, UK

Myles R. Joyce

Clinical Associate, Colorectal Surgery
Digestive Disease Institute
Cleveland Clinic Cleveland, OH, USA

Loren C. Karp

Cedars-Sinai Medical Center
Los Angeles, CA, USA

John Keohane

Alimentary Pharmabiotic Centre
Department of Medicine
University College Cork
National University of Ireland
Cork, Ireland

Christopher G. Kevil

Associate Professor Department of Pathology
Louisiana State University Health Sciences Center
Shreveport, LA, USA

Pokala Ravi Kiran

Clinical Fellow
Department of Colorectal Surgery
The Cleveland Clinic Foundation
Cleveland, OH, USA

Louise Langmead

Consultant Physician and Gastroenterologist
Digestive Diseases Clinical Academic Unit
Barts and the London NHS Trust London, UK

Keith Leiper

Consultant Gastroenterologist
Royal Liverpool University Hospital
School of Clinical Sciences
University of Liverpool
Liverpool, UK

William D. Leslie

Department of Medicine, University of Manitoba;
University of Manitoba Inflammatory Bowel Disease
Center;
Manitoba Bone Density Program University of Manitoba Winnipeg, Manitoba, Canada

James D. Lewis

Center for Clinical Epidemiology and Biostatistics
University of Pennsylvania
Philadelphia, PA, USA

Simon K. Lo

Director of Endoscopy
Clinical Professor
David Geffen School of Medicine at UCLA
Cedars-Sinai Medical Center
Los Angeles, CA, USA

Edward V. Loftus Jr

Professor of Medicine
Inflammatory Bowel Disease Clinic
Division of Gastroenterology and Hepatology
Mayo Clinic
Rochester, MN, USA

Thomas T. MacDonald

Dean for Research and Professor of Immunology
Centre for Immunology and Infectious Disease
Blizard Institute of Cell and Molecular Science
Barts and the
London School of Medicine and Dentistry London, UK

Uma Mahadevan

Associate Professor of Medicine
UCSF Center for Colitis and Crohn’s Disease
San Francisco, CA, USA

Michel H. Maillard

Center for the Study of Inflammatory Bowel Diseases
Gastrointestinal Unit
Massachusetts General Hospital
Harvard Medical School
Boston, MA, USA;
Gastroenterology and Hepatology Unit
CHUV-University of Lausanne Lausanne,
Switzerland

Finbar MacCarthy

Department of Pharmacology and Therapeutics
National University of Ireland
Galway, Ireland

Dermot P. McGovern

Immunobiology Research Institute and IBD Center
Cedars-Sinai Medical Center
Los Angeles, CA, USA

Ian McGowan

Professor of Medicine
Division of Gastroenterology, Hepatology and Nutrition
Department of Medicine, University of Pittsburgh
Pittsburgh, PA, USA

Robin S. McLeod

Professor of Surgery and Health Policy, Management
and Evaluation
University of Toronto;
Angelo and Alfredo De Gasperis Families Chair in
Colorectal Cancer and IBD Research
Zane Cohen Digestive Disease Research Unit and Samuel
Lunenfeld Research Institute
Mount Sinai Hospital
Toronto, ON, Canada

Giovanni Monteleone

Professor of Gastroenterology
University of Rome “Tor Vergata”
Rome, Italy

Division of Gastroenterology
University of Washington School of Medicine
Seattle, WA, USA

Markus F. Neurath

Laboratory of Immunology
Department of Medicine
University of Mainz
Mainz, Germany

Diarmuid O’Donoghue

Consultant Physician/Gastroenterologist
Newman Professor of Clinical Research
Centre for Colorectal Disease
St Vincent’s University Hospital
Dublin, Ireland

Seamus O’Mahony

Consultant Physician/Gastroenterologist
Cork University Hospital;
Senior Lecturer in Gastroenterology
University College Cork
Cork, Ireland

Timothy R. Orchard

Department of Gastroenterology and Hepatology
Imperial College London
London, UK

Mark T. Osterman

Assistant Professor
Department of Medicine
University of Pennsylvania
Philadelphia, PA, USA

Konstantinos A. Papadakis

Associate Professor of Medicine
University of Crete Medical School
Division of Gastroenterology
University Hospital of
Heraklion Heraklion, Crete, Greece

Raymond J. Playford

Vice Principal (NHS Liaison) and Vice Principal
(Science and Engineering)
Queen Mary, University of London Barts and the London School of Medicine and Dentistry
London, UK

Daniel K. Podolsky

President
University of Texas Southwestern Medical Center at Dallas
Dallas, TX, USA

Graham L. Radford-Smith

Head, Inflammatory Bowel Disease Unit
Department of Gastroenterology, Royal Brisbane and
Women’s Hospital
Visiting Scientist, Queensland Institute of Medical Research
Associate Professor, Department of Medicine,
University of Queensland
Brisbane, Queensland, Australia

Parvaneh Rafiee

Associate Professor of Surgery
Department of Surgery
Medical College of Wisconsin
Milwaukee, WI, USA

David S. Rampton

Professor of Clinical Gastroenterology
Digestive Diseases Clinical Academic Unit
Institute of Cell and Molecular Science
Barts and the London Queen Mary School of Medicine
and Dentistry
London, UK

Jonathan Rhodes

Professor of Medicine,
School of Clinical Sciences
University of Liverpool
Liverpool, UK

Gerhard Rogler

Division of Gastroenterology and Hepatology
Department of Medicine
University Hospital of Zürich
Zürich, Switzerland

Daniel J. Royston

John Radcliffe Hospital
Headington, Oxford, UK

Sarah Rushworth

Gastroenterology Fellow
School of Clinical Sciences
University of Liverpool
Liverpool, UK

Paul Rutgeerts

Department of Gastroenterology
University Hospital Gasthuisberg
Leuven, Belgium

William J. Sandborn

Inflammatory Bowel Disease Clinic
Division of Gastroenterology and Hepatology
Mayo Clinic and Mayo Clinic College of Medicine
Rochester, MN, USA

Bruce E. Sands

Associate Professor of Medicine
Harvard Medical School
Acting Chief, Gastrointestinal Unit
Medical Co-Director, MGH Crohn’s and Colitis Center Massachusetts General Hospital
Boston, MA, USA

Christine Schlenker

Professor of Medicine
Division of Gastroenterology
Assistant Dean for Faculty of Development
University of Washington
Seattle, WA, USA

Ernest G. Seidman

Professor of Medicine and Pediatrics
Canada Research Chair in Immune Mediated Gastrointestinal
Disorders
Bruce Kaufman Endowed Chair in IBD
McGill University
Montreal, QC, Canada

Fergus Shanahan

Alimentary Pharmabiotic Centre
Department of Medicine
University College Cork
National University of Ireland
Cork, Ireland

Kieran Sheahan

Consultant Histopathologist and Associate Clinical Professor
Centre for Colorectal Disease
St Vincent’s University Hospital and University College Dublin
Dublin, Ireland

Bo Shen

Staff Gastroenterologist
Digestive Disease Institute
Cleveland Clinic
Cleveland, OH, USA

Corey A. Siegel

Assistant Professor of Medicine
Dartmouth Medical School
Director, Dartmouth-Hitchcock IBD Center
Section of Gastroenterology and Hepatology
Lebanon, NH, USA

Scott B Snapper

Associate Chief of Research
Center for the Study of Inflammatory Bowel Diseases
Gastrointestinal Unit
Massachusetts General Hospital
Associate Professor of Medicine
Harvard Medical School
Boston, MA, USA

Christina M. Surawicz

Stephan R. Targan

Cedars-Sinai Medical Center
Los Angeles, CA, USA

Simon Travis

Gastroenterology Unit
John Radcliffe Hospital
Oxford, UK

Gert Van Assche

Associate Professor of Medicine
Department of Gastroenterology
University Hospital Gasthuisberg
Leuven, Belgium

Séverine Vermeire

Department of Gastroenterology
University Hospital Gasthuisberg
Leuven, Belgium

Alissa J. Walsh

Consultant Gastroenterologist
Department of Gastroenterology
St Vincent’s Hospital
Sydney, NSW, Australia

Bryan F. Warren

Honorary Professor Queen Mary College, University of London
Consultant Gastrointestinal Pathologist and Honorary
Senior Lecturer
John Radcliffe Hospital
Headington, Oxford, UK

Casey T. Weaver

Department of Pathology
University of Alabama at Birmingham
Birmingham, AL, USA

Jarrad Wilson

IBD Fellow
Department of Gastroenterology
St Vincent’s Hospital Melbourne
Fitzroy, Victoria, Australia

Sebastian Zeissig

Laboratory of Mucosal Immunology
Brigham and Women’s Hospital
Harvard Medical School
Boston, MA, USA

Renyu Zhang

Clinical Research Fellow
Department of Colorectal Surgery
Cleveland Clinic
Cleveland, OH, USA

Chapter 1

Introduction: the Science and the Art of Inflammatory Bowel Disease

Fergus Shanahan, Loren C. Karp2 & Stephan R. Targan

University College Cork, National University of Ireland, Cork, Ireland

Inflammatory Bowel and Immunobiology Research Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA

This book is about the science and the art and the science of the art of gastroenterology as it pertains to inflammatory bowel disease. Once described as disabling and under-researched diseases, the inflammatory bowel diseases now attract intense interest from clinical and basic investigators, but remain an important cause of suffering and a major burden on healthcare resources.

Why another textbook, in this era of rapid information access? The answer is simple – there is a continuing need for informed opinion and perspective on the deluge of data generated in recent years spanning a diversity of aspects of inflammatory bowel disease. Many wish for a single repository of information from authoritative sources. With this in mind, the authors for this textbook were selected because they are expert and currently active contributors to their respective areas of the field. Each was charged with delivering a crisp, timely and opinionated account of their area with a futuristic perspective.

A recurring theme within modern biology in general and inflammatory bowel disease, in particular, is the need to think across traditional boundaries of intellectual pursuit and to be aware of research at the interface of disparate disciplines. The convergence of different research avenues in inflammatory bowel disease is represented by the host–microbe interface; other pertinent examples have been variably expressed as the brain–gut axis, immunoepithelial dialogue and neuroimmunology. Each is embraced in this textbook in various chapters dealing with disease mechanisms.

One of the great lessons of the recent past in gastroenterology was the failure of traditional epidemiologic and biologic approaches to identify a transmissible agent as the cause of peptic ulcer disease. A more important lesson was that the solution to some complex diseases may never be found by research focused exclusively on the host, without due regard for host–environment interactions, particularly host–microbe interactions. In the future, investigators involved in epidemiologic, genetic or other areas of research in inflammatory bowel disease will have to approach their challenge with some form of rapprochement with disease mechanisms. It is noteworthy, for example, that the genetic risk factors for inflammatory bowel disease are responsible for sensing and interpreting the microenvironment (e.g. NOD2/CARD15) or are involved in the regulation of the host immune response to that microenvironment (e.g. autophagy, IL23R). The complexity and clinical implications of these interactions are discussed by several authors in this volume.

Advances in technology have greatly facilitated research in inflammatory bowel disease. These include automated approaches to gene sequencing and genotyping large numbers of study subjects and molecular strategies for studying the intestinal microbiota, most of which is still unculturable and, therefore, neglected or considered until recently to be obscure. The human organism is now viewed as a composite of the human genome and its commensal microbial genome (microbiome), both of which interact with environmental and lifestyle modifying factors. As the human microbiome project and other similar metagenomic collaborations around the world deliver new information on the diversity and individual variations in the intestinal microbiota, it is anticipated that some of the heterogeneity of inflammatory bowel disease may be resolved. Thus, genetic risk factors will have to be reconciled with variations in microbial composition and with patterns of immunologic responsiveness to the microbiota. The challenge for epidemiologists and biologists will be to relate the aspects of a modern lifestyle with changes in the microbiota and thence with immunologic behavior and susceptibility to disease. Thus, the elucidation of the “IBD genome” provides the foundation for micro- and macro-environmental epidemiologic investigation. The contributing authors to this text have provided the background to this futuristic scenario.

Has the relentless march of the biotech and genotech era of research delivered for the patient? Unquestionably patients are better off today than they were only a generation ago. A more coherent understanding of fundamental disease mechanisms is being translated into improved patient management with a progressive shift toward evidence-based approaches and away from therapeutic empiricism. This is reflected throughout those chapters of this book dedicated to patient care.

Although not quite at the stage of personalized health-care, the splitters are in the ascendancy over the lumpers in today’s approach to the patient with inflammatory bowel disease. Refinement of clinical phenotypes by fusing genetic variation and the functional consequences thereof will lead to the reclassification of standard clinical phenotypes into physiologically determined subgroups and ultimately to individualized therapeutic targeting. These critical steps will continue to inform the interpretation of data on the genotype. This represents just one of many opportunities for clinicians and basic scientists to engage in a mutually beneficial manner in translating bench-to-bedside research to improved management of inflammatory bowel disease.

But some things never change. Clinical care of chronic disease will always require attention to detail, compassion and a commitment to long-term follow-up. In the face of the extraordinary advances in therapeutics, which continue apace, there is substantial patient dissatisfaction with modern medicine, either because of increasing expectations or reduced tolerance of illness. Most patients place greatest emphasis on the doctor–patient relationship. In this relationship, the attitude and level of interest of the former will always be a major determinant of the outcome of the latter.

Textbooks like this cannot confer attitude, energy or enthusiasm on the reader, but they can sensitize and equip the reader with the necessary background information, opinion and perspective. Therein lies the essence of what is intended with this book – to provide stimulus and steerage for the interested clinician, scientist and clinician–scientist in what is already an intriguing and rewarding field of endeavor.