Joint Disease in the Horse, 2e PDF
Preview Joint Disease in the Horse, 2e
JOINT DISEASE IN THE HORSE SECOND EDITION Edited by C. Wayne McIlwraith, BVSc, PhD, Dr med vet Christopher E. Kawcak, DVM, PhD, Diplomate (h.c. Vienna), DSc (Purdue), DSc (h.c. Massey), ACVS & ACVSMR Laurea Dr (h.c. Turin), D vet med (h.c. London), Professor FRCVS, Diplomate ACVS, ECVS, & ACVSMR Iron Rose Ranch University Chair in University Distinguished Professor Musculoskeletal Research Barbara Cox Anthony University Chair in Gail Holmes Equine Orthopaedic Research Center Orthopaedics College of Veterinary Medicine and Biomedical Director Orthopaedic Research Center Sciences Gail Holmes Equine Orthopaedic Research Center School of Biomedical Engineering College of Veterinary Medicine and Biomedical Director of Equine Clinical Services Sciences Colorado State University School of Biomedical Engineering Fort Collins, Colorado Colorado State University P. René van Weeren, DVM, PhD, Diplomate ECVS Fort Collins, Colorado Professor of Equine Musculoskeletal Biology David D. Frisbie, DVM, PhD, Diplomate ACVS & Department of Equine Sciences ACVSMR Faculty of Veterinary Medicine Professor Utrecht University Gail Holmes Equine Orthopaedic Research Center Utrecht, The Netherlands College of Veterinary Medicine and Biomedical Sciences School of Biomedical Engineering Colorado State University Fort Collins, Colorado 3251 Riverport Lane St. Louis, Missouri 63043 JOINT DISEASE IN THE HORSE, SECOND EDITION ISBN: 978-1-4557-5969-9 Copyright © 2016 by Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechani- cal, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permis- sions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher. Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. With respect to any drug or pharmaceutical products identified, readers are advised to check the most current information provided (i) on procedures featured or (ii) by the manufacturer of each product to be administered, to verify the recommended dose or formula, the method and duration of administration, and contraindications. It is the responsibility of practitioners, relying on their own experience and knowledge of their patients, to make diagnoses, to determine dosages and the best treatment for each individual patient, and to take all appropriate safety precautions. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Previous edition copyrighted 1996. Library of Congress Cataloging-in-Publication Data Joint disease in the horse / edited by C. Wayne McIlwraith, David D. Frisbie, Christopher E. Kawcak, P. René van Weeren. -- Second edition. p. ; cm. Includes bibliographical references and index. ISBN 978-1-4557-5969-9 (hardcover : alk. paper) I. McIlwraith, C. Wayne, editor. II. Frisbie, David D., editor. III. Kawcak, Christopher E., editor. IV. van Weeren, P. René 1957- , editor. [DNLM: 1. Horse Diseases. 2. Joint Diseases--veterinary. SF 959.J64] SF959.J64J385 2016 636.1’089672--dc23 2015015062 Vice President and Publisher: Loren Wilson Content Strategy Director: Penny Rudolph Content Development Manager: Jolynn Gower Content Development Specialist: Brandi Graham Publishing Services Manager: Jeffrey Patterson Project Manager: Bill Drone Designer: Brian Salisbury Printed in China. Last digit is the print number: 9 8 7 6 5 4 3 2 1 To Nancy, Myra, Erin, and Madelon for their continued participation in what we do, as well as their support and patience, AND to the horse, whose unselfish efforts and willingness to serve have inspired much of the basic and clinical research reported in this text. C O N T R I B U T O R S Myra F. Barrett, DVM, MS, Diplomate ACVR Christopher E. Kawcak, DVM, PhD, Diplomate ACVS & Assistant Professor of Diagnostic Imaging ACVSMR Gail Holmes Equine Orthopaedic Research Center Professor College of Veterinary Medicine and Biomedical Sciences Iron Rose Ranch University Chair in Musculoskeletal Research Environmental and Radiological Health Sciences Gail Holmes Equine Orthopaedic Research Center Colorado State University College of Veterinary Medicine and Biomedical Sciences Fort Collins, Colorado School of Biomedical Engineering Director of Equine Clinical Services Pieter A. J. Brama, DVM, MBA, PhD, Diplomate ECVS Colorado State University Professor of Veterinary Surgery Fort Collins, Colorado School of Veterinary Medicine Veterinary Science Centre Melissa R. King, DVM, PhD, Diplomate ACVSMR University College Dublin Assistant Professor Belfield, Dublin, Ireland Equine Sports Medicine and Rehabilitation Gail Holmes Equine Orthopaedic Research Center Janny C. de Grauw, DVM, PhD College of Veterinary Medicine and Biomedical Sciences Resident in Veterinary Anesthesiology School of Biomedical Engineering Faculty of Veterinary Medicine Colorado State University Department of Equine Sciences Fort Collins, Colorado Utrecht University Utrecht, The Netherlands C. Wayne McIlwraith, BVSc, PhD, Dr med vet (h.c. Vienna), DSc (Purdue), DSc (h.c. Massey), David D. Frisbie, DVM, PhD, Diplomate ACVS & ACVSMR Laurea Dr (h.c. Turin), D vet med (h.c. London), Professor FRCVS, Diplomate ACVS, ECVS, & ACVSMR Gail Holmes Equine Orthopaedic Research Center University Distinguished Professor College of Veterinary Medicine and Biomedical Sciences Barbara Cox Anthony University Chair in Orthopaedics School of Biomedical Engineering Director Orthopaedic Research Center Colorado State University Gail Holmes Equine Orthopaedic Research Center Fort Collins, Colorado College of Veterinary Medicine and Biomedical Sciences School of Biomedical Engineering Laurie R. Goodrich, DVM, PhD, Diplomate ACVS Colorado State University Associate Professor in Equine Surgery and Lameness Fort Collins, Colorado Gail Holmes Equine Orthopaedic Research Center College of Veterinary Medicine and Biomedical Sciences Kurt Selberg, MS, DVM, MS, Diplomate ACVR School of Biomedical Engineering Assistant Professor Colorado State University Department of Veterinary Biosciences and Diagnostic Fort Collins, Colorado Imaging College of Veterinary Medicine Kevin K. Haussler, DVM, DC, PhD, Diplomate ACVSMR University of Georgia Associate Professor Athens, Georgia Gail Holmes Equine Orthopaedic Research Center College of Veterinary Medicine and Biomedical Sciences School of Biomedical Engineering Colorado State University Fort Collins, Colorado vii viii CONTRIBUTORS P. René van Weeren, DVM, PhD, Diplomate ECVS Natasha M. Werpy, DVM, Diplomate ACVR Professor of Equine Musculoskeletal Biology Associate Professor Department of Equine Sciences Department of Large Animal Clinical Sciences Faculty of Veterinary Medicine College of Veterinary Medicine Utrecht University University of Florida Utrecht, The Netherlands Gainesville, Florida P R E FA C E T O T H E F I R S T E D I T I O N Lameness is the most important cause of wastage in rac- It is the first time a book has been devoted to the subject of ing horses as well as in horses that perform in other athletic joint disease in the horse, and the amount of new information events. Joint injury and joint disease are the most common is impressive. With this book, we hope that clinicians now causes of lameness, and together they represent a major part have a reference base with supportive data to provide more of the caseload for equine clinicians. Many medical and sur- realistic answers to their clients and that the person involved gical treatments exist for various joint problems, but many in research becomes more aware of what work has been com- of these treatments are controversial, particularly with regard pleted to date. to treatment selection and definitive treatment results. In Three issues of semantics require mention. For consis- recent years, much progress has been made in basic research tency, we have chosen to use the word osteoarthritis instead in inflammatory and degenerative joint problems in the of degenerative joint disease, which was previously used by horse. In addition, prospective and retrospective studies have the editors and others as a synonym for osteoarthritis. Osteo- resulted in more realistic figures for the prognosis and treat- arthritis is the preferred term today in the nonequine litera- ment of many clinical entities. Much of the basic work in joint ture and has been adopted in this text. With our international disease was originally done in laboratory animals, but more authorship, as second issue is the use of the term “infectious” recently, considerable original work has been reported in the versus “infective.” As a British author has pointed out to us, horse and in vitro work with equine tissue. infectious is frequently defined as “capable of being spread The purpose of this book is to define the current status of from one host to another with or without direct contact,” the rapidly changing area of developmental and degenerative thus, the equine influenza virus or equine herpesvirus could joint disease, which is of significant clinical importance to the be regarded as an infectious organism. However, “infective” horse. We have been fortunate to obtain contributors who by usage is more restricted in its definition, and Churchill’s have done much of the original work. The principal objec- Medical Dictionary suggests “capable of causing infection” as tives of this book are to present current scientific information its only definition. Therefore, it is felt that in the case of infec- on the basic joint pathobiology and translate it into practical, tive arthritis, bacteria could not be regarded as infectious as clinical usage for the equine clinician. At times, this can be in the case of respiratory viruses, although the bacteria could difficult, and in some instances, only anecdotal information be regarded as infective because it is capable of causing infec- is available. The contents are designed to be of value to both tion. The editors and scrutineers are concerned about this researchers and clinicians. distinction in Britain; whereas in American literature vari- Section I covers general principles in joint pathobiology ous terms (including septic) have been used synonymously. and consists of eight chapters, written by contributors who Both terms are used in this text according to the contributor’s have done original research in their areas. This section pro- preference. Hyaluronic acid, sodium hyaluronate, and hyal- vides the necessary background information to effectively uronan are also used interchangeably. It has been suggested evaluate and interpret the diagnostic and surgical aspects of that when the cation of polysaccharide is undetermined, the the diseases covered later. Section II presents the pathology, compound is properly referred to as hyaluronan; therefore, pathogenesis, and clinical diagnosis of traumatic and degen- this term is used. erative joint disease. Section III discusses the treatments We would like to recognize the editorial and production available for traumatic arthritis and osteoarthritis, includ- staffs of the W.B. Saunders Company for their professional ing physical therapy, nonsteroidal antiinflammatory drugs, efforts on this project. We want to thank the authors for intraarticular corticosteroids, hyaluronan, polysulfated gly- their excellent contributions, and Helen Mawhiney for sec- cosaminoglycan, other chondroprotective drugs, and surgery. retarial assistance. We would also like to acknowledge Tom In Section IV, osteochondritis dissecans, subchondral cystic McCracken, Phil Guzzy, and Conery Calhoun of Biograph- lesions, infective arthritis, and other entities affecting joints ics; and Jenger Smith and Charley Kerlee of CSU Multi-Media are presented. Section V includes current research relative to Instructional Development for their help with illustrations. equine joint disease that has not been presented previously. Dr. McIlwraith gratefully acknowledges Drs. John F. Fessler This includes the use of experimental models in the investi- and David C. Van Sickle for their early influence and mentor- gation of equine arthritis, chondrocyte culturing and explant ing in starting a career in investigating equine joint disease. culture systems, cellular responses and receptor mechanisms Finally, because many joint-associated (or orthopedic) associated with bacterial lipopolysaccharide-induced joint problems remain to be solved for our equine patients, all roy- damage, and finally, a summary by Dr. A. Robin Poole on the alties from this text will be used for ongoing research in our future direction of arthritis research. Equine Orthopedic Research Laboratory at Colorado State In the time since the W.B. Saunders Company approached University. one of us (CWM) to write a book on equine joint disease, C. Wayne McIlwraith considerable new work has been undertaken and, fortunately, much of this is captured in timely fashion by the contributors. Gayle W. Trotter ix P R E FA C E T O T H E S E C O N D E D I T I O N As discussed in the preface to the first edition of this book, future directions in joint disease that will continue to improve lameness is the most important cause of wastage in rac- our ability to treat horses are featured. ing horses as well as in horses that perform in other athletic events. Joint injury and joint disease are the most common ACKNOWLEDGMENTS causes of lameness, and together they represent most of the caseload for equine clinicians. Many medical and surgical Much of the book has been written by the four of us, but we have treatments exist for various joint problems, and there have had particularly critical contributions from Dr. Myra Barrett in been many advances in this area since 1996 as well as much both content and organization with the imaging parts of Chapter clarification of the value of various treatments with evidence- 9 as well as Chapters 20 through 26. Drs. Natasha Werpy and based research. Whereas in 1996 we extrapolated much of Kurt Selberg have also contributed to the imaging chapters; Dr. our information from laboratory animal research and human Janny de Grauw contributed to the chapter on synovial fluid and studies, the majority of this text now provides evidence based serum biomarkers; and Dr. Laurie Goodrich added her expertise on experimental and clinical research in the horse. This to Chapter 27, and Dr. Jos Malda commented on Chapter 1 and increases both the appropriateness of the findings and the Dr. van Weeren’s part of Chapter 27. We also wish to acknowl- clinical translation for the veterinarian. edge Lynsey Bosch for typing and patience and Paula Vander- The purpose of this book is to redefine the current status linden for typing and organization as we have prepared these of the continually changing area of developmental and trau- manuscripts. We also thank Dave Carlson for the line drawings matic joint disease. We are fortunate to have contributors who to go with the radiographs in Chapter 9 and the editorial and pro- have done much of the original work. New biologic therapies duction staffs of Elsevier with special mention to Penny Rudolph that are targeted against specific mediators that have been who started this project; Brandi Graham for her great support, identified with different pathobiologic and biomechanical patience, and editing; and William Drone for copyediting. etiologies. These basics will be presented but limited to what Drs. McIlwraith, Frisbie, and Kawcak wish to acknowledge is clinically relevant. the incredible contributions and assistance of faculty and staff The text begins with a discussion of general anatomy and of the Orthopaedic Research Center and the more recent physiology of joints as well as biomechanics, followed by the program of Equine Sports Medicine and Rehabilitation. This pathogenetic pathways of traumatic arthritis and posttrau- team has facilitated acquisition of much of the information in matic osteoarthritis and the pathologic manifestations of this book and will advance our knowledge for future editions. joint disease. Osteochondritis dissecans, subchondral cystic Dr. van Weeren also acknowledges the great contributions of lesions, septic arthritis, and the effect of loading on joint tis- the present and past members of his research team at Utrecht, sues are then reviewed. The principles of diagnosis follow, with special mention of Dr. Pieter Brama, on whose research with much increased detail on the current state-of-the-art efforts a large part of the content of Chapter 8 is based. in clinical examination and intraarticular injection (includ- In addition, Wayne, Dave, Chris, and René are fortunate to ing simulations based on computed tomography) as well as in be married to experts in this or related areas. Dr. Nancy Good- imaging, which has probably progressed the most in equine man has been Wayne’s major clinical mentor starting in 1983 joint disease use in the 19 years since the first edition was and has given great professional and personal support. Dave published. Frisbie thanks Dr. Myra Barrett-Frisbie, and her major contri- There is a chapter on synovial fluid and serum biomarkers, butions to this text have been previously noted. Chris Kawcak followed by separate chapters with discussion of the validation is married to Dr. Erin Contino, who is a product of our Equine of the various treatment options including nonsteroidal antiin- Sports Medicine and Rehabilitation program as well as our flammatory drugs, intraarticular corticosteroids, hyaluronan, graduate research program and is soon to be a faculty mem- polysulfated glycosaminoglycan, and pentosan polysulfate. ber at Colorado State University. René van Weeren is married Newer therapies that are presented for the first time include to Madelon Bitterling, who is both a human and an animal biologic therapies (including the autologous-conditioned physiotherapist and an expert in veterinary ergonomics. serum products as well as the platelet-rich plasma products We would also like to recognize the funding agencies that and mesenchymal stem cells). Various types of rehabilita- have supported our research. This includes Grayson-Jockey tion including underwater treadmilling as well as a careful Club Research Foundation, American Quarter Horse Associa- discussion of oral joint supplements and their use in equine tion, United States Equestrian Foundation, and Morris Animal joint disease are also new materials included for the first time. Foundation, as well as the National Institute of Health. Finances Chapters 20 through 26 then cover all details on pathogen- limit us answering many important relevant questions and, to esis, diagnosis, and treatment of the various joint entities by support much of this work, we at the ORC owe it to our fantas- region including separate chapters on distal limb, fetlock, car- tic donors who contribute to answering these questions. These pus, elbow and shoulder, tarsus, stifle, and hip. We conclude discretionary dollars have allowed a considerable amount of with a chapter on joint disease; both current research and the research to be translated into clinical reality here. xi SECTION I General Principles of Joint Pathobiology 1 General Anatomy and Physiology of Joints P. René van Weeren The horse has always taken a special position among the spe- privileged place in the big family of animal species with which cies that have been domesticated by humankind. The horse humankind has surrounded itself. was domesticated rather late, around 3500 BC,1 millennia Where the role of the horse in society has changed pro- after such species as goat, sheep, and cattle. Unlike these other foundly in the past century, the underlying reasons of its use species, the main purpose of the horse’s domestication was and popularity have not changed at all. It is still the stamina of not the provision of edible products or products that could be the animal and athletic capacity of its locomotor system that somehow transformed into clothing, such as meat, milk, fur, form the basis for almost all present-day use. The most critical or skin, but for a less tangible commodity: the combination of body systems for athletic performance are the cardiorespira- physical power and athletic capacity. tory system and the musculoskeletal system. Within the lat- Horses have been the major power source for all Eurasian ter system, joints are literally pivotal elements. It may not be and Northern African civilizations since their introduc- surprising that orthopedic malfunctioning or other musculo- tion from roughly 3500 to 500 BC until the invention of the skeletal disorders account for the vast majority of reasons to steam engine that started the Industrial Revolution in the late consult an equine vet.3 Of the specific elements of the muscu- 1700s. The ultimate personification of the role of the horse in loskeletal system, joint disorders invariably rank first or sec- society is perhaps Bucephalus, the legendary horse of Alex- ond in importance (together with tendinopathies, depending ander the Great, who conquered the vastest land empire the on discipline). Most figures come from the racing industry,4,5 world has ever known. Bucephalus served Alexander who, but the relatively scarce data for sport horses also point in the according to legend, was the only person able to mount the same direction.6,7 In a survey of U.S. horse owners in 1998 it stallion, from a young age to its death at the age of 30 after was estimated that 60% of all lameness was related to osteo- the battle of Hydaspes in what is now Pakistan, 2900 miles arthritis (OA) and approximately $145 million was spent on from its native Macedonia. There, Alexander named the veterinary bills relating to the problem.8 In this respect, the city of Bucephala (present-day Jhelum) after him. After the clinical importance of joint disorders in the equine species is Industrial Revolution horses still remained essential for many very comparable to the situation in humans where musculo- sectors of human society until after World War II, when the skeletal disorders in general and articular pathologies in par- combustion engine definitively took over all traditional roles ticular represent an enormous burden to society in terms of of the horse in warfare, transport, and agriculture. Some loss of quality of life and costs of healthcare with 151 million have predicted that the loss of its classic duties would make sufferers of OA worldwide.9 For this and a number of impor- the horse into a zoo species,2 but they were proven entirely tant biologic reasons the horse is increasingly recognized as wrong by the rapidly increasing popularity of the horse as a a suitable, if not the best, model for human joint disease.10 sports and leisure animal from the mid-1960s onwards. Over This translational aspect of equine joint disease will be dealt the millennia, humans and horses appeared to have bonded with in more detail in Chapter 27, which discusses arthritis in a way that goes far beyond economic value or utility and research and future directions in joint disease. is more profound than with any other domesticated species, This first chapter gives a general introduction into the with the exception of the dog. Though admittedly the equine anatomy and physiology of the (equine) joint, as a basis for industry is susceptible to the fluctuations of economic pros- the understanding of the following chapters that address in perity, this fascination for the equine species is not likely to detail specific disorders, diagnostic possibilities, and thera- disappear soon, if ever. This obviously guarantees the horse its peutic interventions. 1 2 SECTION I General Principles of Joint Pathobiology JOINT FUNCTIONS disk and the symphysis of the pubic bones in both humans and horses. In synovial joints there is no structural connec- Whereas the necessary stability of the equine musculoskel- tion between the bony parts of the skeleton, but both ends etal system is provided by the rigid bony components, joints are capped with hyaline cartilage and articulate by gliding permit motion of these bony components in relation to each over each other although contained in a joint capsule that is other and, indirectly, the displacement of the entire indi- filled with synovial fluid, a viscous liquid. A sliding bearing in vidual with respect to the environment, that is, locomotion. mechanical engineering basically functions according to the To accomplish this, joints have to meet several requirements. same principle. They have to be as robust as the bony elements of the mus- In a functional sense, there are several other ways to clas- culoskeletal system, as the forces generated by locomotion sify joints. A common way is according to the degree of and other (athletic) activities are transmitted through joints motion they permit. Although the following nomenclature as they are through bones. They also have to allow for smooth is currently seen as obsolete,15 it is still widely used and will and as frictionless as possible motion of the bony ends that hence be mentioned here. A synarthrosis is a joint permitting articulate with respect to each other. Lastly, they have a role, little mobility. Most of these joints are of fibrous nature, such together with other structures, such as the digital cushion in as the sutures that connect the bony components that make the foot, to mitigate and dampen the accelerations and associ- up the skull. Amphiarthroses are joints that permit more, but ated vibrations that are generated during the impact peak of still very limited, mobility. They are generally of either fibrous the stride cycle at hoof landing. This latter aspect has been or cartilaginous nature, with the intervertebral joints (again relatively well studied in the equine literature.11,12 with the exception of C1-C2) as the best examples. Finally, All the aforementioned requirements that are at least par- diarthrodial joints permit maximal motion. These are always tially contradictory (strength comparable to bone, smooth synovial joints and their motion is limited by periarticular or surfaces for supple gliding, and resilience for shock absorp- intraarticular structures such as capsules or ligaments, but tion) have to be accommodated in a single structure, which not by the nature of the joint. Virtually all joints of the appen- is a challenging task. As will be explained, nature deals with dicular skeleton of the horse are diarthrodial joints. these challenges in an ingenious way, however, at the cost of Other functional classifications are based on the degrees flexibility and repair capacity. For reasons of clarity the com- of freedom a joint has. Any three-dimensional body in space ponents that make up a joint will be dealt with separately, but has six potential degrees of freedom within the global coor- it is important to stress that a joint is more than a collection dinate system: three translations along the x, y, and z axes of of tissues with separate characteristics and functions. There is the coordinate system, and three rotations around these axes. common agreement nowadays that the joint should be seen as In aeronautical terms these rotations are indicated as pitch, a complex multicomposite organ not unlike structures such yaw, and roll. In joints, translations of bony parts with respect as the liver, kidney or heart.13,14 Within this organ the consti- to each other are limited (but may occur, for instance in the tuting elements act together to ensure proper joint function. middle carpal joint), but rotations can be substantial and may There is a strong interplay of all these components in health comprise rotations around more than one axis, as is the case and disease and mutual influencing of physiologic function- in the hip joint. The horse has evolved as a flight-and-fright ing; malfunctioning of the components will also inevitably animal specialized in fast motion, for which reason most of affect the other constituents and hence performance of the the joints of the appendicular skeleton are largely monoaxial, entire joint at a shorter or longer term. permitting excursions that are basically restricted to flexion- extension in the sagittal plane. TYPES OF JOINTS This chapter is limited to the general anatomy and physiol- ogy of diarthrodial joints only, as the other joint types in the Joints can be classified in several ways. A gross division can horse hardly, if ever, give rise to clinical problems. be made between classification according to structural char- acteristics, that is, the type of tissue(s) that form the inter- EMBRYONIC JOINT DEVELOPMENT face between the articulating bony parts of the skeleton, and classification according to function, or the degree and type of The axial and limb skeleton is derived from the embryonic movement joints allow. paraxial and lateral plate mesoderm, which is the precur- The currently used basic classification is three major cat- sor tissue of, among other tissues, the hyaline cartilage that egories, which are fibrous joints with the bone connected by is found in diarthrodial joints. The mesenchymal progenitor dense connective tissue, cartilaginous joints where cartilage is cells, originating from the lateral plate mesoderm, differenti- the interface, and synovial joints in which there is a fluid-filled ate into chondrocytes that form a cartilaginous skeletal anla- cavity.15 In the horse, the articulations between the bodies of gen as precursor for the later bony skeleton and connecting the vertebrae that make up the axial skeleton are fibrous joints, diarthrodial joints.16 Joint formation occurs when cells at the with the exception of the articulation between the first and future joint site start to flatten and form a region that is dis- second cervical vertebrae (C1-C2), which is a synovial joint. tinct from the adjacent cartilaginous areas.17 This zone, once A cartilaginous joint has an interface consisting of hyaline morphologically distinct, is called the interzone. The cells in or fibrous cartilage; examples are the human intervertebral this zone lose their chondrogenic phenotype and cease the CHAPTER 1 General Anatomy and Physiology of Joints 3 expression of collagen type II. The interzone is further char- acterized by the expression of growth/differentiation fac- tor 5 (Gdf5), Wnt9a, double cortin, and versican, whereas Trabecular bone matrilin-1 is not expressed anymore.16,18 The importance of the interzone for joint formation has been demonstrated Joint capsule unequivocally by the experimental removal of the interzone from the elbow joint in chicken embryos, which led to the Synovial Subchondral fusion of the humerus with the radius and the ulna in the membrane bone plate absence of joint formation.19 Articular The moment when interzone development starts dur- Joint cavity cartilage containing ing embryonic development varies per species. Recently, synovial fluid equine embryonic development has been mapped in detail using magnetic resonance imaging.20 When taking the day in which ovulation was first detected as day 0 of pregnancy and hence of embryonic life (E0), it has been shown that at E40 the interzone is fully formed and consists of three dis- FIGURE 1-1 Schematic representation of a diarthrodial joint. tinct layers: the inner interzone (II) that will develop into the (Adapted from: De Grauw J.C. (2010). Molecular monitoring of equine joint homeostasis. Thesis, Utrecht University.) joint cavity, intraarticular structures, and articular cartilage, and two adjacent outer interzones, which are precursors to the epiphyseal growth cartilage and will eventually turn into and temporomandibular joints. These constituting struc- bone.21 Using laser capture microdissection to harvest tis- tures of the joint will be discussed separately in the following sue samples from outer and inner interzones, respectively, it paragraphs. was shown that the mRNA expression patterns of both tissue Articular Cartilage types varied markedly for genes related to chondrogenesis. Further, several genes involved in cell adhesion, transcription The functional characteristics of a construction are largely regulation, and various signaling pathways were expressed determined by the interplay of the material properties of the differentially. The top 25 genes expressed more in the outer building blocks or components that construction is made than in the intermediate interzone were mostly associated of and the way these components are arranged and inter- with endochondral ossification, cartilage, and growth plate connected, that is, the architecture of the construction. For matrix composition. Examples are genes for matrilin-1 and structured tissues, such as articular cartilage or bone, this is 3, BMP5, and Col2al. They also partake in Wnt/b-catenin similar. However, as in all living tissues, the situation is more signaling, bone morphogenetic protein (BMP) signaling, complex as cellular action, driven by a wide variety of cues and sonic hedgehog signaling, which are essential regulatory and effected through various signaling pathways, determines pathways for chondrogenesis and osteogenesis.21 This infor- tissue homeostasis and the response to external stimuli. If mation is important for the further development of regenera- that response can somehow not cope with the demands made tive techniques for articular lesions in which the full recovery by these stimuli, pathology may ensue. of the original structure and function is still a major challenge The major components of the extracellular matrix (ECM) (see also Chapter 27). of articular cartilage are collagen, proteoglycans (PGs), and water. Water content varies from 70% to 80%, depending on PRINCIPLES OF JOINT ANATOMY age. The other components account for approximately 50% (collagen) and 35% (PGs) on a dry weight basis. The remain- Figure 1-1 presents a semischematic and simplified draw- ing 15% consists of about two thirds (10% of total dry weight) ing of a diarthrodial joint. The basic structures common to of glycoproteins (substances such as proteinases and inhibi- all synovial joints are layers of articular cartilage covering tors of these, growth factors, specific molecules such as fibro- the ends of the articulating bones that together constitute the nectin, lubricin, cartilage oligomeric protein [COMP], etc.) joint, subchondral bone beneath this cartilage, synovial fluid Minor fractions are minerals (3%), lipids (1%), and miscella- that surrounds the articulating bone ends, and some struc- neous components (1%).22 The cellular component of articu- ture that restrains the synovial fluid within the joint. This lat- lar cartilage is relatively small and accounts for approximately ter structure will often be a joint capsule, but other structures 1% to 12% volume percentage, depending on the location may serve this purpose as well, as is the case of the proximal within the joint and the depth in relation to the surface.22 interphalangeal joint that has no capsule but in which the Layered Composition of Articular Cartilage synovial fluid is retained by the ligamentous and tendinous structures that surround the joint. Additional structures that Whereas cartilage macroscopically is seemingly a homo- serve principally to stabilize the joint and to restrict motion in geneous tissue, there are large differences in structure and unwanted directions are collateral or other periarticular liga- composition from the surface down to the transition to the ments, intraarticular ligaments, such as the cruciate ligaments subchondral bone. Classically, four layers or zones are dis- in the femorotibial joint, and menisci, as in the femorotibial cerned, although the transitions between these layers are
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