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Arthritis Research & Therapy volume 14, Article number: 212 (2012) Cite this article

Abstract

Osteoarthritis is a prevalent and disabling disease affecting an increasingly large swathe of the world population. While clinical osteoarthritis is a late-stage condition for which disease-modifying opportunities are limited, osteoarthritis typically develops over decades, offering a long window of time to potentially alter its course. The etiology of osteoarthritis is multifactorial, showing strong associations with highly modifiable risk factors of mechanical overload, obesity and joint injury. As such, characterization of pre-osteoarthritic disease states will be critical to support a paradigm shift from palliation of late disease towards prevention, through early diagnosis and early treatment of joint injury and degeneration to reduce osteoarthritis risk. Joint trauma accelerates development of osteoarthritis from a known point in time. Human joint injury cohorts therefore provide a unique opportunity for evaluation of pre-osteoarthritic conditions and potential interventions from the earliest stages of degeneration. This review focuses on recent advances in imaging and biochemical biomarkers suitable for characterization of the pre-osteoarthritic joint as well as implications for development of effective early treatment strategies.

Introduction

Osteoarthritis (OA), a leading cause of morbidity and disability, carries high socioeconomic costs. In 2004 arthritis was estimated to cost the United States $336 billion, or 3% of gross domestic product [1]. OA is by far the most common form of arthritis. With increasing obesity and age in the population, a massive rise in morbidity and costs attributed to OA is expected. While joint replacement is effective for treating end-stage OA in older people, evaluation of potential disease-modifying treatments in populations meeting current clinical criteria for OA has had limited success. Early diagnosis and early treatment strategies in rheumatoid arthritis have reduced patient morbidity and associated costs in the past decade. New concepts for early diagnosis and treatment of pre-osteoarthritic conditions may similarly improve outcomes and reduce disability and costs for OA, the most prevalent form of arthritis.

Pre-osteoarthritis is a modifiable disease process

Epidemiological and genetic studies of OA indicate that many pre-OA disease states can be modified. While OA can affect any joint, substantial disability is attributed to OA of the weight-bearing joints, primarily the hip and knee. OA is a multifactorial decades-long process reflecting a complex interplay between intrinsic and extrinsic factors. While there is evidence for heritability of OA [2, 3], the polygenic nature of the disease with multiple genes contributing small effects has made it difficult to identify the genetic etiologies of OA [4]. Genome-wide association studies have yielded few common genetic targets [5]. Whereas OA is the culmination of multivariate interactions between genetic, epigenetic, and environmental factors, extrinsic factors such as obesity, trauma, and joint loading patterns are known to heighten OA risk and to offer more definable targets for disease modification. The systematic study of large cohorts at increased risk for accelerated OA development therefore has potential not only to yield new disease-modifying treatments but to facilitate improved understanding of the complex interactions between genes and the environment in OA development [6].

Extrinsic events such as joint trauma accelerate osteoarthritis development

Post-traumatic OA illustrates the concept that modifiable extrinsic factors play a substantial role in OA development. Joint trauma such as intra-articular fracture, dislocations, anterior cruciate ligament tear (ACLT), and other injuries lead to rapid joint degeneration in a high proportion of patients [7, 8]. Articular surface incongruity, joint instability, altered kinematics, articular cartilage injury, and other joint-tissue changes attributable to the traumatic event accelerate OA development. In a long-term prospective cohort study, young adults with knee injuries showed substantially increased risk for later development of osteoarthritis of the index knee [8]. Another study showed that roughly one-half of individuals with ACLTs or meniscus tears developed radiographic signs of OA 10 to 20 years after injury [9]. Since ACLT is most frequently sustained by teenagers and young adults, it can be considered the cause of premature knee OA in these patients - a devastating outcome with costly social and economic consequences.

Joint injury cohorts enable characterization of preosteoarthritic processes from the earliest stages

For the study of pre-OA conditions, joint injury cohorts offer the potential to study, characterize, and modify the disease process from its earliest stages. A recent American Orthopaedic Society for Sports Medicine/National Institutes of Health U-13 multidisciplinary conference focused on post-joint injury OA described advantages for studying meniscus-injured and anterior cruciate ligament (ACL)-injured cohorts [6]. These cohorts represent populations that do not meet the classic radiographic or clinical criteria for OA [10]. Rather, subjects have joint pathologies placing them at risk for accelerated OA development. These populations offer opportunities to define and treat pre-OA conditions. The acute ACL and meniscal injury populations are well suited for bench-to-bedside translational studies of new treatment strategies because they are more similar to popular animal models of pre-clinical OA such as ACL transection and meniscus injury than the more heterogeneous older human cohorts with established multi-site OA traditionally used to evaluate potential disease-modifying treatments [6].

Defining and characterizing pre-OA in its earliest stages is crucial not only for understanding the disease process, but also for identifying potential disease-modifying treatments and evaluating their effectiveness. Early diagnosis will permit earlier treatment to modify the course of this disease. This review will focus on recent advances in imaging and biochemical biomarkers suitable for characterization of the pre-osteoarthritic joint.

Imaging of the pre-osteoarthritic joint

Radiographs have been used for more than a century to assist diagnosis of bone and joint disorders. The radiographic hallmarks of structural changes in classic OA include osteophyte formation, joint-space narrowing, subchondral bone thickening, and cyst formation. Clinical criteria of pain, stiffness, and age are poorly correlated to radiographic findings. Radiographic joint-space narrowing, an indirect and highly insensitive measure of articular cartilage integrity, is the current standard by which clinical efficacy of disease-modifying therapies for OA are measured [11]. Injuries to menisci, articular cartilage, and other joint structures readily apparent at arthroscopy or arthrotomy, as well as stress fractures and even early avascular necrosis, are not detectable by standard radiographic examination. Efforts to develop and assess disease-modifying treatments for OA have been hampered by the insensitivity of these traditional clinical and radiographic measures to joint-tissue health prior to the development of end-stage disease.

Advances in optical imaging and magnetic resonance imaging (MRI) have permitted direct imaging of joint tissues. Arthroscopy permits direct visualization and palpation of intra-articular structures. The sensitivity of MRI for soft tissue assessments and bone marrow changes exceeds that of conventional radiographs. While MRI lacks the tactile and dynamic examination capabilities of arthroscopy, it permits noninvasive and quantitative assessments of joint-tissue structure. As such, MRI offers many advantages for diagnosis and staging of pre-OA joints. While assessment of thin and geometrically complex tissues such as articular cartilage remains challenging for MRI due to low resolution, newer techniques of quantitative, volumetric, and physiologic MRI show promise. Optical coherence tomography (OCT), a new high-resolution imaging technology permitting microscopic cross-sectional imaging of soft tissues in near real time, has been used arthroscopically as a translational research tool to assist in evaluating quantitative MRI of articular cartilage [12]. Finally, measuring joint synovitis reflects increasing recognition of an inflammatory component in pre-OA conditions and in OA pathogenesis.

Arthroscopy and arthroscopic optical coherence tomography

Although the first known report of knee arthroscopy was presented in 1912 [13], only after key advances in fiberoptic and video technologies occurred in the 1970s and 1980s did arthroscopy became widely used for direct visualization, examination, and treatment of intra-articular soft tissues. Radiographically invisible pathologies such as meniscal tears, articular cartilage lesions, and cruciate ligament tears can be readily seen and palpated by arthroscopy. While subjective, the surgeon''s 11 participants [70]. In another study, higher concentrations of IL-6, IFNγ, MIP-1β, and MCP-1 were measured in the synovial fluid of ACL-injured patients versus uninjured controls [71]. Synovial biomarkers from meniscus-injured populations, including both acute and chronic injury, had higher levels of cytokines IFNγ, IL-6, MCP-1, MIP-1β, IL-2, IL-4, IL-10, and IL-13 compared with asymptomatic populations with IL-6, MCP-1, MIP-1β, and IFNγ concentrations correlating with patient-reported pain outcome scores [72].

These studies demonstrate that inflammatory mediators transiently increase following acute ACL injury, with levels decreasing over time. The data from meniscus-injured subjects suggest persistence or resurgence of inflammation, especially in those with pain. These data support the need for continued longitudinal assessment of inflammatory mediators in joint-injured cohorts as potential biomarkers for diagnosis and staging of pre-osteoarthritic conditions.

Collagen and bone metabolites

Byproducts of articular cartilage and bone metabolism were some of the first biomarkers assessed [73]. Early studies focused on biochemical biomarkers in populations with radiographic OA, typically in patients with Kellgren-Lawrence score 2 or higher. Recent studies of the synovial fluid in subjects with ACLT show that elevations of C-terminal cross-linked telopeptide type I and type II collagen, N-terminal telopeptides of type I collagen, and C1,2C - all biomarkers of collagen turnover - peak several weeks after injury [70]. There was also an increase in biomarkers associated with bone resorption. In the same study, strong correlations were found between serum and synovial fluid concentrations of bone metabolism biomarkers [70]. This study has refined the potential utility of biochemical biomarkers of cartilage and bone metabolism in early OA; however, further studies are needed.

Arthritis Curehow to Arthritis Cure for Glycosaminoglycans and hyaluronic acid

Proteoglycans are important articular cartilage matrix components considered sensitive to changes in cartilage homeostasis [74, 75]. Glycosaminoglycan and aggrecan ARGS fragments have been found to be transiently elevated in the synovial fluid of ACL-injured patients [76, 77]. Aggrecan fragment ARGS-SELE remains elevated for at least 2 years after injury [76]. Serum is easier to obtain than synovial fluid and is of particular interest in biomarker analysis for screening purposes and for longitudinal studies. In a recent study, the concentration of W6F (a chondroitin sulfate epitope) was higher in the serum of ACL-injured subjects compared with uninjured controls [78]. Appropriate analysis of serum biomarkers probably cannot be performed in isolation because the detected concentrations represent processes within the entire body, while synovial fluid is more reflective of metabolism within the affected joints. These studies show promise in the use of biochemical biomarkers, particularly synovial fluid analysis, to characterize joint changes following ACL and meniscus injury. Analyses of serum, urine, and synovial fluid from these cohorts in conjunction with advanced structural imaging have the potential to yield candidate biomarkers that can be used for characterization of other pre-OA states.

Conclusion

OA is a prevalent, disabling disease that currently lacks disease-modifying treatments. Clinical OA typically develops over decades and is strongly associated with modifiable factors such as joint injury, obesity, and mechanical overload. The ability to detect pre-osteoarthritic changes prior to the onset of irreversible changes is crucial for understanding the disease process, identifying potential disease-modifying treatments, and evaluating the effectiveness of new therapies. Comprehensive longitudinal studies of joint-injured cohorts allow for characterization of the earliest stages of joint degeneration, thereby maximizing opportunities for development and validation of biochemical and imaging biomarkers and for early intervention. The validation of tools suitable for diagnosis and staging of joint injury and early degeneration is needed to support a paradigm shift towards early treatment of pre-osteoarthritic conditions as a strategy to prevent or delay the onset of classic OA.

Note

This article is part of the series on Cutting edge research and advances in orthopaedic research, edited by Edward Schwarz and Jay Lieberman. Other articles in this series can be found at http://arthritis-research.com/series/orthopaedics

Abbreviations

ACL:

anterior cruciate ligament

ACLT:

anterior cruciate ligament tear

BML:

Arthritis Curehow to Arthritis Cure for bone marrow lesions

dGEMRIC:

delayed gadolinium-enhanced magnetic resonance for 1 last update 2020/05/25 imaging of cartilagedelayed gadolinium-enhanced magnetic resonance imaging of cartilage

IFN:

Arthritis Curehow to Arthritis Cure for interferon

IL:

interleukin

MCP-1:

monocyte chemotactic protein-1

MIP-1β:

macrophage inflammatory protein-1 beta

MRI:

magnetic resonance imaging

OA:

osteoarthritis

OCT:

optical coherence tomography

qMRI:

quantitative magnetic resonance imaging

UTE-T2*:

ultrashort echo-time the 1 last update 2020/05/25 enhanced T2*.ultrashort echo-time enhanced T2*.

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Scholar""http://scholar.google.com/scholar_lookup?&title=Chondroitin%20sulfate%20epitope%20%28WF6%29%20and%20hyaluronic%20acid%20as%20serum%20markers%20of%20cartilage%20degeneration%20in%20patients%20following%20anterior%20cruciate%20ligament%20injury&journal=J%20Sci%20Med%20Sport&doi=10.1016%2Fj.jsams.2008.02.003&volume=12&pages=445-448&publication_year=2009&author=Pruksakorn%2CD&author=Rojanasthien%2CS&author=Pothacharoen%2CP&author=Luevitoonvechkij%2CS&author=Wongtreratanachai%2CP&author=Ong-Chai%2CS&author=Kongtawelert%2CP""c-article-references__download u-hide-print""click""download citation references""article body""link""/articles/10.1186/ar3845-references.ris""16""16""u-icon""http://www.w3.org/1999/xlink""#global-icon-download""Ack1""c-article-section""Ack1-section""c-article-section__title u-h2 js-section-title 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01.5-.5H1v-.5a.5.5 0 01.5-.5H3V9a1 1 0 112 0v6h8V9a1 1 0 011-1zM6 8l2 1v4l-2 1zm6 0v6l-2-1V9zM9.573.401l7.036 4.925A.92.92 0 0116.081 7H1.92a.92.92 0 01-.528-1.674L8.427.401a1 1 0 011.146 0zM9 2.441L5.345 5h7.31z""evenodd""global-icon-search""0 0 14 14""M13.545 12.648a.641.641 0 01.006.903.646.646 0 01-.903-.006l-2.664-2.663a6.125 6.125 0 11.897-.898l2.664 2.664zm-7.42-1.273a5.25 5.25 0 100-10.5 5.25 5.25 0 000 10.5z"> Evangelou E, Chapman K, Meulenbelt I, Karassa FB, Loughlin J, Carr A, Doherty M, Doherty S, Gomez-Reino JJ, Gonzalez A, Halldorsson BV, Hauksson VB, Hofman A, Hart DJ, Ikegawa S, Ingvarsson T, Jiang Q, Jonsdottir I, Jonsson H, Kerkhof HJM, Kloppenburg M, Lane NE, Li J, Lories RJ, van Meurs JBJ, Na""c-article-references__links u-hide-print""click""outbound reference""article body""link""http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4412885""View reference 5 on PubMed Central""nofollow""click""outbound reference""article 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