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Bone Biology

Defining the extracellular matrix in non-cartilage soft-tissues in osteoarthritis: a systematic review

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Abstract

Aims

Extracellular matrix (ECM) is a critical determinant of tissue mechanobiology, yet remains poorly characterized in joint tissues beyond cartilage in osteoarthritis (OA). This review aimed to define the composition and architecture of non-cartilage soft joint tissue structural ECM in human OA, and to compare the changes observed in humans with those seen in animal models of the disease.

Methods

A systematic search strategy, devised using relevant matrix, tissue, and disease nomenclature, was run through the MEDLINE, Embase, and Scopus databases. Demographic, clinical, and biological data were extracted from eligible studies. Bias analysis was performed.

Results

A total of 161 studies were included, which covered capsule, ligaments, meniscus, skeletal muscle, synovium, and tendon in both humans and animals, and fat pad and intervertebral disc in humans only. These studies covered a wide variety of ECM features, including individual ECM components (i.e. collagens, proteoglycans, and glycoproteins), ECM architecture (i.e. collagen fibre organization and diameter), and viscoelastic properties (i.e. elastic and compressive modulus). Some ECM changes, notably calcification and the loss of collagen fibre organization, have been extensively studied across osteoarthritic tissues. However, most ECM features were only studied by one or a few papers in each tissue. When comparisons were possible, the results from animal experiments largely concurred with those from human studies, although some findings were contradictory.

Conclusion

Changes in ECM composition and architecture occur throughout non-cartilage soft tissues in the osteoarthritic joint, but most of these remain poorly defined due to the low number of studies and lack of healthy comparator groups.

Cite this article: Bone Joint Res 2024;13(12):703–715.

Article focus

  • Extracellular matrix (ECM) is a critical determinant of tissue mechanobiology and cell behaviour, but it is poorly described in osteoarthritic joint tissues beyond cartilage.

  • The main aim of this systematic review is to consolidate existing data describing the architecture and composition of structural ECM in the synovium, joint capsule, skeletal muscle, tendon, ligament, meniscus, intervertebral disc, and fat pad of osteoarthritic joints.

Key messages

  • Our study highlights the global nature of ECM dysregulation across the osteoarthritic joint.

  • While some ECM changes, notably calcification and the loss of collagen fibre organization, have been extensively studied across osteoarthritic tissues, most ECM features were only studied by one or a few papers in each tissue.

  • Results from animal studies generally concurred with human studies, but some findings contradicted observations from human studies, highlighting the importance of the choice of animal model and the need for validation from human studies.

Strengths and limitations

  • This systematic review consolidates existing knowledge of a poorly defined aspect of osteoarthritis pathophysiology.

  • While a wide range of tissues and ECM components have been reported on, the qualitative nature of papers, the lack of control groups, and the paucity of reports on each ECM component means that the depth of knowledge remains poor.

Introduction

Osteoarthritis (OA) is the most common joint disease globally, affecting over 500 million people. OA is typically attributed to mechanically driven joint damage and is characterized by articular cartilage degeneration and subchondral bone remodelling.1 However, these tissues are not affected in isolation from the wider joint, with pathology in other soft joint tissues contributing to the symptoms and progression of OA.2,3 Damage to menisci and ligaments disrupts joint biomechanics, while inflammation, fibrosis, and distension of the synovium and joint capsule are associated with joint pain and stiffness.4-8 Despite significant clinical need and substantial efforts to identify disease-modifying OA drugs, there is no effective way of inhibiting or decelerating OA-related joint damage by targeting cartilage directly. Given the important role of other soft-tissues in joint biomechanics and the release of pro-inflammatory and matrix-degrading mediators into the synovial fluid,9,10 understanding the biological landscape of the whole joint in OA might provide novel therapeutic strategies and prognostic markers.

Joint tissues are rich in extracellular matrix (ECM), a network of structural and regulatory macromolecules within which cells are embedded.11 The role of ECM as a major determinant of the biophysical properties of a tissue has clear relevance in a disease such as OA.12,13 ECM not only provides structure to the tissue, but can also affect cell function through receptor engagement, mechanical cues, and the sequestration of growth factors and cytokines.14-17 Significant crosstalk occurs between cells and matrix components, such that pathological ECM may exacerbate cellular dysfunction in disease.16,18 Therefore, ECM composition and architecture cannot be disregarded when attempting to understand OA pathophysiology. However, outside of cartilage, ECM remodelling in OA tissues has received relatively little attention.

Studying OA in the clinical setting is challenging due to the slow and unpredictable nature of the course of the disease. In addition, clinical symptoms often appear late in the disease process, making it difficult to study its onset and early progression. Therefore, many animal models for OA have been developed to overcome these issues and facilitate the development and evaluation of new therapies and diagnostic tools.19 However, since there is no single “gold standard” animal model that accurately reflects all aspects of human disease, a major challenge is selecting the “right” model for each study.20

The main aim of this systematic review is to consolidate existing data describing the architecture and composition of structural ECM in the synovium, joint capsule, skeletal muscle, tendon, ligament, meniscus, intervertebral disc, and fat pad of osteoarthritic joints. The second aim is to define the changes in the architecture and composition of structural ECM in these tissues in animal models of OA, in order to address their ability to replicate human disease pathophysiology.

Methods

Systematic review protocol and registration number

This review was conducted according to a protocol registered on the PROSPERO database (CRD42021231241) and guidelines set out in the PRISMA statement.21

Database and search strategy

The search strategy, written by JYM and a medical librarian, can be found in the Supplementary Material. ECM components and architectural features were defined using National Centre for Biotechnology Information Medical Subject Heading terms.22 Non-cartilage soft joint tissues and disease nomenclature were also specified. The search strategy was validated against relevant papers identified in a preliminary literature search. The search strategy was run on the Ovid MEDLINE, Ovid EMBASE, and Scopus platforms on 30 October 2020 and repeated on 1 October 2021 and 1 June 2023.

Eligibility criteria and screening

Abstracts were de-duplicated in Mendeley Reference Manager (Elsevier B.V., Netherlands) before being imported into the Covidence platform. The remaining studies were screened independently at title/abstract and full-text stages by two reviewers (JYM, IGAR), with conflicts resolves through consensus or a third reviewer (SJBS). Included studies were required to have ≥ three OA participants.

In human studies, eligible patients and controls were aged ≥ 18 years. Non-OA diseases, including inflammatory arthritides and crystalline arthropathies, were excluded. The presence of a valid control group was not a requirement for human studies. However, control groups were included if present and a minimum of three participants were included in this group. Valid control groups included tissues from healthy people or near-healthy tissues, including cadavers, individuals with osteosarcoma, and traumatic joint injuries provided that the comparator tissue was not directly damaged by the trauma.

In contrast to human studies, all animal studies required a control group. Studies that induced OA unilaterally and only used a contralateral control joint were excluded, as non-physiological loading of the contralateral joint induces ECM remodelling.23,24 Excluded animal models included the genetic deletion of ECM components, the introduction of matrix-degrading enzymes into the joint, surgical damage of a tissue subsequently reported on, and the ovariectomized rat model, as this is more commonly used as a model for osteoporosis.25,26

Regarding outcome measures, included studies evaluated at least one of the following tissues: intervertebral disc, ligament, skeletal muscle, tendon, meniscus, articular capsule, synovium, and fat pad. Papers that only studied these tissues after treatment, including – but not limited to – surgical or drug treatment, or after these tissues were purposely injured to induce the development of OA, were excluded. Papers evaluating non-ECM tissue components (cells, cytokines, matrix-degrading enzymes) were ineligible for inclusion. Given the focus on structural ECM, regulatory matricellular proteins, as well as neoepitopes generated during ECM turnover, were not included. Studies using in vitro or ex vivo culture systems were excluded as the ECM proteins that cells synthesize differ in culture and in vivo. Transcriptomic analyses were excluded as gene expression is a determinant, not a measure, of protein abundance. Finally, only English-language articles were included.

Data extraction and bias analysis

Data were extracted from all included studies by one reviewer (JYM or IGAR) using a standardized extraction form in Microsoft Excel (Microsoft, USA); the extraction was verified by the other reviewer (IGAR or JYM). Where there was uncertainty, extraction was performed in duplicate by both reviewers. Number of participants (or animals) in each group was recorded as well as the presence/absence of a control group; if a control group was present, the control population and control tissue were described. For animal studies, the species, strain, and type of OA model were recorded. When available, participant age, sex, BMI, and disease severity were recorded, as were the joint and tissue being studied. Relevant ECM components and architectural features were described; comparisons to control tissues and statistical analysis were noted when applicable. Results were grouped by tissue, followed by ECM feature, and finally the direction of change compared to control (increase, no change, decrease, or no control group present) and presented in Supplementary Table i (human studies) and Supplementary Table ii (animal studies). Due to the large number of different included ECM features, accepted research methods, and accepted measures of effect, a quantitative meta-analysis was not deemed appropriate. Bias analysis was performed by IGAR, with all included studies assessed using the 2015 Office of Health Assessment and Translation (OHAT) Risk of Bias Rating Tool for Human and Animal Studies. The results of the bias analysis can be found in Supplementary Table iii.

Results

Study overview

A total of 22,140 potentially relevant articles were identified by the search strategy (Figure 1). Following the removal of duplicates, 10,204 abstracts were screened. Of the 456 studies assessed for eligibility at full-text screening, 161 met all criteria for inclusion in this review. The characteristics of all included studies are summarized in Supplementary Tables iv and v (human and animal studies, respectively). A schematic overview of the included studies can be found in Figure 2.

Fig. 1 PRISMA 2022 flow diagram. ECM, extracellular matrix; OA, osteoarthritis.

Fig. 1

PRISMA 2022 flow diagram. ECM, extracellular matrix; OA, osteoarthritis.
Fig. 2 Schematic overview of the study population, anatomical locations, and extracellular matrix (ECM) features studied in the included studies. One study investigated ECM in both human osteoarthritis (OA) and an animal model of OA. Created with BioRender.com. TMJ, temporomandibular joint.

Fig. 2

Schematic overview of the study population, anatomical locations, and extracellular matrix (ECM) features studied in the included studies. One study investigated ECM in both human osteoarthritis (OA) and an animal model of OA. Created with BioRender.com. TMJ, temporomandibular joint.

Human studies

Most studies investigated meniscus (n = 46) and synovium (n = 42), followed by ligaments (n = 18), capsule (n = 7), tendon (n = 5), skeletal muscle (n = 4), fat pad (n = 2), and intervertebral disc (n = 1) (Supplementary Table i). Studies most commonly investigated the knee joint (n = 86), but papers on hip (n = 10), spine (n = 3), thumb (n = 2), temporomandibular joint (TMJ) (n = 2), and shoulder (n = 2) were also identified. While most studies on synovium, tendon, and capsule focused on the presence/absence and distribution of specific ECM components, a large proportion of the papers on meniscus and ligaments investigated ECM architecture and viscoelastic properties (Supplementary Table i).

Capsule in human OA

Of seven studies which assessed the capsule (hip (n = 3), knee (n = 3), and spine (n = 1)),27-33 four were published before the year 2000. These studies covered both ECM components and architectural features, but only collagen content was covered by more than one study, with two papers describing increased collagen staining.28,29 Voelker et al30 looked at several ECM components, showing an increase in type I collagen and no difference in type III collagen and elastin in OA facet joint capsule compared to cadaver controls.30 Of note, DiFrancesco et al27 studied several ECM features (calcification, collagen fibre organization, elastic fibres, and GAG/proteoglycan content) in parallel,27 providing an overview of hip capsule in OA. Other studies showed decreased collagen fibre organization,32 the presence of several GAGs,33 and an increase in collagen cross-links in OA.31

Fat pad in human OA

Two studies were identified for infrapatellar fat pad.34,35 Grevenstein et al35 found no change in cartilage oligomeric matrix protein (COMP) content between OA and control fat pads,35 while Belluzzi et al34 showed that the osteoarthritic fat pad contains less collagen type I and III than controls.

Intervertebral disc in human OA

One study was identified for intervertebral disc. Cheng et al36 showed an increase in calcification with increasing OA grade in intervertebral discs.

Ligaments in human OA

Of the 18 studies on ligaments, 14 focused on anterior cruciate ligament (ACL) and/or posterior cruciate ligament (PCL) of the knee.37-50 Two studies looked at ligaments in the thumb (palmar beak ligament,51 volar anterior oblique (AOL), and dorsoradial (DRL)52), while two other studies investigated ligaments in the spine (transverse ligament53 and the ligamentum flavum).30 Studies mostly focused on collagen fibre organization, which generally decreased in OA compared to control.42-44 Studies without controls also reported disorganized and irregular collagen fibre organization in OA ligaments. Other identified studies confirmed the presence of collagens I, II, and III, but found no change in overall collagen content compared to control. In contrast, calcification and proteoglycan content appear to increase in OA.

Meniscus in human OA

Studies on human meniscus (n = 46) covered a wide range of ECM components, architectural changes, and viscoelastic properties.54-99 Most studies concur on an increase in calcification and proteoglycan content, and consistently show a decrease in collagen fibre diameter and organization. The presence or change in many other ECM components has been studied, including aggrecan, biglycan, cartilage intermediate layer protein, collagens and collagen cross-links, COMP, decorin, fibromodulin, glycosaminoglycan (GAG) components, hydroxyproline, keratocan, lubricin, and lumican. Notably, three out of four proteomics studies included in this systematic review evaluated human OA meniscus, identifying a range of ECM and ECM-associated proteins.97-99 Two of these studies (Folkesson et al97 and Roller et al98) also analyzed control samples and found several proteins to be changed in OA compared to control tissue. For example, both studies report an increase in type VI α 1 collagen and type VI α 2 collagen in OA, and Folkesson et al97 found a change in protein abundance in several small leucin-rich proteoglycans, such as an increase in lumican and decrease in decorin, an increase in the proteoglycans aggrecan and versican, and a decrease in type III and V collagens.97,98 Finally, the results on viscoelastic properties are conflicting: while some studies show an increase in elastic modulus89 and instantaneous modulus,90 another study showed a decrease in these parameters.61

Skeletal muscle in human OA

All four studies on human skeletal muscle studied the ECM components in the vastus medialis or vastus lateralis of the quadriceps muscle.100-103 These studies demonstrated the presence103 or increase102 in type I, III, and IV collagens compared to control. In addition, these studies show the presence of calcification and laminin,100,102 and an increase in collagen and GAG content.101

Synovium in human OA

Synovial tissue was studied in several joints, including the knee (n = 18),94,104-120 hip (n = 5),121-125 both knee and hip (n = 6),126-131 TMJ (n = 2),132,133 or an unspecified joint (n = 12).130,134-144 The ECM components most often studied in human synovium were collagens, fibronectins, and laminins. Other ECM features covered by the included studies are aggrecan, calcification, collagen content, collagen fibre organization, collagen cross-links, COMP, elastin, fibromodulin, GAG components, latent transforming growth factor (TGF)-β-binding protein 1, lumican, reticulin, and vitronectin. While the presence and tissue distribution of these components has been clearly shown by several studies, the changes between OA and normal tissue remain unclear, with most studies lacking healthy control groups; instead, OA is often the comparator group in studies investigating rheumatoid arthritis (RA). This includes the identified proteomics study, which compared the OA and RA synovium. They found that several ECM proteins, including type 2 α 1 collagen, versican, and cartilage intermediate layer protein 1 were higher in OA than RA synovium.143

Tendon in human OA

Human tendon studies covered a range of different tendons across the body, including Achilles, (long head of) biceps, subscapularis, gluteus medius, and internal obturator.145-149 Discordant results between studies of anatomically distinct tendons are unsurprising, but disagreement was also seen for two studies on biceps tendon. For example, GAG/proteoglycan content was increased in the long head of biceps and internal obturator tendon,145,148 unchanged in another study on biceps tendon and subscapularis tendon,146 and decreased in gluteus medius tendon in OA compared to control.149 Similarly, increased calcification was seen in obturator tendon,145 while there was no difference in subscapularis, and a decrease in biceps tendon.146 In terms of architecture, three out of four studies reporting on collagen fibre organization report a decrease in organization,145,146,149 while the last reported no difference compared to control.148 An increase in collagen fibre diameter was found in internal obturator and biceps tendon,145,146 while no difference was seen in subscapularis and gluteus medius tendons.146,149 Finally, no difference was found in the percentage area stained for type I and II collagen and decorin.148

Animal studies

Animal studies followed a similar pattern as human studies regarding the most studied tissues: synovium (n = 18), meniscus (n = 14), ligament (n = 7), skeletal muscle (n = 2), tendon (n = 1), and capsule (n = 1) (Supplementary Table ii). A broad range of species, strains, and models were used, all looking at the stifle joint of these animals. Overall, these studies generally found increases in ECM components such as collagen and disrupted ECM architecture, including a decrease in collagen fibre organization in most tissues (Supplementary Table ii). Viscoelastic properties were mainly studied in meniscus, where the elastic and instantaneous modulus tended to decrease.

Capsule in animal models of OA

Only one study was identified on capsule. Loeser et al150 studied capsule in the DMM model in C57BL/6 mice.150 Type III collagen was found to be diffusely expressed in OA capsule, predominantly in vascular endothelium. Interestingly, this study also assessed the meniscus, ligament, and synovium, taking a whole-joint approach to OA; they report a diffuse distribution of type III collagen similar to capsule in ligaments and synovium, while there was a pericellular distribution in meniscus.

Ligament in animal models of OA

Ligaments were studied in OA models in mice (n = 4),150-153 rabbits (n = 2),154,155 and sheep (n = 2).156,157 A decrease in collagen fibre organization was reported by two studies.155,157 While one study reported an increase in GAG staining using toluidine blue in ACL of STR/ort mice,151 another showed a decrease in Raman spectroscopy peaks related to GAG content in MCL/LCL of ACL transection (ACLT) rabbits.154 All other reported ECM features were only present in one study. These features include calcification, mineralization, collagen content, types II and III collagen, collagen cross-links, collagen fibre diameter, and mechanical strength.

Meniscus in animal models of OA

ECM changes in meniscus in animal models of OA were investigated by six studies using mouse models,150,151,158-161 five studies using rabbit models,162-166 one study using a rat model,167 and two studies using a pig model.168,169 Overall, these studies show an increase in calcification/mineralization and types I, II, III, and X collagen, and a decrease in collagen fibre organization. Most studies show a decrease in GAG/proteoglycan content and viscoelastic properties in at least parts of the meniscus. In addition, thickening of the collagen fibres and no change in fibromodulin were found.

Skeletal muscle in animal models of OA

Two studies were identified that investigated skeletal muscle. Shi et al170 studied the elastic modulus in biceps femoris and rectus femoris muscles in an adapted Videman method in rabbits; they report an increase in elastic modulus in OA compared to control.170 Lee et al171 investigated the rectus femoris muscle using a monoiodoacetate (MIA) model in rats; they reported a decrease in collagen levels on days 56 and 87 in OA rats compared to the naïve group.171

Synovium in animal models of OA

Synovium was investigated in three studies using mouse models,150,158,172 13 studies using rat models,104,173-184 and two studies using rabbit models.185,186 All studies on calcification, collagen content, and collagen I showed an increase in OA compared to control. However, results on collagen fibre organization and collagen fibre diameter were less clear, with some studies reporting no change, while others reported a decrease in collagen fibre organization and increase in collagen fibre diameter. Other studied features included types III, V, and XIV collagen, COMP, fibromodulin, lubricin, and viscoelastic properties (elastic modulus), which were each reported on by a single study.

Tendon in animal models of OA

Tendon was investigated in one study by McErlain et al187 using an ACLT model in rats. They found calcification of the patellar tendon to be more common in OA than control animals.187

Bias analysis

The risk of bias varied between studies but was generally high (Supplementary Table iii). The potential for confounding bias was common, with many human studies failing to report on the age, sex, and BMI of participants. Frequently, OA diagnoses were stated without reference to the diagnostic criteria used. Most studies failed to report on the blinding of assessors, even when qualitative histological observations were made. Purely qualitative observations were common, although semiquantitative scoring systems were increasingly used in more recent studies. However, many quantitative and semiquantitative differences between healthy and osteoarthritic tissues were not statistically analyzed.

Discussion

Despite OA becoming more widely accepted as a whole joint disease, the role of and the changes to non-cartilage soft joint tissues remain underexplored. This study aimed to collate current knowledge on the structural ECM of these tissues to summarize and highlight gaps in existing knowledge. For instance, tissues such as the joint capsule and fat pad are very poorly defined, perhaps reflecting their perceived importance in OA. Overall, the studies included in this review show that the presence and/or abundance of many structural ECM components changes in disease, within an ECM that becomes less organized with increasing cartilage damage or increasing tissue-specific degeneration scores.

Human studies covered a range of tissues and ECM features, but focused mainly on calcification, the presence and abundance of proteoglycans, and the presence, abundance, fibre diameter, and fibre organization of collagens. While recent studies begin to define the presence and distribution of many ECM components, a frequent absence of well-defined control groups limits our understanding of the changes in disease. Most ECM features are only described by one or a few studies, highlighting the need for studies that cover multiple ECM features. While studies that did look at the same ECM feature mostly agreed, this was not always the case. This included studies with control groups that investigated the collagen content in meniscus,54,72 elastic modulus in meniscus,61,89 chondroitin sulphate in synovium,119,130 and calcification and GAG/proteoglycan content in tendon,145,146,148,149 which all contradict each other in terms of the direction of change. The summary and results tables highlight several potential factors for these differences already, including differences in analysis methods, tissue joint origin, and microanatomical area of studied tissue, emphasizing the importance of in-depth reporting of tissue metadata and methods.

Several recent human studies, mostly in ligaments, tendon, and meniscus, have begun to interrogate both compositional and architectural ECM features within a single tissue. Importantly, such studies can begin to dissect the relationship, including causality, between changes in ECM composition, ECM architecture, and viscoelastic properties. For example, studies in the field have shown that calcification of tendon changes its viscoelastic properties,188 while the mechanical properties of fibril-forming collagens are dependent on covalent cross-linking,189 and different matrix proteoglycans differ in their effects on cell-mediated collagen reorganization.190

Whole tissue proteomics, which can be used to study the ECM composition of a tissue holistically, was performed in four studies: three on meniscus97-99 and one on synovium.143 While the study of ECM proteins using proteomic techniques is subject to methodological biases due to their large size, extensive post-translational modification, and insolubility,191 they are a powerful tool to better understand relative abundance of ECM proteins and overall tissue composition and formulate new research questions. The application of this technique to other osteoarthritic tissues is likely to provide important insights.

In animal models, OA is induced in a range of species using varied surgical techniques and pharmacological interventions, with no animal model truly replicating human disease.19,192 Joint mechanics, inflammatory responses, and disease chronicity all vary between animal models.192,193 If ECM remodelling also differs between species and procedures, it can be assumed that not all animal models are equally suited to the study of changes in osteoarthritic ECM. Certain models may be generally more representative of changes seen in human OA, or better suited to the study of particular joint tissues or ECM features. This review covers a range of ECM changes in several different musculoskeletal soft-tissues across different species and models. Although limited animal studies were eligible for inclusion in this review, some changes in ECM features could be compared between human OA and animal models. Generally similar trends could be seen as in humans, including a decrease in collagen fibre organization and an increase in calcification across ligaments, meniscus, and synovium. However, other observations seem to contradict those in humans; for example, the presence and abundance of collagens seemed to decrease in human osteoarthritic menisci, especially with increasing degeneration of the meniscus,54,73,75 while this is not reflected in data from any of the animal models in this review, which mainly showed increases in collagens in OA menisci.151,161,163 Therefore, the models used by these studies, namely the mouse STR/ort, rabbit ACLT, and mouse DMM models, respectively, might not be suitable to infer OA-related changes in human menisci. These results emphasize that more studies on ECM changes in non-cartilage soft joint tissues in human OA and animal models must be compared before the validity of the latter can be accurately defined.

Another important point to note is the difference in the ratio of female/male subjects in human studies compared to this ratio in animal studies: while most human studies include a higher ratio of female than male subjects, many animal studies are done exclusively using male animals. The predominance of women in human studies likely reflects disease prevalence; sex-specific differences in pain, inflammation, cartilage volume, and physical difficulty exist in OA,194 as well as in the presence of risk factors for the incidence of radiological knee OA.195 The presence of a sex bias in preclinical research is well established, with many fields having a strong male bias during animal studies.196 Encouragingly, sex-specific differences in animal models of OA are increasingly being addressed and reported on, including differences in the progression of the disease and response to pain.197-201 This emphasizes the importance of accounting for sex during the interpretation of results from both human and animal research studies to the human OA patient population.

The strength of any systematic review is partly contingent on the quality of included studies. As discussed in the Results section on bias analysis, the methodology of many studies conferred a high risk of bias, resulting in a low confidence in the evidence provided. In basic science studies utilizing human samples, the baseline characteristics and clinical characterization of OA patients are often missing, or lack necessary detail. Clinical background is a particularly important consideration in the context of soft-tissue calcification, given that crystal depositional diseases, such as pseudogout, can drive OA.202 Patients’ clinical background is poorly reported throughout the literature, as is disease severity, despite ECM and other tissue components differing more from the physiological state with OA progression.42 As clinical information might not always be available for collection due to ethical constraints, making this clear to readers allows findings to be interpreted in the correct clinical context. Although the search strategy covered many non-cartilage soft joint tissues, some tissues, such as the temporomandibular joint disc and acetabular labrum, were not included. In addition, the focus of this review was on structural components of the ECM, which are the elements that are studied most extensively and make up the majority of tissue ECM. However, this does mean that this work does not provide a complete account of all OA ECM, as non-structural matrix elements such as matricellular proteins or neoepitopes have not been reported on. Finally, a limitation of the review process is the data extraction, which was not done by two independent reviewers, but rather extracted by one reviewer and verified by the other reviewer. However, the effect of this is likely limited as a previous study has reported that while extraction by two independent reviewers is preferable, extraction by one reviewer with verification by a second reviewer has limited influence on the conclusions of a systematic review, especially considering a meta-analysis was not performed in the current work.203

In the process of consolidating the current literature on this topic, this work highlights several practical and methodological challenges that have limited progress in the understanding of structural ECM components, architectural features, and viscoelastic properties in non-cartilage soft-tissues in OA. One of these problems is the cross-sectional nature of studies, which is popular in the OA field as tissues are only accessible at the time of joint arthroplasty. Since OA can take decades to progress, the study of end-stage or advanced OA might not be fully informative of the processes that are driving these changes. In addition, the lack of a healthy, or non-OA, comparator group, in combination with the fact that many studies only report qualitative results, vastly reduces the depth of knowledge that can be gained from these studies. Finally, while many screened human and animal studies investigated both cartilage and other soft joint tissues, ECM is often studied exclusively in cartilage, with other features, such as cellularity and inflammatory markers, being the focus in other tissues. This shows that while there is access to both the tissues and the methods to study ECM changes in non-cartilage soft-tissues, the analysis of these tissues is not seen as a priority. However, due to the limited characterization of ECM in these tissues and their unknown contribution to disease development and progression, it is also possible that it remains unclear which ECM feature(s) should be focused on. Structural ECM encompasses a wide range of features that can be investigated with a plethora of different methods. To evaluate the most critical ECM features and applicable methods, studies investigating multiple ECM features in non-cartilage soft-tissues across different stages of disease are required.

Recent studies have started to highlight the importance of ECM as a determinant of tissue architecture and cell behaviour in disease. For example, a recent review highlights that the changes in microenvironment in early RA form important extracellular cues that shape the pathogenic cell behaviour during the onset and progression of disease.204 Therefore, the authors argue that understanding the ECM changes across different tissues in a particular disease might not only be able to help with disease classification and patient stratification, but could also hold promise for the development of treatments that target ECM.204 These treatments might not only be able to modify pathogenic cell behaviour that could be driving the disease, but also impact on joint stiffness, which is one of the most common symptoms of OA.205 All in all, more research is needed to unravel the presence and distribution of different ECM components and architectural features in joint tissues in health and in (different stages of) OA, and interplay with tissue-resident and tissue-infiltrating cells. Future research will also help to differentiate between the remodelling process in different joint tissues, which contain unique cell populations and are exposed to different mechanical and inflammatory stimuli in OA. ECM remodelling may also differ between synovial joints, given their varied anatomical locations, mechanical functions, and the presence of joint-specific tissues such as menisci. Potential variation in pathophysiology between OA joints has received little attention, with the predominance of studies on knee OA likely due to high disease prevalence in this joint and tissue being relatively accessible during commonly performed knee arthroplasties. Therefore, the future of this field is both dependent on the thorough investigation of ECM features in non-cartilage soft joint tissues across multiple OA joints and varied stages of disease progression, as well as the rigorous reporting of patient characteristics of all tissue donors.

In conclusion, this systematic review consolidates existing knowledge of a poorly defined aspect of OA pathophysiology. While a wide range of tissues and ECM components have been reported on, the qualitative nature of papers, the lack of control groups, and the paucity of reports on each ECM component means that the depth of knowledge remains poor. Overall, the studies included in this review show that the presence and abundance of many structural ECM components change in OA, and that the ECM architecture becomes more disorganized with increasing cartilage damage or increasing tissue-specific degeneration scores. While results from animal studies generally concurred with human studies, some findings contradicted observations from human studies, highlighting the importance of the choice of animal model and the need for validation in human studies. Given the role of ECM in influencing cell behaviour, further research to elucidate the broad context within which cartilage is damaged in OA will provide more insight into the disease as well as potential treatments.

Correspondence should be sent to Jolet Y. Mimpen. E-mail:

S. J. B. Snelling and J. Y. Mimpen are joint senior authors.

References

1. Goldring SR , Goldring MB . Changes in the osteochondral unit during osteoarthritis: structure, function and cartilage-bone crosstalk . Nat Rev Rheumatol . 2016 ; 12 ( 11 ): 632 – 644 . Crossref PubMed Google Scholar

2. Mimpen JY , Snelling SJB . Chondroprotective factors in osteoarthritis: a joint affair . Curr Rheumatol Rep . 2019 ; 21 ( 8 ): 41 . Crossref PubMed Google Scholar

3. Poole AR . Osteoarthritis as a whole joint disease . HSS J . 2012 ; 8 ( 1 ): 4 – 6 . Crossref PubMed Google Scholar

4. Zhang K , Li L , Yang L , et al. The biomechanical changes of load distribution with longitudinal tears of meniscal horns on knee joint: a finite element analysis . J Orthop Surg Res . 2019 ; 14 ( 1 ): 237 . Crossref PubMed Google Scholar

5. Shirazi R , Shirazi-Adl A . Analysis of partial meniscectomy and ACL reconstruction in knee joint biomechanics under a combined loading . Clin Biomech (Bristol, Avon) . 2009 ; 24 ( 9 ): 755 – 761 . Crossref PubMed Google Scholar

6. Wellsandt E , Gardinier ES , Manal K , Axe MJ , Buchanan TS , Snyder-Mackler L . Decreased knee joint loading associated with early knee osteoarthritis after anterior cruciate ligament injury . Am J Sports Med . 2016 ; 44 ( 1 ): 143 – 151 . Crossref PubMed Google Scholar

7. Hill CL , Hunter DJ , Niu J , et al. Synovitis detected on magnetic resonance imaging and its relation to pain and cartilage loss in knee osteoarthritis . Ann Rheum Dis . 2007 ; 66 ( 12 ): 1599 – 1603 . Crossref PubMed Google Scholar

8. Hill CL , Gale DG , Chaisson CE , et al. Knee effusions, popliteal cysts, and synovial thickening: association with knee pain in osteoarthritis . J Rheumatol . 2001 ; 28 ( 6 ): 1330 – 1337 . PubMed Google Scholar

9. Sanchez-Lopez E , Coras R , Torres A , Lane NE , Guma M . Synovial inflammation in osteoarthritis progression . Nat Rev Rheumatol . 2022 ; 18 ( 5 ): 258 – 275 . Crossref PubMed Google Scholar

10. Wang M , Tan G , Jiang H , et al. Molecular crosstalk between articular cartilage, meniscus, synovium, and subchondral bone in osteoarthritis . Bone Joint Res . 2022 ; 11 ( 12 ): 862 – 872 . Crossref PubMed Google Scholar

11. Theocharis AD , Skandalis SS , Gialeli C , Karamanos NK . Extracellular matrix structure . Adv Drug Deliv Rev . 2016 ; 97 : 4 – 27 . Crossref PubMed Google Scholar

12. Urbanczyk M , Layland SL , Schenke-Layland K . The role of extracellular matrix in biomechanics and its impact on bioengineering of cells and 3D tissues . Matrix Biol . 2020 ; 85–86 : 1 – 14 . Crossref PubMed Google Scholar

13. Felson DT . Osteoarthritis as a disease of mechanics . Osteoarthritis Cartilage . 2013 ; 21 ( 1 ): 10 – 15 . Crossref PubMed Google Scholar

14. Klees RF , Salasznyk RM , Kingsley K , Williams WA , Boskey A , Plopper GE . Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway . Mol Biol Cell . 2005 ; 16 ( 2 ): 881 – 890 . Crossref PubMed Google Scholar

15. Du J , Zu Y , Li J , et al. Extracellular matrix stiffness dictates Wnt expression through integrin pathway . Sci Rep . 2016 ; 6 ( 1 ): 20395 . Crossref PubMed Google Scholar

16. Allen JL , Cooke ME , Alliston T . ECM stiffness primes the TGFβ pathway to promote chondrocyte differentiation . Mol Biol Cell . 2012 ; 23 ( 18 ): 3731 – 3742 . Crossref PubMed Google Scholar

17. Wijelath ES , Rahman S , Namekata M , et al. Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain . Circ Res . 2006 ; 99 ( 8 ): 853 – 860 . Crossref PubMed Google Scholar

18. Thomas CM , Murray R , Sharif M . Chondrocyte apoptosis determined by caspase-3 expression varies with fibronectin distribution in equine articular cartilage . Int J Rheum Dis . 2011 ; 14 ( 3 ): 290 – 297 . Crossref PubMed Google Scholar

19. McCoy AM . Animal models of osteoarthritis: comparisons and key considerations . Vet Pathol . 2015 ; 52 ( 5 ): 803 – 818 . Crossref PubMed Google Scholar

20. Teeple E , Jay GD , Elsaid KA , Fleming BC . Animal models of osteoarthritis: challenges of model selection and analysis . AAPS J . 2013 ; 15 ( 2 ): 438 – 446 . Crossref PubMed Google Scholar

21. Page MJ , McKenzie JE , Bossuyt PM , et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews . BMJ . 2021 ; 372 : 71 . Crossref PubMed Google Scholar

22. No authors listed . National Library of Medicine . https://www.nlm.nih.gov/mesh/meshhome.html ( date last accessed 28 October 2024 ). Google Scholar

23. Poulet B , de Souza R , Kent AV , et al. Intermittent applied mechanical loading induces subchondral bone thickening that may be intensified locally by contiguous articular cartilage lesions . Osteoarthritis Cartilage . 2015 ; 23 ( 6 ): 940 – 948 . Crossref PubMed Google Scholar

24. Zhu J , Zhu Y , Xiao W , Hu Y , Li Y . Instability and excessive mechanical loading mediate subchondral bone changes to induce osteoarthritis . Ann Transl Med . 2020 ; 8 ( 6 ): 350 . Crossref PubMed Google Scholar

25. Kalu DN . The ovariectomized rat model of postmenopausal bone loss . Bone Miner . 1991 ; 15 ( 3 ): 175 – 191 . Crossref PubMed Google Scholar

26. Yousefzadeh N , Kashfi K , Jeddi S , Ghasemi A . Ovariectomized rat model of osteoporosis: a practical guide . EXCLI J . 2020 ; 19 : 89 – 107 . Crossref PubMed Google Scholar

27. DiFrancesco L , Sokoloff L . Lipochondral degeneration of capsular tissue in osteoarthritic hips . Am J Surg Pathol . 1995 ; 19 ( 3 ): 278 – 283 . Crossref PubMed Google Scholar

28. Campbell TM , Trudel G , Laneuville O . Knee flexion contractures in patients with osteoarthritis: clinical features and histologic characterization of the posterior capsule . PM R . 2015 ; 7 ( 5 ): 466 – 473 . Crossref PubMed Google Scholar

29. Limberg AK , Salib CG , Tibbo ME , et al. Immune cell populations differ in patients undergoing revision total knee arthroplasty for arthrofibrosis . Sci Rep . 2022 ; 12 ( 1 ): 22627 . Crossref PubMed Google Scholar

30. Voelker A , Schroeter F , Steinke H , Heyde CE . Degeneration of the lumbar spine and its relation to the expression of collagen and elastin in facet joint capsules and ligament flavum . Acta Orthop Traumatol Turc . 2022 ; 56 ( 3 ): 210 – 216 . Crossref PubMed Google Scholar

31. Herbert C , Jayson MI , Bailey AJ . Joint capsule collagen in osteoarthrosis . Ann Rheum Dis . 1973 ; 32 ( 6 ): 510 – 514 . Crossref PubMed Google Scholar

32. Cameron HU , Macnab I . Scanning electron microscopic studies of the hip joint capsule and synovial membrane . Can J Surg . 1973 ; 16 : 388 – 392 . PubMed Google Scholar

33. Heinegård D , Hernborg J , Lundberg BJ . The glycosaminoglycans of the human joint capsule: isolation and characterizaion . Arthritis Rheum . 1968 ; 11 ( 6 ): 787 – 795 . Crossref PubMed Google Scholar

34. Belluzzi E , Macchi V , Fontanella CG , et al. Infrapatellar fat pad gene expression and protein production in patients with and without osteoarthritis . Int J Mol Sci . 2020 ; 21 ( 17 ): 6016 . Crossref PubMed Google Scholar

35. Grevenstein D , Heilig J , Dargel J , et al. COMP in the infrapatellar fat pad-results of a prospective histological, immunohistological, and biochemical case-control study . J Orthop Res . 2020 ; 38 ( 4 ): 747 – 758 . Crossref PubMed Google Scholar

36. Cheng XG , Brys P , Nijs J , et al. Radiological prevalence of lumbar intervertebral disc calcification in the elderly: an autopsy study . Skel Radiol . 1996 ; 25 ( 3 ): 231 – 235 . Crossref PubMed Google Scholar

37. Kumagai K , Sakai K , Kusayama Y , et al. The extent of degeneration of cruciate ligament is associated with chondrogenic differentiation in patients with osteoarthritis of the knee . Osteoarthr Cartil . 2012 ; 20 ( 11 ): 1258 – 1267 . Crossref PubMed Google Scholar

38. Komro J , Gonzales J , Marberry K , Main DC , Cramberg M , Kondrashov P . Fibrocartilaginous metaplasia and neovascularization of the anterior cruciate ligament in patients with osteoarthritis . Clin Anat . 2020 ; 33 ( 6 ): 899 – 905 . Crossref PubMed Google Scholar

39. Nakamura Y , Ogawa H , Sohmiya K , et al. Relationship between histological changes of the anterior cruciate ligament and knee function in osteoarthritis patients . Orthop Traumatol Surg Res . 2022 ; 108 ( 8 ): 103341 . Crossref PubMed Google Scholar

40. Akisue T , Stulberg BN , Bauer TW , McMahon JT , Wilde AH , Kurosaka M . Histologic evaluation of posterior cruciate ligaments from osteoarthritic knees . Clin Orthop Relat Res . 2002 ; 400 : 165 – 173 . Crossref PubMed Google Scholar

41. Zhu J , Zhang X , Ma Y , Zhou C , Ao Y . Ultrastructural and morphological characteristics of human anterior cruciate ligament and hamstring tendons . Anat Rec (Hoboken) . 2012 ; 295 ( 9 ): 1430 – 1436 . Crossref PubMed Google Scholar

42. Levy YD , Hasegawa A , Patil S , Koziol JA , Lotz MK , D’Lima DD . Histopathological changes in the human posterior cruciate ligament during aging and osteoarthritis: correlations with anterior cruciate ligament and cartilage changes . Ann Rheum Dis . 2013 ; 72 ( 2 ): 271 – 277 . Crossref PubMed Google Scholar

43. Marczak D , Kowalczewski J , Okoń T , Synder M , Sibiński M . An evaluation of the posterior cruciate ligament function in total knee arthroplasty with regard to its morphology and clinical properties . Folia Morphol (Warsz) . 2017 ; 76 ( 1 ): 94 – 99 . Crossref PubMed Google Scholar

44. Nakahara H , Hasegawa A , Otabe K , et al. Transcription factor Mohawk and the pathogenesis of human anterior cruciate ligament degradation . Arthritis Rheum . 2013 ; 65 ( 8 ): 2081 – 2089 . Crossref PubMed Google Scholar

45. Abdul Sahib NS , Al-Sharqi SAH , Wahab MS . Study histopathological changes in the anterior and posterior cruciate ligament after knee replacement: correlations with vitamin D, calcium and c-reactive protein in iraqi patients with osteoarthritis . Pak J Biotechnol . 2017 ; 14 : 393 – 400 . Google Scholar

46. Allain J , Goutallier D , Voisin MC . Macroscopic and histological assessments of the cruciate ligaments in arthrosis of the knee . Acta Orthop Scand . 2001 ; 72 ( 3 ): 266 – 269 . Crossref PubMed Google Scholar

47. Martins GC , Camanho G , Rodrigues MI , Filho LFM , Demange MK . Histopathological analysis of the posterior cruciate ligament in primary osteoarthritis . Eur J Orthop Surg Traumatol . 2018 ; 28 ( 4 ): 691 – 699 . Crossref PubMed Google Scholar

48. Nelissen RG , Hogendoorn PC . Retain or sacrifice the posterior cruciate ligament in total knee arthroplasty? A histopathological study of the cruciate ligament in osteoarthritic and rheumatoid disease . J Clin Pathol . 2001 ; 54 ( 5 ): 381 – 384 . Crossref PubMed Google Scholar

49. Rajgopal A , Vasdev N , Pathak A , Gautam D , Vasdev A . Histological changes and neural elements in the posterior cruciate ligament in osteoarthritic knees . J Orthop Surg (Hong Kong) . 2014 ; 22 ( 2 ): 142 – 145 . Crossref PubMed Google Scholar

50. Tokumoto M , Nakasa T , Shirakawa Y , et al. The role of substance P on maintaining ligament homeostasis by inhibiting endochondral ossification during osteoarthritis progression . Connect Tissue Res . 2023 ; 64 ( 1 ): 82 – 92 . Crossref PubMed Google Scholar

51. Doerschuk SH , Hicks DG , Chinchilli VM , Pellegrini VD . Histopathology of the palmar beak ligament in trapeziometacarpal osteoarthritis . J Hand Surg Am . 1999 ; 24 ( 3 ): 496 – 504 . Crossref PubMed Google Scholar

52. Mobargha N , Ludwig C , Ladd AL , Hagert E . Ultrastructure and innervation of thumb carpometacarpal ligaments in surgical patients with osteoarthritis . Clin Orthop Relat Res . 2014 ; 472 ( 4 ): 1146 – 1154 . Crossref PubMed Google Scholar

53. Suga Y , Shigematsu H , Tanaka M , et al. Factors associated with the increased risk of atlantoaxial osteoarthritis: a retrospective study . Eur Spine J . 2022 ; 31 ( 12 ): 3418 – 3425 . Crossref PubMed Google Scholar

54. Sun Y , Mauerhan DR , Kneisl JS , et al. Histological examination of collagen and proteoglycan changes in osteoarthritic menisci . Open Rheumatol J . 2012 ; 6 ( 1 ): 24 – 32 . Crossref PubMed Google Scholar

55. Kodama Y , Furumatsu T , Maehara A , Ozaki T . Composition of cell clusters in torn menisci and their extracellular matrix components . Acta Med Okayama . 2018 ; 72 ( 5 ): 499 – 506 . Crossref PubMed Google Scholar

56. Numpaisal PO , Jiang CC , Hsieh CH , Chiang H , Chien CL . Prospective application of partially digested autologous chondrocyte for meniscus tissue engineering . Pharmaceutics . 2022 ; 14 ( 3 ): 605 . Crossref PubMed Google Scholar

57. Melrose J , Fuller ES , Roughley PJ , et al. Fragmentation of decorin, biglycan, lumican and keratocan is elevated in degenerate human meniscus, knee and hip articular cartilages compared with age-matched macroscopically normal and control tissues . Arthritis Res Ther . 2008 ; 10 ( 4 ): R79 . Crossref PubMed Google Scholar

58. Battistelli M , Favero M , Burini D , et al. Morphological and ultrastructural analysis of normal, injured and osteoarthritic human knee menisci . Eur J Histochem . 2019 ; 63 ( 1 ): 11 . Crossref PubMed Google Scholar

59. McDaniel D , Tilton E , Dominick K , et al. Histological characteristics of knee menisci in patients with osteoarthritis . Clin Anat . 2017 ; 30 ( 6 ): 805 – 810 . Crossref PubMed Google Scholar

60. Hellberg I , Karjalainen V-P , Finnilä MAJ , et al. 3D analysis and grading of calcifications from ex vivo human meniscus . Osteoarthritis Cartilage . 2023 ; 31 ( 4 ): 482 – 492 . Crossref PubMed Google Scholar

61. Abraham AC , Pauly HM , Donahue TLH . Deleterious effects of osteoarthritis on the structure and function of the meniscal enthesis . Osteoarthritis Cartilage . 2014 ; 22 ( 2 ): 275 – 283 . Crossref PubMed Google Scholar

62. Dessombz A , Nguyen C , Ea H-K , et al. Combining μX-ray fluorescence, μXANES and μXRD to shed light on Zn2+ cations in cartilage and meniscus calcifications . J Trace Elem Med Biol . 2013 ; 27 ( 4 ): 326 – 333 . Crossref PubMed Google Scholar

63. Johnson K , Hashimoto S , Lotz M , Pritzker K , Goding J , Terkeltaub R . Up-regulated expression of the phosphodiesterase nucleotide pyrophosphatase family member PC-1 is a marker and pathogenic factor for knee meniscal cartilage matrix calcification . Arthritis Rheum . 2001 ; 44 ( 5 ): 1071 – 1081 . Crossref PubMed Google Scholar

64. Kiraly AJ , Roberts A , Cox M , Mauerhan D , Hanley E , Sun Y . Comparison of meniscal cell-mediated and chondrocyte-mediated calcification . Open Orthop J . 2017 ; 11 : 225 – 233 . Crossref PubMed Google Scholar

65. López-Franco M , López-Franco O , Murciano-Antón MA , et al. Meniscal degeneration in human knee osteoarthritis: in situ hybridization and immunohistochemistry study . Arch Orthop Trauma Surg . 2016 ; 136 ( 2 ): 175 – 183 . Crossref PubMed Google Scholar

66. Park DY , Min B-H , Choi BH , et al. The degeneration of meniscus roots is accompanied by fibrocartilage formation, which may precede meniscus root tears in osteoarthritic knees . Am J Sports Med . 2015 ; 43 ( 12 ): 3034 – 3044 . Crossref PubMed Google Scholar

67. Sun Y , Mauerhan DR , Honeycutt PR , et al. Calcium deposition in osteoarthritic meniscus and meniscal cell culture . Arthritis Res Ther . 2010 ; 12 ( 2 ): R56 . Crossref PubMed Google Scholar

68. Takahashi M , Suzuki M , Kushida K , Hoshino H , Inoue T . The effect of aging and osteoarthritis on the mature and senescent cross-links of collagen in human meniscus . Arthroscopy . 1998 ; 14 ( 4 ): 366 – 372 . Crossref PubMed Google Scholar

69. Zhang D , Cheriyan T , Martin SD , Schmid TM , Spector M . Lubricin distribution in the menisci and labra of human osteoarthritic joints . Cartilage . 2012 ; 3 ( 2 ): 165 – 172 . Crossref PubMed Google Scholar

70. Prokopi N , Andrikopoulos KS , Beobide AS , Voyiatzis GA , Papachristou DJ . Collagen orientation probed by polarized Raman spectra can serve as differential diagnosis indicator between different grades of meniscus degeneration . Sci Rep . 2021 ; 11 ( 1 ): 20299 . Crossref PubMed Google Scholar

71. Sirotti S , Becce F , Sconfienza LM , et al. Reliability and diagnostic accuracy of radiography for the diagnosis of calcium pyrophosphate deposition: performance of the novel definitions developed by an international multidisciplinary working group . Arthritis Rheumatol . 2023 ; 75 ( 4 ): 630 – 638 . Crossref PubMed Google Scholar

72. Roller BL , Monibi FA , Stoker AM , Kuroki K , Bal BS , Cook JL . Characterization of knee meniscal pathology: correlation of gross, histologic, biochemical, molecular, and radiographic measures of disease . J Knee Surg . 2015 ; 28 ( 2 ): 175 – 182 . Crossref PubMed Google Scholar

73. Ghosh P , Ingman AM , Taylor TK . Variations in collagen, non-collagenous proteins, and hexosamine in menisci derived from osteoarthritic and rheumatoid arthritic knee joints . J Rheumatol . 1975 ; 2 ( 1 ): 100 – 107 . PubMed Google Scholar

74. Son M , Goodman SB , Chen W , Hargreaves BA , Gold GE , Levenston ME . Regional variation in T1ρ and T2 times in osteoarthritic human menisci: correlation with mechanical properties and matrix composition . Osteoarthritis Cartilage . 2013 ; 21 ( 6 ): 796 – 805 . Crossref PubMed Google Scholar

75. Warnecke D , Balko J , Haas J , et al. Degeneration alters the biomechanical properties and structural composition of lateral human menisci . Osteoarthritis Cartilage . 2020 ; 28 ( 11 ): 1482 – 1491 . Crossref PubMed Google Scholar

76. Mine T , Ihara K , Kawamura H , Date R , Umehara K . Collagen expression in various degenerative meniscal changes: an immunohistological study . J Orthop Surg (Hong Kong) . 2013 ; 21 ( 2 ): 216 – 220 . Crossref PubMed Google Scholar

77. Sladojević I , Krivokuća Z , Gajanin V , Manojlović S . Expression of collagen type I in unaltered and osteoarthritic menisci of knee joint . Med Pregl . 2016 ; 69 ( 1–2 ): 16 – 23 . Crossref PubMed Google Scholar

78. Hino T , Furumatsu T , Miyazawa S , et al. A histological study of the medial meniscus posterior root tibial insertion . Connect Tissue Res . 2020 ; 61 ( 6 ): 546 – 553 . Crossref PubMed Google Scholar

79. Ishizuka S , Sakai T , Hiraiwa H , et al. Hypoxia-inducible factor-2α induces expression of type X collagen and matrix metalloproteinases 13 in osteoarthritic meniscal cells . Inflamm Res . 2016 ; 65 ( 6 ): 439 – 448 . Crossref PubMed Google Scholar

80. Katsuragawa Y , Saitoh K , Tanaka N , et al. Changes of human menisci in osteoarthritic knee joints . Osteoarthritis Cartilage . 2010 ; 18 ( 9 ): 1133 – 1143 . Crossref PubMed Google Scholar

81. Jacquet C , Erivan R , Argenson JN , Parratte S , Ollivier M . Effect of 3 preservation methods (freezing, cryopreservation, and freezing + irradiation) on human menisci ultrastructure: an ex vivo comparative study with fresh tissue as a gold standard . Am J Sports Med . 2018 ; 46 ( 12 ): 2899 – 2904 . Crossref PubMed Google Scholar

82. Karjalainen V-P , Kestilä I , Finnilä MA , et al. Quantitative three-dimensional collagen orientation analysis of human meniscus posterior horn in health and osteoarthritis using micro-computed tomography . Osteoarthritis Cartilage . 2021 ; 29 ( 5 ): 762 – 772 . Crossref PubMed Google Scholar

83. Atik OŞ , Erdoğan D , Seymen CM , Bozkurt HH , Kaplanoğlu GT . Is there crosstalk between subchondral bone, cartilage, and meniscus in the pathogenesis of osteoarthritis? Eklem Hast Cerr . 2016 ; 27 ( 2 ): 62 – 67 . Crossref PubMed Google Scholar

84. Haut Donahue TL , Pauly HM . Osteoarthritic meniscal entheses exhibit altered collagen fiber orientation . Connect Tissue Res . 2022 ; 63 ( 2 ): 151 – 155 . Crossref PubMed Google Scholar

85. Nagata N , Koshino T , Saito T . Up-regulation of CD44-positive cells in medial meniscus of medial compartmental osteoarthritis of the knee . Knee . 2000 ; 7 ( 1 ): 3 – 9 . Crossref Google Scholar

86. Wang J , Roberts S , Kuiper JH , et al. Characterization of regional meniscal cell and chondrocyte phenotypes and chondrogenic differentiation with histological analysis in osteoarthritic donor-matched tissues . Sci Rep . 2020 ; 10 ( 1 ): 21658 . Crossref PubMed Google Scholar

87. Gouldin AG , Patel NK , Golladay GJ , Puetzer JL . Advanced glycation end-product accumulation differs by location and sex in aged osteoarthritic human menisci . Osteoarthritis Cartilage . 2023 ; 31 ( 3 ): 363 – 373 . Crossref PubMed Google Scholar

88. Fischenich KM , Lewis J , Kindsfater KA , Bailey TS , Haut Donahue TL . Effects of degeneration on the compressive and tensile properties of human meniscus . J Biomech . 2015 ; 48 ( 8 ): 1407 – 1411 . Crossref PubMed Google Scholar

89. Kwok J , Grogan S , Meckes B , Arce F , Lal R , D’Lima D . Atomic force microscopy reveals age-dependent changes in nanomechanical properties of the extracellular matrix of native human menisci: implications for joint degeneration and osteoarthritis . Nanomedicine . 2014 ; 10 ( 8 ): 1777 – 1785 . Crossref PubMed Google Scholar

90. Pordzik J , Bernstein A , Mayr HO , et al. Analysis of proteoglycan content and biomechanical properties in arthritic and arthritis-free menisci . Appl Sci (Basel) . 2020 ; 10 ( 24 ): 9012 . Crossref Google Scholar

91. Fuhrmann IK , Steinhagen J , Rüther W , Schumacher U . Comparative immunohistochemical evaluation of the zonal distribution of extracellular matrix and inflammation markers in human meniscus in osteoarthritis and rheumatoid arthritis . Acta Histochem . 2015 ; 117 ( 3 ): 243 – 254 . Crossref PubMed Google Scholar

92. Monibi FA , Pannellini T , Otero M , Warren RF , Rodeo SA . Histologic and molecular features in pathologic human menisci from knees with and without osteoarthritis . J Orthop Res . 2022 ; 40 ( 2 ): 504 – 512 . Crossref PubMed Google Scholar

93. Karube S , Shoji H . Compositional changes of glycosaminoglycans of the human menisci with age and degenerative joint disease . Nippon Seikeigeka Gakkai Zasshi . 1982 ; 56 ( 1 ): 51 – 57 . PubMed Google Scholar

94. Masuda I , Ishikawa K , Usuku G . A histologic and immunohistochemical study of calcium pyrophosphate dihydrate crystal deposition disease . Clin Orthop Relat Res . 1991 ; 263 : 272 – 287 . PubMed Google Scholar

95. Musumeci G , Trovato FM , Loreto C , et al. Lubricin expression in human osteoarthritic knee meniscus and synovial fluid: a morphological, immunohistochemical and biochemical study . Acta Histochem . 2014 ; 116 ( 5 ): 965 – 972 . Crossref PubMed Google Scholar

96. Jacquet C , Erivan R , Sharma A , et al. Preservation methods influence the biomechanical properties of human lateral menisci: an ex vivo comparative study of 3 methods . Orthop J Sports Med . 2019 ; 7 ( 4 ): 2325967119841622 . Crossref PubMed Google Scholar

97. Folkesson E , Turkiewicz A , Ali N , et al. Proteomic comparison of osteoarthritic and reference human menisci using data-independent acquisition mass spectrometry . Osteoarthritis Cartilage . 2020 ; 28 ( 8 ): 1092 – 1101 . Crossref PubMed Google Scholar

98. Roller BL , Monibi F , Stoker AM , Bal BS , Stannard JP , Cook JL . Characterization of meniscal pathology using molecular and proteomic analyses . J Knee Surg . 2015 ; 28 ( 6 ): 496 – 505 . Crossref PubMed Google Scholar

99. Park J , Lee H-S , Go E-B , et al. Proteomic analysis of the meniscus cartilage in osteoarthritis . Int J Mol Sci . 2021 ; 22 ( 15 ): 8181 . Crossref PubMed Google Scholar

100. Fink B , Egl M , Singer J , Fuerst M , Bubenheim M , Neuen-Jacob E . Morphologic changes in the vastus medialis muscle in patients with osteoarthritis of the knee . Arthritis Rheum . 2007 ; 56 ( 11 ): 3626 – 3633 . Crossref PubMed Google Scholar

101. Noehren B , Kosmac K , Walton RG , et al. Alterations in quadriceps muscle cellular and molecular properties in adults with moderate knee osteoarthritis . Osteoarthritis Cartilage . 2018 ; 26 ( 10 ): 1359 – 1368 . Crossref PubMed Google Scholar

102. Serrão PR , Vasilceac FA , Gramani-Say K , et al. Expression of receptors of advanced glycation end product (RAGE) and types I, III and IV collagen in the vastus lateralis muscle of men in early stages of knee osteoarthritis . Connect Tissue Res . 2014 ; 55 ( 5–6 ): 331 – 338 . Crossref PubMed Google Scholar

103. Mattiello-Sverzut AC , Petersen SG , Kjaer M , Mackey AL . Morphological adaptation of muscle collagen and receptor of advanced glycation end product (RAGE) in osteoarthritis patients with 12 weeks of resistance training: influence of anti-inflammatory or glucosamine treatment . Rheumatol Int . 2013 ; 33 ( 9 ): 2215 – 2224 . Crossref PubMed Google Scholar

104. Krawetz RJ , Wu YE , Bertram KL , et al. Synovial mesenchymal progenitor derived aggrecan regulates cartilage homeostasis and endogenous repair capacity . Cell Death Dis . 2022 ; 13 ( 5 ): 470 . Crossref PubMed Google Scholar

105. Rafael MS , Cavaco S , Viegas CSB , et al. Insights into the association of Gla‐rich protein and osteoarthritis, novel splice variants and γ‐carboxylation status . Mol Nutr Food Res . 2014 ; 58 ( 8 ): 1636 – 1646 . Crossref PubMed Google Scholar

106. Ea H-K , Chobaz V , Nguyen C , et al. Pathogenic role of basic calcium phosphate crystals in destructive arthropathies . PLoS One . 2013 ; 8 ( 2 ): e57352 . Crossref PubMed Google Scholar

107. Nakashima K , Koshino T , Saito T . Synovial immunohistochemical changes after high tibial osteotomy for osteoarthritis of the knee. Two-year prospective follow-up . Bull Hosp Jt Dis . 1998 ; 57 ( 4 ): 187 – 194 . PubMed Google Scholar

108. Saito I , Koshino T , Nakashima K , Uesugi M , Saito T . Increased cellular infiltrate in inflammatory synovia of osteoarthritic knees . Osteoarthritis Cartilage . 2002 ; 10 ( 2 ): 156 – 162 . Crossref PubMed Google Scholar

109. Richardot P , Charni-Ben Tabassi N , Toh L , et al. Nitrated type III collagen as a biological marker of nitric oxide-mediated synovial tissue metabolism in osteoarthritis . Osteoarthritis Cartilage . 2009 ; 17 ( 10 ): 1362 – 1367 . Crossref PubMed Google Scholar

110. Ene R , Sinescu RD , Ene P , Cîrstoiu MM , Cîrstoiu FC . Synovial inflammation in patients with different stages of knee osteoarthritis . Rom J Morphol Embryol . 2015 ; 56 ( 1 ): 169 – 173 . PubMed Google Scholar

111. Kaufmann J , Mueller A , Voigt A , et al. Hydroxypyridinium collagen crosslinks in serum, urine, synovial fluid and synovial tissue in patients with rheumatoid arthritis compared with osteoarthritis . Rheumatol (Oxford) . 2003 ; 42 ( 2 ): 314 – 320 . Crossref PubMed Google Scholar

112. Takahashi M , Kushida K , Hoshino H , et al. Concentrations of pyridinoline and deoxypyridinoline in joint tissues from patients with osteoarthritis or rheumatoid arthritis . Ann Rheum Dis . 1996 ; 55 ( 5 ): 324 – 327 . Crossref PubMed Google Scholar

113. Di Cesare PE , Fang C , Leslie MP , et al. Localization and expression of cartilage oligomeric matrix protein by human rheumatoid and osteoarthritic synovium and cartilage . J Orthop Res . 1999 ; 17 ( 3 ): 437 – 445 . Crossref PubMed Google Scholar

114. Cillero-Pastor B , Eijkel GB , Blanco FJ , Heeren RMA . Protein classification and distribution in osteoarthritic human synovial tissue by matrix-assisted laser desorption ionization mass spectrometry imaging . Anal Bioanal Chem . 2015 ; 407 ( 8 ): 2213 – 2222 . Crossref PubMed Google Scholar

115. Cutolo M , Picasso M , Ponassi M , Sun MZ , Balza E . Tenascin and fibronectin distribution in human normal and pathological synovium . J Rheumatol . 1992 ; 19 ( 9 ): 1439 – 1447 . PubMed Google Scholar

116. Fan L , Wang Q , Liu R , et al. Citrullinated fibronectin inhibits apoptosis and promotes the secretion of pro-inflammatory cytokines in fibroblast-like synoviocytes in rheumatoid arthritis . Arthritis Res Ther . 2012 ; 14 ( 6 ): R266 . Crossref PubMed Google Scholar

117. Kragstrup TW , Sohn DH , Lepus CM , et al. Fibroblast-like synovial cell production of extra domain A fibronectin associates with inflammation in osteoarthritis . BMC Rheumatol . 2019 ; 3 : 46 . Crossref PubMed Google Scholar

118. Nikkari L , Haapasalmi K , Aho H , et al. Localization of the alpha V subfamily of integrins and their putative ligands in synovial lining cell layer . J Rheumatol . 1995 ; 22 ( 1 ): 16 – 23 . PubMed Google Scholar

119. Nishida K , Inoue H , Toda K , Murakami T . Localization of the glycosaminoglycans in the synovial tissues from osteoarthritic knees . Acta Med Okayama . 1995 ; 49 ( 6 ): 287 – 294 . Crossref PubMed Google Scholar

120. Wang X , Dong C , Li N , et al. Modulation of TGF‑β activity by latent TGF‑β‑binding protein 1 in human osteoarthritis fibroblast‑like synoviocytes . Mol Med Rep . 2018 ; 17 : 1893 – 1900 . Crossref PubMed Google Scholar

121. Turdean SG , Jung I , Gurzu S , et al. Histopathological evaluation and expression of the pluripotent mesenchymal stem cell-like markers CD105 and CD44 in the synovial membrane of patients with primary versus secondary hip osteoarthritis . J Investig Med . 2017 ; 65 ( 2 ): 363 – 369 . Crossref PubMed Google Scholar

122. Konttinen YT , Li TF , Mandelin J , et al. Hyaluronan synthases, hyaluronan, and its CD44 receptor in tissue around loosened total hip prostheses . J Pathol . 2001 ; 194 ( 3 ): 384 – 390 . Crossref PubMed Google Scholar

123. Christensen AF , Sorensen GL , Junker K , et al. Site-specific absence of microfibrillar-associated protein 4 (MFAP4) from the internal elastic membrane of arterioles in the rheumatoid arthritis synovial membrane: an immunohistochemical study in patients with advanced rheumatoid arthritis versus osteoarthritis . APMIS . 2019 ; 127 ( 8 ): 588 – 593 . Crossref PubMed Google Scholar

124. Li TF , Xu JW , Santavirta S , et al. Distribution of fibronectins and their integrin receptors in interface tissue from aseptic loosening of hip prostheses . Clin Exp Rheumatol . 2000 ; 18 ( 2 ): 221 – 225 . PubMed Google Scholar

125. Konttinen YT , Li TF , Xu JW , et al. Expression of laminins and their integrin receptors in different conditions of synovial membrane and synovial membrane-like interface tissue . Ann Rheum Dis . 1999 ; 58 ( 11 ): 683 – 690 . Crossref PubMed Google Scholar

126. van Linthoudt D , Beutler A , Clayburne G , Sieck M , Fernandes L , Schumacher HR . Morphometric studies on synovium in advanced osteoarthritis: is there an association between apatite-like material and collagen deposits? Clin Exp Rheumatol . 1997 ; 15 ( 5 ): 493 – 497 . PubMed Google Scholar

127. Pollock LE , Lalor P , Revell PA . Type IV collagen and laminin in the synovial intimal layer: an immunohistochemical study . Rheumatol Int . 1990 ; 9 ( 6 ): 277 – 280 . Crossref PubMed Google Scholar

128. Mapp PI , Revell PA . Fibronectin production by synovial intimal cells . Rheumatol Int . 1985 ; 5 ( 5 ): 229 – 237 . Crossref PubMed Google Scholar

129. Scott DL , Wainwright AC , Walton KW , Williamson N . Significance of fibronectin in rheumatoid arthritis and osteoarthrosis . Ann Rheum Dis . 1981 ; 40 ( 2 ): 142 – 153 . Crossref PubMed Google Scholar

130. Worrall JG , Wilkinson LS , Bayliss MT , Edwards JCW . Zonal distribution of chondroitin-4-sulphate/dermatan sulphate and chondroitin-6-sulphate in normal and diseased human synovium . Ann Rheum Dis . 1994 ; 53 ( 1 ): 35 – 38 . Crossref PubMed Google Scholar

131. Rinaldi N , Barth TF , Weis D , et al. Loss of laminin and of the laminin receptor integrin subunit alpha 6 in situ correlates with cytokine induced down regulation of alpha 6 on fibroblast-like synoviocytes from rheumatoid arthritis . Ann Rheum Dis . 1998 ; 57 ( 9 ): 559 – 565 . Crossref PubMed Google Scholar

132. Dijkgraaf LC , Liem RSB , de Bont LGM . Ultrastructural characteristics of the synovial membrane in osteoarthritic temporomandibular joints . J Oral Maxillofac Surg . 1997 ; 55 ( 11 ): 1269 – 1279 . Crossref PubMed Google Scholar

133. Okamoto K , Kiga N , Shinohara Y , Tojyo I , Fujita S . Effect of interleukin-1beta and dehydroepiandrosterone on the expression of lumican and fibromodulin in fibroblast-like synovial cells of the human temporomandibular joint . Eur J Histochem . 2015 ; 59 ( 1 ): 2440 . Crossref PubMed Google Scholar

134. Schneider M , Voss B , Rauterberg J , et al. Basement membrane proteins in synovial membrane: distribution in rheumatoid arthritis and synthesis by fibroblast-like cells . Clin Rheumatol . 1994 ; 13 ( 1 ): 90 – 97 . Crossref PubMed Google Scholar

135. Klareskog L , Johnell O , Hulth A , Holmdahl R , Rubin K . Reactivity of monoclonal anti‐type II collagen antibodies with cartilage and synovial tissue in rheumatoid arthritis and osteoarthritis . Arthritis Rheum . 1986 ; 29 ( 6 ): 730 – 738 . Crossref PubMed Google Scholar

136. Scott DL , Salmon M , Morris CJ , Wainwright AC , Walton KW . Laminin and vascular proliferation in rheumatoid arthritis . Ann Rheum Dis . 1984 ; 43 ( 4 ): 551 – 555 . Crossref PubMed Google Scholar

137. Chang X , Yamada R , Suzuki A , Kochi Y , Sawada T , Yamamoto K . Citrullination of fibronectin in rheumatoid arthritis synovial tissue . Rheumatology (Oxford) . 2005 ; 44 ( 11 ): 1374 – 1382 . Crossref PubMed Google Scholar

138. Hino K , Shiozawa S , Kuroki Y , et al. EDA-containing fibronectin is synthesized from rheumatoid synovial fibroblast-like cells . Arthritis Rheum . 1995 ; 38 ( 5 ): 678 – 683 . Crossref PubMed Google Scholar

139. Kriegsmann J , Berndt A , Hansen T , et al. Expression of fibronectin splice variants and oncofetal glycosylated fibronectin in the synovial membranes of patients with rheumatoid arthritis and osteoarthritis . Rheumatol Int . 2004 ; 24 ( 1 ): 25 – 33 . Crossref PubMed Google Scholar

140. Itokazu M , Shinozaki M , Ohno T . Quantitative analysis of hyaluronan in the synovial tissues of patients with joint disorders . Clin Rheumatol . 1998 ; 17 ( 3 ): 261 – 262 . Crossref PubMed Google Scholar

141. Santiago B , Baleux F , Palao G , et al. CXCL12 is displayed by rheumatoid endothelial cells through its basic amino-terminal motif on heparan sulfate proteoglycans . Arthritis Res Ther . 2006 ; 8 ( 2 ): R43 . Crossref PubMed Google Scholar

142. Poduval P , Sillat T , Virtanen I , Dabagh M , Konttinen YT . Immigration check for neutrophils in RA lining: laminin alpha5 low expression regions act as exit points . Scand J Rheumatol . 2010 ; 39 ( 2 ): 132 – 140 . Crossref PubMed Google Scholar

143. Ren X , Geng M , Xu K , et al. Quantitative proteomic analysis of synovial tissue reveals that upregulated OLFM4 aggravates inflammation in rheumatoid arthritis . J Proteome Res . 2021 ; 20 ( 10 ): 4746 – 4757 . Crossref PubMed Google Scholar

144. Worrall JG , Bayliss MT , Edwards JCW . Morphological localization of hyaluronan in normal and diseased synovium . J Rheumatol . 1991 ; 18 ( 10 ): 1466 – 1472 . PubMed Google Scholar

145. Meknas K , Johansen O , Steigen SE , Olsen R , Jørgensen L , Kartus J . Could tendinosis be involved in osteoarthritis? Scand J Med Sci Sports . 2012 ; 22 ( 5 ): 627 – 634 . Crossref PubMed Google Scholar

146. Ibrahim M , Kartus JT , Steigen SE , Olsen R , Meknas K . More tendon degeneration in patients with shoulder osteoarthritis . Knee Surg Sports Traumatol Arthrosc . 2019 ; 27 ( 1 ): 267 – 275 . Crossref PubMed Google Scholar

147. Expósito Molinero MR , de Miguel Mendieta E . Discriminant validity study of Achilles enthesis ultrasound . Reum Clin . 2016 ; 12 ( 4 ): 206 – 209 . Crossref PubMed Google Scholar

148. Mazzocca AD , McCarthy MBR , Ledgard FA , et al. Histomorphologic changes of the long head of the biceps tendon in common shoulder pathologies . Arthroscopy . 2013 ; 29 ( 6 ): 972 – 981 . Crossref PubMed Google Scholar

149. Ibrahim M , Hedlundh U , Sernert N , et al. Histological and ultrastructural degenerative findings in the gluteus medius tendon after hip arthroplasty . J Orthop Surg Res . 2021 ; 16 ( 1 ): 339 . Crossref PubMed Google Scholar

150. Loeser RF , Olex AL , McNulty MA , et al. Disease progression and phasic changes in gene expression in a mouse model of osteoarthritis . PLoS One . 2013 ; 8 ( 1 ): e54633 . Crossref PubMed Google Scholar

151. Ramos-Mucci L , Javaheri B , van’t Hof R , et al. Meniscal and ligament modifications in spontaneous and post-traumatic mouse models of osteoarthritis . Arthritis Res Ther . 2020 ; 22 ( 1 ): 171 . Crossref PubMed Google Scholar

152. Walton M . Degenerative joint disease in the mouse knee; radiological and morphological observations . J Pathol . 1977 ; 123 ( 2 ): 97 – 107 . Crossref PubMed Google Scholar

153. Anderson-MacKenzie JM , Billingham ME , Bailey AJ . Collagen remodeling in the anterior cruciate ligament associated with developing spontaneous murine osteoarthritis . Biochem Biophys Res Commun . 1999 ; 258 ( 3 ): 763 – 767 . Crossref PubMed Google Scholar

154. Cui P , Sun B-H , Dai Y-F , et al. Healing of the torn anterior horn of rabbit medial meniscus to bone after transtibial pull-out repair and autologous platelet-rich plasma gel injection . Orthop Surg . 2023 ; 15 ( 2 ): 617 – 627 . Crossref PubMed Google Scholar

155. Miller D , DeSutter C , Scott A , et al. Vascular structure and function in the medial collateral ligament of anterior cruciate ligament transected rabbit knees . J Orthop Res . 2014 ; 32 ( 9 ): 1104 – 1110 . Crossref PubMed Google Scholar

156. Funakoshi Y , Hariu M , Tapper JE , et al. Periarticular ligament changes following ACL/MCL transection in an ovine stifle joint model of osteoarthritis . J Orthop Res . 2007 ; 25 ( 8 ): 997 – 1006 . Crossref PubMed Google Scholar

157. Barton KI , Heard BJ , Kroker A , et al. Structural consequences of a partial anterior cruciate ligament injury on remaining joint integrity: evidence for ligament and bone changes over time in an ovine model . Am J Sports Med . 2021 ; 49 ( 3 ): 637 – 648 . Crossref PubMed Google Scholar

158. Bedingfield SK , Colazo JM , Di Francesco M , et al. Top-down fabricated microPlates for prolonged, intra-articular matrix metalloproteinase 13 siRNA nanocarrier delivery to reduce post-traumatic osteoarthritis . ACS Nano . 2021 ; 15 ( 9 ): 14475 – 14491 . Crossref PubMed Google Scholar

159. Muschter D , Fleischhauer L , Taheri S , Schilling AF , Clausen-Schaumann H , Grässel S . Sensory neuropeptides are required for bone and cartilage homeostasis in a murine destabilization-induced osteoarthritis model . Bone . 2020 ; 133 : 115181 . Crossref PubMed Google Scholar

160. Catheline SE , Bell RD , Oluoch LS , et al. IKKβ-NF-κB signaling in adult chondrocytes promotes the onset of age-related osteoarthritis in mice . Sci Signal . 2021 ; 14 ( 701 ): eabf3535 . Crossref PubMed Google Scholar

161. Lee KI , Gamini R , Olmer M , et al. Mohawk is a transcription factor that promotes meniscus cell phenotype and tissue repair and reduces osteoarthritis severity . Sci Transl Med . 2020 ; 12 ( 567 ): 28 . Crossref PubMed Google Scholar

162. Le Graverand MPH , Sciore P , Eggerer J . Formation and phenotype of cell clusters in osteoarthritic meniscus . Arthritis Rheum . 2001 ; 44 ( 8 ): 1808 – 1818 . Crossref PubMed Google Scholar

163. Hellio Le Graverand MP , Vignon E , Otterness IG , Hart DA . Early changes in lapine menisci during osteoarthritis development: Part I: Cellular and matrix alterations . Osteoarthritis Cartilage . 2001 ; 9 ( 1 ): 56 – 64 . Crossref PubMed Google Scholar

164. Zhao J , Huang S , Zheng J , et al. Changes of rabbit meniscus influenced by hyaline cartilage injury of osteoarthritis . Int J Clin Exp Med . 2014 ; 7 ( 9 ): 2948 – 2956 . PubMed Google Scholar

165. Levillain A , Magoariec H , Boulocher C , Decambron A , Viateau V , Hoc T . Viscoelastic properties of rabbit osteoarthritic menisci: A correlation with matrix alterations . J Mech Behav Biomed Mater . 2017 ; 65 : 1 – 10 . Crossref PubMed Google Scholar

166. Levillain A , Magoariec H , Boulocher C , Decambron A , Viateau V , Hoc T . Effects of a viscosupplementation therapy on rabbit menisci in an anterior cruciate ligament transection model of osteoarthritis . J Biomech . 2017 ; 58 : 147 – 154 . Crossref PubMed Google Scholar

167. Endo J , Sasho T , Akagi R , et al. Comparative analysis of gene expression between cartilage and menisci in early-phase osteoarthritis of the knee-an animal model study . J Knee Surg . 2018 ; 31 ( 7 ): 664 – 669 . Crossref PubMed Google Scholar

168. Bansal S , Miller LM , Patel JM , et al. Transection of the medial meniscus anterior horn results in cartilage degeneration and meniscus remodeling in a large animal model . J Orthop Res . 2020 ; 38 ( 12 ): 2696 – 2708 . Crossref PubMed Google Scholar

169. Bansal S , Meadows KD , Miller LM , et al. Six-month outcomes of clinically relevant meniscal injury in a large-animal model . Orthop J Sports Med . 2021 ; 9 ( 11 ): 23259671211035444 . Crossref PubMed Google Scholar

170. Shi X , Yu W , Wang T , et al. Electroacupuncture alleviates cartilage degradation: Improvement in cartilage biomechanics via pain relief and potentiation of muscle function in a rabbit model of knee osteoarthritis . Biomed Pharmacother . 2020 ; 123 : 109724 . Crossref PubMed Google Scholar

171. Lee K , Gang GG , Kang YG , Jung SS , Park HG , Jang JH . Alleviation of osteoarthritis-induced pain and motor deficits in rats by a novel device for the intramuscular insertion of cog polydioxanone filament . Appl Sci (Basel) . 2021 ; 11 ( 22 ): 10534 . Crossref Google Scholar

172. Tavallaee G , Lively S , Rockel JS , et al. Contribution of microRNA-27b-3p to synovial fibrotic responses in knee osteoarthritis . Arthritis Rheumatol . 2022 ; 74 ( 12 ): 1928 – 1942 . Crossref PubMed Google Scholar

173. Gamal N , Abou-Rabia NM , El Ebiary FH , Khalaf G , Raafat MH . The possible therapeutic role of platelet rich plasma on a model of osteoarthritis in male albino rat. Histological and immunohistochemical study . Egypt J Histol . 2019 ; 42 ( 3 ): 554 – 566 . Crossref Google Scholar

174. Zhang L , Zhang L , Huang Z , et al. Increased HIF-1α in knee osteoarthritis aggravate synovial fibrosis via fibroblast-like synoviocyte pyroptosis . Oxid Med Cell Longev . 2019 ; 2019 : 6326517 . Crossref PubMed Google Scholar

175. Zhang L , Li X , Zhang H , et al. Agnuside alleviates synovitis and fibrosis in knee osteoarthritis through the inhibition of HIF-1α and NLRP3 inflammasome . Mediators Inflamm . 2021 ; 2021 : 5534614 . Crossref PubMed Google Scholar

176. Li M , Zhang L , Liu Z , et al. Sanse powder essential oil nanoemulsion negatively regulates TRPA1 by AMPK/mTOR signaling in synovitis: knee osteoarthritis rat model and fibroblast-like synoviocyte isolates . Mediators Inflamm . 2021 ; 2021 : 4736670 . Crossref PubMed Google Scholar

177. Sriwatananukulkit O , Desclaux S , Tawonsawatruk T , et al. Effectiveness of losartan on infrapatellar fat pad/synovial fibrosis and pain behavior in the monoiodoacetate-induced rat model of osteoarthritis pain . Biomed Pharmacother . 2023 ; 158 : 114121 . Crossref PubMed Google Scholar

178. Zhang L , Xing R , Huang Z , et al. Inhibition of synovial macrophage pyroptosis alleviates synovitis and fibrosis in knee osteoarthritis . Mediators Inflamm . 2019 ; 2019 : 2165918 . Crossref PubMed Google Scholar

179. Zhang L , Li M , Li X , et al. Characteristics of sensory innervation in synovium of rats within different knee osteoarthritis models and the correlation between synovial fibrosis and hyperalgesia . J Adv Res . 2022 ; 35 : 141 – 151 . Crossref PubMed Google Scholar

180. Li X , Mei W , Huang Z , et al. Casticin suppresses monoiodoacetic acid-induced knee osteoarthritis through inhibiting HIF-1α/NLRP3 inflammasome signaling . Int Immunopharmacol . 2020 ; 86 : 106745 . Crossref PubMed Google Scholar

181. Almasry SM , Soliman HM , El-Tarhouny SA , Algaidi SA , Ragab EM . Platelet rich plasma enhances the immunohistochemical expression of platelet derived growth factor and vascular endothelial growth factor in the synovium of the meniscectomized rat models of osteoarthritis . Ann Anat . 2015 ; 197 : 38 – 49 . Crossref PubMed Google Scholar

182. Dai S , Liang T , Fujii T , et al. Increased elastic modulus of the synovial membrane in a rat ACLT model of osteoarthritis revealed by atomic force microscopy . Braz J Med Biol Res . 2020 ; 53 ( 11 ): e10058 . Crossref PubMed Google Scholar

183. Bryk M , Chwastek J , Mlost J , Kostrzewa M , Starowicz K . Sodium monoiodoacetate dose-dependent changes in matrix metalloproteinases and inflammatory components as prognostic factors for the progression of osteoarthritis . Front Pharmacol . 2021 ; 12 : 643605 . Crossref PubMed Google Scholar

184. Castrogiovanni P , Di Rosa M , Ravalli S , et al. Moderate physical activity as a prevention method for knee osteoarthritis and the role of synoviocytes as biological key . Int J Mol Sci . 2019 ; 20 ( 3 ): 511 . Crossref PubMed Google Scholar

185. Wei Q , Kong N , Liu X , et al. Pirfenidone attenuates synovial fibrosis and postpones the progression of osteoarthritis by anti-fibrotic and anti-inflammatory properties in vivo and in vitro . J Transl Med . 2021 ; 19 ( 1 ): 157 . Crossref PubMed Google Scholar

186. Lapadula G , Nico B , Cantatore FP , La Canna R , Roncali L , Pipitone V . Early ultrastructural changes of articular cartilage and synovial membrane in experimental vitamin A-induced osteoarthritis . J Rheumatol . 1995 ; 22 ( 10 ): 1913 – 1921 . PubMed Google Scholar

187. McErlain DD , Appleton CTG , Litchfield RB , et al. Study of subchondral bone adaptations in a rodent surgical model of OA using in vivo micro-computed tomography . Osteoarthritis Cartilage . 2008 ; 16 ( 4 ): 458 – 469 . Crossref PubMed Google Scholar

188. Dabrowska S , Ekiert-Radecka M , Karbowniczek J , et al. Calcification alters the viscoelastic properties of tendon fascicle bundles depending on matrix content . Acta Biomater . 2023 ; 166 : 360 – 374 . Crossref PubMed Google Scholar

189. Ricard-Blum S . The collagen family . Cold Spring Harb Perspect Biol . 2011 ; 3 ( 1 ): a004978 . Crossref PubMed Google Scholar

190. Chen D , Smith LR , Khandekar G , et al. Distinct effects of different matrix proteoglycans on collagen fibrillogenesis and cell-mediated collagen reorganization . Sci Rep . 2020 ; 10 ( 1 ): 19065 . Crossref PubMed Google Scholar

191. Naba A . Ten years of extracellular matrix proteomics: accomplishments, challenges, and future perspectives . Mol Cell Proteomics . 2023 ; 22 ( 4 ): 100528 . Crossref PubMed Google Scholar

192. Cope PJ , Ourradi K , Li Y , Sharif M . Models of osteoarthritis: the good, the bad and the promising . Osteoarthritis Cartilage . 2019 ; 27 ( 2 ): 230 – 239 . Crossref PubMed Google Scholar

193. Proffen BL , McElfresh M , Fleming BC , Murray MM . A comparative anatomical study of the human knee and six animal species . Knee . 2012 ; 19 ( 4 ): 493 – 499 . Crossref PubMed Google Scholar

194. Tschon M , Contartese D , Pagani S , Borsari V , Fini M . Gender and sex are key determinants in osteoarthritis not only confounding variables. A systematic review of clinical data . J Clin Med . 2021 ; 10 ( 14 ): 3178 . Crossref PubMed Google Scholar

195. Szilagyi IA , Waarsing JH , Schiphof D , van Meurs JBJ , Bierma-Zeinstra SMA . Towards sex-specific osteoarthritis risk models: evaluation of risk factors for knee osteoarthritis in males and females . Rheumatology (Oxford) . 2022 ; 61 ( 2 ): 648 – 657 . Crossref PubMed Google Scholar

196. Karp NA , Reavey N . Sex bias in preclinical research and an exploration of how to change the status quo . Br J Pharmacol . 2019 ; 176 ( 21 ): 4107 – 4118 . Crossref PubMed Google Scholar

197. Pucha KA , McKinney JM , Fuller JM , Willett NJ . Characterization of OA development between sexes in the rat medial meniscal transection model . Osteoarthr Cartil Open . 2020 ; 2 ( 3 ): 100066 . Crossref PubMed Google Scholar

198. Temp J , Labuz D , Negrete R , Sunkara V , Machelska H . Pain and knee damage in male and female mice in the medial meniscal transection-induced osteoarthritis . Osteoarthritis Cartilage . 2020 ; 28 ( 4 ): 475 – 485 . Crossref PubMed Google Scholar

199. Hwang HS , Park IY , Hong JI , Kim JR , Kim HA . Comparison of joint degeneration and pain in male and female mice in DMM model of osteoarthritis . Osteoarthritis Cartilage . 2021 ; 29 ( 5 ): 728 – 738 . Crossref PubMed Google Scholar

200. Malfait AM , Miller RE . Why we should study osteoarthritis pain in experimental models in both sexes . Osteoarthritis Cartilage . 2020 ; 28 ( 4 ): 397 – 399 . Crossref PubMed Google Scholar

201. Franke M , Mancino C , Taraballi F . Reasons for the sex bias in osteoarthritis research: a review of preclinical studies . Int J Mol Sci . 2023 ; 24 ( 12 ): 10386 . Crossref PubMed Google Scholar

202. Derfus BA , Kurian JB , Butler JJ , et al. The high prevalence of pathologic calcium crystals in pre-operative knees . J Rheumatol . 2002 ; 29 ( 3 ): 570 – 574 . PubMed Google Scholar

203. Mathes T , Klaßen P , Pieper D . Frequency of data extraction errors and methods to increase data extraction quality: a methodological review . BMC Med Res Methodol . 2017 ; 17 ( 1 ): 152 . Crossref PubMed Google Scholar

204. Buckley CD , Ospelt C , Gay S , Midwood KS . Location, location, location: how the tissue microenvironment affects inflammation in RA . Nat Rev Rheumatol . 2021 ; 17 ( 4 ): 195 – 212 . Crossref PubMed Google Scholar

205. Sharma L . Osteoarthritis of the knee . N Engl J Med . 2021 ; 384 ( 1 ): 51 – 59 . Crossref PubMed Google Scholar

Author contributions

I. G. A. Raza: Data curation, Formal analysis, Investigation, Writing – original draft

S. J. B. Snelling: Conceptualization, Investigation, Project administration, Writing – review & editing

J. Y. Mimpen: Conceptualization, Data curation, Formal analysis, Investigation, Project administration, Writing – original draft

Funding statement

This work was supported by the National Institute for Health Research Oxford Biomedical Research Centre. J. Y. Mimpen is funded by Versus Arthritis (22873) and was supported the Chan-Zuckerberg Initiative (CZIF2019-002426). S. J. B. Snelling is funded by the Chan-Zuckerberg Initiative (CZIF2019-002426 and CZIF2021-240342) and supported by the National Institute for Health Research Oxford Biomedical Research Centre. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

ICMJE COI statement

J. Y. Mimpen reports grants for this study from Versus Arthritis (22873), the National Institute for Health Research Oxford Biomedical Research Centre, and the Chan-Zuckerberg Initiative (CZIF2019-002426). J. Y. Mimpen also reports an Oxford University Medical Sciences Division Pump-priming grant, unrelated to this study. S. J. B. Snelling reports grant support for salary during the timeframe of this study from the Chan-Zuckerberg Initiative and the National Institute for Health Research Oxford Biomedical Research Centre.

Data sharing

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials. In addition, the raw data from the data extraction process, which were used to populate Supplementary Tables i, ii, iv, and v, are available upon reasonable request from the corresponding author.

Acknowledgements

We would like to thank Oxford University medical librarian Eli Harriss for her support in generating and executing the search strategy. We would like to thank Dr Mathew Baldwin for his helpful feedback on the design of this study.

Open access funding

Versus Arthritis (22873) provided funding for the Open Access CC-BY licence.

Supplementary material

Search strategy for Ovid MEDLINE, Ovid Embase, and Scopus platforms; tables of structural extracellular matrix components and architectural features in non-cartilage soft tissues of human osteoarthritic joints and animal models of osteoarthritis; table of the 2015 OHAT risk of bias analysis of all included studies; and tables of characteristics of the included human and animal studies.

Social media

Follow S. J. B. Snelling on X @Sarah_JB_S

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© 2024 Raza et al. Open Access This article is distributed under the terms of the Creative Commons Attributions (CC BY 4.0) licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium or format, provided the original author and source are credited.

Information

Journal

Bone & Joint Research

Volume

13 No.12 | Pages 703 - 715

Section

Bone Biology

Published

03 December 2024

DOI

PubMed

39622273

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Medical Student

Medical Sciences Division, University of Oxford, Oxford, UK

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Associate Professor

Botnar Institute for Musculoskeletal Sciences, Nuffield Department of Orthopaedics Rheumatology and Musculoskeletal Sciences, University of Oxford, Oxford, UK

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Postdoctoral Research Fellow

Botnar Institute for Musculoskeletal Sciences, Nuffield Department of Orthopaedics Rheumatology and Musculoskeletal Sciences, University of Oxford, Oxford, UK

Kennedy Institute of Rheumatology, Nuffield Department of Orthopaedics Rheumatology and Musculoskeletal Sciences, University of Oxford, Oxford, UK

jolet.mimpen@ndorms.ox.ac.uk

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Figures

Fig. 1 PRISMA 2022 flow diagram. ECM, extracellular matrix; OA, osteoarthritis.

Fig. 1

PRISMA 2022 flow diagram. ECM, extracellular matrix; OA, osteoarthritis.
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Fig. 2 Schematic overview of the study population, anatomical locations, and extracellular matrix (ECM) features studied in the included studies. One study investigated ECM in both human osteoarthritis (OA) and an animal model of OA. Created with BioRender.com. TMJ, temporomandibular joint.

Fig. 2

Schematic overview of the study population, anatomical locations, and extracellular matrix (ECM) features studied in the included studies. One study investigated ECM in both human osteoarthritis (OA) and an animal model of OA. Created with BioRender.com. TMJ, temporomandibular joint.
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References

1. Find in article

Goldring SR , Goldring MB . Changes in the osteochondral unit during osteoarthritis: structure, function and cartilage-bone crosstalk . Nat Rev Rheumatol . 2016 ; 12 ( 11 ): 632 – 644 .

Crossref PubMed Google Scholar
2. Find in article

Mimpen JY , Snelling SJB . Chondroprotective factors in osteoarthritis: a joint affair . Curr Rheumatol Rep . 2019 ; 21 ( 8 ): 41 .

Crossref PubMed Google Scholar
3. Find in article

Poole AR . Osteoarthritis as a whole joint disease . HSS J . 2012 ; 8 ( 1 ): 4 – 6 .

Crossref PubMed Google Scholar
4. Find in article

Zhang K , Li L , Yang L , et al. The biomechanical changes of load distribution with longitudinal tears of meniscal horns on knee joint: a finite element analysis . J Orthop Surg Res . 2019 ; 14 ( 1 ): 237 .

Crossref PubMed Google Scholar
5. Find in article

Shirazi R , Shirazi-Adl A . Analysis of partial meniscectomy and ACL reconstruction in knee joint biomechanics under a combined loading . Clin Biomech (Bristol, Avon) . 2009 ; 24 ( 9 ): 755 – 761 .

Crossref PubMed Google Scholar
6. Find in article

Wellsandt E , Gardinier ES , Manal K , Axe MJ , Buchanan TS , Snyder-Mackler L . Decreased knee joint loading associated with early knee osteoarthritis after anterior cruciate ligament injury . Am J Sports Med . 2016 ; 44 ( 1 ): 143 – 151 .

Crossref PubMed Google Scholar
7. Find in article

Hill CL , Hunter DJ , Niu J , et al. Synovitis detected on magnetic resonance imaging and its relation to pain and cartilage loss in knee osteoarthritis . Ann Rheum Dis . 2007 ; 66 ( 12 ): 1599 – 1603 .

Crossref PubMed Google Scholar
8. Find in article

Hill CL , Gale DG , Chaisson CE , et al. Knee effusions, popliteal cysts, and synovial thickening: association with knee pain in osteoarthritis . J Rheumatol . 2001 ; 28 ( 6 ): 1330 – 1337 .

PubMed Google Scholar
9. Find in article

Sanchez-Lopez E , Coras R , Torres A , Lane NE , Guma M . Synovial inflammation in osteoarthritis progression . Nat Rev Rheumatol . 2022 ; 18 ( 5 ): 258 – 275 .

Crossref PubMed Google Scholar
10. Find in article

Wang M , Tan G , Jiang H , et al. Molecular crosstalk between articular cartilage, meniscus, synovium, and subchondral bone in osteoarthritis . Bone Joint Res . 2022 ; 11 ( 12 ): 862 – 872 .

Crossref PubMed Google Scholar
11. Find in article

Theocharis AD , Skandalis SS , Gialeli C , Karamanos NK . Extracellular matrix structure . Adv Drug Deliv Rev . 2016 ; 97 : 4 – 27 .

Crossref PubMed Google Scholar
12. Find in article

Urbanczyk M , Layland SL , Schenke-Layland K . The role of extracellular matrix in biomechanics and its impact on bioengineering of cells and 3D tissues . Matrix Biol . 2020 ; 85–86 : 1 – 14 .

Crossref PubMed Google Scholar
13. Find in article

Felson DT . Osteoarthritis as a disease of mechanics . Osteoarthritis Cartilage . 2013 ; 21 ( 1 ): 10 – 15 .

Crossref PubMed Google Scholar
14. Find in article

Klees RF , Salasznyk RM , Kingsley K , Williams WA , Boskey A , Plopper GE . Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway . Mol Biol Cell . 2005 ; 16 ( 2 ): 881 – 890 .

Crossref PubMed Google Scholar
15. Find in article

Du J , Zu Y , Li J , et al. Extracellular matrix stiffness dictates Wnt expression through integrin pathway . Sci Rep . 2016 ; 6 ( 1 ): 20395 .

Crossref PubMed Google Scholar
16. Find in article

Allen JL , Cooke ME , Alliston T . ECM stiffness primes the TGFβ pathway to promote chondrocyte differentiation . Mol Biol Cell . 2012 ; 23 ( 18 ): 3731 – 3742 .

Crossref PubMed Google Scholar
17. Find in article

Wijelath ES , Rahman S , Namekata M , et al. Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain . Circ Res . 2006 ; 99 ( 8 ): 853 – 860 .

Crossref PubMed Google Scholar
18. Find in article

Thomas CM , Murray R , Sharif M . Chondrocyte apoptosis determined by caspase-3 expression varies with fibronectin distribution in equine articular cartilage . Int J Rheum Dis . 2011 ; 14 ( 3 ): 290 – 297 .

Crossref PubMed Google Scholar
19. Find in article

McCoy AM . Animal models of osteoarthritis: comparisons and key considerations . Vet Pathol . 2015 ; 52 ( 5 ): 803 – 818 .

Crossref PubMed Google Scholar
20. Find in article

Teeple E , Jay GD , Elsaid KA , Fleming BC . Animal models of osteoarthritis: challenges of model selection and analysis . AAPS J . 2013 ; 15 ( 2 ): 438 – 446 .

Crossref PubMed Google Scholar
21. Find in article

Page MJ , McKenzie JE , Bossuyt PM , et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews . BMJ . 2021 ; 372 : 71 .

Crossref PubMed Google Scholar
22. Find in article

No authors listed . National Library of Medicine . ( date last accessed 28 October 2024 ).

https://www.nlm.nih.gov/mesh/meshhome.html Google Scholar
23. Find in article

Poulet B , de Souza R , Kent AV , et al. Intermittent applied mechanical loading induces subchondral bone thickening that may be intensified locally by contiguous articular cartilage lesions . Osteoarthritis Cartilage . 2015 ; 23 ( 6 ): 940 – 948 .

Crossref PubMed Google Scholar
24. Find in article

Zhu J , Zhu Y , Xiao W , Hu Y , Li Y . Instability and excessive mechanical loading mediate subchondral bone changes to induce osteoarthritis . Ann Transl Med . 2020 ; 8 ( 6 ): 350 .

Crossref PubMed Google Scholar
25. Find in article

Kalu DN . The ovariectomized rat model of postmenopausal bone loss . Bone Miner . 1991 ; 15 ( 3 ): 175 – 191 .

Crossref PubMed Google Scholar
26. Find in article

Yousefzadeh N , Kashfi K , Jeddi S , Ghasemi A . Ovariectomized rat model of osteoporosis: a practical guide . EXCLI J . 2020 ; 19 : 89 – 107 .

Crossref PubMed Google Scholar
27. Find in article

DiFrancesco L , Sokoloff L . Lipochondral degeneration of capsular tissue in osteoarthritic hips . Am J Surg Pathol . 1995 ; 19 ( 3 ): 278 – 283 .

Crossref PubMed Google Scholar
28. Find in article

Campbell TM , Trudel G , Laneuville O . Knee flexion contractures in patients with osteoarthritis: clinical features and histologic characterization of the posterior capsule . PM R . 2015 ; 7 ( 5 ): 466 – 473 .

Crossref PubMed Google Scholar
29. Find in article

Limberg AK , Salib CG , Tibbo ME , et al. Immune cell populations differ in patients undergoing revision total knee arthroplasty for arthrofibrosis . Sci Rep . 2022 ; 12 ( 1 ): 22627 .

Crossref PubMed Google Scholar
30. Find in article

Voelker A , Schroeter F , Steinke H , Heyde CE . Degeneration of the lumbar spine and its relation to the expression of collagen and elastin in facet joint capsules and ligament flavum . Acta Orthop Traumatol Turc . 2022 ; 56 ( 3 ): 210 – 216 .

Crossref PubMed Google Scholar
31. Find in article

Herbert C , Jayson MI , Bailey AJ . Joint capsule collagen in osteoarthrosis . Ann Rheum Dis . 1973 ; 32 ( 6 ): 510 – 514 .

Crossref PubMed Google Scholar
32. Find in article

Cameron HU , Macnab I . Scanning electron microscopic studies of the hip joint capsule and synovial membrane . Can J Surg . 1973 ; 16 : 388 – 392 .

PubMed Google Scholar
33. Find in article

Heinegård D , Hernborg J , Lundberg BJ . The glycosaminoglycans of the human joint capsule: isolation and characterizaion . Arthritis Rheum . 1968 ; 11 ( 6 ): 787 – 795 .

Crossref PubMed Google Scholar
34. Find in article

Belluzzi E , Macchi V , Fontanella CG , et al. Infrapatellar fat pad gene expression and protein production in patients with and without osteoarthritis . Int J Mol Sci . 2020 ; 21 ( 17 ): 6016 .

Crossref PubMed Google Scholar
35. Find in article

Grevenstein D , Heilig J , Dargel J , et al. COMP in the infrapatellar fat pad-results of a prospective histological, immunohistological, and biochemical case-control study . J Orthop Res . 2020 ; 38 ( 4 ): 747 – 758 .

Crossref PubMed Google Scholar
36. Find in article

Cheng XG , Brys P , Nijs J , et al. Radiological prevalence of lumbar intervertebral disc calcification in the elderly: an autopsy study . Skel Radiol . 1996 ; 25 ( 3 ): 231 – 235 .

Crossref PubMed Google Scholar
37. Find in article

Kumagai K , Sakai K , Kusayama Y , et al. The extent of degeneration of cruciate ligament is associated with chondrogenic differentiation in patients with osteoarthritis of the knee . Osteoarthr Cartil . 2012 ; 20 ( 11 ): 1258 – 1267 .

Crossref PubMed Google Scholar
38. Find in article

Komro J , Gonzales J , Marberry K , Main DC , Cramberg M , Kondrashov P . Fibrocartilaginous metaplasia and neovascularization of the anterior cruciate ligament in patients with osteoarthritis . Clin Anat . 2020 ; 33 ( 6 ): 899 – 905 .

Crossref PubMed Google Scholar
39. Find in article

Nakamura Y , Ogawa H , Sohmiya K , et al. Relationship between histological changes of the anterior cruciate ligament and knee function in osteoarthritis patients . Orthop Traumatol Surg Res . 2022 ; 108 ( 8 ): 103341 .

Crossref PubMed Google Scholar
40. Find in article

Akisue T , Stulberg BN , Bauer TW , McMahon JT , Wilde AH , Kurosaka M . Histologic evaluation of posterior cruciate ligaments from osteoarthritic knees . Clin Orthop Relat Res . 2002 ; 400 : 165 – 173 .

Crossref PubMed Google Scholar
41. Find in article

Zhu J , Zhang X , Ma Y , Zhou C , Ao Y . Ultrastructural and morphological characteristics of human anterior cruciate ligament and hamstring tendons . Anat Rec (Hoboken) . 2012 ; 295 ( 9 ): 1430 – 1436 .

Crossref PubMed Google Scholar
42. Find in article

Levy YD , Hasegawa A , Patil S , Koziol JA , Lotz MK , D’Lima DD . Histopathological changes in the human posterior cruciate ligament during aging and osteoarthritis: correlations with anterior cruciate ligament and cartilage changes . Ann Rheum Dis . 2013 ; 72 ( 2 ): 271 – 277 .

Crossref PubMed Google Scholar
43. Find in article

Marczak D , Kowalczewski J , Okoń T , Synder M , Sibiński M . An evaluation of the posterior cruciate ligament function in total knee arthroplasty with regard to its morphology and clinical properties . Folia Morphol (Warsz) . 2017 ; 76 ( 1 ): 94 – 99 .

Crossref PubMed Google Scholar
44. Find in article

Nakahara H , Hasegawa A , Otabe K , et al. Transcription factor Mohawk and the pathogenesis of human anterior cruciate ligament degradation . Arthritis Rheum . 2013 ; 65 ( 8 ): 2081 – 2089 .

Crossref PubMed Google Scholar
45. Find in article

Abdul Sahib NS , Al-Sharqi SAH , Wahab MS . Study histopathological changes in the anterior and posterior cruciate ligament after knee replacement: correlations with vitamin D, calcium and c-reactive protein in iraqi patients with osteoarthritis . Pak J Biotechnol . 2017 ; 14 : 393 – 400 .

Google Scholar
46. Find in article

Allain J , Goutallier D , Voisin MC . Macroscopic and histological assessments of the cruciate ligaments in arthrosis of the knee . Acta Orthop Scand . 2001 ; 72 ( 3 ): 266 – 269 .

Crossref PubMed Google Scholar
47. Find in article

Martins GC , Camanho G , Rodrigues MI , Filho LFM , Demange MK . Histopathological analysis of the posterior cruciate ligament in primary osteoarthritis . Eur J Orthop Surg Traumatol . 2018 ; 28 ( 4 ): 691 – 699 .

Crossref PubMed Google Scholar
48. Find in article

Nelissen RG , Hogendoorn PC . Retain or sacrifice the posterior cruciate ligament in total knee arthroplasty? A histopathological study of the cruciate ligament in osteoarthritic and rheumatoid disease . J Clin Pathol . 2001 ; 54 ( 5 ): 381 – 384 .

Crossref PubMed Google Scholar
49. Find in article

Rajgopal A , Vasdev N , Pathak A , Gautam D , Vasdev A . Histological changes and neural elements in the posterior cruciate ligament in osteoarthritic knees . J Orthop Surg (Hong Kong) . 2014 ; 22 ( 2 ): 142 – 145 .

Crossref PubMed Google Scholar
50. Find in article

Tokumoto M , Nakasa T , Shirakawa Y , et al. The role of substance P on maintaining ligament homeostasis by inhibiting endochondral ossification during osteoarthritis progression . Connect Tissue Res . 2023 ; 64 ( 1 ): 82 – 92 .

Crossref PubMed Google Scholar
51. Find in article

Doerschuk SH , Hicks DG , Chinchilli VM , Pellegrini VD . Histopathology of the palmar beak ligament in trapeziometacarpal osteoarthritis . J Hand Surg Am . 1999 ; 24 ( 3 ): 496 – 504 .

Crossref PubMed Google Scholar
52. Find in article

Mobargha N , Ludwig C , Ladd AL , Hagert E . Ultrastructure and innervation of thumb carpometacarpal ligaments in surgical patients with osteoarthritis . Clin Orthop Relat Res . 2014 ; 472 ( 4 ): 1146 – 1154 .

Crossref PubMed Google Scholar
53. Find in article

Suga Y , Shigematsu H , Tanaka M , et al. Factors associated with the increased risk of atlantoaxial osteoarthritis: a retrospective study . Eur Spine J . 2022 ; 31 ( 12 ): 3418 – 3425 .

Crossref PubMed Google Scholar
54. Find in article

Sun Y , Mauerhan DR , Kneisl JS , et al. Histological examination of collagen and proteoglycan changes in osteoarthritic menisci . Open Rheumatol J . 2012 ; 6 ( 1 ): 24 – 32 .

Crossref PubMed Google Scholar
55. Find in article

Kodama Y , Furumatsu T , Maehara A , Ozaki T . Composition of cell clusters in torn menisci and their extracellular matrix components . Acta Med Okayama . 2018 ; 72 ( 5 ): 499 – 506 .

Crossref PubMed Google Scholar
56. Find in article

Numpaisal PO , Jiang CC , Hsieh CH , Chiang H , Chien CL . Prospective application of partially digested autologous chondrocyte for meniscus tissue engineering . Pharmaceutics . 2022 ; 14 ( 3 ): 605 .

Crossref PubMed Google Scholar
57. Find in article

Melrose J , Fuller ES , Roughley PJ , et al. Fragmentation of decorin, biglycan, lumican and keratocan is elevated in degenerate human meniscus, knee and hip articular cartilages compared with age-matched macroscopically normal and control tissues . Arthritis Res Ther . 2008 ; 10 ( 4 ): R79 .

Crossref PubMed Google Scholar
58. Find in article

Battistelli M , Favero M , Burini D , et al. Morphological and ultrastructural analysis of normal, injured and osteoarthritic human knee menisci . Eur J Histochem . 2019 ; 63 ( 1 ): 11 .

Crossref PubMed Google Scholar
59. Find in article

McDaniel D , Tilton E , Dominick K , et al. Histological characteristics of knee menisci in patients with osteoarthritis . Clin Anat . 2017 ; 30 ( 6 ): 805 – 810 .

Crossref PubMed Google Scholar
60. Find in article

Hellberg I , Karjalainen V-P , Finnilä MAJ , et al. 3D analysis and grading of calcifications from ex vivo human meniscus . Osteoarthritis Cartilage . 2023 ; 31 ( 4 ): 482 – 492 .

Crossref PubMed Google Scholar
61. Find in article

Abraham AC , Pauly HM , Donahue TLH . Deleterious effects of osteoarthritis on the structure and function of the meniscal enthesis . Osteoarthritis Cartilage . 2014 ; 22 ( 2 ): 275 – 283 .

Crossref PubMed Google Scholar
62. Find in article

Dessombz A , Nguyen C , Ea H-K , et al. Combining μX-ray fluorescence, μXANES and μXRD to shed light on Zn2+ cations in cartilage and meniscus calcifications . J Trace Elem Med Biol . 2013 ; 27 ( 4 ): 326 – 333 .

Crossref PubMed Google Scholar
63. Find in article

Johnson K , Hashimoto S , Lotz M , Pritzker K , Goding J , Terkeltaub R . Up-regulated expression of the phosphodiesterase nucleotide pyrophosphatase family member PC-1 is a marker and pathogenic factor for knee meniscal cartilage matrix calcification . Arthritis Rheum . 2001 ; 44 ( 5 ): 1071 – 1081 .

Crossref PubMed Google Scholar
64. Find in article

Kiraly AJ , Roberts A , Cox M , Mauerhan D , Hanley E , Sun Y . Comparison of meniscal cell-mediated and chondrocyte-mediated calcification . Open Orthop J . 2017 ; 11 : 225 – 233 .

Crossref PubMed Google Scholar
65. Find in article

López-Franco M , López-Franco O , Murciano-Antón MA , et al. Meniscal degeneration in human knee osteoarthritis: in situ hybridization and immunohistochemistry study . Arch Orthop Trauma Surg . 2016 ; 136 ( 2 ): 175 – 183 .

Crossref PubMed Google Scholar
66. Find in article

Park DY , Min B-H , Choi BH , et al. The degeneration of meniscus roots is accompanied by fibrocartilage formation, which may precede meniscus root tears in osteoarthritic knees . Am J Sports Med . 2015 ; 43 ( 12 ): 3034 – 3044 .

Crossref PubMed Google Scholar
67. Find in article

Sun Y , Mauerhan DR , Honeycutt PR , et al. Calcium deposition in osteoarthritic meniscus and meniscal cell culture . Arthritis Res Ther . 2010 ; 12 ( 2 ): R56 .

Crossref PubMed Google Scholar
68. Find in article

Takahashi M , Suzuki M , Kushida K , Hoshino H , Inoue T . The effect of aging and osteoarthritis on the mature and senescent cross-links of collagen in human meniscus . Arthroscopy . 1998 ; 14 ( 4 ): 366 – 372 .

Crossref PubMed Google Scholar
69. Find in article

Zhang D , Cheriyan T , Martin SD , Schmid TM , Spector M . Lubricin distribution in the menisci and labra of human osteoarthritic joints . Cartilage . 2012 ; 3 ( 2 ): 165 – 172 .

Crossref PubMed Google Scholar
70. Find in article

Prokopi N , Andrikopoulos KS , Beobide AS , Voyiatzis GA , Papachristou DJ . Collagen orientation probed by polarized Raman spectra can serve as differential diagnosis indicator between different grades of meniscus degeneration . Sci Rep . 2021 ; 11 ( 1 ): 20299 .

Crossref PubMed Google Scholar
71. Find in article

Sirotti S , Becce F , Sconfienza LM , et al. Reliability and diagnostic accuracy of radiography for the diagnosis of calcium pyrophosphate deposition: performance of the novel definitions developed by an international multidisciplinary working group . Arthritis Rheumatol . 2023 ; 75 ( 4 ): 630 – 638 .

Crossref PubMed Google Scholar
72. Find in article

Roller BL , Monibi FA , Stoker AM , Kuroki K , Bal BS , Cook JL . Characterization of knee meniscal pathology: correlation of gross, histologic, biochemical, molecular, and radiographic measures of disease . J Knee Surg . 2015 ; 28 ( 2 ): 175 – 182 .

Crossref PubMed Google Scholar
73. Find in article

Ghosh P , Ingman AM , Taylor TK . Variations in collagen, non-collagenous proteins, and hexosamine in menisci derived from osteoarthritic and rheumatoid arthritic knee joints . J Rheumatol . 1975 ; 2 ( 1 ): 100 – 107 .

PubMed Google Scholar
74. Find in article

Son M , Goodman SB , Chen W , Hargreaves BA , Gold GE , Levenston ME . Regional variation in T1ρ and T2 times in osteoarthritic human menisci: correlation with mechanical properties and matrix composition . Osteoarthritis Cartilage . 2013 ; 21 ( 6 ): 796 – 805 .

Crossref PubMed Google Scholar
75. Find in article

Warnecke D , Balko J , Haas J , et al. Degeneration alters the biomechanical properties and structural composition of lateral human menisci . Osteoarthritis Cartilage . 2020 ; 28 ( 11 ): 1482 – 1491 .

Crossref PubMed Google Scholar
76. Find in article

Mine T , Ihara K , Kawamura H , Date R , Umehara K . Collagen expression in various degenerative meniscal changes: an immunohistological study . J Orthop Surg (Hong Kong) . 2013 ; 21 ( 2 ): 216 – 220 .

Crossref PubMed Google Scholar
77. Find in article

Sladojević I , Krivokuća Z , Gajanin V , Manojlović S . Expression of collagen type I in unaltered and osteoarthritic menisci of knee joint . Med Pregl . 2016 ; 69 ( 1–2 ): 16 – 23 .

Crossref PubMed Google Scholar
78. Find in article

Hino T , Furumatsu T , Miyazawa S , et al. A histological study of the medial meniscus posterior root tibial insertion . Connect Tissue Res . 2020 ; 61 ( 6 ): 546 – 553 .

Crossref PubMed Google Scholar
79. Find in article

Ishizuka S , Sakai T , Hiraiwa H , et al. Hypoxia-inducible factor-2α induces expression of type X collagen and matrix metalloproteinases 13 in osteoarthritic meniscal cells . Inflamm Res . 2016 ; 65 ( 6 ): 439 – 448 .

Crossref PubMed Google Scholar
80. Find in article

Katsuragawa Y , Saitoh K , Tanaka N , et al. Changes of human menisci in osteoarthritic knee joints . Osteoarthritis Cartilage . 2010 ; 18 ( 9 ): 1133 – 1143 .

Crossref PubMed Google Scholar
81. Find in article

Jacquet C , Erivan R , Argenson JN , Parratte S , Ollivier M . Effect of 3 preservation methods (freezing, cryopreservation, and freezing + irradiation) on human menisci ultrastructure: an ex vivo comparative study with fresh tissue as a gold standard . Am J Sports Med . 2018 ; 46 ( 12 ): 2899 – 2904 .

Crossref PubMed Google Scholar
82. Find in article

Karjalainen V-P , Kestilä I , Finnilä MA , et al. Quantitative three-dimensional collagen orientation analysis of human meniscus posterior horn in health and osteoarthritis using micro-computed tomography . Osteoarthritis Cartilage . 2021 ; 29 ( 5 ): 762 – 772 .

Crossref PubMed Google Scholar
83. Find in article

Atik OŞ , Erdoğan D , Seymen CM , Bozkurt HH , Kaplanoğlu GT . Is there crosstalk between subchondral bone, cartilage, and meniscus in the pathogenesis of osteoarthritis? Eklem Hast Cerr . 2016 ; 27 ( 2 ): 62 – 67 .

Crossref PubMed Google Scholar
84. Find in article

Haut Donahue TL , Pauly HM . Osteoarthritic meniscal entheses exhibit altered collagen fiber orientation . Connect Tissue Res . 2022 ; 63 ( 2 ): 151 – 155 .

Crossref PubMed Google Scholar
85. Find in article

Nagata N , Koshino T , Saito T . Up-regulation of CD44-positive cells in medial meniscus of medial compartmental osteoarthritis of the knee . Knee . 2000 ; 7 ( 1 ): 3 – 9 .

Crossref Google Scholar
86. Find in article

Wang J , Roberts S , Kuiper JH , et al. Characterization of regional meniscal cell and chondrocyte phenotypes and chondrogenic differentiation with histological analysis in osteoarthritic donor-matched tissues . Sci Rep . 2020 ; 10 ( 1 ): 21658 .

Crossref PubMed Google Scholar
87. Find in article

Gouldin AG , Patel NK , Golladay GJ , Puetzer JL . Advanced glycation end-product accumulation differs by location and sex in aged osteoarthritic human menisci . Osteoarthritis Cartilage . 2023 ; 31 ( 3 ): 363 – 373 .

Crossref PubMed Google Scholar
88. Find in article

Fischenich KM , Lewis J , Kindsfater KA , Bailey TS , Haut Donahue TL . Effects of degeneration on the compressive and tensile properties of human meniscus . J Biomech . 2015 ; 48 ( 8 ): 1407 – 1411 .

Crossref PubMed Google Scholar
89. Find in article

Kwok J , Grogan S , Meckes B , Arce F , Lal R , D’Lima D . Atomic force microscopy reveals age-dependent changes in nanomechanical properties of the extracellular matrix of native human menisci: implications for joint degeneration and osteoarthritis . Nanomedicine . 2014 ; 10 ( 8 ): 1777 – 1785 .

Crossref PubMed Google Scholar
90. Find in article

Pordzik J , Bernstein A , Mayr HO , et al. Analysis of proteoglycan content and biomechanical properties in arthritic and arthritis-free menisci . Appl Sci (Basel) . 2020 ; 10 ( 24 ): 9012 .

Crossref Google Scholar
91. Find in article

Fuhrmann IK , Steinhagen J , Rüther W , Schumacher U . Comparative immunohistochemical evaluation of the zonal distribution of extracellular matrix and inflammation markers in human meniscus in osteoarthritis and rheumatoid arthritis . Acta Histochem . 2015 ; 117 ( 3 ): 243 – 254 .

Crossref PubMed Google Scholar
92. Find in article

Monibi FA , Pannellini T , Otero M , Warren RF , Rodeo SA . Histologic and molecular features in pathologic human menisci from knees with and without osteoarthritis . J Orthop Res . 2022 ; 40 ( 2 ): 504 – 512 .

Crossref PubMed Google Scholar
93. Find in article

Karube S , Shoji H . Compositional changes of glycosaminoglycans of the human menisci with age and degenerative joint disease . Nippon Seikeigeka Gakkai Zasshi . 1982 ; 56 ( 1 ): 51 – 57 .

PubMed Google Scholar
94. Find in article

Masuda I , Ishikawa K , Usuku G . A histologic and immunohistochemical study of calcium pyrophosphate dihydrate crystal deposition disease . Clin Orthop Relat Res . 1991 ; 263 : 272 – 287 .

PubMed Google Scholar
95. Find in article

Musumeci G , Trovato FM , Loreto C , et al. Lubricin expression in human osteoarthritic knee meniscus and synovial fluid: a morphological, immunohistochemical and biochemical study . Acta Histochem . 2014 ; 116 ( 5 ): 965 – 972 .

Crossref PubMed Google Scholar
96. Find in article

Jacquet C , Erivan R , Sharma A , et al. Preservation methods influence the biomechanical properties of human lateral menisci: an ex vivo comparative study of 3 methods . Orthop J Sports Med . 2019 ; 7 ( 4 ): 2325967119841622 .

Crossref PubMed Google Scholar
97. Find in article

Folkesson E , Turkiewicz A , Ali N , et al. Proteomic comparison of osteoarthritic and reference human menisci using data-independent acquisition mass spectrometry . Osteoarthritis Cartilage . 2020 ; 28 ( 8 ): 1092 – 1101 .

Crossref PubMed Google Scholar
98. Find in article

Roller BL , Monibi F , Stoker AM , Bal BS , Stannard JP , Cook JL . Characterization of meniscal pathology using molecular and proteomic analyses . J Knee Surg . 2015 ; 28 ( 6 ): 496 – 505 .

Crossref PubMed Google Scholar
99. Find in article

Park J , Lee H-S , Go E-B , et al. Proteomic analysis of the meniscus cartilage in osteoarthritis . Int J Mol Sci . 2021 ; 22 ( 15 ): 8181 .

Crossref PubMed Google Scholar
100. Find in article

Fink B , Egl M , Singer J , Fuerst M , Bubenheim M , Neuen-Jacob E . Morphologic changes in the vastus medialis muscle in patients with osteoarthritis of the knee . Arthritis Rheum . 2007 ; 56 ( 11 ): 3626 – 3633 .

Crossref PubMed Google Scholar
101. Find in article

Noehren B , Kosmac K , Walton RG , et al. Alterations in quadriceps muscle cellular and molecular properties in adults with moderate knee osteoarthritis . Osteoarthritis Cartilage . 2018 ; 26 ( 10 ): 1359 – 1368 .

Crossref PubMed Google Scholar
102. Find in article

Serrão PR , Vasilceac FA , Gramani-Say K , et al. Expression of receptors of advanced glycation end product (RAGE) and types I, III and IV collagen in the vastus lateralis muscle of men in early stages of knee osteoarthritis . Connect Tissue Res . 2014 ; 55 ( 5–6 ): 331 – 338 .

Crossref PubMed Google Scholar
103. Find in article

Mattiello-Sverzut AC , Petersen SG , Kjaer M , Mackey AL . Morphological adaptation of muscle collagen and receptor of advanced glycation end product (RAGE) in osteoarthritis patients with 12 weeks of resistance training: influence of anti-inflammatory or glucosamine treatment . Rheumatol Int . 2013 ; 33 ( 9 ): 2215 – 2224 .

Crossref PubMed Google Scholar
104. Find in article

Krawetz RJ , Wu YE , Bertram KL , et al. Synovial mesenchymal progenitor derived aggrecan regulates cartilage homeostasis and endogenous repair capacity . Cell Death Dis . 2022 ; 13 ( 5 ): 470 .

Crossref PubMed Google Scholar
105. Find in article

Rafael MS , Cavaco S , Viegas CSB , et al. Insights into the association of Gla‐rich protein and osteoarthritis, novel splice variants and γ‐carboxylation status . Mol Nutr Food Res . 2014 ; 58 ( 8 ): 1636 – 1646 .

Crossref PubMed Google Scholar
106. Find in article

Ea H-K , Chobaz V , Nguyen C , et al. Pathogenic role of basic calcium phosphate crystals in destructive arthropathies . PLoS One . 2013 ; 8 ( 2 ): e57352 .

Crossref PubMed Google Scholar
107. Find in article

Nakashima K , Koshino T , Saito T . Synovial immunohistochemical changes after high tibial osteotomy for osteoarthritis of the knee. Two-year prospective follow-up . Bull Hosp Jt Dis . 1998 ; 57 ( 4 ): 187 – 194 .

PubMed Google Scholar
108. Find in article

Saito I , Koshino T , Nakashima K , Uesugi M , Saito T . Increased cellular infiltrate in inflammatory synovia of osteoarthritic knees . Osteoarthritis Cartilage . 2002 ; 10 ( 2 ): 156 – 162 .

Crossref PubMed Google Scholar
109. Find in article

Richardot P , Charni-Ben Tabassi N , Toh L , et al. Nitrated type III collagen as a biological marker of nitric oxide-mediated synovial tissue metabolism in osteoarthritis . Osteoarthritis Cartilage . 2009 ; 17 ( 10 ): 1362 – 1367 .

Crossref PubMed Google Scholar
110. Find in article

Ene R , Sinescu RD , Ene P , Cîrstoiu MM , Cîrstoiu FC . Synovial inflammation in patients with different stages of knee osteoarthritis . Rom J Morphol Embryol . 2015 ; 56 ( 1 ): 169 – 173 .

PubMed Google Scholar
111. Find in article

Kaufmann J , Mueller A , Voigt A , et al. Hydroxypyridinium collagen crosslinks in serum, urine, synovial fluid and synovial tissue in patients with rheumatoid arthritis compared with osteoarthritis . Rheumatol (Oxford) . 2003 ; 42 ( 2 ): 314 – 320 .

Crossref PubMed Google Scholar
112. Find in article

Takahashi M , Kushida K , Hoshino H , et al. Concentrations of pyridinoline and deoxypyridinoline in joint tissues from patients with osteoarthritis or rheumatoid arthritis . Ann Rheum Dis . 1996 ; 55 ( 5 ): 324 – 327 .

Crossref PubMed Google Scholar
113. Find in article

Di Cesare PE , Fang C , Leslie MP , et al. Localization and expression of cartilage oligomeric matrix protein by human rheumatoid and osteoarthritic synovium and cartilage . J Orthop Res . 1999 ; 17 ( 3 ): 437 – 445 .

Crossref PubMed Google Scholar
114. Find in article

Cillero-Pastor B , Eijkel GB , Blanco FJ , Heeren RMA . Protein classification and distribution in osteoarthritic human synovial tissue by matrix-assisted laser desorption ionization mass spectrometry imaging . Anal Bioanal Chem . 2015 ; 407 ( 8 ): 2213 – 2222 .

Crossref PubMed Google Scholar
115. Find in article

Cutolo M , Picasso M , Ponassi M , Sun MZ , Balza E . Tenascin and fibronectin distribution in human normal and pathological synovium . J Rheumatol . 1992 ; 19 ( 9 ): 1439 – 1447 .

PubMed Google Scholar
116. Find in article

Fan L , Wang Q , Liu R , et al. Citrullinated fibronectin inhibits apoptosis and promotes the secretion of pro-inflammatory cytokines in fibroblast-like synoviocytes in rheumatoid arthritis . Arthritis Res Ther . 2012 ; 14 ( 6 ): R266 .

Crossref PubMed Google Scholar
117. Find in article

Kragstrup TW , Sohn DH , Lepus CM , et al. Fibroblast-like synovial cell production of extra domain A fibronectin associates with inflammation in osteoarthritis . BMC Rheumatol . 2019 ; 3 : 46 .

Crossref PubMed Google Scholar
118. Find in article

Nikkari L , Haapasalmi K , Aho H , et al. Localization of the alpha V subfamily of integrins and their putative ligands in synovial lining cell layer . J Rheumatol . 1995 ; 22 ( 1 ): 16 – 23 .

PubMed Google Scholar
119. Find in article

Nishida K , Inoue H , Toda K , Murakami T . Localization of the glycosaminoglycans in the synovial tissues from osteoarthritic knees . Acta Med Okayama . 1995 ; 49 ( 6 ): 287 – 294 .

Crossref PubMed Google Scholar
120. Find in article

Wang X , Dong C , Li N , et al. Modulation of TGF‑β activity by latent TGF‑β‑binding protein 1 in human osteoarthritis fibroblast‑like synoviocytes . Mol Med Rep . 2018 ; 17 : 1893 – 1900 .

Crossref PubMed Google Scholar
121. Find in article

Turdean SG , Jung I , Gurzu S , et al. Histopathological evaluation and expression of the pluripotent mesenchymal stem cell-like markers CD105 and CD44 in the synovial membrane of patients with primary versus secondary hip osteoarthritis . J Investig Med . 2017 ; 65 ( 2 ): 363 – 369 .

Crossref PubMed Google Scholar
122. Find in article

Konttinen YT , Li TF , Mandelin J , et al. Hyaluronan synthases, hyaluronan, and its CD44 receptor in tissue around loosened total hip prostheses . J Pathol . 2001 ; 194 ( 3 ): 384 – 390 .

Crossref PubMed Google Scholar
123. Find in article

Christensen AF , Sorensen GL , Junker K , et al. Site-specific absence of microfibrillar-associated protein 4 (MFAP4) from the internal elastic membrane of arterioles in the rheumatoid arthritis synovial membrane: an immunohistochemical study in patients with advanced rheumatoid arthritis versus osteoarthritis . APMIS . 2019 ; 127 ( 8 ): 588 – 593 .

Crossref PubMed Google Scholar
124. Find in article

Li TF , Xu JW , Santavirta S , et al. Distribution of fibronectins and their integrin receptors in interface tissue from aseptic loosening of hip prostheses . Clin Exp Rheumatol . 2000 ; 18 ( 2 ): 221 – 225 .

PubMed Google Scholar
125. Find in article

Konttinen YT , Li TF , Xu JW , et al. Expression of laminins and their integrin receptors in different conditions of synovial membrane and synovial membrane-like interface tissue . Ann Rheum Dis . 1999 ; 58 ( 11 ): 683 – 690 .

Crossref PubMed Google Scholar
126. Find in article

van Linthoudt D , Beutler A , Clayburne G , Sieck M , Fernandes L , Schumacher HR . Morphometric studies on synovium in advanced osteoarthritis: is there an association between apatite-like material and collagen deposits? Clin Exp Rheumatol . 1997 ; 15 ( 5 ): 493 – 497 .

PubMed Google Scholar
127. Find in article

Pollock LE , Lalor P , Revell PA . Type IV collagen and laminin in the synovial intimal layer: an immunohistochemical study . Rheumatol Int . 1990 ; 9 ( 6 ): 277 – 280 .

Crossref PubMed Google Scholar
128. Find in article

Mapp PI , Revell PA . Fibronectin production by synovial intimal cells . Rheumatol Int . 1985 ; 5 ( 5 ): 229 – 237 .

Crossref PubMed Google Scholar
129. Find in article

Scott DL , Wainwright AC , Walton KW , Williamson N . Significance of fibronectin in rheumatoid arthritis and osteoarthrosis . Ann Rheum Dis . 1981 ; 40 ( 2 ): 142 – 153 .

Crossref PubMed Google Scholar
130. Find in article

Worrall JG , Wilkinson LS , Bayliss MT , Edwards JCW . Zonal distribution of chondroitin-4-sulphate/dermatan sulphate and chondroitin-6-sulphate in normal and diseased human synovium . Ann Rheum Dis . 1994 ; 53 ( 1 ): 35 – 38 .

Crossref PubMed Google Scholar
131. Find in article

Rinaldi N , Barth TF , Weis D , et al. Loss of laminin and of the laminin receptor integrin subunit alpha 6 in situ correlates with cytokine induced down regulation of alpha 6 on fibroblast-like synoviocytes from rheumatoid arthritis . Ann Rheum Dis . 1998 ; 57 ( 9 ): 559 – 565 .

Crossref PubMed Google Scholar
132. Find in article

Dijkgraaf LC , Liem RSB , de Bont LGM . Ultrastructural characteristics of the synovial membrane in osteoarthritic temporomandibular joints . J Oral Maxillofac Surg . 1997 ; 55 ( 11 ): 1269 – 1279 .

Crossref PubMed Google Scholar
133. Find in article

Okamoto K , Kiga N , Shinohara Y , Tojyo I , Fujita S . Effect of interleukin-1beta and dehydroepiandrosterone on the expression of lumican and fibromodulin in fibroblast-like synovial cells of the human temporomandibular joint . Eur J Histochem . 2015 ; 59 ( 1 ): 2440 .

Crossref PubMed Google Scholar
134. Find in article

Schneider M , Voss B , Rauterberg J , et al. Basement membrane proteins in synovial membrane: distribution in rheumatoid arthritis and synthesis by fibroblast-like cells . Clin Rheumatol . 1994 ; 13 ( 1 ): 90 – 97 .

Crossref PubMed Google Scholar
135. Find in article

Klareskog L , Johnell O , Hulth A , Holmdahl R , Rubin K . Reactivity of monoclonal anti‐type II collagen antibodies with cartilage and synovial tissue in rheumatoid arthritis and osteoarthritis . Arthritis Rheum . 1986 ; 29 ( 6 ): 730 – 738 .

Crossref PubMed Google Scholar
136. Find in article

Scott DL , Salmon M , Morris CJ , Wainwright AC , Walton KW . Laminin and vascular proliferation in rheumatoid arthritis . Ann Rheum Dis . 1984 ; 43 ( 4 ): 551 – 555 .

Crossref PubMed Google Scholar
137. Find in article

Chang X , Yamada R , Suzuki A , Kochi Y , Sawada T , Yamamoto K . Citrullination of fibronectin in rheumatoid arthritis synovial tissue . Rheumatology (Oxford) . 2005 ; 44 ( 11 ): 1374 – 1382 .

Crossref PubMed Google Scholar
138. Find in article

Hino K , Shiozawa S , Kuroki Y , et al. EDA-containing fibronectin is synthesized from rheumatoid synovial fibroblast-like cells . Arthritis Rheum . 1995 ; 38 ( 5 ): 678 – 683 .

Crossref PubMed Google Scholar
139. Find in article

Kriegsmann J , Berndt A , Hansen T , et al. Expression of fibronectin splice variants and oncofetal glycosylated fibronectin in the synovial membranes of patients with rheumatoid arthritis and osteoarthritis . Rheumatol Int . 2004 ; 24 ( 1 ): 25 – 33 .

Crossref PubMed Google Scholar
140. Find in article

Itokazu M , Shinozaki M , Ohno T . Quantitative analysis of hyaluronan in the synovial tissues of patients with joint disorders . Clin Rheumatol . 1998 ; 17 ( 3 ): 261 – 262 .

Crossref PubMed Google Scholar
141. Find in article

Santiago B , Baleux F , Palao G , et al. CXCL12 is displayed by rheumatoid endothelial cells through its basic amino-terminal motif on heparan sulfate proteoglycans . Arthritis Res Ther . 2006 ; 8 ( 2 ): R43 .

Crossref PubMed Google Scholar
142. Find in article

Poduval P , Sillat T , Virtanen I , Dabagh M , Konttinen YT . Immigration check for neutrophils in RA lining: laminin alpha5 low expression regions act as exit points . Scand J Rheumatol . 2010 ; 39 ( 2 ): 132 – 140 .

Crossref PubMed Google Scholar
143. Find in article

Ren X , Geng M , Xu K , et al. Quantitative proteomic analysis of synovial tissue reveals that upregulated OLFM4 aggravates inflammation in rheumatoid arthritis . J Proteome Res . 2021 ; 20 ( 10 ): 4746 – 4757 .

Crossref PubMed Google Scholar
144. Find in article

Worrall JG , Bayliss MT , Edwards JCW . Morphological localization of hyaluronan in normal and diseased synovium . J Rheumatol . 1991 ; 18 ( 10 ): 1466 – 1472 .

PubMed Google Scholar
145. Find in article

Meknas K , Johansen O , Steigen SE , Olsen R , Jørgensen L , Kartus J . Could tendinosis be involved in osteoarthritis? Scand J Med Sci Sports . 2012 ; 22 ( 5 ): 627 – 634 .

Crossref PubMed Google Scholar
146. Find in article

Ibrahim M , Kartus JT , Steigen SE , Olsen R , Meknas K . More tendon degeneration in patients with shoulder osteoarthritis . Knee Surg Sports Traumatol Arthrosc . 2019 ; 27 ( 1 ): 267 – 275 .

Crossref PubMed Google Scholar
147. Find in article

Expósito Molinero MR , de Miguel Mendieta E . Discriminant validity study of Achilles enthesis ultrasound . Reum Clin . 2016 ; 12 ( 4 ): 206 – 209 .

Crossref PubMed Google Scholar
148. Find in article

Mazzocca AD , McCarthy MBR , Ledgard FA , et al. Histomorphologic changes of the long head of the biceps tendon in common shoulder pathologies . Arthroscopy . 2013 ; 29 ( 6 ): 972 – 981 .

Crossref PubMed Google Scholar
149. Find in article

Ibrahim M , Hedlundh U , Sernert N , et al. Histological and ultrastructural degenerative findings in the gluteus medius tendon after hip arthroplasty . J Orthop Surg Res . 2021 ; 16 ( 1 ): 339 .

Crossref PubMed Google Scholar
150. Find in article

Loeser RF , Olex AL , McNulty MA , et al. Disease progression and phasic changes in gene expression in a mouse model of osteoarthritis . PLoS One . 2013 ; 8 ( 1 ): e54633 .

Crossref PubMed Google Scholar
151. Find in article

Ramos-Mucci L , Javaheri B , van’t Hof R , et al. Meniscal and ligament modifications in spontaneous and post-traumatic mouse models of osteoarthritis . Arthritis Res Ther . 2020 ; 22 ( 1 ): 171 .

Crossref PubMed Google Scholar
152. Find in article

Walton M . Degenerative joint disease in the mouse knee; radiological and morphological observations . J Pathol . 1977 ; 123 ( 2 ): 97 – 107 .

Crossref PubMed Google Scholar
153. Find in article

Anderson-MacKenzie JM , Billingham ME , Bailey AJ . Collagen remodeling in the anterior cruciate ligament associated with developing spontaneous murine osteoarthritis . Biochem Biophys Res Commun . 1999 ; 258 ( 3 ): 763 – 767 .

Crossref PubMed Google Scholar
154. Find in article

Cui P , Sun B-H , Dai Y-F , et al. Healing of the torn anterior horn of rabbit medial meniscus to bone after transtibial pull-out repair and autologous platelet-rich plasma gel injection . Orthop Surg . 2023 ; 15 ( 2 ): 617 – 627 .

Crossref PubMed Google Scholar
155. Find in article

Miller D , DeSutter C , Scott A , et al. Vascular structure and function in the medial collateral ligament of anterior cruciate ligament transected rabbit knees . J Orthop Res . 2014 ; 32 ( 9 ): 1104 – 1110 .

Crossref PubMed Google Scholar
156. Find in article

Funakoshi Y , Hariu M , Tapper JE , et al. Periarticular ligament changes following ACL/MCL transection in an ovine stifle joint model of osteoarthritis . J Orthop Res . 2007 ; 25 ( 8 ): 997 – 1006 .

Crossref PubMed Google Scholar
157. Find in article

Barton KI , Heard BJ , Kroker A , et al. Structural consequences of a partial anterior cruciate ligament injury on remaining joint integrity: evidence for ligament and bone changes over time in an ovine model . Am J Sports Med . 2021 ; 49 ( 3 ): 637 – 648 .

Crossref PubMed Google Scholar
158. Find in article

Bedingfield SK , Colazo JM , Di Francesco M , et al. Top-down fabricated microPlates for prolonged, intra-articular matrix metalloproteinase 13 siRNA nanocarrier delivery to reduce post-traumatic osteoarthritis . ACS Nano . 2021 ; 15 ( 9 ): 14475 – 14491 .

Crossref PubMed Google Scholar
159. Find in article

Muschter D , Fleischhauer L , Taheri S , Schilling AF , Clausen-Schaumann H , Grässel S . Sensory neuropeptides are required for bone and cartilage homeostasis in a murine destabilization-induced osteoarthritis model . Bone . 2020 ; 133 : 115181 .

Crossref PubMed Google Scholar
160. Find in article

Catheline SE , Bell RD , Oluoch LS , et al. IKKβ-NF-κB signaling in adult chondrocytes promotes the onset of age-related osteoarthritis in mice . Sci Signal . 2021 ; 14 ( 701 ): eabf3535 .

Crossref PubMed Google Scholar
161. Find in article

Lee KI , Gamini R , Olmer M , et al. Mohawk is a transcription factor that promotes meniscus cell phenotype and tissue repair and reduces osteoarthritis severity . Sci Transl Med . 2020 ; 12 ( 567 ): 28 .

Crossref PubMed Google Scholar
162. Find in article

Le Graverand MPH , Sciore P , Eggerer J . Formation and phenotype of cell clusters in osteoarthritic meniscus . Arthritis Rheum . 2001 ; 44 ( 8 ): 1808 – 1818 .

Crossref PubMed Google Scholar
163. Find in article

Hellio Le Graverand MP , Vignon E , Otterness IG , Hart DA . Early changes in lapine menisci during osteoarthritis development: Part I: Cellular and matrix alterations . Osteoarthritis Cartilage . 2001 ; 9 ( 1 ): 56 – 64 .

Crossref PubMed Google Scholar
164. Find in article

Zhao J , Huang S , Zheng J , et al. Changes of rabbit meniscus influenced by hyaline cartilage injury of osteoarthritis . Int J Clin Exp Med . 2014 ; 7 ( 9 ): 2948 – 2956 .

PubMed Google Scholar
165. Find in article

Levillain A , Magoariec H , Boulocher C , Decambron A , Viateau V , Hoc T . Viscoelastic properties of rabbit osteoarthritic menisci: A correlation with matrix alterations . J Mech Behav Biomed Mater . 2017 ; 65 : 1 – 10 .

Crossref PubMed Google Scholar
166. Find in article

Levillain A , Magoariec H , Boulocher C , Decambron A , Viateau V , Hoc T . Effects of a viscosupplementation therapy on rabbit menisci in an anterior cruciate ligament transection model of osteoarthritis . J Biomech . 2017 ; 58 : 147 – 154 .

Crossref PubMed Google Scholar
167. Find in article

Endo J , Sasho T , Akagi R , et al. Comparative analysis of gene expression between cartilage and menisci in early-phase osteoarthritis of the knee-an animal model study . J Knee Surg . 2018 ; 31 ( 7 ): 664 – 669 .

Crossref PubMed Google Scholar
168. Find in article

Bansal S , Miller LM , Patel JM , et al. Transection of the medial meniscus anterior horn results in cartilage degeneration and meniscus remodeling in a large animal model . J Orthop Res . 2020 ; 38 ( 12 ): 2696 – 2708 .

Crossref PubMed Google Scholar
169. Find in article

Bansal S , Meadows KD , Miller LM , et al. Six-month outcomes of clinically relevant meniscal injury in a large-animal model . Orthop J Sports Med . 2021 ; 9 ( 11 ): 23259671211035444 .

Crossref PubMed Google Scholar
170. Find in article

Shi X , Yu W , Wang T , et al. Electroacupuncture alleviates cartilage degradation: Improvement in cartilage biomechanics via pain relief and potentiation of muscle function in a rabbit model of knee osteoarthritis . Biomed Pharmacother . 2020 ; 123 : 109724 .

Crossref PubMed Google Scholar
171. Find in article

Lee K , Gang GG , Kang YG , Jung SS , Park HG , Jang JH . Alleviation of osteoarthritis-induced pain and motor deficits in rats by a novel device for the intramuscular insertion of cog polydioxanone filament . Appl Sci (Basel) . 2021 ; 11 ( 22 ): 10534 .

Crossref Google Scholar
172. Find in article

Tavallaee G , Lively S , Rockel JS , et al. Contribution of microRNA-27b-3p to synovial fibrotic responses in knee osteoarthritis . Arthritis Rheumatol . 2022 ; 74 ( 12 ): 1928 – 1942 .

Crossref PubMed Google Scholar
173. Find in article

Gamal N , Abou-Rabia NM , El Ebiary FH , Khalaf G , Raafat MH . The possible therapeutic role of platelet rich plasma on a model of osteoarthritis in male albino rat. Histological and immunohistochemical study . Egypt J Histol . 2019 ; 42 ( 3 ): 554 – 566 .

Crossref Google Scholar
174. Find in article

Zhang L , Zhang L , Huang Z , et al. Increased HIF-1α in knee osteoarthritis aggravate synovial fibrosis via fibroblast-like synoviocyte pyroptosis . Oxid Med Cell Longev . 2019 ; 2019 : 6326517 .

Crossref PubMed Google Scholar
175. Find in article

Zhang L , Li X , Zhang H , et al. Agnuside alleviates synovitis and fibrosis in knee osteoarthritis through the inhibition of HIF-1α and NLRP3 inflammasome . Mediators Inflamm . 2021 ; 2021 : 5534614 .

Crossref PubMed Google Scholar
176. Find in article

Li M , Zhang L , Liu Z , et al. Sanse powder essential oil nanoemulsion negatively regulates TRPA1 by AMPK/mTOR signaling in synovitis: knee osteoarthritis rat model and fibroblast-like synoviocyte isolates . Mediators Inflamm . 2021 ; 2021 : 4736670 .

Crossref PubMed Google Scholar
177. Find in article

Sriwatananukulkit O , Desclaux S , Tawonsawatruk T , et al. Effectiveness of losartan on infrapatellar fat pad/synovial fibrosis and pain behavior in the monoiodoacetate-induced rat model of osteoarthritis pain . Biomed Pharmacother . 2023 ; 158 : 114121 .

Crossref PubMed Google Scholar
178. Find in article

Zhang L , Xing R , Huang Z , et al. Inhibition of synovial macrophage pyroptosis alleviates synovitis and fibrosis in knee osteoarthritis . Mediators Inflamm . 2019 ; 2019 : 2165918 .

Crossref PubMed Google Scholar
179. Find in article

Zhang L , Li M , Li X , et al. Characteristics of sensory innervation in synovium of rats within different knee osteoarthritis models and the correlation between synovial fibrosis and hyperalgesia . J Adv Res . 2022 ; 35 : 141 – 151 .

Crossref PubMed Google Scholar
180. Find in article

Li X , Mei W , Huang Z , et al. Casticin suppresses monoiodoacetic acid-induced knee osteoarthritis through inhibiting HIF-1α/NLRP3 inflammasome signaling . Int Immunopharmacol . 2020 ; 86 : 106745 .

Crossref PubMed Google Scholar
181. Find in article

Almasry SM , Soliman HM , El-Tarhouny SA , Algaidi SA , Ragab EM . Platelet rich plasma enhances the immunohistochemical expression of platelet derived growth factor and vascular endothelial growth factor in the synovium of the meniscectomized rat models of osteoarthritis . Ann Anat . 2015 ; 197 : 38 – 49 .

Crossref PubMed Google Scholar
182. Find in article

Dai S , Liang T , Fujii T , et al. Increased elastic modulus of the synovial membrane in a rat ACLT model of osteoarthritis revealed by atomic force microscopy . Braz J Med Biol Res . 2020 ; 53 ( 11 ): e10058 .

Crossref PubMed Google Scholar
183. Find in article

Bryk M , Chwastek J , Mlost J , Kostrzewa M , Starowicz K . Sodium monoiodoacetate dose-dependent changes in matrix metalloproteinases and inflammatory components as prognostic factors for the progression of osteoarthritis . Front Pharmacol . 2021 ; 12 : 643605 .

Crossref PubMed Google Scholar
184. Find in article

Castrogiovanni P , Di Rosa M , Ravalli S , et al. Moderate physical activity as a prevention method for knee osteoarthritis and the role of synoviocytes as biological key . Int J Mol Sci . 2019 ; 20 ( 3 ): 511 .

Crossref PubMed Google Scholar
185. Find in article

Wei Q , Kong N , Liu X , et al. Pirfenidone attenuates synovial fibrosis and postpones the progression of osteoarthritis by anti-fibrotic and anti-inflammatory properties in vivo and in vitro . J Transl Med . 2021 ; 19 ( 1 ): 157 .

Crossref PubMed Google Scholar
186. Find in article

Lapadula G , Nico B , Cantatore FP , La Canna R , Roncali L , Pipitone V . Early ultrastructural changes of articular cartilage and synovial membrane in experimental vitamin A-induced osteoarthritis . J Rheumatol . 1995 ; 22 ( 10 ): 1913 – 1921 .

PubMed Google Scholar
187. Find in article

McErlain DD , Appleton CTG , Litchfield RB , et al. Study of subchondral bone adaptations in a rodent surgical model of OA using in vivo micro-computed tomography . Osteoarthritis Cartilage . 2008 ; 16 ( 4 ): 458 – 469 .

Crossref PubMed Google Scholar
188. Find in article

Dabrowska S , Ekiert-Radecka M , Karbowniczek J , et al. Calcification alters the viscoelastic properties of tendon fascicle bundles depending on matrix content . Acta Biomater . 2023 ; 166 : 360 – 374 .

Crossref PubMed Google Scholar
189. Find in article

Ricard-Blum S . The collagen family . Cold Spring Harb Perspect Biol . 2011 ; 3 ( 1 ): a004978 .

Crossref PubMed Google Scholar
190. Find in article

Chen D , Smith LR , Khandekar G , et al. Distinct effects of different matrix proteoglycans on collagen fibrillogenesis and cell-mediated collagen reorganization . Sci Rep . 2020 ; 10 ( 1 ): 19065 .

Crossref PubMed Google Scholar
191. Find in article

Naba A . Ten years of extracellular matrix proteomics: accomplishments, challenges, and future perspectives . Mol Cell Proteomics . 2023 ; 22 ( 4 ): 100528 .

Crossref PubMed Google Scholar
192. Find in article

Cope PJ , Ourradi K , Li Y , Sharif M . Models of osteoarthritis: the good, the bad and the promising . Osteoarthritis Cartilage . 2019 ; 27 ( 2 ): 230 – 239 .

Crossref PubMed Google Scholar
193. Find in article

Proffen BL , McElfresh M , Fleming BC , Murray MM . A comparative anatomical study of the human knee and six animal species . Knee . 2012 ; 19 ( 4 ): 493 – 499 .

Crossref PubMed Google Scholar
194. Find in article

Tschon M , Contartese D , Pagani S , Borsari V , Fini M . Gender and sex are key determinants in osteoarthritis not only confounding variables. A systematic review of clinical data . J Clin Med . 2021 ; 10 ( 14 ): 3178 .

Crossref PubMed Google Scholar
195. Find in article

Szilagyi IA , Waarsing JH , Schiphof D , van Meurs JBJ , Bierma-Zeinstra SMA . Towards sex-specific osteoarthritis risk models: evaluation of risk factors for knee osteoarthritis in males and females . Rheumatology (Oxford) . 2022 ; 61 ( 2 ): 648 – 657 .

Crossref PubMed Google Scholar
196. Find in article

Karp NA , Reavey N . Sex bias in preclinical research and an exploration of how to change the status quo . Br J Pharmacol . 2019 ; 176 ( 21 ): 4107 – 4118 .

Crossref PubMed Google Scholar
197. Find in article

Pucha KA , McKinney JM , Fuller JM , Willett NJ . Characterization of OA development between sexes in the rat medial meniscal transection model . Osteoarthr Cartil Open . 2020 ; 2 ( 3 ): 100066 .

Crossref PubMed Google Scholar
198. Find in article

Temp J , Labuz D , Negrete R , Sunkara V , Machelska H . Pain and knee damage in male and female mice in the medial meniscal transection-induced osteoarthritis . Osteoarthritis Cartilage . 2020 ; 28 ( 4 ): 475 – 485 .

Crossref PubMed Google Scholar
199. Find in article

Hwang HS , Park IY , Hong JI , Kim JR , Kim HA . Comparison of joint degeneration and pain in male and female mice in DMM model of osteoarthritis . Osteoarthritis Cartilage . 2021 ; 29 ( 5 ): 728 – 738 .

Crossref PubMed Google Scholar
200. Find in article

Malfait AM , Miller RE . Why we should study osteoarthritis pain in experimental models in both sexes . Osteoarthritis Cartilage . 2020 ; 28 ( 4 ): 397 – 399 .

Crossref PubMed Google Scholar
201. Find in article

Franke M , Mancino C , Taraballi F . Reasons for the sex bias in osteoarthritis research: a review of preclinical studies . Int J Mol Sci . 2023 ; 24 ( 12 ): 10386 .

Crossref PubMed Google Scholar
202. Find in article

Derfus BA , Kurian JB , Butler JJ , et al. The high prevalence of pathologic calcium crystals in pre-operative knees . J Rheumatol . 2002 ; 29 ( 3 ): 570 – 574 .

PubMed Google Scholar
203. Find in article

Mathes T , Klaßen P , Pieper D . Frequency of data extraction errors and methods to increase data extraction quality: a methodological review . BMC Med Res Methodol . 2017 ; 17 ( 1 ): 152 .

Crossref PubMed Google Scholar
204. Find in article

Buckley CD , Ospelt C , Gay S , Midwood KS . Location, location, location: how the tissue microenvironment affects inflammation in RA . Nat Rev Rheumatol . 2021 ; 17 ( 4 ): 195 – 212 .

Crossref PubMed Google Scholar
205. Find in article

Sharma L . Osteoarthritis of the knee . N Engl J Med . 2021 ; 384 ( 1 ): 51 – 59 .

Crossref PubMed Google Scholar
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