Low-energy impact of human cartilage: predictors for microcracking the network of collagen

Kaleem, B.; Maier, Franz Michael; Drissi, Hicham; Pierce, David M.

doi:10.1016/j.joca.2016.11.009

Cited by 23 publications

(21 citation statements)

References 46 publications

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“…The observations were done in the entire 100 µm‐section and in adjacent thick sections and were always confined to the necrotic areas. Furthermore, almost identical ripples and microsplits were observed using SHG in osteoarthritic cartilage and a similar fissure or microcrack was revealed by SHG in cartilage upon low‐energy impact . The findings were therefore assumed to be valid and not artifacts from sample preparation.…”

Section: Discussionmentioning

confidence: 56%

Characterization of cellular and matrix alterations in the early pathogenesis of osteochondritis dissecans in pigs using second harmonic generation and two‐photon excitation fluorescence microscopy

Finnøy

Olstad

Lilledahl

2018

Journal Orthopaedic Research

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Osteochondritis dissecans is a joint disease that is observed in several species. The disease can develop as a cause of ischemic chondronecrosis in the epiphyseal growth cartilage. Some lesions of chondronecrosis undergo spontaneous resolution, but it is not possible to predict whether a lesion will resolve or progress and require intervention. Proliferation of cells into clusters occurs at the lesion margin, but it is unclear if the clusters have a repair function. The aims of the current study were to examine clusters and potential matrix changes in response to ischemic chondronecrosis in the distal femur of 10 pigs aged 70-180 days using advanced microscopy based on two-photon excitation fluorescence and second harmonic generation. These microscopy techniques can perform 3D imaging of cells and collagen without staining. The results indicated a lower collagen density in the chondronecrotic areas compared to the normal growth cartilage, and fissures and breaks in the matrix integrity were demonstrated that potentially can propagate and cause osteochondritis dissecans. A higher number of cells in clusters was correlated with reduction in collagen density in the lesions. Some of the cells in the clusters had a morphology similar to progenitor cells, suggesting a potential repair role of the clusters. The study has shed further light on the secondary responses after initial lesion formation, which information can be of potential use to create models that can predict lesion progression and that may hence avoid unnecessary interventions in the future. © 2018 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res.

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Section: Discussionmentioning

confidence: 56%

Characterization of cellular and matrix alterations in the early pathogenesis of osteochondritis dissecans in pigs using second harmonic generation and two‐photon excitation fluorescence microscopy

Finnøy

Olstad

Lilledahl

2018

Journal Orthopaedic Research

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“…It has further been shown that tissue softening due to excessive loading can precede collagen denaturation, which seems logical since the interconnections between the collagen fibrils are weaker in tension than the fibrils themselves . Cartilage exhibits increased swelling and softening with higher loads, reveals more microcracks within the collagen network with higher impact energy or applied stress or stress rate, and levels of degraded collagen coincide with or come at a later stage than cell death indicating that this is also caused by excessive microstrains . The increased compliance within the tissue as a result of collagen network de‐structuring has the potential to affect chondrocyte metabolism and the microstructural response to compression.…”

Section: In Vitro Studies; Short‐term Resultsmentioning

confidence: 99%

Comparison between in vitro and in vivo cartilage overloading studies based on a systematic literature review

Nickien

Heuijerjans

Ito

et al. 2018

Journal Orthopaedic Research

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Methodological differences between in vitro and in vivo studies on cartilage overloading complicate the comparison of outcomes. The rationale of the current review was to (i) identify consistencies and inconsistencies between in vitro and in vivo studies on mechanically‐induced structural damage in articular cartilage, such that variables worth interesting to further explore using either one of these approaches can be identified; and (ii) suggest how the methodologies of both approaches may be adjusted to facilitate easier comparison and therewith stimulate translation of results between in vivo and in vitro studies. This study is anticipated to enhance our understanding of the development of osteoarthritis, and to reduce the number of in vivo studies. Generally, results of in vitro and in vivo studies are not contradicting. Both show subchondral bone damage and intact cartilage above a threshold value of impact energy. At lower loading rates, excessive loads may cause cartilage fissuring, decreased cell viability, collagen network de‐structuring, decreased GAG content, an overall damage increase over time, and low ability to recover. This encourages further improvement of in vitro systems, to replace, reduce, and/or refine in vivo studies. However, differences in experimental set up and analyses complicate comparison of results. Ways to bridge the gap include (i) bringing in vitro set‐ups closer to in vivo, for example, by aligning loading protocols and overlapping experimental timeframes; (ii) synchronizing analytical methods; and (iii) using computational models to translate conclusions from in vitro results to the in vivo environment and vice versa. © 2018 The Authors. Journal of Orthopaedic Research® Published by Wiley Periodicals, Inc. on behalf of the Orthopaedic Research Society. J Orthop Res 36:2076–2086, 2018.

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“…Based on preliminary studies, we selected LI ¼ 1.5e2.5 mJ/mm 3 and HI ¼ 2.5e4.0 mJ/mm 3 . Based on our previous work, 1 we selected the intended impact velocity v Ã imp ¼ 0:5 m/s. We calculated the required drop height h ¼ ðv Ã imp Þ 2 =2g, with g as gravitational acceleration.…”

Section: Low-energy Impactmentioning

confidence: 99%

“…4,5 While microcracks in bone have been characterized extensively, 6e10 and sub-millimeter-scale surface fissures in cartilage are well known for early to advanced osteoarthritis (OA), 11e14 we recently demonstrated that low-energy impact usually considered non-injurious can in fact cause micrometer-scale cracks (microcracks) in the collagen network of human cartilage. 1 In previous work we defined collagen-network microcracks as fractures in the collagen network that are no wider than the diameter of chondrocyte lacunae ( < 30 mm). 15,16 Furthermore, we probed the diminished functional response of cartilage under progressive cyclic loading 17 and found statistically significant microcracking under some loading conditions.…”

Section: Introductionmentioning

confidence: 99%

“…Microcracks also present in vivo, as seen by us and others, e.g., in mice with surgically induced OA 20 and in ICRS Grade-I human femoral cartilage. 21 In this study, we aimed to determine: (1) what combinations of impact and cyclic compression initiate microcracks in the network of collagen; and (2) whether and how cartilage microcracks propagate during cyclic, mechanical loading which simulates walking. Understanding these aims contributes understanding to the initial mechanisms of microscale damage in the network of collagen that may be a precursor to degradation characteristic of OA.…”

Section: Introductionmentioning

confidence: 99%

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Propagation of microcracks in collagen networks of cartilage under mechanical loads

Santos

Emery

Neu

et al. 2019

Osteoarthritis and Cartilage

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Objective: We recently demonstrated that low-energy mechanical impact to articular cartilage, usually considered non-injurious, can in fact cause microscale cracks (widths < 30 mm) in the collagen network of visually pristine human cartilage. While research on macro-scale cracks in cartilage and microcracks in bone abounds, how microcracks within cartilage initiate and propagate remains unknown. We quantified the extent to which microcracks initiate and propagate in the collagen network during mechanical loading representative of normal activities. Design: We tested 76 full-thickness, cylindrical osteochondral plugs. We imaged untreated specimens (pristine phase) via second harmonic generation and assigned specimens to three low-energy impact groups (none, low, high), and thereafter to three cyclic compression groups (none, low, high) which simulate walking. We re-imaged specimens in the post-impact and post-cyclic compression phases to identify and track microcracks. Results: Microcracks in the network of collagen did not present in untreated controls but did initiate and propagate under mechanical treatments. We found that the length and width of microcracks increased from post-impact to post-cyclic compression in tracked microcracks, but neither depth nor angle presented statistically significant differences. Conclusions: The microcracks we initiated under low-energy impact loading increased in length and width during subsequent cyclic compression that simulated walking. The extent of this propagation depended on the combination of impact and cyclic compression. More broadly, the initiation and propagation of microcracks may characterize pathogenesis of osteoarthritis, and may suggest therapeutic targets for future studies.

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Low-energy impact of human cartilage: predictors for microcracking the network of collagen

Abstract: An impact energy density of 1.0 mJ/mm corresponded to a ∼20% probability of microcracking. Such changes may initiate a degenerative cascade leading to post-traumatic osteoarthritis.

Cited by 23 publications

References 46 publications

Characterization of cellular and matrix alterations in the early pathogenesis of osteochondritis dissecans in pigs using second harmonic generation and two‐photon excitation fluorescence microscopy

Characterization of cellular and matrix alterations in the early pathogenesis of osteochondritis dissecans in pigs using second harmonic generation and two‐photon excitation fluorescence microscopy

Comparison between in vitro and in vivo cartilage overloading studies based on a systematic literature review

Propagation of microcracks in collagen networks of cartilage under mechanical loads

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