Skip to main content
Erschienen in: European Radiology 12/2019

11.06.2019 | Magnetic Resonance

Differentiation of human cartilage degeneration by functional MRI mapping—an ex vivo study

verfasst von: Daniel Truhn, Björn Sondern, Simon Oehrl, Markus Tingart, Matthias Knobe, Dorit Merhof, Christiane Kuhl, Johannes Thüring, Sven Nebelung

Erschienen in: European Radiology | Ausgabe 12/2019

Einloggen, um Zugang zu erhalten

Abstract

Objective

To evaluate whether the response to loading of cartilage samples as assessed ex vivo by quantitative MRI (qMRI) mapping techniques can differentiate intact and early degenerative cartilage.

Methods

Upon IRB approval and written informed consent, 59 macroscopically intact osteochondral samples were obtained from the central lateral femoral condyles of patients undergoing total knee replacement. Spatially resolved T1, T2, T2*, and T1ρ maps were generated prior to and during displacement-controlled quasi-static indentation loading to 405 μm (Δ1/2) and 810 μm (Δ1). Upon manual segmentation, absolute qMRI parameters and loading-induced relative changes (δ1/2, δ1) were determined for the entire cartilage sample and distinct zones and regions. Based on their histologically determined degeneration as quantified according to Mankin (Mankin sum scores [MSS], range 0–14), samples were dichotomised into intact (int; MSS 0–4, n = 35) and early degenerative (ed, MSS 5–8, n = 24).

Results

For T1ρ, consistent loading-induced increases were found for δ1/2 and δ1. Throughout the entire sample, increases in T1ρ were significantly higher in early degenerative than in intact samples (Δ1/2(ed) = 23.8 [q25 = 18.1, q75 = 29.0] %; Δ1/2(int) = 12.7 [q25 = 5.9, q75 = 19.5] %; p < 0.0005), according to Wilcoxon’s signed-rank test). Zonal and regional analysis revealed these changes to be most pronounced in the sub-pistonal area. No significant degeneration-dependent loading-induced changes were found for T1, T2, or T2*.

Conclusion

Aberrant load-bearing of early degenerative cartilage may be detected using T1ρ mapping as a function of loading. Hence, the diagnostic differentiation of intact versus early degenerative cartilage may allow the reliable identification of early and potentially reversible cartilage degeneration, thereby opening new opportunities for diagnosis and treatment of cartilage pathologies.

Key Points

• T1ρ mapping of the cartilage response to loading allows the reliable identification of early degenerative changes ex vivo.
• Distinct response-to-loading patterns of cartilage tissue as assessed by functional MRI techniques are associated with biomechanical and histological tissue properties.
• Non-invasive functional MR imaging techniques may facilitate the more sensitive monitoring of therapeutic outcomes and treatment strategies.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Bay-Jensen AC, Hoegh-Madsen S, Dam E et al (2010) Which elements are involved in reversible and irreversible cartilage degradation in osteoarthritis? Rheumatol Int 30:435–442CrossRef Bay-Jensen AC, Hoegh-Madsen S, Dam E et al (2010) Which elements are involved in reversible and irreversible cartilage degradation in osteoarthritis? Rheumatol Int 30:435–442CrossRef
2.
Zurück zum Zitat Palmer AJ, Brown CP, McNally EG et al (2013) Non-invasive imaging of cartilage in early osteoarthritis. Bone Joint J 95-B:738–746CrossRef Palmer AJ, Brown CP, McNally EG et al (2013) Non-invasive imaging of cartilage in early osteoarthritis. Bone Joint J 95-B:738–746CrossRef
3.
Zurück zum Zitat Guermazi A, Alizai H, Crema MD, Trattnig S, Regatte RR, Roemer FW (2015) Compositional MRI techniques for evaluation of cartilage degeneration in osteoarthritis. Osteoarthritis Cartilage 23:1639–1653CrossRef Guermazi A, Alizai H, Crema MD, Trattnig S, Regatte RR, Roemer FW (2015) Compositional MRI techniques for evaluation of cartilage degeneration in osteoarthritis. Osteoarthritis Cartilage 23:1639–1653CrossRef
4.
Zurück zum Zitat Saarakkala S, Julkunen P, Kiviranta P, Mäkitalo J, Jurvelin JS, Korhonen RK (2010) Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics. Osteoarthritis Cartilage 18:73–81CrossRef Saarakkala S, Julkunen P, Kiviranta P, Mäkitalo J, Jurvelin JS, Korhonen RK (2010) Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics. Osteoarthritis Cartilage 18:73–81CrossRef
5.
Zurück zum Zitat Neu CP (2014) Functional imaging in OA: role of imaging in the evaluation of tissue biomechanics. Osteoarthritis Cartilage 22:1349–1359CrossRef Neu CP (2014) Functional imaging in OA: role of imaging in the evaluation of tissue biomechanics. Osteoarthritis Cartilage 22:1349–1359CrossRef
6.
Zurück zum Zitat Xia Y, Wang N, Lee J, Badar F (2011) Strain-dependent T1 relaxation profiles in articular cartilage by MRI at microscopic resolutions. Magn Reson Med 65:1733–1737CrossRef Xia Y, Wang N, Lee J, Badar F (2011) Strain-dependent T1 relaxation profiles in articular cartilage by MRI at microscopic resolutions. Magn Reson Med 65:1733–1737CrossRef
7.
Zurück zum Zitat Nebelung S, Brill N, Tingart M et al (2016) Quantitative OCT and MRI biomarkers for the differentiation of cartilage degeneration. Skeletal Radiol 45:505–516CrossRef Nebelung S, Brill N, Tingart M et al (2016) Quantitative OCT and MRI biomarkers for the differentiation of cartilage degeneration. Skeletal Radiol 45:505–516CrossRef
8.
Zurück zum Zitat Shiomi T, Nishii T, Tanaka H et al (2010) Loading and knee alignment have significant influence on cartilage MRI T2 in porcine knee joints. Osteoarthritis Cartilage 18:902–908CrossRef Shiomi T, Nishii T, Tanaka H et al (2010) Loading and knee alignment have significant influence on cartilage MRI T2 in porcine knee joints. Osteoarthritis Cartilage 18:902–908CrossRef
9.
Zurück zum Zitat Hamada H, Nishii T, Tamura S, Tanaka H, Wakayama T, Sugano N (2015) Comparison of load responsiveness of cartilage T1rho and T2 in porcine knee joints: an experimental loading MRI study. Osteoarthritis Cartilage 23:1776–1779CrossRef Hamada H, Nishii T, Tamura S, Tanaka H, Wakayama T, Sugano N (2015) Comparison of load responsiveness of cartilage T1rho and T2 in porcine knee joints: an experimental loading MRI study. Osteoarthritis Cartilage 23:1776–1779CrossRef
10.
Zurück zum Zitat Souza RB, Kumar D, Calixto N et al (2014) Response of knee cartilage T1rho and T2 relaxation times to in vivo mechanical loading in individuals with and without knee osteoarthritis. Osteoarthritis Cartilage 22:1367–1376CrossRef Souza RB, Kumar D, Calixto N et al (2014) Response of knee cartilage T1rho and T2 relaxation times to in vivo mechanical loading in individuals with and without knee osteoarthritis. Osteoarthritis Cartilage 22:1367–1376CrossRef
11.
Zurück zum Zitat Subburaj K, Souza RB, Stehling C et al (2012) Association of MR relaxation and cartilage deformation in knee osteoarthritis. J Orthop Res 30:919–926CrossRef Subburaj K, Souza RB, Stehling C et al (2012) Association of MR relaxation and cartilage deformation in knee osteoarthritis. J Orthop Res 30:919–926CrossRef
12.
Zurück zum Zitat Lange T, Knowles BR, Herbst M, Izadpanah K, Zaitsev M (2017) Comparative T2 and T1rho mapping of patellofemoral cartilage under in situ mechanical loading with prospective motion correction. J Magn Reson Imaging 46:452–460CrossRef Lange T, Knowles BR, Herbst M, Izadpanah K, Zaitsev M (2017) Comparative T2 and T1rho mapping of patellofemoral cartilage under in situ mechanical loading with prospective motion correction. J Magn Reson Imaging 46:452–460CrossRef
13.
Zurück zum Zitat Souza RB, Stehling C, Wyman BT et al (2010) The effects of acute loading on T1rho and T2 relaxation times of tibiofemoral articular cartilage. Osteoarthritis Cartilage 18:1557–1563CrossRef Souza RB, Stehling C, Wyman BT et al (2010) The effects of acute loading on T1rho and T2 relaxation times of tibiofemoral articular cartilage. Osteoarthritis Cartilage 18:1557–1563CrossRef
14.
Zurück zum Zitat Nebelung S, Sondern B, Oehrl S et al (2017) Functional MR imaging mapping of human articular cartilage response to loading. Radiology 282:464–474CrossRef Nebelung S, Sondern B, Oehrl S et al (2017) Functional MR imaging mapping of human articular cartilage response to loading. Radiology 282:464–474CrossRef
16.
Zurück zum Zitat Cameron ML, Briggs KK, Steadman JR (2003) Reproducibility and reliability of the outerbridge classification for grading chondral lesions of the knee arthroscopically. Am J Sports Med 31:83–86CrossRef Cameron ML, Briggs KK, Steadman JR (2003) Reproducibility and reliability of the outerbridge classification for grading chondral lesions of the knee arthroscopically. Am J Sports Med 31:83–86CrossRef
17.
Zurück zum Zitat Nebelung S, Brill N, Müller F et al (2016) Towards optical coherence tomography-based elastographic evaluation of human cartilage. J Mech Behav Biomed Mater 56:106–119CrossRef Nebelung S, Brill N, Müller F et al (2016) Towards optical coherence tomography-based elastographic evaluation of human cartilage. J Mech Behav Biomed Mater 56:106–119CrossRef
18.
Zurück zum Zitat Nebelung S, Sondern B, Jahr H et al (2018) Non-invasive T1rho mapping of the human cartilage response to loading and unloading. Osteoarthritis Cartilage 26:236–244CrossRef Nebelung S, Sondern B, Jahr H et al (2018) Non-invasive T1rho mapping of the human cartilage response to loading and unloading. Osteoarthritis Cartilage 26:236–244CrossRef
19.
Zurück zum Zitat Mankin HJ, Dorfman H, Lippiello L, Zarins A (1971) Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 53:523–537CrossRef Mankin HJ, Dorfman H, Lippiello L, Zarins A (1971) Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 53:523–537CrossRef
20.
Zurück zum Zitat Gahunia HK, Lemaire C, Babyn PS, Cross AR, Kessler MJ, Pritzker KP (1995) Osteoarthritis in rhesus macaque knee joint: quantitative magnetic resonance imaging tissue characterization of articular cartilage. J Rheumatol 22:1747–1756PubMed Gahunia HK, Lemaire C, Babyn PS, Cross AR, Kessler MJ, Pritzker KP (1995) Osteoarthritis in rhesus macaque knee joint: quantitative magnetic resonance imaging tissue characterization of articular cartilage. J Rheumatol 22:1747–1756PubMed
21.
Zurück zum Zitat Thuring J, Linka K, Itskov M et al (2018) Multiparametric MRI and computational modelling in the assessment of human articular cartilage properties: a comprehensive approach. Biomed Res Int 2018:9460456CrossRef Thuring J, Linka K, Itskov M et al (2018) Multiparametric MRI and computational modelling in the assessment of human articular cartilage properties: a comprehensive approach. Biomed Res Int 2018:9460456CrossRef
22.
Zurück zum Zitat van Tiel J, Kotek G, Reijman M et al (2016) Is T1rho mapping an alternative to delayed gadolinium-enhanced MR imaging of cartilage in the assessment of sulphated glycosaminoglycan content in human osteoarthritic knees? An in vivo validation study. Radiology 279:523–531CrossRef van Tiel J, Kotek G, Reijman M et al (2016) Is T1rho mapping an alternative to delayed gadolinium-enhanced MR imaging of cartilage in the assessment of sulphated glycosaminoglycan content in human osteoarthritic knees? An in vivo validation study. Radiology 279:523–531CrossRef
23.
Zurück zum Zitat Li X, Cheng J, Lin K et al (2011) Quantitative MRI using T1rho and T2 in human osteoarthritic cartilage specimens: correlation with biochemical measurements and histology. Magn Reson Imaging 29:324–334CrossRef Li X, Cheng J, Lin K et al (2011) Quantitative MRI using T1rho and T2 in human osteoarthritic cartilage specimens: correlation with biochemical measurements and histology. Magn Reson Imaging 29:324–334CrossRef
24.
Zurück zum Zitat Gründer W, Kanowski M, Wagner M, Werner A (2000) Visualization of pressure distribution within loaded joint cartilage by application of angle-sensitive NMR microscopy. Magn Reson Med 43:884–891CrossRef Gründer W, Kanowski M, Wagner M, Werner A (2000) Visualization of pressure distribution within loaded joint cartilage by application of angle-sensitive NMR microscopy. Magn Reson Med 43:884–891CrossRef
25.
Zurück zum Zitat Gründer W (2006) MRI assessment of cartilage ultrastructure. NMR Biomed 19:855–876CrossRef Gründer W (2006) MRI assessment of cartilage ultrastructure. NMR Biomed 19:855–876CrossRef
26.
Zurück zum Zitat Hesper T, Miese FR, Hosalkar HS et al (2015) Quantitative T2(*) assessment of knee joint cartilage after running a marathon. Eur J Radiol 84:284–289CrossRef Hesper T, Miese FR, Hosalkar HS et al (2015) Quantitative T2(*) assessment of knee joint cartilage after running a marathon. Eur J Radiol 84:284–289CrossRef
27.
Zurück zum Zitat Chavhan GB, Babyn PS, Thomas B, Shroff MM, Haacke EM (2009) Principles, techniques, and applications of T2*-based MR imaging and its special applications. Radiographics 29:1433–1449CrossRef Chavhan GB, Babyn PS, Thomas B, Shroff MM, Haacke EM (2009) Principles, techniques, and applications of T2*-based MR imaging and its special applications. Radiographics 29:1433–1449CrossRef
28.
Zurück zum Zitat Kim T, Min BH, Yoon SH et al (2014) An in vitro comparative study of T2 and T2* mappings of human articular cartilage at 3-Tesla MRI using histology as the standard of reference. Skeletal Radiol 43:947–954CrossRef Kim T, Min BH, Yoon SH et al (2014) An in vitro comparative study of T2 and T2* mappings of human articular cartilage at 3-Tesla MRI using histology as the standard of reference. Skeletal Radiol 43:947–954CrossRef
29.
Zurück zum Zitat Bittersohl B, Hosalkar HS, Miese FR et al (2015) Zonal T2* and T1Gd assessment of knee joint cartilage in various histological grades of cartilage degeneration: an observational in vitro study. BMJ Open 5:e006895CrossRef Bittersohl B, Hosalkar HS, Miese FR et al (2015) Zonal T2* and T1Gd assessment of knee joint cartilage in various histological grades of cartilage degeneration: an observational in vitro study. BMJ Open 5:e006895CrossRef
31.
Zurück zum Zitat Kleemann RU, Krocker D, Cedraro A, Tuischer J, Duda GN (2005) Altered cartilage mechanics and histology in knee osteoarthritis: relation to clinical assessment (ICRS grade). Osteoarthritis Cartilage 13:958–963CrossRef Kleemann RU, Krocker D, Cedraro A, Tuischer J, Duda GN (2005) Altered cartilage mechanics and histology in knee osteoarthritis: relation to clinical assessment (ICRS grade). Osteoarthritis Cartilage 13:958–963CrossRef
32.
Zurück zum Zitat Franz T, Hasler EM, Hagg R, Weiler C, Jakob RP, Mainil-Varlet P (2001) In situ compressive stiffness, biochemical composition, and structural integrity of articular cartilage of the human knee joint. Osteoarthritis Cartilage 9:582–592CrossRef Franz T, Hasler EM, Hagg R, Weiler C, Jakob RP, Mainil-Varlet P (2001) In situ compressive stiffness, biochemical composition, and structural integrity of articular cartilage of the human knee joint. Osteoarthritis Cartilage 9:582–592CrossRef
33.
Zurück zum Zitat Chan DD, Cai L, Butz KD, Trippel SB, Nauman EA, Neu CP (2016) In vivo articular cartilage deformation: noninvasive quantification of intratissue strain during joint contact in the human knee. Sci Rep 6:19220CrossRef Chan DD, Cai L, Butz KD, Trippel SB, Nauman EA, Neu CP (2016) In vivo articular cartilage deformation: noninvasive quantification of intratissue strain during joint contact in the human knee. Sci Rep 6:19220CrossRef
34.
Zurück zum Zitat Du YP, Parker DL, Davis WL, Cao G (1994) Reduction of partial-volume artifacts with zero-filled interpolation in three-dimensional MR angiography. J Magn Reson Imaging 4:733–741CrossRef Du YP, Parker DL, Davis WL, Cao G (1994) Reduction of partial-volume artifacts with zero-filled interpolation in three-dimensional MR angiography. J Magn Reson Imaging 4:733–741CrossRef
Metadaten
Titel
Differentiation of human cartilage degeneration by functional MRI mapping—an ex vivo study
verfasst von
Daniel Truhn
Björn Sondern
Simon Oehrl
Markus Tingart
Matthias Knobe
Dorit Merhof
Christiane Kuhl
Johannes Thüring
Sven Nebelung
Publikationsdatum
11.06.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 12/2019
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-019-06283-9

Weitere Artikel der Ausgabe 12/2019

European Radiology 12/2019 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.