Top

Magnetic Resonance Materials in Physics, Biology and Medicine

Published in:

Open Access 01-06-2021 | Research Article

Can sodium MRI be used as a method for mapping of cartilage stiffness?

Authors: Sander Brinkhof, Martijn Froeling, Rob P. A. Janssen, Keita Ito, Dennis W. J. Klomp

Published in: Magnetic Resonance Materials in Physics, Biology and Medicine | Issue 3/2021

Abstract

Objective

Sodium concentration is responsible for (at least part of) the stiffness of articular cartilage due to the osmotic pressure it generates. Therefore, we hypothesized that we could use sodium MRI to approximate the stiffness of cartilage to assess early cartilage degeneration.

Methods

Four human tibial plateaus were retrieved from patients undergoing total knee replacement (TKR), and their cartilage stiffness mapped with indentation testing, after which samples were scanned in a 7 T MRI to determine sodium concentration. The relation of biomechanical parameters to MRI sodium and glycosaminoglycan (GAG) concentration was explored by a linear mixed model.

Results

Weak correlations of GAG concentration with apparent peak modulus (p = 0.0057) and apparent equilibrium modulus (p = 0.0181) were observed and lack of correlation of GAG concentration versus MRI sodium concentration was observed. MRI sodium concentration was not correlated with apparent peak modulus, though a moderate correlation of MRI sodium concentration with permeability was shown (p = 0.0014).

Discussion and conclusion

Although there was correlation between GAG concentration and cartilage stiffness, this was not similar with sodium concentration as measured by MRI. Thus, if the correlation between MRI sodium imaging and GAG concentration could be resolved, this strategy for assessing cartilage functional quality still holds promise.

Available only for authorised users

Heir S, Nerhus TK, Røtterud JH, Løken S, Ekeland A, Engebretsen L, Årøen A (2010) Focal cartilage defects in the knee impair quality of life as much as severe osteoarthritis: a comparison of knee injury and osteoarthritis outcome score in 4 patient categories scheduled for knee surgery. Am J Sports Med 38:231–237PubMedCrossRef

Fox AJ, Bedi A, Rodeo SA (2009) The basic science of articular cartilage: structure, composition, and function. Sports Health 1:461–468CrossRef

Bekkers JEJ, Creemers LB, Dhert WJA, Saris DBF (2010) Diagnostic modalities for diseased articular cartilage-from defect to degeneration: a review. Cartilage 1:157–164PubMedPubMedCentralCrossRef

Oakley SP, Portek I, Szomor Z, Appleyard RC, Ghosh P, Kirkham BW, Murrell GAC, Lassere MN (2005) Arthroscopy—a potential “gold standard” for the diagnosis of the chondropathy of early osteoarthritis. Osteoarthr Cartil 13:368–378CrossRef

Brittberg M, Aglietti P, Gambardella R, Hangody L, Hauselmann HJ, Jakob RP, Levine D, Lohmander S, Mandelbaum BR, Peterson L, Staubli H-U (2000) ICRS Cartilage Injury Evaluation Package. ICRS 1–16

Lai WM, Hou JS, Mow VC (1991) A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113:245–258PubMedCrossRef

Gandhi NS, Mancera RL (2008) The structure of glycosaminoglycans and their interaction with proteins. Chem Biol Drug Des 72:455–482PubMedCrossRef

Shapiro EM, Borthakur A, Gougoutas A, Reddy R (2002) 23NA MRI accurately measures fixed charge density in articular cartilage. Magn Reson Med 47:284–291PubMedPubMedCentralCrossRef

Wheaton AJ, Borthakur A, Shapiro EM, Regatte RR, Akella SVS, Kneeland JB, Reddy R (2004) Proteoglycan loss in human knee cartilage: quantitation with sodium MR imaging–feasibility study. Radiology 231:900–905PubMedCrossRef

10.

Chang G, Madelin G, Sherman OH, Strauss EJ, Xia D, Recht MP, Jerschow A, Regatte RR (2012) Improved assessment of cartilage repair tissue using fluid-suppressed 23Na inversion recovery MRI at 7 Tesla: preliminary results. Eur Radiol 22:1341–1349PubMedPubMedCentralCrossRef

11.

Madelin G, Babb J, Xia D, Chang G, Krasnokutsky S, Abramson SB, Jerschow A, Regatte RR (2013) Articular cartilage: evaluation with fluid-suppressed 7.0-T sodium MR imaging in subjects with and subjects without osteoarthritis. Radiology 268:481–491PubMedPubMedCentralCrossRef

12.

Brinkhof S, Ali Haghnejad A, Ito K, Markenroth Bloch K, Klomp DWJ (2019) Uncompromised MRI of knee cartilage while incorporating sensitive sodium MRI. NMR Biomed 32:1–9CrossRef

13.

Farndale RW, Buttle DJ, Barrett AJ (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. BBA Gen Subj 883:173–177CrossRef

14.

Madelin G, Jerschow A, Regatte RR (2012) Sodium relaxation times in the knee joint in vivo at 7T. NMR Biomed 25:530–537PubMedCrossRef

15.

Madelin G, Xia D, Brown R, Babb J, Chang G, Krasnokutsky S, Regatte RR (2018) Longitudinal study of sodium MRI of articular cartilage in patients with knee osteoarthritis: initial experience with 16- month follow-up. Eur Radiol 28:133–412PubMedCrossRef

16.

Kumar R, Pierce DM, Isaksen V, Davies CDL, Drogset JO, Lilledahl MB (2018) Comparison of compressive stress-relaxation behavior in osteoarthritic (ICRS graded) human articular cartilage. Int J Mol Sci. https://doi.org/10.3390/ijms19020413PubMedPubMedCentralCrossRef

17.

Nieminen MT, Töyräs J, Laasanen MS, Silvennoinen J, Helminen HJ, Jurvelin JS (2004) Prediction of biomechanical properties of articular cartilage with quantitative magnetic resonance imaging. J Biomech 37:321–328PubMedCrossRef

18.

Linka K, Schäfer A, Hillgärtner M, Itskov M, Knobe M, Kuhl C, Hitpass L, Truhn D, Thuering J, Nebelung S (2019) Towards patient-specific computational modelling of articular cartilage on the basis of advanced multiparametric MRI techniques. Sci Rep 9:1–13CrossRef

19.

Brinkhof S, te Moller N, Froeling M, Brommer H, Weeren R, Ito K, Klomp D (2020) T2* mapping in an equine articular groove model—visualizing changes in collagen orientation. J Orthop Res. https://doi.org/10.1002/jor.24764PubMedPubMedCentralCrossRef

20.

Baldassarr M, Farley ML, Goodwin JSL, Bierbaum BE, Goldring SR, Goldring MB, Burstein D, Gray ML (2007) Relationship between cartilage stiffness and dGEMRIC Index: correlation and prediction. J Orthop Res 25:904–912CrossRef

21.

Samosky JT, Burstein D, Grimson WE, Howe R, Martin S, Gray ML (2005) Spatially-localized correlation of dGEMRIC-measured GAG distribution and mechanical stiffness in the human tibial plateau. J Orthop Res 23:93–101PubMedCrossRef

22.

Staroswiecki E, Bangerter NK, Gurney PT, Grafendorfer T, Gold GE, Hargreaves BA (2010) In vivo sodium imaging of human patellar cartilage with a 3D cones sequence at 3 T and 7 T. J Magn Reson Imaging 32:446–451PubMedPubMedCentralCrossRef

23.

Zbýň Š, Schreiner M, Juras V, Mlynarik V, Szomolanyi P, Laurent D, Scotti C, Haber H, Deligianni X, Bieri O, Nieminen MT, Trattnig S (2020) Assessment of low-grade focal cartilage lesions in the knee with sodium MRI at 7 T. Invest Radiol 00:1–8

24.

Nagel AM, Laun FB, Weber M-A, Matthies C, Semmler W, Schad LR (2009) Sodium MRI using a density-adapted 3D radial acquisition technique. Magn Reson Med 62:1565–1573PubMedCrossRef

25.

Yang B, Wendland MF, O’Connell GD (2020) Direct quantification of intervertebral disc water content using MRI. J Magn Reson Imaging 52:1152–1162PubMedCrossRef

26.

Wang L, Wu Y, Chang G, Oesingmann N, Schweitzer ME, Jerschow A, Regatte RR (2009) Rapid isotropic 3D-sodium MRI of the knee joint in vivo at 7T. J Magn Reson Imaging 30:606–614PubMedPubMedCentralCrossRef

27.

Brinkhof S, Nizak R, Khlebnikov V, Prompers JJ, Klomp DWJ, Saris DBF (2018) Detection of early cartilage damage: feasibility and potential of gagCEST imaging at 7T. Eur Radiol 28:2874–2881PubMedPubMedCentralCrossRef

28.

Koller U, Apprich S, Schmitt B, Windhager R, Trattnig S (2017) Evaluating the cartilage adjacent to the site of repair surgery with glycosaminoglycan-specific magnetic resonance imaging. Int Orthop 41:969–974PubMedCrossRef

29.

Kulkarni P, Deshpande S, Koppikar S, Patil S, Ingale D, Harsulkar A (2016) Glycosaminoglycan measured from synovial fluid serves as a useful indicator for progression of Osteoarthritis and complements Kellgren-Lawrence Score. BBA Clin 6:1–4PubMedPubMedCentralCrossRef

30.

Wang C, McArdle E, Fenty M, Witschey W, Elliott M, Sochor M, Reddy R, Borthakur A (2010) Validation of sodium MRI of intervertebral disc. Spine (Phila Pa 1976) 35:505–510CrossRef

31.

Zbýň Š, Brix MO, Juras V, Domayer SE, Walzer SM, Mlynarik V, Apprich S, Buckenmaier K, Windhager R, Trattnig S (2015) Sodium magnetic resonance imaging of ankle joint in cadaver specimens, volunteers, and patients after different cartilage repair techniques at 7 T: initial results. Invest Radiol 50:246–254PubMedPubMedCentralCrossRef

Title: Can sodium MRI be used as a method for mapping of cartilage stiffness?
Authors: Sander Brinkhof
Martijn Froeling
Rob P. A. Janssen
Keita Ito
Dennis W. J. Klomp
Publication date: 01-06-2021
Publisher: Springer International Publishing
Published in: Magnetic Resonance Materials in Physics, Biology and Medicine / Issue 3/2021
Print ISSN: 0968-5243
Electronic ISSN: 1352-8661
DOI: https://doi.org/10.1007/s10334-020-00893-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Can sodium MRI be used as a method for mapping of cartilage stiffness?

Abstract

Objective

Methods

Results

Discussion and conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objective

Methods

Results

Discussion and conclusion

Please log in to get access to this content

Other articles of this Issue 3/2021

A radiomics pipeline dedicated to Breast MRI: validation on a multi-scanner phantom study

On the reproducibility of hippocampal MEGA-sLASER GABA MRS at 7T using an optimized analysis pipeline

OPERA: a novel method to reduce ghost and aliasing artifacts

Feasibility of quantitative susceptibility mapping (QSM) of the human kidney

Variable echo time imaging for detecting the short T2* components of the sciatic nerve: a validation study

In memoriam: John R. Mallard (1927–2021)