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Layer-specific analysis of femorotibial cartilage t2 relaxation time based on registration of segmented double echo steady state (dess) to multi-echo-spin-echo (mese) images

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Abstract

Objective

To develop and validate a 3D registration approach by which double echo steady state (DESS) MR images with cartilage thickness segmentations are used to extract the cartilage transverse relaxation time (T2) from multi-echo-spin-echo (MESE) MR images, without direct segmentations for MESE.

Materials and methods

Manual DESS segmentations of 89 healthy reference knees (healthy) and 60 knees with early radiographic osteoarthritis (early ROA) from the Osteoarthritis Initiative were registered to corresponding MESE images that had independent direct T2 segmentations. For validation purposes, (a) regression analysis of deep and superficial cartilage T2 was performed and (b) between-group differences between healthy vs. early ROA knees were compared for registered vs. direct MESE analysis.

Results

Moderate to high correlations were observed for the deep (r = 0.80) and the superficial T2 (r = 0.81), with statistically significant between-group differences (ROA vs. healthy) of + 1.4 ms (p = 0.002) vs. + 1.3 ms (p < 0.001) for registered vs. direct T2 segmentation in the deep, and + 1.3 ms (p = 0.002) vs. + 2.3 ms (p < 0.001) in the superficial layer.

Discussion

This registration approach enables extracting cartilage T2 from MESE scans using DESS (cartilage thickness) segmentations, avoiding the need for direct MESE T2 segmentations.

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References

  1. Mosher TJ, Dardzinski BJ (2004) Cartilage MRI T2 relaxation time map**: overview and applications. Semin Musculoskelet Radiol 8:355–368

    Article  Google Scholar 

  2. Jungmann PM, Kraus MS, Nardo L, Liebl H, Alizai H, Joseph GB, Liu F, Lynch J, McCulloch CE, Nevitt MC, Link TM (2013) T2 relaxation time measurements are limited in monitoring progression, once advanced cartilage defects at the knee occur: longitudinal data from the osteoarthritis initiative. J Magn Reson 38:1415–1424

    Google Scholar 

  3. Liess C, Luesse S, Karger N, Heller M, Glueer CC (2002) Detection of changes in cartilage water content using MRI T2-map** in vivo. Osteoarthritis Cartilage 10:907–913

    Article  CAS  Google Scholar 

  4. Kim T, Min BH, Yoon SH, Kim H, Park S, Lee HY, Kwack KS (2014) An in vitro comparative study of T2 and T2* map**s of human articular cartilage at 3-Tesla MRI using histology as the standard of reference. Skelet Radiol 43:947–954

    Article  Google Scholar 

  5. Lammentausta E, Kiviranta P, Nissi MJ, Laasanen MS, Kiviranta I, Nieminen MT, Jurvelin JS (2006) T2 relaxation time and delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) of human patellar cartilage at 1.5 T and 9.4 T: Relationships with tissue mechanical properties. JOrthopRes 24:366–374

    Article  CAS  Google Scholar 

  6. Liebl H, Joseph G, Nevitt MC, Singh N, Heilmeier U, Subburaj K, Jungmann PM, McCulloch CE, Lynch JA, Lane NE, Link TM (2015) Early T2 changes predict onset of radiographic knee osteoarthritis: data from the osteoarthritis initiative. AnnRheum Dis 74:1353–1359

    Article  Google Scholar 

  7. Prasad AP, Nardo L, Schooler J, Joseph GB, Link TM (2013) T(1)rho and T(2) relaxation times predict progression of knee osteoarthritis. Osteoarthr Cart 21:69–76

    Article  CAS  Google Scholar 

  8. Wirth W, Maschek S, Beringer P, Eckstein F (2017) Subregional laminar cartilage MR spin-spin relaxation times (T2) in osteoarthritic knees with and without medial femorotibial cartilage loss - data from the osteoarthritis initiative (OAI). Osteoarthr Cartil 25:1313–1323

    Article  CAS  Google Scholar 

  9. Eckstein F, Le Graverand MP, Charles HC, Hunter DJ, Kraus VB, Sunyer T, Nemirovskyi O, Wyman BT, Buck R (2011) Clinical, radiographic, molecular and MRI-based predictors of cartilage loss in knee osteoarthritis. Ann Rheum Dis 70:1223–1230

    Article  CAS  Google Scholar 

  10. Dardzinski BJ, Mosher TJ, Li S, Van Slyke MA, Smith MB (1997) Spatial variation of T2 in human articular cartilage. Radiology 205:546–550

    Article  CAS  Google Scholar 

  11. Wirth W, Maschek S, Roemer FW, Sharma L, Duda GN, Eckstein F (2019) Radiographically normal knees with contralateral joint space narrowing display greater change in cartilage transverse relaxation time than those with normal contralateral knees: a model of early OA?—data from the Osteoarthritis Initiative (OAI). Osteoarthr Cartil 27:1663–1668

    Article  CAS  Google Scholar 

  12. Wirth W, Maschek S, Eckstein F (2017) Sex- and age-dependence of region- and layer-specific knee cartilage composition (spin–spin–relaxation time) in healthy reference subjects. Ann Anat Anat Anzeiger 210:1–8

    Article  Google Scholar 

  13. Wirth W, Maschek S, Roemer FW, Eckstein F (2016) Layer-specific femorotibial cartilage T2 relaxation time in knees with and without early knee osteoarthritis: data from the osteoarthritis initiative (OAI). Sci Rep 6:34202

    Article  CAS  Google Scholar 

  14. Chaudhari AS, Kogan F, Pedoia V, Majumdar S, Gold GE, Hargreaves BA (2019) Rapid knee MRI acquisition and analysis techniques for imaging osteoarthritis. J Magn Reson Imaging. https://doi.org/10.1002/jmri.26991

    Article  PubMed  Google Scholar 

  15. Eckstein F, Kwoh CK, Link TM (2014) Imaging research results from the osteoarthritis initiative (OAI): a review and lessons learned 10 years after start of enrolment. Ann Rheum Dis 73:1289–1300

    Article  Google Scholar 

  16. Graichen H, Eisenhart-Rothe RV, Vogl T, Englmeier KH, Eckstein F (2004) Quantitative assessment of cartilage status in osteoarthritis by quantitative magnetic resonance imaging: technical validation for use in analysis of cartilage volume and further morphologic parameters. Arthritis Rheum 50:811–816

    Article  Google Scholar 

  17. Schneider E, Nevitt M, McCulloch C, Cicuttini FM, Duryea J, Eckstein F, Tamez-Pena J (2012) Equivalence and precision of knee cartilage morphometry between different segmentation teams, cartilage regions, and MR acquisitions. Osteoarthritis Cartilage 20:869–879

    Article  CAS  Google Scholar 

  18. Gold GE, Han E, Stainsby J, Wright G, Brittain J, Beaulieu C (2004) Musculoskeletal MRI at 3.0 T: Relaxation times and image contrast. Am J Roentgenol. https://doi.org/10.2214/ajr.183.2.1830343

    Article  Google Scholar 

  19. Eckstein F, Kunz M, Schutzer M, Hudelmaier M, Jackson RD, Yu J, Eaton CB, Schneider E (2007) Brief report 2 year longitudinal change and testeretest-precision of knee cartilage morphology in a pilot study for the osteoarthritis initiative 1, 2. Osteoarthr Cart 15:1326–1332

    Article  CAS  Google Scholar 

  20. Wirth W, Nevitt M, Hellio Le Graverand MP, Benichou O, Dreher D, Davies RY, Lee J, Picha K, Gimona A, Maschek S, Hudelmaier M, Eckstein F (2010) Sensitivity to change of cartilage morphometry using coronal FLASH, sagittal DESS, and coronal MPR DESS protocols–comparative data from the osteoarthritis initiative (OAI). OsteoarthritisCartilage 18:547–554

    CAS  Google Scholar 

  21. Wirth W, Eckstein F, Boeth H, Diederichs G, Hudelmaier M, Duda GNN (2014) Longitudinal analysis of MR spin–spin relaxation times (T2) in medial femorotibial cartilage of adolescent vs mature athletes: dependence of deep and superficial zone properties on sex and age. Osteoarthr Cartil 22:1554–1558

    Article  CAS  Google Scholar 

  22. Urish KL, Williams AA, Durkin JR, Chu CR (2013) Registration of magnetic resonance image series for knee articular cartilage analysis: data from the osteoarthritis initiative. Cartilage 4:20–27

    Article  Google Scholar 

  23. Johnson HJ, McCormick MM, Ibanez L (2015) The ITK software guide: design and functionality, Fourth Ed. Kitware Inc.

  24. Pluim JPW, Maintz JBAA, Viergever MA (2003) Mutual-information-based registration of medical images: a survey. IEEE Trans Med Imaging. https://doi.org/10.1109/TMI.2003.815867

    Article  PubMed  Google Scholar 

  25. Peterfy CG, Schneider E, Nevitt M (2008) The osteoarthritis initiative: report on the design rationale for the magnetic resonance imaging protocol for the knee. Osteoarthr Cartil 16:1433–1441

    Article  CAS  Google Scholar 

  26. Eckstein F, Boudreau RM, Wang Z, Hannon MJ, Wirth W, Cotofana S, Guermazi A, Roemer FW, Nevitt M, John MR, Ladel C, Sharma L, Hunter DJ, Kwoh CK (2014) Trajectory of cartilage loss within 4 years of knee replacement—a nested case-control study from the osteoarthritis initiative. Osteoarthr Cartil 22:1542–1549

    Article  CAS  Google Scholar 

  27. Eckstein F, Collins JE, Nevitt MC, Lynch JA, Kraus V, Katz JN, Losina E, Wirth W, Guermazi A, Roemer FW, Hunter DJ (2015) Cartilage thickness change as an imaging biomarker of knee osteoarthritis progression—data from the fnih OA biomarkers consortium. Arthritis Rheumatol (Hoboken, NJ) 67:3184–3189

    Article  CAS  Google Scholar 

  28. Wirth W, Hunter DJ, Nevitt MC, Sharma L, Kwoh CK, Ladel C, Eckstein F (2017) Predictive and concurrent validity of cartilage thickness change as a marker of knee osteoarthritis progression: data from the osteoarthritis initiative. Osteoarthr Cartil 25:2063–2071

    Article  CAS  Google Scholar 

  29. Eckstein F, Maschek S, Roemer FW, Duda GN, Sharma L, Wirth W (2019) Cartilage loss in radiographically normal knees depends on radiographic status of the contralateral knee—data from the osteoarthritis initiative. Osteoarthr Cartil 27:273–277

    Article  CAS  Google Scholar 

  30. Frobell RB, Nevitt MC, Hudelmaier M, Wirth W, Wyman BT, Benichou O, Dreher D, Davies R, Lee JH, Baribaud F, Gimona A, Eckstein F (2010) Femorotibial subchondral bone area and regional cartilage thickness: a cross-sectional description in healthy reference cases and various radiographic stages of osteoarthritis in 1003 knees from the osteoarthritis initiative. Arthritis Care Res (Hoboken) 62:1612–1623

    Article  Google Scholar 

  31. Chaudhari AS, Black MS, Eijgenraam S, Wirth W, Maschek S, Sveinsson B, Eckstein F, Oei EHG, Gold GE, Hargreaves BA (2018) Five-minute knee MRI for simultaneous morphometry and T2 relaxometry of cartilage and meniscus and for semiquantitative radiological assessment using double-echo in steady-state at 3T. J Magn Reson Imaging 47:1328–1341

    Article  Google Scholar 

  32. Chaudhari AS, Stevens KJ, Sveinsson B, Wood JP, Beaulieu CF, Oei EHG, Rosenberg JK, Kogan F, Alley MT, Gold GE, Hargreaves BA (2019) Combined 5-minute double-echo in steady-state with separated echoes and 2-minute proton-density-weighted 2D FSE sequence for comprehensive whole-joint knee MRI assessment. J Magn Reson Imaging. https://doi.org/10.1002/jmri.26582

    Article  PubMed  Google Scholar 

  33. Eijgenraam SM, Chaudhari AS, Reijman M, Bierma-Zeinstra SMA, Hargreaves BA, Runhaar J, Heijboer FWJ, Gold GE, Oei EHG (2019) Time-saving opportunities in knee osteoarthritis: T2 map** and structural imaging of the knee using a single 5-min MRI scan. Eur Radiol. https://doi.org/10.1007/s00330-019-06542-9

    Article  PubMed  PubMed Central  Google Scholar 

  34. Fripp J, Crozier S, Warfield SK, Ourselin S (2007) Automatic segmentation of the bone and extraction of the bone-cartilage interface from magnetic resonance images of the knee. Phys Med Biol. https://doi.org/10.1088/0031-9155/52/6/005

    Article  PubMed  Google Scholar 

  35. Shan L, Zach C, Charles C, Niethammer M (2014) Automatic atlas-based three-label cartilage segmentation from MR knee images. Med Image Anal. https://doi.org/10.1016/j.media.2014.05.008

    Article  PubMed  PubMed Central  Google Scholar 

  36. Lee HS, Kim HA, Kim H, Hong H, Yoon YC, Kim J (2016) Multi-atlas segmentation of the cartilage in knee MR images with sequential volume- and bone-mask-based registrations. Med Imaging 2016 Comput Diagnosis 10(1117/12):2216630

    Google Scholar 

  37. Raj A, Vishwanathan S, Ajani B, Krishnan K, Agarwal H (2018) Automatic knee cartilage segmentation using fully volumetric convolutional neural networks for evaluation of osteoarthritis. Proc Int Symp Biomed Imaging. https://doi.org/10.1109/ISBI.2018.8363705

    Article  Google Scholar 

  38. Tack A, Mukhopadhyay A, Zachow S (2018) Knee menisci segmentation using convolutional neural networks: data from the Osteoarthritis Initiative. Osteoarthr Cartil. https://doi.org/10.1016/j.joca.2018.02.907

    Article  Google Scholar 

  39. Liu F, Zhou Z, Samsonov A, Blankenbaker D, Larison W, Kanarek A, Lian K, Kambhampati S, Kijowski R (2018) Deep learning approach for evaluating knee MR images: achieving high diagnostic performance for cartilage lesion detection. Radiology. https://doi.org/10.1148/radiol.2018172986

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank the Ludwig Bolzmann Gesellschaft for funding this study and would like to thank the OAI participants, OAI study investigators, and OAI Clinical Center staff for generating this publicly available image sets.

Funding

This work was funded by the Ludwig Boltzmann Institute for Arthritis and Rehabilitation, Austria. The MRI acquisition of data used in this analysis was funded by the Osteoarthritis Initiative, a public–private partnership comprised of five contracts (N01-AR-2-2258; N01-AR-2-2259; N01-AR-2-2260; N01-AR-2-2261; N01-AR-2-2262) funded by the National Institutes of Health, a branch of the Department of Health and Human Services, and conducted by the Osteoarthritis Initiative study Investigators. Private funding partners of the OAI include Merck Research Laboratories, Novartis Pharmaceuticals Corporation, GlaxoSmithKline, and Pfizer, Inc. Private-sector funding for the Osteoarthritis Initiative is managed by the Foundation for the National Institutes of Health. The sponsors were not involved in the design and conduct of this particular study, in the analysis and interpretation of the data, and in the preparation, review, or approval of the manuscript.

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Authors

Contributions

Fürst: Study conception and design, Acquisition of data, Analysis and interpretation of data, Drafting of the manuscript; Wirth: Analysis and interpretation of data, Drafting of the manuscript, Critical revision; Chaudhari: Analysis and interpretation of data, Drafting of the manuscript, Critical revision; Eckstein: Study conception and design, Analysis and interpretation of data, Drafting of the manuscript, Critical revision.

Corresponding author

Correspondence to David Fürst.

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Conflict of interest

David Fürst and Wolfgang Wirth have a part-time employment with Chondrometrics GmbH; Wolfgang Wirth is a co-owner of Chondrometrics GmbH and has provided consulting services to Galapagos. Felix Eckstein is CEO of Chondrometrics GmbH, a company providing MR image analysis services to academic researchers and industry. He has provided consulting services to Merck KGaA, Abbvie, Tissuegene, Servier, Roche, Galapagos, and Novartis. Akshay Chaudhari has provided consulting services to SkopeMR, Inc., Subtle Medical, Chondrometrics GmbH, Image Analysis Group, and Culvert Engineering; and is a shareholder of Subtle Medical, LVIS Corporation, and BrainKey Inc.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

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Informed consent was obtained from all individual participants included in the OAI.

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Fürst, D., Wirth, W., Chaudhari, A. et al. Layer-specific analysis of femorotibial cartilage t2 relaxation time based on registration of segmented double echo steady state (dess) to multi-echo-spin-echo (mese) images. Magn Reson Mater Phy 33, 819–828 (2020). https://doi.org/10.1007/s10334-020-00852-6

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