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Ex vivo quantitative multiparametric MRI mapping of human meniscus degeneration

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Abstract

Objectives

To evaluate the diagnostic performance of T1, T1ρ, T2, T2*, and UTE-T2* (ultrashort-echo time-enhanced T2*) mapping in the refined graduation of human meniscus degeneration with histology serving as standard-of-reference.

Materials and methods

This IRB-approved intra-individual comparative ex vivo study was performed on 24 lateral meniscus body samples obtained from 24 patients undergoing total knee replacement. Samples were assessed on a 3.0-T MRI scanner using inversion-recovery (T1), spin-lock multi-gradient-echo (T1ρ), multi-spin-echo (T2) and multi-gradient-echo (T2* and UTE-T2*) sequences to determine relaxation times of quantitative MRI (qMRI) parameters. Relaxation times were calculated on the respective maps, averaged to the entire meniscus and to its zones. Histologically, samples were analyzed on a four-point score according to Williams (0-III). QMRI results and Williams (sub)scores were correlated using Spearman’s ρ, while Williams grade-dependent differences were assessed using Kruskal–Wallis and Dunn’s tests. Sensitivities and specificities in the detection of intact (Williams grade [WG]-0) and severely degenerate meniscus (WG-II-III) were calculated.

Results

Except for T2*, significant increases in qMRI parameters with increasing Williams grades were observed. T1, T1ρ, T2, and UTE-T2* exhibited high sensitivity and variable specificity rates. Significant marked-to-strong correlations were observed for these parameters with each other, with histological WGs and the subscores tissue integrity and cellularity.

Conclusions

QMRI mapping holds promise in the objective evaluation of human meniscus. Although sufficient discriminatory power of T1, T1ρ, T2, and UTE-T2* was only demonstrated for the histological extremes, these data may aid in the future MRI-based parameterization and quantification of human meniscus degeneration.

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Abbreviations

ρ:

Spearman’s correlation coefficient

CEL:

Cellularity

ECM:

Extracellular matrix

MOA:

Matrix organization and alignment

MRI:

Magnetic resonance imaging

OA:

Osteoarthritis

qMRI:

Quantitative MRI

SAF:

Matrix staining intensity

SMI:

Surface and matrix integrity

UTE:

Ultrashort echo time-enhanced

WG:

Williams grade

References

  1. Englund M, Guermazi A, Gale D, Hunter DJ, Aliabadi P, Clancy M, et al. Incidental meniscal findings on knee MRI in middle-aged and elderly persons. N Engl J Med. 2008;359(11):1108–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. McDermott I. Meniscal tears, repairs and replacement: their relevance to osteoarthritis of the knee. Br J Sports Med. 2011;45(4):292–7.

    Article  PubMed  Google Scholar 

  3. Hutchinson ID, Moran CJ, Potter HG, Warren RF, Rodeo SA. Restoration of the meniscus: form and function. Am J Sports Med. 2014;42(4):987–98.

    Article  PubMed  Google Scholar 

  4. Oei EH, Nikken JJ, Verstijnen AC, Ginai AZ, Myriam Hunink MG. MR imaging of the menisci and cruciate ligaments: a systematic review. Radiology. 2003;226(3):837–48.

    Article  PubMed  Google Scholar 

  5. Madhusudhan TR, Kumar TM, Bastawrous SS, Sinha A. Clinical examination. MRI and arthroscopy in meniscal and ligamentous knee injuries—a prospective study. J Orthop Surg Res. 2008;3:19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. De Smet AA, Mukherjee R. Clinical, MRI, and arthroscopic findings associated with failure to diagnose a lateral meniscal tear on knee MRI. AJR Am J Roentgenol. 2008;190(1):22–6.

    Article  PubMed  Google Scholar 

  7. Baum T, Joseph GB, Karampinos DC, Jungmann PM, Link TM, Bauer JS. Cartilage and meniscal T2 relaxation time as non-invasive biomarker for knee osteoarthritis and cartilage repair procedures. Osteoarthritis Cartil. 2013;21(10):1474–84.

    Article  CAS  Google Scholar 

  8. Rauscher I, Stahl R, Cheng J, Li X, Huber MB, Luke A, et al. Meniscal measurements of T1rho and T2 at MR imaging in healthy subjects and patients with osteoarthritis. Radiology. 2008;249(2):591–600.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Williams A, Qian Y, Golla S, Chu CR. UTE-T2 * mapping detects sub-clinical meniscus injury after anterior cruciate ligament tear. Osteoarthritis Cart. 2012;20(6):486–94.

    Article  CAS  Google Scholar 

  10. Chang EY, Campos JC, Bae WC, Znamirowski R, Statum S, Du J, et al. Ultrashort echo time T1 rho is sensitive to enzymatic degeneration of human menisci. J Comput Assis Tomogr. 2015;39(5):637–42.

    Article  Google Scholar 

  11. Gelber PE, Gonzalez G, Lloreta JL, Reina F, Caceres E, Monllau JC. Freezing causes changes in the meniscus collagen net: a new ultrastructural meniscus disarray scale. Knee Surg Sports Traumatol Arthrosc. 2008;16(4):353–9.

    Article  PubMed  Google Scholar 

  12. Pauli C, Grogan SP, Patil S, Otsuki S, Hasegawa A, Koziol J, et al. Macroscopic and histopathologic analysis of human knee menisci in aging and osteoarthritis. Osteoarthritis Cart. 2011;19(9):1132–41.

    Article  CAS  Google Scholar 

  13. Witschey 2nd WR, Borthakur A, Elliott MA, Mellon E, Niyogi S, Wallman DJ, et al. Artifacts in T1 rho-weighted imaging: compensation for B(1) and B(0) field imperfections. J Magn Reson. 2007;186(1):75–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Nebelung S, Sondern B, Oehrl S, Tingart M, Rath B, Pufe T, et al. Functional MR imaging mapping of human articular cartilage response to loading. Radiology. 2016;160053.

  15. Nebelung S, Brill N, Tingart M, Pufe T, Kuhl C, Jahr H, et al. Quantitative OCT and MRI biomarkers for the differentiation of cartilage degeneration. Skelet Radiol. 2016;45(4):505–16.

    Article  Google Scholar 

  16. Palmer AJ, Brown CP, McNally EG, Price AJ, Tracey I, Jezzard P, et al. Non-invasive imaging of cartilage in early osteoarthritis. Bone Joint J. 2013;95-B(6):738–46.

    Article  CAS  PubMed  Google Scholar 

  17. Bae WC, Du J, Bydder GM, Chung CB. Conventional and ultrashort time-to-echo magnetic resonance imaging of articular cartilage, meniscus, and intervertebral disk. Top Magn Reson Imaging: TMRI. 2010;21(5):275–89.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Herwig J, Egner E, Buddecke E. Chemical changes of human knee joint menisci in various stages of degeneration. Ann Rheum Dis. 1984;43(4):635–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Son M, Goodman SB, Chen W, Hargreaves BA, Gold GE, Levenston ME. Regional variation in T1 rho and T2 times in osteoarthritic human menisci: correlation with mechanical properties and matrix composition. Osteoarthr Cartil. 2013;21(6):796–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Calixto NE, Kumar D, Subburaj K, Singh J, Schooler J, Nardo L, et al. Zonal differences in meniscus MR relaxation times in response to in vivo static loading in knee osteoarthritis. J Orthop Res. 2015.

  21. Tsai PH, Chou MC, Lee HS, Lee CH, Chung HW, Chang YC, et al. MR T2 values of the knee menisci in the healthy young population: zonal and sex differences. Osteoarthr Cart. 2009;17(8):988–94.

    Article  Google Scholar 

  22. Petersen W, Tillmann B. Collagenous fibril texture of the human knee joint menisci. Anat Embryology. 1998;197(4):317–24.

    Article  CAS  Google Scholar 

  23. Messner K, Gao J. The menisci of the knee joint. Anatomical and functional characteristics, and a rationale for clinical treatment. J Anat. 1998;193(Pt 2):161–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bolbos RI, Link TM, Ma CB, Majumdar S, Li X. T1rho relaxation time of the meniscus and its relationship with T1 rho of adjacent cartilage in knees with acute ACL injuries at 3 T. Osteoarthritis Cart. 2009;17(1):12–8.

    Article  CAS  Google Scholar 

  25. Wang L, Regatte RR. T1rho MRI of human musculoskeletal system. J Magn Resonance Imaging: JMRI. 2015;41(3):586–600.

    Article  PubMed  Google Scholar 

  26. Adams ME, Muir H. The glycosaminoglycans of canine menisci. Biochem J. 1981;197(2):385–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Berberat JE, Nissi MJ, Jurvelin JS, Nieminen MT. Assessment of interstitial water content of articular cartilage with T1 relaxation. Magn Reson Imaging. 2009;27(5):727–32.

    Article  PubMed  Google Scholar 

  28. Williams A, Qian Y, Bear D, Chu CR. Assessing degeneration of human articular cartilage with ultra-short echo time (UTE) T2* mapping. Osteoarthr Cart. 2010;18(4):539–46.

    Article  CAS  Google Scholar 

  29. Neu CP. Functional imaging in OA: role of imaging in the evaluation of tissue biomechanics. Osteoarthritis Cartilage. 2014;22(10):1349–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Krishnan N, Shetty SK, Williams A, Mikulis B, McKenzie C, Burstein D. Delayed gadolinium-enhanced magnetic resonance imaging of the meniscus: an index of meniscal tissue degeneration? Arthritis Rheum. 2007;56(5):1507–11.

    Article  PubMed  Google Scholar 

  31. Kim T, Min BH, Yoon SH, Kim H, Park S, Lee HY, et al. 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 Radiology. 2014;43(7):947–54.

    Article  PubMed  Google Scholar 

  32. Maier CF, Tan SG, Hariharan H, Potter HG. T2 quantitation of articular cartilage at 1.5 T. J Magnet Res Imaging: JMRI. 2003;17(3):358–64.

    Article  Google Scholar 

  33. Friedrich KM, Shepard T, de Oliveira VS, Wang L, Babb JS, Schweitzer M, et al. T2 measurements of cartilage in osteoarthritis patients with meniscal tears. AJR Am J Roentgenol. 2009;193(5):W411–415.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Juras V, Apprich S, Zbyn S, Zak L, Deligianni X, Szomolanyi P, et al. Quantitative MRI analysis of menisci using biexponential T2* fitting with a variable echo time sequence. Magn Reson Med: Off J Soc Magn Reson Med/ Soc Magn Reson Med. 2014;71(3):1015–23.

    Article  Google Scholar 

  35. Tyler DJ, Robson MD, Henkelman RM, Young IR, Bydder GM. Magnetic resonance imaging with ultrashort TE (UTE) PULSE sequences: technical considerations. J Magn Reson Imaging: JMRI. 2007;25(2):279–89.

    Article  PubMed  Google Scholar 

  36. Lukas VA, Fishbein KW, Lin PC, Schar M, Schneider E, Neu CP, et al. Classification of histologically scored human knee osteochondral plugs by quantitative analysis of magnetic resonance images at 3T. J Orthop Res. 2015

  37. Lohmander LS, Englund PM, Dahl LL, Roos EM. The long-term consequence of anterior cruciate ligament and meniscus injuries: osteoarthritis. Am J Sports Med. 2007;35(10):1756–69.

    Article  PubMed  Google Scholar 

  38. Jahr H, Brill N, Nebelung S. Detecting early stage osteoarthritis by optical coherence tomography? Biomarkers: biochemical indicators of exposure, response, and susceptibility to chemicals. 2016:1–7.

  39. Bottomley PA, Foster TH, Argersinger RE, Pfeifer LM. A review of normal tissue hydrogen NMR relaxation times and relaxation mechanisms from 1–100 MHz: dependence on tissue type, NMR frequency, temperature, species, excision, and age. Med Phys. 1984;11(4):425–48.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Sven Nebelung.

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Nebelung, S., Tingart, M., Pufe, T. et al. Ex vivo quantitative multiparametric MRI mapping of human meniscus degeneration. Skeletal Radiol 45, 1649–1660 (2016). https://doi.org/10.1007/s00256-016-2480-x

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  • DOI: https://doi.org/10.1007/s00256-016-2480-x

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