Skip to main content
Top
Published in: Skeletal Radiology 12/2016

01-12-2016 | Scientific Article

Ex vivo quantitative multiparametric MRI mapping of human meniscus degeneration

Authors: Sven Nebelung, Markus Tingart, Thomas Pufe, Christiane Kuhl, Holger Jahr, Daniel Truhn

Published in: Skeletal Radiology | Issue 12/2016

Login to get access

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.
Literature
1.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
2.
go back to reference McDermott I. Meniscal tears, repairs and replacement: their relevance to osteoarthritis of the knee. Br J Sports Med. 2011;45(4):292–7.CrossRefPubMed McDermott I. Meniscal tears, repairs and replacement: their relevance to osteoarthritis of the knee. Br J Sports Med. 2011;45(4):292–7.CrossRefPubMed
3.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
5.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
6.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
7.
go back to reference 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.CrossRef 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.CrossRef
8.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
9.
go back to reference 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.CrossRef 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.CrossRef
10.
go back to reference 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.CrossRef 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.CrossRef
11.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
12.
go back to reference 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.CrossRef 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.CrossRef
13.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
14.
go back to reference 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. 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.
go back to reference 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.CrossRef 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.CrossRef
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
18.
19.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
20.
go back to reference 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. 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.
go back to reference 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.CrossRef 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.CrossRef
22.
go back to reference Petersen W, Tillmann B. Collagenous fibril texture of the human knee joint menisci. Anat Embryology. 1998;197(4):317–24.CrossRef Petersen W, Tillmann B. Collagenous fibril texture of the human knee joint menisci. Anat Embryology. 1998;197(4):317–24.CrossRef
23.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
24.
go back to reference 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.CrossRef 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.CrossRef
25.
go back to reference Wang L, Regatte RR. T1rho MRI of human musculoskeletal system. J Magn Resonance Imaging: JMRI. 2015;41(3):586–600.CrossRefPubMed Wang L, Regatte RR. T1rho MRI of human musculoskeletal system. J Magn Resonance Imaging: JMRI. 2015;41(3):586–600.CrossRefPubMed
27.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
28.
go back to reference 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.CrossRef 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.CrossRef
29.
30.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference 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.CrossRef 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.CrossRef
33.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
34.
go back to reference 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.CrossRef 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.CrossRef
35.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
36.
go back to reference 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 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
38.
go back to reference 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. 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
Metadata
Title
Ex vivo quantitative multiparametric MRI mapping of human meniscus degeneration
Authors
Sven Nebelung
Markus Tingart
Thomas Pufe
Christiane Kuhl
Holger Jahr
Daniel Truhn
Publication date
01-12-2016
Publisher
Springer Berlin Heidelberg
Published in
Skeletal Radiology / Issue 12/2016
Print ISSN: 0364-2348
Electronic ISSN: 1432-2161
DOI
https://doi.org/10.1007/s00256-016-2480-x

Other articles of this Issue 12/2016

Skeletal Radiology 12/2016 Go to the issue