European Radiology

, Volume 19, Issue 1, pp 132–143 | Cite as

T1rho, T2 and focal knee cartilage abnormalities in physically active and sedentary healthy subjects versus early OA patients—a 3.0-Tesla MRI study

  • Robert Stahl
  • Anthony Luke
  • Xiaojuan Li
  • Julio Carballido-Gamio
  • C. Benjamin Ma
  • Sharmila Majumdar
  • Thomas M. Link
Musculoskeletal

Abstract

(1) To assess the degree of focal cartilage abnormalities in physically active and sedentary healthy subjects as well as in patients with early osteoarthritis (OA). (2) To determine the diagnostic value of T2 and T1rho measurements in identifying asymptomatic physically active subjects with focal cartilage lesions. Thirteen asymptomatic physically active subjects, 7 asymptomatic sedentary subjects, and 17 patients with mild OA underwent 3.0-T MRI of the knee joint. T1rho and T2 values, cartilage volume and thickness, as well as the WORMS scores were obtained. Nine out of 13 active healthy subjects had focal cartilage abnormalities. T1rho and T2 values in active subjects with and without focal cartilage abnormalities differed significantly (p < 0.05). T1rho and T2 values were significantly higher (p < 0.05) in early OA patients compared to healthy subjects. T1rho measurements were superior to T2 in differentiating OA patients from healthy subjects, yet T1rho was moderately age-dependent. (1) Active subjects showed a high prevalence of focal cartilage abnormalities and (2) active subjects with and without focal cartilage abnormalities had different T1rho and T2 composition of cartilage. Thus, T1rho and T2 could be a parameter suited to identify active healthy subjects at higher risk for developing cartilage pathology.

Keywords

Magnetic resonance imaging Osteoarthritis Cartilage T1rho relaxation time T2 relaxation time 

Notes

Acknowledgments

This work was supported by the Research Evaluation and Allocation Committee (REAC) of the University of California, San Francisco, CA, USA, through the Clough G. Memorial Endowment Fund and by Glaxo Smith Kline (GSK) Inc., Research and Development, London, UK.

References

  1. 1.
    Lawrence RC, Helmick CG, Arnett FC, Deyo RA, Felson DT, Giannini EH, Heyse SP, Hirsch R, Hochberg MC, Hunder GG, Liang MH, Pillemer SR, Steen VD, Wolfe F (1998) Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States. Arthritis Rheum 41:778–799PubMedCrossRefGoogle Scholar
  2. 2.
    Peyron JG (1984) The epidemiology of osteoarthritis. WB Sanders, Philadelphia, pp 9–27Google Scholar
  3. 3.
    Sharma L, Kapoor D, Issa S (2006) Epidemiology of osteoarthritis: an update. Curr Opin Rheumatol 18:147–156PubMedCrossRefGoogle Scholar
  4. 4.
    Brandt KD, Mazzuca SA, Katz BP, Lane KA, Buckwalter KA, Yocum DE, Wolfe F, Schnitzer TJ, Moreland LW, Manzi S, Bradley JD, Sharma L, Oddis CV, Hugenberg ST, Heck LW (2005) Effects of doxycycline on progression of osteoarthritis: results of a randomized, placebo-controlled, double-blind trial. Arthritis Rheum 52:2015–2025PubMedCrossRefGoogle Scholar
  5. 5.
    Knutsen G, Drogset JO, Engebretsen L, Grontvedt T, Isaksen V, Ludvigsen TC, Roberts S, Solheim E, Strand T, Johansen O (2007) A randomized trial comparing autologous chondrocyte implantation with microfracture. Findings at 5 years. J Bone Joint Surg Am 89:2105–2112CrossRefGoogle Scholar
  6. 6.
    Felson DT, McLaughlin S, Goggins J, LaValley MP, Gale ME, Totterman S, Li W, Hill C, Gale D (2003) Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med 139:330–336PubMedGoogle Scholar
  7. 7.
    Link TM, Steinbach LS, Ghosh S, Ries M, Lu Y, Lane N, Majumdar S (2003) Osteoarthritis: MR imaging findings in different stages of disease and correlation with clinical findings. Radiology 226:373–381PubMedCrossRefGoogle Scholar
  8. 8.
    Bruyere O, Genant H, Kothari M, Zaim S, White D, Peterfy C, Burlet N, Richy F, Ethgen D, Montague T, Dabrowski C, Reginster JY (2007) Longitudinal study of magnetic resonance imaging and standard X-rays to assess disease progression in osteoarthritis. Osteoarthr Cartil 15(1):98–103, Epub 2006 Aug 4PubMedCrossRefGoogle Scholar
  9. 9.
    Raynauld JP, Martel-Pelletier J, Berthiaume MJ, Beaudoin G, Choquette D, Haraoui B, Tannenbaum H, Meyer JM, Beary JF, Cline GA, Pelletier JP (2006) Long term evaluation of disease progression through the quantitative magnetic resonance imaging of symptomatic knee osteoarthritis patients: correlation with clinical symptoms and radiographic changes. Arthritis Res Ther 8:R21PubMedCrossRefGoogle Scholar
  10. 10.
    Dijkgraaf LC, de Bont LG, Boering G, Liem RS (1995) The structure, biochemistry, and metabolism of osteoarthritic cartilage: a review of the literature. J Oral Maxillofac Surg 53:1182–1192PubMedCrossRefGoogle Scholar
  11. 11.
    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. J Orthop Res 24:366–374PubMedCrossRefGoogle Scholar
  12. 12.
    Link TM, Sell CA, Masi JN, Phan C, Newitt D, Lu Y, Steinbach L, Majumdar S (2006) 3.0 vs 1.5 T MRI in the detection of focal cartilage pathology-ROC analysis in an experimental model. Osteoarthr Cartil 14:63–70PubMedCrossRefGoogle Scholar
  13. 13.
    Bashir A, Gray ML, Hartke J, Burstein D (1999) Nondestructive imaging of human cartilage glycosaminoglycan concentration by MRI. Magn Reson Med 41:857–865PubMedCrossRefGoogle Scholar
  14. 14.
    Fragonas E, Mlynarik V, Jellus V, Micali F, Piras A, Toffanin R, Rizzo R, Vittur F (1998) Correlation between biochemical composition and magnetic resonance appearance of articular cartilage. Osteoarthr Cartil 6:24–32PubMedCrossRefGoogle Scholar
  15. 15.
    Liess C, Lusse S, Karger N, Heller M, Gluer CC (2002) Detection of changes in cartilage water content using MRI T2-mapping in vivo. Osteoarthr Cartil 10:907–913PubMedCrossRefGoogle Scholar
  16. 16.
    Lusse S, Claassen H, Gehrke T, Hassenpflug J, Schunke M, Heller M, Gluer CC (2000) Evaluation of water content by spatially resolved transverse relaxation times of human articular cartilage. Magn Reson Imaging 18:423–430PubMedCrossRefGoogle Scholar
  17. 17.
    Mlynarik V, Trattnig S, Huber M, Zembsch A, Imhof H (1999) The role of relaxation times in monitoring proteoglycan depletion in articular cartilage. J Magn Reson Imaging 10:497–502PubMedCrossRefGoogle Scholar
  18. 18.
    Menezes NM, Gray ML, Hartke JR, Burstein D (2004) T2 and T1rho MRI in articular cartilage systems. Magn Reson Med 51:503–509PubMedCrossRefGoogle Scholar
  19. 19.
    Goodwin DW, Wadghiri YZ, Zhu H, Vinton CJ, Smith ED, Dunn JF (2004) Macroscopic structure of articular cartilage of the tibial plateau: influence of a characteristic matrix architecture on MRI appearance. AJR Am J Roentgenol 182:311–318PubMedGoogle Scholar
  20. 20.
    Goodwin DW, Zhu H, Dunn JF (2000) In vitro MR imaging of hyaline cartilage: correlation with scanning electron microscopy. AJR Am J Roentgenol 174:405–409PubMedGoogle Scholar
  21. 21.
    Xia Y, Moody JB, Burton-Wurster N, Lust G (2001) Quantitative in situ correlation between microscopic MRI and polarized light microscopy studies of articular cartilage. Osteoarthr Cartil 9:393–406PubMedCrossRefGoogle Scholar
  22. 22.
    Bachmann GF, Basad E, Rauber K, Damian MS, Rau WS (1999) Degenerative joint disease on MRI and physical activity: a clinical study of the knee joint in 320 patients. Eur Radiol 9:145–152PubMedCrossRefGoogle Scholar
  23. 23.
    Blumenkrantz G, Lindsey CT, Dunn TC, Jin H, Ries MD, Link TM, Steinbach LS, Majumdar S (2004) A pilot, 2-year longitudinal study of the interrelationship between trabecular bone and articular cartilage in the osteoarthritic knee. Osteoarthr Cartil 12:997–1005PubMedCrossRefGoogle Scholar
  24. 24.
    Regatte RR, Akella SV, Lonner JH, Kneeland JB, Reddy R (2006) T1rho relaxation mapping in human osteoarthritis (OA) cartilage: comparison of T1rho with T2. J Magn Reson Imaging 23:547–553PubMedCrossRefGoogle Scholar
  25. 25.
    David-Vaudey E, Ghosh S, Ries M, Majumdar S (2004) T2 relaxation time measurements in osteoarthritis. Magn Reson Imaging 22:673–682PubMedCrossRefGoogle Scholar
  26. 26.
    Dunn TC, Lu Y, Jin H, Ries MD, Majumdar S (2004) T2 relaxation time of cartilage at MR imaging: comparison with severity of knee osteoarthritis. Radiology 232:592–598PubMedCrossRefGoogle Scholar
  27. 27.
    Redfield AG (1969) Nuclear Spin Thermodynamics in the Rotating Frame. Science 164:1015–1023PubMedCrossRefGoogle Scholar
  28. 28.
    Makela HI, Grohn OH, Kettunen MI, Kauppinen RA (2001) Proton exchange as a relaxation mechanism for T1 in the rotating frame in native and immobilized protein solutions. Biochem Biophys Res Commun 289:813–818PubMedCrossRefGoogle Scholar
  29. 29.
    Akella SV, Regatte RR, Gougoutas AJ, Borthakur A, Shapiro EM, Kneeland JB, Leigh JS, Reddy R (2001) Proteoglycan-induced changes in T1rho-relaxation of articular cartilage at 4T. Magn Reson Med 46:419–423PubMedCrossRefGoogle Scholar
  30. 30.
    Duvvuri U, Reddy R, Patel SD, Kaufman JH, Kneeland JB, Leigh JS, Nugent AC, Johnson GA, Makela HI, Grohn OH, Kettunen MI, Kauppinen RA (1997) T1rho-relaxation in articular cartilage: effects of enzymatic degradation T1rho imaging using magnetization-prepared projection encoding (MaPPE) Proton exchange as a relaxation mechanism for T1 in the rotating frame in native and immobilized protein solutions. Magn Reson Med 38:863–867PubMedCrossRefGoogle Scholar
  31. 31.
    Regatte RR, Akella SV, Borthakur A, Kneeland JB, Reddy R (2002) Proteoglycan depletion-induced changes in transverse relaxation maps of cartilage: comparison of T2 and T1rho. Acad Radiol 9:1388–1394PubMedCrossRefGoogle Scholar
  32. 32.
    Wheaton AJ, Dodge GR, Elliott DM, Nicoll SB, Reddy R (2005) Quantification of cartilage biomechanical and biochemical properties via T1rho magnetic resonance imaging. Magn Reson Med 54:1087–1093PubMedCrossRefGoogle Scholar
  33. 33.
    Li X, Benjamin Ma C, Link TM, Castillo DD, Blumenkrantz G, Lozano J, Carballido-Gamio J, Ries M, Majumdar S (2007) In vivo T(1rho) and T(2) mapping of articular cartilage in osteoarthritis of the knee using 3 T MRI. Osteoarthr Cartil 15:789–797PubMedCrossRefGoogle Scholar
  34. 34.
    Li X, Han ET, Ma CB, Link TM, Newitt DC, Majumdar S (2005) In vivo 3T spiral imaging based multi-slice T(1rho) mapping of knee cartilage in osteoarthritis. Magn Reson Med 54:929–536PubMedCrossRefGoogle Scholar
  35. 35.
    Regatte RR, Akella SV, Wheaton AJ, Lech G, Borthakur A, Kneeland JB, Reddy R (2004) 3D-T1rho-relaxation mapping of articular cartilage: in vivo assessment of early degenerative changes in symptomatic osteoarthritic subjects. Acad Radiol 11:741–749PubMedGoogle Scholar
  36. 36.
    Buckwalter JA, Martin JA (2004) Sports and osteoarthritis. Curr Opin Rheumatol 16:634–639PubMedCrossRefGoogle Scholar
  37. 37.
    Kaplan LD, Schurhoff MR, Selesnick H, Thorpe M, Uribe JW (2005) Magnetic resonance imaging of the knee in asymptomatic professional basketball players. Arthroscopy 21:557–561PubMedCrossRefGoogle Scholar
  38. 38.
    Major NM, Helms CA (2002) MR imaging of the knee: findings in asymptomatic collegiate basketball players. AJR Am J Roentgenol 179:641–644PubMedGoogle Scholar
  39. 39.
    Kellgren JH, Lawrence JS (1957) Radiological assessment of osteo-arthrosis. Ann Rheum Dis 16:494–502PubMedCrossRefGoogle Scholar
  40. 40.
    Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, Christy W, Cooke TD, Greenwald R, Hochberg M et al (1986) Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 29:1039–1049PubMedCrossRefGoogle Scholar
  41. 41.
    Tegner Y, Lysholm J (1985) Rating systems in the evaluation of knee ligament injuries. Clin Orthop Relat Res 43–49Google Scholar
  42. 42.
    Bellamy N, Buchanan WW, Goldsmith CH, Campbell J, Stitt LW (1988) Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee. J Rheumatol 15:1833–1840PubMedGoogle Scholar
  43. 43.
    Krug R, Han ET, Banerjee S, Majumdar S (2006) Fully balanced steady-state 3D-spin-echo (bSSSE) imaging at 3 Tesla. Magn Reson Med 56:1033–1040PubMedCrossRefGoogle Scholar
  44. 44.
    Oh J, Cha S, Aiken AH, Han ET, Crane JC, Stainsby JA, Wright GA, Dillon WP, Nelson SJ (2005) Quantitative apparent diffusion coefficients and T2 relaxation times in characterizing contrast enhancing brain tumors and regions of peritumoral edema. J Magn Reson Imaging 21:701–708PubMedCrossRefGoogle Scholar
  45. 45.
    Carballido-Gamio J, Bauer JS, Keh-Yang L, Krause S, Majumdar S. Combined Image Processing Techniques for Characterization of MRI Cartilage of the Knee. In: IEEE-EMBS. 2005. ShanghaiGoogle Scholar
  46. 46.
    Stahl R, Blumenkrantz G, Carballido-Gamio J, Zhao S, Munoz T, Hellio Le Graverand-Gastineau MP, Li X, Majumdar S, Link TM (2007) MRI-derived T2 relaxation times and cartilage morphometry of the tibio-femoral joint in subjects with and without osteoarthritis during a 1-year follow-up. Osteoarthr Cartil 15(11):1225–1234, Epub 2007 Jun 11PubMedCrossRefGoogle Scholar
  47. 47.
    Faber SC, Eckstein F, Lukasz S, Muhlbauer R, Hohe J, Englmeier KH, Reiser M (2001) Gender differences in knee joint cartilage thickness, volume and articular surface areas: assessment with quantitative three-dimensional MR imaging. Skeletal Radiol 30:144–150PubMedCrossRefGoogle Scholar
  48. 48.
    Peterfy CG, Guermazi A, Zaim S, Tirman PF, Miaux Y, White D, Kothari M, Lu Y, Fye K, Zhao S, Genant HK (2004) Whole-Organ Magnetic Resonance Imaging Score (WORMS) of the knee in osteoarthritis. Osteoarthr Cartil 12:177–190PubMedCrossRefGoogle Scholar
  49. 49.
    Duvvuri U, Charagundla SR, Kudchodkar SB, Kaufman JH, Kneeland JB, Rizi R, Leigh JS, Reddy R (2001) Human knee: in vivo T1(rho)-weighted MR imaging at 1.5 T-preliminary experience. Radiology 220:822–826PubMedCrossRefGoogle Scholar
  50. 50.
    Nissi MJ, Rieppo J, Toyras J, Laasanen MS, Kiviranta I, Jurvelin JS, Nieminen MT (2006) T(2) relaxation time mapping reveals age- and species-related diversity of collagen network architecture in articular cartilage. Osteoarthr Cartil 14(12):1265–1271, Epub 2006 Jul 14PubMedCrossRefGoogle Scholar
  51. 51.
    Nissi MJ, Toyras J, Laasanen MS, Rieppo J, Saarakkala S, Lappalainen R, Jurvelin JS, Nieminen MT (2004) Proteoglycan and collagen sensitive MRI evaluation of normal and degenerated articular cartilage. J Orthop Res 22:557–564PubMedCrossRefGoogle Scholar
  52. 52.
    Akella SV, Regatte RR, Wheaton AJ, Borthakur A, Reddy R (2004) Reduction of residual dipolar interaction in cartilage by spin-lock technique. Magn Reson Med 52:1103–1109PubMedCrossRefGoogle Scholar
  53. 53.
    Raynauld JP, Martel-Pelletier J, Berthiaume MJ, Labonte F, Beaudoin G, de Guise JA, Bloch DA, Choquette D, Haraoui B, Altman RD, Hochberg MC, Meyer JM, Cline GA, Pelletier JP (2004) Quantitative magnetic resonance imaging evaluation of knee osteoarthritis progression over two years and correlation with clinical symptoms and radiologic changes. Arthritis Rheum 50:476–487PubMedCrossRefGoogle Scholar
  54. 54.
    Mosher TJ, Dardzinski BJ, Smith MB (2000) Human articular cartilage: influence of aging and early symptomatic degeneration on the spatial variation of T2-preliminary findings at 3 T. Radiology 214:259–266PubMedGoogle Scholar
  55. 55.
    Mosher TJ, Liu Y, Yang QX, Yao J, Smith R, Dardzinski BJ, Smith MB (2004) Age dependency of cartilage magnetic resonance imaging T2 relaxation times in asymptomatic women. Arthritis Rheum 50:2820–2828PubMedCrossRefGoogle Scholar
  56. 56.
    Baysal O, Baysal T, Alkan A, Altay Z, Yologlu S (2004) Comparison of MRI graded cartilage and MRI based volume measurement in knee osteoarthritis. Swiss Med Wkly 134:283–288PubMedGoogle Scholar
  57. 57.
    Cicuttini F, Hankin J, Jones G, Wluka A (2005) Comparison of conventional standing knee radiographs and magnetic resonance imaging in assessing progression of tibiofemoral joint osteoarthritis. Osteoarthr Cartil 13:722–727PubMedCrossRefGoogle Scholar
  58. 58.
    Cicuttini F, Wluka A, Hankin J, Wang Y (2004) Longitudinal study of the relationship between knee angle and tibiofemoral cartilage volume in subjects with knee osteoarthritis. Rheumatology (Oxford) 43:321–324CrossRefGoogle Scholar
  59. 59.
    Cicuttini FM, Wluka AE, Wang Y, Stuckey SL (2004) Longitudinal study of changes in tibial and femoral cartilage in knee osteoarthritis. Arthritis Rheum 50:94–97PubMedCrossRefGoogle Scholar
  60. 60.
    Ding C, Cicuttini F, Scott F, Boon C, Jones G (2005) Association of prevalent and incident knee cartilage defects with loss of tibial and patellar cartilage: a longitudinal study. Arthritis Rheum 52:3918–3927PubMedCrossRefGoogle Scholar
  61. 61.
    Wluka AE, Forbes A, Wang Y, Hanna F, Jones G, Cicuttini FM (2006) Knee cartilage loss in symptomatic knee osteoarthritis over 4.5 years. Arthritis Res Ther 8:R90PubMedCrossRefGoogle Scholar
  62. 62.
    Wluka AE, Stuckey S, Snaddon J, Cicuttini FM (2002) The determinants of change in tibial cartilage volume in osteoarthritic knees. Arthritis Rheum 46:2065–2072PubMedCrossRefGoogle Scholar
  63. 63.
    Wluka AE, Wolfe R, Stuckey S, Cicuttini FM (2004) How does tibial cartilage volume relate to symptoms in subjects with knee osteoarthritis? Ann Rheum Dis 63:264–268PubMedCrossRefGoogle Scholar
  64. 64.
    Gandy SJ, Dieppe PA, Keen MC, Maciewicz RA, Watt I, Waterton JC (2002) No loss of cartilage volume over three years in patients with knee osteoarthritis as assessed by magnetic resonance imaging. Osteoarthr Cartil 10:929–937PubMedCrossRefGoogle Scholar
  65. 65.
    Yoshioka H, Stevens K, Hargreaves BA, Steines D, Genovese M, Dillingham MF, Winalski CS, Lang P (2004) Magnetic resonance imaging of articular cartilage of the knee: comparison between fat-suppressed three-dimensional SPGR imaging, fat-suppressed FSE imaging, and fat-suppressed three-dimensional DEFT imaging, and correlation with arthroscopy. J Magn Reson Imaging 20:857–864PubMedCrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2008

Authors and Affiliations

  • Robert Stahl
    • 1
    • 2
  • Anthony Luke
    • 3
  • Xiaojuan Li
    • 1
  • Julio Carballido-Gamio
    • 1
  • C. Benjamin Ma
    • 3
  • Sharmila Majumdar
    • 1
  • Thomas M. Link
    • 1
  1. 1.Musculoskeletal and Quantitative Imaging Group, Department of RadiologyUniversity of California, San FranciscoSan FranciscoUSA
  2. 2.Department of Clinical RadiologyUniversity Hospitals-Campus Grosshadern, Ludwig Maximilians University of MunichMunichGermany
  3. 3.Department of Orthopedic SurgeryUniversity of California, San FranciscoSan FranciscoUSA

Personalised recommendations