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Magnetic resonance imaging and histology of ovine hip joint cartilage in two age populations: a sheep model with assumed healthy cartilage

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Abstract

Objective

To compare morphologically normal appearing cartilage in two age groups with delayed gadolinium-enhanced magnetic resonance imaging of cartilage (dGEMRIC) and correlate magnetic resonance imaging (MRI) findings with histology.

Materials and methods

Twenty femoral head specimens collected from ten lambs (group I) and ten young adult sheep (group II) underwent dGEMRIC and histological assessment. A region of 2 cm2 with morphologically normal-appearing cartilage was marked with a surgical suture for subsequent matching of MRI and histological sections. The MRI protocol included a three-dimensional (3D) double-echo steady-state sequence for morphological cartilage assessment, a B1 pre-scan with various flip angles for B1 field heterogeneity correction, and 3D volumetric interpolated breathhold examination for T1Gd mapping (dGEMRIC). Histological analysis was performed according to the Mankin scoring system.

Results

A total of 303 regions of interest (ROI; 101 MRI reformats matching 101 histological sections) was assessed. Twenty-six ROIs were excluded owing to morphologically apparent cartilage damage or insufficient MR image quality. Therefore, 277 ROIs were analyzed. Histological analyses revealed distinct degenerative changes in various cartilage samples of group II (young adult sheep). Corresponding T1Gd values were significantly lower in the group of sheep (mean T1Gd = 540.4 ms) compared with the group of lambs (mean T1Gd = 623.6 ms; p < 0.001).

Conclusions

Although morphologically normal, distinct cartilage degeneration may be present in young adult sheep cartilage. dGEMRIC can reveal these changes and may be a tool for the assessment of early cartilage degeneration.

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References

  1. Bashir A, Gray ML, Boutin RD, Burstein D. Glycosaminoglycan in articular cartilage: in vivo assessment with delayed Gd(DTPA)(2-)-enhanced MR imaging. Radiology. 1997;205(2):551–8.

    PubMed  CAS  Google Scholar 

  2. Maroudas A. Physiochemical properties of articular cartilage. In: Freeman M, editor. Adult articular cartilage. London: Pitman Medical; 1979. p. 215–90.

    Google Scholar 

  3. Bashir A, Boutin RD, Gray ML, Burstein ML. MRI of glycosaminoglycan distribution in cartilage using Gd(DTPA)2- in vivo. Berkeley: Fifth Annual Meeting of the International Society for Magnetic Resonance in Medicine; 1997. p. 345.

    Google Scholar 

  4. Burstein D, Velyvis J, Scott KT, Stock KW, Kim YJ, Jaramillo D, et al. Protocol issues for delayed Gd(DTPA)(2-)-enhanced MRI (dGEMRIC) for clinical evaluation of articular cartilage. Magn Reson Med. 2001;45(1):36–41.

    Article  PubMed  CAS  Google Scholar 

  5. Tiderius CJ, Olsson LE, Leander P, Ekberg O, Dahlberg L. Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis. Magn Reson Med. 2003;49(3):488–92.

    Article  PubMed  Google Scholar 

  6. Tiderius CJ, Svensson J, Leander P, Ola T, Dahlberg L. dGEMRIC (delayed gadolinium-enhanced MRI of cartilage) indicates adaptive capacity of human knee cartilage. Magn Reson Med. 2004;51(2):286–90.

    Article  PubMed  Google Scholar 

  7. Williams A, Gillis A, McKenzie C, Po B, Sharma L, Micheli L, et al. Glycosaminoglycan distribution in cartilage as determined by delayed gadolinium-enhanced MRI of cartilage (dGEMRIC): potential clinical applications. Am J Roentgenol. 2004;182(1):167–72.

    Article  Google Scholar 

  8. Nojiri T, Watanabe N, Namura T, Narita W, Ikoma K, Suginoshita T, et al. Utility of delayed gadolinium-enhanced MRI (dGEMRIC) for qualitative evaluation of articular cartilage of patellofemoral joint. Knee Surg Sports Traumatol Arthrosc. 2006;14(8):718–23.

    Article  PubMed  Google Scholar 

  9. Tiderius C, Hori M, Williams A, Sharma L, Prasad PV, Finnell M, et al. dGEMRIC as a function of BMI. Osteoarthritis Cartilage. 2006;14(11):1091–7.

    Article  PubMed  CAS  Google Scholar 

  10. Burstein D, Bashir A, Gray ML. MRI techniques in early stages of cartilage disease. Invest Radiol. 2000;35(10):622–38.

    Article  PubMed  CAS  Google Scholar 

  11. Bashir A, Gray ML, Burstein D. Gd-DTPA2- as a measure of cartilage degradation. Magn Reson Med. 1996;36(5):665–73.

    Article  PubMed  CAS  Google Scholar 

  12. Bashir A, Gray ML, Hartke J, Burstein D. Nondestructive imaging of human cartilage glycosaminoglycan concentration by MRI. Magn Reson Med. 1999;41(5):857–65.

    Article  PubMed  CAS  Google Scholar 

  13. Zilkens C, Miese F, Kim Y-J, Hosalkar H, Antoch G, Krauspe R, et al. Three-dimensional delayed gadolinium-enhanced magnetic resonance imaging of hip joint cartilage at 3 T: a prospective controlled study. Eur J Radiol. 2012;81(11):3420–5.

    Article  PubMed  Google Scholar 

  14. Burger C, Mueller M, Wlodarczyk P, Goost H, Tolba RH, Rangger C, et al. The sheep as a knee osteoarthritis model: early cartilage changes after meniscus injury and repair. Lab Anim. 2007;41(4):420–31.

    Article  PubMed  CAS  Google Scholar 

  15. Elliott DM, Yerramalli CS, Beckstein JC, Boxberger JI, Johannessen W, Vresilovic EJ. The effect of relative needle diameter in puncture and sham injection animal models of degeneration. Spine. 2008;33(6):588–96.

    Article  PubMed  Google Scholar 

  16. Phillips TW, Gurr K. A preconditioned arthritic hip model. J Arthroplasty. 1989;4(3):193–200.

    Article  PubMed  CAS  Google Scholar 

  17. Hawezi ZK, Lammentausta E, Svensson J, Dahlberg LE, Tiderius CJ. In vivo transport of Gd-DTPA(2-) in human knee cartilage assessed by depth-wise dGEMRIC analysis. J Magn Reson Imaging. 2011;34(6):1352–8.

    Article  PubMed  Google Scholar 

  18. Bittersohl B, Hosalkar HS, Werlen S, Trattnig S, Siebenrock KA, Mamisch TC. Intravenous versus intra-articular delayed gadolinium-enhanced magnetic resonance imaging in the hip joint: a comparative analysis. Invest Radiol. 2010;45(9):538–42.

    Article  PubMed  CAS  Google Scholar 

  19. Bittersohl B, Mamisch TC, Welsch GH, Stratmann J, Forst R, Swoboda B, et al. Experimental model to evaluate in vivo and in vitro cartilage MR imaging by means of histological analyses. Eur J Radiol. 2009;70(3):561–9.

    Article  PubMed  CAS  Google Scholar 

  20. Zilkens C, Miese F, Herten M, Kurzidem S, Jäger M, König D, et al. Reliability of gradient-echo three-dimensional delayed gadolinium-enhanced magnetic resonance imaging of hip joint cartilage: a histologically controlled study; Eur J Radiol. 2012 doi: 10.1016/j.ejrad.2012.09.024

    Google Scholar 

  21. Andreisek G, White LM, Yang Y, Robinson E, Cheng HL, Sussman MS. Delayed gadolinium-enhanced MR imaging of articular cartilage: three-dimensional T1 mapping with variable flip angles and B1 correction. Radiology. 2009;252(3):865–73.

    Article  PubMed  Google Scholar 

  22. Donath K. The diagnostic value of the new method for the study of undecalcified bones and teeth with attached soft tissue (Säge-Schliff (sawing and grinding) technique). Pathol Res Pract. 1985;179(6):631–3.

    Article  PubMed  CAS  Google Scholar 

  23. Mankin HJ, Dorfman H, Lippiello L, Zarins A. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am. 1971;53(3):523–37.

    PubMed  CAS  Google Scholar 

  24. Simon WH. Scale effects in animal joints. I. Articular cartilage thickness and compressive stress. Arthritis Rheum. 1970;13(3):244–56.

    Article  PubMed  CAS  Google Scholar 

  25. Peretti GM, Xu JW, Bonassar LJ, Kirchhoff CH, Yaremchuk MJ, Randolph MA. Review of injectable cartilage engineering using fibrin gel in mice and swine models. Tissue Eng. 2006;12(5):1151–68.

    Article  PubMed  CAS  Google Scholar 

  26. Thomas CM, Fuller CJ, Whittles CE, Sharif M. Chondrocyte death by apoptosis is associated with cartilage matrix degradation. Osteoarthritis Cartilage. 2007;15(1):27–34.

    Article  PubMed  CAS  Google Scholar 

  27. Tiderius CJ. Another step towards the understanding of the earliest stages of osteoarthritis. Osteoarthritis Cartilage. 2009;17(12):1534–5.

    Article  PubMed  CAS  Google Scholar 

  28. Bittersohl B, Steppacher S, Haamberg T, Kim YJ, Werlen S, Beck M, et al. Cartilage damage in femoroacetabular impingement (FAI): preliminary results on comparison of standard diagnostic vs delayed gadolinium-enhanced magnetic resonance imaging of cartilage (dGEMRIC). Osteoarthritis Cartilage. 2009;17(10):1297–306.

    Article  PubMed  CAS  Google Scholar 

  29. Schulze-Tanzil G, Muller RD, Kohl B, Schneider N, Ertel W, Ipaktchi K, et al. Differing in vitro biology of equine, ovine, porcine and human articular chondrocytes derived from the knee joint: an immunomorphological study. Histochem Cell Biol. 2009;131(2):219–29.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was funded by a research grant of the research commission of the University of Düsseldorf, Medical Faculty.

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Correspondence to Christoph Zilkens.

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Zilkens, C., Miese, F.R., Crumbiegel, C. et al. Magnetic resonance imaging and histology of ovine hip joint cartilage in two age populations: a sheep model with assumed healthy cartilage. Skeletal Radiol 42, 699–705 (2013). https://doi.org/10.1007/s00256-012-1554-7

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  • DOI: https://doi.org/10.1007/s00256-012-1554-7

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