Contrast-enhanced CT using a cationic contrast agent enables non-destructive assessment of the biochemical and biomechanical properties of mouse tibial plateau cartilage

Journal of Orthopaedic Research

Volumn 34, Issue 7, 2016, Pages 1130-1138

  Lakin, Benjamin A ^a,b   Patel, Harsh ^a,b   Holland, Conor ^b   Freedman, Jonathan D ^a,c   Shelofsky, Joshua S ^a,b   Snyder, Brian D ^a,d   Stok, Kathryn S ^e,f   Grinstaff, Mark W ^b,g  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Boston University   (United States)

^c BOSTON UNIVERSITY   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e ETH ZURICH   (Switzerland)

^f SCANCO MEDICAL AG   (Switzerland)

^g USA   (United States)

Author keywords

coefficient of friction; compressive modulus; glycosaminoglycan; micro computed tomography; osteoarthritis

Indexed keywords

CONTRAST MEDIUM; GLYCOSAMINOGLYCAN; N ACETYLGALACTOSAMINE 4 SULFATASE;

ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BIOCHEMICAL ANALYSIS; BIOMECHANICS; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; EX VIVO STUDY; FEASIBILITY STUDY; FEMALE; FRICTION; HISTOLOGY; KNEE; MOUSE; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; TIBIAL PLATEAU; YOUNG MODULUS;

EID: 84978532228     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.23141     Document Type: Article

References (50)

1. Fässler R, Schnegelsberg P, Dausman J, et al. 1994. Mice lacking alpha 1 (IX) collagen develop noninflammatory degenerative joint disease. Proc Natl Acad Sci USA 91:5070–5074.
2. Hu K, Xu L, Cao L, et al. 2006. Pathogenesis of osteoarthritis-like changes in the joints of mice deficient in type IX collagen. Arthritis Rheum 54:2891–2900.
3. Matsui Y, Iwasaki N, Kon S, et al. 2009. Accelerated development of aging-associated and instability-induced osteoarthritis in osteopontin-deficient mice. Arthritis Rheum 60:2362–2371.
4. Glasson SS, Askew R, Sheppard B, et al. 2004. Characterization of and osteoarthritis susceptibility in ADAMTS-4-knockout mice. Arthritis Rheum 50:2547–2558.
5. Li J, Anemaet W, Diaz MA, et al. 2011. Knockout of ADAMTS5 does not eliminate cartilage aggrecanase activity but abrogates joint fibrosis and promotes cartilage aggrecan deposition in murine osteoarthritis models. J Orthop Res 29:516–522.
6. Glasson SS, Blanchet TJ, Morris EA. 2007. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage 15:1061–1069.
7. Moodie JP, Stok KS, Müller R, et al. 2011. Multimodal imaging demonstrates concomitant changes in bone and cartilage after destabilisation of the medial meniscus and increased joint laxity. Osteoarthritis Cartilage 19:163–170.
8. Mason RM, Chambers MG, Flannelly J, et al. 2001. The STR/ort mouse and its use as a model of osteoarthritis. Osteoarthritis Cartilage 9:85–91.
9. Stok KS, Pelled G, Zilberman Y, et al. 2009. Revealing the interplay of bone and cartilage in osteoarthritis through multimodal imaging of murine joints. Bone 45:414–422.
10. Li J, Gorski DJ, Anemaet W, et al. 2012. Hyaluronan injection in murine osteoarthritis prevents TGFbeta 1-induced synovial neovascularization and fibrosis and maintains articular cartilage integrity by a CD44-dependent mechanism. Arthritis Res Ther 14:R151.
11. Takamatsu A, Ohkawara B, Ito M, et al. 2014. Verapamil protects against cartilage degradation in osteoarthritis by inhibiting wnt/β-catenin signaling. PLoS ONE 9:e92699.
12. Felson DT, Lawrence RC, Dieppe PA, et al. 2000. Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 133:635–646.
13. Maroudas A, Leaback D, Stockwell R. 1975. Glycosaminoglycan turn-over in articular cartilage [and discussion]. Philos Trans R Soc Lond B Biol Sci 271:293–313.
14. Xu L, Flahiff CM, Waldman BA, et al. 2003. Osteoarthritis-like changes and decreased mechanical function of articular cartilage in the joints of mice with the chondrodysplasia gene (cho). Arthritis Rheum 48:2509–2518.
15. Glasson S, Chambers M, Van Den Berg W, et al. 2010. The OARSI histopathology initiative-recommendations for histological assessments of osteoarthritis in the mouse. Osteoarthritis Cartilage 18:S17–S23.
16. Hyttinen MM, Töyräs J, Lapveteläinen T, et al. 2001. Inactivation of one allele of the type II collagen gene alters the collagen network in murine articular cartilage and makes cartilage softer. Ann Rheum Dis 60:262–268.
17. Cao L, Youn I, Guilak F, et al. 2006. Compressive properties of mouse articular cartilage determined in a novel micro-indentation test method and biphasic finite element model. J Biomech Eng 128:766–771.
18. Jay GD, Torres JR, Rhee DK, et al. 2007. Association between friction and wear in diarthrodial joints lacking lubricin. Arthritis Rheum 56:3662–3669.
19. Drewniak EI, Jay GD, Fleming BC, et al. 2009. Comparison of two methods for calculating the frictional properties of articular cartilage using a simple pendulum and intact mouse knee joints. J Biomech 42:1996–1999.
20. Drewniak EI, Jay GD, Fleming BC, et al. 2012. Cyclic loading increases friction and changes cartilage surface integrity in lubricin-mutant mouse knees. Arthritis Rheum 64:465–473.
21. Ruan MZC, Dawson B, Jiang MM, et al. 2013. Quantitative imaging of murine osteoarthritic cartilage by phase-contrast micro-computed tomography. Arthritis Rheum 65:388–396.
22. Kotwal N, Li J, Sandy J, et al. 2012. Initial application of EPIC-µCT to assess mouse articular cartilage morphology and composition: effects of aging and treadmill running. Osteoarthritis Cartilage 20:887–895.
23. Kerckhofs G, Sainz J, Wevers M, et al. 2013. Contrast-enhanced nanofocus computed tomography images the cartilage subtissue architecture in three dimensions. Eur Cell Mater 25:179–189.
24. Joshi NS, Bansal PN, Stewart RC, et al. 2009. Effect of contrast agent charge on visualization of articular cartilage using computed tomography: exploiting electrostatic interactions for improved sensitivity. J Am Chem Soc 131:13234–13235.
25. Baumgarten M, Bloebaum RD, Ross SD, et al. 1985. Normal human synovial fluid: osmolality and exercise-induced changes. J Bone Joint Surg Am 67:1336–1339.
26. Stewart RC, Bansal PN, Entezari V, et al. 2013. Contrast-enhanced CT with a high-affinity cationic contrast agent for imaging ex vivo bovine, intact ex vivo rabbit, and in vivo rabbit cartilage. Radiology 266:141–150.
27. Lakin BA, Ellis DJ, Shelofsky JS, et al. 2015. Contrast-enhanced CT facilitates rapid, non-destructive assessment of cartilage and bone properties of the human metacarpal. Osteoarthritis Cartilage 23:2158–2166.
28. Spilker RL, Suh JK, Mow VC. 1992. A finite element analysis of the indentation stress-relaxation response of linear biphasic articular cartilage. J Biomech Eng 114:191–201.
29. Stok KS, Lisignoli G, Cristino S, et al. 2010. Mechano-functional assessment of human mesenchymal stem cells grown in three-dimensional hyaluronan-based scaffolds for cartilage tissue engineering. J Biomed Mater Res A 93:37–45.
30. Flahiff CM, Narmoneva DA, Huebner JL, et al. 2002. Osmotic loading to determine the intrinsic material properties of guinea pig knee cartilage. J Biomech 35:1285–1290.
31. Farndale RW, Buttle DJ, Barrett AJ. 1986. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883:173–177.
32. Lusic H, Grinstaff MW. 2013. X-ray-computed tomography contrast agents. Chem Rev 113:1641–1666.
33. Bansal PN, Joshi NS, Entezari V, et al. 2010. Contrast enhanced computed tomography can predict the glycosaminoglycan content and biomechanical properties of articular cartilage. Osteoarthritis Cartilage 18:184–191.
34. Bansal PN, Stewart RC, Entezari V, et al. 2011. Contrast agent electrostatic attraction rather than repulsion to glycosaminoglycans affords a greater contrast uptake ratio and improved quantitative CT imaging in cartilage. Osteoarthritis Cartilage 19:970–976.
35. Bansal PN, Joshi NS, Entezari V, et al. 2011. Cationic contrast agents improve quantification of glycosaminoglycan (GAG) content by contrast enhanced CT imaging of cartilage. J Orthop Res 29:704–709.
36. Kallioniemi AS, Jurvelin JS, Nieminen MT, et al. 2007. Contrast agent enhanced pQCT of articular cartilage. Phys Med Biol 52:1209–1219.
37. Palmer AW, Guldberg RE, Levenston ME. 2006. Analysis of cartilage matrix fixed charge density and three-dimensional morphology via contrast-enhanced microcomputed tomography. Proc Natl Acad Sci USA 103:19255–19260.
38. Siebelt M, van Tiel J, Waarsing JH, et al. 2011. Clinically applied CT arthrography to measure the sulphated glycosaminoglycan content of cartilage. Osteoarthritis Cartilage 19:1183–1189.
39. Silvast TS, Jurvelin JS, Aula AS, et al. 2009. Contrast agent-enhanced computed tomography of articular cartilage: association with tissue composition and properties. Acta Radiol 50:78–85.
40. Silvast TS, Jurvelin JS, Lammi MJ, et al. 2009. pQCT study on diffusion and equilibrium distribution of iodinated anionic contrast agent in human articular cartilage—associations to matrix composition and integrity. Osteoarthritis Cartilage 17:26–32.
41. Lakin BA, Grasso DJ, Shah SS, et al. 2013. Cationic agent contrast-enhanced computed tomography imaging of cartilge correlates with the compressive modulus and coefficient of friction. Osteoarthritis Cartilage 21:60–68.
42. Das Neves Borges P, Forte AE, Vincent TL, et al. 2014. Rapid, automated imaging of mouse articular cartilage by microCT for early detection of osteoarthritis and finite element modelling of joint mechanics. Osteoarthritis Cartilage 22:1419–1428.
43. Hu X, Wang Q, Liu Y, et al. 2014. Optical imaging of articular cartilage degeneration using near-infrared dipicolylamine probes. Biomaterials 35:7511–7521.
44. Martin I, Obradovic B, Freed LE, et al. 1999. Method for quantitative analysis of glycosaminoglycan distribution in cultured natural and engineered cartilage. Ann Biomed Eng 27:656–662.
45. Mow VC, Huiskes R. 2005. Basic orthopedic biomechanics and mechanobiology. 3rd ed. Philadelphia: Lippincott Williams & Wilkins.
46. Katta J, Stapleton T, Ingham E, et al. 2008. The effect of glycosaminoglycan depletion on the friction and deformation of articular cartilage. Proc Inst Mech Eng H 222:1–11.
47. Krishnan R, Kopacz M, Ateshian GA. 2004. Experimental verification of the role of interstitial fluid pressurization in cartilage lubrication. J Orthop Res 22:565–570.
48. Basalo IM, Raj D, Krishnan R, et al. 2005. Effects of enzymatic degradation on the frictional response of articular cartilage in stress relaxation. J Biomech 38:1343–1349.
49. Schmidt TA, Sah RL. 2007. Effect of synovial fluid on boundary lubrication of articular cartilage. Osteoarthritis Cartilage 15:35–47.
50. Gleghorn JP, Bonassar LJ. 2008. Lubrication mode analysis of articular cartilage using stribeck surfaces. J Biomech 41:1910–1918.