The effect of intermittent static biaxial tensile strains on tissue engineered cartilage

Annals of Biomedical Engineering

Volumn 38, Issue 4, 2010, Pages 1672-1682

  Fan, Jackie C Y ^a,b   Waldman, Stephen D ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b KINGSTON GENERAL HOSPITAL   (Canada)

Author keywords

Articular cartilage; Chondrocytes; Mechanical stimulation; Tension; Tissue engineering

Indexed keywords

APPLIED LOADS; ARTICULAR CARTILAGES; BIAXIAL TENSILE STRAIN; CHONDROCYTES; COMPRESSION AND SHEAR; DESIGN LOADINGS; ENGINEERED CARTILAGE; EXTRACELLULAR MATRIX SYNTHESIS; IN-VIVO; LONG TERM EXPOSURE; MECHANICAL STIMULATION; OPTIMAL CONDITIONS; PRE-TENSION; PROCESS NEEDS; PROTEOGLYCANS; STATIC TENSION; TIME PERIODS; TISSUE CONSTRUCTS; TISSUE ENGINEERED CARTILAGE; TISSUE FORMATION;

BIOMECHANICS; BODY FLUIDS; CARTILAGE; LIGAMENTS; MECHANICAL PROPERTIES; OPTIMIZATION; SYNTHESIS (CHEMICAL); TENSILE STRAIN; ULTRASONIC MEASUREMENT;

TISSUE ENGINEERING;

ANIMAL; ARTICLE; CARTILAGE; CARTILAGE CELL; CATTLE; CELL CULTURE; CYTOLOGY; MECHANICAL STRESS; MECHANOTRANSDUCTION; METHODOLOGY; PHYSIOLOGY; TENSILE STRENGTH; TISSUE ENGINEERING; YOUNG MODULUS;

ANIMALS; CARTILAGE; CATTLE; CELLS, CULTURED; CHONDROCYTES; ELASTIC MODULUS; MECHANOTRANSDUCTION, CELLULAR; STRESS, MECHANICAL; TENSILE STRENGTH; TISSUE ENGINEERING;

EID: 77952009468     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-010-9917-5     Document Type: Article

References (59)

1. LJ Bonassar AJ Grodzinsky EH Frank SG Davila NR Bhaktav SB Trippel 2001 The effect of dynamic compression on the response of articular cartilage to insulin-like growth factor-I J. Orthop. Res. 19 11 17 10.1016/S0736-0266(00) 00004-8 1:CAS:528:DC%2BD3MXjvVChtLs%3D 11332605 (Pubitemid 32288632)
2. H Bostrom B Mansson 1952 On the enzymatic exchange of the sulfate group of chondroitinsulfuric acid in slices of cartilage J. Biol. Chem. 196 483 488 1:CAS:528:DyaG38XmvVShug%3D%3D 12980991
3. J Boyle B Luan TF Cruz RA Kandel 1995 Characterization of proteoglycan accumulation during formation of cartilagenous tissue in vitro Osteoarthr. Cartil. 3 117 125 10.1016/S1063-4584(05)80044-5 1:STN:280:DyaK28%2FhtVCmtw%3D%3D 7584317
4. Buckwalter, J. A., T. A. Einhorn, and S. R. Simon. Orthopaedic basic science: biology and biomechanics of the musculoskeletal system. Am. Acad. Orthop. Surg. 2000.
5. MD Buschmann YA Gluzband AJ Grodzinsky EB Hunziker 1995 Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture J. Cell Sci. 108 Pt 4 1497 1508 1:CAS:528:DyaK2MXls12lt7g%3D 7615670
6. MD Buschmann YA Gluzband AJ Grodzinsky JH Kimura EB Hunziker 1992 Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix J. Orthop. Res. 10 745 758 10.1002/jor.1100100602 1:CAS:528:DyaK3sXlslSmug%3D%3D 1403287
7. A Chevrier E Rossomacha MD Buschmann CD Hoemann 2005 Optimization of histoprocessing methods to detect glycosaminoglycan, collagen type II, and collagen type I in decalcified rabbit osteochondral sections J. Histotechnol. 28 165 175 1:CAS:528:DC%2BD2MXhtVyhsbjN
8. JT Connelly EJ Vanderploeg ME Levenston 2004 The influence of cyclic tension amplitude on chondrocyte matrix synthesis: experimental and finite element analyses Biorheology 41 377 387 1:CAS:528:DC%2BD2cXlvF2iu7Y%3D 15299270
9. JN De Croos SS Dhaliwal MD Grynpas RM Pilliar RA Kandel 2006 Cyclic compressive mechanical stimulation induces sequential catabolic and anabolic gene changes in chondrocytes resulting in increased extracellular matrix accumulation Matrix Biol. 25 323 331 10.1016/j.matbio.2006.03.005 16697175 (Pubitemid 44175829)
10. RW Farndale DJ Buttle AJ Barrett 1986 Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue Biochim. Biophys. Acta 883 173 177 1:CAS:528:DyaL28Xls1yhsrs%3D 3091074
11. HJ Fry 1974 The interlocked stresses of articular cartilage Br. J. Plast. Surg. 27 363 364 10.1016/0007-1226(74)90040-X 1:STN:280:DyaE2M%2Fjs1Knug%3D%3D 4429815
12. GEHR Plastics, I. Technical data sheet: acrylnitrile butadiene styrene copolymer, 2008.
13. T Gibson WB Davis 1958 The distortion of autogenous cartilage grafts: its cause and prevention Br. J. Plast. Surg. 10 257 274 10.1016/S0007-1226(57) 80042-3
14. RL Goldberg LM Kolibas 1990 An improved method for determining proteoglycans synthesized by chondrocytes in culture Connect. Tissue Res. 24 265 275 10.3109/03008209009152154 1:STN:280:DyaK3czivFOrsg%3D%3D 2376128
15. Goodfellow. Polytetrafluoroethylene (PTFE) material information, 2008.
16. Goodfellow. Technical information-polyacrylonitrile-butadiene-styrene, 2008.
17. WC Hayes LM Keer G Herrmann LF Mockros 1972 A mathematical analysis for indentation tests of articular cartilage J. Biomech. 5 541 551 10.1016/0021-9290(72)90010-3 1:STN:280:DyaE3s3lsl2ktA%3D%3D 4667277
18. Heinegard, D., M. Bayliss, and P. Lorenzo. Biochemistry and metabolism of normal and osteoarthritic cartilage. In: Osteoarthritis, edited by K. D. Brandt, M. Doherty, and L. S. Lohmander. New York: Oxford University Press, 1998, pp. 74-84.
19. Y Hirano N Ishiguro M Sokabe M Takigawa K Naruse 2008 Effects of tensile and compressive strains on response of a chondrocytic cell line embedded in type I collagen gel J. Biotechnol. 133 245 252 10.1016/j.jbiotec.2007.07.955 1:CAS:528:DC%2BD2sXhsVOltrbJ 17868945 (Pubitemid 350266896)
20. DH Hoch AJ Grodzinsky TJ Koob ML Albert DR Eyre 1983 Early changes in material properties of rabbit articular cartilage after meniscectomy J. Orthop. Res. 1 4 12 10.1002/jor.1100010102 1:CAS:528:DyaL3sXlsleqtrw%3D 6689609
21. K Honda S Ohno K Tanimoto C Ijuin N Tanaka T Doi Y Kato K Tanne 2000 The effects of high magnitude cyclic tensile load on cartilage matrix metabolism in cultured chondrocytes Eur. J. Cell Biol. 79 601 609 10.1078/0171-9335-00089 1:CAS:528:DC%2BD3cXot1Squ7c%3D 11043401
22. J Huang LR Ballou KA Hasty 2007 Cyclic equibiaxial tensile strain induces both anabolic and catabolic responses in articular chondrocytes Gene 404 101 109 10.1016/j.gene.2007.09.007 1:CAS:528:DC%2BD2sXhtFyku7nM 17913398 (Pubitemid 47562648)
23. EB Hunziker 2002 Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects Osteoarthr. Cartil. 10 432 463 10.1053/joca.2002.0801 1:STN:280:DC%2BD38zhsFyhtw%3D%3D 12056848 (Pubitemid 34679298)
24. T Ikenoue MC Trindade MS Lee EY Lin DJ Schurman SB Goodman RL Smith 2003 Mechanoregulation of human articular chondrocyte aggrecan and type II collagen expression by intermittent hydrostatic pressure in vitro J. Orthop. Res. 21 110 116 10.1016/S0736-0266(02)00091-8 1:CAS:528:DC%2BD38XpvVWnt7w%3D 12507587 (Pubitemid 36157627)
25. M Jin EH Frank TM Quinn EB Hunziker AJ Grodzinsky 2001 Tissue shear deformation stimulates proteoglycan and protein biosynthesis in bovine cartilage explants Arch. Biochem. Biophys. 395 41 48 10.1006/abbi.2001.2543 1:CAS:528:DC%2BD3MXnslWhurw%3D 11673864 (Pubitemid 33030141)
26. JA Kaupp SD Waldman 2008 Mechanical vibrations increase the proliferation of articular chondrocytes in high-density culture Proc. Inst. Mech. Eng. [H] 222 695 703 1:CAS:528:DC%2BD1cXhtFWqtb3E
27. AA Khan JM Suits RA Kandel SD Waldman 2009 The effect of continuous culture on the growth and structure of tissue-engineered cartilage Biotechnol. Prog. 25 508 515 10.1002/btpr.108 1:CAS:528:DC%2BD1MXmtF2mtbs%3D 19294749
28. YJ Kim RL Sah JY Doong AJ Grodzinsky 1988 Fluorometric assay of DNA in cartilage explants using Hoechst 33258 Anal. Biochem. 174 168 176 10.1016/0003-2697(88)90532-5 1:CAS:528:DyaL1cXmt1Kju7o%3D 2464289 (Pubitemid 18261664)
29. JD Kisiday M Jin MA DiMicco B Kurz AJ Grodzinsky 2004 Effects of dynamic compressive loading on chondrocyte biosynthesis in self-assembling peptide scaffolds J. Biomech. 37 595 604 10.1016/j.jbiomech.2003.10.005 15046988 (Pubitemid 38445021)
30. WM Lai JS Hou VC Mow 1991 A triphasic theory for the swelling and deformation behaviors of articular cartilage J. Biomech. Eng. 113 245 258 10.1115/1.2894880 1:STN:280:DyaK38%2Fhs1equg%3D%3D 1921350
31. CP Leblond B Messier B Kopriwa 1959 Thymidine-H3 as a tool for the investigation of the renewal of cell populations Lab. Invest. 8 296 306 1:CAS:528:DyaF3MXktlCluw%3D%3D 13621628 discussion 306-308
32. DA Lee T Noguchi SP Frean P Lees DL Bader 2000 The influence of mechanical loading on isolated chondrocytes seeded in agarose constructs Biorheology 37 149 161 1:STN:280:DC%2BD3czptFCitg%3D%3D 10912187
33. A Maroudas M Venn 1977 Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling Ann. Rheum. Dis. 36 399 406 10.1136/ard.36.5.399 1:CAS:528:DyaE1cXjsFCrtA%3D%3D 200188 (Pubitemid 8201500)
34. I Martin B Obradovic S Treppo AJ Grodzinsky R Langer LE Freed G Vunjak-Novakovic 2000 Modulation of the mechanical properties of tissue engineered cartilage Biorheology 37 141 147 1:STN:280:DC%2BD3czptFCisQ%3D%3D 10912186
35. RL Mauck MA Soltz CC Wang DD Wong PH Chao WB Valhmu CT Hung GA Ateshian 2000 Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels J. Biomech. Eng. 122 252 260 10.1115/1.429656 1:STN:280:DC%2BD3M%2Fkt1WmtQ%3D%3D 10923293 (Pubitemid 30483241)
36. ® Culture Plate Inserts 1-6, 2004.
37. DA Narmoneva JY Wang LA Setton 1999 Nonuniform swelling-induced residual strains in articular cartilage J. Biomech. 32 401 408 10.1016/S0021-9290(98) 00184-5 1:STN:280:DyaK1M3ivVSiug%3D%3D 10213030 (Pubitemid 29156706)
38. AP Newman 1998 Articular cartilage repair Am. J. Sports Med. 26 309 324 1:STN:280:DyaK1c3gsl2jtQ%3D%3D 9548130
39. Parker-TexLoc. PTFE detailed properties (polytetrafluoroethylene), 2008.
40. B Peterkofsky R Diegelmann 1971 Use of a mixture of proteinase-free collagenases for the specific assay of radioactive collagen in the presence of other proteins Biochemistry 10 988 994 10.1021/bi00782a009 1:CAS:528: DyaE3MXhtVyjtrY%3D 4323854
41. TM Quinn AJ Grodzinsky MD Buschmann YJ Kim EB Hunziker 1998 Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants J. Cell Sci. 111 Pt 5 573 583 1:CAS:528:DyaK1cXit1egtLc%3D 9454731
42. N Ramakrishnan VS Arunachalam 1990 Effective elastic moduli of porous solids J. Mater. Sci. Mater. Med. 25 3930 3937
43. LK Saxon AG Robling I Alam CH Turner 2005 Mechanosensitivity of the rat skeleton decreases after a long period of loading, but is improved with time off Bone 36 454 464 10.1016/j.bone.2004.12.001 1:STN:280:DC%2BD2M7ptVSmsg%3D%3D 15777679 (Pubitemid 40403843)
44. JL Schriefer SJ Warden LK Saxon AG Robling CH Turner 2005 Cellular accommodation and the response of bone to mechanical loading J. Biomech. 38 1838 1845 10.1016/j.jbiomech.2004.08.017 16023471 (Pubitemid 40967960)
45. Stratasys Inc. ABS, 2007.
46. RS Tare D Howard JC Pound HI Roach RO Oreffo 2005 Tissue engineering strategies for cartilage generation-micromass and three dimensional cultures using human chondrocytes and a continuous cell line Biochem. Biophys. Res. Commun. 333 609 621 10.1016/j.bbrc.2005.05.117 1:CAS:528:DC%2BD2MXlsVCgsrs%3D 15946652 (Pubitemid 40848333)
47. CH Turner 1998 Three rules for bone adaptation to mechanical stimuli Bone 23 399 407 10.1016/S8756-3282(98)00118-5 1:STN:280:DyaK1M%2FktVOkuw%3D%3D 9823445 (Pubitemid 28470608)
48. EJ Vanderploeg SM Imler KR Brodkin AJ Garcia ME Levenston 2004 Oscillatory tension differentially modulates matrix metabolism and cytoskeletal organization in chondrocytes and fibrochondrocytes J. Biomech. 37 1941 1952 10.1016/j.jbiomech.2004.02.048 15519602 (Pubitemid 39440506)
49. EJ Vanderploeg CG Wilson ME Levenston 2008 Articular chondrocytes derived from distinct tissue zones differentially respond to in vitro oscillatory tensile loading Osteoarthr. Cartil. 16 1228 1236 10.1016/j.joca.2008.02.016 1:STN:280:DC%2BD1crpslaltw%3D%3D 18400525
50. G Vunjak-Novakovic I Martin B Obradovic S Treppo AJ Grodzinsky R Langer LE Freed 1999 Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage J. Orthop. Res. 17 130 138 10.1002/jor.1100170119 1:STN:280:DyaK1M7ntFKltw%3D%3D 10073657 (Pubitemid 29096015)
51. SD Waldman DC Couto SJ Omelon RA Kandel 2004 Effect of sodium bicarbonate on extracellular pH, matrix accumulation, and morphology of cultured articular chondrocytes Tissue Eng. 10 1633 1640 10.1089/ten.2004.10.1633 1:CAS:528:DC%2BD2MXhtVOrtL4%3D 15684672
52. SD Waldman MD Grynpas RM Pilliar RA Kandel 2002 Characterization of cartilagenous tissue formed on calcium polyphosphate substrates in vitro J. Biomed. Mater. Res. 62 323 330 10.1002/jbm.10235 1:CAS:528:DC%2BD38XntFOktbs%3D 12209917 (Pubitemid 35332195)
53. SD Waldman CG Spiteri MD Grynpas RM Pilliar J Hong RA Kandel 2003 Effect of biomechanical conditioning on cartilaginous tissue formation in vitro J. Bone Joint Surg. Am. 85-A Suppl 2 101 105 12721351
54. SD Waldman CG Spiteri MD Grynpas RM Pilliar RA Kandel 2004 Long-term intermittent compressive stimulation improves the composition and mechanical properties of tissue-engineered cartilage Tissue Eng. 10 1323 1331 1:CAS:528:DC%2BD2cXhtVSgurvF 15588393
55. SD Waldman CG Spiteri MD Grynpas RM Pilliar RA Kandel 2003 Long-term intermittent shear deformation improves the quality of cartilaginous tissue formed in vitro J. Orthop. Res. 21 590 596 10.1016/S0736-0266(03)00009-3 1:CAS:528:DC%2BD3sXkt1OksLY%3D 12798056 (Pubitemid 36758201)
56. RJ Wilkins AC Hall 1995 Control of matrix synthesis in isolated bovine chondrocytes by extracellular and intracellular pH J. Cell. Physiol. 164 474 481 10.1002/jcp.1041640305 1:CAS:528:DyaK2MXnvVemu7s%3D 7650057
57. JF Woessner Jr 1961 The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid Arch. Biochem. Biophys. 93 440 447 10.1016/0003-9861(61)90291-0 1:CAS:528:DyaF3MXht1Ghu7c%3D 13786180
58. M Wong M Siegrist K Goodwin 2003 Cyclic tensile strain and cyclic hydrostatic pressure differentially regulate expression of hypertrophic markers in primary chondrocytes Bone 33 685 693 10.1016/S8756-3282(03)00242-4 1:CAS:528:DC%2BD3sXnvVersLo%3D 14555274 (Pubitemid 37222395)
59. Z Zhang JM McCaffery RG Spencer CA Francomano 2004 Hyaline cartilage engineered by chondrocytes in pellet culture: histological, immunohistochemical and ultrastructural analysis in comparison with cartilage explants J. Anat. 205 229 237 10.1111/j.0021-8782.2004.00327.x 15379928 (Pubitemid 39341580)