Top

Journal of Orthopaedic Surgery and Research

Published in:

Open Access 01-12-2019 | Knee Osteoarthritis | Research article

Viscoelasticity and histology of the human cartilage in healthy and degenerated conditions of the knee

Authors: Michael Seidenstuecker, Julius Watrinet, Anke Bernstein, Norbert P. Suedkamp, Sergio H. Latorre, Anastasija Maks, Hermann O. Mayr

Published in: Journal of Orthopaedic Surgery and Research | Issue 1/2019

Abstract

Background

There are many studies on osteoarthritis, but only a few studies deal with human arthrosis, comparing the mechanical properties of healthy and diseased samples. In most of these studies, only isolated areas of the tibia are examined. There is currently only one study investigating the complete mapping of cartilage tissue but not the difference between instantaneous modulus (IM) in healthy and diseased samples. The aim of this study is to investigate the relationship between the biomechanical and histological changes of articular cartilage in the pathogenesis of osteoarthritis.

Methods

The study compared 25 tibiae with medial gonarthrosis and 13 healthy controls. The IM was determined by automated indentation mapping using a Mach-1 V500css testing machine. A grid was projected over the sample and stored so that all measurements could be taken at the same positions (100 ± 29 positions across the tibiae). This grid was then used to perform the thickness measurement using the needle method. Samples were then taken for histological examinations using a hollow milling machine. Then Giemsa and Safranin O staining were performed. In order to determine the degree of arthrosis according to histological criteria, the assessment was made with regard to Osteoarthritis Research Society International (OARSI) and AHO scores.

Results

A significant difference (p < 0.05) could be observed in the measured IM between the controls with 3.43 ± 0.36 MPa and the samples with 2.09 ± 0.18 MPa. In addition, there was a significant difference in IM in terms of meniscus-covered and meniscus-uncovered areas. The difference in cartilage thickness between 2.25 ± 0.11 mm controls and 2.0 ± 0.07 mm samples was highly significant with p < 0.001. With regard to the OARSI and AHO scores, the samples differed significantly from the controls. The OARSI and AHO scores showed a significant difference between meniscus-covered and meniscus-uncovered areas.

Conclusions

The controls showed significantly better viscoelastic behavior than the arthrotic samples in the measured IM. The measured biomechanical values showed a direct correlation between histological changes and altered biomechanics in gonarthrosis.

Destatis. Gesundheit - fallpauschalenbezogene krankenhausstatistik (drg-statistik) operationen und prozeduren der vollstationären patientinnen und patienten in krankenhäusern (4-steller). Wiesbadem: Statistisches Bundesamt (Destatis); 2016. p. 72.

Bijlsma JW, Berenbaum F, Lafeber FP. Osteoarthritis: an update with relevance for clinical practice. Lancet. 2011;377:2115–26. https://doi.org/10.1016/S0140-6736(11)60243-2.CrossRefPubMed

Roemer FW, Kwoh CK, Fujii T, Hannon MJ, Boudreau RM, Hunter DJ, Eckstein F, John MR, Guermazi A. From early radiographic knee osteoarthritis to joint arthroplasty: determinants of structural progression and symptoms. Arthritis Care Res. 2018. https://doi.org/10.1002/acr.23545.CrossRef

Schiphof D, van den Driest JJ, Runhaar J. Osteoarthritis year in review 2017: Rehabilitation and outcomes. Osteoarthr Cartil. 2018. https://doi.org/10.1016/j.joca.2018.01.006.CrossRef

Mathiessen A, Conaghan PG. Synovitis in osteoarthritis: current understanding with therapeutic implications. Arthritis Res Ther. 2017;19:18. https://doi.org/10.1186/s13075-017-1229-9.CrossRefPubMedPubMedCentral

Thomas E, Peat G, Croft P. Defining and mapping the person with osteoarthritis for population studies and public health. Rheumatology. 2014;53:338–45. https://doi.org/10.1093/rheumatology/ket346.CrossRefPubMed

Roos EM, Arden NK. Strategies for the prevention of knee osteoarthritis. Nat Rev Rheumatol. 2016;12:92–101. https://doi.org/10.1038/nrrheum.2015.135.CrossRefPubMed

Bailey AJ, Mansell JP, Sims TJ, Banse X. Biochemical and mechanical properties of subchondral bone in osteoarthritis. Biorheology. 2004;41:349–58.PubMed

Madry H, van Dijk CN, Mueller-Gerbl M. The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc. 2010;18:419–33. https://doi.org/10.1007/s00167-010-1054-z.CrossRefPubMed

10.

Milz S, Putz R. Quantitative morphology of the subchondral plate of the tibial plateau. J. Anat. 1994;185:103–10.PubMedPubMedCentral

11.

Mezhov V, Teichtahl AJ, Strasser R, Wluka AE, Cicuttini FM. Meniscal pathology - the evidence for treatment. Arthrit Res Ther. 2014;16:206. https://doi.org/10.1186/ar4515.CrossRef

12.

Kummer B. Biomechanik. Form und funktion des bewegungsapparates. Dtsch Arztebl Int. 2006;103:850.

13.

Beaufils P, Becker R, Verdonk R, Aagaard H, Karlsson J. Focusing on results after meniscus surgery. Knee Surg Sports Traumatol Arthrosc. 2015;23:3–7. https://doi.org/10.1007/s00167-014-3471-x.CrossRefPubMed

14.

Pereira H, Caridade SG, Frias AM, Silva-Correia J, Pereira DR, Cengiz IF, Mano JF, Oliveira JM, Espregueira-Mendes J, Reis RL. Biomechanical and cellular segmental characterization of human meniscus: building the basis for tissue engineering therapies. Osteoarthr Cartil. 2014;22:1271–81. https://doi.org/10.1016/j.joca.2014.07.001.CrossRefPubMed

15.

Antons J, Marascio MGM, Nohava J, Martin R, Applegate LA, Bourban PE, Pioletti DP. Zone-dependent mechanical properties of human articular cartilage obtained by indentation measurements. J Mater Sci Mater Med. 2018;29:57. https://doi.org/10.1007/s10856-018-6066-0.CrossRefPubMed

16.

Deneweth JM, Newman KE, Sylvia SM, McLean SG, Arruda EM. Heterogeneity of tibial plateau cartilage in response to a physiological compressive strain rate. J Orth Res. 2013;31:370–5. https://doi.org/10.1002/jor.22226.CrossRef

17.

Chen AC, Bae WC, Schinagl RM, Sah RL. Depth- and strain-dependent mechanical and electromechanical properties of full-thickness bovine articular cartilage in confined compression. J Biomech. 2001;34:1–12. https://doi.org/10.1016/S0021-9290(00)00170-6.CrossRefPubMed

18.

Franke O, Durst K, Maier V, Göken M, Birkholz T, Schneider H, Hennig F, Gelse K. Mechanical properties of hyaline and repair cartilage studied by nanoindentation. Acta Biomater. 2007;3:873–81 https://doi.org/10.1016/j.actbio.2007.04.005.CrossRef

19.

Robinson DL, Kersh ME, Walsh NC, Ackland DC, de Steiger RN, Pandy MG. Mechanical properties of normal and osteoarthritic human articular cartilage. J Mech Behav Biomed Mater. 2016;61:96–109. https://doi.org/10.1016/j.jmbbm.2016.01.015.CrossRefPubMed

20.

Waldstein W, Perino G, Gilbert SL, Maher SA, Windhager R, Boettner F. Oarsi osteoarthritis cartilage histopathology assessment system: a biomechanical evaluation in the human knee. J Orth Res. 2016;34:135–40. https://doi.org/10.1002/jor.23010.CrossRef

21.

Thambyah A, Nather A, Goh J. Mechanical properties of articular cartilage covered by the meniscus. Osteoarthr Cartil. 2006;14:580–8. https://doi.org/10.1016/j.joca.2006.01.015.CrossRefPubMed

22.

Sim S, Chevrier A, Garon M, Quenneville E, Yaroshinsky A, Hoemann CD, Buschmann MD. Non-destructive electromechanical assessment (arthro-bst) of human articular cartilage correlates with histological scores and biomechanical properties. Osteoarthr Cartil. 2014;22:1926–35. https://doi.org/10.1016/j.joca.2014.08.008.CrossRefPubMed

23.

Sim S, Chevrier A, Garon M, Quenneville E, Lavigne P, Yaroshinsky A, Hoemann CD, Buschmann MD. Electromechanical probe and automated indentation maps are sensitive techniques in assessing early degenerated human articular cartilage. J Orth Res. 2017;35:858–67. https://doi.org/10.1002/jor.23330.CrossRef

24.

Kellgren JH, Lawrence JS. Radiological assessment of osteo-arthrosis. Ann Rheum Dis. 1957;16:494–502.CrossRef

25.

Sim S, Chevrier A, Garon M, Quenneville E, Lavigne P, Yaroshinsky A, Hoemann CD, Buschmann MD. Electromechanical probe and automated indentation maps are sensitive techniques in assessing early degenerated human articular cartilage. J Orthop Res. 2016, n/a-n/a. https://doi.org/10.1002/jor.23330.CrossRef

26.

Abedian R, Willbold E, Becher C, Hurschler C. In vitro electro-mechanical characterization of human knee articular cartilage of different degeneration levels: a comparison with icrs and mankin scores. J Biomech. 2013;46:1328–34. https://doi.org/10.1016/j.jbiomech.2013.02.004.CrossRefPubMed

27.

McKee CT, Last JA, Russell P, Murphy CJ. Indentation versus tensile measurements of young’s modulus for soft biological tissues. Tissue Eng Part B Rev. 2011;17:155–64. https://doi.org/10.1089/ten.teb.2010.0520.CrossRefPubMedPubMedCentral

28.

Zhou Y, Tang Y, Hoff T, Garon M, Zhao FY. The verification of the mechanical properties of binder jetting manufactured parts by instrumented indentation testing. Procedia Manufacturing. 2015;1:327–42. https://doi.org/10.1016/j.promfg.2015.09.038.CrossRef

29.

Martin Seitz A, Galbusera F, Krais C, Ignatius A, Durselen L. Stress-relaxation response of human menisci under confined compression conditions. J Mech Behav Biomed Mater. 2013;26:68–80. https://doi.org/10.1016/j.jmbbm.2013.05.027.CrossRefPubMed

30.

Sweigart MA, Zhu CF, Burt DM, DeHoll PD, Agrawal CM, Clanton TO, Athanasiou KA. Intraspecies and interspecies comparison of the compressive properties of the medial meniscus. Ann Biomed Eng. 2004;32:1569–79.CrossRef

31.

Bursać PM, Obitz TW, Eisenberg SR, Stamenović D. Confined and unconfined stress relaxation of cartilage: appropriateness of a transversely isotropic analysis. J Biomech. 1999;32:1125–30. https://doi.org/10.1016/S0021-9290(99)00105-0.CrossRefPubMed

32.

Buschmann MD, Soulhat J, Shirazi-Adl A, Jurvelin JS, Hunziker EB. Confined compression of articular cartilage : linearity in ramp and sinusoidal tests and the importance of interdigitation and incomplete confinement. J Biomech. 1997;31:171–8. https://doi.org/10.1016/S0021-9290(97)00124-3.CrossRef

33.

Patil S, Steklov N, Song L, Bae WC, D'Lima DD. Comparative biomechanical analysis of human and caprine knee articular cartilage. The Knee. 2014;21:119–25. https://doi.org/10.1016/j.knee.2013.03.009.CrossRefPubMed

34.

Griffin MF, Premakumar Y, Seifalian AM, Szarko M, Butler PE. Biomechanical characterisation of the human auricular cartilages; implications for tissue engineering. Ann Biomed Eng. 2016. https://doi.org/10.1007/s10439-016-1688-1.CrossRef

35.

Jurvelin JS, Räsänen T, Kolmonens P, Lyyra T. Comparison of optical, needle probe and ultrasonic techniques for the measurement of articular cartilage thickness. J Biomech. 1995;28:231–5. https://doi.org/10.1016/0021-9290(94)00060-H.CrossRefPubMed

36.

Schmal H, Kowal JM, Kassem M, Seidenstuecker M, Bernstein A, Boettiger K, Xiong T, Suedkamp NP, Kubosch EJ. Comparison of regenerative tissue quality following matrix-associated cell implantation using amplified chondrocytes compared to synovium-derived stem cells in a rabbit model for cartilage lesions. Stem Cells International. 2018;2018:12. https://doi.org/10.1155/2018/4142031.CrossRef

37.

Hayes WC, Keer LM, Herrmann G, Mockros LF. A mathematical analysis for indentation tests of articular cartilage. J Biomech. 1972;5:541–51. https://doi.org/10.1016/0021-9290(72)90010-3.CrossRefPubMed

38.

Schmitz N, Laverty S, Kraus VB, Aigner T. Basic methods in histopathology of joint tissues. Osteoarthr Cartil. 2010;18(Supplement 3):S113–6. https://doi.org/10.1016/j.joca.2010.05.026.CrossRefPubMed

39.

Pritzker KPH, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, Salter D, van den Berg WB. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthr Cartil. 2006;14:13–29. https://doi.org/10.1016/j.joca.2005.07.014.CrossRefPubMed

40.

Glasson SS, Chambers MG, Van Den Berg WB, Little CB. The oarsi histopathology initiative – recommendations for histological assessments of osteoarthritis in the mouse. Osteoarthritis and Cartilage. 2010;18(Supplement 3):S17–23. https://doi.org/10.1016/j.joca.2010.05.025.CrossRefPubMed

41.

Aho O-M, Finnilä M, Thevenot J, Saarakkala S, Lehenkari P. Subchondral bone histology and grading in osteoarthritis. PLOS ONE. 2017;12:e0173726. https://doi.org/10.1371/journal.pone.0173726.CrossRefPubMedPubMedCentral

42.

Faber SC, Eckstein F, Lukasz S, Mühlbauer R, Hohe J, Englmeier K-H, Reiser M. Gender differences in knee joint cartilage thickness, volume and articular surface areas: assessment with quantitative three-dimensional mr imaging. Skeletal Radiol. 2001;30:144–50. https://doi.org/10.1007/s002560000320.CrossRefPubMed

43.

Chen Y, Huang Y-C, Yan CH, Chiu KY, Wei Q, Zhao J, Guo XE, Leung F, Lu WW. Abnormal subchondral bone remodeling and its association with articular cartilage degradation in knees of type 2 diabetes patients. Bone Res. 2017;5:17034. https://doi.org/10.1038/boneres.2017.34.CrossRefPubMedPubMedCentral

Title: Viscoelasticity and histology of the human cartilage in healthy and degenerated conditions of the knee
Authors: Michael Seidenstuecker
Julius Watrinet
Anke Bernstein
Norbert P. Suedkamp
Sergio H. Latorre
Anastasija Maks
Hermann O. Mayr
Publication date: 01-12-2019
Publisher: BioMed Central
Keywords: Knee Osteoarthritis
Osteoarthrosis
Osteoarthrosis
Knee Osteoarthritis
Published in: Journal of Orthopaedic Surgery and Research / Issue 1/2019
Electronic ISSN: 1749-799X
DOI: https://doi.org/10.1186/s13018-019-1308-5

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Viscoelasticity and histology of the human cartilage in healthy and degenerated conditions of the knee

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2019

Correction to: The 2018 new definition of periprosthetic joint infection improves the diagnostic efficiency in the Chinese population

Microwaves increase the effectiveness of systemic antibiotic treatment in acute bone infection: experimental study in a rat model

Lateral wall osteotomy combined with embedded biodegradable implants for displaced intra-articular calcaneal fractures

A systematic review of the single-stage treatment of chronic osteomyelitis

Correction to: Treatment of cam-type femoroacetabular impingement using anterolateral mini-open and arthroscopic osteochondroplasty

Letter to the editor regarding “Is minimally invasive superior than open transforaminal lumbar interbody fusion for single-level degenerative lumbar diseases: a meta-analysis”