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The Role of Buckling Instabilities in the Global and Local Mechanical Response in Porous Collagen Scaffolds

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Abstract

Background

Porous polymer scaffolds are commonly used for regenerative medicine and tissue-engineered therapies in the repair and regeneration of structural tissues which require sufficient mechanical integrity to resist loading prior to tissue ingrowth. 

Objective

Investigate the connection between scaffold architecture and mechanical response of collagen scaffolds used in human tissue-engineered cartilage.

Methods

We performed multi-scale mechanical analysis on two types of porous collagen scaffolds with honeycomb and sponge architectures. Confined compression testing was used to assess global non-linear mechanical response of scaffolds. Additionally, we performed confocal strain mapping combined with digital image correlation (DIC) to visualize local mechanical instabilities and compared local strain distributions between scaffold architectures.

Results

The global response of both scaffold architectures followed a pattern characteristic of cellular solids, with a linear region, a plateau region, and a densification region. Macro-scale non-linear responses corresponded to local-scale instabilities such as snap-through buckling. On the local-scale, a construct’s compressive response depended heavily on the architecture type. Scaffolds with honeycomb architecture experienced a unimodal strain distribution throughout the scaffold depth. In contrast, scaffolds with sponge architecture tended to collapse at the boundaries.

Conclusions

We demonstrated that differences in mechanical response between scaffold architectures were detected primarily at the micro-scale which stems from the disparity in pore architecture. As such, tools like confocal strain mapping combined with DIC are critical for designing and optimizing architectures for porous materials. Observing local instabilities in porous materials is important not only for tuning mechanical response, but also for controlling mechanical events that influence cellular and tissue behavior.

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References

  1. Hunziker EB, Lippuner K, Keel MJB, Shintani N (2015) An educational review of cartilage repair: Precepts & practice - myths & misconceptions - progress & prospects. Osteoarthritis Cartilage 23:334–350. https://doi.org/10.1016/j.joca.2014.12.011

    Article  Google Scholar 

  2. Brittberg M (2010) Cell carriers as the next generation of cell therapy for cartilage repair: A review of the matrix-induced autologous chondrocyte implantation procedure. Am J Sports Med 38:1259–1271. https://doi.org/10.1177/0363546509346395

    Article  Google Scholar 

  3. O’Brien FJ, Harley BA, Yannas IV, Gibson LJ (2005) The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials. https://doi.org/10.1016/j.biomaterials.2004.02.052

    Article  Google Scholar 

  4. Harley BAC, Gibson LJ (2008) In vivo and in vitro applications of collagen-GAG scaffolds. Chem Eng J 137:102–121. https://doi.org/10.1016/j.cej.2007.09.009

    Article  Google Scholar 

  5. Crawford DC, Heveran CM, Cannon WD et al (2009) An Autologous Cartilage Tissue Implant NeoCart for Treatment of Grade III Chondral Injury to the Distal Femur. Am J Sports Med 37:1334–1343. https://doi.org/10.1177/0363546509333011

    Article  Google Scholar 

  6. Kon E, Filardo G, Di Martino A, Marcacci M (2012) ACI and MACI. J Knee Surg 25:17–22. https://doi.org/10.1055/s-0031-1299651

    Article  Google Scholar 

  7. Crawford DC, DeBerardino TM, Williams RJ (2012) NeoCart, an autologous cartilage tissue implant, compared with microfracture for treatment of distal femoral cartilage lesions: An FDA phase-II prospective, randomized clinical trial after two years. Journal of Bone and Joint Surgery - Series A 94:979–989. https://doi.org/10.2106/JBJS.K.00533

    Article  Google Scholar 

  8. Bingham JT, Papannagari R, Van de velde SK, et al (2008) In vivo cartilage contact deformation in the healthy human tibiofemoral joint. Rheumatology 47:1622–1627. https://doi.org/10.1093/rheumatology/ken345

    Article  Google Scholar 

  9. Chan DD, Cai L, Butz KD et al (2016) In vivo articular cartilage deformation: Noninvasive quantification of intratissue strain during joint contact in the human knee. Sci Rep 6:1–14. https://doi.org/10.1038/srep19220

    Article  Google Scholar 

  10. Butz KD, Chan DD, Nauman EA, Neu CP (2011) Stress distributions and material properties determined in articular cartilage from MRI-based finite strains. J Biomech 44:2667–2672. https://doi.org/10.1016/j.jbiomech.2011.08.005

    Article  Google Scholar 

  11. Middendorf JM, Diamantides N, Shortkroff S et al (2020) Multiscale Mechanics of Tissue Engineered Cartilage Grown from Human Chondrocytes and Human Induced Pluripotent Stem Cells. J Orthop Res jor 24643. https://doi.org/10.1002/jor.24643

  12. Harley BA, Freyman TM, Wong MQ, Gibson LJ (2007) A new technique for calculating individual dermal fibroblast contractile forces generated within collagen-GAG scaffolds. Biophys J 93:2911–2922. https://doi.org/10.1529/biophysj.106.095471

    Article  Google Scholar 

  13. Middendorf JM, Shortkroff S, Dugopolski C et al (2017) In vitro culture increases mechanical stability of human tissue engineered cartilage constructs by prevention of microscale scaffold buckling. J Biomech 64:77–84. https://doi.org/10.1016/j.jbiomech.2017.09.007

    Article  Google Scholar 

  14. Bartell LR, Fortier LA, Bonassar LJ, Cohen I (2015) Measuring microscale strain fields in articular cartilage during rapid impact reveals thresholds for chondrocyte death and a protective role for the superficial layer. J Biomech 48:3440–3446. https://doi.org/10.1016/j.jbiomech.2015.05.035

    Article  Google Scholar 

  15. Gibson LJ (2005) Biomechanics of cellular solids. J Biomech 38:377–399. https://doi.org/10.1016/j.jbiomech.2004.09.027

    Article  Google Scholar 

  16. Gaitanaros S, Kyriakides S, Kraynik AM (2018) On the crushing of polydisperse foams. European Journal of Mechanics, A/Solids 67:243–253. https://doi.org/10.1016/j.euromechsol.2017.09.010

    Article  Google Scholar 

  17. Dong C, Lv Y (2016) Application of collagen scaffold in tissue engineering: Recent advances and new perspectives. Polymers 8:1–20. https://doi.org/10.3390/polym8020042

    Article  Google Scholar 

  18. Chan EC, Kuo SM, Kong AM et al (2016) Three dimensional collagen scaffold promotes intrinsic vascularisation for tissue engineering applications. PLoS ONE 11:1–15. https://doi.org/10.1371/journal.pone.0149799

    Article  Google Scholar 

  19. George J, Onodera J, Miyata T (2008) Biodegradable honeycomb collagen scaffold for dermal tissue engineering. Journal of Biomedical Materials Research - Part A 87:1103–1111. https://doi.org/10.1002/jbm.a.32277

    Article  Google Scholar 

  20. Zhang Q, Lu H, Kawazoe N, Chen G (2014) Pore size effect of collagen scaffolds on cartilage regeneration. Acta Biomater 10:2005–2013. https://doi.org/10.1016/j.actbio.2013.12.042

    Article  Google Scholar 

  21. Middendorf JM, Dugopolski C, Kennedy S et al (2020) Heterogeneous matrix deposition in human tissue engineered cartilage changes the local shear modulus and resistance to local construct buckling. J Biomech 105:109760. https://doi.org/10.1016/j.jbiomech.2020.109760

    Article  Google Scholar 

  22. Buckley MR, Gleghorn JP, Bonassar LJ, Cohen I (2008) Mapping the depth dependence of shear properties in articular cartilage. J Biomech 41:2430–2437. https://doi.org/10.1016/j.jbiomech.2008.05.021

    Article  Google Scholar 

  23. Buckley MR, Bergou AJ, Fouchard J et al (2010) High-resolution spatial mapping of shear properties in cartilage. J Biomech 43:796–800. https://doi.org/10.1016/j.jbiomech.2009.10.012

    Article  Google Scholar 

  24. Middendorf JM, Bonassar LJ, Bartell LR, Cohen I (2019) Methods for determining tissue engineered construct readiness

  25. Middendorf JM, Griffin DJ, Shortkroff S et al (2017) Mechanical properties and structure-function relationships of human chondrocyte-seeded cartilage constructs after in vitro culture. J Orthop Res 35:2298–2306. https://doi.org/10.1002/jor.23535

    Article  Google Scholar 

  26. Blaber J, Adair B, Antoniou A (2015) Ncorr: Open-Source 2D Digital Image Correlation Matlab Software. Exp Mech 55:1105–1122. https://doi.org/10.1007/s11340-015-0009-1

    Article  Google Scholar 

  27. Crawford R, Jones GF, You L, Wu Q (2011) Compression-dependent permeability measurement for random soft porous media and its implications to lift generation. Chem Eng Sci 66:294–302. https://doi.org/10.1016/j.ces.2010.10.037

    Article  Google Scholar 

  28. Lin ASP, Barrows TH, Cartmell SH, Guldberg RE (2003) Microarchitectural and mechanical characterization of oriented porous polymer scaffolds. Biomaterials 24:481–489. https://doi.org/10.1016/S0142-9612(02)00361-7

    Article  Google Scholar 

  29. Javid F, Liu J, Shim J et al (2016) Mechanics of instability-induced pattern transformations in elastomeric porous cylinders. J Mech Phys Solids 96:1–17. https://doi.org/10.1016/j.jmps.2016.06.015

    Article  MathSciNet  Google Scholar 

  30. Salisbury C, Cronin D, Lien F-S (2015) Deformation Mechanics of a Non-Linear Hyper-Viscoelastic Porous Material, Part II: Porous Material Micro-Scale Model. J dynamic behavior mater 1:249–258. https://doi.org/10.1007/s40870-015-0027-1

    Article  Google Scholar 

  31. Mercer C, He MY, Wang R, Evans AG (2006) Mechanisms governing the inelastic deformation of cortical bone and application to trabecular bone. Acta Biomater 2:59–68. https://doi.org/10.1016/j.actbio.2005.08.004

    Article  Google Scholar 

  32. Kee Paik J, Thayamballi AK, Sung Kim G (1999) Strength characteristics of aluminum honeycomb sandwich panels. Thin-Walled Structures 35:205–231. https://doi.org/10.1016/S0263-8231(99)00026-9

    Article  Google Scholar 

  33. Cai L, Zhang D, Zhou S, Xu W (2018) Investigation on Mechanical Properties and Equivalent Model of Aluminum Honeycomb Sandwich Panels. J Mater Eng Perform 27:6585–6596. https://doi.org/10.1007/s11665-018-3771-2

    Article  Google Scholar 

  34. Ashab ASM, Ruan D, Lu G et al (2015) Experimental investigation of the mechanical behavior of aluminum honeycombs under quasi-static and dynamic indentation. Mater Des 74:138–149. https://doi.org/10.1016/j.matdes.2015.03.004

    Article  Google Scholar 

  35. Wilbert A, Jang WY, Kyriakides S, Floccari JF (2011) Buckling and progressive crushing of laterally loaded honeycomb. Int J Solids Struct 48:803–816. https://doi.org/10.1016/j.ijsolstr.2010.11.014

    Article  MATH  Google Scholar 

  36. Gaitanaros S, Kyriakides S, Kraynik AM (2012) On the crushing response of random open-cell foams. In: Int J Solids and Struct 2733–2743

  37. Jang WY, Kyriakides S (2015) On the buckling and crushing of expanded honeycomb. Int J Mech Sci 91:81–90. https://doi.org/10.1016/j.ijmecsci.2014.02.008

    Article  Google Scholar 

  38. Harley BA, Leung JH, Silva ECCM, Gibson LJ (2007) Mechanical characterization of collagen-glycosaminoglycan scaffolds. Acta Biomater 3:463–474. https://doi.org/10.1016/j.actbio.2006.12.009

    Article  Google Scholar 

  39. Itoh H, Aso Y, Furuse M et al (2001) A honeycomb collagen carrier for cell culture as a tissue engineering scaffold. Artif Organs 25:213–217. https://doi.org/10.1046/j.1525-1594.2001.025003213.x

    Article  Google Scholar 

  40. Freed LE, Vunjak-Novakovic G, Biron RJ et al (1994) Biodegradable Polymer Scaffolds for Tissue Engineering

  41. Freyman TM, Yannas IV, Gibson LJ (2001) Cellular materials as porous scaffolds for tissue engineering. Prog Mater Sci 46:273–282. https://doi.org/10.1016/S0079-6425(00)00018-9

    Article  Google Scholar 

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Acknowledgements

This study is partially funded by NSF CMMI 2129776 and Histogenics Corp.

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Authors and Affiliations

  1. Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, NY, USA

    B. Kim, J. M. Middendorf, N. Bouklas & L. J. Bonassar

  2. Meinig School of Biomedical Engineering, Cornell University, Ithaca, NY, USA

    N. Diamantides & L. J. Bonassar

  3. Histogenics Corporation, Waltham, MA, USA

    C. Dugopolski, S. Kennedy & E. Blahut

  4. Department of Physics, Cornell University, Ithaca, NY, USA

    I. Cohen

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Correspondence to L. J. Bonassar.

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Conflicts of Interest

C.D., S.K., E.B., were full time employees and stockholders of Histogenics Corp. B.K., N.D., J.M., and L.J.B., were partially funded by an award from Histogenics to Cornell University.

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Kim, B., Middendorf, J.M., Diamantides, N. et al. The Role of Buckling Instabilities in the Global and Local Mechanical Response in Porous Collagen Scaffolds. Exp Mech 62, 1067–1077 (2022). https://doi.org/10.1007/s11340-022-00853-7

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