Adaptable test bench for ASTM-compliant permeability measurement of porous scaffolds for tissue engineering.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
19 Jan 2024
Historique:
received: 24 10 2023
accepted: 15 01 2024
medline: 20 1 2024
pubmed: 20 1 2024
entrez: 19 1 2024
Statut: epublish

Résumé

Intrinsic permeability describes the ability of a porous medium to be penetrated by a fluid. Considering porous scaffolds for tissue engineering (TE) applications, this macroscopic variable can strongly influence the transport of oxygen and nutrients, the cell seeding process, and the transmission of fluid forces to the cells, playing a crucial role in determining scaffold efficacy. Thus, accurately measuring the permeability of porous scaffolds could represent an essential step in their optimization process. In literature, several methods have been proposed to characterize scaffold permeability. Most of the currently adopted approaches to assess permeability limit their applicability to specific scaffold structures, hampering protocols standardization, and ultimately leading to incomparable results among different laboratories. The content of novelty of this study is in the proposal of an adaptable test bench and in defining a specific testing protocol, compliant with the ASTM International F2952-22 guidelines, for reliable and repeatable measurements of the intrinsic permeability of TE porous scaffolds. The developed permeability test bench (PTB) exploits the pump-based method, and it is composed of a modular permeability chamber integrated within a closed-loop hydraulic circuit, which includes a peristaltic pump and pressure sensors, recirculating demineralized water. A specific testing protocol was defined for characterizing the pressure drop associated with the scaffold under test, while minimizing the effects of uncertainty sources. To assess the operational capabilities and performance of the proposed test bench, permeability measurements were conducted on PLA scaffolds with regular (PS) and random (RS) micro-architecture and on commercial bovine bone matrix-derived scaffolds (CS) for bone TE. To validate the proposed approach, the scaffolds were as well characterized using an alternative test bench (ATB) based on acoustic measurements, implementing a blind randomized testing procedure. The consistency of the permeability values measured using both the test benches demonstrated the reliability of the proposed approach. A further validation of the PTB's measurement reliability was provided by the agreement between the measured permeability values of the PS scaffolds and the theory-based predicted permeability value. Once validated the proposed PTB, the performed measurements allowed the investigation of the scaffolds' transport properties. Samples with the same structure (guaranteed by the fused-deposition modeling technique) were characterized by similar permeability values, and CS and RS scaffolds showed permeability values in agreement with the values reported in the literature for bovine trabecular bone. In conclusion, the developed PTB and the proposed testing protocol allow the characterization of the intrinsic permeability of porous scaffolds of different types and dimensions under controlled flow regimes, representing a powerful tool in view of providing a reliable and repeatable framework for characterizing and optimizing scaffolds for TE applications.

Identifiants

pubmed: 38242930
doi: 10.1038/s41598-024-52159-4
pii: 10.1038/s41598-024-52159-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1722

Informations de copyright

© 2024. The Author(s).

Références

Vacanti, J. P. & Langer, R. Tissue engineering: The design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet 354, S32–S34 (1999).
doi: 10.1016/S0140-6736(99)90247-7
Amini, A. R., Laurencin, C. T. & Nukavarapu, S. P. Bone tissue engineering: Recent advances and challenges. Crit. Rev. Biomed. Eng. 40, 363–408 (2012).
pubmed: 23339648 pmcid: 3766369 doi: 10.1615/CritRevBiomedEng.v40.i5.10
Truskey, G. A., Yuan, F. & Katz, D. F. Transport Phenomena in Biological Systems (Pearson/Prentice Hall, 2004).
Hollister, S. J. Porous scaffold design for tissue engineering. Nat. Mater. 4, 518–524 (2005).
pubmed: 16003400 doi: 10.1038/nmat1421
O’Brien, F. J. et al. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol. Health Care Off. J. Eur. Soc. Eng. Med. 15, 3–17 (2007).
Abbasi, N., Hamlet, S., Love, R. M. & Nguyen, N.-T. Porous scaffolds for bone regeneration. J. Sci. Adv. Mater. Dev. 5, 1–9 (2020).
Mattei, G., Magliaro, C., Pirone, A. & Ahluwalia, A. Bioinspired liver scaffold design criteria. Organogenesis 14, 129–146 (2018).
pubmed: 30156955 pmcid: 6300109 doi: 10.1080/15476278.2018.1505137
Zhao, F., Lacroix, D., Ito, K., van Rietbergen, B. & Hofmann, S. Changes in scaffold porosity during bone tissue engineering in perfusion bioreactors considerably affect cellular mechanical stimulation for mineralization. Bone Rep. 12, 100265 (2020).
pubmed: 32613033 pmcid: 7315008 doi: 10.1016/j.bonr.2020.100265
Dias, M. R., Fernandes, P. R., Guedes, J. M. & Hollister, S. J. Permeability analysis of scaffolds for bone tissue engineering. J. Biomech. 45, 938–944 (2012).
pubmed: 22365847 doi: 10.1016/j.jbiomech.2012.01.019
Kelly, C. N., Miller, A. T., Hollister, S. J., Guldberg, R. E. & Gall, K. Design and structure-function characterization of 3D printed synthetic porous biomaterials for tissue engineering. Adv. Healthc. Mater. 7, 1701095 (2018).
doi: 10.1002/adhm.201701095
Chor, M. V. & Li, W. A permeability measurement system for tissue engineering scaffolds. Meas. Sci. Technol. 18, 208–216 (2007).
doi: 10.1088/0957-0233/18/1/026
Massai, D. et al. Image-based three-dimensional analysis to characterize the texture of porous scaffolds. BioMed Res. Int. 2014, e161437 (2014).
doi: 10.1155/2014/161437
Li, S., de Wijn, J. R., Li, J., Layrolle, P. & de Groot, K. Macroporous biphasic calcium phosphate scaffold with high permeability/porosity ratio. Tissue Eng. 9, 535–548 (2003).
pubmed: 12857421 doi: 10.1089/107632703322066714
Nield, D. A. & Bejan, A. Convection in Porous Media (Springer, 2006).
Rahbari, A., Montazerian, H., Davoodi, E. & Homayoonfar, S. Predicting permeability of regular tissue engineering scaffolds: Scaling analysis of pore architecture, scaffold length, and fluid flow rate effects. Comput. Methods Biomech. Biomed. Eng. 20, 231–241 (2017).
doi: 10.1080/10255842.2016.1215436
Vossenberg, P., Higuera, G. A., van Straten, G., van Blitterswijk, C. A. & van Boxtel, A. J. B. Darcian permeability constant as indicator for shear stresses in regular scaffold systems for tissue engineering. Biomech. Model. Mechanobiol. 8, 499–507 (2009).
pubmed: 19360445 doi: 10.1007/s10237-009-0153-6
Agrawal, C. M., McKinney, J. S., Lanctot, D. & Athanasiou, K. A. Effects of fluid flow on the in vitro degradation kinetics of biodegradable scaffolds for tissue engineering. Biomaterials 21, 2443–2452 (2000).
pubmed: 11055292 doi: 10.1016/S0142-9612(00)00112-5
Nasrollahzadeh, N., Applegate, L. A. & Pioletti, D. P. Development of an effective cell seeding technique: Simulation, implementation, and analysis of contributing factors. Tissue Eng. Part C Methods 23, 485–496 (2017).
pubmed: 28602135 doi: 10.1089/ten.tec.2017.0108
Truscello, S. et al. Prediction of permeability of regular scaffolds for skeletal tissue engineering: A combined computational and experimental study. Acta Biomater. 8, 1648–1658 (2012).
pubmed: 22210520 doi: 10.1016/j.actbio.2011.12.021
Wittkowske, C., Reilly, G. C., Lacroix, D. & Perrault, C. M. In vitro bone cell models: Impact of fluid shear stress on bone formation. Front. Bioeng. Biotechnol. 4, 14 (2016).
doi: 10.3389/fbioe.2016.00087
Fan, J., Jia, X., Huang, Y., Fu, B. M. & Fan, Y. Greater scaffold permeability promotes growth of osteoblastic cells in a perfused bioreactor. J. Tissue Eng. Regen. Med. 9, E210–E218 (2015).
pubmed: 23349107 doi: 10.1002/term.1701
Jeong, C. G. & Hollister, S. J. Mechanical, permeability, and degradation properties of 3D designed poly(1,8 octanediol-co-citrate) scaffolds for soft tissue engineering. J. Biomed. Mater. Res. B Appl. Biomater. 93B, 141–149 (2010).
Pennella, F. et al. A survey of methods for the evaluation of tissue engineering scaffold permeability. Ann. Biomed. Eng. 41, 2027–2041 (2013).
pubmed: 23612914 doi: 10.1007/s10439-013-0815-5
Innocentini, M. D. M. et al. Permeability of porous gelcast scaffolds for bone tissue engineering. J. Porous Mater. 17, 615–627 (2010).
doi: 10.1007/s10934-009-9331-2
Wang, Y., Tomlins, P. E., Coombes, A. G. A. & Rides, M. On the determination of Darcy permeability coefficients for a microporous tissue scaffold. Tissue Eng. Part C Methods 16, 281–289 (2010).
pubmed: 19922263 doi: 10.1089/ten.tec.2009.0116
Offeddu, G. S., Ashworth, J. C., Cameron, R. E. & Oyen, M. L. Structural determinants of hydration, mechanics and fluid flow in freeze-dried collagen scaffolds. Acta Biomater. 41, 193–203 (2016).
pubmed: 27255358 doi: 10.1016/j.actbio.2016.05.024
Mohee, L., Offeddu, G. S., Husmann, A., Oyen, M. L. & Cameron, R. E. Investigation of the intrinsic permeability of ice-templated collagen scaffolds as a function of their structural and mechanical properties. Acta Biomater. 83, 189–198 (2019).
pubmed: 30366136 doi: 10.1016/j.actbio.2018.10.034
Lipowiecki, M. et al. Permeability of rapid prototyped artificial bone scaffold structures. J. Biomed. Mater. Res. A 102, 4127–4135 (2014).
pubmed: 24443032 doi: 10.1002/jbm.a.35084
Nasrollahzadeh, N. & Pioletti, D. P. Experimental method to characterize the strain dependent permeability of tissue engineering scaffolds. J. Biomech. 49, 3749–3752 (2016).
pubmed: 27720229 doi: 10.1016/j.jbiomech.2016.09.021
Sanz-Herrera, J. A. et al. Mechanical and flow characterization of Sponceram
Ochoa, I. et al. Permeability evaluation of 45S5 Bioglass
pubmed: 19105999 doi: 10.1016/j.jbiomech.2008.10.030
Podichetty, J. T., Bhaskar, P. R., Khalf, A. & Madihally, S. V. Modeling pressure drop using generalized scaffold characteristics in an axial-flow bioreactor for soft tissue regeneration. Ann. Biomed. Eng. 42, 1319–1330 (2014).
pubmed: 24719051 doi: 10.1007/s10439-014-1009-5
Santos, J., Pires, T., Gouveia, B. P., Castro, A. P. G. & Fernandes, P. R. On the permeability of TPMS scaffolds. J. Mech. Behav. Biomed. Mater. 110, 103932 (2020).
pubmed: 32957226 doi: 10.1016/j.jmbbm.2020.103932
ASTM International F2952–22. Guide for Determining the Mean Darcy Permeability Coefficient for a Porous Tissue Scaffold. https://doi.org/10.1520/F2952-22 (2022).
Schiavi, A., Guglielmone, C., Pennella, F. & Morbiducci, U. Acoustic method for permeability measurement of tissue-engineering scaffold. Meas. Sci. Technol. 23, 105702 (2012).
doi: 10.1088/0957-0233/23/10/105702
Fiume, E. et al. Comprehensive assessment of bioactive glass and glass-ceramic scaffold permeability: Experimental measurements by pressure wave drop, modelling and computed tomography-based analysis. Acta Biomater. 119, 405–418 (2021).
pubmed: 33091624 doi: 10.1016/j.actbio.2020.10.027
Fernandez, M., Vink, J., Yoshida, K., Wapner, R. & Myers, K. M. Direct measurement of the permeability of human cervical tissue. J. Biomech. Eng. 135, 3 (2013).
doi: 10.1115/1.4023380
Fujie, H. & Imade, K. Effects of low tangential permeability in the superficial layer on the frictional property of articular cartilage. Biosurf. Biotribol. 1, 124–129 (2015).
doi: 10.1016/j.bsbt.2015.06.001
Benalla, M., Palacio-Mancheno, P. E., Fritton, S. P., Cardoso, L. & Cowin, S. C. Dynamic permeability of the lacunar–canalicular system in human cortical bone. Biomech. Model. Mechanobiol. 13, 801–812 (2014).
pubmed: 24146291 doi: 10.1007/s10237-013-0535-7
Grimm, M. J. & Williams, J. L. Measurements of permeability in human calcaneal trabecular bone. J. Biomech. 30, 743–745 (1997).
pubmed: 9239556 doi: 10.1016/S0021-9290(97)00016-X
Kleinhans, K. L. & Jackson, A. R. Hydraulic permeability of meniscus fibrocartilage measured via direct permeation: Effects of tissue anisotropy, water volume content, and compressive strain. J. Biomech. 72, 215–221 (2018).
pubmed: 29605083 doi: 10.1016/j.jbiomech.2018.03.011
Pecci, R., Baiguera, S., Ioppolo, P., Bedini, R. & Del Gaudio, C. 3D printed scaffolds with random microarchitecture for bone tissue engineering applications: Manufacturing and characterization. J. Mech. Behav. Biomed. Mater. 103, 103583 (2020).
pubmed: 32090912 doi: 10.1016/j.jmbbm.2019.103583
Zenobi, E. et al. Tailoring the microarchitectures of 3D printed bone-like scaffolds for tissue engineering applications. Bioengineering 10, 567 (2023).
pubmed: 37237637 pmcid: 10215619 doi: 10.3390/bioengineering10050567
Perale, G. et al. Biomimetic biomolecules in next generation xeno-hybrid bone graft material show enhanced in vitro bone cells response. J. Clin. Med. 8, 2159 (2019).
pubmed: 31817744 pmcid: 6947180 doi: 10.3390/jcm8122159
Bear, J. Dynamics of Fluids in Porous Media (Dover, 1988).
Fand, R. M., Kim, B. Y. K., Lam, A. C. C. & Phan, R. T. Resistance to the flow of fluids through simple and complex porous media whose matrices are composed of randomly packed spheres. J. Fluids Eng. 109, 268–273 (1987).
doi: 10.1115/1.3242658
Dybbs, A. & Edwards, R. V. A new look at porous media fluid mechanics—Darcy to turbulent. In Fundamentals of Transport Phenomena in Porous Media (eds. Bear, J. & Corapcioglu, M. Y.). 199–256 https://doi.org/10.1007/978-94-009-6175-3_4 (Springer Netherlands, 1984).
JCGM 100:2008 (GUM 1995 with minor corrections). Evaluation of Measurement Data—Guide to the Expression of Uncertainty in Measurement (2008).
ISO/IEC 17043:2023. Conformity Assessment. General Requirements for the Competence of Proficiency Testing Providers (2023).
JCGM 200:2012. International Vocabulary of Metrology—Basic and General Concepts and Associated Terms (VIM) (2012).
Kozeny, J. Uber Kapillare Leitung der Wasser in Boden. R. Acad. Sci. Vienna Proc. Cl. I(136), 271–306 (1927).
Carman, P. C. Fluid flow through granular beds. Chem. Eng. Res. Des. 75, S32–S48 (1937).
doi: 10.1016/S0263-8762(97)80003-2
Mauret, E. & Renaud, M. Transport phenomena in multi-particle systems—I. Limits of applicability of capillary model in high voidage beds-application to fixed beds of fibers and fluidized beds of spheres. Chem. Eng. Sci. 52, 1807–1817 (1997).
doi: 10.1016/S0009-2509(96)00499-X
Ghanbarian, B., Hunt, A. G., Ewing, R. P. & Sahimi, M. Tortuosity in porous media: A critical review. Soil Sci. Soc. Am. J. 77, 1461–1477 (2013).
doi: 10.2136/sssaj2012.0435
Comiti, J. & Renaud, M. A new model for determining mean structure parameters of fixed beds from pressure drop measurements: Application to beds packed with parallelepipedal particles. Chem. Eng. Sci. 44, 1539–1545 (1989).
doi: 10.1016/0009-2509(89)80031-4
Hussaini, S. R. & Dvorkin, J. Specific surface area versus porosity from digital images. J. Pet. Sci. Eng. 196, 107773 (2021).
doi: 10.1016/j.petrol.2020.107773
Nakayama, A., Kuwahara, F. & Sano, Y. Concept of equivalent diameter for heat and fluid flow in porous media. AIChE J. 53, 732–736 (2007).
doi: 10.1002/aic.11092
Lam, R. C. & Kardos, J. L. The permeability and compressibility of aligned and cross-plied carbon fiber beds during processing of composites. Polym. Eng. Sci. 31, 1064–1070 (1991).
doi: 10.1002/pen.760311411
Kohles, S. S. et al. Direct perfusion measurements of cancellous bone anisotropic permeability. J. Biomech. 34, 1197–1202 (2001).
pubmed: 11506790 doi: 10.1016/S0021-9290(01)00082-3
Prakoso, A. T. et al. The effect of tortuosity on permeability of porous scaffold. Biomedicines 11, 427 (2023).
pubmed: 36830961 pmcid: 9953537 doi: 10.3390/biomedicines11020427
Lim, T.-H. & Hong, J. H. Poroelastic properties of bovine vertebral trabecular bone. J. Orthop. Res. 18, 671–677 (2000).
pubmed: 11052505 doi: 10.1002/jor.1100180421
Nauman, E. A., Fong, K. E. & Keaveny, T. M. Dependence of intertrabecular permeability on flow direction and anatomic site. Ann. Biomed. Eng. 27, 517–524 (1999).
pubmed: 10468236 doi: 10.1114/1.195
Gabetti, S. et al. An automated 3D-printed perfusion bioreactor combinable with pulsed electromagnetic field stimulators for bone tissue investigations. Sci. Rep. 12, 13859 (2022).
pubmed: 35974079 pmcid: 9381575 doi: 10.1038/s41598-022-18075-1
Ledda, M. et al. Biological response to bioinspired microporous 3D-printed scaffolds for bone tissue engineering. Int. J. Mol. Sci. 23, 5383 (2022).
pubmed: 35628195 pmcid: 9140815 doi: 10.3390/ijms23105383
Yamada, S., Yassin, M. A., Schwarz, T., Mustafa, K. & Hansmann, J. Optimization and validation of a custom-designed perfusion bioreactor for bone tissue engineering: Flow assessment and optimal culture environmental conditions. Front. Bioeng. Biotechnol. 10, 811942 (2022).
pubmed: 35402393 pmcid: 8990132 doi: 10.3389/fbioe.2022.811942
Born, G. et al. Mini- and macro-scale direct perfusion bioreactors with optimized flow for engineering 3D tissues. Biotechnol. J. 1, 2200405 (2022).
Pires, T. et al. Numerical–experimental analysis of the permeability–porosity relationship in triply periodic minimal surfaces scaffolds. J. Biomech. 117, 110263 (2021).
pubmed: 33493715 doi: 10.1016/j.jbiomech.2021.110263
d’Adamo, A. et al. Experimental measurements and CFD modelling of hydroxyapatite scaffolds in perfusion bioreactors for bone regeneration. Regen. Biomater. 10, rbad002 (2023).

Auteurs

Stefano Gabetti (S)

Department of Mechanical and Aerospace Engineering and PolitoBIOMed Lab, Politecnico di Torino, Corso Duca Degli Abruzzi, 24, 10129, Turin, Italy.
Centro 3R, Interuniversity Center for the Promotion of the 3Rs Principles in Teaching and Research, Turin, Italy.

Beatrice Masante (B)

Department of Mechanical and Aerospace Engineering and PolitoBIOMed Lab, Politecnico di Torino, Corso Duca Degli Abruzzi, 24, 10129, Turin, Italy.
Centro 3R, Interuniversity Center for the Promotion of the 3Rs Principles in Teaching and Research, Turin, Italy.
Department of Surgical Sciences, CIR-Dental School, University of Turin, Turin, Italy.

Alessandro Schiavi (A)

Applied Metrology and Engineering Division, INRiM-National Institute of Metrological Research, Turin, Italy.

Elisa Scatena (E)

E. Amaldi Foundation, Rome, Italy.

Eleonora Zenobi (E)

E. Amaldi Foundation, Rome, Italy.

Simone Israel (S)

Department of Mechanical and Aerospace Engineering and PolitoBIOMed Lab, Politecnico di Torino, Corso Duca Degli Abruzzi, 24, 10129, Turin, Italy.
Centro 3R, Interuniversity Center for the Promotion of the 3Rs Principles in Teaching and Research, Turin, Italy.

Alessandro Sanginario (A)

Department of Electronics and Telecommunications, Politecnico di Torino, Turin, Italy.

Costantino Del Gaudio (C)

Italian Space Agency, Rome, Italy.

Alberto Audenino (A)

Department of Mechanical and Aerospace Engineering and PolitoBIOMed Lab, Politecnico di Torino, Corso Duca Degli Abruzzi, 24, 10129, Turin, Italy.
Centro 3R, Interuniversity Center for the Promotion of the 3Rs Principles in Teaching and Research, Turin, Italy.

Umberto Morbiducci (U)

Department of Mechanical and Aerospace Engineering and PolitoBIOMed Lab, Politecnico di Torino, Corso Duca Degli Abruzzi, 24, 10129, Turin, Italy.
Centro 3R, Interuniversity Center for the Promotion of the 3Rs Principles in Teaching and Research, Turin, Italy.

Diana Massai (D)

Department of Mechanical and Aerospace Engineering and PolitoBIOMed Lab, Politecnico di Torino, Corso Duca Degli Abruzzi, 24, 10129, Turin, Italy. diana.massai@polito.it.
Centro 3R, Interuniversity Center for the Promotion of the 3Rs Principles in Teaching and Research, Turin, Italy. diana.massai@polito.it.

Classifications MeSH