Abstract
Automobile crashes and blunt trauma often lead to life-threatening thoracic injuries, especially to the lung tissues. These injuries can be simulated using finite element-based human body models that need dynamic material properties of lung tissue. The strain-rate-dependent material parameters of human parenchymal tissues were determined in this study using uniaxial quasi-static (1 mm/s) and dynamic (1.6, 3, and 5 m/s) compression tests. A bilinear material model was used to capture the nonlinear behavior of the lung tissue, which was implemented using a user-defined material in LS-DYNA. Inverse mapping using genetic algorithm-based optimization of all experimental data with the corresponding FE models yielded a set of strain-rate-dependent material parameters. The bilinear material parameters are obtained for the strain rates of 0.1, 100, 300, and 500 s−1. The estimated elastic modulus increased from 43 to 153 kPa, while the toe strain reduced from 0.39 to 0.29 when the strain rate was increased from 0.1 to 500 s−1. The optimized bilinear material properties of parenchymal tissue exhibit a piecewise linear relationship with the strain rate.
Similar content being viewed by others
Data availability
The data that support the findings within this study are available from the corresponding author upon a reasonable request.
References
Andrikakou P, Vickraman K, Arora H (2016) On the behaviour of lung tissue under tension and compression. Sci Rep. https://doi.org/10.1038/srep36642
Birzle AM, Hobrack SMK, Martin C et al (2019) Constituent-specific material behavior of soft biological tissue: experimental quantification and numerical identification for lung parenchyma. Biomech Model Mechanobiol 18:1383–1400. https://doi.org/10.1007/s10237-019-01151-3
Brannen M, Kang G, Dutrisac S et al (2022) The influence of the tertiary bronchi on dynamic lung deformation. J Mech Behav Biomed Mater 130:105181. https://doi.org/10.1016/j.jmbbm.2022.105181
Chawla A, Mukherjee S, Karthikeyan B (2009) Characterization of human passive muscles for impact loads using genetic algorithm and inverse finite element methods. Biomech Model Mechanobiol 8:67–76. https://doi.org/10.1007/s10237-008-0121-6
Chen WW (2016) Experimental methods for characterizing dynamic response of soft materials. J Dyn Behav Mater 2:2–14. https://doi.org/10.1007/s40870-016-0047-5
Cheng S, Bilston LE (2007) Unconfined compression of white matter. J Biomech 40:117–124. https://doi.org/10.1016/j.jbiomech.2005.11.004
Concha F, Hurtado DE (2020) Upscaling the poroelastic behavior of the lung parenchyma: A finite-deformation micromechanical model. J Mech Phys Solids. https://doi.org/10.1016/j.jmps.2020.104147
Eskandari M, Arvayo AL, Levenston ME (2018) Mechanical properties of the airway tree: heterogeneous and anisotropic pseudoelastic and viscoelastic tissue responses. J Appl Physiol 125:878–888. https://doi.org/10.1152/japplphysiol.00090
Eskandari F, Shafieian M, Aghdam MM, Laksari K (2021a) Structural anisotropy vs. mechanical anisotropy: the contribution of axonal fibers to the material properties of brain white matter. Ann Biomed Eng 49:991–999. https://doi.org/10.1007/s10439-020-02643-5
Eskandari F, Shafieian M, Aghdam MM, Laksari K (2021b) Tension strain-softening and compression strain-stiffening behavior of brain white matter. Ann Biomed Eng 49:276–286. https://doi.org/10.1007/s10439-020-02541-w
Fung YC, Yen RT, Tao ZL, Liu SQ (1988) A hypothesis on the mechanism of trauma of lung tissue subjected to impact load. J Biomech Eng 110:50–56. https://doi.org/10.1115/1.3108405
Ganpule S, Alai A, Plougonven E, Chandra N (2013) Mechanics of blast loading on the head models in the study of traumatic brain injury using experimental and computational approaches. Biomech Model Mechanobiol 12:511–531. https://doi.org/10.1007/s10237-012-0421-8
Gayzik FS, Hoth JJ, Stitzel JD (2011) Finite element-based injury metrics for pulmonary contusion via concurrent model optimization. Biomech Model Mechanobiol 10:505–520. https://doi.org/10.1007/s10237-010-0251-5
Gupta S, Haiat G, Laporte C, Belanger P (2021) Effect of the acoustic impedance mismatch at the bone-soft tissue interface as a function of frequency in transcranial ultrasound: a simulation and in vitro experimental study. IEEE Trans Ultrason Ferroelectr Freq Control 68:1653–1663. https://doi.org/10.1109/TUFFC.2020.3043893
Hildebrandt J (1970) Pressure-volume data of cat lung interpreted by a plastoelastic, linear viscoelastic model. J Appl Physiol 28:365–372. https://doi.org/10.1152/jappl.1970.28.3.365
Hosseini-Farid M, Ramzanpour M, McLean J et al (2020) A poro-hyper-viscoelastic rate-dependent constitutive modeling for the analysis of brain tissues. J Mech Behav Biomed Mater 102:103475. https://doi.org/10.1016/j.jmbbm.2019.103475
Johnson B, Campbell S, Campbell-Kyureghyan N (2021) Characterizing the material properties of the kidney and liver in unconfined compression and probing protocols with special reference to varying strain rate. Biomechanics 1:264–280. https://doi.org/10.3390/biomechanics1020022
Karunaratne A, Li S, Bull AMJ (2018) Nano-scale mechanisms explain the stiffening and strengthening of ligament tissue with increasing strain rate. Sci Rep 8:1–9. https://doi.org/10.1038/s41598-018-21786-z
Li D, Robertson AM (2009) A structural multi-mechanism constitutive equation for cerebral arterial tissue. Int J Solids Struct 46:2920–2928. https://doi.org/10.1016/j.ijsolstr.2009.03.017
Lichtenberger JP, Kim AM, Fisher D et al (2018) Imaging of combat-related thoracic trauma - blunt trauma and blast lung injury. Mil Med 183:E89–E96. https://doi.org/10.1093/milmed/usx033
Lucas SR, Bass CR, Crandall JR et al (2009) Viscoelastic and failure properties of spine ligament collagen fascicles. Biomech Model Mechanobiol 8:487–498. https://doi.org/10.1007/s10237-009-0152-7
Maghsoudi-Ganjeh M, Mariano CA, Sattari S et al (2021) Developing a lung model in the age of COVID-19: a digital image correlation and inverse finite element analysis framework. Front Bioeng Biotechnol 9:1–14. https://doi.org/10.3389/fbioe.2021.684778
Mariano CA, Sattari S, Quiros KAM et al (2022) Examining lung mechanical strains as influenced by breathing volumes and rates using experimental digital image correlation. Respir Res 23:92. https://doi.org/10.1186/s12931-022-01999-7
Mariano CA, Sattari S, Ramirez GO, Eskandari M (2023) Effects of tissue degradation by collagenase and elastase on the biaxial mechanics of porcine airways. Respir Res. https://doi.org/10.1186/s12931-023-02376-8
Masri C, Chagnon G, Favier D et al (2018) Experimental characterization and constitutive modeling of the biomechanical behavior of male human urethral tissues validated by histological observations. Biomech Model Mechanobiol 17:939–950. https://doi.org/10.1007/s10237-018-1003-1
Mattucci SFE, Moulton JA, Chandrashekar N, Cronin DS (2012) Strain rate dependent properties of younger human cervical spine ligaments. J Mech Behav Biomed Mater 10:216–226. https://doi.org/10.1016/j.jmbbm.2012.02.004
Michalaki C, Dean C, Johansson C (2022) The use of precision-cut lung slices for studying innate immunity to viral infections. Curr Protoc 2:1–14. https://doi.org/10.1002/cpz1.505
Neelakantan S, Xin Y, Gaver DP et al (2022) Computational lung modelling in respiratory medicine. J R Soc Interface. https://doi.org/10.1098/rsif.2022.0062
O’Neill JD, Anfang R, Anandappa A et al (2013) Decellularization of human and porcine lung tissues for pulmonary tissue engineering. Ann Thorac Surg 96:1046–1056. https://doi.org/10.1016/j.athoracsur.2013.04.022
Oikonomou A, Prassopoulos P (2011) CT imaging of blunt chest trauma. Insights Imaging 2:281–295. https://doi.org/10.1007/s13244-011-0072-9
Polio SR, Kundu AN, Dougan CE et al (2018) Cross-platform mechanical characterization of lung tissue. PLoS ONE 13:e0204765. https://doi.org/10.1371/journal.pone.0204765
Prabhu R, Horstemeyer MF, Tucker MT et al (2011) Coupled experiment/finite element analysis on the mechanical response of porcine brain under high strain rates. J Mech Behav Biomed Mater 4:1067–1080. https://doi.org/10.1016/j.jmbbm.2011.03.015
Quiros KAM, Nelson TM, Sattari S et al (2022) Mouse lung mechanical properties under varying inflation volumes and cycling frequencies. Sci Rep 12:1–10. https://doi.org/10.1038/s41598-022-10417-3
Ramzanpour M, Hosseini-Farid M, McLean J et al (2020) Visco-hyperelastic characterization of human brain white matter micro-level constituents in different strain rates. Med Biol Eng Comput 58:2107–2118. https://doi.org/10.1007/s11517-020-02228-3
Rashid B, Destrade M, Gilchrist MD (2014) Mechanical characterization of brain tissue in tension at dynamic strain rates. J Mech Behav Biomed Mater 33:43–54. https://doi.org/10.1016/j.jmbbm.2012.07.015
Rausch SMK, Martin C, Bornemann PB et al (2011) Material model of lung parenchyma based on living precision-cut lung slice testing. J Mech Behav Biomed Mater 4:583–592. https://doi.org/10.1016/j.jmbbm.2011.01.006
Ravindran S, Koohbor B, Malchow P, Kidane A (2018) Experimental characterization of compaction wave propagation in cellular polymers. Int J Solids Struct 139–140:270–282. https://doi.org/10.1016/j.ijsolstr.2018.02.003
Sattari S, Eskandari M (2020) Characterizing the viscoelasticity of extra- and intra-parenchymal lung bronchi. J Mech Behav Biomed Mater 110:103824. https://doi.org/10.1016/j.jmbbm.2020.103824
Shi L, Han Y, Huang H et al (2020) Evaluation of injury thresholds for predicting severe head injuries in vulnerable road users resulting from ground impact via detailed accident reconstructions. Biomech Model Mechanobiol 19:1845–1863. https://doi.org/10.1007/s10237-020-01312-9
Sicard D, Fredenburgh LE, Tschumperlin DJ (2017) Measured pulmonary arterial tissue stiffness is highly sensitive to AFM indenter dimensions. J Mech Behav Biomed Mater 74:118–127. https://doi.org/10.1016/j.jmbbm.2017.05.039
Snedeker JG, Niederer P, Schmidlin FR et al (2005) Strain-rate dependent material properties of the porcine and human kidney capsule. J Biomech 38:1011–1021. https://doi.org/10.1016/j.jbiomech.2004.05.036
Song B, Chen W (2004) Dynamic stress equilibration in split Hopkinson pressure bar tests on soft materials. Exp Mech 44:300–312. https://doi.org/10.1177/0014485104041543
Suki B, Ito S, Stamenović D et al (2005) Biomechanics of the lung parenchyma: critical roles of collagen and mechanical forces. J Appl Physiol 98:1892–1899. https://doi.org/10.1152/japplphysiol.01087.2004
Tai RC, Lee GC (1981) Isotropy and homogeneity of lung tissue deformation. J Biomech 14:243–252. https://doi.org/10.1016/0021-9290(81)90069-5
Upadhyay K, Subhash G, Spearot D (2020) Visco-hyperelastic constitutive modeling of strain rate sensitive soft materials. J Mech Phys Solids 135:103777. https://doi.org/10.1016/j.jmps.2019.103777
van Oosten ASG, Chen X, Chin LK et al (2019) Emergence of tissue-like mechanics from fibrous networks confined by close-packed cells. Nature 573:96–101. https://doi.org/10.1038/s41586-019-1516-5
Verma K (2018) Characterization of human heart and lung under dynamic impact. IIT Delhi, New Delhi
Verma K, Mukherjee S, Gaur P et al (2018) High strain rate compressive behaviour of human heart. Int J Exp Comput Biomech 4:152. https://doi.org/10.1504/ijecb.2018.092276
Weed B, Patnaik S, Rougeau-Browning M et al (2015) Experimental evidence of mechanical isotropy in porcine lung parenchyma. Materials (basel) 8:2454–2466. https://doi.org/10.3390/ma8052454
Weinberg K, Ortiz M (2009) Kidney damage in extracorporeal shock wave lithotripsy: a numerical approach for different shock profiles. Biomech Model Mechanobiol 8:285–299. https://doi.org/10.1007/s10237-008-0135-0
Yousefi AAK, Nazari MA, Perrier P et al (2018) A visco-hyperelastic constitutive model and its application in bovine tongue tissue. J Biomech 71:190–198. https://doi.org/10.1016/j.jbiomech.2018.02.008
Zeng YJ, Yager D, Fung YC (1987) Measurement of the mechanical properties of the human lung tissue. J Biomech Eng 109:169–174. https://doi.org/10.1115/1.3138661
Zhang X, Gan RZ (2011) Experimental measurement and modeling analysis on mechanical properties of incudostapedial joint. Biomech Model Mechanobiol 10:713–726. https://doi.org/10.1007/s10237-010-0268-9
Zwirner J, Scholze M, Ondruschka B, Hammer N (2020) What is considered a variation of biomechanical parameters in tensile tests of collagen-rich human soft tissues?—critical considerations using the human cranial dura mater as a representative morpho-mechanic model. Med 56:1–14. https://doi.org/10.3390/medicina56100520
Funding
The authors acknowledge the financial support received from Joint Advanced Technology Centre, DRDO (DFTM/03/3203/M/01/JATC).
Author information
Authors and Affiliations
Contributions
YSP and AN performed the experimental studies, developed optimization methodology and wrote the manuscript. RM and SL gave the inputs on the human tissues from AIIMS, India. AC, SM, and NVD contributed to conceptualization, supervision, editing the manuscript and arranging the support from the funding agency.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
Required ethical approval has been taken from vide sanction number IEC-302/03.05.2019 from the institutional ethics committee.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pydi, Y.S., Nath, A., Chawla, A. et al. Strain-rate-dependent material properties of human lung parenchymal tissue using inverse finite element approach. Biomech Model Mechanobiol 22, 2083–2096 (2023). https://doi.org/10.1007/s10237-023-01751-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10237-023-01751-0