Abstract
Cranial dura mater is a dense interwoven vascularized connective tissue that helps regulate neurocranial remodeling by responding to strains from the growing brain. Previous ex vivo experimentation has failed to account for the role of prestretch in the mechanical behavior of the dura. Here we aim to estimate the prestretch in mouse cranial dura mater and determine its dependency on direction and age. We performed transverse and longitudinal incisions in parietal dura excised from newborn (day \(\sim\)4) and mature (12 weeks) mice and calculated the ex vivo normalized incision opening (measured width over length). Then, similar incisions were simulated under isotropic stretching within Abaqus/Standard. Finally, prestretch was estimated by comparing the ex vivo and in silico normalized openings. There were no significant differences between the neonatal and adult mice when comparing cuts in the same direction, but adult mice were found to have significantly greater stretch in the anterior–posterior direction than in the medial–lateral direction, while neonatal dura was essentially isotropic. Additionally, our simulations show that increasing curvature impacts the incision opening, indicating that flat in silico models may overestimate prestretch.
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Original data (images, measurements, etc.) and scripts to run all simulations and analysis are available at https://github.com/mholla/BMMB24.
References
Abuzayed B, Kafadar AM, Oğuzoğlu A, Canbaz B, Kaynar MY (2009) Duraplasty using autologous fascia lata reenforced by on-site pedicled muscle flap: technical note. J Craniofac Surg 20(2):435–438. https://doi.org/10.1097/SCS.0b013e31819b968f
Aydin S, Kucukyuruk B, Abuzayed B, Aydin S, Sanus GZ (2011) Cranioplasty: review of materials and techniques. J Neurosci Rural Pract 02(2):162–167. https://doi.org/10.4103/0976-3147.83584
Aydin HE, Kizmazoglu C, Kaya I, Husemoglu B, Sozer G, Havitcioglu H, Arslantas A (2019) Biomechanical properties of the cranial dura mater with puncture defects : an in vitro study. J Korean Neurosurg Soc 62(4):382–388. https://doi.org/10.3340/jkns.2018.0130
Becker SS, Jackler RK, Pitts LH (2003) Cerebrospinal fluid leak after acoustic neuroma surgery: a comparison of the translabyrinthine, middle fossa, and retrosigmoid approaches. Otol Neurotol Off Publ Am Otol Soc Am Neurotol Soc Eur Acad Otol Neurotol 24(1):107–112. https://doi.org/10.1097/00129492-200301000-00021
Borghi A, Rodriguez-Florez N, Rodgers W, James G, Hayward R, Dunaway D, Jeelani O, Schievano S (2018) Spring assisted cranioplasty: a patient specific computational model. Med Eng Phys 53:58–65. https://doi.org/10.1016/j.medengphy.2018.01.001
Bradshaw DRS, Ivarsson J, Morfey CL, Viano DC (2001) Simulation of acute subdural hematoma and diffuse axonal injury in coronal head impact. J Biomech 34(1):85–94. https://doi.org/10.1016/s0021-9290(00)00135-4
Buganza Tepole A, Gart M, Gosain AK, Kuhl E (2014) Characterization of living skin using multi-view stereo and isogeometric analysis. Acta Biomater 10(11):4822–4831. https://doi.org/10.1016/j.actbio.2014.06.037
Buganza Tepole A, Gart M, Purnell CA, Gosain AK, Kuhl E (2015) Multi-view stereo analysis reveals anisotropy of prestrain, deformation, and growth in living skin. Biomech Model Mechanobiol 14(5):1007–1019. https://doi.org/10.1007/s10237-015-0650-8
Bylski DI, Kriewall TJ, Akkas N, Melvin JW (1986) Mechanical behavior of fetal dura mater under large deformation biaxial tension. J Biomech 19(1):19–26. https://doi.org/10.1016/0021-9290(86)90105-3
Chaudhry HR, Bukiet B, Findley T, Ritter AB (1998) Evaluation of residual stress in rabbit skin and the relevant material constants. J Theor Biol 192(2):191–195. https://doi.org/10.1006/jtbi.1997.0616
Clancy B, Kersh B, Hyde J, Darlington RB, Anand KJS, Finlay BL (2007) Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 5(1):79–94. https://doi.org/10.1385/NI:5:1:79
Constantinescu GM (2018) Comparative anatomy of the mouse and the rat: a color atlas and text. CRC Press, Taylor & Francis Group. 262 pp. ISBN: 9781138624030
Curtis N, Jones MEH, Evans SE, O’Higgins P, Fagan MJ (2013) Cranial sutures work collectively to distribute strain throughout the reptile skull. J R Soc Interface 10(86):20130442. https://doi.org/10.1098/rsif.2013.0442
Fabris G, Suar ZM, Kurt M (2019) Micromechanical heterogeneity of the rat pia-arachnoid complex. Acta Biomater 100:29–37. https://doi.org/10.1016/j.actbio.2019.09.044
Fam MD, Potash A, Potash M, Robinson R, Karnell L, O’Brien E, Greenlee JDW (2018) Skull base dural thickness and relationship to demographic features: a postmortem study and literature review. J Neurol Surg Part B Skull Base 79(6):614–620. https://doi.org/10.1055/s-0038-1651501
Fong KD, Warren SM, Loboa EG, Henderson JH, Fang TD, Cowan CM, Carter DR, Longaker MT (2003) Mechanical strain affects dura mater biological processes: implications for immature calvarial healing. Plastic Reconstruct Surg 112(5):1312–1327. https://doi.org/10.1097/01.PRS.0000079860.14734.D6
Frohlich J (2020) Rats and mice. Ferrets Rabbits Rodents. https://doi.org/10.1016/B978-0-323-48435-0.00025-3
Fung YC, Liu SQ (1989) Change of residual strains in arteries due to hypertrophy caused by aortic constriction. Circ Res 65(5):1340–1349
Gagan JR, Tholpady SS, Ogle RC (2007) Cellular dynamics and tissue interactions of the dura mater during head development. Birth Defects Res Part C Embryo Today Rev 81(4):297–304. https://doi.org/10.1002/bdrc.20104
Greenwald JA, BJ Mehrara, JA Spector, SM Warren, FE Crisera, PJ Fagenholz, PJ Bouletreau, MT Longaker (2000) Regional differentiation of cranial suture-associated dura mater in vivo and in vitro: implications for suture fusion and patency. J Bone Miner Res 15 (12):2413-2430. https://doi.org/10.1359/jbmr.2000.15.12.2413.
Gregersen H, Kassab G, Fung Y (2000) REVIEW: the zero-stress state of the gastrointestinal tract. Dig Dis Sci 45(12):2271–2281. https://doi.org/10.1023/A:1005649520386
Han H, Fung Y (1991) Residual strains in porcine and canine trachea. J Biomech 24(5):307–315. https://doi.org/10.1016/0021-9290(91)90349-R
Henderson JH, Nacamuli RP, Zhao B, Longaker MT, Carter DR (2005) Age-dependent residual tensile strains are present in the dura mater of rats. J R Soc Interface 2(3):159–167. https://doi.org/10.1098/rsif.2005.0035
Herring SW, Teng S (2000) Strain in the braincase and its sutures during function. Am J Phys Anthropol 112(4):575. https://doi.org/10.1002/1096-8644(200008)112:4<575::AIDAJPA10>3.0.CO;2-0
Holland MA (2018). Hitchhiker’s guide to abaqus. https://doi.org/10.5281/zenodo.1243270
Jaslow CR (1990) Mechanical properties of cranial sutures. J Biomech 23(4):313–321. https://doi.org/10.1016/0021-9290(90)90059-C
Jimenez Hamann MC, Sacks MS, Malinin TI (1998) Quantification of the collagen fiber architecture of human cranial dura mater. J Anat 192(Pt 1):99–106. https://doi.org/10.1046/j.1469-7580.1998.19210099.x
Kamenskiy AV II, Pipinos YA Dzenis, Lomneth CS, Kazmi SAJ, Phillips NY, MacTaggart JN (2014) Passive biaxial mechanical properties and in vivo axial pre-stretch of the diseased human femoropopliteal and tibial arteries. Acta Biomater 10(3):1301–1313. https://doi.org/10.1016/j.actbio.2013.12.027
Kamenskiy AV II, Pipinos YA Dzenis, Phillips NY, Desyatova AS, Kitson J, Bowen R, MacTaggart JN (2015) Effects of age on the physiological and mechanical characteristics of human femoropopliteal arteries. Acta Biomaterialia 11:304–313. https://doi.org/10.1016/j.actbio.2014.09.050
Kawakami M, Yamamura KI (2008) Cranial bone morphometric study among mouse strains. BMC Evol Biol 8(1):73. https://doi.org/10.1186/1471-2148-8-73
Kinaci A, Bergmann W, Bleys RL, van der Zwan A, van Doormaal TP (2020) Histologic Comparison of the Dura Mater among Species. Comp Med 70 (2):170-175. https://doi.org/10.30802/AALASCM-19-000022
Kriewall TJ, Akkas N, Bylski DI, Melvin JW, Work BA (1983) Mechanical behavior of fetal dura mater under large axisymmetric inflation. J Biomech Eng 105(1):71–76. https://doi.org/10.1115/1.3138388
Kuchiwaki H, Inao S, Ishii N, Ogura Y, Gu SP (1997) Human dural thickness measured by ultrasonographic method: reflection of intracranial pressure. J Ultrasound Med 16(11):725–730. https://doi.org/10.7863/jum.1997.16.11.725
Laurence DW, Ross CJ, Hsu MC, Mir A, Burkhart HM, Holzapfel GA, Lee CH (2022) Benchtop characterization of the tricuspid valve leaflet pre-strains. Acta Biomaterialia. https://doi.org/10.1016/j.actbio.2022.08.046
Liu SSY, Opperman LA, Kyung HM, Buschang PH (2011) Is there an optimal force level for sutural expansion. Am J Orthod Dentofac Orthop Off Publ Am Assoc Orthod Its Const Soc Am Board Orthod 139(4):446–455. https://doi.org/10.1016/j.ajodo.2009.03.056
Maikos JT, Elias RA, Shreiber DI (2008) Mechanical properties of dura mater from the rat brain and spinal cord. J Neurotrauma 25(1):38–51. https://doi.org/10.1089/neu.2007.0348
McGarvey KA, Lee JM, Boughner DR (1984) Mechanical suitability of glycerol-preserved human dura mater for construction of prosthetic cardiac valves. Biomaterials 5(2):109–117. https://doi.org/10.1016/0142-9612(84)90011-5
Melvin JW, JH McElhaney, VL Roberts (1970). Development of a mechanical model of the human head–determination of tissue properties and synthetic substitute materials. SAE Trans 79:Publisher: SAE International, 2685-2694. ISSN: 0096-736X
Ogle RC, Tholpady SS, McGlynn KA, Ogle RA (2004) Regulation of cranial suture morphogenesis. Cells Tissues Organs 176(1):54–66. https://doi.org/10.1159/000075027
Opperman LA, Passarelli RW, Morgan EP, Reintjes M, Ogle RC (1995) Cranial sutures require tissue interactions with dura mater to resist osseous obliteration in vitro. J Bone Miner Res 10(12):1978–1987. https://doi.org/10.1002/jbmr.5650101218
O’Reilly MA, A Muller, K Hynynen (2011). Ultrasound insertion loss of rat parietal bone appears to be proportional to animal mass at sub-megahertz frequencies. Ultrasound Med Biol 37 (11):1930-1937. https://doi.org/10.1016/j.ultrasmedbio.2011.08.001.
Patin DJ, Eckstein EC, Harum K, Pallares VS (1993) Anatomic and biomechanical properties of human lumbar dura mater. Anesth Analgesia 76(3):535–540
Pierrat B, Carroll L, Merle F, MacManus DB, Gaul R, Lally C, Gilchrist MD, Ní Annaidh A (2020) Mechanical characterization and modeling of the porcine cerebral meninges. Front Bioeng Biotechnol 8:801. https://doi.org/10.3389/fbioe.2020.00801
Protasoni M, Sangiorgi S, Cividini A, Culuvaris GT, Tomei G, Dell’Orbo C, Raspanti M, Balbi S, Reguzzoni M (2011) The collagenic architecture of human dura mater: laboratory investigation. J Neurosurg 114(6):1723–1730. https://doi.org/10.3171/2010.12.JNS101732
Rasband WS (2018) ImageJ. Bethesda, Maryland, USA
Rausch MK, Kuhl E (2013) On the effect of prestrain and residual stress in thin biological membranes. J Mech Phys Solids 61(9):1955–1969. https://doi.org/10.1016/j.jmps.2013.04.005
Richtsmeier JT, Flaherty K (2013) Hand in glove: brain and skull in development and dysmorphogenesis. Acta Neuropathol 125:469–489. https://doi.org/10.1007/s00401-013-1104-y
Rodriguez EK, Hoger A, McCulloch AD (1994) Stress-dependent finite growth in soft elastic tissues. J Biomech 27(4):455–467. https://doi.org/10.1016/0021-9290(94)90021-3
Shulyakov AV, Cenkowski SS, Buist RJ, Del Bigio MR (2011) Age-dependence of intracranial viscoelastic properties in living rats. J Mech Behav Biomed Mater 4(3):484–497. https://doi.org/10.1016/j.jmbbm.2010.12.012
Suh DC (2020) Where Did the dura mater come from. Neurointervention 15(1):2–3. https://doi.org/10.5469/neuroint.2020.00045
van Noort R, Black MM, Martin TRP, Meanley S (1981) A study of the uniaxial mechanical properties of human dura mater preserved in glycerol. Biomaterials 2(1):41–45. https://doi.org/10.1016/0142-9612(81)90086-7
Vandenabeele F, Creemers J, Lambrichts I (1996) Ultrastructure of the human spinal arachnoid mater and dura mater. J Anat 189(Pt 2):417–430
Weickenmeier J, Fischer C, Carter D, Kuhl E, Goriely A (2017) Dimensional, geometrical, and physical constraints in skull growth. Phys Rev Lett 118(24):248101
Weiss-Bilka HE, Brill JA, Ravosa MJ (2018) Non-sutural basicranium-derived cells undergo a unique mineralization pathway via a cartilage intermediate in vitro. PeerJ 6:e5757. https://doi.org/10.7717/peerj.5757
Wolfinbarger L Jr, Zhang Y, Adam BLT, Homsi D, Gates K, Sutherland V (1994) Biomechanical aspects on rehydrated freeze-dried human allograft dura mater tissues. J Appl Biomater 5(3):265–270. https://doi.org/10.1002/jab.770050313
Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009) Bayesian analysis of neuroimaging data in FSL. NeuroImage 45(1):S173–S186. https://doi.org/10.1016/j.neuroimage.2008.10.055
Workman AD, Charvet CJ, Clancy B, Darlington RB, Finlay BL (2013) Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species. J Neurosci 33(17):7368–7383. https://doi.org/10.1523/JNEUROSCI.5746-12.2013
Xu G, Bayly PV, Taber LA (2009) Residual stress in the adult mouse brain. Biomech Model Mechanobiol 8(4):253–262. https://doi.org/10.1007/s10237-008-0131-4
Yamaki T, Uede T, Tano-oka A, Asakura K, Tanabe S, Hashi K (1991) Vascularized omentum graft for the reconstruction of the skull base after removal of a nasoethmoidal tumor with intracranial extension: case report. Neurosurgery 28(6):877–880. https://doi.org/10.1097/00006123-199106000-00015
Yu JC, Buchman SR, Gosain AK, Havlik RJ, Wang TH, Lam PS, Masoumy M (2021) Basic biomechanics for craniofacial surgeons: the responses of alloplastic materials and living tissues to mechanical forces. FACE 2(4):446–461
Zwirner J, Scholze M, Waddell JN, Ondruschka B, Hammer N (2019) Mechanical properties of human dura mater in tension–an analysis at an age range of 2 to 94 years. Sci Reports 9(1):16655. https://doi.org/10.1038/s41598-019-52836-9
Acknowledgements
This project was supported by NSF Grant Nos. IIS-1850102 (to M. A. Holland) and BCS-1848884 (to M. J. Ravosa), the Indiana Clinical and Translational Sciences Institute (to M. A. Holland, M. J. Ravosa, and C. J. Goergen; funded, in part, by grant no. UL1TR002529 from the NIH National Center for Advancing Translational Sciences, Clinical and Translational Sciences Award), the NIH National Heart, Lung, and Blood Institute (F30-HL145980 to F. W. Damen), and the Leslie A. Geddes Endowment at Purdue University (to C. J. Goergen). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or NSF.
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Consolini, J., Oberman, A.G., Sayut, J. et al. Investigation of direction- and age-dependent prestretch in mouse cranial dura mater. Biomech Model Mechanobiol (2024). https://doi.org/10.1007/s10237-023-01802-6
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DOI: https://doi.org/10.1007/s10237-023-01802-6