Propagation of damage in brain tissue: coupling the mechanics of oedema and oxygen delivery

Biomechanics and Modeling in Mechanobiology

Volumn 14, Issue 6, 2015, Pages 1197-1216

  Lang, Georgina E ^a   Vella, Dominic ^a   Waters, Sarah L ^a   Goriely, Alain ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Brain mechanics; Mathematical modelling; Oxygen delivery; Tissue swelling; Triphasic model

Indexed keywords

BRAIN; MECHANICS; OXYGEN SUPPLY; SWELLING;

BRAIN MECHANIC; BRAIN STROKES; BRAIN TISSUE; MATHEMATICAL MODELING; MECHANICAL COMPRESSION; OXYGEN DELIVERY; TISSUE SWELLING; TRAUMATIC BRAIN INJURIES; TRIPHASIC MODELS; VASCULATURE;

TISSUE;

OXYGEN;

ARTICLE; BRAIN BLOOD FLOW; BRAIN CELL; BRAIN EDEMA; BRAIN TISSUE; GEOMETRY; HUMAN; MATHEMATICAL MODEL; MECHANICS; OXYGEN CONCENTRATION; OXYGEN CONSUMPTION; OXYGEN SUPPLY; OXYGEN TRANSPORT; PRIORITY JOURNAL; STRESS; ANIMAL; BIOLOGICAL MODEL; BRAIN; BRAIN INJURY; COMPLICATION; COMPUTER SIMULATION; DECOMPRESSION SURGERY; INTRACRANIAL PRESSURE; METABOLISM; PATHOPHYSIOLOGY; RAT; TREATMENT OUTCOME;

ANIMALS; BRAIN; BRAIN EDEMA; BRAIN INJURIES; COMPUTER SIMULATION; DECOMPRESSION, SURGICAL; HUMANS; INTRACRANIAL PRESSURE; MODELS, NEUROLOGICAL; OXYGEN; RATS; TREATMENT OUTCOME;

EID: 84942984893     PISSN: 16177959     EISSN: 16177940     Source Type: Journal    
DOI: 10.1007/s10237-015-0665-1     Document Type: Article

References (41)

1. Atala A, Lanza RP (2002) Methods of tissue engineering. Gulf Professional Publishing, Houston
2. Bain AC, Meaney DF (2000) Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. J Biomech Eng 122(6):615–622
3. Ben Amar M, Goriely A (2005) Growth and instability in elastic tissues. J Mech Phys Solids 53(10):2284–2319
4. Cheng S, Bilston EL (2007) Unconfined compression of white matter. J Biomech 40(1):117–124. doi:10.1016/j.jbiomech.2005.11.004 ISSN 0021–9290
5. Cooper DJ, Rosenfeld JV, Murray L, Arabi YM, Davies AR, D’Urso P, Kossmann T, Ponsford J, Seppelt I, Reilly P et al (2011) Decompressive craniectomy in diffuse traumatic brain injury. New Engl J Med 364(16):1493–1502
6. Cowin SC, Doty SB (2009) Tissue mechanics. Springer, Berlin
7. Dhawan V, DeGeorgia M (2012) Neurointensive care biophysiological monitoring. J Neurointerv Surg 4(6):407–413
8. Donnan FG (1924) The theory of membrane equilibria. Chem Rev 1(1):73–90
9. Elkin BS, Shaik MA, Morrison III B (2010) Fixed negative charge and the Donnan effect: a description of the driving forces associated with brain tissue swelling and edema. Philos Trans Royal Soc Lond A 368(1912):585–603. doi:10.1098/rsta.2009.0223
10. Erecińska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128(3):263–276
11. Flechsenhar J, Woitzik J, Zweckberger K, Amiri H, Hacke W, Jüttler E (2013) Hemicraniectomy in the management of space-occupying ischemic stroke. J Clin Neurosci 20(1):6–12
12. Fisher M, Garcia JH (1996) Evolving stroke and the ischemic penumbra. Neurology 47(4):884–888
13. Ganfield R, Nair P, Whalen W (1970) Mass transfer, storage, and utilization of o2 in cat cerebral cortex. Am J Physiol 219:814821
14. García JJ, Smith JH (2009) A biphasic hyperelastic model for the analysis of fluid and mass transport in brain tissue. Ann Biomed Eng 37:375–386. doi:10.1007/s10439-008-9610-0 ISSN 0090–6964
15. Go KG (1997) The normal and pathological physiology of brain water. Adv Tech Stand Neurosurg 23:47–142
16. Goriely A, van Dommelen JAW, Geers MGD, Holzapfel G, Jayamohan J, Jérusalem A, Sivaloganathan S, Squier W, Waters S, Kuhl E. Mechanics of the brain: perspectives, challenges, and opportunities. http://link.springer.com/article/10.1007/s10237-015-0662-4
17. Gerriets T, Stolz E, Walberer M, Müller C, Kluge A, Bachmann A, Fisher M, Kaps M, Bachmann G (2004) Noninvasive quantification of brain edema and the space-occupying effect in rat stroke models using magnetic resonance imaging. Stroke 35:566–571. doi:10.1161/01.STR.0000113692.38574.57
18. Hatashita S, Hoff JT, Salamat SM (1988) Ischemic brain edema and the osmotic gradient between blood and brain. J Cereb Blood Flow Metab 8(4):525–559. doi:10.1038/jcbfm.1988.96
19. Huyghe JMRJ, Janssen JD (1997) Quadriphasic mechanics of swelling incompressible porous media. Int J Eng Sci 35(8):793–802
20. Homer LD, Shelton JB, Williams TJ (1983) Diffusion of oxygen in slices of rat brain. Am J Physiol Regul Integr Comp Physiol 244:R15–R22
21. Keener JP, Sneyd J (1998) Mathematical physiology, vol 8. Springer, Berlin
22. Lai WM, Hou JS, Mow VC (1991) A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113(3):245–258
23. Lang GE, Stewart PS, Vella D, Waters SL, Goriely A (2014) Is the Donnan effect sufficient to explain swelling in brain tissue slices? J R Soc Interface 11(96): doi:10.1098/rsif.2014.0123
24. Lang GE: Mechanics of swelling and damage in brain tissue: a theoretical approach. PhD Thesis, University of Oxford, (2014)
25. MacLaurin J, Chapman SJ, Jones GW, Roose T (2012) The buckling of capillaries in solid tumours. Proc R Soc A 468(2148):4123–4145
26. Marmarou A, Fatouros PP, Barza P, Portella G, Yoshihara M, Tsuji O, Yamamoto T, Laine F, Signoretti S, Ward JD, Bullock MR, Young HF (2000) Contribution of edema and cerebral blood volume to traumatic brain swelling in head-injured patients. J Neurosurg 93(2):183–193. doi:10.3171/jns.2000.93.2.0183
27. Narotam PK, Morrison JF, Nathoo N (2009) Brain tissue oxygen monitoring in traumatic brain injury and major trauma: outcome analysis of a brain tissue oxygen-directed therapy: Clinical article. J Neurosurg 111(4):672–682
28. Ogden RW (1972) Large deformation isotropic elasticity-on the correlation of theory and experiment for incompressible rubberlike solids. Proc R Soc Lond A Math Phys Sci 326(1567):565–584
29. Ogden RW (1984) Non linear elastic deformations. Ellis-Horwood, Chichester
30. Østergaard L, Nørhøj Jespersen S, Mouridsen K, Klærke Mikkelsen I, Ýr Jonsdottír K, Tietze A, Blicher JU, Aamand R, Hjort N, Kerting Iversen N et al (2013) The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. J Cereb Blood Flow Metab 33(5):635–648
31. Pardridge WM (1997) Drug delivery to the brain. J Cereb Blood Flow Metab 17(7):713–731
32. Papadopoulos MC, Krishna S, Verkman A (2002) Aquaporin water channels and brain edema. Mt Sinai J Med 69:242?248
33. Raslan A, Bhardwaj A (2007) Medical management of cerebral edema. Neurosurg Focus 22(5):1–12. doi:10.3171/foc.2007.22.5.13
34. Secomb TW, Hsu R, Beamer NB, Coull BM (2000) Theoretical simulation of oxygen transport to brain by networks of microvessels: effects of oxygen supply and demand on tissue hypoxia. Microcirculation 7(4):237–247. doi:10.1111/j.1549-8719.2000.tb00124.x ISSN 1549–8719
35. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V (2007) Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 6:258–268. doi:10.1016/S1474-4422(07)70055-8
36. Steiner LA, Andrews PJD (2006) Monitoring the injured brain: ICP and CBF. Br J Anaesth 97(1):26–38. doi:10.1093/bja/ael110
37. Strandgaard S, Olesen J, Skinhøj E, Lassen NA (1973) Autoregulation of brain circulation in severe arterial hypertension. Br Med J 1(5852):507–510
38. Sun DN, Gu WY, Guo XE, Lai WM, Mow VC (1999) A mixed finite element formulation of triphasic mechano-electrochemical theory for charged, hydrated biological soft tissues. Int J Numer Methods Eng 45:13751402
39. Tang-Schomer MD, Patel AR, Baas PW, Smith DH (2010) Mechanical breaking of microtubules in axons during dynamic stretch injury underlies delayed elasticity, microtubule disassembly, and axon degeneration. FASEB J 24(5):1401–1410. doi:10.1096/fj.09-142844
40. Thiex R, Tsirka SE (2007) Brain edema after intracerebral hemorrhage: mechanisms, treatment options, management strategies, and operative indications. Neurosurg Focus 22(5):1–7. doi:10.3171/foc.2007.22.5.7
41. Walberer M, Ritschel N, Nedelmann M, Volk K, Müller C, Tschernatsch M, Stolz E, Blaes F, Bachmann G, Gerriets T (2008) Aggravation of infarct formation by brain swelling in a large territorial stroke: a target for neuroprotection? J Neurosurg 109(2):287–293. doi:10.3171/JNS/2008/109/8/028