Modeling autoregulation in three-dimensional simulations of retinal hemodynamics
Full text

How to Cite

1.
Aletti M, Gerbeau J-F, Lombardi D. Modeling autoregulation in three-dimensional simulations of retinal hemodynamics. MAIO [Internet]. 2016 Feb. 24 [cited 2024 Dec. 27];1(1):88-115. Available from: https://www.maio-journal.com/index.php/MAIO/article/view/17

Copyright notice

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication, with the work twelve (12) months after publication simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work’s authorship and initial publication in this journal.

  2. After 12 months from the date of publication, authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

Keywords

retina; autoregulation; 3D hemodynamics

Abstract

Purpose: Autoregulation is a mechanism necessary to maintain an approximately constant blood flow rate in the microcirculation when acute changes in systemic pressure occur. Failure of autoregulation in the retina has been associated with various diseases, including glaucoma. In this work, we propose an initial attempt to model autoregulation in a 3D network of retinal arteries.

Methods: The blood flow is modeled with the time-dependent Stokes equations. The arterial wall model includes the endothelium and the smooth muscle fibers. Various simplifying assumptions lead to a fluid-structure model where the structural part appears as a boundary condition for the fluid. The numerical simulations are performed on a patient-specific network of 25 segments of retinal arteries located in the inferior temporal quadrant.

Results: The simulations performed on the patient-specific artertial network have provided velocities which are in good agreement with published experimental data. In addition, the model allowed to reproduce flow rate-pressure curves which are comparable with experimental data or results obtained with 0D models. In particular, a characteristic plateau of the flow rate has been found for pressures ranging from 40 to 60 mmHg.

Conclusion: This work proposes the first 3D simulation of blood flow in a real network of retinal arteries and it also incorporates an autoregulation mechanism. This can be viewed as a first step towards a more complete 3D model of the hemodynamic of the eye.

https://doi.org/10.35119/maio.v1i1.17
Full text

References

R. Schubert, M. J. Mulvany, The myogenic response: established facts and attractive hypotheses, Clinical Science 96 (1999) 313–326.

E. M. Kohner, V. Patel, S. M. Rassam, Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy, Diabetes 44 (6) (1995) 603–607.

S. Rassam, V. Patel, E. Kohner, The effect of experimental hypertension on retinal vascular autoregulation in humans: a mechanism for the progression of diabetic retinopathy, Experimental physiology 80 (1) (1995) 53–68.

Retinal autoregulation in open-angle glaucoma, Ophthalmology 91 (12) (1984) 1690–1694.

P. Jeppesen, C. Aalkjær, T. Bek, Myogenic response in isolated porcine retinal arterioles, Current eye research 27 (4) (2003) 217–222.

P. Jeppesen, J. Sanaye-Hajari, TO. Be, Increased blood pressure induces a diameter response of retinal arterioles that increases with decreasing arteriolar diameter, Investigative ophthalmology & visual science 48 (1) (2007) 328–331.

M. Blum, K. Bachmann, D. Wintzer, T. Riemer, W. Vilser, J. Strobel, Noninvasive measurement of the bayliss effect in retinal autoregulation, Graefe’s archive for clinical and experimental ophthalmology 237 (4) (1999) 296–300.

A. Harris, O. Arend, K. Bohnke, E. Kroepfl, R. Danis, B. Martin, Retinal blood flow during dynamic exercise, Graefe’s archive for clinical and experimental ophthalmology 234 (7) (1996) 440–444.

M. J. Dumskyj, J. E. Eriksen, C. J. Dor´e, E. M. Kohner, Autoregulation in the human retinal circulation: assessment using isometric exercise, laser doppler velocimetry, and computer-assisted image analysis, Microvascular research 51 (3) (1996) 378–392.

F Robinson; C E Riva; J E Grunwald; B L Petrig; S H Sinclair. Retinal blood flow autoregulation in response to an acute increase in blood pressure. Investigative ophthalmology & visual science 27 (5) (1986) 722–726.

T. Nagaoka, F. Mori, A. Yoshida, Retinal artery response to acute systemic blood pressure increase during cold pressor test in humans, Investigative ophthalmology & visual science 43 (6) (2002) 1941–1945.

J. C. Arciero, B. E. Carlson, T. W. Secomb, Theoretical model of metabolic blood flow regulation: roles of ATP release by red blood cells and conducted responses, American Journal of Physiology - Heart and Circulatory Physiology 295 (4) (2008) H1562–H1571. doi:10.1152/ajpheart.00261.2008.

J. Arciero, A. Harris, B. Siesky, A. Amireskandari, V. Gershuny, A. Pickrell, G. Guidoboni, Theoretical analysis of vascular regulatory mechanisms contributing to retinal blood flow autoregulation, Investigative Ophthalmology & Visual Science 54 (8) (2013) 5584– 5593. arXiv:http://www.iovs.org/content/54/8/5584.full.pdf+html, doi:10.1167/iovs.12-11543.

R. L. Hester, L. W. Hammer, Venular-arteriolar communication in the regulation of blood flow, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 282 (5) (2002) R1280–R1285.

P. Moireau, C. Bertoglio, N. Xiao, C. A. Figueroa, C. Taylor, D. Chapelle, J.-F. Gerbeau, Sequential identification of boundary support parameters in a fluid-structure vascular model using patient image data, Biomechanics and Modeling in Mechanobiology 12 (3) (2012) 475– 496.

C. Bertoglio, D. Barber, N. Gaddum, I. Valverde, M. Rutten, P. Beerbaum, P. Moireau, R. Hose, J.-F. Gerbeau, Identification of artery wall stiffness: in vitro validation and in vivo results of a data assimilation procedure applied to a 3D fluid-structure interaction model, Journal of Biomechanics 47 (5) (2014) 1027–1034.

M. Ferna´ndez, J.-F. Gerbeau, Algorithms for fluid-structure interaction problems, in: L. Formaggia, A. Quarteroni, A. Veneziani (Eds.), Cardiovascular Mathematics. Modeling and simulation of the circulatory system, Springer Verlag, 2009, Ch. 9, pp. 307–346.

Y. Bazilevs, V. Calo, Y. Zhang, T. J. Hughes, Isogeometric fluid– structure interaction analysis with applications to arterial blood flow, Computational Mechanics 38 (4-5) (2006) 310–322.

P. Crosetto, P. Reymond, S. Deparis, D. Kontaxakis, N. Stergiopulos, A. Quarteroni, Fluid–structure interaction simulation of aortic blood flow, Computers & Fluids 43 (1) (2011) 46–57.

P. Moireau, N. Xiao, M. Astorino, C. A. Figueroa, D. Chapelle, C. A. Taylor, J.-F. Gerbeau, External tissue support and fluid-structure simulation in blood flows, Biomechanics and Modeling in Mechanobiology 11 (1) (2012) 1–18. doi:10.1007/s10237-011-0289-z.

M. A. Fern´andez, M. Landajuela, M. Vidrascu, Fully decoupled timemarching schemes for incompressible fluid/thin-walled structure interaction, Journal of Computational Physics 297 (2015) 156–181.

Figueroa CA, Vignon-Clementel IE, Jansen KE, Hughes TJR, Taylor CA. A coupled momentum method for modeling blood flow in three-dimensional deformable arteries. COMPUTER METHODS IN APPLIED MECHANICS AND ENGINEERING. 2006 Aug 15;195(41-43):5685-5706.

F. Nobile, C. Vergara, An effective fluid-structure interaction formulation for vascular dynamics by generalized robin conditions, SIAM Journal on Scientific Computing 30 (2) (2008) 731–763.

O. Pironneau, Simplified Fluid-Structure Interactions for Hemodynamics, in: S. R. Idelsohn (Ed.), Numerical Simulations of Coupled Problems in Engineering, Vol. 33 of Computational Methods in Applied Sciences, Springer International Publishing, 2014, pp. 57–70.

C. M. Colciago, S. Deparis, A. Quarteroni, Comparisons between reduced order models and full 3D models for fluid–structure interaction problems in haemodynamics, Journal of Computational and Applied Mathematics 265 (2014) 120–138.

M. Aletti, J.-F. Gerbeau, D. Lombardi. A simplified fluid-structure model for arterial flow. Application to retinal hemodynamics., submitted (2015).

T. Y. Wong, R. Klein, B. E. Klein, S. M. Meuer, L. D. Hubbard, Retinal vessel diameters and their associations with age and blood pressure, Investigative ophthalmology & visual science 44 (11) (2003) 4644–4650.

C. J. Pournaras, E. Rungger-Bra¨ndle, C. E. Riva, S. H. Hardarson, E. Stefansson, Regulation of retinal blood flow in health and disease, Progress in retinal and eye research 27 (3) (2008) 284–330.

P. G. Ciarlet, Mathematical elasticity. Vol. III, Vol. 29 of Studies in Mathematics and its Applications, North-Holland Publishing Co., Amsterdam, 2000, theory of shells.

S.-I. Murtada, M. Kroon, G. A. Holzapfel, A calcium-driven mechanochemical model for prediction of force generation in smooth muscle, Biomechanics and modeling in mechanobiology 9 (6) (2010) 749– 762.

W. R. Milnor, Cardiovascular physiology, Oxford University Press, 1990.

A. M. Laties, Central retinal artery innervation: absence of adrenergic innervation to the intraocular branches, Archives of Ophthalmology 77 (3) (1967) 405–409.

T. Bek, Regional morphology and pathophysiology of retinal vascular disease, Progress in retinal and eye research 36 (2013) 247–259.

C.-M. Hai, R. A. Murphy, Cross-bridge phosphorylation and regulation of latch state in smooth muscle, Am J Physiol 254 (1 Pt 1) (1988) C99– 106.

J. Yang, J. W. Clark Jr, R. M. Bryan, C. Robertson, The myogenic response in isolated rat cerebrovascular arteries: smooth muscle cell model, Medical engineering & physics 25 (8) (2003) 691–709.

J. Yang, J. W. Clark Jr, R. M. Bryan, C. S. Robertson, The myogenic response in isolated rat cerebrovascular arteries: vessel model, Medical engineering & physics 25 (8) (2003) 711–717.

J. St˚alhand, A. Klarbring, G. A. Holzapfel, Smooth muscle contraction: mechanochemical formulation for homogeneous finite strains, Progress in biophysics and molecular biology 96 (1) (2008) 465–481.

B. Sharifimajd, J. St˚alhand, A continuum model for excitation– contraction of smooth muscle under finite deformations, Journal of theoretical biology 355 (2014) 1–9.

C. E. Riva, J. E. Grunwald, S. H. Sinclair, B. Petrig. Blood velocity and volumetric flow rate in human retinal vessels. Investigative ophthalmology & visual science 26 (8) (1985) 1124–1132.

J. Staal, M. Abramoff, M. Niemeijer, M. Viergever, B. van Ginneken, Ridge based vessel segmentation in color images of the retina, IEEE Transactions on Medical Imaging 23 (4) (2004) 501–509.

B. Al-Diri, A. Hunter, D. Steel, An active contour model for segmenting and measuring retinal vessels, IEEE Transactions on Medical Imaging 28 (9) (2009) 1488–1497.

Geuzaine C, Remacle JF. Gmsh: A 3-D finite element mesh generator with built-in pre-and post-processing facilities. International Journal for Numerical Methods in Engineering 2009;79(11):1309-1331.

C. Geuzaine, J.-F. Remacle, Gmsh: A 3-D finite element mesh generator with built-in pre-and post-processing facilities, International Journal for Numerical Methods in Engineering 79 (11) (2009) 1309–1331.

G. Guidoboni, A. Harris, S. Cassani, J. Arciero, B. Siesky, A. Amireskandari, L. Tobe, P. Egan, I. Januleviciene, J. Park, Intraocular pressure, blood pressure, and retinal blood flow autoregulation: A mathematical model to clarify their relationship and clinical relevance. Investigative ophthalmology & visual science 55 (7) (2014) 4105.

A. Pries, D. Neuhaus, P. Gaehtgens, Blood viscosity in tube flow: dependence on diameter and hematocrit, American Journal of Physiology 263 (1992) H1770–H1770.

A. Pries, K. Ley, M. Claassen, P. Gaehtgens, Red cell distribution at microvascular bifurcations, Microvascular research 38 (1) (1989) 81–101.

isolated rat cerebrovascular arteries: smooth muscle cell model, Medical

engineering & physics 25(8) (2003) 691--709.

J.Yang, J.W. ClarkJr, R.M. Bryan, C.S. Robertson, The myogenic response in

Full text