Abstract
Image-based computational fluid dynamics (CFD) studies conducted at rest have shown that atherosclerotic plaque in the thoracic aorta (TA) correlates with adverse wall shear stress (WSS), but there is a paucity of such data under elevated flow conditions. We developed a pedaling exercise protocol to obtain phase contrast magnetic resonance imaging (PC-MRI) blood flow measurements in the TA and brachiocephalic arteries during three-tiered supine pedaling at 130, 150, and 170 % of resting heart rate (HR), and relate these measurements to non-invasive tissue oxygen saturation \((\hbox {StO}_{2})\) acquired by near-infrared spectroscopy (NIRS) while conducting the same protocol. Local quantification of WSS indices by CFD revealed low time-averaged WSS on the outer curvature of the ascending aorta and the inner curvature of the descending aorta (dAo) that progressively increased with exercise, but that remained low on the anterior surface of brachiocephalic arteries. High oscillatory WSS observed on the inner curvature of the aorta persisted during exercise as well. Results suggest locally continuous exposure to potentially deleterious indices of WSS despite benefits of exercise. Linear relationships between flow distributions and tissue oxygen extraction calculated from \(\hbox {StO}_{2}\) were found between the left common carotid versus cerebral tissue \((r^{2}=0.96)\) and the dAo versus leg tissue \((r^{2}=0.87)\). A resulting six-step procedure is presented to use NIRS data as a surrogate for exercise PC-MRI when setting boundary conditions for future CFD studies of the TA under simulated exercise conditions. Relationships and ensemble-averaged PC-MRI inflow waveforms are provided in an online repository for this purpose.
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Abbreviations
- AAo:
-
Ascending aorta
- BF:
-
Blood flow
- BP:
-
Blood pressure
- BSA:
-
Body surface area
- \(\hbox {CexO}_{2}\) :
-
Oxygen extraction
- \(\hbox {CaO}_{2}\), \(\hbox {CtO}_{2}\), \(\hbox {CvO}_{2}\) :
-
Arterial, tissue and venous oxygen concentration/content, respectively
- CFD:
-
Computational fluid dynamics
- CHD:
-
Congenital heart disease
- CI:
-
Cardiac index
- CPET:
-
Cardiopulmonary exercise testing
- CO:
-
Cardiac output
- dAo:
-
Descending aorta
- FD:
-
Flow distribution
- HR:
-
Heart rate
- IA:
-
Innominate artery
- LCCA:
-
Left common carotid artery
- LSA:
-
Left subclavian artery
- MRI:
-
Magnetic resonance imaging
- NMF:
-
Normalized mean flow
- NIRS:
-
Near-infrared spectroscopy
- PC:
-
Phase contrast
- \(\hbox {SaO}_{2}, \hbox {StO}_{2}\), \(\hbox {SvO}_{2}\) :
-
Arterial, tissue and venous oxygen saturation, respectively
- TA:
-
Thoracic aorta
- TAWSS:
-
Time-averaged wall shear stress
- WSS:
-
Wall shear stress
References
Antiga L, Piccinelli M, Botti L, Ene-Iordache B, Remuzzi A, Steinman DA (2008) An image-based modeling framework for patient-specific computational hemodynamics. Med Biol Eng Comput 46:1097–1112. doi:10.1007/s11517-008-0420-1
Baris RR, Israel AL, Amory DW, Benni P (1995) Regional cerebral oxygenation during cardiopulmonary bypass. Perfusion 10:245–248
Berens RJ et al (2006) Near infrared spectroscopy monitoring during pediatric aortic coarctation repair. Paediatr Anaesth 16:777–781. doi:10.1111/j.1460-9592.2006.01956.x
Blanco PJ, Trenhago PR, Fernandes LG, Feijoo RA (2012) On the integration of the baroreflex control mechanism in a heterogeneous model of the cardiovascular system. Int J Numer Methods Biomed Eng 28:412–433. doi:10.1002/cnm.1474
Boron WF, Boulpaep EL (eds) (2005) Medical physiology, 2nd edn. Elsevier Inc, Philadelphia
Braden DS, Carroll JF (1999) Normative cardiovascular responses to exercise in children. Pediatr Cardiol 20:4–10 discussion 11
Calbet JA, Gonzalez-Alonso J, Helge JW, Sondergaard H, Munch-Andersen T, Boushel R, Saltin B (2007) Cardiac output and leg and arm blood flow during incremental exercise to exhaustion on the cycle ergometer. J Appl Physiol 103:969–978
Celermajer DS, Greaves K (2002) Survivors of coarctation repair: fixed but not cured. Heart 88:113–114
Chakravarti S, Srivastava S, Mittnacht AJ (2008) Near infrared spectroscopy (NIRS) in children. Semin Cardiothorac Vasc Anesth 12:70–79. doi:10.1177/1089253208316444
Chatzis AC et al (2008) Mid-term results following surgical treatment of congenital cardiac malformations in adults. Cardiol Young 18:461–466. doi:10.1017/S1047951108002576
Cheng CP, Herfkens RJ, Lightner AL, Taylor CA, Feinstein JA (2004) Blood flow conditions in the proximal pulmonary arteries and vena cavae: healthy children during upright cycling exercise. Am J Physiol Heart Circ Physiol 287:H921–926. doi:10.1152/ajpheart.00022.2004
Cheng CP, Schwandt DF, Topp EL, Anderson JH, Herfkens RJ, Taylor CA (2003) Dynamic exercise imaging with an MR-compatible stationary cycle within the general electric open magnet. Magn Reson Med 49:581–585. doi:10.1002/mrm.10364
Covidien INVOS 5100C Cerebral/Somatic Oximeter (2009). http://www.covidien.com/rms/products/cerebral-somatic-oximetry/invos-5100c-cerebral-somatic-oximeter
Dagianti A, Penco M, Bandiera A, Sgorbini L, Fedele F (1998) Clinical application of exercise stress echocardiography: Supine bicycle or treadmill? Am J Cardiol 81:62G–67G
Denis R, Perrey S (2006) Influence of posture on pulmonary O\(_2\) uptake kinetics, muscle deoxygenation and myolectrical activity during heavy-intensity exercise. J Sports Sci Med 5:254–265
Dillon-Murphy D, Noorani A, Nordsletten D, Figueroa CA (2015) Multi-modality image-based computational analysis of haemodynamics in aortic dissection. Biomech Model Mechanobiol. doi:10.1007/s10237-015-0729-2
Faggiano E, Antiga L, Puppini G, Quarteroni A, Luciani GB, Vergara C (2013) Helical flows and asymmetry of blood jet in dilated ascending aorta with normally functioning bicuspid valve. Biomech Model Mechanobiol 12:801–813. doi:10.1007/s10237-012-0444-1
Frydrychowicz A et al (2008) Multidirectional flow analysis by cardiovascular magnetic resonance in aneurysm development following repair of aortic coarctation. J Cardiovasc Magn Reson 10:30. doi:10.1186/1532-429X-10-30
Frydrychowicz A et al (2009) Three-dimensional analysis of segmental wall shear stress in the aorta by flow-sensitive four-dimensional-MRI. J Magn Reson Imaging 30:77–84. doi:10.1002/jmri.21790
Ganong WF (2005) Review of medical physiology, 22nd edn. McGraw-Hill, New York
Gonzalez-Alonso J, Mortensen SP, Dawson EA, Secher NH, Damsgaard R (2006) Erythrocytes and the regulation of human skeletal muscle blood flow and oxygen delivery: role of erythrocyte count and oxygenation state of haemoglobin. J Physiol 572:295–305. doi:10.1113/jphysiol.2005.101121
Gonzalez-Alonso J, Richardson RS, Saltin B (2001) Exercising skeletal muscle blood flow in humans responds to reduction in arterial oxyhaemoglobin, but not to altered free oxygen. J Physiol 530:331–341
Grassi B, Pogliaghi S, Rampichini S, Quaresima V, Ferrari M, Marconi C, Cerretelli P (2003) Muscle oxygenation and pulmonary gas exchange kinetics during cycling exercise on-transitions in humans. J Appl Physiol 95:149–158. doi:10.1152/japplphysiol.00695.2002
Green D, Cheetham C, Reed C, Dembo L, O’Driscoll G (2002) Assessment of brachial artery blood flow across the cardiac cycle: retrograde flows during cycle ergometry. J Appl Physiol 93:361–368
Hansen J, Sander M, Hald CF, Victor RG, Thomas GD (2000) Metabolic modulation of sympathetic vasoconstriction in human skeletal muscle: role of tissue hypoxia. J Physiol Lond 527:387–396. doi:10.1111/j.1469-7793.2000.00387.x
Heiberg E, Sjögren J, Ugander M, Carlsson M, Engblom H, Arheden H (2010) Design and validation of segment-freely available software for cardiovascular image analysis. BMC Med Imaging 10:1. doi:10.1186/1471-2342-10-1
Hoffman GM et al (2004) Changes in cerebral and somatic oxygenation during stage 1 palliation of hypoplastic left heart syndrome using continuous regional cerebral perfusion. J Thorac Cardiovasc Surg 127:223–233. doi:10.1016/j.jtcvs.2003.08.021
Hsia TY, Khambadkone S, Redington AN, Migliavacca F, Deanfield JE, de Leval MR (2000) Effects of respiration and gravity on infradiaphragmatic venous flow in normal and Fontan patients. Circulation 102:148–153
Ide K, Horn A, Secher NH (1999) Cerebral metabolic response to submaximal exercise. J Appl Physiol 87:1604–1608
Kautz SA, Brown DA (1998) Relationships between timing of muscle excitation and impaired motor performance during cyclical lower extremity movement in post-stroke hemiplegia. Brain 121(Pt 3):515–526
Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB (1993) Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 88:2235–2247
Kim HJ, Figueroa CA, Hughes TJR, Jansen KE, Taylor CA (2009) Augmented Lagrangian method for constraining the shape of velocity profiles at outlet boundaries for three-dimensional finite element simulations of blood flow. Comput Method Appl Mech Eng 198:3551–3566. doi:10.1016/j.cma.2009.02.012
Kim HJ, Jansen KE, Taylor CA (2010) Incorporating autoregulatory mechanisms of the cardiovascular system in three-dimensional finite element models of arterial blood flow. Ann Biomed Eng 38:2314–2330. doi:10.1007/s10439-010-9992-7
Kim HJ, Vignon-Clementel IE, Figueroa CA, LaDisa JF, Jansen KE, Feinstein JA, Taylor CA (2009b) On coupling a lumped parameter heart model and a three-dimensional finite element aorta model. Ann Biomed Eng 37:2153–2169. doi:10.1007/s10439-009-9760-8
Kurth CD, Uher B (1997) Cerebral hemoglobin and optical pathlength influence near-infrared spectroscopy measurement of cerebral oxygen saturation. Anesth Analg 84:1297–1305
Kwon S, Feinstein JA, Dholakia RJ, LaDisa JF Jr (2014) Quantification of local hemodynamic alterations caused by virtual implantation of three commercially available stents for the treatment of aortic coarctation. Pediatr Cardiol 35:732–740. doi:10.1007/s00246-013-0845-7
LaDisa JF et al (2011a) Computational simulations for aortic coarctation: representative results from a sampling of patients. J Biomech Eng 133:091008. doi:10.1115/1.4004996
LaDisa JF et al (2011) Computational simulations demonstrate altered wall shear stress in aortic coarctation patients treated by resection with end-to-end anastomosis. Congenit Heart Dis 6:432–443. doi:10.1111/j.1747-0803.2011.00553.x
Ladisa JF Jr, Taylor CA, Feinstein JA (2010) Aortic oarctation: recent developments in experimental and computational methods to assess treatments for this simple condition. Prog Pediatr Cardiol 30:45–49. doi:10.1016/j.ppedcard.2010.09.006
Lau KD, Figueroa CA (2015) Simulation of short-term pressure regulation during the tilt test in a coupled 3D–0D closed-loop model of the circulation. Biomech Model Mechanobiol 14:915–929. doi:10.1007/s10237-014-0645-x
Les AS et al (2010) Quantification of hemodynamics in abdominal aortic aneurysms during rest and exercise using magnetic resonance imaging and computational fluid dynamics. Ann Biomed Eng 38:1288–1313. doi:10.1007/s10439-010-9949-x
Liu X, Sun A, Fan Y, Deng X (2015) Physiological significance of helical flow in the arterial system and its potential clinical applications. Ann Biomed Eng 43:3–15. doi:10.1007/s10439-014-1097-2
Loomba RS, Danduran ME, Dixon JE, Rao RP (2014) Effect of Fontan fenestration on regional venous oxygen saturation during exercise: further insights into Fontan fenestration closure. Pediatr Cardiol 35:514–520. doi:10.1007/s00246-013-0817-y
Macdonald J, Forouzan O, Warczytowa J, Wieben O, Francois CJ, Chesler NC (2015) MRI assessment of aortic flow and pulse wave velocity in response to exercise. J Cardiovasc Magn Reson 17:M2–M2. doi:10.1186/1532-429X-17-S1-M2
MacPhee SL, Shoemaker JK, Paterson DH, Kowalchuk JM (2005) Kinetics of O\(_2\) uptake, leg blood flow, and muscle deoxygenation are slowed in the upper compared with lower region of the moderate-intensity exercise domain. J Appl Physiol 99:1822–1834. doi:10.1152/japplphysiol.01183.2004
Malek AM, Alper SL, Izumo S (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282:2035–2042
Markl M et al (2003) Generalized reconstruction of phase contrast MRI: analysis and correction of the effect of gradient field distortions. Magn Reson Med 50:791–801. doi:10.1002/mrm.10582
Mehta JP, Verber MD, Wieser JA, Schmit BD, Schindler-Ivens SM (2009) A novel technique for examining human brain activity associated with pedaling using fMRI. J Neurosci Methods 179:230–239. doi:10.1016/j.jneumeth.2009.01.029
Moireau P, Xiao N, Astorino M, Figueroa CA, Chapelle D, Taylor CA, Gerbeau JF (2012) External tissue support and fluid-structure simulation in blood flows. Biomech Model Mechanobiol 11:1–18. doi:10.1007/s10237-011-0289-z
Mosteller RD (1987) Simplified calculation of body-surface area. N Engl J Med 317:1098. doi:10.1056/NEJM198710223171717
Muller J, Sahni O, Li X, Jansen KE, Shephard MS, Taylor CA (2005) Anisotropic adaptive finite element method for modelling blood flow. Comput Methods Biomech Biomed Engin 8:295–305
Niezen RA, Doornbos J, van der Wall EE, de Roos A (1998) Measurement of aortic and pulmonary flow with MRI at rest and during physical exercise. J Comput Assist Tomogr 22:194–201
Pedersen EM, Kozerke S, Ringgaard S, Scheidegger MB, Boesiger P (1999) Quantitative abdominal aortic flow measurements at controlled levels of ergometer exercise. Magn Reson Imaging 17:489–494 doi:S0730725X98002094 [pii]
Peeters JM, Bos C, Bakker CJ (2005) Analysis and correction of gradient nonlinearity and B0 inhomogeneity related scaling errors in two-dimensional phase contrast flow measurements. Magn Reson Med 53:126–133. doi:10.1002/mrm.20309
Poliner LR, Dehmer GJ, Lewis SE, Parkey RW, Blomqvist CG, Willerson JT (1980) Left ventricular performance in normal subjects: a comparison of the responses to exercise in the upright and supine positions. Circulation 62:528–534
Rao RP et al (2009) Measurement of regional tissue bed venous weighted oximetric trends during exercise by near infrared spectroscopy. Pediatr Cardiol 30:465–471. doi:10.1007/s00246-009-9393-6
Rao RP, Danduran MJ, Loomba RS, Dixon JE, Hoffman GM (2012) Near-infrared spectroscopic monitoring during cardiopulmonary exercise testing detects anaerobic threshold. Pediatr Cardiol 33:791–796. doi:10.1007/s00246-012-0217-8
Sahni O, Muller J, Jansen KE, Shephard MS, Taylor CA (2006) Efficient anisotropic adaptive discretization of the cardiovascular system. Comput Methods Biomech Biomed Eng 195:5634–5655
Sampath S, Derbyshire JA, Ledesma-Carbayo MJ, McVeigh ER (2011) Imaging left ventricular tissue mechanics and hemodynamics during supine bicycle exercise using a combined tagging and phase-contrast MRI pulse sequence. Magn Reson Med 65:51–59. doi:10.1002/mrm.22668
Samyn MM et al (2015) Cardiovascular magnetic resonance imaging-based computational fluid dynamics/fluid-structure interaction pilot study to detect early vascular changes in pediatric patients with type 1 diabetes. Pediatr Cardiol 36:851–861. doi:10.1007/s00246-014-1071-7
Sidhu P, Peng HT, Cheung B, Edginton A (2011) Simulation of differential drug pharmacokinetics under heat and exercise stress using a physiologically based pharmacokinetic modeling approach. Can J Physiol Pharmacol 89:365–382. doi:10.1139/y11-030
Steeden JA, Atkinson D, Taylor AM, Muthurangu V (2010) Assessing vascular response to exercise using a combination of real-time spiral phase contrast MR and noninvasive blood pressure measurements. J Magn Reson Imaging 31:997–1003. doi:10.1002/jmri.22105
Stergiopulos N, Meister JJ, Westerhof N (1994) Simple and accurate way for estimating total and segmental arterial compliance: the pulse pressure method. Ann Biomed Eng 22:392–397
Stergiopulos N, Segers P, Westerhof N (1999) Use of pulse pressure method for estimating total arterial compliance in vivo. Am J Physiol Heart Circ Physiol 276:H424–428
Tanaka H, Shimizu S, Ohmori F, Muraoka Y, Kumagai M, Yoshizawa M, Kagaya A (2006) Increases in blood flow and shear stress to nonworking limbs during incremental exercise. Med Sci Sports Exerc 38:81–85
Tang BT, Cheng CP, Draney MT, Wilson NM, Tsao PS, Herfkens RJ, Taylor CA (2006) Abdominal aortic hemodynamics in young healthy adults at rest and during lower limb exercise: quantification using image-based computer modeling. Am J Physiol Heart Circ Physiol 291:H668–676
Taylor CA, Cheng CP, Espinosa LA, Tang BT, Parker D, Herfkens RJ (2002) In vivo quantification of blood flow and wall shear stress in the human abdominal aorta during lower limb exercise. Ann Biomed Eng 30:402–408
Thomas SN, Schroeder T, Secher NH, Mitchell JH (1989) Cerebral blood flow during submaximal and maximal dynamic exercise in humans. J Appl Physiol 67:744–748
Trojnarska O et al (2007) Cardiopulmonary exercise test in the evaluation of exercise capacity, arterial hypertension, and degree of descending aorta stenosis in adults after repair of coarctation of the aorta. Cardiol J 14:76–82
Varjavand N (2000) The Interactive Oxyhemoglobin Dissociation Curve (2011). http://www.ventworld.com/resources/oxydisso/dissoc.html
Vignon-Clementel IE, Figueroa CA, Jansen KE, Taylor CA (2006) Outflow boundary conditions for three-dimensional finite element modeling of blood flow and pressure in arteries. Comput Methods Appl Mech Eng 195:3776–3796
Voight ML, Hoogenboom BT, Prentice WE (2007) Musculoskeletal interventions: techniques for therapeutic exercise. McGraw-Hill, New York
Weber TF, von Tengg-Kobligk H, Kopp-Schneider A, Ley-Zaporozhan J, Kauczor HU, Ley S (2011) High-resolution phase-contrast MRI of aortic and pulmonary blood flow during rest and physical exercise using a MRI compatible bicycle ergometer. Eur J Radiol 80:103–108. doi:10.1016/j.ejrad.2010.06.045
Wendell DC et al (2013) Including aortic valve morphology in computational fluid dynamics simulations: initial findings and application to aortic coarctation. Med Eng Phys 35:723–735. doi:10.1016/j.medengphy.2012.07.015
Wentzel JJ et al (2005) Does shear stress modulate both plaque progression and regression in the thoracic aorta? Human study using serial magnetic resonance imaging. J Am Coll Cardiol 45:846–854. doi:10.1016/j.jacc.2004.12.026
Westerhof N, Stergiopulos N, Noble MIM (2005) Snapshots of hemodynamics: an aid for clinical research and graduate education. Springer, New York
Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. NeuroImage 31:1116–1128. doi:10.1016/j.neuroimage.2006.01.015
Zamir M, Sinclair P, Wonnacott TH (1992) Relation between diameter and flow in major branches of the arch of the aorta. J Biomech 25:1303–1310
Zanjani KS et al (2008) Feasibility and efficacy of stent redilatation in aortic coarctation. Catheter Cardiovasc Interv 72:552–556. doi:10.1002/ccd.21701
Acknowledgments
This work was supported by an American Heart Association Postdoctoral Fellowship, 10POST4210030 (to LE) and a National Institutes of Health Award R15HL096096-01 (to JFL). We also gratefully acknowledge the guidance and contributions of Mary Krolikowski RN, MSN, Kristen Andersen, Sheila Moore MD FACR, Robert Prost PhD, Barbara Hilker, Marjorie Bissette, Jim Joers PhD, David Wendell PhD, Brett Arand MS, Timothy Gundert MS, Nutta-On Promjunyakul PhD, and Atefeh Razavi MS.
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Ellwein, L., Samyn, M.M., Danduran, M. et al. Toward translating near-infrared spectroscopy oxygen saturation data for the non-invasive prediction of spatial and temporal hemodynamics during exercise. Biomech Model Mechanobiol 16, 75–96 (2017). https://doi.org/10.1007/s10237-016-0803-4
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DOI: https://doi.org/10.1007/s10237-016-0803-4