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Rarefaction and blood pressure in systemic and pulmonary arteries

Published online by Cambridge University Press:  02 July 2012

Mette S. Olufsen
Affiliation:
Department of Mathematics, North Carolina State University, Raleigh, NC 27502, USA
N. A. Hill*
Affiliation:
School of Mathematics and Statistics, University of Glasgow, Glasgow G12 8QW, UK
Gareth D. A. Vaughan
Affiliation:
School of Mathematics and Statistics, University of Glasgow, Glasgow G12 8QW, UK
Christopher Sainsbury
Affiliation:
BHF Glasgow Cardiovascular Research Centre, University of Glasgow, Glasgow G12 8QQ, UK
Martin Johnson
Affiliation:
Scottish Pulmonary Vascular Unit, Golden Jubilee National Hospital, Glasgow G81 4HX, UK
*
Email address for correspondence: N.A.Hill@maths.gla.ac.uk

Abstract

The effects of vascular rarefaction (the loss of small arteries) on the circulation of blood are studied using a multiscale mathematical model that can predict blood flow and pressure in the systemic and pulmonary arteries. We augmented a model originally developed for the systemic arteries by Olufsen and coworkers and Ottesen et al. (2004) to (a) predict flow and pressure in the pulmonary arteries, and (b) predict pressure propagation along the small arteries in the vascular beds. The systemic and pulmonary arteries are modelled as separate bifurcating trees of compliant and tapering vessels. Each tree is divided into two parts representing the ‘large’ and ‘small’ arteries. Blood flow and pressure in the large arteries are predicted using a nonlinear cross-sectional-area-averaged model for a Newtonian fluid in an elastic tube with inflow obtained from magnetic resonance measurements. Each terminal vessel within the network of the large arteries is coupled to a vascular bed of small ‘resistance’ arteries, which are modelled as asymmetric structured trees with specified area and asymmetry ratios between the parent and daughter arteries. For the systemic circulation, each structured tree represents a specific vascular bed corresponding to major organs and limbs. For the pulmonary circulation, there are four vascular beds supplied by the interlobar arteries. This paper presents the first theoretical calculations of the propagation of the pressure and flow waves along systemic and pulmonary large and small arteries. Results for all networks are in agreement with published observations. Two studies were done with this model. First, we showed how rarefaction can be modelled by pruning the tree of arteries in the microvascular system. This was done by modulating parameters used for designing the structured trees. Results showed that rarefaction leads to increased mean and decreased pulse pressure in the large arteries. Second, we investigated the impact of decreasing vessel compliance in both large and small arteries. Results showed that the effects of decreased compliance in the large arteries far outweigh the effects observed when decreasing the compliance of the small arteries. We further showed that a decrease of compliance in the large arteries results in pressure increases consistent with observations of isolated systolic hypertension, as occurs in ageing.

Type
Papers
Copyright
Copyright © Cambridge University Press 2012

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References

1. Antonios, T. F. 2006 Microvascular rarefaction in hypertension – reversal or over-correction by treatment? Am. J. Hypertens. 19, 484485.CrossRefGoogle ScholarPubMed
2. Antonios, T. F., Rattrat, F. M., Singer, D. R. J., Markandu, N. D., Mortimer, P. S. & MacGregor, G. A. 2003 Rarefaction of skin capillaries in normotensive offspring of individuals with essential hypertension. Heart J. 89, 175178.CrossRefGoogle ScholarPubMed
3. Antonios, T. F., Singer, D. R. J., Markandu, N. D., Mortimer, P. S. & MacGregor, G. A. 1999 Rarefaction of skin capillaries in borderline essential hypertension suggests an early structural abnormality. Hypertension 34, 655658.CrossRefGoogle ScholarPubMed
4. Atabek, H. B. 1968 Wave propagation through a viscous fluid contained in a tethered, initially stressed, orthotropic elastic tube. Biophys. J. 8, 626649.CrossRefGoogle Scholar
5. Atabek, H. B. & Lew, H. S. 1966 Wave propagation through a viscous incompressible fluid contained in an initially stressed elastic tube. Biophys. J. 6, 481503.CrossRefGoogle Scholar
6. Azer, K. & Peskin, C. S. 2007 A one-dimensional model of blood flow in arteries with friction and convection based on the Womersley velocity profile. Cardiovascular Engng 7, 5173.CrossRefGoogle ScholarPubMed
7. Caro, C., Pedley, T., Schroter, R. & Seed, W. 1978 The Mechanics of the Circulation. Oxford University Press.Google Scholar
8. Christensen, K. L. & Mulvany, M. J. 2001 Location of resistance arteries. J. Vascu. Res. 38, 112.CrossRefGoogle ScholarPubMed
9. Feihl, F., Liaudet, L., Waeber, B. & Levy, B. I. 2006 Hypertension: a disease of the microcirculation? Hypertension 48, 10121017.CrossRefGoogle ScholarPubMed
10. Franklin, S. 2004 Systolic blood pressure. Am. J. Hypertens. 17, 49S54S.CrossRefGoogle ScholarPubMed
11. Fung, Y. C. 1996 Biomechanics: Circulation. Springer.Google Scholar
12. Greene, A. S., Tonellato, P. J., Lui, J., Lombard, J. H. & Cowley, A. W. 1989 Microvascular rarefaction and tissue vascular resistance in hypertension. Am. J. Physiol. 256, 126131.Google ScholarPubMed
13. Griffith, T., Klassen, P. & Franklin, S. 2005 Systolic hypertension: an overview. Am. Heart J. 149, 769775.CrossRefGoogle ScholarPubMed
14. Hopkins, N. & McLoughlin, P. 2002 The structural basis of pulmonary hypertension in chronic lung disease: remodelling, rarefaction or angionesis? J. Anat. 201, 335348.CrossRefGoogle ScholarPubMed
15. Huang, W., Yen, R. T., McLaurine, M. & Bledsoe, G. 1996 Morphometry of the human pulmonary vasculature. J. Appl. Physiol. 81, 21232133.CrossRefGoogle ScholarPubMed
16. Hudetz, A. G. 1993 Percolation phenomenon: the effect of capillary network rarefaction. Microvasc. Res. 45, 110.CrossRefGoogle ScholarPubMed
17. Iberall, A. 1967 Anatomy and steady flow characteristics of the arterial system with an introduction to its pulsatile characteristics. Math. Biosci. 1, 375385.CrossRefGoogle Scholar
18. Krenz, G. S. & Dawson, C. A. 2003 Flow and pressure distributions in vascular networks consisting of distensible vessels. Am. J. Physiol. 284, H2192H2203.Google ScholarPubMed
19. Levy, B. I., Ambrosio, G., Pries, A. R. & Struijker-Boudier, H. A. 2001 Microcirculation in hypertension: a new target for treatment? Circulation 735740.CrossRefGoogle ScholarPubMed
20. Nichols, W. W. 2005 Clinical measurement of arterial stiffness obtained from noninvasive pressure waveforms. Am. J. Hypertens. 18, 3S10S.CrossRefGoogle ScholarPubMed
21. le Noble, J. L., Tangelder, G. J., Slaaf, D. W., van Essen, H., Reneman, R. S. & Struyker–Boudier, H. A. 1990 A functional morphometric study of the cremaster muscle microcirculation in young spontaneously hypertensive rats. J. Hypertens. 8, 741748.CrossRefGoogle ScholarPubMed
22. Noon, J. P., Walker, B. R., Webb, D. J., Shore, A. C., Holton, D. W., Edwards, H. V. & Watt, G. C. 1997 Impaired microvascular dilatation and capillary rarefaction in young adults with a predisposition to high blood pressure. J. Clin. Invest. 99, 18731879.CrossRefGoogle ScholarPubMed
23. Olufsen, M. S. 1998 Modeling the arterial system with reference to an anesthesia simulator. PhD thesis, Department of Mathematics, Roskilde University, Denmark.Google Scholar
24. Olufsen, M. S. 1999 Structured tree outflow condition for blood flow in larger systemic arteries. Am. J. Physiol. Heart Circ. Physiol. 276, H257H268.CrossRefGoogle ScholarPubMed
25. Olufsen, M. S., Peskin, C. S., Kim, W. Y., Pedersen, E. M. & Nadim, A. 2000 Numerical simulation and experimental validation of blood flow in arteries with structured-tree outflow conditions. Ann. Biomed. Engng 28, 12811299.CrossRefGoogle ScholarPubMed
26. Ottesen, J. T., Olufsen, M. S. & Larsen, J. K. 2004 Applied Mathematical Models in Human Physiology. SIAM.CrossRefGoogle Scholar
27. Peacock, A. J. & Rubin, L. J. 2004 Pulmonary Circulation: Diseases and their Treatment, 2nd edn. Hodder Arnold Publication.Google Scholar
28. Pedley, T. J. 1980 The Fluid Mechanics of Large Blood Vessels. Cambridge University Press.CrossRefGoogle Scholar
29. Popel, A. S. & Johnson, P. C. 2005 Microcirculation and Hemorheology. Annu. Rev. Fluid Mech. 37, 4369.CrossRefGoogle ScholarPubMed
30. Pries, A. R., Secomb, T. W. & Gaehtgens, P. 1995 Design principles of vascular beds. Circulat. Res. 77, 10171023.CrossRefGoogle ScholarPubMed
31. Roy, A. G. & Woldenberg, M. J. 1982 A generalization of the optimal models of arterial branching. Bull. Math. Biol. 44, 349360.CrossRefGoogle ScholarPubMed
32. Simonneau, G., Galie, N., Rubin, L. J., Langleben, D., Seeger, W., Domenighetti, G., Gibbs, S., Lebrec, D., Speich, R., Beghetti, M., Rich, S. & Fishman, A. 2004 Clinical classification of pulmonary hypertension. J. Am. Coll. Cardiol. 43, 512.CrossRefGoogle ScholarPubMed
33. Singhal, S., Henderson, R., Horsfield, K., Harding, K. & Cumming, G. 1973 Morphometry of the human pulmonary arterial tree. Circulat. Res. 33, 190197.CrossRefGoogle ScholarPubMed
34. Steele, B. N., Olufsen, M. S. & Taylor, C. A. 2007 Fractal network model for simulating abdominal and lower extremity blood flow during resting and exercise conditions. Comput. Meth. Biomech. Biomed. Engng 10, 3951.CrossRefGoogle ScholarPubMed
35. Syyed, R., Reeves, J. T., Welsh, D., Raeside, D., Johnson, M. K. & Peacock, A. J. 2008 The relationship between the components of pulmonary artery pressure remains constant under all conditions in both health and disease. Chest 133, 633639.CrossRefGoogle ScholarPubMed
36. Tuder, R. M., Yun, J. H., Bhunia, A. & Fijalkowska, I. 2007 Hypoxia and chronic lung disease. J. Molec. Med. 85, 13171324.CrossRefGoogle ScholarPubMed
37. Vaughan, G. D. A. 2010 Pulse propagation in the pulmonary and systemic arteries. PhD thesis, Faculty of Information and Mathematical Sciences, University of Glasgow, UK.Google Scholar