Scaling Laws of Flow Rate, Vessel Blood Volume, Lengths, and Transit Times With Number of Capillaries

The structure-function relation is one of the oldest hypotheses in biology and medicine; i.e., form serves function and function influences form. Here, we derive and validate form-function relations for volume, length, flow, and mean transit time in vascular trees and capillary numbers of various organs and species. We define a vessel segment as a “stem” and the vascular tree supplied by the stem as a “crown.” We demonstrate form-function relations between the number of capillaries in a vascular network and the crown volume, crown length, and blood flow that perfuses the network. The scaling laws predict an exponential relationship between crown volume and the number of capillaries with the power, λ, of 4/3 < λ < 3/2. It is also shown that blood flow rate and vessel lengths are proportional to the number of capillaries in the entire stem-crown systems. The integration of the scaling laws then results in a relation between transit time and crown length and volume. The scaling laws are both intra-specific (i.e., within vasculatures of various organs, including heart, lung, mesentery, skeletal muscle and eye) and inter-specific (i.e., across various species, including rats, cats, rabbits, pigs, hamsters, and humans). This study is fundamental to understanding the physiological structure and function of vascular trees to transport blood, with significant implications for organ health and disease.

[1]  Yunlong Huo,et al.  Intraspecific scaling laws of vascular trees , 2012, Journal of The Royal Society Interface.

[2]  G S Kassab,et al.  Morphometry of pig coronary arterial trees. , 1993, The American journal of physiology.

[3]  B Dawant,et al.  Analysis of vascular pattern and dimensions in arteriolar networks of the retractor muscle in young hamsters. , 1987, Microvascular research.

[4]  J. Karbowski Scaling of Brain Metabolism and Blood Flow in Relation to Capillary and Neural Scaling , 2011, PloS one.

[5]  T F Sherman,et al.  On connecting large vessels to small. The meaning of Murray's law , 1981, The Journal of general physiology.

[6]  B. Fenton,et al.  Microcirculatory model relating geometrical variation to changes in pressure and flow rate , 1981, Annals of Biomedical Engineering.

[7]  J. Weitz,et al.  Re-examination of the "3/4-law" of metabolism. , 2000, Journal of theoretical biology.

[8]  G. Kassab Scaling laws of vascular trees: of form and function. , 2006, American journal of physiology. Heart and circulatory physiology.

[9]  J. LaManna,et al.  Regional Cerebral Metabolites, Blood Flow, Plasma Volume, and Mean Transit Time in Total Cerebral Ischemia in the Rat , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[10]  K. Zierler,et al.  On the theory of the indicator-dilution method for measurement of blood flow and volume. , 1954, Journal of applied physiology.

[11]  R. Yen,et al.  Morphometry of the human pulmonary vasculature. , 1996, Journal of applied physiology.

[12]  C. D. Murray,et al.  The Physiological Principle of Minimum Work: II. Oxygen Exchange in Capillaries. , 1926, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Y. Huo,et al.  Intraspecific scaling laws are preserved in ventricular hypertrophy but not in heart failure. , 2016, American journal of physiology. Heart and circulatory physiology.

[14]  Chengpei Xu,et al.  Arterial enlargement, tortuosity, and intimal thickening in response to sequential exposure to high and low wall shear stress. , 2004, Journal of vascular surgery.

[15]  E. Ziegel,et al.  Bootstrapping: A Nonparametric Approach to Statistical Inference , 1993 .

[16]  K. Horsfield,et al.  Morphometry of pulmonary veins in man , 2007, Lung.

[17]  Y C Fung,et al.  Morphometry of cat's pulmonary arterial tree. , 1984, Journal of biomechanical engineering.

[18]  James H. Brown,et al.  A General Model for the Origin of Allometric Scaling Laws in Biology , 1997, Science.

[19]  G S Kassab,et al.  Topology and dimensions of pig coronary capillary network. , 1994, The American journal of physiology.

[20]  R M Lehman,et al.  Mechanism of enlargement of major cerebral collateral arteries in rabbits. , 1991, Stroke.

[21]  Ghassan S. Kassab,et al.  Design of coronary circulation: A minimum energy hypothesis , 2007 .

[22]  H. Uylings,et al.  Optimization of diameters and bifurcation angles in lung and vascular tree structures. , 1977, Bulletin of mathematical biology.

[23]  G Cumming,et al.  Morphometry of the Human Pulmonary Arterial Tree , 1973, Circulation research.

[24]  B Dawant,et al.  Quantitative analysis of arteriolar network architecture in cat sartorius muscle. , 1987, The American journal of physiology.

[25]  A. Pries,et al.  Resistance to blood flow in microvessels in vivo. , 1994, Circulation research.

[26]  Y C Fung,et al.  Morphometry of cat pulmonary venous tree. , 1983, Journal of applied physiology: respiratory, environmental and exercise physiology.

[27]  G. Hutchins,et al.  Vessel Caliber and Branch‐Angle of Human Coronary Artery Branch‐Points , 1976, Circulation research.

[28]  G. S. Kassab,et al.  A Computer Reconstruction of the Entire Coronary Arterial Tree Based on Detailed Morphometric Data , 2005, Annals of Biomedical Engineering.

[29]  G. Coppini,et al.  Hypoxia- or hyperoxia-induced changes in arteriolar vasomotion in skeletal muscle microcirculation. , 1991, The American journal of physiology.

[30]  W J Powers,et al.  Cerebral hemodynamic impairment , 1999, Neurology.

[31]  M. Labarbera Principles of design of fluid transport systems in zoology. , 1990, Science.

[32]  G S Kassab,et al.  Diameter-defined Strahler system and connectivity matrix of the pulmonary arterial tree. , 1994, Journal of applied physiology.

[33]  C. R. White,et al.  Mammalian basal metabolic rate is proportional to body mass2/3 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Ghassan S. Kassab,et al.  Analysis of pig’s coronary arterial blood flow with detailed anatomical data , 2007, Annals of Biomedical Engineering.

[35]  J D Humphrey,et al.  Fundamental role of axial stress in compensatory adaptations by arteries. , 2009, Journal of biomechanics.

[36]  A. Pries,et al.  Origins of heterogeneity in tissue perfusion and metabolism. , 2009, Cardiovascular research.

[37]  C. F. Wu JACKKNIFE , BOOTSTRAP AND OTHER RESAMPLING METHODS IN REGRESSION ANALYSIS ' BY , 2008 .

[38]  Y. Huo,et al.  Capillary Perfusion and Wall Shear Stress Are Restored in the Coronary Circulation of Hypertrophic Right Ventricle , 2007, Circulation research.

[39]  A. Pries,et al.  Topological structure of rat mesenteric microvessel networks. , 1986, Microvascular research.