Direct observation of epicardial coronary capillary hemodynamics during reactive hyperemia and during adenosine administration by intravital video microscopy.

Using high-resolution intravital charge-coupled device video microscopy, we visualized the epicardial capillary network of the beating canine heart in vivo to elucidate its functional role under control conditions, during reactive hyperemia (RH), and during intracoronary adenosine administration. The pencil-lens video-microscope probe was placed over capillaries fed by the left anterior descending artery in atrioventricular-blocked hearts of open-chest, anesthetized dogs paced at 60-90 beats/min (n = 17). In individual capillaries under control conditions, red blood cell flow was predominant during systole or diastole, indicating that the watershed between diastolic arterial and systolic venous flows is located within the capillaries. Capillary flow increased during RH and reached a peak flow velocity (2.1 +/- 0.6 mm/s), twice as high as control (1.2 +/- 0.5 mm/s), with enhancement of intercapillary cross-connection flow and enlargement of diameter (by 17%). With adenosine, capillary flow velocity significantly increased (1.8 +/- 0.7 mm/s). However, the increase in volumetric capillary flow with adenosine estimated from red blood cell velocity and diameter was less than the increase in arterial flow, whereas that during RH was nearly equivalent to the increase in arterial flow. There was a time lag of approximately 1.5 s for refilling of capillaries during RH, indicating their function as capacitance vessels. In conclusion, the coronary capillary network functions as 1) the major watershed between diastolic-dominant arterial and systolic-dominant venous flows, 2) a capacitor, and 3) a significant local flow amplifier and homogenizer of blood supply during RH, but with adenosine the increase in capillary flow velocity was less than the increase in arterial flow.

[1]  J. Spaan,et al.  Oxidized lipoproteins degrade the endothelial surface layer : implications for platelet-endothelial cell adhesion. , 2000, Circulation.

[2]  P. Lunkenheimer,et al.  [Morphology and function of an intramyocardial "Sinusoidal" flow net (author's transl)]. , 1974, Thoraxchirurgie, vaskulare Chirurgie.

[3]  J D Laird,et al.  Diastolic‐Systolic Coronary Flow Differences are Caused by Intramyocardial Pump Action in the Anesthetized Dog , 1981, Circulation research.

[4]  Yasuo Ogasawara,et al.  Evaluation of phasic blood flow velocity in the great cardiac vein by a laser Doppler method , 1985, Heart and Vessels.

[5]  Eiji Toyota,et al.  Dynamic Changes in Three-Dimensional Architecture and Vascular Volume of Transmural Coronary Microvasculature Between Diastolic- and Systolic-Arrested Rat Hearts , 2002, Circulation.

[6]  J B Bassingthwaighte,et al.  Microvasculature of the dog left ventricular myocardium. , 1974, Microvascular research.

[7]  F. Kajiya,et al.  Effect of coronary stenosis on phasic pattern of septal artery in dogs. , 1992, The American journal of physiology.

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

[9]  Yasuo Ogasawara,et al.  Intramyocardial Influences on Blood Flow Distributions in the Myocardial Wall , 2000, Annals of Biomedical Engineering.

[10]  Hans Vink,et al.  The Endothelial Glycocalyx Protects Against Myocardial Edema , 2003, Circulation research.

[11]  C. Desjardins,et al.  Heparinase treatment suggests a role for the endothelial cell glycocalyx in regulation of capillary hematocrit. , 1990, The American journal of physiology.

[12]  Hoffman Ji A critical view of coronary reserve. , 1987, Circulation.

[13]  F. Crea,et al.  Role of adenosine in pathogenesis of anginal pain. , 1990, Circulation.

[14]  F. Kajiya,et al.  Quantitative Blood Velocity Mapping in Glomerular Capillaries by in vivo Observation with an Intravital Videomicroscope , 2000, Methods of Information in Medicine.

[15]  T Takishima,et al.  Phasic Blood Flow Velocity Pattern in Epimyocardial Microvessels in the Beating Canine Left Ventricle , 1986, Circulation research.

[16]  P A Lachenbruch,et al.  Quantitative Changes in the Capillary Bed during Developing, Peak, and Stabilized Cardiac Hypertrophy in the Spontaneously Hypertensive Rat , 1982, Circulation research.

[17]  J. Hoffman A critical view of coronary reserve. , 1987, Circulation.

[18]  P A Wieringa,et al.  Oxygen diffusion in a network model of the myocardial microcirculation. , 1993, International journal of microcirculation, clinical and experimental.

[19]  F Kajiya,et al.  In vivo observation of subendocardial microvessels of the beating porcine heart using a needle-probe videomicroscope with a CCD camera. , 1993, Circulation research.

[20]  Klassen Ga The coronary circulation: quo vadis? , 1999 .

[21]  Ghassan S Kassab,et al.  A hemodynamic analysis of coronary capillary blood flow based on anatomic and distensibility data. , 1999, American journal of physiology. Heart and circulatory physiology.

[22]  F. Kajiya,et al.  Direct in vivo observation of subendocardial arteriolar response during reactive hyperemia. , 1995, Circulation research.

[23]  A. Kovalik,et al.  A simple technique for production of chronic complete heart block in dogs. , 1968, Journal of applied physiology.

[24]  A. Pries,et al.  Biophysical aspects of blood flow in the microvasculature. , 1996, Cardiovascular research.

[25]  Yasuo Ogasawara,et al.  Functional Characteristics of Intramyocardial Capacitance Vessels during Diastole in the Dog , 1986, Circulation research.

[26]  D. Slaaf,et al.  Capillary diameter changes during low perfusion pressure and reactive hyperemia in rabbit skeletal muscle. , 1995, The American journal of physiology.

[27]  R. Bing,et al.  Studies of the coronary microcirculation of the cat. , 1971, The American journal of cardiology.

[28]  J M Fauvel,et al.  Microcirculation in the Ventricle of the Dog and Turtle , 1974, Circulation research.

[29]  C. Jones,et al.  Role of nitric oxide in the coronary microvascular responses to adenosine and increased metabolic demand. , 1995, Circulation.

[30]  F Kajiya,et al.  In vivo observations of the intramural arterioles and venules in beating canine hearts , 1998, The Journal of physiology.

[31]  J I Hoffman,et al.  Does systolic subepicardial perfusion come from retrograde subendocardial flow? , 1992, The American journal of physiology.

[32]  J Dankelman,et al.  Dynamics of flow, resistance, and intramural vascular volume in canine coronary circulation. , 2000, American journal of physiology. Heart and circulatory physiology.

[33]  B. Duling,et al.  Adenosine A3 Receptor Activation Modulates the Capillary Endothelial Glycocalyx , 2004, Circulation research.

[34]  E. Bassenge,et al.  Intracapillary hemoglobin oxygen saturation and oxygen consumption in different layers of the left ventricular myocardium , 1977, Pflügers Archiv.

[35]  M. Marcus,et al.  Redistribution of coronary microvascular resistance produced by dipyridamole. , 1989, The American journal of physiology.

[36]  J. Hoffman,et al.  Changes in contractility and afterload have only slight effects on subendocardial systolic flow impediment. , 1995, The American journal of physiology.

[37]  M. Marcus,et al.  Phasic Coronary Blood Flow Velocity in Intramural and Epicardial Coronary Arteries , 1982, Circulation research.

[38]  G. Klassen The coronary circulation: quo vadis? , 1999, Cardiologia.

[39]  J. Spaan,et al.  Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL. , 2001, American journal of physiology. Heart and circulatory physiology.

[40]  T. E. Gayeski,et al.  Precapillary O2 loss and arteriovenous O2 diffusion shunt are below limit of detection in myocardium. , 1989, Advances in experimental medicine and biology.

[41]  F. Kajiya,et al.  Intravital videomicroscopy of peritubular capillaries in renal ischemia. , 2002, American journal of physiology. Renal physiology.

[42]  J. Spaan,et al.  Forward coronary flow normally seen in systole is the result of both forward and concealed back flow , 1981, Basic Research in Cardiology.

[43]  M. Steinhausen,et al.  Microcirculation of the epimyocardial layer of the heart , 1978, Pflügers Archiv.