Trabeculae carneae as models of the ventricular walls: implications for the delivery of oxygen

Trabeculae carneae are the smallest naturally arising collections of linearly arranged myocytes in the heart. They are the preparation of choice for studies of function of intact myocardium in vitro. In vivo, trabeculae are unique in receiving oxygen from two independent sources: the coronary circulation and the surrounding ventricular blood. Because oxygen partial pressure (PO2) in the coronary arterioles is identical in specimens from both ventricles, whereas that of ventricular blood is 2.5-fold higher in the left ventricle than in the right ventricle, trabeculae represent a “natural laboratory” in which to examine the influence of “extravascular” PO2 on the extent of capillarization of myocardial tissue. We exploit this advantage to test four hypotheses. (1) In trabeculae from either ventricle, a peripheral annulus of cells is devoid of capillaries. (2) Hence, sufficiently small trabeculae from either ventricle are totally devoid of capillaries. (3) The capillary-to-myocyte ratios in specimens from either ventricle are identical to those of their respective walls. (4) Capillary-to-myocyte ratios are comparable in specimens from either ventricle, reflecting equivalent energy demands in vivo, driven by identical contractile frequencies and comparable wall stresses. We applied confocal fluorescent imaging to trabeculae in cross section, subsequently using semi-automated segmentation techniques to distinguish capillaries from myocytes. We quantified the capillary-to-myocyte ratios of trabeculae from both ventricles and compared them to those determined for the ventricular free walls and septum. Quantitative interpretation was furthered by mathematical modeling, using both the classical solution to the diffusion equation for elliptical cross sections, and a novel approach applicable to cross sections of arbitrary shape containing arbitrary disposition of capillaries and non-respiring collagen cords.

[1]  D. Loiselle Stretch-induced increase in resting metabolism of isolated papillary muscle. , 1982, Biophysical journal.

[2]  Bruce H Smaill,et al.  Automated imaging of extended tissue volumes using confocal microscopy , 2005, Microscopy research and technique.

[3]  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.

[4]  J. Daut,et al.  The energy expenditure of actomyosin‐ATPase, Ca(2+)‐ATPase and Na+,K(+)‐ATPase in guinea‐pig cardiac ventricular muscle. , 1994, The Journal of physiology.

[5]  Purva Joshi,et al.  Surface imaging microscopy using an ultramiller for large volume 3D reconstruction of wax‐ and resin‐embedded tissues , 2007, Microscopy research and technique.

[6]  F. Hossler,et al.  Anatomy and morphometry of myocardial capillaries studied with vascular corrosion casting and scanning electron microscopy: a method for rat heart. , 1986, Scanning electron microscopy.

[7]  J. Tune,et al.  Mechanisms of Oxygen Demand/Supply Balance in the Right Ventricle , 2005, Experimental biology and medicine.

[8]  H. T. ter Keurs,et al.  Tension Development and Sarcomere Length in Rat Cardiac Trabeculae: Evidence of Length‐Dependent Activation , 1980, Circulation research.

[9]  G. Zahalak,et al.  The effect of hyperosmolality on the rate of heat production of quiescent trabeculae isolated from the rat heart , 1996, The Journal of general physiology.

[10]  J. Murray,et al.  On the role of myoglobin in muscle respiration. , 1974, Journal of theoretical biology.

[11]  D. Loiselle The effect of myoglobin-facilitated oxygen transport on the basal metabolism of papillary muscle. , 1987, Biophysical journal.

[12]  K Rakusan,et al.  Principles underlying vascular adaptation/angiogenesis. , 1999, Advances in experimental medicine and biology.

[13]  H. Keurs,et al.  Force and velocity of sarcomere shortening in trabeculae from rat heart. Effects of temperature. , 1990 .

[14]  D. Le,et al.  Anatomy and morphometry of myocardial capillaries studied with vascular corrosion casting and scanning electron microscopy: a method for rat heart. , 1986 .

[15]  M. Gao,et al.  Myocyte hypertrophy and capillarization in spontaneously hypertensive stroke-prone rats. , 1997, Advances in experimental medicine and biology.

[16]  Ron B. H. Wills,et al.  Effects of temperature. , 2007 .

[17]  R. Jaspers,et al.  Krogh's diffusion coefficient for oxygen in isolated Xenopus skeletal muscle fibers and rat myocardial trabeculae at maximum rates of oxygen consumption. , 2005, Journal of applied physiology.

[18]  Joseph T. Wearn,et al.  THE EXTENT OF THE CAPILLARY BED OF THE HEART , 1928, The Journal of experimental medicine.

[19]  Ginés Viscor,et al.  Capillary supply and fiber morphometry in rat myocardium after intermittent exposure to hypobaric hypoxia. , 2007, High altitude medicine & biology.

[20]  G. Elzinga,et al.  Heat production of quiescent ventricular trabeculae isolated from guinea‐pig heart. , 1988, The Journal of physiology.

[21]  K. Rakušan Verification of coronary angiogenesis by quantitative morphology , 2004, Molecular and Cellular Biochemistry.

[22]  I. LeGrice,et al.  3‐Dimensional configuration of perimysial collagen fibres in rat cardiac muscle at resting and extended sarcomere lengths , 1999, The Journal of physiology.

[23]  J. Gatica,et al.  Oxygen diffusion through natural extracellular matrices: implications for estimating "critical thickness" values in tendon tissue engineering. , 2008, Tissue engineering. Part A.

[24]  C. Barclay Modelling diffusive O(2) supply to isolated preparations of mammalian skeletal and cardiac muscle. , 2005, Journal of muscle research and cell motility.

[25]  G. Elzinga,et al.  Substrate dependence of energy metabolism in isolated guinea‐pig cardiac muscle: a microcalorimetric study. , 1989, The Journal of physiology.

[26]  P. Janssen,et al.  Effect of muscle dimensions on trabecular contractile performance under physiological conditions , 2006, Pflügers Archiv.

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

[28]  H. T. ter Keurs,et al.  Spontaneous and propagated contractions in rat cardiac trabeculae , 1989, The Journal of general physiology.

[29]  A unique micromechanocalorimeter for simultaneous measurement of heat rate and force production of cardiac trabeculae carneae. , 2009, Journal of applied physiology.

[30]  Archibald Vivian Hill,et al.  The Diffusion of Oxygen and Lactic Acid through Tissues , 1928 .

[31]  C. Barclay Modelling diffusive O2 supply to isolated preparations of mammalian skeletal and cardiac muscle , 2005, Journal of Muscle Research & Cell Motility.

[32]  Jeffrey L Clendenon,et al.  Voxx: a PC-based, near real-time volume rendering system for biological microscopy. , 2002, American journal of physiology. Cell physiology.

[33]  B. Katz TRAILS AND TRIALS IN PHYSIOLOGY , 1965 .

[34]  Steven Goodman Toward Evidence-Based Medical Statistics. 2: The Bayes Factor , 1999, Annals of Internal Medicine.