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Cardiac Basal Metabolism Japanese Journal of Physiology, 51, 399–426, 2001 REVIEW Cardiac Basal Metabolism C. L. GIBBS and D. S. LOISELLE* Department of Physiology, Faculty of Medicine, Nursing and Health Sciences, Monash University, PO Box 13F, Monash University, Victoria 3800, Australia; and *Department of Physiology, Faculty of Medicine and Health Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand Abstract: We endeavor to show that the me- usage remain unresolved. We consider many of tabolism of the nonbeating heart can vary over the physiological factors that can alter the basal an extreme range: from values approximating metabolic rate, stressing the importance of sub- those measured in the beating heart to values of strate supply. We point out that the protective ef- only a small fraction of normal—perhaps mimick- fect of hypothermia may be less than is com- ing the situation of nonflow arrest during cardiac monly assumed in the literature and suggest that bypass surgery. We discuss some of the techni- hypoxia and ischemia may be able to regulate cal issues that make it difficult to establish the basal metabolic rate, thus making an important magnitude of basal metabolism in vivo. We con- contribution to the phenomenon of cardiac hiber- sider some of the likely contributors to its magni- nation. [Japanese Journal of Physiology, 51, tude and point out that the biochemical reasons 399–426, 2001] for a sizable fraction of the heart’s basal ATP Key words: whole hearts, isolated preparations, biochemical contributors, modifiers, species differ- ence, temperature, substrate, hypoxia. heart operations are performed on arrested hearts I. Definition and Introduction worldwide each year, it would seem imperative that The cardiac basal metabolism is the rate of energy we understand the cellular mechanisms that can expenditure of the quiescent myocardium. It is also change the magnitude of basal metabolism. called the resting metabolism or the arrested heart me- A. V. Hill [4] has pointed out that in examining tabolism. It has been measured in numerous ways, and physiological activities, it is necessary to assume a in vivo there is good evidence that it accounts for baseline from which some quantity or rate can be about 1/5 to 1/3 of the total energy flux. The difficulty measured. If the energy flux produced by the beating arises, however, when the heart is stopped because the heart were very large compared with the energy flux magnitude of the basal metabolism depends, as blood of the arrested heart, baseline ambiguity would be rel- viscosity, on how and under what physiological condi- atively unimportant. But this is not so in regard to the tion it is measured. It is possible for the in vivo basal heart; its basal metabolism is high. Within a species, value to fall to less than 1/5 of its original value with- the basal metabolism of cardiac tissue is several-fold out cellular damage or to increase to values 5 times higher than the resting metabolism of skeletal muscle greater than its probable in vivo magnitude (i.e., to and is an order of magnitude greater than the resting rise to values in excess of the energy flux of the nor- metabolism of amphibian skeletal muscle. mally beating heart) by altering the composition of the Species differences are clearly evident in the mag- perfusion medium. We have written on this subject nitude of cardiac basal metabolism, and we believe several times [1–3], but believe that developments in that the major reason for these differences relates to knowledge now make it possible for us to speculate in the leakiness of cell membranes, such as those of the a more informed manner. Since several million open- sarcolemma and sarcoplasmic reticulum and those of Received on June 11, 2001; accepted on June 15, 2001 Correspondence should be addressed to: Colin Gibbs, Department of Physiology, Monash University, PO Box 13F, Monash University, Vic- toria 3800, Australia. Tel: 161–3–9905–2513, Fax: 161–3–9905–5583, E–mail: [email protected] Japanese Journal of Physiology Vol. 51, No. 4, 2001 399 C. L. GIBBS and D. S. LOISELLE intracellular organelles [5]. The ratio of mitochondrial Table 1. Interconversion of commonly encountered to cell volume is higher in the smaller species [6], and units. the mitochondria in the smaller mammals have a Oxygen usage Thermal equivalent higher proton leak [7], thus establishing a cellular futile cycle. It is also well known that the protein 1 mcal/g/min 0.07 mW g21 turnover rate increases in the smaller species [8]. 1 ml/100 g/min 3.3 mW g21 m 21 The nonbeating metabolism of the heart continues 1 l/mgdry/h 1.23 mW g 21 to be an enigma in regard to its biochemical and phys- 1 ml/gdry/min 74 mW g 1 nmol/g/s 0.47 mW g21 iological basis. In a recent paper [9] it has been shown 21 1 mmol/gdry/min 1.74 mW g that for a variety of organs, about 10% of their O 21 2 1 mmol/gdry/h 29 mW g 21 usage is nonmitochondrial in origin, which agrees 1 nmol/mgprotein/min 1.3 mW g with cardiac data from Challoner [10]. Approximately 1 ng atom O/mg/min 0.25 mW g21* 2 20–30% is used to maintain the mitochondrial mem- 1 mM ATP/s 0.05 mW g 1† brane potential against a leak of protons. Indeed, Ha- A conversion from units of oxygen consumption requires an worth et al. [11] showed a few years ago in myocyte estimate of the energetic equivalent of oxygen. This value studies that mitochondrial ATPase usage is a signifi- depends on the fuel being oxidized, being less for fats cant drain on the energy resources of quiescent hearts, (19.8 kJ l21 [12]) than for carbohydrates (21.4 kJ l21). The and that cardiac contracture can be delayed by inhibit- latter value (appropriate for STP: standard temperature ing mitochondrial ATP usage with oligomycin. The [0°C] and pressure [101 kPa]) represents the product of the energy yield and stoichiometry of complete combustion of remaining 60–70% of O2 usage is needed for mito- glucose: 2.87 MJ mol21 and 6 mol oxygen per mol glucose, chondrial ATP manufacture to provide energy for pro- respectively. The energetic equivalent of oxygen falls to tein synthesis (20–25%), maintenance of transmem- 19.9 and 18.8 kJ l21 at 20 and 37°C, respectively from 21.4 brane Na1 gradients (,20%) and Ca21 gradients kJ l21 at 0°C. This reflects the corresponding values of 2 (5%), and resting actomyosin ATPase (,5%), with 25.4 l mol 1, 22.4, and 24.0, oxygen, respectively, at these activities such as nucleic acid synthesis and substrate three commonly encountered temperatures. In most stud- ies, the metabolic proportion of carbohydrates to fats is un- cycling accounting for the remaining ATP turnover known, as is detailed knowledge of the substrate species. [9]. To what extent does this energy balance apply to Furthermore, when volume units are employed, the temper- quiescent cardiac muscle? ature to which they are referred is commonly unreported. One difficulty with energetic studies in the litera- For these reasons we have adopted a single value for the energetic equivalent of oxygen: 20 kJ mol21. The error in ture is the different way energy flux is reported. In this 2 2 this simplification may not be insubstantial. 1 W51Js 1; review we will usually express the data on a mW g 1 1g;1 g wet wt; 1 g dry wt;4.5 g wet wt (i.e., H2O content wet-weight basis, and in Table 1 we list many of the of tissue is 78% [13]); 1 cm3;0.233 g dry wt [14]; alternative ways it has been expressed. 1cm3;60 mg mitochondrial protein [14]; 1 g;162 mg dry protein [15]; †Assuming 50 kJ/mol ATP; *Assuming 32 g II. Preparations and Methods atom O/mol O2. of Measurements For the experimentalist interested in cardiac basal me- fusates can be circulated either at constant pressure or tabolism, a wide choice of preparations and methods at a constant rate of volume flow. For isolated whole- of arrest is available. Whereas this degree of choice heart preparations, Langendorff-perfusion [16] is the provides latitude to address different questions, there common choice whereby flow is retrograde through seems to be little doubt that it also contributes to the the distal stump of the aorta but anterograde through wide range of values reported in the literature for the the coronary vessels. Adequate perfusion of the tis- magnitude of the basal metabolic rate of cardiac mus- sues thus relies on the competency of the aortic valve. cle. Choice of metabolic index: Whole-heart basal (i) Whole hearts. metabolic rate has been assessed by using the methods Choice of perfusion: Whole-heart preparations can of NMR spectroscopy [32]. But the rate of oxygen be employed in complete isolation [16, 17], as a heart- consumption (V˙O2) has been the metabolic measure- lung preparation [18–21] or in situ during cardiac by- ment of choice, reflecting the overwhelmingly aerobic pass [22–25]. Circulation is commonly extracorporeal nature of cardiac metabolism, though some investiga- but may be from the heart of a donor animal via cross- tors have carefully assessed the rate of anaerobic me- perfusion [26, 27]. The coronary circulation can be tabolism, usually indexed as the rate of production of saline-, blood- [28, 29], perfluorocarbon-supple- lactate [22, 24, 28, 33, 34]. V˙O2 is then commonly as- mented [30], or even gas- [31] perfused.
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