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ACTA MEDICA (Hradec Kralove) 1996; 39: 95-99

. REVIEW ARTICLE

Hibernating Myocardium - Mechanisms and Clinical Implications

Jan Knap, Jan Harrer, Jan Dominik

Department of Cardiac Surgery Charles University, Faculty of Medicine and Faculty Hospital;
(Head: doc. MUDr. J. Dominik, CSc.)

Summary: Hibernating myocardium is defined as persistently impaired myocardial and left ventricular function at rest resulting from reduced myocardial blood flow. It is postulated that despite the reduced coronary blood flow, metabolic activity is sufficient to prevent tissue necrosis. Recovery of the hibernating myocardium has clearly been shown to occur with the establishment of successful revascularization either by coronary bypass surgery or by percutaneous transluminal coronary angioplasty. The differentiation of viable, hibernating myocardium from non-viable myocardium in patients with coronary artery disease and left ventricular dysfunction is a key issue in the current era of myocardial revascularization.


Key words: Hibernating myocardium; Stunned myocardium; Coronary artery disease; Left ventricular dysfunction; Coronary artery bypass surgery


Introduction

Ischemic myocardial dysfunction, defined as a transient impairment of contractile function due to reduced coronary blood flow, has been well documented (34). Persistent impairment of contractile function was initially believed to represent irreversible myocardial damage resulting from myocardial infarction (13). In the 1970s several studies demonstrated that chronically dysfunctioning myocardium was able to resume contraction to some extent after revascularization (14). Thus, some areas of myocardium exhibiting left ventricular asynergy at rest had to be viable, since they recovered after the restoration of coronary flow.
In 1985, Rahimtoola proposed the concept of hibernating myocardium to describe a state of persistently impaired myocardial and left ventricular function at rest due to reduced coronary blood flow that can be partially or completely restored to normal if the myocardial oxygen supply/demand relationship is favorably altered, either by improving blood flow and/or by reducing demand (27). In his theory, based on clinical observations, hibernating myocardium was a result of downgrading of cardiac function so that blood flow and function were once again in equilibrium. As a result, neither myocardial necrosis, nor ischemia symptoms were present (15). The concept of hibernation presupposed that a reduction in coronary blood flow, i.e. the initial or triggering event, was followed by a downregulation in cardiac function to a point at which the limited oxygen supply enabled the maintenance of the biochemical functions that sustained cell integrity (16,27). If the myocardial oxygen supply/demand balance was subsequently altered either temporarily or permanently, then sypmtoms and signs of ischemia and/or of necrosis might occur (29).
The hibernating response of the heart, namely a reduction of cardiac function to cope with a reduced myocardial blood flow, was considered as an act of self-preservation (little blood, little work) and the hibernating heart was considered to be "a smart heart" (29).


A Historical Background

The initial investigators in the 1970s believed that persistent contractile left ventricular dysfunction in patients with coronary heart disease represented irreversible myocardial damage (13).
With the widespread use of coronary bypass surgery it became apparent that successful coronary revascularization was often associated with the return of myocardial contractility in the asynergic regions. Thus, it was hypothesised that some areas of myocardium exhibiting dysfunction at rest had to be viable, since they recovered after the restoration of coronary flow (14). Investigations focused on predicting which of these areas would recover contractile function using a variety of interventions aimed at either increasing the contractile function with catecholamine administration or postextrasystolic potentiation or reducing myocardial oxygen demand and/or increasing coronary blood flow with nitroglycerin (13,34). Subsequently, with the advent of nuclear cardiology, it became possible to gain better knowledge about the correlation between myocardial perfusion and the contractile function of the left ventricle. The work correlating myocardial perfusion with function was pivotal in describing the presence of severe wall-motion abnormatilies associated with coronary artery stenoses exceeding a 90% reduction of the coronary intraluminal diameter. The histopathology of these areas revealed a myocardium exhibiting an increased amount of fibrosis but with preserved myocardial cell integrity (1).
With the introduction of stunned myocardium by Braunwald and Kloner (4) in 1982, the interest of cardiologists focused on the new concept of persistent ischemic dysfunction (20,22). Myocardial stunning or postischemic left ventricular dysfunction, described a clinical state that persisted after reperfusion despite the absence of irreversible damage and despite the restoration of normal or near-normal coronary blood flow (2,4,10). The two "despites" were important to distinguish stunning from other causes of persistent ischemic dysfunction after reperfusion (such as infarction or persistent ischemia) that had nothing to do with stunning.
The last decade has witnessed an explosion of research effort in the area of stunned myocardium (3,19). The substantial evidence has been obtained that myocardial stunning is a widespread and important phenomenon readily seen in a number of clinical situations, e.g. the occurence of stunning after myocardial infarction and, more recently, following coronary reperfusion with thrombolysis or angioplasty (16,22,27). Perhaps the most common and important clinical manifestation of stunning occurs in the hearts of patients who have undergone ischemic cardiac arrest during cardiopulmonary bypass, despite the protection offered by hypothermia and cardioplegia. Following reperfusion many such hearts require support with inotropic agents and/or mechanical assistance for hours or days untill the stunning subsides (3,16). It should be noted that myocardial stunning is a fully reversible abnormality, provided of course that sufficient time is allowed for the myocardium to recover (4,20). It is a mild, sublethal injury where the hallmark is the presence of a flow-function "mismatch", i.e., a depression of function is out of proportion to a mild depresion of flow (32). The basic mechanisms of myocardial stunning are not yet completely elucidated, however, most probably it is not a problem of energy production, but rather of energy utilization.
In 1985, Rahimtoola proposed the concept of hibernating myocardium to describe a state when myocardial blood flow falls to a level sufficient to maintain cell viability, but not myocardial contraction (26). He considered the hibernation as a response to a chronic reduction in resting coronary blood flow, leading to a new equilibrium where myocardial metabolism was altered with a subsequent reduction in energy production and myocardial contractility (27). In contrast to other forms of reversible myocardial dysfunction, such as stunning, in hibernating myocardium flow and function were appropriately matched (31,32). This chronic adaptation could occur in the absence of angina (the lack of resting angina is a unique sign of chronic hibernation) or electrocardiographic evidence of ischemia and was thought to be a protective mechanism, reducing the oxygen demand of hypoperfused myocardium and preserving long-term viability (11). On imaging the heart, it presented as areas of left ventricular wall that could have been hypokinetic, akinetic or dyskinetic (29).
Hibernating and stunned myocardium are clinically very important conditions of contractile asynergy, since they are potentially reversible (16). Hibernating myocardium is similar to stunned myocardium in that both are characterized by viable myocardial cells with depressed function. More recently, some clinical studies have suggested that when ischemia is relieved, the hibernating myocardium exhibits nearly immediate return of function, whereas stunned myocardium exhibits gradual recovery (27). However, hibernating myocardium,once reperfused, may go through a phase of stunning before normal contractile function is restored (29).
According to the role of calcium in stunning, it has been suggested that calcium overload may play a crucial role and therefore calcium antagonists could have a beneficial effect on recovery of myocardial stunning (17,21,25). By contrast, in hibernation, where there is an ongoing reduction in the contractile function of the myocardium, calcium antagonists may further depress the inotropic state (25). The hibernating myocardium can only recover after successful revascularization either by coronary bypass surgery or by percutaneous transluminal coronary angioplasty (7).


Clinical and Biochemical Evidence
for Hibernating Myocardium

What is the clinical evidence that supports the concept of hibernating myocardium? Several studies have shown that persistent left ventricular wall-motion abnormalities in patients with chronic angina were reversed to normal by successful coronary artery bypass surgery (7,14). Rankin et al. (30) observed an improvement in regional wall-motion abnormalities in 34% of patients, with an increase in global left ventricular ejection fraction from 53% to 71% at 7-14 days after surgery. Breisblatt et al. (6) documented a case of reversal of a longstanding ventricular aneurysm following coronary revascularization supporting the concept that chronically ischemic (hibernating) myocardium could actually mimic an infarction. Topol et al. (35) reported the immediate improvement in dysfunctional myocardial segments after coronary revascularization.
Regions of myocardium supplied by severely diseased coronary arteries may develop chronic ischemia at rest and exhibit reduced contractility, contributing to a reduction in global left ventricular function. These regions of asynergy described as hibernating myocardium, in which normal contractility may be restored, often coexist with areas of either infarcted or scar tissue, supporting the hypothesis of jeopardized but viable myocardium (7,9,30). Chatterjee et al. reported that up to 66% of myocardial segments with wall-motion abnormalities showed improvement or a return to normal after bypass surgery. Improvement also occured in 29% of myocardial regions with prior infarction, implying the coexistence of scar and viable myocardium in the same territory (14).
Recently some authors have suggested that anaerobic or minimal but relevant preservation of oxidative metabolism may generate enough ATP to sustain tissue viability (22,23). To maintain these metabolic conditions it is necessary for the regional coronary blood flow to remain between 20-40% of normal (33).
The data obtained suggest that progressive decline of oxygen supply leads to cellular hypoxia. Anaerobiosis accelerates the transport and utilization of exogeneous glucose as well as the breakdown of glycogen stores. Products of anaerobic glycolysis, namely protons, reduced coenzymens and lactic acid, can feed back to inhibit glycolysis at various levels (12). The inhibitory effect of acidosis is one factor explaining the difference between the effect of acute, severe ischemia, which inhibits glycolysis, and chronic, mild ischemia, which accelerates it. These differences are reflected in the increased glucose uptake of the mildly ischemic (hibernating) heart versus decreased glucose uptake of the severely ischemic heart. Hypoperfused (hibernating) myocardium retains its responsiveness to an inotropic agent that also suggests that some dysfunctional myocardium has maintained the ability to contract (8,36).
However, several key issues remain to be resolved. First, the length of time the ischemic myocardium can maintain its metabolic integrity and responsiveness to an inotropic challenge is not known. It is possible that the metabolic status deteriorates again over time and the responsiveness is eventually lost. In this scenario, the early lost of contractile function during low-flow ischemia is only a temporary mechanism to prolong myocardial viability but is inherently time limited (16). On the other hand, it is possible that the myocardium can maintain such a state indefinitely. Second, it may be postulated that the ability of the myocardium to adjust to the ischemia is related to the absolute level of the ischemia present. Total ischemia, as studied experimentally or as observed during coronary thrombosis or vasospasm in a patient without substantial collateral vessels, is well known to produce cell death within approximately 20 minutes, starting in the inner wall and progressing transmurally acros the wall over time, the so-called "wave front" of infarct formation (37). Whether there is a minimal flow requirement permitting hibernation is still not known.


Clinical Detection of Hibernating Myocardium

The differentiation of viable from nonviable myocardium in patients with coronary artery disease and left ventricular dysfunction is a key issue in the current era of myocardial revascularization (26). Reperfusion of viable, hibernating myocardium causes a recovery of mechanical function of the left ventricle that correlates with improvement in survival (5,7). This is in agreement with the current understanding of left ventricular function as a critically important determinant of long-term prognosis in patients with coronary artery disease.
In order to fulfill the working hypothesis of Rahimtoola that hibernation is "a state of myocardial hypocontractility during chronic hypoperfusion, in the presence of completely viable myocardium which recovers functionally upon revascularization" (27) - three major criteria should be present, i.e.:

  1. chronic wall motion abnormalities
  2. presence of chronic hypoperfusion
  3. evidence for functional recovery after reperfusion
For clinical decision making, reliable diagnostic tools are required to distinguish between hibernating myocardium and scar tissue. In general, the distinction can be made by:
  1. functional testing - such tests include unloading of the heart with nitroglycerin, catecholamine stimulation or postextrasystolic potentiation
  2. demonstration of residual perfusion and metabolism - such tests include radionuclide ventriculography, positron-emission tomography (PET) etc.
It has been shown that both the two-dimensional echocardiography during infusion of inotropic agent (e.g. dobutamine 5-10 mcg/kg/min.) and the radionuclide detection can be considered as routine and practical diagnostic tools for identification of patients with chronic ventricular dysfunction likely to benefit from revascularization (24,28). Although some studies have underlined the fact that conventional myocardial scintigraphy with thallium-201 may underestimate viability compared to metabolic imaging with positron emission tomography, it is quite clear that this diagnostic tool still remains highly accurate in prediction of the early recovery of contractility upon revascularization (32). For example, low dose dobutamine echocardiography predicts the early improvement after coronary artery revascularization with 86% of sensitivity and 82% of specificity (18). Myocardial scintigraphy can predict the improvement after successful revascularization with 92% of sensitivity and 85% of specificity (22). Although PET is the best nonivasive method for quantifying regional myocardial blood flow and metabolism it cannot be used as a routine diagnostic technique because it is available only in a few centers.
From the surgical point of view, the recommendation for a revascularization procedure in the high-risk patient with severe left ventricular dysfunction, is dependent on a number of considerations. These are:
  1. presence of one or more coronary arteries related to the hibernating zone with anatomy suitable for bypass grafting
  2. demonstration of viable myocardium by one or more of the possible imaging modalities
  3. extension of the underperfused but viable myocardium demonstrating contractile reserve of hibernating myocardium
  4. symptomatic status of the patient, including symptoms of myocardial ischemia or congestive heart failure.
Thus, it appears quite clear that decision making in surgical treatment of patients with coronary artery disease and left ventricular dysfunction is dependent on a number of factors, of which myocardial viabilty is the most important one. This topic, however, will be the source of interesting and exciting results over the next few years and revascularization of hibernating myocardium could be considered, at least in some severely sick patients, as an alternative to cardiac transplantation (29).


Conclusion

Hibernating myocardium refers to the presence of persistent myocardial and left ventricular dysfunction at rest, associated with conditions of severely reduced coronary blood flow. Hibernation is thought to occur as a response to a chronic reduction in resting coronary blood flow, leading to a new equilibrium where myocardial metabolism is altered with a subsequent reduction in energy production and myocardial contractility.
The identification of hibernating but still viable myocardium in regions of left ventricular dysfunction is an increasingly relevant issue in the management of patients with severe coronary artery disease and left ventricular dysfunction.
Revascularization of hibernating myocardium should lead to the greatest improvement in left ventricular function and, thus, improvement in survival.


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Submitted July 1996.
Accepted September 1996.

MUDr. Jan Knap,
Hradecka 1124, 500 02 Hradec Kralove 2,
Czech Republic.