Medstudents Cardiovascular Physiology

Hibernating and Stunned Myocardium

Author: Glauber Gouvea

Fifth Year Medical Student - The Federal University of Rio de Janeiro




Introduction

Myocardial blood flow (MBF), oxygen consumption (MVO2) and contractile function are tightly linked. These parameters are very important in cardiac physiology. One can think that, in normal healthy individuals, there should be optimal MBF, at any time, therefore matching myocardial demand to provide optimal function, or contractility. Coronary artery disease (CAD) has a variety of clinical presentations, ranging from stable angina to sudden death. The three parameters above are almost invariably changed in CAD: if MBF is not adequade, contractility may not be optimal, which is expressed clinically as regional or segmental ventricular dysfunction. Indeed, ischemia can produce various degrees of myocardial dysfunction, and if severe and prolonged, leads to necrosis. The other two consequences of isquemia will be discussed.

Historical Perspectives

Until the early 80's, regional dysfunction were equated by almost every cardiologist to irreversible injuried tissue (3). Diamond et al was the first to use the term "hibernating" supposing that some of these areas could improve after revascularisation. Rahimtoola (3), Braunwald and Rutherford popularized the terms hibernating and stunned, in mid 80's. There were more acceptance at that time, presumaly because of the concept of silent isquemia was getting more interest.

Defining Terms

Hibernating myocardium (HM) must be differentited by stunning, although both processes may coexist on clinical grounds (7), and in some instances, it is difficult to say which of them predominates in a individual patient (3).

a) Hibernating - can be defined as wall abnormalities (hypo, aki, dyskinetic segments) present in the setting of chronic isquemia, which are potentially reversible after revascularisation. This is actually a proof that they were not "dead", therefore representing viable myocardium. There is a new steady state between MBF and function, in other words, these two parameters are matched: MBF reduced, then function is reduced too (4). The clinical scenario where HM may be present is, eg., chronic stable angina (8) and unstable angina (possibly because of the silent ischemia) (3).

b) Stunned - Acute isquemia (eg., major coronary occlusion) can lead to stunning (segmental dysfunction) which is persistent for a variable period of time, up to two weeks, even after isquemia has been relieved. There is here a mismatched situation, in which MBF is normal, but function is depressed. (If isquemia lasts longer than 20 minutes, subendocardial necrosis usually begins.)4. The clinical scenario is, eg., acute myocardial infarction (AMI) (1,3,4) and during percutaneous transluminal coronary angioplasty (PTCA) or cardiac surgery (1,3,8)

Tissue Heterogenicity

If we take a sample of myocardial tissue in patients with CAD, we can found various degrees of myocardial injury on hystological examination, as necrosis, hibernating myocytes, stunned myocytes and why not, completely normal myocytes. This heterogenicity (1,7) is a important concept and should be kept in mind.

Evidences

Several animal studies (5) have been trying to create a model of hybernation, although it is quite difficult (1,2,4,6). Many studies in humans come from coronary artery bypass surgery (CABG) showing improvment of regional dysfunction after surgery. One study showed that 7% of akinetic segments and 52% of dyskinetic segments, seen at ventriculography, were composed by viable tissue, as visualized at autopsy (3). Rahimtoola (3) proposed that patients with significant coronary occlusion (>70%), filled with collaterals, with correspondent dysfunctional segments and with no q waves in the ECG would have a great chance to contain hibernating tissue , altough some argue that no clinical and images datas are efficient to determine hibernation.(7)

Regional Flow

If one cerefully read the text, could expect that the heart is smart: as coronary flow is reduced, myocardium downgrades its function, diminishing MVO2 and preventing cell death. Although this smart heart hypothesisis is exciting there is convincing evidence that regional flow to hibernating myocytes are not reduced at rest, as well as oxygen consumption. Vanoverschelde et al (1,2) studied 26 patients with clinical evidence of hibernating myocardium as proposed initially by Rahimtoola. None of them had evidence of previous AMI (therefore, minimized tissue heterogenicity). Regional flow at rest, measured by Positron emission tomography (PET), was found to be normal in patients with and without regional dysfunction. However, flow reserve to these areas were severely blunted when exposed to hyperemic agent (as adenosine). Marinho et al, using radioactive water, showed that 80-90% of the supposed hybernating segments had normal basal flow.(1)

Hibernating Phenotype

Stunned cells do not show major structural abnormalities, except some small vacuoles near mitochondria, and the crists of the latter showed more tortuos on electronic microscope (1). However, hibernating cells do show major structural abnormalities (1). Flameng et al was the pioneer in the study of these cells (1) . He made transmural biopsy of dysfunctional segments representative of hibernating muscle during CABG and described the morphology. Posterior studies confirmed the first one. Below, some of these alterations:

a) Irregular nucleus with altered chromatin
b) High concentration of PAS+ granules, consistent with glycogen.
c) Loss of contractile material
d) Lack of smooth sarcoplasmic reticulum and T tubules
e) Altered mithochondria but with normal function (ADP/ATP ratio)

This normal ATP pool is consistent with the previously suggested theory that MVO2 is unaltered in these cells.

The myocardial cells normally oxidizes more fatty acids (80%) (7). In hibernating cells, there is increased uptake in glucose (1,2,8), which was comproved by studies with PET and fluordeoxyglucose and by the presence of glycogen on these cells. Glucose membrane transporters may be increased in number (GLUT1,GLUT4), possibly by increased gene expression of these transporters (1). Another explanation is that glycogen synthase may be actived more avidly in the setting of ischemia (1). Some of the alterations in the hibernating phenotype is quite, though not completely, similar to the fetal cardiomyocytes. This process have been called partial deddiferentiation (1).

Pathophysiology

Stunning probably is related to altered calcium homeostasis, and oxygen free radicals may also play a role in the development of stunned cells. (1,6,8). In contrast, many theories have been proposed to explain HM: if bloof flow to these areas are not reduced at rest (2,9), these segments are not ischemic. If one read above the definition of HM, could become confused. Indeed, much is argued but little is truth about the mecanisms that lead to the hibernating phenotype. Some of the numerous hypotheses are listed below:

a) Repeated stunning - Acute ischemic episodes, as said above, can lead to stunning. If this event occurs several times over a long period, could indeed lead to hibernation.
b) Ischemic preconditioning - It is hypothesized that cardiac cells have a mechanism of self-protect from repetitive ischemia, increasing their threshold for ischemic damage. This mechanism could have a role in the genesis of hibernation.
c) Gene expression - Ischemia can induce altered expression of some gens that could change cell phenotype.
d) Apoptosis - Although there is no documented morphology evidence of cell apoptosis, some argue that byochemical signals of apoptosis may be present in hibernation.
e) Mechanical alterations - Isquemia per se may lead to physical damage, which can lead to structural changes in cardiac cells.

Myocyte phenotype very similar to the HM one has been found in fibrillating atria cells, in goat but also in humans, suggesting that ischemia may not be a mandatory nor necessary factor to generate HM. (1)

Detecting HM

The golden standard to detect viable tissue is PET (7). Stress echo with dobutamine and scintilography are currently used. Contrast echocardiogram, with microbubbles, is a recent and promising technique.(7) The stress echo is based on the contractile reserve of these viable cells, although HM, because of the loss of the contractile material, may not respond so well as the stunned one (1). Some authors have postulated that up to 25% of hibernating myocardium do not respond to any doses of dobutamine.

Clinical Implications

The usefullness to detect HM comes from the logical point that revascularization should be attempted to reperfuse predominantly viable myocardium, not "dead" tissue. However, the patients may have to be carefully selected to gain beneficits of this exams. One of the most important prognostic factor in patients with CAD is left ventricular ejection fraction (LVEF), which is the most used clinical parameter of global ventricle function. Although improvement of regional dysfunction (hibernating segments) may perhaps be associated with better outcome, there is no clearly documented effect on mortality. Indeed, it is supposed that at least three (possibly two) segments may have to improve, to LVEF raises significantly (3,7). Patients with congestive heart failure and depressed LVEF<30%, would be a good candidate to detect viable tissue (7). In contrast, most patients with good left ventricular function that will be submitted to revascularisation will not beneficit so much from the exam (7). If a revascularization is being attempted in a patient with recent AMI in which the reperfusion criteria were not fully matched, the search for viable tissue would be of major interest. Finally, there is increasing body of evidence that the presence of HM should not be faced as a successfull adaptation, but indeed, a suffering myocardium who is avid for revascularization and restore its normal function. (7)

Bibliography

1. Vanoverschelde JLJ et al. Chronic myocardial hibernation in humans: from bedside to bench. Circulation 1997; 95:1961-71
2. Vanoverschelde JLJ et al. Mecanism of chronic regional postischemic dysfunction in humans. New insights from the study of noninfarcted collateral dependent myocardium. Circulation 1993: 87(5)
3. Rahimtoola SH. The hibernating myocardium. Am Heart J 1989:117(1):211-19
4. Kloner RA et al. Altered myocardial states: the stunned and hybernating myocardium. AmJMed 1989;86(SupIA):14-21
5. Bolukoglu H et al. Na animal model of chronic coronary stenosis resulting in hibernating myocardium. Am Phy Soc 1992; H20-H28
6. Ferrari R et al. Metabolic disturbances during myocardial ischemia and reperfusion. The Am J Cardiol 1995;76:17B-24B
7. Iskandrian AS et al. Myocardial viability: methods of assessment and clinical relevance. Am Heart J 1996;132:1226-35
8. Vroom MB, van Wezel HB. Myocardial stunning, hibernation, and ischemic preconditioning. Journal of Cardiothoracic and Vascular Anesthesia 1996;10(6):789-99
9. Uren NG et al. Relation between myocardial blood flow and the severity of coronary artery stenosis. NEJM 1994;330(25):1782


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