Ventricular Fibrillation durinp: Cardiopulmonary B ass: Lo&Term Effects on Myocardial Morp yfl ology and Function
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1 Ventricular Fibrillation durinp: Cardiopulmonary B ass: Lo&Term Effects on Myocardial Morp yfl ology and Function Wolfgang Schraut, M.D., John J. Lamberti, M.D., Ken Kampman, M.D., and Seymour Glagov, M.D. With the Technical Assistance of Marilyn Robertson, B.S. ABSTRACT Mongrel dogs were subjected to hypothermic (28" to 30 C) cardiopulmonary bypass with hemodilution by 50%. In two groups of 8 dogs each, ventricular fibrillation was induced for 60 and 90 minutes, respectively, while the dogs were on bypass. A group of 6 dogs with the heart beating but nonworking served as control. Seven weeks after operation, hernodynamic measurements were made in the sumvors (6 in each group) and the heart was fixed by perfusion with glutaraldehyde. Multiple transmural samples were taken from both vent+ cles. Light microscopy revealed solitary left ventricular scars (0.5 to 3 mm wide) in 2 hearts each from Groups 2 and 3. None of the hearts exhibited diffuse subendocardial fibrosis indicative of healed ischemic injury. All animals were hernodynamically normal. We conclude that in the nonhypertrophied heart, ventricular fibrillation up to 90 minutes with continuous bypass-sustained coronary perfusion (perfusion pressure at or above 70 mm Hg) offers protection from permanent myocardial injury. Ventricular fibrillation is an attractive method of cardiac arrest during cardiopulmonary bypass (CPB) since it offers a quiet operative field with apparent myocardial protection due to continuous coronary perfusion with oxygenated blood. Extensive experimental evaluation of ventricular fibrillation during CPB has been From the Departments of Surgery and Pathology, The University of Chicago, Pritzker School of Medicine, Chicago, IL. Supported by the Louis L. Block Fund of The University of Chicago, Grant HL17648 from the National Heart, Lung, and Blood Institute, Chicago Heart Association Grants A75-11 and C76-5, and American Heart Association Grant Accepted for publication Aug 28, Address reprint requests to Dr. Schraut, The University of Chicago Hospitals and Clinics, 950 E 59th St, Chicago, IL performed in the nonhypertrophied canine heart. Many immediate and postoperative detrimental effects have been reported, such as increased myocardial consumption of oxygen [8, 91, relative underperfusion of the subendocardial myocardium [9, 151, metabolic derangement with increased myocardial production of lactate [81, and release of myocardial enzymes [lo]. All are suggestive of imbalance between myocardial oxygen supply and demand. Other experimental studies did not confirm these harmful effects [I, 5,141, and clinical experience with induced ventricular fibrillation during heart operations has been favorable in general [13, 161. We designed the present study to determine if the potentially detrimental effects of ventricular fibrillation during CPB result in permanent injury to the myocardium. Materials and Methods Twenty-two dogs weighing 18 to 22 kg were placed on hypothermic (28" to 30 C) cardiopulmonary bypass (CPB) and divided into three groups based on the experimental intervention used at bypass. Group 1 (6 dogs) served as control. The heart remained beating but nonworking (left ventricular vent) with anatomical coronary perfusion through the aortic root for 60 minutes. In Group 2 (8 dogs) ventricular fibrillation was induced after placing the left ventricular vent. Coronary perfusion again was bypass-sustained during the experimental interval of 60 minutes. In Group 3 (8 dogs), the experimental interval with ventricular fibrillation was extended to 90 minutes under the same conditions as in Group 2. The dogs were anesthetized with sodium pentobarbitol (20 mg per kilogram of body weight) and maintained on ventilatory support. Electrocardiogram, central venous pressure, by Wolfgang Schraut
2 231 Schraut et al: Ventricular Fibrillation during CPB femoral artery pressure, and rectal temperature were monitored and recorded continuously. Through a right lateral thoracotomy the pericardial sac was opened longitudinally. Following systemic heparinization (2.5 mg per kilogram), the right atrium and femoral artery were cannulated. Bypass was maintained with a pediatric-sized bubble oxygenator with an integral heat exchanger (Bentley Laboratories), primed with 500 ml of fresh nonmatched dog blood, 1,000 ml of balanced electrolyte solution, and 12.5 gm of mannitol. Immediately after bypass was begun, a left ventricular vent was inserted through an apical stab incision. In Groups 2 and 3, ventricular fibrillation was induced by a brief episode of alternating current. Fibrillation was then allowed to continue spontaneously for 60 and 90 minutes, respectively. During CPB, blood temperature was maintained at 28" to 30 C. Bypass flow ranged from 70 to 100 ml per minute per kilogram to maintain perfusion pressure at or above 70 mm Hg. Once the experimental time interval had passed, rewarming was begun, and within 3 to 4 minutes blood temperature rose to 36 C allowing defibrillation. Total CPB was continued for another 15 minutes. After the left ventricular vent had been removed, the animal was weaned from bypass, heparin was reversed with protamine sulfate, and the thorax was closed anatomically. Within 4 hours, ventilatory support was discontinued. No cardiotonic drugs were administered during test and recovery periods. Preparation and Examination of the Hearts Before the dogs were killed, 45 to 50 days after the operation, the following hemodynamic variables were measured through a left thoracotomy: cardiac output, left ventricular pressure, left atrial pressure, central venous pressure, aortic pressure, heart rate, and maximal rate of rise of left ventricular pressure (LV dpldt max). After the aortic arch was cannulated, the heart was fibrillated and the coronary vasculature flushed with lactated Ringer's solution, immediately followed by controlled pressure (100 mm Hg) perfusion fixation with isotonic 2% glutaraldehyde for 30 minutes. The hearts were then excised and opened, and the endocardium was inspected for evidence of myocardial injury. Transmural ventricular samples were taken from five anatomically defined locations: the anterior and posterior papillary muscles (including the subjacent ventricular wall), the midseptum, the lateral left ventricular free wall, and the right ventricular free wall (at the obtuse and acute margin, both midway between the coronary sulcus and apex). The samples were embedded in paraffin, and multiple sections, stained with hematoxylin and eosin or two connective tissue stains (Weigertvan Gieson and Gomori-trichrome with aldehyde fuchsin), were studied for myocardial fibrosis and scarring. Whenever such lesions were found in a sample, additional samples and sections from the heart were inspected. Results Survival All animals in Group 1 (nonworking heart) survived and were killed 45 to 50 days later. Six of the 8 dogs in both Group 2 (60 minutes of ventricular fibrillation) and Group 3 (90 minutes of ventricular fibrillation) survived. Three dogs died six to seven hours after CPB of hypoxia due to edema and hemorrhage in either the left lung (1 animal) or both lungs (2 animals). The other dog died of multiple rhythm disturbances. Hemorrhage of unexplained cause was found in the area of the atrioventricular node at postmortem examination. Hemodynamic Studies Hemodynamic data obtained before death are summarized in the Table. No statistical difference was found among the groups. The numerical values of LV dpldt max calculated from measurements made before death correspond well to those values considered normal for mongrel dogs by other investigators. Myocardial Morphology Macroscopic inspection revealed normal endocardium free from fibrosis and cut myocardial surfaces without gross scars. Light microscopic study demonstrated normal myocardium and endocardium in all hearts of the control group. Equally unremarkable were 4 of the 6 hearts in Group 2. Three samples from the left
3 232 The Annals of Thoracic Surgery Vol 27 No 3 March 1979 Hemodynarnic Data as Mean Values within Each Group (Range of Observed Values in Parentheses) No. of Dogs HR LVP LVEDP co LV dpldt max Group Studied (beatslmin) (mm Hg) (mm Hg) (Llmin) (mm Hglsec) Group ,600 (Control) ( ) ( ) (0-10) ( ) (1,800-3,320) Group ,460 (VF 60 min) ( ) ( ) (2-8) ( ) (1,880-3,280) Group ,900 (VF 90 min) ( ) ( ) (0-5) ( ) (1,800-3,760) HR = heart rate; LW = peak left ventricular pressure; LVEDP = left ventricular end-diastolic pressure; C 3 = cardiac output; LV dpldt max = maximal rate of rise of left ventricular pressure; VF = ventricular fibrillation. ventricle of 1 of the remaining hearts exhibited a solitary, minute, subendocardial scar (0.5 mm wide). The anterior papillary muscle of the sixth heart showed a solitary scar smaller than 0.5 mm in diameter. Additional samples and sections were unremarkable. All samples from 4 hearts of Group 3 dogs were free from lesions suggestive of healed myocardial injury. A single linear subendocardial scar (1 mm wide) was found in a section through the anterior papillary muscle of 1 animal. The other heart revealed evidence of left ventricular ischemic injury in sections from anterior papillary muscle (solitary scar, 2 x 3 mm), posterior papillary muscle (area of subendocardial fibrosis, 1.5 x 3 mm), and free left ventricular wall (two scars, 0.5 mm wide). This animal sustained a 15-minute hypotensive episode (blood pressure, 50 mm Hg) during bypass. Additional samples taken from these animals revealed normal myocardial morphology. Comment Clinical experience utilizing ventricular fibrillation during open-heart procedures, especially coronary artery bypass operations, is extensive and the results have been favorable in general [13, 161. Griepp and co-workers [7], however, found an increased postoperative infarction rate following aortocoronary revascularization procedures employing ventricular fibrillation. Najafi and associates [ll] reported a series of patients who died of left ventricular hemorrhagic subendocardial necrosis following open-heart operation. Prolonged ventricular fibrillation was identified as the causal factor. This report in particular led to extensive reevaluation of ventricular fibrillation as a method of elective cardiac arrest with associated myocardial protection by coronary perfusion. Acute experimental studies on the normal canine heart by Baird [ll, Cox [51, Proctor [121, and their colleagues corroborate the reports of favorable clinical experience. No differences in measurable indices of acute ischemic or hypoxic myocardial injury (lactate production, enzyme release, myocardial adenosine triphosphate content, oxygen consumption, regional blood flow, or contractility) could be found between the fibrillating and the beating nonworking heart. In seeming contradiction are multiple reports by Buckberg [3, 41, Brazier [21, Hottenrott [91, and their associates who found that subendocardial blood flow during ventricular fibrillation was notably reduced, if not inadequate. Buckberg and co-workers [3, 41 thought that the detrimental effects of ventricular fibrillation (in the nonhypertrophied canine heart) could be averted if the perfusion pressure was maintained at 100 mm Hg, if the left ventricle remained decompressed by a vent, if hemodilution and moderate hypothermia (32 C) were avoided, and if ventricular fibrillation was limited to 60 minutes. All of these experiments were performed acutely and none of the derangements noted were shown to be irreversible. In clinical practice, hypothermia, hemodilution, and perfusion pressures of less than 100 mg Hg are frequently employed with ventricular fibrillation during cardiac operations. If the
4 233 Schraut et al: Ventricular Fibrillation during CPB abnormalities of metabolism, ventricular function, and regional myocardial blood flow detected by Buckberg [3, 41, Grover [8], and their colleagues are significant, permanent but sublethal impairment of the myocardium, i.e., myocardial fibrosis, might occur. Such an injury pattern might not be detected by survival statistics but only by late systematic histological examination of the myocardium. Our experimental model was designed to simulate clinical techniques, although the procedures were carried out in healthy dogs. This may limit the relevance of our findings in terms of clinical practice. Commonly used bypass techniques were applied. Perfusion pressure was maintained at about 70 mm Hg; bypass flow ranged from 70 to 100 ml per kilogram per minute; and hypothermia to 30 C with hemodilution was utilized. Although these techniques do not necessarily avoid temporary myocardial impairment and damage, we found that under these experimental conditions ventricular fibrillation with coronary perfusion for 60 to 90 minutes is not followed by permanent myocardial injury. This suggests that within our experimental setting, myocardial oxygen supply and demand were balanced. The conclusions of our study are based on thorough histological examination of the heart as advocated by Ferrans [6] and were made possible by the method of preparation. Perfusion at physiological pressures with isomolar glutaraldehyde renders the heart fixed in near-diastolic configuration, which allows easy identification of anatomical landmarks for transmural sampling. In particular, thorough study of the papillary muscles, the preferential site of ischemic damage, was undertaken. Evidence of diffuse subendocardial fibrosis could not be found in any heart. The scattered, isolated microscopic scars detected in 4 of the hearts subjected to ventricular fibrillation may be a result of the fibrillation. It is possible, however, that these lesions predated the experimental study or were a result of embolic phenomena during or after CPB. In the absence of demonstrable anatomical injury, i.e., diffuse myocardial scarring, hemodynamic measurements within the normal range were expected. In fact, cardiac performance as expressed by heart rate, cardiac output, blood pressure, and LV dpldt max before death correlated with the histological findings of normalcy. Comparing the groups of dogs undergoing ventricular fibrillation with the control group in respect to hemodynamic performance (LV dpldt max) did not demonstrate a significant difference, probably because of the wide variation in observed values. None of the dogs that underwent CPB and ventricular fibrillation and that died in the early postoperative period showed evidence of subendocardia1 hemorrhage or necrosis. It could be argued that this subset of animals would have exhibited long-term evidence of myocardial injury if survival had occurred. If a spectrum of injury occurs with the use of ventricular fibrillation during CPB, survivors would have been expected to show a range of myocardial scarring. Since no survivor, except possibly 1 animal that underwent 90 minutes of ventricular fibrillation showed any marked morphological impairment, we conclude that any functional derangement associated with 60 or 90 minutes of ventricular fibrillation during CPB is potentially completely reversible. References 1. Baird RJ, Dutka F, Okumori M, et al: Surgical aspects of regional myocardial blood flow and myocardial pressure. J Thorac Cardiovasc Surg 69:17, Brazier JR, Cooper N, McConnell DH, et al: Studies of the effects of hypothermia on regional myocardial blood flow and metabolism during cardiopulmonary bypass: 111. Effects of temperature, time, and perfusion pressure in fibrillating hearts. J Thorac Cardiovasc Surg 73:102, Buckberg GD, Brazier JR, Nelson RL, et al: Studies of the effects of hypothermia on regional myocardial blood flow and metabolism during cardiopulmonary bypass: I. The adequately perfused beating, fibrillating, and arrested heart. J Thorac Cardiovasc Surg 7337, Buckberg GD, Hottenrott CE: Ventricular fibrillation: its effect on myocardial flow, distribution, and performance. Ann Thorac Surg 20:76, Cox JL, Anderson RW, Pass HI, et al: The safety of induced ventricular fibrillation during cardiopulmonary bypass in nonhypertrophied hearts. J Thorac Cardiovasc Surg 74:423, Ferrans VJ: Morphological methods for evaluation of myocardial protection. Ann Thorac Surg 20:11, 1975
5 234 The Annals of Thoracic Surgery Vol 27 No 3 March Griepp RB, Stinson EB, Oyer PE, et al: The superiority of aortic cross-clamping with profound local hypothermia for myocardial protection during aorto-coronary bypass grafting. J Thorac Cardiovasc Surg 7095, Grover FL, Fewel JG, Ghidoni JJ, et al: Effects of ventricular fibrillation on coronary blood flow and myocardial metabolism. J Thorac Cardiovasc Surg 73:616, Hottenrott C, Maloney JV, Buckberg G: Studies of the effects of ventricular fibrillation on the adequacy of regional myocardial flow. J Thorac Cardiovasc Surg 68:615, Isom OW, Kutin ND, Falk EA, et al: Patterns of myocardial metabolism during cardiopulmonary bypass and coronary perfusion. J Thorac Cardiovasc Surg 66:705, Najafi H, Henson D, Dye WS, et al: Left ventricular hemorrhagic necrosis. Ann Thorac Surg 7:550, Proctor E, Parker R: Total circulatory support by peripheral cannulation and pump oxygenation during 8 hours of ventricular fibrillation in the dog. J Thorac Cardiovasc Surg 57:702, Race D, Stirling GR, Moms KN: Induced ventricular fibrillation in open heart surgery. J Thorac Cardiovasc Surg 47:271, Reis RL, Cohn LH, Morrow AG: Effects of induced ventricular fibrillation on ventricular performance and cardiac metabolism. Circulation 36:Suppl 1:234, Reuben CF, Singh HM, Tector AJ, et al: The dynamics of subendocardial flow during cardiopulmonary bypass. J Thorac Cardiovasc Surg 70:989, Wilson HE, Dalton ML, Kiphart RJ, et al: Increased safety of aorto-coronary artery bypass surgery with induced ventricular fibrillation to avoid anoxia. J Thorac Cardiovasc Surg 64:193, 1972
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