Departments of Surgery (Neurosurgery), Medicine (Cardiology), and Anesthesiology, Duke University Medical Center, Durham, North Carolina
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1 J Neurosurg 98: , 2003 Use of the peak troponin value to differentiate myocardial infarction from reversible neurogenic left ventricular dysfunction associated with aneurysmal subarachnoid hemorrhage KETAN R. BULSARA, M.D., MATTHEW J. MCGIRT, B.S., LAWRENCE LIAO, M.D., ALAN T. VILLAVICENCIO, M.D., CECIL BOREL, M.D., MICHAEL J. ALEXANDER, M.D., AND ALLAN H. FRIEDMAN, M.D. Departments of Surgery (Neurosurgery), Medicine (Cardiology), and Anesthesiology, Duke University Medical Center, Durham, North Carolina Object. Differentiating myocardial infarction (MI) from reversible neurogenic left ventricular dysfunction (stunned myocardium [SM]) associated with aneurysmal subarachnoid hemorrhage (SAH) is critical for early surgical intervention. The authors hypothesized that the cardiac troponin (ctn) trend and/or echocardiogram could be used to differentiate between the two entities. Methods. A retrospective study was conducted for the period between 1995 and All patients included in the study met the following criteria: 1) no history of cardiac problems; 2) new onset of abnormal cardiac function (ejection fraction [EF] 40% on echocardiograms); 3) serial cardiac markers (ctn and creatine kinase MB isoform [CK-MB]); 4) surgical intervention for their aneurysm; and 5) cardiac output monitoring either by repeated echocardiograms or invasive hemodynamic monitoring during the first 4 days post-sah when the patients were euvolemic. Of the 350 patients with SAH, 10 (2.9%) had severe cardiac dysfunction. Of those 10, six were women and four were men. The patients mean age was 53.5 years (range years) and their SAH was classified as Hunt and Hess Grade III or IV. Aneurysm distribution was as follows: basilar artery tip (four); anterior communicating artery (two); middle cerebral artery (one); posterior communicating artery (two); and posterior inferior cerebellar artery (one). The mean EF at onset was 33%. The changes on echocardiograms in these patients did not match the findings on electrocardiograms (EKGs). Within 4.5 days, dramatic improvement was seen in cardiac output (from L/minute to L/minute). Compared with historical controls in whom there were similar levels of left ventricular dysfunction after MI, there was no difference in peak CK-MB. A 10-fold difference, however, was noted in ctn values ( ng/ml; control 2.8 ng/ml; p 0.001). Conclusions. The authors determined the following: 1) that the CK-MB trend does not allow differentiation between SM and MI; 2) that echocardiograms revealing significant inconsistencies with EKGs are indicative of SM; and 3) that ctn values less than 2.8 ng/ml in patients with EFs less than 40% are consistent with SM. KEY WORDS aneurysm cardiac function subarachnoid hemorrhage troponin I N 1938, Aschenbrenner and Bodechtel 2 reported that intracranial lesions may result in abnormalities on EKGs. The frequent association of these abnormalities with SAH was described as early as Transient cardiac abnormalities are now a well-recognized phenomenon that occurs in a large percentage of patients with acute aneurysmal SAH. 8,16,46,47,55 57 Prospective studies show a high frequency of abnormalities on EKGs among patients with SAH; 23,44 it has been estimated that 50 to 72% of these patients have EKG abnormalities. 35,41 Changes seen on EKGs commonly include depression or Abbreviations used in this paper: CK-MB = creatine kinase MB isoform; ctn = cardiac troponin; EF = ejection fraction; EKG = electrocardiogram; ICU = intensive care unit; MI = myocardial infarction; SAH = subarachnoid hemorrhage; SM = stunned myocardium. 524 elevation of ST segments, prolongation of Q T intervals, U waves, and T-wave inversions. 9,27 Furthermore, elevation of CK-MB levels, 22 left ventricular wall hy, and florid cardiac failure can also be seen. 19,46,52 These findings indicate myocardial ischemia, yet there is no evidence of coronary disease, coronary vasospasm, or cardiac hypoperfusion. 40,68 Furthermore, resolution of changes on EKGs occurs after clinical recovery from SAH. 5,24 The incidence of florid cardiac failure in patients with aneurysmal SAH is not known, which poses a significant clinical dilemma. Differentiating MI from reversible neurogenic left ventricular dysfunction (SM) associated with aneurysmal SAH is critical for early surgical intervention. There is currently no reliable test that can be used to differentiate between the two entities. In recent years, considerable interest has been directed at ctn, a regulatory protein highly specific for cardiac mus-
2 Troponin values in stunned myocardium TABLE 1 Patient demographics, EKG changes, peak CK-MB and ctn levels, and changes in cardiac output in 10 patients with SM* Findings 24 Hrs From Admission Peak Level (ng/ml) Case Age (yrs), Aneurysm FU Rise in co No. Sex Location EKG EF ECHO EF (L/min) CK-MB ctn 1 43, F PICA lat leads 25% global hy 50% , M BA tip ant leads 30% lat wall hy ND 3 61, F ACoA inf leads 35% ant/inf wall hypoki- 45% ND nesis 4 36, F PCoA inf leads 35% ant/septal/apical hy ND 5 68, M BA tip lat leads 40% ant/septal/apical hy , F ACoA ant leads 15% global hy 55% , F PCoA normal EKG 40% global hy , M MCA lat leads 35% ant/septal/apical hy , M BA tip inf leads 35% lat wall hy , F BA tip lat leads 35% global hy * ACoA = anterior communicating artery; ant = anterior; BA = basilar artery; co = cardiac output; ECHO = echocardiogram; FU = follow up; inf = inferior; MCA = middle cerebral artery; ND = not done; PCoA = posterior communicating artery; PICA = posterior inferior cerebellar artery. Ejection fraction on echocardiogram. Measured with invasive cardiac monitoring. Readings showed T-wave inversion. cle. 11 Commercial assays are available for two specific isoforms: ctnt and ctni, both of which have comparable elevations in detecting acute MI. 53 A small amount of ctn is released after sublethal myocyte injury, but larger amounts may signal irreversible cell death and breakdown of the contractile apparatus. 6 The major advantage of ctn is its ability to detect, with high sensitivity and specificity, myocardial cell damage that is undetectable by conventional enzyme methods. 1 Outcomes in patients with SAH have improved with advances in neurosurgery and neurocritical care with an emphasis on early aneurysm clip placement or coil occlusion. 30 An impediment to early intervention is the difficulty involved in differentiating reversible SM from MI. 58 There is considerable confusion when assessing the cardiac risk associated with surgery in patients with SM. 54 There are currently no criteria to determine what level of ctn release signals irreversible injury. In this study, we evaluated the utility of assessing ctn levels to differentiate between SM and MI in patients with aneurysmal SAH. Establishing such criteria influences patient outcome by providing an objective measure to determine if early surgical intervention is feasible in patients with clinically significant left ventricular dysfunction. Inclusion Criteria Clinical Material and Methods The medical records of all patients with SAH who were admitted to our institution between 1995 and 2000 were retrospectively reviewed. The electrocardiographic tracings obtained in all patients with SAH admitted to the ICU during this period were reviewed. Patients were identified who demonstrated new-onset, transient cardiac dysfunction. Because of the retrospective nature of this study, new onset of abnormal cardiac function was based on patient history. Patients with a history of coronary artery disease, hypertension, renal disease, or arrhythmias were excluded. All patients included in the study met the following criteria: 1) no history of cardiac problems; 2) new onset of abnormal cardiac function (EF 40% on echocardiograms); 3) serial cardiac markers (CK-MB and ctni) obtained once per day; 4) surgical treatment of their aneurysms; and 5) cardiac monitoring either by repeated echocardiograms or invasive hemodynamic monitoring (recording the mean cardiac output for the day) during the first 4 days post-sah when patients were euvolemic. The trend in cardiac output has been found to be a more reliable indicator of improvement than the absolute value. 47 Patient Population Fifty patients in whom SAH was classified as Hunt and Hess 33 Grade V did not undergo surgery and were not included in this study. Three hundred fifty patients with SAH were treated surgically between 1995 and Of these, 10 (2.9%) had severe new-onset cardiac dysfunction (Table 1). This group consisted of six women and four men whose mean age was 53.5 years (range years). Subarachnoid hemorrhage in all patients was categorized as Hunt and Hess Grade III or IV. Aneurysm distribution was as follows: basilar artery tip (four patients), anterior communicating artery (two), middle cerebral artery (one), posterior communicating artery (two), and posterior inferior cerebellar artery (one). During the period being reviewed, several management parameters were standard for all patients with SAH admitted to our institution. Diagnostic cerebral angiography was performed during the first 24 hours after admission. Nimodipine, Dilantin, and gastrointestinal prophylaxis (H 2 blockers or proton pump inhibitors) were administered on the day of admission and were continued throughout the patient s 525
3 K. R. Bulsara, et al. stay in the ICU. Patients demonstrating acute changes in cardiac output on invasive hemodynamic monitoring underwent transthoracic echocardiography. All patients demonstrating cardiac dysfunction were kept euvolemic. Of these, three patients with severe SM demonstrated systemic cardiovascular instability and were treated with intravenously administered dopamine. All three patients were successfully weaned from the dopamine over a 5-day period as their cardiac output improved. Invasive hemodynamic monitoring was continued until patients were discharged from the ICU. Results The mean EF was 33%. Four patients had global hy, three had anterior/septal/apical hy, two had lateral wall hy, and one had anterior/inferior hy. The changes on echocardiograms obtained in these patients did not match the findings on EKGs that have been previously described in SAH-associated cardiac dysfunction (four with lateral T-wave inversion, two with anterior T-wave inversion, three with inferior T-wave inversion, and one with normal T-wave inversion; Table 1). 67 None of the patients had Q waves. Improvements in cardiac output and contractility were seen on invasive hemodynamic monitoring and follow-up echocardiograms, respectively. Within 4.5 days, a mean improvement in cardiac output of L/minute was seen (Table 1). Compared with historical controls of patients with MI, there was no difference in peak CK-MB (SM, ng/ml [10 patients]; MI control, 7.5 ng/ml). 32,43 Compared with historical controls with similar levels of left ventricular dysfunction after MI, a 10-fold difference was noted in peak ctn values (SM, ng/ml [seven patients]; MI control, 2.8 ng/ml) (p 0.001, Student t-test). 51 Resolution of EKG abnormalities paralleled a time frame for recovery of cardiac function. Two patients admitted with SAH (Hunt and Hess Grade IV), a history of coronary artery disease, and acute MI (defined by sustained echocardiographic dysfunction for 1 month) had ctn values greater than 2.8 ng/ml with Q waves present on EKG traces. All patients tolerated the anesthetic and craniotomy with no intraoperative or perioperative cardiopulmonary complications. Discussion Subarachnoid hemorrhage may lead to subendocardial ischemia and local areas of necrosis. 27,38,39 The presence of elevated levels of ctn is 100% sensitive and specific for cardiac injury, 6,11,51 and this substance is elevated in up to 20% of patients with aneurysmal SAH. 31,51 In this retrospective study, we have demonstrated that ctni can be used as an indicator of reversible SM in a select patient population. This has important implications regarding timing for surgical intervention after aneurysmal SAH. As has previously been reported, CK-MB/CK and EKG findings cannot be used reliably to differentiate MI from SM. 6,16 18,21,22,28,31,40, 41,44 46,58,59,61,63,64,66 68 Peak ctn values can occur within 12 hours after an acute MI, 12 with the plateau phase lasting up to 48 hours. 53 Radionuclide studies have demonstrated that the amount of ctnt release closely relates to infarct size. 62 Furthermore, ctnt elevation greater than 2.8 ng/ml reliably predicts a left ventricular EF of less than 40%, with a sensitivity of 100% and a specificity of 92.9%. 53 All patients included in this study had EFs less than 40%, yet only a one-tenth elevation of ctnt was seen. Early surgical intervention in these patients, accompanied by careful intraoperative hemodynamic monitoring, did not lead to worse outcomes, as has been associated with acute MI. 14,26 Based on our findings we propose the following criteria to differentiate acute MI from reversible SM associated with aneurysmal SAH: 1) no history of cardiac problems; 2) new onset of abnormal cardiac function (EF 40%); 3) cardiac wall motion abnormalities on echocardiogram that do not correlate with the coronary vascular distribution noted on EKGs; and 4) ctn values less than 2.8 ng/ml in patients with an EF less than 40%. The mechanism of cardiac dysfunction after aneurysmal SAH is not fully understood. Autopsy studies have demonstrated that SAH results in vascular damage to the hypothalamus. 20 Most studies implicate the hypothalamus as the primary center of dysfunction. 25,44 The affected regions influence the autonomic nervous system. 25 Stimulating the posterior hypothalamus and midbrain reticular formation results in EKG changes similar to those following SAH. 3,37,48 The assertion that cardiac alterations are mediated by catecholamine 35,60 is supported by the fact that disrupting the sympathetic chain at the cervical level stops the arrhythmias, whereas a vagotomy does not. These changes can be inhibited by catecholamine blocking agents. 15,50 Furthermore, myocardial catecholamine concentrations rise and fall rapidly after an intracranial catastrophe. 49 Catecholamine-mediated myocardial injury is believed to be multifactorial: tachycardia, coronary spasm and vasoconstriction, toxic effects on cardiac myocytes, and an increased intracellular concentration of calcium. 10,42 Myocardial hemorrhages confined to the subintimal tissues and superficial muscle layers of the left ventricle have been noted. 38 The histologically confirmed lesions in the myocardium are contraction band necrosis and myocytolysis. 7,34,36,65 Focal areas of myofibrillar and fuchsinophilic degeneration are also noted in the subendocardium of the left ventricle. 13,27,29 It has previously been demonstrated that more severe grades of SAH are associated with ctn elevations, and a ctn leak in this setting may be associated with myocardial dysfunction. 51 Ay, et al., 4 demonstrated that CK-MB but not ctn is elevated following stroke and they suggested that elevated CK-MB combined with normal levels of ctnt may not be a biological marker for myocytolysis. Elevations of CK-MB in patients with stroke may be noncardiac in origin and may underlie the CK-MB and ctnt trends observed after SAH. Nevertheless, the presence of elevated ctn levels raises two anesthetic management issues: first, the optimum timing of anesthesia induction and surgery and, second, the risk of perioperative cardiovascular deterioration. A recent MI has been consistently identified as a risk factor for perioperative cardiac events. 14,26,51 The pendulum of opinion has swung toward immediate management of ruptured intracranial aneurysms; this facilitates the treatment of vasospasm and decreases the risk of rebleeding. Cardiac troponin has proven to be a valuable marker in estimating the size of the MI and predicting the EF after acute MI. These trends do not hold for reversible 526
4 Troponin values in stunned myocardium SM and therefore can be used to differentiate between SM and MI. The retrospective nature of this study, the small patient population with reversible neurogenic left ventricular dysfunction, and the use of a historical control group are the limitations of this study. The results obtained from this pilot study, however, indicate that ctn values could be used as objective criteria to determine the feasibility of early operative intervention. A larger prospective study will be needed to validate these findings. Conclusions Differentiating between MI and reversible SM associated with aneurysmal SAH influences the time of surgical intervention. Cardiac troponins are the most sensitive serological markers for myocardial injury. In this study, we have established criteria that should help distinguish SM associated with aneurysmal SAH. 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