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   Table of Contents      
ORIGINAL ARTICLE
Year : 2020  |  Volume : 6  |  Issue : 2  |  Page : 113-120

Study of the Clinical, Electrocardiographic and Biochemical Spectrum of Cardiovascular Complications in Patients With Aneurysmal Subarachnoid Hemorrhage − An Initial Experience at a Tertiary Centre in India


1 Department of Neurosurgery, Maulana Azad Medical College, Lok Nayak Jai Prakash Narayan Hospital, Guru Nanak Eye Centre and G. B. Pant Institute of Postgraduate Medical Education and Research (G.I.P.M.E.R.), New Delhi, India
2 Department of Pediatric Endocrinology, Bai Jerbai Wadia Hospital for Children, Parel, Mumbai, Maharashtra, India
3 Department of Biochemistry, Maulana Azad Medical College, Lok Nayak Jai Prakash Narayan Hospital, Guru Nanak Eye Centre and G. B. Pant Institute of Postgraduate Medical Education and Research (G.I.P.M.E.R.), New Delhi, India
4 Department of Anaesthesiology Maulana Azad Medical College, Lok Nayak Jai Prakash Narayan Hospital, Guru Nanak Eye Centre and G. B. Pant Institute of Postgraduate Medical Education and Research (G.I.P.M.E.R.), New Delhi, India
5 Department of Cardiology, Maulana Azad Medical College, Lok Nayak Jai Prakash Narayan Hospital, Guru Nanak Eye Centre and G. B. Pant Institute of Postgraduate Medical Education and Research (G.I.P.M.E.R.), New Delhi, India

Date of Submission01-Oct-2019
Date of Decision24-Jun-2020
Date of Acceptance07-Jul-2020
Date of Web Publication29-Aug-2020

Correspondence Address:
Charandeep Singh Gandhoke
9B, Cycle Merchant Society, Rasta Peth, (2nd Floor), Near YMCA, Near Hotel Shantai, Pune 411011, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mamcjms.mamcjms_77_19

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  Abstract 


Objectives: Aneurysmal subarachnoid hemorrhage (SAH) is an extremely fatal condition with mortality as high as 45%. Apart from the intra-cranial causes, there are cardiovascular events, which add to the morbidity and mortality. These can manifest with deranged cardiac biomarkers. However, quantitative assessment of these biochemical markers and its correlation with prognosis has not been adequately studied. We tried to analyse the spectrum and outcome of cardiovascular complications in patients with aneurysmal SAH and whether elevated levels of serum biochemical markers have any association with the prognosis. Study Design: Prospective observational study. Materials and Method: We included patients of all grades of aneurysmal SAH with ictus less than 48 hours at the time of admission. The patient’s serum biochemical marker levels [troponin T (TnT), total creatine phosphokinase (CPK), cardiac-specific creatine phosphokinase (CPK − MB), brain natriuretic peptide (BNP) and C reactive protein (CRP)] were measured for 6 consecutive days from the day of admission (Day 0). Patient also underwent 12 lead Electrocardiography (ECG) and two dimensional echocardiography (2D Echo) on Day 0, Day 1 and Day 5. Statistical Analysis: Data analysis was performed by using Statistical Package for Social Sciences (SPSS) version 20:0. Chi-square test and Fisher’s exact test were used to find the association between diagnosis and various data variables associated with diagnosis. P value less than 0.05 was considered as significant. Data was graphically depicted with the help of box plots. Receiver Operating Characteristic (ROC) curves were plotted for TnT, CPK and BNP. Results: Twenty five patients were enrolled in the study. Out of the five serum biochemical markers studied, TnT, CPK and BNP were statistically associated with outcome. Serum TnT levels on day 4; serum CPK levels on day 3 and day 4; and serum BNP levels on day 3, day 4 and day 5 were statistically significant. BNP was the serum biochemical marker which had the strongest statistical association with outcome. ECG abnormalities were observed in 76% of the cases. Prolonged corrected QT (QTc) interval was the most common abnormal ECG finding among the patients who died. One patient developed 3rd degree heart block and another patient developed left ventricular dysfunction with an ejection fraction of 40% on 2D Echo following aneurysmal SAH. Conclusion: Cardiovascular complications are common in patients with aneurysmal SAH. Serum quantitative levels of TnT, CPK and BNP can be incorporated in the battery of routine blood tests in SAH patients for predicting outcome.

Keywords: Aneurysmal subarachnoid hemorrhage, biochemical markers, brain natriuretic peptide, cardiovascular complications, total creatine phosphokinase, troponin T


How to cite this article:
Gandhoke CS, Syal SK, Gupta RH, Singh D, Sharma J, Mahajan B, Tandon M, Trehan VK, Bansal A. Study of the Clinical, Electrocardiographic and Biochemical Spectrum of Cardiovascular Complications in Patients With Aneurysmal Subarachnoid Hemorrhage − An Initial Experience at a Tertiary Centre in India. MAMC J Med Sci 2020;6:113-20

How to cite this URL:
Gandhoke CS, Syal SK, Gupta RH, Singh D, Sharma J, Mahajan B, Tandon M, Trehan VK, Bansal A. Study of the Clinical, Electrocardiographic and Biochemical Spectrum of Cardiovascular Complications in Patients With Aneurysmal Subarachnoid Hemorrhage − An Initial Experience at a Tertiary Centre in India. MAMC J Med Sci [serial online] 2020 [cited 2020 Sep 21];6:113-20. Available from: http://www.mamcjms.in/text.asp?2020/6/2/113/293892




  Introduction Top


Subarachnoid hemorrhage (SAH) following aneurysmal rupture is an extremely fatal condition with mortality as high as 45%.[1] The causes of death include raised intracranial pressure, failure of auto-regulation mechanisms and delayed ischemic neurological deficits (DIND) due to cerebral vasospasm. Apart from the intra-cranial causes, there are cardiovascular events, which add to the morbidity and mortality. These include cardiac arrhythmias, ECG changes like ST segment alteration, T wave inversion, prominent U waves, corrected QT (QTc) prolongation, conduction abnormalities and sinus bradycardia or tachycardia; left ventricular wall motion abnormalities with reduced ejection fractions on two dimensional echocardiography (2D Echo) and transient left ventricular apical ballooning cardiomyopathy also known as Takotsubo cardiomyopathy.[2],[3]

Patients with aneurysmal SAH can manifest with deranged cardiac biomarkers. However, quantitative assessment of these biochemical markers and its correlation with prognosis has not been adequately studied.


  Materials and Method Top


After obtaining ethical clearance from the Institutional Review Board, we conducted a prospective observational study in our department. The study included patients of all grades of aneurysmal SAH with ictus less than 48 hours at the time of admission. An informed consent was taken from the patient or the next of kin before enrolling the patient for the study. Patients who had a past history of coronary artery disease with or without coronary angioplasty and/or any cardiac surgery were excluded from the study.

All patients admitted and diagnosed to have aneurysmal SAH on computed tomography (CT) angiography/ magnetic resonance (MR) angiography/digital subtraction angiography (DSA) were included in this study. The patient’s heart rate, blood pressure, pupillary response, Glasgow Coma Scale (GCS) Score, any neurodeficits, cranial nerve palsies, Hunt and Hess grade of SAH, World Federation of Neurosurgical Societies (WFNS) grade of SAH and Fisher’s grade were noted on admission. The patient’s serum biochemical marker levels [troponin T (TnT), total creatine phosphokinase (CPK), cardiac specific creatine phosphokinase (CPK − MB), brain natriuretic peptide (BNP) and C reactive protein (CRP)] were measured for 6 consecutive days from the day of admission (Day 0). Patient also underwent 12 lead electrocardiography (ECG) and 2D Echo on Day 0, Day 1 and Day 5. ECGs were interpreted and 2D Echos were performed by a dedicated team of cardiologists. Serum TnT and BNP levels were measured by electro-chemiluminescence immunoassay on CLIA e411 Elecsys 2010 (Roche diagnostics, Mannheim, Germany). Serum CPK levels were measured by kinetic method, serum CPK − MB levels by immunoinhibition and serum CRP levels by immunoturbidimetry on fully automated autoanalyser c501 (Roche diagnostics, Mannheim, Germany). The kits and reagents were procured by Roche (Roche diagnostics India Pvt Ltd, Mumbai, India). Outcome was analyzed as survival/death and with the help of Glasgow Outcome Score.

Statistical evaluation

At the end of the study, data was collected and data analysis was performed by using Statistical Package for Social Sciences (SPSS) version 20:0 [International Business Machines Corporation (IBM), New York, United States of America]. Qualitative data variables were expressed by using frequency and percentage (%). Quantitative data variables were expressed by using mean and standard deviation (SD). Chi-square test and Fisher’s exact test were used to find the association between diagnosis and various data variables associated with diagnosis. P-value less than 0.05 was considered as significant. Data were graphically depicted with the help of box plots. The bottom and top of the box represented the first and third quartiles and the band inside the box represented the median (second quartile). Box plots also had lines extending vertically from the boxes (whiskers) which indicated variability of the data. Extremely high values were plotted as individual points (outliers). Receiver Operating Characteristic (ROC) curves were plotted for serum TnT, CPK and BNP.


  Results Top


Out of the 40 patients with aneurysmal SAH that were examined, 15 were excluded as they did not fulfil the eligibility criteria. The 25 patients that were enrolled in the study included 11 males and 14 females. The mean age at presentation was 51 years. The mortality rate in our study was 32% (8 out of 25 patients).

Higher the grade, worse the outcome

As already established in the literature, even in our study, higher age (P =.016); higher Hunt and Hess grade of SAH (P =.03); higher WFNS grade of SAH (P =.001) and higher Fisher’s grade (P =.001) were statistically associated with a poor outcome (survival/death) [Figure 1].
Figure 1 Graphical representation showing that higher age group, higher Hunt and Hess grade of SAH, higher WFNS grade of SAH and higher Fisher’s grade were statistically associated with a poor outcome. SAH, subarachnoid hemorrhage; WFNS, World Federation of Neurosurgical Societies

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Electrocardiographic and echocardiographic changes following aneurysmal SAH

ECG changes following aneurysmal SAH were observed in 19 of the 25 patients (76%) enrolled in the study. These included ST segment depression/elevation/flattening, T wave inversion/tall peaked T wave, prominent U wave, prolonged QTc interval, sinus bradycardia or tachycardia and right bundle branch block. Prolonged QTc interval was the most common abnormal ECG finding among the patients who died (6 out of 8 patients). One patient developed 3rd degree heart block and another patient developed left ventricular dysfunction with an ejection fraction of 40% on 2D echo following aneurysmal SAH.

Serum biochemical markers in aneurysmal SAH

Out of the five serum biochemical markers studied, three (TnT, CPK and BNP) were statistically associated with outcome. Serum TnT levels on day 4 (P =.04); serum CPK levels on day 3 (P =.01) and day 4 (P =.035); and serum BNP levels on day 3 (P =.045), day 4 (P =.023) and day 5 (P =.045) were statistically significant [Figure 2]. Abnormal high levels of these three biochemical markers were associated with poor prognosis. BNP was the serum biochemical marker which had the strongest statistical association with outcome. There was no statistical association for CPK − MB and CRP with outcome.
Figure 2 Graphical representation showing that serum troponin T levels on day 4; serum total creatine phosphokinase levels on day 3 and day 4; and serum brain natriuretic peptide levels on day 3, day 4 and day 5 were statistically associated with outcome

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Box plot and ROC curve analysis for TnT, CPK and BNP

Graphical representation of the levels of TnT (normal level is less than 0.01 ng/ml) in the form of a ‘box plot’ showed that some patients had abnormally high levels of TnT (∼1 ng/ml, which were marked as outliers in the box plot) [Figure 3]. These patients with aneurysmal SAH had a poor outcome. On ROC curve analysis for TnT, the day 4 cut off level was 0.014 ng/ml [Figure 4]. Day 4 TnT level of more than 0.014 ng/ml had 80% sensitivity for predicting a poor outcome. Day 4 TnT level of less than 0.014 ng/ml had 76.5% specificity for predicting survival.
Figure 3 Box and whisker plots of troponin T, total creatine phosphokinase and BNP showing that, in a few patients, abnormally high levels of these serum biochemical markers were observed which were associated with a poor outcome

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Figure 4 Receiver Operating Characteristic (ROC) curve analysis for troponin T, total creatine phosphokinase and BNP (C.I − Confidence Interval; +LR − Positive Likelihood Ratio; −LR − Negative Likelihood Ratio; total CK − total creatine phosphokinase; BNP − Brain Natriuretic Peptide)

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Similarly, graphical representation of the levels of CPK (normal level is 25 − 195 U/L) and BNP (normal level < 100 pg/ml) in the form of a ‘box plot’ were also performed [Figure 3]. In a few patients, abnormally high levels of CPK (∼2500 U/L) and BNP (∼4000 to 8000 pg/ml) were observed which were also associated with a poor outcome. On ROC curve analysis for CPK, the day 3 cut-off level was 213 U/L and the day 4 cut-off level was 260 U/L [Figure 4]. Day 3 CPK level of more than 213 U/L and day 4 CPK level of more than 260 U/L, both, had 80 % sensitivity for predicting a poor outcome. Day 3 CPK level of less than 213 U/L and day 4 CPK level of less than 260 U/L, both, had 82.4 % specificity for predicting survival. On ROC curve analysis for BNP, the day 3 cut-off level was 295 pg/ml; the day 4 cut-off level was 453 pg/ml and the day 5 cut-off level was 254 pg/ml [Figure 4]. Day 3 BNP level of more than 295 pg/ml, day 4 BNP level of more than 453 pg/ml and day 5 BNP level of more than 254 pg/ml had 80%, 80% and 100% sensitivity, respectively, for predicting a poor outcome. Day 3 BNP level of less than 295 pg/ml, day 4 BNP level of less than 453 pg/ml and day 5 BNP level of less than 254 pg/ml had 76.5%, 94.1% and 75% specificity, respectively, for predicting survival.


  Discussion Top


Possible mechanisms of nonneurologic complications following aneurysmal SAH [Figure 5]

Massive sympathetic nervous system activation occurs in patients with aneurysmal SAH. In the beginning, this results in a hyperdynamic cardiovascular state. As a result of this catecholamine surge, there is an intense systemic vasoconstriction which leads to an increase in cardiac afterload, myocardial workload and oxygen demand. Because of simultaneous coronary vasoconstriction, the increase in myocardial oxygen demand is not associated with an increase in oxygen delivery. This leads to subendocardial ischemia and impaired ventricular function may follow. This can further lead to cardiogenic pulmonary edema and systemic hypotension.[4] Systemic hypotension can precipitate vasospasm leading to DINDs. The classic histological picture of catecholamine induced cardiomyopathy includes myocardial contraction band necrosis, which is most dense in the subendocardial regions of the heart with relative apical sparing, corresponding with areas of sympathetic innervations rather than specific vascular territories.[5]
Figure 5 Flowchart showing mechanisms of nonneurologic complications following aneurysmal SAH.

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Catecholamines also potentiate the activation of endothelin, which plays a role in the development of vasospasm.[6],[7],[8] Catecholamine induced stress may lead to the production of toxic cytokines, stress hyperglycemia, electrolyte imbalance and leucocytosis. Renin- Angiotensin- Aldosterone System (RAAS) is also activated in the early stages of aneurysmal SAH. Elevated plasma renin levels are also associated with poor prognosis in these patients.[9] Aneurysmal SAH is frequently accompanied by fever, leucocytosis and elevated levels of interleukin 6 (IL-6) and CRP, which are markers of Systemic Inflammatory Response Syndrome (SIRS). SIRS, not only promotes extracerebral organ dysfunction, but also exacerbates delayed cerebral ischemia, which contributes to a poor outcome after SAH.[10],[11]

Other relevant studies published in the literature

Mayer et al. in their study concluded that symmetrical T wave inversion and severe QTc segment prolongation best identified patients at risk for myocardial dysfunction and may serve as a useful criterion for echocardiographic screening following SAH.[12] Sakr et al. in their paper observed that 66.7% of the patients had abnormal ECGs following aneurysmal SAH.[13] They concluded that repolarization abnormalities were the commonest ECG alterations, and ST depression was more common in patients with poor outcome.[13] Ibrahim et al. in their study concluded that QT prolongation and tachycardia on ECG were independently associated with angiographic vasospasm after aneurysmal SAH on multivariate analysis.[14] Di Pasquale et al. found that 90% of patients had ECG abnormalities within the first 48 hours following SAH.[15] Marafioti et al. in their paper concluded that prolonged QTc interval was a powerful predictor of non-cardiac mortality in patients with aneurysmal SAH independent of traditional risk factors.[16] In our study also, 76% of the patients had ECG changes following aneurysmal SAH and prolonged QTc interval was the most common abnormal ECG finding among the patients who died.

Oras et al. in their study concluded that increased serum levels of highly sensitive TnT were independently associated with poor one year outcome in patients with aneurysmal SAH.[17] Furthermore, increased levels of highly sensitive TnT and N terminal pro-BNP were independently associated with cerebral infarction due to delayed cerebral ischemia.[17] Van der Bilt et al. in their paper concluded that on multivariate analyses, poor WFNS grade, sinus tachycardia, ST segment depression, ST segment elevation and elevated TnT on admission predicted early myocardial wall motion abnormalities (WMAs) and myocardial infarct pattern on admission ECG; increased TnT also predicted late WMAs.[18] In patients with aneurysmal SAH, myocardial wall motion abnormalities were associated with a poor outcome, independent of other predictors.[18] Ahmadian et al. reported that troponin levels of greater than 1ng/ml had 10 times increased risk of death.[19] However, some studies failed to prove the prognostic significance of elevated serum troponin levels in patients with aneurysmal SAH. Pereira et al. observed in their study that only higher mean 8 day S100B value and persistent intracranial hypertension predicted a poor outcome after one year.[20] Sanchez Pena et al. in their paper concluded that after multivariate analysis, only mean 15 day S100B values significantly predicted outcome.[21] Poor outcome was associated with serum troponin initial value but in a univariate manner.[21] Tung et al. in their study observed that higher mean serum BNP levels in patients with aneurysmal SAH were present in those with regional WMAs (550 versus 261 pg/ml), diastolic dysfunction (360 versus 44 pg/ml), pulmonary edema (719 versus 204 pg/ml), elevated troponin I levels (662 versus 240 pg/ml) and left ventricular ejection fraction less than 50% (644 versus 281 pg/ml) which were all statistically significant.[22] Therefore, they concluded that elevated BNP levels were associated with myocardial necrosis, pulmonary edema, and both systolic and diastolic dysfunction of the left ventricle.[22] According to Taub et al., in their study, BNP level of greater than 276 pg/ml was associated with increased odds of cerebral infarction.[23] Audibert et al. in their study concluded that increased BNP was associated with an unfavourable outcome.[24] McAteer et al. in their study observed that there were significant relationships between BNP, troponin I and poor outcomes after aneurysmal SAH.[25]

In our study also, serum levels of TnT, CPK and BNP were statistically associated with outcome. We could not find any statistical association for serum CPK − MB and serum CRP levels with outcome. One of the limitations of the study was the small sample size.


  Conclusion Top


Cardiovascular complications are common in patients with aneurysmal SAH and these cardiovascular events can lead to a poor outcome. Serum quantitative levels of TnT, CPK and BNP showed statistically significant association with outcome and can be incorporated in the battery of routine blood tests in aneurysmal SAH patients for predicting outcome.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Hop JW, Rinkel GJ, Algra A, Gijn JV. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 1997;28:660-4.  Back to cited text no. 1
    
2.
Jain R, Deveikis J, Thompson BG. Management of patients with stunned myocardium associated with subarachnoid hemorrhage. Am J Neuroradiol 2004;25:126-9.  Back to cited text no. 2
    
3.
Franco C, Khaled B, Afonso L, Raufi M. Acute subarachnoid hemorrhage and cardiac abnormalities: takotsubo cardiomyopathy or neurogenic stunned myocardium? A case report. Cases Journal 2010;3:81.  Back to cited text no. 3
    
4.
Nguyen H, Zaroff J. Neurogenic stunned myocardium. Curr Neurol Neurosci Rep 2009;9:486-91.  Back to cited text no. 4
    
5.
Gregory T, Smith M. Cardiovascular complications of brain injury. Continuing Education in Anaesthesia Critical Care & Pain 2012;12:67-71.  Back to cited text no. 5
    
6.
Johansson P, Haase N, Perner A, Ostrowski S. Association between sympathoadrenal activation, fibrinolysis and endothelial damage in septic patients: a prospective study. J Crit Care 2014;29:327-33.  Back to cited text no. 6
    
7.
Yeung P, Shen J, Chung S, Chung SK. Targeted over-expression of endothelin-1 in astrocytes leads to more severe brain damage and vasospasm after subarachnoid hemorrhage. BMC Neurosci 2013;14:131.  Back to cited text no. 7
    
8.
Bellapart J, Jones L, Bandeshe H, Boots R. Plasma endothelin-1 as screening marker for cerebral vasospasm after subarachnoid hemorrhage. Neurocrit Care 2014;20:77-83.  Back to cited text no. 8
    
9.
Neil-Dwyer G, Walter P, Shaw H, Doshi R, Hodge M. Plasma renin activity in patients after a subarachnoid hemorrhage—a possible predictor of outcome. Neurosurgery 1980;7:578-82.  Back to cited text no. 9
    
10.
Dhar R, Diringer M. The burden of the systemic inflammatory response predicts vasospasm and outcome after subarachnoid hemorrhage. Neurocrit Care 2008;8:404-12.  Back to cited text no. 10
    
11.
Kitamura Y, Nomura M, Shima H, Kuwana N, Kuramitsu T, Chang CC et al. Acute lung injury associated with systemic inflammatory response syndrome following subarachnoid hemorrhage: a survey by the Shonan Neurosurgical Association. Neurol Med Chir (Tokyo) 2010;50:456-60.  Back to cited text no. 11
    
12.
Mayer SA, LiMandri G, Sherman D, Lennihan L, Fink ME, Solomon RA et al. Electrocardiographic markers of abnormal left ventricular wall motion in acute subarachnoid hemorrhage. J Neurosurg 1995;83:889-96.  Back to cited text no. 12
    
13.
Sakr YL, Lim N, Amaral AC, Ghosn I, Carvalho FB, Renard M et al. Relation of ECG changes to neurological outcome in patients with aneurysmal subarachnoid hemorrhage. Int J Cardiol 2004;96:369-73.  Back to cited text no. 13
    
14.
Ibrahim GM, Macdonald RL. Electrocardiographic changes predict angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Stroke 2012;43:2102-7.  Back to cited text no. 14
    
15.
Di Pasquale G, Pinelli G, Andreoli A, Manini G, Grazi P, Tognetti F. Holter detection of cardiac arrhythmias in intracranial subarachnoid hemorrhage. Am J Cardiol 1987;59:596-600.  Back to cited text no. 15
    
16.
Marafioti V, Rossi A, Carbone V, Pasqualin A, Vassanelli C. Prolonged QTc interval is a powerful predictor of non-cardiac mortality in patients with aneurysmal subarachnoid hemorrhage independently of traditional risk factors. Int J Cardiol 2013;170:e5-e6.  Back to cited text no. 16
    
17.
Oras J, Grivans C, Bartley A, Rydenhag B, Ricksten SE, Seeman-Lodding H. Elevated high-sensitive troponin T on admission is an indicator of poor long-term outcome in patients with subarachnoid hemorrhage: a prospective observational study. Crit Care 2016;20:11.  Back to cited text no. 17
    
18.
Van der Bilt IA, Hasan D, van den Brink RB, Cramer MJ, van der Jagt M, van Kooten F et al. Time course and risk factors for myocardial dysfunction after aneurysmal subarachnoid hemorrhage. Neurosurgery 2015;76:700-6.  Back to cited text no. 18
    
19.
Ahmadian A, Mizzi A, Banasiak M, Downes K, Camporesi EM, Sullebarger JT et al. Cardiac manifestations of subarachnoid hemorrhage. Heart Lung Vessel 2013;5:168-78.  Back to cited text no. 19
    
20.
Pereira AR, Sanchez-Pena P, Biondi A, Sourour N, Boch AL, Colonne C et al. Predictors of 1-year outcome after coiling for poor grade subarachnoid aneurysmal hemorrhage. Neurocrit Care 2007;7:18-26.  Back to cited text no. 20
    
21.
Sanchez-Pena P, Pereira AR, Sourour NA, Biondi A, Lejean L, Colonne C et al. S100B as an additional prognostic marker in subarachnoid aneurysmal hemorrhage. Crit Care Med 2008;36:2267-73.  Back to cited text no. 21
    
22.
Tung PP, Olmsted E, Kopelnik A, Banki NM, Drew BJ, Ko N et al. Plasma B-type natriuretic peptide levels are associated with early cardiac dysfunction after subarachnoid hemorrhage. Stroke 2005;36:1567-9.  Back to cited text no. 22
    
23.
Taub PR, Fields JD, Wu AH, Miss JC, Lawton MT, Smith WS et al. Elevated BNP is associated with vasospasm-independent cerebral infarction following aneurysmal subarachnoid hemorrhage. Neurocrit Care 2011;15:13-8.  Back to cited text no. 23
    
24.
Audibert G, Steinmann G, de Talance N, Charpentier C, Laurens MH, Mertes PM. Brain natriuretic peptide (BNP) is a marker of subarachnoid hemorrhage severity. Eur J Anaesthesiol 2005;22:20.  Back to cited text no. 24
    
25.
McAteer A, Hravnak M, Chang Y, Crago EA, Gallek MJ, Yousef KM. The relationships between bnp and neurocardiac injury severity, noninvasive cardiac output, and outcomes after aneurysmal subarachnoid hemorrhage. Biol Res Nurs 2017;19:531-7.  Back to cited text no. 25
    


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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]



 

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