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Impact of echocardiographic wall motion abnormality and cardiac biomarker elevation on outcome after subarachnoid hemorrhage: a meta-analysis

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Abstract

Cardiac abnormalities (echocardiographic wall motion abnormality (WMA), biomarker elevation of cardiac troponin (cTn), B-type natriuretic peptide (BNP), or N-terminal prohormone of B-type natriuretic peptide (NT-proBNP)) frequently occur after subarachnoid hemorrhage (SAH). The clinical significance of cardiac abnormalities after SAH remains controversial. This meta-analysis was performed to assess the association between cardiac abnormalities and patient outcomes, including delayed cerebral ischemia (DCI), poor outcome, and death in SAH patients. PubMed and Embase were searched for observational studies reporting an association between cardiac abnormalities and outcome after SAH that were published before 31 December 2017. We extracted data regarding patient characteristics, cardiac abnormalities, and outcome measurements (DCI, poor outcome, or death). Risk ratios (RRs) and 95% confidence intervals (CIs) were calculated using a random-effects model. Twenty-six studies involving 3917 patients were included in our data analysis. WMA showed significant associations with higher rates of DCI (RR, 2.03; 95% CI, 0.99–4.15), poor outcome (RR, 1.45; 95% CI, 1.08–1.93), and death (RR, 2.54; 95% CI, 1.59–4.05). cTn elevation was associated with an increased risk of DCI (RR, 1.48; 95% CI, 1.23–1.79), poor outcome (RR, 1.85; 95% CI, 1.49–2.30), and death (RR, 2.68; 95% CI, 2.19–3.27). Elevation of BNP or NT-proBNT was significantly associated with higher rates of DCI (RR, 1.87; 95% CI, 1.16–3.02). WMA and elevation of cTn, BNP, and NT-proBNP in SAH patients are associated with an increased risk of DCI, poor outcome, and death after SAH.

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References

  1. Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ (2009) Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 8:635–642

    PubMed  Google Scholar 

  2. van der Bilt IA, Hasan D, Vandertop WP, Wilde AA, Algra A, Visser FC, Rinkel GJ (2009) Impact of cardiac complications on outcome after aneurysmal subarachnoid hemorrhage: a meta-analysis. Neurology 72:635–642

    PubMed  Google Scholar 

  3. Jaeger M, Soehle M, Schuhmann MU, Meixensberger J (2012) Clinical significance of impaired cerebrovascular autoregulation after severe aneurysmal subarachnoid hemorrhage. Stroke 43:2097–2101

    PubMed  Google Scholar 

  4. Mayer SA, Lin J, Homma S, Solomon RA, Lennihan L, Sherman D, Fink ME, Beckford A, Klebanoff LM (1999) Myocardial injury and left ventricular performance after subarachnoid hemorrhage. Stroke 30:780–786

    CAS  PubMed  Google Scholar 

  5. Cremers CH, van der Bilt IA, van der Schaaf IC, Vergouwen MD, Dankbaar JW, Cramer MJ, Wilde AA, Rinkel GJ, Velthuis BK (2016) Relationship between cardiac dysfunction and cerebral perfusion in patients with aneurysmal subarachnoid hemorrhage. Neurocrit Care 24:202–206

    CAS  PubMed  Google Scholar 

  6. van Gijn J, Kerr RS, Rinkel GJ (2007) Subarachnoid haemorrhage. Lancet 369:306–318

    PubMed  Google Scholar 

  7. Zhang L, Qi S (2016) Electrocardiographic abnormalities predict adverse clinical outcomes in patients with subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 25:2653–2659

    PubMed  Google Scholar 

  8. Hunt WE, Hess RM (1968) Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20

    CAS  PubMed  Google Scholar 

  9. [No authors listed] (1988) Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale. J Neurosurg 68:985–986

  10. Teasdale G, Jennett B (1974) Assessment of coma and impaired consciousness. A practical scale. Lancet 2:81–84

    CAS  PubMed  Google Scholar 

  11. Higgins JPT, Green S, eds (2011) Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration. Available at: http://www.cochrane-handbook.org. Accessed 10 January 2014

  12. Pollick C, Cujec B, Parker S, Tator C (1988) Left ventricular wall motion abnormalities in subarachnoid hemorrhage: an echocardiographic study. J Am Coll Cardiol 12:600–605

    CAS  PubMed  Google Scholar 

  13. Parekh N, Venkatesh B, Cross D, Leditschke A, Atherton J, Miles W, Winning A, Clague A, Rickard C (2000) Cardiac troponin I predicts myocardial dysfunction in aneurysmal subarachnoid hemorrhage. J Am Coll Cardiol 36:1328–1335

    CAS  PubMed  Google Scholar 

  14. Deibert E, Barzilai B, Braverman AC, Edwards DF, Aiyagari V, Dacey R, Diringer M (2003) Clinical significance of elevated troponin I levels in patients with nontraumatic subarachnoid hemorrhage. J Neurosurg 98:741–746

    PubMed  Google Scholar 

  15. Sviri GE, Shik V, Raz B, Soustiel JF (2003) Role of brain natriuretic peptide in cerebral vasospasm. Acta Neurochir 145:851–860

    PubMed  Google Scholar 

  16. Naidech AM, Kreiter KT, Janjua N, Ostapkovich ND, Parra A, Commichau C, Fitzsimmons BF, Connolly ES, Mayer SA (2005) Cardiac troponin elevation, cardiovascular morbidity, and outcome after subarachnoid hemorrhage. Circulation 112:2851–2856

    CAS  PubMed  Google Scholar 

  17. Schuiling WJ, Dennesen PJ, Tans JT, Kingma LM, Algra A, Rinkel GJ (2005) Troponin I in predicting cardiac or pulmonary complications and outcome in subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 76:1565–1569

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Banki N, Kopelnik A, Tung P, Lawton MT, Gress D, Drew B, Dae M, Foster E, Parmley W, Zaroff J (2006) Prospective analysis of prevalence, distribution, and rate of recovery of left ventricular systolic dysfunction in patients with subarachnoid hemorrhage. J Neurosurg 105:15–20

    PubMed  Google Scholar 

  19. Kothavale A, Banki NM, Kopelnik A, Yarlagadda S, Lawton MT, Ko N, Smith WS, Drew B, Foster E, Zaroff JG (2006) Predictors of left ventricular regional wall motion abnormalities after subarachnoid hemorrhage. Neurocrit Care 4:199–205

    PubMed  Google Scholar 

  20. Yarlagadda S, Rajendran P, Miss JC, Banki NM, Kopelnik A, Wu AH, Ko N, Gelb AW, Lawton MT, Smith WS, Young WL, Zaroff JG (2006) Cardiovascular predictors of in-patient mortality after subarachnoid hemorrhage. Neurocrit Care 5:102–107

    PubMed  Google Scholar 

  21. Ramappa P, Thatai D, Coplin W, Gellman S, Carhuapoma JR, Quah R, Atkinson B, Marsh JD (2008) Cardiac troponin-I: a predictor of prognosis in subarachnoid hemorrhage. Neurocrit Care 8:398–403

    PubMed  Google Scholar 

  22. Sandhu R, Aronow WS, Rajdev A, Sukhija R, Amin H, D'aquila K, Sangha A (2008) Relation of cardiac troponin I levels with in-hospital mortality in patients with ischemic stroke, intracerebral hemorrhage, and subarachnoid hemorrhage. Am J Cardiol 102:632–634

    CAS  PubMed  Google Scholar 

  23. Sugimoto K, Watanabe E, Yamada A, Iwase M, Sano H, Hishida H, Ozaki Y (2008) Prognostic implications of left ventricular wall motion abnormalities associated with subarachnoid hemorrhage. Int Heart J 49:75–85

    PubMed  Google Scholar 

  24. Hravnak M, Frangiskakis JM, Crago EA, Chang Y, Tanabe M, Gorcsan J 3rd, Horowitz MB (2009) Elevated cardiac troponin I and relationship to persistence of electrocardiographic and echocardiographic abnormalities after aneurysmal subarachnoid hemorrhage. Stroke 40:3478–3484

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Miketic JK, Hravnak M, Sereika SM, Crago EA (2010) Elevated cardiac troponin I and functional recovery and disability in patients after aneurysmal subarachnoid hemorrhage. Am J Crit Care 19:522–528

    PubMed  PubMed Central  Google Scholar 

  26. Jyotsna M, Prasad V, Indrani G, Trikamji BV (2010) Importance of detection of segmental wall motion abnormalities of left ventricle in nontraumatic subarachnoid hemorrhage: a prospective study. Echocardiography 27:496–500

    PubMed  Google Scholar 

  27. Ichinomiya T, Terao Y, Miura K, Higashijima U, Tanise T, Fukusaki M, Sumikawa K (2010) QTc interval and neurological outcomes in aneurysmal subarachnoid hemorrhage. Neurocrit Care 13:347–354

    PubMed  Google Scholar 

  28. Temes RE, Tessitore E, Schmidt JM, Naidech AM, Fernandez A, Ostapkovich ND, Frontera JA, Wartenberg KE, Di Tullio MR, Badjatia N, Connolly ES, Mayer SA, Parra A (2010) Left ventricular dysfunction and cerebral infarction from vasospasm after subarachnoid hemorrhage. Neurocrit Care 13:359–365

    PubMed  Google Scholar 

  29. Taub PR, Fields JD, Wu AH, Miss JC, Lawton MT, Smith WS, Young WL, Zaroff JG, Ko NU (2011) Elevated BNP is associated with vasospasm-independent cerebral infarction following aneurysmal subarachnoid hemorrhage. Neurocrit Care 15:13–18

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Degos V, Apfel CC, Sanchez P, Colonne C, Renuit I, Clarençon F, Nouet A, Boch AL, Pourmohamad T, Kim H, Gourraud PA, Young WL, Puybasset L (2012) An admission bioclinical score to predict 1-year outcomes in patients undergoing aneurysm coiling. Stroke 43:1253–1259

    PubMed  Google Scholar 

  31. Gupte M, John S, Prabhakaran S, Lee VH (2013) Troponin elevation in subarachnoid hemorrhage does not impact in-hospital mortality. Neurocrit Care 18:368–373

    CAS  PubMed  Google Scholar 

  32. Kilbourn KJ, Levy S, Staff I, Kureshi I, McCullough L (2013) Clinical characteristics and outcomes of neurogenic stress cadiomyopathy in aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg 115:909–914

    PubMed  Google Scholar 

  33. van der Bilt HD, van den Brink R, Cramer MJ, van der Jagt M, van Kooten F, Meertens J, van den Berg M, Groen R, Ten Cate F, Kamp O, Götte M, Horn J, Groeneveld J, Vandertop P, Algra A, Visser F, Wilde A, Rinkel G (2014) Cardiac dysfunction after aneurysmal subarachnoid hemorrhage: relationship with outcome. Neurology 82:1–8

    Google Scholar 

  34. Kilbourn KJ, Ching G, Silverman DI, McCullough L, Brown RJ (2015) Clinical outcomes after neurogenic stress induced cardiomyopathy in aneurysmal sub-arachnoid hemorrhage: a prospective cohort study. Clin Neurol Neurosurg 128:4–9

    PubMed  Google Scholar 

  35. Duello KM, Nagel JP, Thomas CS, Blackshear JL, Freeman WD (2015) Relationship of troponin T and age- and sex-adjusted BNP elevation following subarachnoid hemorrhage with 30-day mortality. Neurocrit Care 23:59–65

    CAS  PubMed  Google Scholar 

  36. Banki NM, Kopelnik A, Dae MW, Miss J, Tung P, Lawton MT, Drew BJ, Foster E, Smith W, Parmley WW, Zaroff JG (2005) Acute neurocardiogenic injury after subarachnoid hemorrhage. Circulation 112:3314–3319

    PubMed  Google Scholar 

  37. Lyon AR, Rees PS, Prasad S, Poole-Wilson PA, Harding SE (2008) Stress (takotsubo) cardiomyopathy: a novel pathophysiological hypothesis to explain catecholamine-induced acute myocardial stunning. Nat Clin Pract Cardiovasc Med 5:22–29

    CAS  PubMed  Google Scholar 

  38. Tanabe M, Crago EA, Suffoletto MS, Hravnak M, Frangiskakis JM, Kassam AB, Horowitz MB, Gorcsan J 3rd (2008) Relation of elevation in cardiac troponin I to clinical severity, cardiac dysfunction, and pulmonary congestion in patients with subarachnoid hemorrhage. Am J Cardiol 102:1545–1550

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Kono T, Morita H, Kuroiwa T, Onaka H, Takatsuka H, Fujiwara A (1994) Left ventricular wall motion abnormalities in patients with subarachnoid hemorrhage: neurogenic stunned myocardium. J Am Coll Cardiol 24:636–640

    CAS  PubMed  Google Scholar 

  40. Mayer SA, LiMandri G, Sherman D, Lennihan L, Fink ME, Solomon RA, DiTullio M, Klebanoff LM, Beckford AR, Homma S (1995) Electrocardiographic markers of abnormal left ventricular wall motion in acute subarachnoid hemorrhage. J Neurosurg 83:889–896

    CAS  PubMed  Google Scholar 

  41. Zaroff JG, Rordorf GA, Ogilvy CS, Picard MH (2000) Regional patterns of left ventricular systolic dysfunction after subarachnoid hemorrhage: evidence for neurally mediated cardiac injury. J Am Soc Echocardiogr 13:774–779

    CAS  PubMed  Google Scholar 

  42. Nguyen H, Zaroff JG (2009) Neurogenic stunned myocardium. Curr Neurol Neurosci Rep 9:486–491

    PubMed  Google Scholar 

  43. Brunetti ND, Ieva R, Rossi G, Barone N, De Gennaro L, Pellegrino PL, Mavilio G, Cuculo A, Di Biase M (2008) Ventricular outflow tract obstruction, systolic anterior motion and acute mitral regurgitation in Tako-Tsubo syndrome. Int J Cardiol 127:152–157

    Google Scholar 

  44. Burri MV, Nanda NC, Lloyd SG, Hsiung MC, Dod HS, Beto RJ, Bhardwaj R, Jain A, Jackson J, Agarwal A, Chaurasia P, Prasad AN, Manda J, Pothineni KR (2008) Assessment of systolic and diastolic left ventricular and left atrial function using vector velocity imaging in Takotsubo cardiomyopathy. Echocardiogr 25:1138–1144

    Google Scholar 

  45. Mansencal N, Abbou N, Pilliere R, El Mahmoud R, Farcot JC, Dubourg O (2009) Usefulness of two-dimensional speckle tracking echocardiography for assessment of Tako-Tsubo cardiomyopathy. Am J Cardiol 103:1020–1024

    PubMed  Google Scholar 

  46. de Lemos JA (2013) Increasingly sensitive assays for cardiac troponins: a review. JAMA 309:2262–2269

    PubMed  Google Scholar 

  47. Tung P, Kopelnik A, Banki N, Ong K, Ko N, Lawton MT, Gress D, Drew B, Foster E, Parmley W, Zaroff J (2004) Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke 35:548–551

    PubMed  Google Scholar 

  48. Apple FS (1999) Tissue specificity of cardiac troponin I, cardiac troponin T and creatine kinase-MB. Clin Chim Acta 284:151–159

    CAS  PubMed  Google Scholar 

  49. Thygesen K, Alpert JS, Jaffe AS et al (2012) Third universal definition of myocardial infarction. Circulation 126:2020–2035

    PubMed  Google Scholar 

  50. Magga J, Vuolteenaho O, Tokola H, Marttila M, Ruskoaho H (1998) B-type natriuretic peptide: a myocyte-specific marker for characterizing load-induced alterations in cardiac gene expression. Ann Med 30(suppl 1):39–45

    CAS  PubMed  Google Scholar 

  51. Magga J, Marttila M, Mantymaa P, Vuolteenaho O, Ruskoaho H (1994) Brain natriuretic peptide in plasma, atria, and ventricles of vasopressinand phenylephrine-infused conscious rats. Endocrinology 134:2505–2515

    CAS  PubMed  Google Scholar 

  52. Sawada Y, Suda M, Yokoyama H, Kanda T, Sakamaki T, Tanaka S, Nagai R, Abe S, Takeuchi T (1997) Stretch-induced hypertrophic growth of cardiocytes and processing of braintype natriuretic peptide are controlled by proprotein-processing endoprotease furin. J Biol Chem 272:20545–20554

    CAS  PubMed  Google Scholar 

  53. Oras J, Grivans C, Dalla K, Omerovic E, Rydenhag B, Ricksten SE, Seeman-Lodding H (2015) High-sensitive troponin T and N-terminal pro B-type natriuretic peptide for early detection of stress-induced cardiomyopathy in patients with subarachnoid hemorrhage. Neurocrit Care 23:233–242

    CAS  PubMed  Google Scholar 

  54. Espiner EA, Leikis R, Ferch RD, MacFarlane MR, Bonkowski JA, Frampton CM, Richards AM (2002) The neuro-cardio-endocrine response to acute subarachnoid haemorrhage. Clin Endocrinol 56:629–635

    CAS  Google Scholar 

  55. Meaudre E, Jego C, Kenane N, Montcriol A, Boret H, Goutorbe P, Habib G, Palmier B (2009) B-type natriuretic peptide release and left ventricular filling pressure assessed by echocardiographic study after subarachnoid hemorrhage: a prospective study in non-cardiac patients. Crit Care 13:R76

    PubMed  PubMed Central  Google Scholar 

  56. Nyberg C, Karlsson T, Ronne-Engström E (2014) Predictors of increased cumulative serum levels of the N-terminal prohormone of brain natriuretic peptide 4 days after acute spontaneous subarachnoid hemorrhage. J Neurosurg 120:599–604

    CAS  PubMed  Google Scholar 

  57. Lang EW, Diehl RR, Mehdorn HM (2001) Cerebral autoregulation testing after aneurysmal subarachnoid hemorrhage: the phase relationship between arterial blood pressure and cerebral blood flow velocity. Crit Care Med 29:158–163

    CAS  PubMed  Google Scholar 

  58. Soehle M, Czosnyka M, Pickard JD, Kirkpatrick PJ (2004) Continuous assessment of cerebral autoregulation in subarachnoid hemorrhage. Anesth Analg 98:1133–1139

    PubMed  Google Scholar 

  59. Hop JW, Rinkel GJE, Algra A, van Gijn J (1999) Initial loss of consciousness and risk of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke 30:2268–2271

    CAS  PubMed  Google Scholar 

  60. Chang HS, Hongo K, Nakagawa H (2000) Adverse effects of limited hypotensive anesthesia on the outcome of patients with subarachnoid hemorrhage. J Neurosurg 92:971–975

    CAS  PubMed  Google Scholar 

  61. Uekusa H, Miyazaki C, Kondo K, Harada N, Nomoto J, Sugo N, Nemoto M (2014) Hydroperoxide in internal jugular venous blood reflects occurrence of subarachnoid hemorrhage-induced delayed cerebral vasospasm. J Stroke Cerebrovasc Dis 23:2217–2224

    PubMed  Google Scholar 

  62. Rabinstein AA, Friedman JA, Weigand SD, McClelland RL, Fulgham JR, Manno EM, Atkinson JL, Wijdicks EF (2004) Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 35:1862–1866

    PubMed  Google Scholar 

  63. Rowland MJ, Hadjipavlou G, Kelly M, Westbrook J, Pattinson KT (2012) Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth 109:315–329

    CAS  PubMed  Google Scholar 

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This work was supported by Harbin Science and Technology Bureau (grant numbers 2013RFQYJ078).

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  1. Department of Anaesthesiology, The Fourth Affiliated Hospital, Harbin Medical University, Yiyuan Street 37, Harbin, 150001, China

    Limin Zhang, Bing Zhang & Sihua Qi

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  1. Limin Zhang
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Zhang, L., Zhang, B. & Qi, S. Impact of echocardiographic wall motion abnormality and cardiac biomarker elevation on outcome after subarachnoid hemorrhage: a meta-analysis. Neurosurg Rev 43, 59–68 (2020). https://doi.org/10.1007/s10143-018-0985-6

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