Vol 53, No 6 (2019)
Research Paper
Published online: 2019-10-28

open access

Page views 2086
Article views/downloads 571
Get Citation

Connect on Social Media

Connect on Social Media

Predictors of unfavourable outcome in aneurysmal subarachnoid haemorrhage

Tijana Nastasovic1, Branko Milakovic12, Mila Stosic1, Jelena Eric Marinkovic2, Rosanda Ilic23, Mihailo Milicevic23, Irena Cvrkota23, Kristina Radinovic4, Olga Petrovic5, Danica Grujicic23
Pubmed: 31657445
Neurol Neurochir Pol 2019;53(6):421-427.

Abstract

Background. Mortality rates following aneurysmal subarachnoid haemorrhage (aSAH) have decreased due to improvements in diagnoses and the management of complications, as well as early obliteration of the aneurysms. Neurogenic pulmonary oedema (NPO) is a clinical syndrome associated with an acute increase in intracranial pressure and a release of catecholamines into the circulation. This study investigated independent predictors of unfavourable outcomes (Glasgow Outcome Scores 1, 2 or 3) in patients with aSAH.

Materials and methods. A total of 262 patients with aSAH (162 females) were included in this prospective study. Clinical characteristics were assessed, and electrocardiographic, serum cardiac and inflammatory biomarker measurements were recorded on admission. Outcomes were assessed three months after admission. Univariate and multivariate analyses of these data were used to predict unfavourable outcomes.

Results. A total of 156 patients (59.54%) had unfavourable outcomes. Compared to those who had favourable outcomes, patients with unfavourable outcomes were significantly older (54.37 ± 10.56 vs. 49.13 ± 10.77 years; p < 0.001) and had more severe aSAHs (Hunt and Hess grades ≥ 3: 82.7% vs. 39.6%; p < 0.001). Patients with unfavourable outcomes were more likely to have NPO (10.3% vs. 2.8%; p = 0.023), hydrocephalus (34.0% vs. 20.8%; p = 0.02), and aneurysm reruptures (28.2% vs. 3.8%; p < 0.001).
Independent predictors of an unfavourable outcome included Hunt and Hess grades ≥ 3 (odds ratio [OR], 4.291; 95% confidence interval [CI], 2.168–8.491; p < 0.001), increased systolic blood pressure on admission (OR, 1.020; 95% CI, 1.002–1.038; p = 0.03), increased heart rate (HR) on admission (OR, 1.024; 95% CI, 1.001–1.048; p = 0.04), and aneurysm rerupture (OR, 4.961; 95% CI, 1.461–16.845; p = 0.01).

Conclusions. These findings suggest that aneurysm reruptures, as well as increased blood pressure and HR, are associated with unfavourable outcomes in patients with aSAH.

Article available in PDF format

View PDF Download PDF file

References

  1. Al-Khindi T, Macdonald RL, Schweizer TA, et al. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2010; 41(8): e519–e536.
  2. Bahloul M, Chaari AN, Kallel H, et al. Neurogenic pulmonary edema due to traumatic brain injury: evidence of cardiac dysfunction. Am J Crit Care. 2006; 15(5): 462–470.
  3. Brouwers PJ, Wijdicks EF, Hasan D, et al. Serial electrocardiographic recording in aneurysmal subarachnoid hemorrhage. Stroke. 1989; 20(9): 1162–1167.
  4. Connolly ES, Rabinstein AA, Carhuapoma JR, et al. American Heart Association Stroke Council, Council on Cardiovascular Radiology and Intervention, Council on Cardiovascular Nursing, Council on Cardiovascular Surgery and Anesthesia, Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012; 43(6): 1711–1737.
  5. De Marchis GM, Lantigua H, Schmidt JM, et al. Impact of premorbid hypertension on haemorrhage severity and aneurysm rebleeding risk after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2014; 85(1): 56–59.
  6. Davison DL, Terek M, Chawla LS. Neurogenic pulmonary edema. Crit Care. 2012; 16(2): 212.
  7. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980; 6(1): 1–9.
  8. Fontes RBV, Aguiar PH, Zanetti MV, et al. Acute neurogenic pulmonary edema: case reports and literature review. J Neurosurg Anesthesiol. 2003; 15(2): 144–150.
  9. Galea JP, Dulhanty L, Patel HC, et al. UK and Ireland Subarachnoid Hemorrhage Database Collaborators. Predictors of Outcome in Aneurysmal Subarachnoid Hemorrhage Patients: Observations From a Multicenter Data Set. Stroke. 2017; 48(11): 2958–2963.
  10. Germanson TP, Lanzino G, Kongable GL, et al. Risk classification after aneurysmal subarachnoid hemorrhage. Surg Neurol. 1998; 49(2): 155–163.
  11. Hop JW, Rinkel GJ, Algra A, et al. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997; 28(3): 660–664.
  12. Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968; 28(1): 14–20.
  13. Ichinomiya T, Terao Y, Miura K, et al. QTc interval and neurological outcomes in aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2010; 13(3): 347–354.
  14. Inamasu J, Nakatsukasa M, Mayanagi K, et al. Subarachnoid hemorrhage complicated with neurogenic pulmonary edema and takotsubo-like cardiomyopathy. Neurol Med Chir (Tokyo). 2012; 52(2): 49–55.
  15. Jaja BNR, Lingsma H, Schweizer TA, et al. SAHIT collaboration. Prognostic value of premorbid hypertension and neurological status in aneurysmal subarachnoid hemorrhage: pooled analyses of individual patient data in the SAHIT repository. J Neurosurg. 2015; 122(3): 644–652.
  16. Jennett B, Bond M. Assessment of outcome after severe brain damage Lancet. 1975; 1: 480–484.
  17. Junttila E, Ala-Kokko T, Ohtonen P, et al. Neurogenic pulmonary edema in patients with nontraumatic intracerebral hemorrhage: predictors and association with outcome. Anesth Analg. 2013; 116(4): 855–861.
  18. Juvela S. Prehemorrhage risk factors for fatal intracranial aneurysm rupture. Stroke. 2003; 34(8): 1852–1857.
  19. Kassell NF, Torner JC, Haley EC, et al. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg. 1990; 73(1): 18–36.
  20. Keller AZ. Hypertension, age and residence in the survival with subarachnoid hemorrhage. Am J Epidemiol. 1970; 91(2): 139–147.
  21. Kilbourn KJ, Ching G, Silverman DI, et al. Clinical outcomes after neurogenic stress induced cardiomyopathy in aneurysmal sub-arachnoid hemorrhage: a prospective cohort study. Clin Neurol Neurosurg. 2015; 128: 4–9.
  22. Kilbourn KJ, Levy S, Staff I, et al. Clinical characteristics and outcomes of neurogenic stress cadiomyopathy in aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2013; 115(7): 909–914.
  23. Le Roux PD, Elliott JP, Newell DW, et al. Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg. 1996; 85(1): 39–49.
  24. Menke J, Larsen J, Kallenberg K. Diagnosing cerebral aneurysms by computed tomographic angiography: meta-analysis. Ann Neurol. 2011; 69(4): 646–654.
  25. Milakovic B, Nastasovic T, Lepic M, et al. Takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: A case report. Vojnosanitetski pregled. 2017(00): 179–179.
  26. Mocco J, Ransom ER, Komotar RJ, et al. Preoperative prediction of long-term outcome in poor-grade aneurysmal subarachnoid hemorrhage. Neurosurgery. 2006; 59(3): 529–38; discussion 529.
  27. Molyneux AJ, Kerr RSC, Yu LM, et al. International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005; 366(9488): 809–817.
  28. Muroi C, Keller M, Pangalu A, et al. Neurogenic pulmonary edema in patients with subarachnoid hemorrhage. J Neurosurg Anesthesiol. 2008; 20(3): 188–192.
  29. Naidech AM, Kreiter KT, Janjua N, et al. Cardiac troponin elevation, cardiovascular morbidity, and outcome after subarachnoid hemorrhage. Circulation. 2005; 112(18): 2851–2856.
  30. Nieuwkamp DJ, Setz LE, Algra A, et al. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009; 8(7): 635–642.
  31. Ochiai H, Yamakawa Y, Kubota E. Deformation of the ventrolateral medulla oblongata by subarachnoid hemorrhage from ruptured vertebral artery aneurysms causes neurogenic pulmonary edema. Neurol Med Chir (Tokyo). 2001; 41(11): 529–34; discussion 534.
  32. O'Kelly CJ, Kulkarni AV, Austin PC, et al. The impact of therapeutic modality on outcomes following repair of ruptured intracranial aneurysms: an administrative data analysis. Clinical article. J Neurosurg. 2010; 113(4): 795–801.
  33. Rosengart AJ, Huo JD, Tolentino J, et al. Outcome in patients with subarachnoid hemorrhage treated with antiepileptic drugs. J Neurosurg. 2007; 107(2): 253–260.
  34. Rosengart AJ, Schultheiss KE, Tolentino J, et al. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007; 38(8): 2315–2321.
  35. Salem R, Vallée F, Dépret F, et al. Subarachnoid hemorrhage induces an early and reversible cardiac injury associated with catecholamine release: one-week follow-up study. Crit Care. 2014; 18(5): 558.
  36. Schmidt JM, Crimmins M, Lantigua H, et al. Prolonged elevated heart rate is a risk factor for adverse cardiac events and poor outcome after subarachnoid hemorrhage. Neurocrit Care. 2014; 20(3): 390–398.
  37. Steiner T, Al-Shahi Salman R, Beer R, et al. European Stroke Organisation. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke. 2014; 9(7): 840–855.
  38. Steiner T, Juvela S, Unterberg A, et al. European Stroke Organization. European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis. 2013; 35(2): 93–112.
  39. Inamasu J, Sugimoto K, Yamada Y, et al. The role of norepinephrine and estradiol in the pathogenesis of cardiac wall motion abnormality associated with subarachnoid hemorrhage. Stroke. 2012; 43(7): 1897–1903.
  40. Tang C, Zhang TS, Zhou LF. Risk factors for rebleeding of aneurysmal subarachnoid hemorrhage: a meta-analysis. PLoS One. 2014; 9(6): e99536.
  41. Taylor CL, Yuan Z, Selman WR, et al. Cerebral arterial aneurysm formation and rupture in 20,767 elderly patients: hypertension and other risk factors. J Neurosurg. 1995; 83(5): 812–819.
  42. Toftdahl DB, Torp-Pedersen CT, Engel UH, et al. [Hypertension and left ventricular hypertrophy in patients with spontaneous subarachnoid hemorrhage]. Ugeskr Laeger. 1997; 159(10): 1434–1437.
  43. Tung PP, Olmsted E, Kopelnik A, et al. Plasma B-type natriuretic peptide levels are associated with early cardiac dysfunction after subarachnoid hemorrhage. Stroke. 2005; 36(7): 1567–1569.
  44. Bilt Iv, Hasan D, Brink Rv, et al. Cardiac dysfunction after aneurysmal subarachnoid hemorrhage: Relationship with outcome. Neurology. 2013; 82(4): 351–358.
  45. Wartenberg KE, Schmidt JM, Claassen J, et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Crit Care Med. 2006; 34(3): 617–23; quiz 624.
  46. 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. 2018 [Epub ahead of print].
  47. Zhao B, Zhao Y, Tan X, et al. Factors and outcomes associated with ultra-early surgery for poor-grade aneurysmal subarachnoid haemorrhage: a multicentre retrospective analysis. BMJ Open. 2015; 5(4): e007410.
  48. Zheng J, Xu R, Liu G, et al. Effect of premorbid hypertension control on outcome of patients with aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2018; 160(12): 2401–2407.