Duration of Intracranial Pressure Increase after Aneurysmal Subarachnoid Hemorrhage: Prognostic Factors and Association with the Outcome
- Authors: Ketelauri P.1, Gümüs M.1, Gull H.H.1, Said M.2, Rauschenbach L.1, Florin Dinger T.1, Chihi M.1, Darkwah Oppong M.1, Ahmadipour Y.1, Dammann P.1, Henning Wrede K.1, Sure U.1, Jabbarli R.1
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Affiliations:
- Department of Neurosurgery and Spine Surgery, Essen University Hospital
- Department of Neurosurgery, Evangelisches Krankenhaus Oldenburg
- Issue: Vol 21, No 3 (2024)
- Pages: 253-262
- Section: Medicine
- URL: https://gynecology.orscience.ru/1567-2026/article/view/644401
- DOI: https://doi.org/10.2174/0115672026312548240610104504
- ID: 644401
Cite item
Full Text
Abstract
Objective:A rupture of the intracranial aneurysm is frequently complicated, with an increase of intracranial pressure (ICP) requiring conservative and/or surgical treatment. We analyzed the risk factors related to the duration of pathologic ICP increase and the relationship between ICP burden and the outcome of subarachnoid hemorrhage (SAH).
Methods:Consecutive cases with aneurysmal SAH treated at our institution between 01/2003 and 06/2016 were eligible for this study. Different admission variables were evaluated to predict the duration of ICP increase >20 mmHg in univariate and multivariate analyses. The association of the ICP course with SAH outcome parameters (risk of cerebral infarction, in-hospital mortality, and unfavorable outcome at 6 months defined as modified Rankin scale >3) was adjusted for major outcome-relevant confounders.
Results:Of 820 SAH patients, 378 individuals (46.1%) developed at least one ICP increase requiring conservative and/or surgical management after aneurysm treatment (mean duration: 1.76 days, range: 1 - 14 days). In the multivariable linear regression analysis, patients age (unstandardized coefficient [UC]=-0.02, p (<0.0001), World Federation of Neurosurgical Societies (WFNS) grade 4-5 at admission (UC=0.71, p (<0.004), regular medication with the angiotensinconverting enzyme (ACE) inhibitors (UC=-0.61, p =0.01), and presence of intracerebral hemorrhage (UC=0.59, p =0.002) were associated with the duration of ICP increase. In turn, patients with longer ICP elevations were at higher risk for cerebral infarction (adjusted odds ratio [aOR]=1.32 per-day-increase, p (<0.0001), in-hospital mortality (aOR=1.30, p (<0.0001) and unfavorable outcome (aOR=1.43, p (<0.0001). SAH patients who underwent primary decompressive craniectomy (DC) showed shorter periods of ICP increase than patients with a secondary decompression (mean: 2.8 vs 4.9 days, p (<0.0001).
Conclusion:The duration of ICP increase after aneurysm rupture is a strong outcome predictor and is related to younger age and higher initial severity of SAH. Further analysis of the factors impacting the course of ICP after SAH is essential for the optimization of ICP management and outcome improvement.
About the authors
Pikria Ketelauri
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Author for correspondence.
Email: info@benthamscience.net
Meltem Gümüs
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Hanah Hadice Gull
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Maryam Said
Department of Neurosurgery, Evangelisches Krankenhaus Oldenburg
Email: info@benthamscience.net
Laurel Rauschenbach
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Thiemo Florin Dinger
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Mehdi Chihi
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Marvin Darkwah Oppong
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Yahya Ahmadipour
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Philipp Dammann
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Karsten Henning Wrede
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Ulrich Sure
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
Ramazan Jabbarli
Department of Neurosurgery and Spine Surgery, Essen University Hospital
Email: info@benthamscience.net
References
- Bederson JB, Connolly ES Jr, Batjer HH, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: A statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 2009; 40(3): 994-1025. doi: 10.1161/STROKEAHA.108.191395 PMID: 19164800
- Kundra S, Mahendru V, Gupta V, Choudhary A. Principles of neuroanesthesia in aneurysmal subarachnoid hemorrhage. J Anaesthesiol Clin Pharmacol 2014; 30(3): 328-37. doi: 10.4103/0970-9185.137261 PMID: 25190938
- Long B, Koyfman A, Runyon MS. Subarachnoid Hemorrhage. Emerg Med Clin North Am 2017; 35(4): 803-24. doi: 10.1016/j.emc.2017.07.001 PMID: 28987430
- Heuer GG, Smith MJ, Elliott JP, Winn HR, Leroux PD. Relationship between intracranial pressure and other clinical variables in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 2004; 101(3): 408-16. doi: 10.3171/jns.2004.101.3.0408 PMID: 15352597
- Cossu G, Messerer M, Stocchetti N, Levivier M, Daniel RT, Oddo M. Intracranial pressure and outcome in critically ill patients with aneurysmal subarachnoid hemorrhage: A systematic review. Minerva Anestesiol 2016; 82(6): 684-96. PMID: 27045637
- Baggiani M, Graziano F, Rebora P, et al. Intracranial pressure monitoring practice, treatment, and effect on outcome in aneurysmal subarachnoid hemorrhage. Neurocrit Care 2023; 38(3): 741-51. doi: 10.1007/s12028-022-01651-8 PMID: 36471182
- Addis A, Baggiani M, Citerio G. Intracranial pressure monitoring and management in aneurysmal subarachnoid hemorrhage. Neurocrit Care 2023; 39(1): 59-69. doi: 10.1007/s12028-023-01752-y PMID: 37280411
- Nagel A, Graetz D, Schink T, et al. Relevance of intracranial hypertension for cerebral metabolism in aneurysmal subarachnoid hemorrhage. J Neurosurg 2009; 111(1): 94-101. doi: 10.3171/2009.1.JNS08587 PMID: 19284237
- Said M, Odensass S, Gümüs M, et al. Comparing radiographic scores for prediction of complications and outcome of aneurysmal subarachnoid hemorrhage: Which performs best? Eur J Neurol 2023; 30(3): 659-70. doi: 10.1111/ene.15634 PMID: 36371646
- Kramer AH. Critical ICP in subarachnoid hemorrhage: How high and how long? Neurocrit Care 2021; 34(3): 714-6. doi: 10.1007/s12028-021-01205-4 PMID: 33655454
- Mak CHK, Lu YY, Wong GKC. Review and recommendations on management of refractory raised intracranial pressure in aneurysmal subarachnoid hemorrhage. Vasc Health Risk Manag 2013; 9: 353-9. PMID: 23874101
- Rinkel GJE, Feigin VL, Algra A, van Gijn J. Circulatory volume expansion therapy for aneurysmal subarachnoid haemorrhage. Cochrane Libr 2004; 2004(4): CD000483. doi: 10.1002/14651858.CD000483.pub2 PMID: 15494997
- Molyneux AJ, Kerr RS. The future management of subarachnoid haemorrhage. J Neuroradiol 2002; 29(2): 74-5.
- Bratton SL, Chestnut RM, Ghajar J, et al. Guidelines for the management of severe traumatic brain injury. VI. Indications for intracranial pressure monitoring. J Neurotrauma 2007; 24 (Suppl. 1): S-37-44. doi: 10.1089/neu.2007.9990 PMID: 17511544
- Aiolfi A, Benjamin E, Khor D, Inaba K, Lam L, Demetriades D. Brain trauma foundation guidelines for intracranial pressure monitoring: Compliance and effect on outcome. World J Surg 2017; 41(6): 1543-9. doi: 10.1007/s00268-017-3898-6 PMID: 28188356
- Mayberg MR, Batjer HH, Dacey R, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage. A statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 1994; 25(11): 2315-28. doi: 10.1161/01.STR.25.11.2315 PMID: 7974568
- van Gijn J, Rinkel GJE. Subarachnoid haemorrhage: Diagnosis, causes and management. Brain 2001; 124(2): 249-78. doi: 10.1093/brain/124.2.249 PMID: 11157554
- Jabbarli R, Oppong MD, Dammann P, et al. Time is brain! analysis of 245 cases with decompressive craniectomy due to subarachnoid hemorrhage. World Neurosurg 2017; 98: 689-694.e2. doi: 10.1016/j.wneu.2016.12.012 PMID: 27993743
- Teasdale GM, Drake CG, Hunt W, et al. A universal subarachnoid hemorrhage scale: Report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry 1988; 51(11): 1457. doi: 10.1136/jnnp.51.11.1457 PMID: 3236024
- Fisher CM, Roberson GH, Ojemann RG. Cerebral vasospasm with ruptured saccular aneurysm-the clinical manifestations. Neurosurgery 1977; 1(3): 245-8. doi: 10.1227/00006123-197711000-00004 PMID: 615969
- Graeb DA, Robertson WD, Lapointe JS, Nugent RA, Harrison PB. Computed tomographic diagnosis of intraventricular hemorrhage. Etiology and prognosis. Radiology 1982; 143(1): 91-6. doi: 10.1148/radiology.143.1.6977795 PMID: 6977795
- Kothari RU, Brott T, Broderick JP, et al. The ABCs of measuring intracerebral hemorrhage volumes. Stroke 1996; 27(8): 1304-5. doi: 10.1161/01.STR.27.8.1304 PMID: 8711791
- van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke 1988; 19(5): 604-7. doi: 10.1161/01.STR.19.5.604 PMID: 3363593
- Ryttlefors M, Howells T, Nilsson P, Ronne-Engström E, Enblad P. Secondary insults in subarachnoid hemorrhage: occurrence and impact on outcome and clinical deterioration. Neurosurgery 2007; 61(4): 704-15. doi: 10.1227/01.NEU.0000298898.38979.E3 PMID: 17986931
- Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: A guideline for healthcare professionals from the American Heart Association. Stroke 2012; 43(6): 1711-37. doi: 10.1161/STR.0b013e3182587839 PMID: 22556195
- Veldeman M, Weiss M, Daleiden L, et al. Decompressive hemicraniectomy after aneurysmal subarachnoid hemorrhagejustifiable in light of long-term outcome? Acta Neurochir 2022; 164(7): 1815-26. doi: 10.1007/s00701-022-05250-6 PMID: 35597877
- Ohbuchi H, Hagiwara S, Arai N, Yoneyama T, Takahashi Y, Inazuka M. Optimal timing and safety of the external ventricular drainage in patients with high-grade aneurysmal subarachnoid hemorrhage treated with endovascular coiling. J Clin Neurosci 2021; 88: 63-9. doi: 10.1016/j.jocn.2021.03.003
- Ohbuchi H, Kasuya H, Hagiwara S, et al. Appropriate treatment within 13 hours after onset may improve outcome in patients with high-grade aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg 2023; 230: 107776. doi: 10.1016/j.clineuro.2023.107776 PMID: 37229951
- Sahuquillo J, Arikan F. Decompressive craniectomy for the treatment of refractory high intracranial pressure in traumatic brain injury. Cochrane Libr 2006; (1): CD003983. doi: 10.1002/14651858.CD003983.pub2 PMID: 16437469
- Schirmer CM, Hoit DA, Malek AM. Decompressive hemicraniectomy for the treatment of intractable intracranial hypertension after aneurysmal subarachnoid hemorrhage. Stroke 2007; 38(3): 987-92. doi: 10.1161/01.STR.0000257962.58269.e2 PMID: 17272765
- Jabbarli R, Darkwah Oppong M, Roelz R, et al. The pressure score to predict decompressive craniectomy after aneurysmal subarachnoid haemorrhage. Brain Commun 2020; 2(2): fcaa134. doi: 10.1093/braincomms/fcaa134 PMID: 33215084
- Zoerle T, Lombardo A, Colombo A, et al. Intracranial pressure after subarachnoid hemorrhage. Crit Care Med 2015; 43(1): 168-76. doi: 10.1097/CCM.0000000000000670 PMID: 25318385
- Czosnyka M, Balestreri M, Steiner L, et al. Age, intracranial pressure, autoregulation, and outcome after brain trauma. J Neurosurg 2005; 102(3): 450-4. doi: 10.3171/jns.2005.102.3.0450 PMID: 15796378
- Stocchetti N, Carbonara M, Citerio G, et al. Severe traumatic brain injury: Targeted management in the intensive care unit. Lancet Neurol 2017; 16(6): 452-64. doi: 10.1016/S1474-4422(17)30118-7 PMID: 28504109
- Lee SH, Oh CW, Han JH, et al. The effect of brain atrophy on outcome after a large cerebral infarction. J Neurol Neurosurg Psychiatry 2010; 81(12): 1316-21. doi: 10.1136/jnnp.2009.197335 PMID: 20650914
- Wagner M, Jurcoane A, Volz S, et al. Age-related changes of cerebral autoregulation: new insights with quantitative T2′-mapping and pulsed arterial spin-labeling MR imaging. AJNR Am J Neuroradiol 2012; 33(11): 2081-7. doi: 10.3174/ajnr.A3138 PMID: 22700750
- Wang X, Chen J, Mao Q, Liu Y, You C. Relationship between intracranial pressure and aneurysmal subarachnoid hemorrhage grades. J Neurol Sci 2014; 346(1-2): 284-7. doi: 10.1016/j.jns.2014.09.011 PMID: 25245175
- Ravishankar N, Nuoman R, Amuluru K, et al. Management strategies for intracranial pressure crises in subarachnoid hemorrhage. J Intensive Care Med 2020; 35(3): 211-8. doi: 10.1177/0885066618813073 PMID: 30514150
- Dodd WS, Laurent D, Dumont AS, et al. Pathophysiology of delayed cerebral ischemia after subarachnoid hemorrhage: A review. J Am Heart Assoc 2021; 10(15): e021845. doi: 10.1161/JAHA.121.021845 PMID: 34325514
- Whittle C, Hollingworth MA, Dulhanty L, Patel HC. What are the predictors of delayed cerebral ischaemia (DCI) after aneurysmal subarachnoid haemorrhage? An up-to-date systematic review. Acta Neurochir 2023; 165(12): 3643-50. doi: 10.1007/s00701-023-05864-4 PMID: 37968365
- Raatikainen E. Delayed cerebral ischemia and blood coagulation changes after aneurysmal subarachnoid hemorrhage. Doctoral program in medicine and life sciences, dissertation, tampere university, 2023.
- Darkwah Oppong M, Gümüs M, Pierscianek D, et al. Aneurysm rebleeding before therapy: A predictable disaster? J Neurosurg 2019; 131(5): 1473-80. doi: 10.3171/2018.7.JNS181119
- Otani N, Takasato Y, Masaoka H, et al. Surgical outcome following decompressive craniectomy for poor-grade aneurysmal subarachnoid hemorrhage in patients with associated massive intracerebral or Sylvian hematomas. Cerebrovasc Dis 2008; 26(6): 612-7. doi: 10.1159/000165115 PMID: 18946217
- Osborn JW, Fink GD. Region‐specific changes in sympathetic nerve activity in angiotensin IIsalt hypertension in the rat. Exp Physiol 2010; 95(1): 61-8. doi: 10.1113/expphysiol.2008.046326 PMID: 19717492
- Wilms H, Rosenstiel P, Unger T, Deuschl G, Lucius R. Neuroprotection with angiotensin receptor antagonists: A review of the evidence and potential mechanisms. Am J Cardiovasc Drug 2005; 5(4): 245-53. doi: 10.2165/00129784-200505040-00004
- Muller F, Lartaud I, Bray L, et al. Chronic treatment with the angiotensin I converting enzyme inhibitor, perindopril, restores the lower limit of autoregulation of cerebral blood flow in the awake renovascular hypertensive rat. J Hypertens 1990; 8(11): 1037-42. doi: 10.1097/00004872-199011000-00010 PMID: 1963186
- Manschot SM, Biessels GJ, Cameron NE, et al. Angiotensin converting enzyme inhibition partially prevents deficits in water maze performance, hippocampal synaptic plasticity and cerebral blood flow in streptozotocin-diabetic rats. Brain Res 2003; 966(2): 274-82. doi: 10.1016/S0006-8993(02)04211-7 PMID: 12618350
- Hatazawa J, Shimosegawa E, Osaki Y, et al. Long-term angiotensin-converting enzyme inhibitor perindopril therapy improves cerebral perfusion reserve in patients with previous minor stroke. Stroke 2004; 35(9): 2117-22. doi: 10.1161/01.STR.0000136034.86144.e9 PMID: 15256675
- Panahpour H, Dehghani GA, Bohlooli S. Enalapril attenuates ischaemic brain oedema and protects the bloodbrain barrier in rats via an anti‐oxidant action. Clin Exp Pharmacol Physiol 2014; 41(3): 220-6. doi: 10.1111/1440-1681.12210 PMID: 24471927
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