Abstract
One of the most serious complications after subarachnoid hemorrhage (SAH) is delayed cerebral ischemia, the cause of which is multifactorial. Delayed cerebral ischemia considerably worsens neurological outcome and increases the risk of death. The targets of hemodynamic management of SAH have widely changed over the past 30 years. Hypovolemia and hypotension were favored prior to the era of early aneurysmal surgery but were subsequently replaced by the use of hypervolemia and hypertension. More recently, the concept of goal-directed therapy targeting euvolemia, with or without hypertension, is gaining preference. Despite the evolving concepts and the vast literature, fundamental questions related to hemodynamic optimization and its effects on cerebral perfusion and patient outcomes remain unanswered. In this review, we explain the rationale underlying the approaches to hemodynamic management and provide guidance on contemporary strategies related to fluid administration and blood pressure and cardiac output manipulation in the management of SAH.
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Neifert SN, Chapman EK, Martini ML, Shuman WH, Schupper AJ, Oermann EK, et al. Aneurysmal subarachnoid hemorrhage: the last decade. Transl Stroke Res. 2021;12(3):428–46.
Lawton MT, Vates GE. Subarachnoid hemorrhage. N Engl J Med. 2017;377(3):257–66.
Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol. 2009;8(7):635–42.
Foreman B. The pathophysiology of delayed cerebral ischemia. J Clin Neurophysiol. 2016;33(3):174–82.
Dhar R, Scalfani MT, Blackburn S, Zazulia AR, Videen T, Diringer M. Relationship between angiographic vasospasm and regional hypoperfusion in aneurysmal subarachnoid hemorrhage. Stroke. 2012;43(7):1788–94.
Rabinstein AA, Weigand S, Atkinson JL, Wijdicks EF. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005;36(5):992–7.
Woitzik J, Dreier JP, Hecht N, Fiss I, Sandow N, Major S, et al. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2012;32(2):203–12.
Diringer MN, Bleck TP, Hemphill IJC, Menon D, Shutter L, Vespa P, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the neurocritical care society’s multidisciplinary consensus conference. Neurocrit Care. 2011;15(2):211–40.
Treggiari-Venzi MM, Suter PM, Romand JA. Review of medical prevention of vasospasm after aneurysmal subarachnoid hemorrhage: a problem of neurointensive care. Neurosurgery. 2001;48(2):249–61 (discussion 61–2).
Meyer R, Deem S, Yanez ND, Souter M, Lam A, Treggiari MM. Current practices of triple-H prophylaxis and therapy in patients with subarachnoid hemorrhage. Neurocrit Care. 2011;14(1):24–36.
Velly LJ, Bilotta F, Fabregas N, Soehle M, Bruder NJ, Nathanson MH, et al. Anaesthetic and ICU management of aneurysmal subarachnoid haemorrhage: a survey of European practice. Eur J Anaesthesiol. 2015;32(3):168–76.
Diringer MN, Bleck TP, Claude Hemphill J III, Menon D, Shutter L, Vespa P, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society’s multidisciplinary consensus conference. Neurocrit Care. 2011;15(2):211–40.
Committee for Guidelines for Management of Aneurysmal Subarachnoid Hemorrhage JSoSfCS. Evidence-based guidelines for the management of aneurysmal subarachnoid hemorrhage. English Edition. Neurol Med Chir (Tokyo). 2012;52(6):355–429.
Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, et al. 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):1711–37.
Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G, et al. European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis. 2013;35(2):93–112.
Cho WS, Kim JE, Park SQ, Ko JK, Kim DW, Park JC, et al. Korean clinical practice guidelines for aneurysmal subarachnoid hemorrhage. J Korean Neurosurg Soc. 2018;61(2):127–66.
Treggiari MM, Rabinstein AA, Busl KM, et al. Guidelines for the neurocritical care management of aneurysmal subarachnoid hemorrhage. Neurocrit Care 2023 In Press.
Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP. The international cooperative study on the timing of aneurysm surgery. Part 2: surgical results. J Neurosurg. 1990;73(1):37–47.
Wijdicks EF, Vermeulen M, Hijdra A, van Gijn J. Hyponatremia and cerebral infarction in patients with ruptured intracranial aneurysms: Is fluid restriction harmful? Ann Neurol. 1985;17(2):137–40.
Wijdicks EF, Vermeulen M, ten Haaf JA, Hijdra A, Bakker WH, van Gijn J. Volume depletion and natriuresis in patients with a ruptured intracranial aneurysm. Ann Neurol. 1985;18(2):211–6.
Solomon RA, Post KD, McMurtry JG. Depression of circulating blood volume in patients after subarachnoid hemorrhage: implications for the management of symptomatic vasospasm. Neurosurgery. 1984;15(3):354–61.
Rosenwasser RH, Delgado TE, Buchheit WA, Freed MH. Control of hypertension and prophylaxis against vasospasm in cases of subarachnoid hemorrhage: a preliminary report. Neurosurgery. 1983;12(6):658–61.
Hasan D, Vermeulen M, Wijdicks EF, Hijdra A, van Gijn J. Effect of fluid intake and antihypertensive treatment on cerebral ischemia after subarachnoid hemorrhage. Stroke. 1989;20(11):1511–5.
Vermeij FH, Hasan D, Bijvoet HW, Avezaat CJ. Impact of medical treatment on the outcome of patients after aneurysmal subarachnoid hemorrhage. Stroke. 1998;29(5):924–30.
Giannotta SL, McGillicuddy JE, Kindt GW. Diagnosis and treatment of postoperative cerebral vasospasm. Surg Neurol. 1977;8(4):286–90.
Kassell NF, Peerless SJ, Durward QJ, Beck DW, Drake CG, Adams HP. Treatment of ischemic deficits from vasospasm with intravascular volume expansion and induced arterial hypertension. Neurosurgery. 1982;11(3):337–43.
Awad IA, Carter LP, Spetzler RF, Medina M, Williams FC Jr. Clinical vasospasm after subarachnoid hemorrhage: response to hypervolemic hemodilution and arterial hypertension. Stroke. 1987;18(2):365–72.
Kosnik EJ, Hunt WE. Postoperative hypertension in the management of patients with intracranial arterial aneurysms. J Neurosurg. 1976;45(2):148–54.
Sen J, Belli A, Albon H, Morgan L, Petzold A, Kitchen N. Triple-H therapy in the management of aneurysmal subarachnoid haemorrhage. Lancet Neurol. 2003;2(10):614–21.
Archer DP, Shaw DA, Leblanc RL, Tranmer BI. Haemodynamic considerations in the management of patients with subarachnoid haemorrhage. Can J Anaesth. 1991;38(4 Pt 1):454–70.
Ekelund A, Reinstrup P, Ryding E, Andersson AM, Molund T, Kristiansson KA, et al. Effects of iso- and hypervolemic hemodilution on regional cerebral blood flow and oxygen delivery for patients with vasospasm after aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2002;144(7):703–12 (discussion 12–3).
Haley EC Jr, Kassell NF, Torner JC. The international cooperative study on the timing of aneurysm surgery. The North American experience. Stroke. 1992;23(2):205–14.
Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):1267–74.
Origitano TC, Wascher TM, Reichman OH, Anderson DE. Sustained increased cerebral blood flow with prophylactic hypertensive hypervolemic hemodilution (“triple-H” therapy) after subarachnoid hemorrhage. Neurosurgery. 1990;27(5):729–39 (discussion 39–40).
Levy ML, Giannotta SL. Cardiac performance indices during hypervolemic therapy for cerebral vasospasm. J Neurosurg. 1991;75(1):27–31.
Levy ML, Rabb CH, Zelman V, Giannotta SL. Cardiac performance enhancement from dobutamine in patients refractory to hypervolemic therapy for cerebral vasospasm. J Neurosurg. 1993;79(4):494–9.
Miller JA, Dacey RG Jr, Diringer MN. Safety of hypertensive hypervolemic therapy with phenylephrine in the treatment of delayed ischemic deficits after subarachnoid hemorrhage. Stroke. 1995;26(12):2260–6.
Solenski NJ, Haley EC Jr, Kassell NF, Kongable G, Germanson T, Truskowski L, et al. Medical complications of aneurysmal subarachnoid hemorrhage: a report of the multicenter, cooperative aneurysm study. Participants of the Multicenter Cooperative Aneurysm Study. Crit Care Med. 1995;23(6):1007–17.
Mayer SA, Solomon RA, Fink ME, Lennihan L, Stern L, Beckford A, et al. Effect of 5% albumin solution on sodium balance and blood volume after subarachnoid hemorrhage. Neurosurgery. 1998;42(4):759–67 (discussion 67–8).
Lennihan L, Mayer SA, Fink ME, Beckford A, Paik MC, Zhang H, et al. Effect of hypervolemic therapy on cerebral blood flow after subarachnoid hemorrhage: a randomized controlled trial. Stroke. 2000;31(2):383–91.
Egge A, Waterloo K, Sjoholm H, Solberg T, Ingebrigtsen T, Romner B. Prophylactic hyperdynamic postoperative fluid therapy after aneurysmal subarachnoid hemorrhage: a clinical, prospective, randomized, controlled study. Neurosurgery. 2001;49(3):593–6.
Togashi K, Joffe AM, Sekhar L, Kim L, Lam A, Yanez D, et al. Randomized pilot trial of intensive management of blood pressure or volume expansion in subarachnoid hemorrhage (IMPROVES). Neurosurgery. 2015;76(2):125–34 (discussion 34–5; quiz 35).
Joffe AM, Khandelwal N, Hallman MR, Treggiari MM. Assessment of circulating blood volume with fluid administration targeting euvolemia or hypervolemia. Neurocrit Care. 2015;22(1):82–8.
Gura M, Elmaci I, Cerci A, Sagiroglu E, Coskun KK. Haemodynamic augmentation in the treatment of vasospasm in aneurysmal subarachnoid hemorrhage. Turk Neurosurg. 2012;22(4):435–40.
Tagami T, Kuwamoto K, Watanabe A, Unemoto K, Yokobori S, Matsumoto G, et al. Effect of triple-h prophylaxis on global end-diastolic volume and clinical outcomes in patients with aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2014;21(3):462–9.
Jost SC, Diringer MN, Zazulia AR, Videen TO, Aiyagari V, Grubb RL, et al. Effect of normal saline bolus on cerebral blood flow in regions with low baseline flow in patients with vasospasm following subarachnoid hemorrhage. J Neurosurg. 2005;103(1):25–30.
Sakr Y, Dunisch P, Santos C, Matthes L, Zeidan M, Reinhart K, et al. Poor outcome is associated with less negative fluid balance in patients with aneurysmal subarachnoid hemorrhage treated with prophylactic vasopressor-induced hypertension. Ann Intensive Care. 2016;6(1):25.
Drevet CM, Opprecht N, Nadji A, Mirek S, Aho S, Ricolfi F, et al. Impact of restrictive fluid protocol on hypoxemia after aneurysmal subarachnoid hemorrhage. J Crit Care. 2017;42:152–6.
Bergmans B, Egal M, Van Bommel J, Bakker J, Van der Jagt M. Effects of cardiac output-guided hemodynamic management on fluid administration after aneurysmal subarachnoid hemorrhage. Crit Care. 2014;18(Suppl. 1):S163–4.
Metzelder SM, Coburn M, Stoppe C, Fries M, Simon TP, Reinges MHT, et al. Accuracy and precision of calibrated arterial pulse contour analysis in patients with subarachnoid hemorrhage requiring high-dose vasopressor therapy: a prospective observational clinical trial. Crit Care. 2014;18(1):R25.
Mutoh T, Kazumata K, Terasaka S, Taki Y, Suzuki A, Ishikawa T. Early intensive versus minimally invasive approach to postoperative hemodynamic management after subarachnoid hemorrhage. Stroke. 2014;45(5):1280–4.
Anetsberger A, Gempt J, Blobner M, Ringel F, Bogdanski R, Heim M, et al. Impact of goal-directed therapy on delayed ischemia after aneurysmal subarachnoid hemorrhage: randomized controlled trial. Stroke. 2020;51(8):2287–96.
Mutoh T, Ishikawa T, Nakase T, Suzuki A, Yasui N. Impact of early goal-directed hemodynamic optimization on clinical course and outcome after subarachnoid hemorrhage. Crit Care Med. 2009;37(12 Suppl.):A449.
Vergouw LJM, Egal M, Bergmans B, Dippel DWJ, Lingsma HF, Vergouwen MDI, et al. High early fluid input after aneurysmal subarachnoid hemorrhage: combined report of association with delayed cerebral ischemia and feasibility of cardiac output-guided fluid restriction. J Intensive Care Med. 2020;35(2):161–9.
Shikata E, Tamura T, Shinno K, Okayama Y, Shinohara N, Shimada K, et al. Importance of managing the water-electrolyte balance by delivering the optimal minimum amount of water and sodium after subarachnoid hemorrhage. World Neurosurg. 2019;129:e352–60.
Otsubo H, Takemae T, Inoue T, Kobayashi S, Sugita K. Normovolaemic induced hypertension therapy for cerebral vasospasm after subarachnoid haemorrhage. Acta Neurochir (Wien). 1990;103(1–2):18–26.
Budohoski KP, Guilfoyle M, Helmy A, Huuskonen T, Czosnyka M, Kirollos R, et al. The pathophysiology and treatment of delayed cerebral ischaemia following subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2014;85(12):1343–53.
Gathier CS, Van Den Bergh WM, Van Der Jagt M, Verweij BH, Dankbaar JW, Muller MC, et al. Induced hypertension for delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage a randomized clinical trial. Stroke. 2018;49(1):76–83.
Haegens NM, Gathier CS, Horn J, Coert BA, Verbaan D, Van Den Bergh WM. Induced hypertension in preventing cerebral infarction in delayed cerebral ischemia after Subarachnoid hemorrhage. Stroke. 2018;49(11):2630–6.
Rondeau N, Cinotti R, Rozec B, Roquilly A, Floch H, Groleau N, et al. Dobutamine-induced high cardiac index did not prevent vasospasm in subarachnoid hemorrhage patients: a randomized controlled pilot study. Neurocrit Care. 2012;17(2):183–90.
Lannes M, Zeiler F, Guichon C, Teitelbaum J. The use of milrinone in patients with delayed cerebral ischemia following subarachnoid hemorrhage: a systematic review. Can J Neurol Sci. 2017;44(2):152–60.
Soliman R, Zohry G. Effect of magnesium sulphate and milrinone on cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a randomized study. Brazilian Journal of Anesthesiology. 2019;69(1):64–71.
Lakhal K, Hivert A, Alexandre PL, Fresco M, Robert-Edan V, Rodie-Talbere PA, et al. Intravenous milrinone for cerebral vasospasm in subarachnoid hemorrhage: the milrispasm controlled before-after study. Neurocrit Care. 2021;35(3):669–79.
Muizelaar JP, Becker DP. Induced hypertension for the treatment of cerebral ischemia after subarachnoid haemorrhage. Direct effect on cerebral blood flow. Surg Neurol. 1986;25(4):317–25.
Muench E, Horn P, Bauhuf C, Roth H, Philipps M, Hermann P, et al. Effects of hypervolemia and hypertension on regional cerebral blood flow, intracranial pressure, and brain tissue oxygenation after subarachnoid hemorrhage. Crit Care Med. 2007;35(8):1844–51.
Gathier CS, Dankbaar JW, van der Jagt M, Verweij BH, Oldenbeuving AW, Rinkel GJ, et al. Effects of induced hypertension on cerebral perfusion in delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: a randomized clinical trial. Stroke. 2015;46(11):3277–81.
Diringer MN, Dhar R, Scalfani M, Zazulia AR, Chicoine M, Powers WJ, et al. Effect of high-dose simvastatin on cerebral blood flow and static autoregulation in subarachnoid hemorrhage. Neurocrit Care. 2016;25(1):56–63.
Joseph M, Ziadi S, Nates J, Dannenbaum M, Malkoff M. Increases in cardiac output can reverse flow deficits from vasospasm independent of blood pressure: a study using xenon computed tomographic measurement of cerebral blood flow. Neurosurgery. 2003;53(5):1044–51 (discussion 51–2).
Raabe A, Beck J, Keller M, Vatter H, Zimmermann M, Seifert V. Relative importance of hypertension compared with hypervolemia for increasing cerebral oxygenation in patients with cerebral vasospasm after subarachnoid hemorrhage. J Neurosurg. 2005;103(6):974–81.
Rass V, Bogossian EG, Ianosi BA, Peluso L, Kofler M, Lindner A, et al. The effect of the volemic and cardiac status on brain oxygenation in patients with subarachnoid hemorrhage: a bi-center cohort study. Ann Intensive Care. 2021;11(1):176.
Meyer R, Deem S, David Yanez N, Souter M, Lam A, Treggiari MM. Current practices of triple-H prophylaxis and therapy in patients with subarachnoid hemorrhage. Neurocrit Care. 2011;14(1):24–36.
Angermann M, Jablawi F, Keulers A, Angermann M, Schubert GA, Weiss M, et al. Posterior reversible encephalopathy syndrome after induced hypertension therapy for delayed cerebral ischemia after subarachnoid hemorrhage: a case-control study. J Neurol Sci. 2021;421:117313.
Elsamadicy AA, Koo AB, Reeves BC, Sujijantarat N, David WB, Malhotra A, et al. Posterior reversible encephalopathy syndrome caused by induced hypertension to treat cerebral vasospasm secondary to aneurysmal subarachnoid hemorrhage. World Neurosurg. 2020;143:e309–23.
Allen ML, Kulik T, Keyrouz SG, Dhar R. Posterior reversible encephalopathy syndrome as a complication of induced hypertension in subarachnoid hemorrhage: a case-control study. Neurosurgery. 2019;85(2):223–30.
Dhar R, Allen M, Kulik T, Keyrouz S. Posterior reversible encephalopathy syndrome as a complication of induced hypertension in subarachnoid hemorrhage: A case-control study. Neurocritical Care. 2017;27(2 Supplement 1):S392.
Muhammad S, Guresir A, Greschus S, Scorzin J, Vatter H, Guresir E. Posterior reversible encephalopathy syndrome as an overlooked complication of induced hypertension for cerebral vasospasm: systematic review and illustrative case. Stroke. 2016;47(2):519–22.
Awori J, Rajajee V, Gemmete JJ, Chaudhary N, Thompson BG, Pandey AS. Posterior reversible encephalopathy syndrome following hemodynamic treatment of aneurysmal subarachnoid hemorrhage-induced vasospasm. J Clin Neurosci. 2016;26:33–6.
Giraldo EA, Fugate JE, Rabinstein AA, Lanzino G, Wijdicks EF. Posterior reversible encephalopathy syndrome associated with hemodynamic augmentation in aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2011;14(3):427–32.
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Steven Deem reports no conflicts of interest or disclosures. Michael Diringer reports no conflicts of interest or disclosures. Sarah Livesay has received consulting fees from Lombardi Hill/Stroke Challenges, has received payment for expert testimony, has received support for attending meetings and/or travel from the Neurocritical Care Society, and has a leadership position in the Neurocritical Care Society. Miriam Treggiari has received grant funding from the National Institutes of Health and the Department of Defense.
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Deem, S., Diringer, M., Livesay, S. et al. Hemodynamic Management in the Prevention and Treatment of Delayed Cerebral Ischemia After Aneurysmal Subarachnoid Hemorrhage. Neurocrit Care 39, 81–90 (2023). https://doi.org/10.1007/s12028-023-01738-w
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DOI: https://doi.org/10.1007/s12028-023-01738-w