Top

Acta Neurochirurgica

Published in:

Open Access 01-12-2020 | Ruptured Aneurysm | Original Article - Vascular Neurosurgery - Aneurysm

Impact of smoking on course and outcome of aneurysmal subarachnoid hemorrhage

Authors: H. Slettebø, T. Karic, A. Sorteberg

Published in: Acta Neurochirurgica | Issue 12/2020

Abstract

Background

While the smoking-related risk of experiencing an aneurysmal subarachnoid hemorrhage (aSAH) is well established, it remains unclear whether smoking has an unexpected “protective effect” in aSAH, or if smokers are more at risk for complications and poor outcomes.

Methods

Prospective, observational study investigating the course and outcome of aSAH in patients admitted during the years 2011 and 2012. Smoking status at admittance, demographic, medical, and radiological variables were registered along with management, complications, and outcome at 1 year in terms of mortality, modified Rankin score, and Glasgow outcome score extended. We compared current smokers with nonsmokers on group level and by paired analysis matched by aSAH severity, age, and severity of vasospasm.

Results

We included 237 patients, thereof 138 current smokers (58.2%). Seventy-four smoker/nonsmoker pairs were matched. Smokers presented more often in poor clinical grade, had less subarachnoid blood, and were younger than nonsmokers. Ruptured aneurysms were larger, and multiple aneurysms more common in smokers. Severe multi-vessel vasospasm was less frequent in smokers, whereas all other complications occurred at similar rates. Mortality at 30 days was lower in smokers and functional outcome was similar in smokers and nonsmokers. Poor clinical grade, age, cerebral infarction, and vertebrobasilar aneurysms were independent predictors of 1-year mortality and of poor functional outcome. Serious comorbidity was a predictor of 1-year mortality. Smoking did not predict mortality or poor functional outcome.

Conclusions

Notwithstanding clinically more severe aSAH, smokers developed less frequently severe vasospasm and had better outcome than expected. The risk for complications after aSAH is not increased in smokers.

Ali SF, Smith EE, Bhatt DL, Fonarow GC, Schwamm LH (2013) Paradoxical association of smoking with in-hospital mortality among patients admitted with acute ischemic stroke. J Am Heart Assoc 2:e000171. https://doi.org/10.1161/JAHA.113.000171CrossRef

Anderson GB, Ashforth R, Steinke DE, Findlay JM (2000) CT angiography for the detection of cerebral vasospasm in patients with acute subarachnoid hemorrhage. AJNR Am J Neuroradiol 21:1011–1015

Bonita R, Beaglehole R (1988) Recovery of motor function after stroke. Stroke 19:1497–1500. https://doi.org/10.1161/01.str.19.12.1497CrossRef

Bradford ST, Stamatovic SM, Dondeti RS, Keep RF, Andjelkovic AV (2011) Nicotine aggravates the brain postischemic inflammatory response. Am J Physiol Heart Circ Physiol 300:H1518–H1529. https://doi.org/10.1152/ajpheart.00928.2010CrossRef

Can A, Castro VM, Ozdemir YH, Dagen S, Yu S, Dligach D, Finan S, Gainer V, Shadick NA, Murphy S, Cai T, Savova G, Dammers R, Weiss ST, Du R (2017) Association of intracranial aneurysm rupture with smoking duration, intensity, and cessation. Neurology 89:1408–1415. https://doi.org/10.1212/WNL.0000000000004419CrossRef

Crobeddu E, Mittal MK, Dupont S, Wijdicks EF, Lanzino G, Rabinstein AA (2012) Predicting the lack of development of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke 43:697–701. https://doi.org/10.1161/STROKEAHA.111.638403CrossRef

Dasenbrock HH, Rudy RF, Rosalind Lai PM, Smith TR, Frerichs KU, Gormley WB, Aziz-Sultan MA, Du R (2018) Cigarette smoking and outcomes after aneurysmal subarachnoid hemorrhage: a nationwide analysis. J Neurosurg 129:446–457. https://doi.org/10.3171/2016.10.JNS16748CrossRef

de Rooij NK, Rinkel GJ, Dankbaar JW, Frijns CJ (2013) Delayed cerebral ischemia after subarachnoid hemorrhage: a systematic review of clinical, laboratory, and radiological predictors. Stroke 44:43–54. https://doi.org/10.1161/STROKEAHA.112.674291CrossRef

Eide PK, Bentsen G, Sorteberg AG, Marthinsen PB, Stubhaug A, Sorteberg W (2011) A randomized and blinded single-center trial comparing the effect of intracranial pressure and intracranial pressure wave amplitude-guided intensive care management on early clinical state and 12-month outcome in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery 69:1105–1115. https://doi.org/10.1227/NEU.0b013e318227e0e1CrossRef

10.

Ellamushi HE, Grieve JP, Jager HR, Kitchen ND (2001) Risk factors for the formation of multiple intracranial aneurysms. J Neurosurg 94:728–732. https://doi.org/10.3171/jns.2001.94.5.0728CrossRef

11.

Etminan N, Beseoglu K, Steiger HJ, Hanggi D (2011) The impact of hypertension and nicotine on the size of ruptured intracranial aneurysms. J Neurol Neurosurg Psychiatry 82:4–7. https://doi.org/10.1136/jnnp.2009.199661CrossRef

12.

Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ES Jr, MacDonald RL, Mayer SA (2006) Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery 59:21–27; discussion 21-27. https://doi.org/10.1227/01.NEU.0000218821.34014.1BCrossRef

13.

Haass M, Kubler W (1997) Nicotine and sympathetic neurotransmission. Cardiovasc Drugs Ther 10:657–665. https://doi.org/10.1007/BF00053022CrossRef

14.

Hammer A, Steiner A, Ranaie G, Yakubov E, Erbguth F, Hammer CM, Killer-Oberpfalzer M, Steiner H, Janssen H (2018) Impact of comorbidities and smoking on the outcome in aneurysmal subarachnoid hemorrhage. Sci Rep 8:12335. https://doi.org/10.1038/s41598-018-30878-9CrossRef

15.

Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE (2002) Immediate administration of tranexamic acid and reduced incidence of early rebleeding after aneurysmal subarachnoid hemorrhage: a prospective randomized study. J Neurosurg 97:771–778. https://doi.org/10.3171/jns.2002.97.4.0771CrossRef

16.

Ho AL, Lin N, Frerichs KU, Du R (2015) Smoking and intracranial aneurysm morphology. Neurosurgery 77:59–66; discussion 66. https://doi.org/10.1227/NEU.0000000000000735CrossRef

17.

Inagawa T (2016) Risk factors for cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a review of the literature. World Neurosurg 85:56–76. https://doi.org/10.1016/j.wneu.2015.08.052CrossRef

18.

Jimenez Caballero PE, Lopez Espuela F, Portilla Cuenca JC, Ramirez Moreno JM, Pedrera Zamorano JD, Casado Naranjo I (2013) Charlson comorbidity index in ischemic stroke and intracerebral hemorrhage as predictor of mortality and functional outcome after 6 months. J Stroke Cerebrovasc Dis 22:e214–e218. https://doi.org/10.1016/j.jstrokecerebrovasdis.2012.11.014CrossRef

19.

Juvela S (2000) Risk factors for multiple intracranial aneurysms. Stroke 31:392–397. https://doi.org/10.1161/01.str.31.2.392CrossRef

20.

Juvela S (2001) Cigarette smoking and death following subarachnoid hemorrhage. J Neurosurg 95:551–554. https://doi.org/10.3171/jns.2001.95.4.0551CrossRef

21.

Juvela S, Porras M, Poussa K (2008) Natural history of unruptured intracranial aneurysms: probability of and risk factors for aneurysm rupture. J Neurosurg 108:1052–1060. https://doi.org/10.3171/JNS/2008/108/5/1052CrossRef

22.

Kim CK, Kim BJ, Ryu WS, Lee SH, Yoon BW (2012) Impact of smoking cessation on the risk of subarachnoid haemorrhage: a nationwide multicentre case control study. J Neurol Neurosurg Psychiatry 83:1100–1103. https://doi.org/10.1136/jnnp-2012-302538CrossRef

23.

Konczalla J, Seifert V, Beck J, Guresir E, Vatter H, Raabe A, Marquardt G (2018) Outcome after Hunt and Hess grade V subarachnoid hemorrhage: a comparison of pre-coiling era (1980-1995) versus post-ISAT era (2005-2014). J Neurosurg 128:100–110. https://doi.org/10.3171/2016.8.JNS161075CrossRef

24.

Korja M, Lehto H, Juvela S, Kaprio J (2016) Incidence of subarachnoid hemorrhage is decreasing together with decreasing smoking rates. Neurology 87:1118–1123. https://doi.org/10.1212/WNL.0000000000003091CrossRef

25.

Kostrzewa RM, Segura-Aguilar J (2003) Novel mechanisms and approaches in the study of neurodegeneration and neuroprotection. A review. Neurotox Res 5:375–383. https://doi.org/10.1007/bf03033166CrossRef

26.

Krishnamurthy S, Kelleher JP, Lehman EB, Cockroft KM (2007) Effects of tobacco dose and length of exposure on delayed neurological deterioration and overall clinical outcome after aneurysmal subarachnoid hemorrhage. Neurosurgery 61:475–480; discussion 480-471. https://doi.org/10.1227/01.NEU.0000290892.46954.12CrossRef

27.

Lantigua H, Ortega-Gutierrez S, Schmidt JM, Lee K, Badjatia N, Agarwal S, Claassen J, Connolly ES, Mayer SA (2015) Subarachnoid hemorrhage: who dies, and why? Crit Care 19:309. https://doi.org/10.1186/s13054-015-1036-0CrossRef

28.

Lasner TM, Weil RJ, Riina HA, King JT Jr, Zager EL, Raps EC, Flamm ES (1997) Cigarette smoking-induced increase in the risk of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg 87:381–384. https://doi.org/10.3171/jns.1997.87.3.0381CrossRef

29.

LeRoux PD, Haglund MM, Newell DW, Grady MS, Winn HR (1992) Intraventricular hemorrhage in blunt head trauma: an analysis of 43 cases. Neurosurgery 31:678–684; discussion 684-675. https://doi.org/10.1227/00006123-199210000-00010CrossRef

30.

Lindbohm JV, Kaprio J, Jousilahti P, Salomaa V, Korja M (2016) Sex, smoking, and risk for subarachnoid hemorrhage. Stroke 47:1975–1981. https://doi.org/10.1161/STROKEAHA.116.012957CrossRef

31.

Lindbohm JV, Kaprio J, Korja M (2019) Survival bias explains improved survival in smokers and hypertensive individuals after aSAH. Neurology 93:e2105–e2109. https://doi.org/10.1212/WNL.0000000000008537CrossRef

32.

Lindegaard KF, Bakke SJ, Sorteberg W, Nakstad P, Nornes H (1986) A non-invasive Doppler ultrasound method for the evaluation of patients with subarachnoid hemorrhage. Acta Radiol Suppl 369:96–98

33.

Lindekleiv H, Sandvei MS, Njolstad I, Lochen ML, Romundstad PR, Vatten L, Ingebrigtsen T, Vik A, Mathiesen EB (2011) Sex differences in risk factors for aneurysmal subarachnoid hemorrhage: a cohort study. Neurology 76:637–643. https://doi.org/10.1212/WNL.0b013e31820c30d3CrossRef

34.

Longstreth WT Jr, Nelson LM, Koepsell TD, van Belle G (1992) Cigarette smoking, alcohol use, and subarachnoid hemorrhage. Stroke 23:1242–1249. https://doi.org/10.1161/01.str.23.9.1242CrossRef

35.

Mendes M (2018) The smoker’s paradox: not an argument against quitting smoking after acute coronary syndrome. Rev Port Cardiol 37:857–858. https://doi.org/10.1016/j.repc.2018.09.003CrossRef

36.

Michalak SM, Rolston JD, Lawton MT (2016) Incidence and predictors of complications and mortality in cerebrovascular surgery: national trends from 2007 to 2012. Neurosurgery 79:182–193. https://doi.org/10.1227/NEU.0000000000001251CrossRef

37.

Mijiti M, Mijiti P, Axier A, Amuti M, Guohua Z, Xiaojiang C, Kadeer K, Xixian W, Geng D, Maimaitili A (2016) Incidence and predictors of angiographic vasospasm, symptomatic vasospasm and cerebral infarction in Chinese patients with aneurysmal subarachnoid hemorrhage. PLoS One 11:e0168657. https://doi.org/10.1371/journal.pone.0168657CrossRef

38.

Milman N, Pedersen AN (2009) Blood haemoglobin concentrations are higher in smokers and heavy alcohol consumers than in non-smokers and abstainers: should we adjust the reference range? Ann Hematol 88:687–694. https://doi.org/10.1007/s00277-008-0647-9CrossRef

39.

Musallam KM, Rosendaal FR, Zaatari G, Soweid A, Hoballah JJ, Sfeir PM, Zeineldine S, Tamim HM, Richards T, Spahn DR, Lotta LA, Peyvandi F, Jamali FR (2013) Smoking and the risk of mortality and vascular and respiratory events in patients undergoing major surgery. JAMA Surg 148:755–762. https://doi.org/10.1001/jamasurg.2013.2360CrossRef

40.

Naidech AM, Drescher J, Ault ML, Shaibani A, Batjer HH, Alberts MJ (2006) Higher hemoglobin is associated with less cerebral infarction, poor outcome, and death after subarachnoid hemorrhage. Neurosurgery 59:775–779; discussion 779-780. https://doi.org/10.1227/01.NEU.0000232662.86771.A9CrossRef

41.

Nornes H (1973) The role of intracranial pressure in the arrest of hemorrhage in patients with ruptured intracranial aneurysm. J Neurosurg 39:226–234. https://doi.org/10.3171/jns.1973.39.2.0226CrossRef

42.

Ohkuma H, Tsurutani H, Suzuki S (2001) Incidence and significance of early aneurysmal rebleeding before neurosurgical or neurological management. Stroke 32:1176–1180. https://doi.org/10.1161/01.str.32.5.1176CrossRef

43.

Pegoli M, Mandrekar J, Rabinstein AA, Lanzino G (2015) Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 122:414–418. https://doi.org/10.3171/2014.10.JNS14290CrossRef

44.

Pobereskin LH (2001) Influence of premorbid factors on survival following subarachnoid hemorrhage. J Neurosurg 95:555–559. https://doi.org/10.3171/jns.2001.95.4.0555CrossRef

45.

Qureshi AI, Sung GY, Suri MF, Straw RN, Guterman LR, Hopkins LN (2000) Factors associated with aneurysm size in patients with subarachnoid hemorrhage: effect of smoking and aneurysm location. Neurosurgery 46:44–50

46.

Qureshi AI, Suri MF, Yahia AM, Suarez JI, Guterman LR, Hopkins LN, Tamargo RJ (2001) Risk factors for subarachnoid hemorrhage. Neurosurgery 49:607–612; discussion 612-603. https://doi.org/10.1097/00006123-200109000-00014CrossRef

47.

Ravikumar R, Flora G, Geddes JW, Hennig B, Toborek M (2004) Nicotine attenuates oxidative stress, activation of redox-regulated transcription factors and induction of proinflammatory genes in compressive spinal cord trauma. Brain Res Mol Brain Res 124:188–198. https://doi.org/10.1016/j.molbrainres.2004.02.018CrossRef

48.

Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale (1988) J Neurosurg 68:985–986. https://doi.org/10.3171/jns.1988.68.6.0985CrossRef

49.

Rosseland LA, Narum J, Stubhaug A, Kongsgaard U, Sorteberg W, Sorteberg A (2015) The effect of tracheotomy on drug consumption in patients with acute aneurysmal subarachnoid hemorrhage: an observational study. BMC Anesthesiol 15:47. https://doi.org/10.1186/s12871-015-0029-5CrossRef

50.

Sandvei MS, Romundstad PR, Muller TB, Vatten L, Vik A (2009) Risk factors for aneurysmal subarachnoid hemorrhage in a prospective population study: the HUNT study in Norway. Stroke 40:1958–1962. https://doi.org/10.1161/STROKEAHA.108.539544CrossRef

51.

Sandvei MS, Mathiesen EB, Vatten LJ, Muller TB, Lindekleiv H, Ingebrigtsen T, Njolstad I, Wilsgaard T, Lochen ML, Vik A, Romundstad PR (2011) Incidence and mortality of aneurysmal subarachnoid hemorrhage in two Norwegian cohorts, 1984-2007. Neurology 77:1833–1839. https://doi.org/10.1212/WNL.0b013e3182377de3CrossRef

52.

Schatlo B, Gautschi OP, Friedrich CM, Ebeling C, Jagersberg M, Kulcsar Z, Pereira VM, Schaller K, Bijlenga P (2019) Association of single and multiple aneurysms with tobacco abuse: an @neurIST risk analysis. Neurosurg Focus 47:E9. https://doi.org/10.3171/2019.4.FOCUS19130CrossRef

53.

Skodvin TO, Johnsen LH, Gjertsen O, Isaksen JG, Sorteberg A (2017) Cerebral aneurysm morphology before and after rupture: nationwide case series of 29 aneurysms. Stroke 48:880–886. https://doi.org/10.1161/STROKEAHA.116.015288CrossRef

54.

Sorteberg W, Slettebo H, Eide PK, Stubhaug A, Sorteberg A (2008) Surgical treatment of aneurysmal subarachnoid haemorrhage in the presence of 24-h endovascular availability: management and results. Br J Neurosurg 22:53–62. https://doi.org/10.1080/02688690701593553CrossRef

55.

Sorteberg A, Bredmose PP, Hansen AE, Sorteberg W (2019) The path from ictus to neurosurgery: chronology and transport logistics of patients with aneurysmal subarachnoid haemorrhage in the south-eastern Norway health region. Acta Neurochir 161:1497–1506. https://doi.org/10.1007/s00701-019-03971-9CrossRef

56.

St Jean P, Hart B, Webster M, Steed D, Adamson J, Powell J, Ferrell R (1996) Alpha-1-antitrypsin deficiency in aneurysmal disease. Hum Hered 46:92–97. https://doi.org/10.1159/000154333CrossRef

57.

van der Mark M, Nijssen PC, Vlaanderen J, Huss A, Mulleners WM, Sas AM, van Laar T, Kromhout H, Vermeulen R (2014) A case-control study of the protective effect of alcohol, coffee, and cigarette consumption on Parkinson disease risk: time-since-cessation modifies the effect of tobacco smoking. PLoS One 9:e95297. https://doi.org/10.1371/journal.pone.0095297CrossRef

58.

Vollset SE, Tverdal A, Gjessing HK (2006) Smoking and deaths between 40 and 70 years of age in women and men. Ann Intern Med 144:381–389. https://doi.org/10.7326/0003-4819-144-6-200603210-00004CrossRef

59.

Weir BK, Kongable GL, Kassell NF, Schultz JR, Truskowski LL, Sigrest A (1998) Cigarette smoking as a cause of aneurysmal subarachnoid hemorrhage and risk for vasospasm: a report of the Cooperative Aneurysm Study. J Neurosurg 89:405–411. https://doi.org/10.3171/jns.1998.89.3.0405CrossRef

60.

Wilson JT, Pettigrew LE, Teasdale GM (1998) Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use. J Neurotrauma 15:573–585. https://doi.org/10.1089/neu.1998.15.573CrossRef

61.

Xia N, Liu Y, Zhong M, Zhuge Q, Fan L, Chen W, Yang Y, Zhao B (2016) Smoking associated with increased aneurysm size in patients with anterior communicating artery aneurysms. World Neurosurg 87:155–161. https://doi.org/10.1016/j.wneu.2015.11.094CrossRef

62.

Zheng K, Zhong M, Zhao B, Chen SY, Tan XX, Li ZQ, Xiong Y, Duan CZ (2019) Poor-grade aneurysmal subarachnoid hemorrhage: risk factors affecting clinical outcomes in intracranial aneurysm patients in a multi-center study. Front Neurol 10:123. https://doi.org/10.3389/fneur.2019.00123CrossRef

Title: Impact of smoking on course and outcome of aneurysmal subarachnoid hemorrhage
Authors: H. Slettebø
T. Karic
A. Sorteberg
Publication date: 01-12-2020
Publisher: Springer Vienna
Keywords: Ruptured Aneurysm
Intracranial Aneurysm
Subarachnoid Hemorrhage
Aneurysm
Aneurysm
Subarachnoid Hemorrhage
Published in: Acta Neurochirurgica / Issue 12/2020
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-020-04506-3

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Impact of smoking on course and outcome of aneurysmal subarachnoid hemorrhage

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 12/2020

Early surgery for superficial supratentorial spontaneous intracerebral hemorrhage: a Finnish Intensive Care Consortium study

A capillary hemangioma of lobular subtype (pyogenic granuloma) in the calvarium of a pregnant woman

Time course of neurological deficits after surgery for primary brain tumours

Letter to the editor regarding: “High prevalence of pro-thrombotic conditions in adult patients with moyamoya disease and moyamoya syndrome: a single center study”

Circumdural extension of perineural spread leading to bilateral disease in neurolymphomatosis

Introductions of technological innovations in neurosurgery