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01-10-2018 | Original Article

Factors associated with clinical and radiological status on admission in patients with aneurysmal subarachnoid hemorrhage

Authors: Daniel W. Zumofen, Michel Roethlisberger, Rita Achermann, Schatlo Bawarjan, Martin N. Stienen, Christian Fung, Donato D’Alonzo, Nicolai Maldaner, Andrea Ferrari, Marco V. Corniola, Daniel Schoeni, Johannes Goldberg, Daniele Valsecchi, Thomas Robert, Rodolfo Maduri, Martin Seule, Jan-Karl Burkhardt, Serge Marbacher, Philippe Bijlenga, Kristine A. Blackham, Heiner C. Bucher, Luigi Mariani, Raphael Guzman, on behalf of the Swiss SOS Study Group

Published in: Neurosurgical Review | Issue 4/2018

Abstract

Grading scales yield objective measure of the severity of aneurysmal subarachnoid hemorrhage and serve as to guide treatment decisions and for prognostication. The purpose of this cohort study was to determine what factors govern a patient’s disease-specific admission scores in a representative Central European cohort. The Swiss Study of Subarachnoid Hemorrhage includes anonymized data from all tertiary referral centers serving subarachnoid hemorrhage patients in Switzerland. The 2009–2014 dataset was used to evaluate the impact of patient and aneurysm characteristics on the patients’ status at admission using descriptive and multivariate regression analysis. The primary/co-primary endpoints were the GCS and the WFNS grade. The secondary endpoints were the Fisher grade, the presence of a thick cisternal or ventricular clot, the presence of a new focal neurological deficit or cranial nerve palsy, and the patient’s intubation status. In our cohort of 1787 consecutive patients, increasing patient age by 10 years and low pre-ictal functional status (mRS 3–5) were inversely correlated with “high” GCS score (GCS ≥ 13) (OR 0.91, 95% CI 0.84–0.97 and OR 0.67, 95% CI 0.31–1.46), “low” WFNS grade (grade VI–V) (OR 1.21, 95% CI 1.04–1.20 and OR 1.47, 95% CI 0.66–3.27), and high Fisher grade (grade III–IV) (OR 1.08, 95% CI 1.00–1.17 and OR 1.54, 95% CI 0.55–4.32). Other independent predictors for the patients’ clinical and radiological condition at admission were the ruptured aneurysms’ location and its size. In sum, chronological age and pre-ictal functional status, as well as the ruptured aneurysm’s location and size, determine the patients’ clinical and radiological condition at admission to the tertiary referral hospital.

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de Rooij NK, Linn FH, van der Plas JA, Algra A, Rinkel GJ (2007) Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends. J Neurol Neurosurg Psychiatry 78(12):1365–1372. https://doi.org/10.1136/jnnp.2007.117655 CrossRefPubMedPubMedCentral

Ingall T, Asplund K, Mahonen M, Bonita R (2000) A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke 31(5):1054–1061. https://doi.org/10.1161/01.STR.31.5.1054 CrossRefPubMed

Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29(1):251–256. https://doi.org/10.1161/01.STR.29.1.251 CrossRefPubMed

Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R, International Subarachnoid Aneurysm Trial Collaborative G (2002) International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360(9342):1267–1274. https://doi.org/10.1016/S0140-6736(02)11314-6 CrossRefPubMed

Mugikura S, Takahashi S, Higano S, Shirane R, Sakurai Y, Yamada S (2002) Predominant involvement of ipsilateral anterior and posterior circulations in moyamoya disease. Stroke 33(6):1497–1500. https://doi.org/10.1161/01.STR.0000016828.62708.21 CrossRefPubMed

Salary M, Quigley MR, Wilberger JE Jr (2007) Relation among aneurysm size, amount of subarachnoid blood, and clinical outcome. J Neurosurg 107(1):13–17. https://doi.org/10.3171/JNS-07/07/0013 CrossRefPubMed

Lanzino G, Kassell NF, Germanson TP, Kongable GL, Truskowski LL, Torner JC, Jane JA (1996) Age and outcome after aneurysmal subarachnoid hemorrhage: why do older patients fare worse? J Neurosurg 85(3):410–418. https://doi.org/10.3171/jns.1996.85.3.0410 CrossRefPubMed

Wostrack M, Sandow N, Vajkoczy P, Schatlo B, Bijlenga P, Schaller K, Kehl V, Harmening K, Ringel F, Ryang YM, Friedrich B, Stoffel M, Meyer B (2013) Subarachnoid haemorrhage WFNS grade V: is maximal treatment worthwhile? Acta Neurochir 155(4):579–586. https://doi.org/10.1007/s00701-013-1634-z CrossRefPubMed

Rosen DS, Macdonald RL (2005) Subarachnoid hemorrhage grading scales: a systematic review. Neurocrit Care 2(2):110–118. https://doi.org/10.1385/NCC:2:2:110 CrossRefPubMed

10.

Jaja BNR, Cusimano MD, Etminan N, Hanggi D, Hasan D, Ilodigwe D, Lantigua H, Le Roux P, Lo B, Louffat-Olivares A et al (2013) Clinical prediction models for aneurysmal subarachnoid hemorrhage: a systematic review. Neurocrit Care 18(1):143–153. https://doi.org/10.1007/s12028-012-9792-z CrossRefPubMed

11.

Teasdale GM, Drake CG, Hunt W, Kassell N, Sano K, Pertuiset B, De Villiers JC (1988) A universal subarachnoid hemorrhage scale: report of a committee of the world federation of neurosurgical societies. J Neurol Neurosurg Psychiatry 51(11):1457. https://doi.org/10.1136/jnnp.51.11.1457 CrossRefPubMedPubMedCentral

12.

Teasdale G, Jennett B (1974) Assessment of coma and impaired consciousness. A practical scale. Lancet 2(7872):81–84CrossRefPubMed

13.

van Heuven AW, Dorhout Mees SM, Algra A, Rinkel GJ (2008) Validation of a prognostic subarachnoid hemorrhage grading scale derived directly from the Glasgow coma scale. Stroke 39(4):1347–1348. https://doi.org/10.1161/STROKEAHA.107.498345 CrossRefPubMed

14.

Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6(1):1–9. https://doi.org/10.1227/00006123-198001000-00001 CrossRefPubMed

15.

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(1):21–27; discussion 21-27. https://doi.org/10.1227/01.NEU.0000218821.34014.1B CrossRefPubMed

16.

Vale FL, Bradley EL, Fisher WS 3rd (1997) The relationship of subarachnoid hemorrhage and the need for postoperative shunting. J Neurosurg 86(3):462–466. https://doi.org/10.3171/jns.1997.86.3.0462 CrossRefPubMed

17.

Demirgil BT, Tugcu B, Postalci L, Guclu G, Dalgic A, Oral Z (2003) Factors leading to hydrocephalus after aneurysmal subarachnoid hemorrhage. Minim Invasive Neurosurg 46(6):344–348. https://doi.org/10.1055/s-2003-812500 CrossRefPubMed

18.

Mocco J, Ransom ER, Komotar RJ, Schmidt JM, Sciacca RR, Mayer SA, Connolly ES Jr (2006) Preoperative prediction of long-term outcome in poor-grade aneurysmal subarachnoid hemorrhage. Neurosurgery 59(3):529–538; discussion 529-538. https://doi.org/10.1227/01.NEU.0000228680.22550.A2 CrossRefPubMed

19.

Rosen DS, Macdonald RL (2004) Grading of subarachnoid hemorrhage: modification of the world World Federation of Neurosurgical Societies scale on the basis of data for a large series of patients. Neurosurgery 54(3):566–575; discussion 575-566. https://doi.org/10.1227/01.NEU.0000108862.32404.A5 CrossRefPubMed

20.

Taki W, Sakai N, Suzuki H, Group P (2011) Determinants of poor outcome after aneurysmal subarachnoid hemorrhage when both clipping and coiling are available: Prospective Registry of Subarachnoid Aneurysms Treatment (PRESAT) in Japan. World Neurosurg 76(5):437–445. https://doi.org/10.1016/j.wneu.2011.04.026 CrossRefPubMed

21.

Lagares A, Gómez PA, Lobato RD, Alén JF, Alday R, Campollo J (2001) Prognostic factors on hospital admission after spontaneous subarachnoid haemorrhage. Acta Neurochir 143(7):665–672. https://doi.org/10.1007/s007010170044 CrossRefPubMed

22.

Pierot L, Cognard C, Anxionnat R, Ricolfi F, Investigators C (2010) Ruptured intracranial aneurysms: factors affecting the rate and outcome of endovascular treatment complications in a series of 782 patients (CLARITY study). Radiology 256(3):916–923. https://doi.org/10.1148/radiol.10092209 CrossRefPubMed

23.

Ruiz-Sandoval JL, Cantu C, Chiquete E, Leon-Jimenez C, Arauz A, Murillo-Bonilla LM, Villarreal-Careaga J, Barinagarrementeria F, Investigators R (2009) Aneurysmal subarachnoid hemorrhage in a Mexican multicenter registry of cerebrovascular disease: the RENAMEVASC study. J Stroke Cerebrovasc Dis 18(1):48–55. https://doi.org/10.1016/j.jstrokecerebrovasdis.2008.09.019 CrossRefPubMed

24.

Lagares A, de Toledo P, Fernandez-Alen JA, Ibanez J, Arikan F, Sarabia R, Ballenilla F, Gabarros A, Horcajadas A, Rodriguez-Boto G et al (2008) Spontaneous Subarachnoid Haemorrhage multicenter database from the Group for the Study of Vascular Pathology of the Spanish Society for Neurosurgery: presentation, inclusion criteria and development of an internet-based registry. Neurocirugia (Astur) 19(5):405–415. https://doi.org/10.1016/S1130-1473(08)70207-0 CrossRef

25.

Jaja BN, Attalla D, Macdonald RL, Schweizer TA, Cusimano MD, Etminan N, Hanggi D, Hasan D, Johnston SC, Le Roux P et al (2014) The Subarachnoid Hemorrhage International Trialists (SAHIT) Repository: advancing clinical research in subarachnoid hemorrhage. Neurocrit Care 21(3):551–559. https://doi.org/10.1007/s12028-014-9990-y CrossRefPubMed

26.

Macdonald RL, Cusimano MD, Etminan N, Hanggi D, Hasan D, Ilodigwe D, Jaja B, Lantigua H, Le Roux P, Lo B et al (2013) Subarachnoid Hemorrhage International Trialists data repository (SAHIT). World Neurosurg 79(3–4):418–422. https://doi.org/10.1016/j.wneu.2013.01.006 CrossRefPubMed

27.

Ikawa F, Ohbayashi N, Imada Y, Matsushige T, Kajihara Y, Inagawa T, Kobayashi S (2004) Analysis of subarachnoid hemorrhage according to the Japanese standard stroke registry study—incidence, outcome, and comparison with the International Subarachnoid Aneurysm Trial. Neurol Med Chir (Tokyo) 44(5):275–276. https://doi.org/10.2176/nmc.44.275 CrossRef

28.

Fischer T, Johnsen SP, Pedersen L, Gaist D, Sorensen HT, Rothman KJ (2005) Seasonal variation in hospitalization and case fatality of subarachnoid hemorrhage—a nationwide Danish study on 9,367 patients. Neuroepidemiology 24(1–2):32–37. https://doi.org/10.1159/000081047 CrossRefPubMed

29.

Schatlo B, Fung C, Fathi AR, Sailer M, Winkler K, Daniel RT, Bijlenga P, Ahlborn P, Seule M, Zumofen D, Reinert M, Woernle C, Stienen M, Levivier M, Hildebrandt G, Mariani L, Bernays R, Fandino J, Raabe A, Keller E, Schaller K (2012) Introducing a nationwide registry: the Swiss study on aneurysmal subarachnoid haemorrhage (Swiss SOS). Acta Neurochir 154(12):2173–2178; discussion 2178. https://doi.org/10.1007/s00701-012-1500-4 CrossRefPubMed

30.

Bederson JB, Connolly ES Jr, Batjer HH, Dacey RG, Dion JE, Diringer MN, Duldner JE Jr, Harbaugh RE, Patel AB, Rosenwasser RH et al (2009) 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 40(3):994–1025. https://doi.org/10.1161/STROKEAHA.108.191395 CrossRefPubMed

31.

Farrell B, Godwin J, Richards S, Warlow C (1991) The United Kingdom transient ischaemic attack (UK-TIA) aspirin trial: final results. J Neurol Neurosurg Psychiatry 54(12):1044–1054. https://doi.org/10.1136/jnnp.54.12.1044 CrossRefPubMedPubMedCentral

32.

Bonferroni C (1937) Teoria statistica delle classi e calcolo delle probabilita. In: Volume in Onore di Ricarrdo dalla Volta. Universita di Firenza, pp 1–62

33.

Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL (2007) Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 38(8):2315–2321. https://doi.org/10.1161/STROKEAHA.107.484360 CrossRefPubMed

34.

Deruty R, Pelissou-Guyotat I, Mottolese C, Amat D, Bognar L (1995) Level of consciousness and age as prognostic factors in aneurysmal SAH. Acta Neurochir 132(1–3):1–8. https://doi.org/10.1007/BF01404840 CrossRefPubMed

35.

Rabinstein AA, Friedman JA, Nichols DA, Pichelmann MA, McClelland RL, Manno EM, Atkinson JL, Wijdicks EF (2004) Predictors of outcome after endovascular treatment of cerebral vasospasm. AJNR Am J Neuroradiol 25(10):1778–1782PubMed

36.

Risselada R, Lingsma HF, Bauer-Mehren A, Friedrich CM, Molyneux AJ, Kerr RS, Yarnold J, Sneade M, Steyerberg EW, Sturkenboom MC (2010) Prediction of 60 day case-fatality after aneurysmal subarachnoid haemorrhage: results from the International Subarachnoid Aneurysm Trial (ISAT). Eur J Epidemiol 25(4):261–266. https://doi.org/10.1007/s10654-010-9432-x CrossRefPubMedPubMedCentral

37.

Avdagic SS, Brkic H, Avdagic H, Smajic J, Hodzic S (2015) Impact of comorbidity on early outcome of patients with subarachnoid hemorrhage caused by cerebral aneurysm rupture. Med Arch 69(5):280–283. https://doi.org/10.5455/medarh.2015.69.280-283 CrossRefPubMedPubMedCentral

38.

Boogaarts HD, Conde MP, Janssen E, van Nuenen WF, de Vries J, Donders R, Westert GP, Grotenhuis JA, Bartels RH (2014) The value of the Charlson co-morbidity index in aneurysmal subarachnoid haemorrhage. Acta Neurochir 156(9):1663–1667. https://doi.org/10.1007/s00701-014-2160-3 CrossRefPubMed

39.

Charlson M, Szatrowski TP, Peterson J, Gold J (1994) Validation of a combined comorbidity index. J Clin Epidemiol 47(11):1245–1251. https://doi.org/10.1016/0895-4356(94)90129-5 CrossRefPubMed

40.

Naval NS, Kowalski RG, Chang TR, Caserta F, Carhuapoma JR, Tamargo RJ (2014) The SAH score: a comprehensive communication tool. J Stroke Cerebrovasc Dis 23(5):902–909. https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.07.035 CrossRefPubMed

41.

Zeiler FA, Lo BW, Akoth E, Silvaggio J, Kaufmann AM, Teitelbaum J, West M (2017) Predicting outcome in subarachnoid hemorrhage (SAH) utilizing the full outline of UnResponsiveness (FOUR) score. Neurocrit Care 27(3):381–391. https://doi.org/10.1007/s12028-017-0396-5 CrossRefPubMed

42.

Fortuny LA, Adams CB, Briggs M (1980) Surgical mortality in an aneurysm population: effects of age, blood pressure and preoperative neurological state. J Neurol Neurosurg Psychiatry 43(10):879–882. https://doi.org/10.1136/jnnp.43.10.879 CrossRefPubMedPubMedCentral

43.

O’Sullivan MG, Dorward N, Whittle IR, Steers AJ, Miller JD (1994) Management and long-term outcome following subarachnoid haemorrhage and intracranial aneurysm surgery in elderly patients: an audit of 199 consecutive cases. Br J Neurosurg 8(1):23–30. https://doi.org/10.3109/02688699409002389 CrossRefPubMed

44.

Ryttlefors M, Enblad P, Kerr RS, Molyneux AJ (2008) International subarachnoid aneurysm trial of neurosurgical clipping versus endovascular coiling: subgroup analysis of 278 elderly patients. Stroke 39(10):2720–2726. https://doi.org/10.1161/STROKEAHA.107.506030 CrossRefPubMed

45.

Rowe JG, Molyneux AJ, Byrne JV, Renowden S, Aziz TZ (1996) Endovascular treatment of intracranial aneurysms: a minimally invasive approach with advantages for elderly patients. Age Ageing 25(5):372–376. https://doi.org/10.1093/ageing/25.5.372 CrossRefPubMed

46.

Laidlaw JD, Siu KH (2003) Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery. Neurosurgery 53(6):1275–1280; discussion 1280-1272. https://doi.org/10.1227/01.NEU.0000093199.74960.FF CrossRefPubMed

47.

Kazumata K, Kamiyama H, Ishikawa T (2006) Reference table predicting the outcome of subarachnoid hemorrhage in the elderly, stratified by age. J Stroke Cerebrovasc Dis 15(1):14–17. https://doi.org/10.1016/j.jstrokecerebrovasdis.2005.08.007 CrossRefPubMed

48.

Nieuwkamp DJ, Rinkel GJ, Silva R, Greebe P, Schokking DA, Ferro JM (2006) Subarachnoid haemorrhage in patients > or = 75 years: clinical course, treatment and outcome. J Neurol Neurosurg Psychiatry 77(8):933–937. https://doi.org/10.1136/jnnp.2005.084350 CrossRefPubMedPubMedCentral

49.

Ryttlefors M, Howells T, Ronne-Engstrom E, Nilsson P, Enblad P (2010) Neurointensive care is justified in elderly patients with severe subarachnoid hemorrhage—an outcome and secondary insults study. Acta Neurochir 152(2):241–249; discussion 249. https://doi.org/10.1007/s00701-009-0496-x CrossRefPubMed

50.

Awe OO, Gonzalez LF, Hasan D, Maltenfort M, Rossenwasser R, Jabbour P (2011) Treatment outcome of aneurysmal subarachnoid hemorrhage in patients aged 70 years and older. Neurosurgery 68(3):753–758; discussion 758. https://doi.org/10.1227/NEU.0b013e318207a9fb CrossRefPubMed

51.

Horiuchi T, Tanaka Y, Hongo K (2005) Surgical treatment for aneurysmal subarachnoid hemorrhage in the 8th and 9th decades of life. Neurosurgery 56(3):469–475; discussion 469-475. https://doi.org/10.1227/01.NEU.0000153926.67713.B8 CrossRefPubMed

52.

Al-Khindi T, Macdonald RL, Schweizer TA (2010) Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 41(8):e519–e536. https://doi.org/10.1161/STROKEAHA.110.581975 CrossRefPubMed

53.

Vlak MH, Rinkel GJ, Greebe P, Greving JP, Algra A (2013) Lifetime risks for aneurysmal subarachnoid haemorrhage: multivariable risk stratification. J Neurol Neurosurg Psychiatry 84(6):619–623. https://doi.org/10.1136/jnnp-2012-303783 CrossRefPubMed

54.

Juvela S (2003) Prehemorrhage risk factors for fatal intracranial aneurysm rupture. Stroke 34(8):1852–1857. https://doi.org/10.1161/01.STR.0000080380.56799.DD CrossRefPubMed

55.

Kassell NF, Torner JC, Haley EC, Jane JA, Adams HP, Kongable GL (1990) The international cooperative study on the timing of aneurysm surgery. Part 1: overall management results. J Neurosurg 73(1):18–36. https://doi.org/10.3171/jns.1990.73.1.0018 CrossRefPubMed

56.

Eskesen V, Rosenorn J, Schmidt K, Ronde F (1987) Pre-existing arterial hypertension in subarachnoid haemorrhage: an unfavourable prognostic factor. Br J Neurosurg 1(4):455–461. https://doi.org/10.3109/02688698708999636 CrossRefPubMed

57.

Germanson TP, Lanzino G, Kongable GL, Torner JC, Kassell NF (1998) Risk classification after aneurysmal subarachnoid hemorrhage. Surg Neurol 49(2):155–163. https://doi.org/10.1016/S0090-3019(97)00337-6 CrossRefPubMed

58.

Juvela S (1992) Alcohol consumption as a risk factor for poor outcome after aneurysmal subarachnoid haemorrhage. BMJ 304(6843):1663–1667. https://doi.org/10.1136/bmj.304.6843.1663 CrossRefPubMedPubMedCentral

59.

Kongable GL, Lanzino G, Germanson TP, Truskowski LL, Alves WM, Torner JC, Kassell NF (1996) Gender-related differences in aneurysmal subarachnoid hemorrhage. J Neurosurg 84(1):43–48. https://doi.org/10.3171/jns.1996.84.1.0043 CrossRefPubMed

Title: Factors associated with clinical and radiological status on admission in patients with aneurysmal subarachnoid hemorrhage
Authors: Daniel W. Zumofen
Michel Roethlisberger
Rita Achermann
Schatlo Bawarjan
Martin N. Stienen
Christian Fung
Donato D’Alonzo
Nicolai Maldaner
Andrea Ferrari
Marco V. Corniola
Daniel Schoeni
Johannes Goldberg
Daniele Valsecchi
Thomas Robert
Rodolfo Maduri
Martin Seule
Jan-Karl Burkhardt
Serge Marbacher
Philippe Bijlenga
Kristine A. Blackham
Heiner C. Bucher
Luigi Mariani
Raphael Guzman
on behalf of the Swiss SOS Study Group
Publication date: 01-10-2018
Publisher: Springer Berlin Heidelberg
Published in: Neurosurgical Review / Issue 4/2018
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI: https://doi.org/10.1007/s10143-018-0952-2

ACC 2024 Congress

Springer Medicine

Factors associated with clinical and radiological status on admission in patients with aneurysmal subarachnoid hemorrhage

Abstract

ACC 2024 Congress

Springer Medicine

Abstract

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