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01-07-2018 | Original Article - Vascular Neurosurgery - Aneurysm

Vasospasm-related complications after subarachnoid hemorrhage: the role of patients’ age and sex

Authors: Marvin Darkwah Oppong, Antonella Iannaccone, Oliver Gembruch, Daniela Pierscianek, Mehdi Chihi, Philipp Dammann, Angela Köninger, Oliver Müller, Michael Forsting, Ulrich Sure, Ramazan Jabbarli

Published in: Acta Neurochirurgica | Issue 7/2018

Abstract

Background

Outcome of aneurysmal subarachnoid hemorrhage (SAH) depends strongly on occurrence of symptomatic vasospasm (SV) leading to delayed cerebral ischemia (DCI). Various demographic, radiographic, and clinical predictors of SV have been reported so far, partially with conflicting results. The aim of this study was to analyze the role of patients’ age and sex on SV/DCI risk, especially to identify age and sex-specific risk groups.

Methods

All patients admitted with acute SAH during a 14-year-period ending in 2016 were eligible for this study. The study endpoints were the following: SV requiring spasmolysis, occurrence of DCI in follow-up computed tomography scans and unfavorable outcome at 6 months (modified Rankin scale > 2).

Results

Nine hundred ninety-four patients were included in this study. The majority was female (666; 67%). SV, DCI, and unfavorable outcomes were observed in 21.5, 21.8, and 43.6% of the patients, respectively. Younger age (p < 0.001; OR = 1.03 per year decrease) and female sex (p = 0.025; OR = 1.510) were confirmed as independent predictors of SV. Regarding the sex differences, there were three age groups for SV/DCI risk ≤ 54, 55–74, and ≥ 75 years. Male patients showed earlier decrease in SV risk (at ≥ 55 vs. ≥ 75 years in females). Therefore, SAH females aged between 55 and 74 years were at the highest risk for DCI and unfavorable outcome, as compared to younger/older females (p = 0.001, OR = 1.77/p = 0.001, OR = 1.80). In contrast, their male counterparts did not show these risk alterations (p = 0.445/p = 0.822).

Conclusion

After acute SAH, female and male patients seem to show different age patterns for the risk of SV and DCI. Females aged between 55 and 74 years are at particular risk of vasospasm-related SAH complications, possibly due to onset of menopause.

Clinical trial registration number

DRKS, Unique identifier: DRKS00008749

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Algra AM, Klijn CJ, Helmerhorst FM, Algra A, Rinkel GJ (2012) Female risk factors for subarachnoid hemorrhage: a systematic review. Neurology 79:1230–1236. https://doi.org/10.1212/WNL.0b013e31826aace6 CrossRefPubMed

Anderson RC, Kan P, Klimo P, Brockmeyer DL, Walker ML, Kestle JR (2004) Complications of intracranial pressure monitoring in children with head trauma. J Neurosurg 101:53–58. https://doi.org/10.3171/ped.2004.101.2.0053 PubMedCrossRef

Calleja-Agius J, Brincat M (2012) The effect of menopause on the skin and other connective tissues. Gynecol Endocrinol 28:273–277. https://doi.org/10.3109/09513590.2011.613970 CrossRefPubMed

Charpentier C, Audibert G, Guillemin F, Civit T, Ducrocq X, Bracard S, Hepner H, Picard L, Laxenaire MC (1999) Multivariate analysis of predictors of cerebral vasospasm occurrence after aneurysmal subarachnoid hemorrhage. Stroke 30:1402–1408CrossRefPubMed

Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA (2001) Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 32:2012–2020CrossRefPubMed

Claus JJ, Breteler MM, Hasan D, Krenning EP, Bots ML, Grobbee DE, Van Swieten JC, Van Harskamp F, Hofman A (1998) Regional cerebral blood flow and cerebrovascular risk factors in the elderly population. Neurobiol Aging 19:57–64CrossRefPubMed

de Moraes-Ruehsen M, Jones GS (1967) Premature ovarian failure. Fertil Steril 18:440–461CrossRefPubMed

Ding C, Toll V, Ouyang B, Chen M (2013) Younger age of menopause in women with cerebral aneurysms. J Neurointerv Surg 5:327–331. https://doi.org/10.1136/neurintsurg-2012-010364 CrossRefPubMed

Dratva J, Gomez Real F, Schindler C, Ackermann-Liebrich U, Gerbase MW, Probst-Hensch NM, Svanes C, Omenaas ER, Neukirch F, Wjst M, Morabia A, Jarvis D, Leynaert B, Zemp E (2009) Is age at menopause increasing across Europe? Results on age at menopause and determinants from two population-based studies. Menopause 16:385–394. https://doi.org/10.1097/gme.0b013e31818aefef CrossRefPubMed

10.

Dumont AS, Crowley RW, Monteith SJ, Ilodigwe D, Kassell NF, Mayer S, Ruefenacht D, Weidauer S, Pasqualin A, Macdonald RL (2010) Endovascular treatment or neurosurgical clipping of ruptured intracranial aneurysms: effect on angiographic vasospasm, delayed ischemic neurological deficit, cerebral infarction, and clinical outcome. Stroke 41:2519–2524. https://doi.org/10.1161/strokeaha.110.579383 CrossRefPubMed

11.

Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1–9CrossRefPubMed

12.

Foreman B (2016) The pathophysiology of delayed cerebral ischemia. J Clin Neurophysiol 33:174–182. https://doi.org/10.1097/wnp.0000000000000273 CrossRefPubMed

13.

Frontera JA, Fernandez A, Schmidt JM, Claassen J, Wartenberg KE, Badjatia N, Connolly ES, Mayer SA (2009) Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke 40:1963–1968. https://doi.org/10.1161/strokeaha.108.544700 CrossRefPubMed

14.

Germans MR, Jaja BNR, de Oliviera Manoel AL, Cohen AH, Macdonald RL (2017) Sex differences in delayed cerebral ischemia after subarachnoid hemorrhage. J Neurosurg:1–7. https://doi.org/10.3171/2017.3.jns162808

15.

Gross BA, Rosalind Lai PM, Frerichs KU, Du R (2014) Treatment modality and vasospasm after aneurysmal subarachnoid hemorrhage. World Neurosurg 82:e725–e730. https://doi.org/10.1016/j.wneu.2013.08.017 CrossRefPubMed

16.

Hirashima Y, Kurimoto M, Hori E, Origasa H, Endo S (2005) Lower incidence of symptomatic vasospasm after subarachnoid hemorrhage owing to ruptured vertebrobasilar aneurysms. Neurosurgery 57:1110–1116 discussion 1110-1116CrossRefPubMed

17.

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

18.

Jabbarli R, Glasker S, Weber J, Taschner C, Olschewski M, Van Velthoven V (2013) Predictors of severity of cerebral vasospasm caused by aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 22:1332–1339. https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.01.006 CrossRefPubMed

19.

Jamous MA, Nagahiro S, Kitazato KT, Satomi J, Satoh K (2005) Role of estrogen deficiency in the formation and progression of cerebral aneurysms. Part I: experimental study of the effect of oophorectomy in rats. J Neurosurg 103:1046–1051. https://doi.org/10.3171/jns.2005.103.6.1046 CrossRefPubMed

20.

Jiang C, Zuo F, Wang Y, Lu H, Yang Q, Wang J (2016) Progesterone changes VEGF and BDNF expression and promotes neurogenesis after ischemic stroke. Mol Neurobiol. https://doi.org/10.1007/s12035-015-9651-y

21.

Jiang C, Zuo F, Wang Y, Wan J, Yang Z, Lu H, Chen W, Zang W, Yang Q, Wang J (2016) Progesterone exerts neuroprotective effects and improves long-term neurologic outcome after intracerebral hemorrhage in middle-aged mice. Neurobiol Aging 42:13–24. https://doi.org/10.1016/j.neurobiolaging.2016.02.029 CrossRefPubMedPubMedCentral

22.

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

23.

Lawton MT, Vates GE (2017) Subarachnoid hemorrhage. N Engl J Med 377:257–266. https://doi.org/10.1056/NEJMcp1605827 CrossRefPubMed

24.

Lin CL, Dumont AS, Wu SC, Wang CJ, Howng SL, Huang YF, Wong WY, Kassell NF, Jeng AY, Kwan AL (2006) 17beta-estradiol inhibits endothelin-1 production and attenuates cerebral vasospasm after experimental subarachnoid hemorrhage. Exp Biol Med 231:1054–1057

25.

Lin CL, Shih HC, Dumont AS, Kassell NF, Lieu AS, Su YF, Hwong SL, Hsu C (2006) The effect of 17beta-estradiol in attenuating experimental subarachnoid hemorrhage-induced cerebral vasospasm. J Neurosurg 104:298–304. https://doi.org/10.3171/jns.2006.104.2.298 CrossRefPubMed

26.

Macdonald RL, Wallace MC, Coyne TJ (1994) The effect of surgery on the severity of vasospasm. J Neurosurg 80:433–439. https://doi.org/10.3171/jns.1994.80.3.0433 CrossRefPubMed

27.

Macdonald RL, Rosengart A, Huo D, Karrison T (2003) Factors associated with the development of vasospasm after planned surgical treatment of aneurysmal subarachnoid hemorrhage. J Neurosurg 99:644–652. https://doi.org/10.3171/jns.2003.99.4.0644 CrossRefPubMed

28.

Magge SN, Chen HI, Ramakrishna R, Cen L, Chen Z, Elliott JP, Winn HR, Le Roux PD (2010) Association of a younger age with an increased risk of angiographic and symptomatic vasospasms following subarachnoid hemorrhage. J Neurosurg 112:1208–1215. https://doi.org/10.3171/2009.9.jns081670 CrossRefPubMed

29.

McGirt MJ, Mavropoulos JC, McGirt LY, Alexander MJ, Friedman AH, Laskowitz DT, Lynch JR (2003) Leukocytosis as an independent risk factor for cerebral vasospasm following aneurysmal subarachnoid hemorrhage. J Neurosurg 98:1222–1226. https://doi.org/10.3171/jns.2003.98.6.1222 CrossRefPubMed

30.

McGirt MJ, Blessing R, Alexander MJ, Nimjee SM, Woodworth GF, Friedman AH, Graffagnino C, Laskowitz DT, Lynch JR (2006) Risk of cerebral vasopasm after subarachnoid hemorrhage reduced by statin therapy: a multivariate analysis of an institutional experience. J Neurosurg 105:671–674. https://doi.org/10.3171/jns.2006.105.5.671 CrossRefPubMed

31.

Meyer JS, Terayama Y, Takashima S (1993) Cerebral circulation in the elderly. Cerebrovasc Brain Metab Rev 5:122–146PubMed

32.

Moss EL, Taneja S, Munir F, Kent C, Robinson L, Potdar N, Sarhanis P, McDermott H (2016) Iatrogenic menopause after treatment for cervical cancer. Clin Oncol (R Coll Radiol) 28:766–775. https://doi.org/10.1016/j.clon.2016.08.016 CrossRef

33.

Nabulsi AA, Folsom AR, White A, Patsch W, Heiss G, Wu KK, Szklo M (1993) Association of hormone-replacement therapy with various cardiovascular risk factors in postmenopausal women. The Atherosclerosis Risk in Communities Study Investigators. N Engl J Med 328:1069–1075. https://doi.org/10.1056/nejm199304153281501 CrossRefPubMed

34.

Parazzini F (2007) Determinants of age at menopause in women attending menopause clinics in Italy. Maturitas 56:280–287. https://doi.org/10.1016/j.maturitas.2006.09.003 CrossRefPubMed

35.

Phipps AI, Ichikawa L, Bowles EJ, Carney PA, Kerlikowske K, Miglioretti DL, Buist DS (2010) Defining menopausal status in epidemiologic studies: a comparison of multiple approaches and their effects on breast cancer rates. Maturitas 67:60–66. https://doi.org/10.1016/j.maturitas.2010.04.015 CrossRefPubMedPubMedCentral

36.

Qureshi AI, Malik AA, Saeed O, Defillo A, Sherr GT, Suri MF (2016) Hormone replacement therapy and the risk of subarachnoid hemorrhage in postmenopausal women. J Neurosurg 124:45–50. https://doi.org/10.3171/2014.12.jns142329 CrossRefPubMed

37.

Rabb CH, Tang G, Chin LS, Giannotta SL (1994) A statistical analysis of factors related to symptomatic cerebral vasospasm. Acta Neurochir 127:27–31CrossRefPubMed

38.

Rosenlrn J, Eskesen V, Schmidt K (1993) Clinical features and outcome in females and males with ruptured intracranial saccular aneurysms. Br J Neurosurg 7:287–290CrossRefPubMed

39.

Ryttlefors M, Enblad P, Ronne-Engstrom E, Persson L, Ilodigwe D, Macdonald RL (2010) Patient age and vasospasm after subarachnoid hemorrhage. Neurosurgery 67:911–917. https://doi.org/10.1227/NEU.0b013e3181ed11ab CrossRefPubMed

40.

Schumacher M, Sitruk-Ware R, De Nicola AF (2008) Progesterone and progestins: neuroprotection and myelin repair. Curr Opin Pharmacol 8:740–746. https://doi.org/10.1016/j.coph.2008.10.002 CrossRefPubMed

41.

Shih HC, Lin CL, Lee TY, Lee WS, Hsu C (2006) 17beta-estradiol inhibits subarachnoid hemorrhage-induced inducible nitric oxide synthase gene expression by interfering with the nuclear factor kappa B transactivation. Stroke 37:3025–3031. https://doi.org/10.1161/01.STR.0000249008.18669.5a CrossRefPubMed

42.

Sobrino A, Mata M, Laguna-Fernandez A, Novella S, Oviedo PJ, Garcia-Perez MA, Tarin JJ, Cano A, Hermenegildo C (2009) Estradiol stimulates vasodilatory and metabolic pathways in cultured human endothelial cells. PLoS One 4:e8242. https://doi.org/10.1371/journal.pone.0008242 CrossRefPubMedPubMedCentral

43.

Stepaniak U, Szafraniec K, Kubinova R, Malyutina S, Peasey A, Pikhart H, Pajak A, Bobak M (2013) Age at natural menopause in three central and eastern European urban populations: the HAPIEE study. Maturitas 75:87–93. https://doi.org/10.1016/j.maturitas.2013.02.008 CrossRefPubMedPubMedCentral

44.

Tabuchi S (2015) Relationship between postmenopausal estrogen deficiency and aneurysmal subarachnoid hemorrhage. Behav Neurol 2015:720141. https://doi.org/10.1155/2015/720141 CrossRefPubMedPubMedCentral

45.

Tada Y, Makino H, Furukawa H, Shimada K, Wada K, Liang EI, Murakami S, Kudo M, Kung DK, Hasan DM, Kitazato KT, Nagahiro S, Lawton MT, Hashimoto T (2014) Roles of estrogen in the formation of intracranial aneurysms in ovariectomized female mice. Neurosurgery 75:690–695; discussion 695. https://doi.org/10.1227/neu.0000000000000528 CrossRefPubMedPubMedCentral

46.

Tada Y, Wada K, Shimada K, Makino H, Liang EI, Murakami S, Kudo M, Shikata F, Pena Silva RA, Kitazato KT, Hasan DM, Kanematsu Y, Nagahiro S, Hashimoto T (2014) Estrogen protects against intracranial aneurysm rupture in ovariectomized mice. Hypertension 63:1339–1344. https://doi.org/10.1161/hypertensionaha.114.03300 CrossRefPubMedPubMedCentral

47.

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 51:1457CrossRefPubMedPubMedCentral

48.

Teunissen LL, Rinkel GJ, Algra A, van Gijn J (1996) Risk factors for subarachnoid hemorrhage: a systematic review. Stroke 27:544–549CrossRefPubMed

49.

van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J (1988) Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19:604–607CrossRefPubMed

50.

Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, Macdonald RL, Diringer MN, Broderick JP, Dreier JP, Roos YB (2010) Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke 41:2391–2395. https://doi.org/10.1161/strokeaha.110.589275 CrossRefPubMed

51.

Yousef K, Crago E, Kuo CW, Horowitz M, Hravnak M (2010) Predictors of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: a cardiac focus. Neurocrit Care 13:366–372. https://doi.org/10.1007/s12028-010-9408-4 CrossRefPubMedPubMedCentral

Title: Vasospasm-related complications after subarachnoid hemorrhage: the role of patients’ age and sex
Authors: Marvin Darkwah Oppong
Antonella Iannaccone
Oliver Gembruch
Daniela Pierscianek
Mehdi Chihi
Philipp Dammann
Angela Köninger
Oliver Müller
Michael Forsting
Ulrich Sure
Ramazan Jabbarli
Publication date: 01-07-2018
Publisher: Springer Vienna
Published in: Acta Neurochirurgica / Issue 7/2018
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-018-3549-1

At a glance: The STEP trials

Springer Medicine

Vasospasm-related complications after subarachnoid hemorrhage: the role of patients’ age and sex

Abstract

Background

Methods

Results

Conclusion

Clinical trial registration number

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Clinical trial registration number

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