Characterization of Risk Factor Differences in Perimesencephalic Subarachnoid Hemorrhage

 

 Buy Article Permissions and Reprints

Abstract

Objective: The non-aneurysmal perimesencephalic subarachnoid hemorrhage (p-SAH) has a favorable outcome. Our objective was to provide a reason for that assessing the association of putative risk factors with this different type of hemorrhage in comparison to the aneurysmal subarachnoid hemorrhage (a-SAH).

Methods: We selected 185 consecutive cases of subarachnoid hemorrhage between September 1994 and August 1998 in a hospital-based case-control study and investigated the influence of hypertension, body weight, smoking and the three interacting blood factors hematocrit, fibrinogen and leukocrit.

Results: 1) Risk factors for SAH: For the entire study group an association of hypertension with the incidence of SAH was found both in the univariate analysis of this variable alone (P = 0.001) and in the multivariate logistic regression (P = 0.0001), aside from the risk factors smoking (P = 0.0047) and hematocrit (P = 0.0001). As to the risk of hypertensive subjects to experience SAH for different reasons, the logistic regression yielded an odds ratio (OR) of 3.54 [CI (95 %): 2.21 - 5.56]. 2) Risk factors for p-SAH: Patients with p-SAH differ in their risk profile from typical aneurysmal SAH cases with respect to their blood pressure status (P = 0.019) and the investigated hemorheological parameters.

Conclusions: A different association between possible risk factors and the two types of subarachnoid hemorrhages was ascertained. In general there seem to be fewer putative risk factors in the perimesencephalic SAH cases compared to the typical aneurysmal hemorrhages.

References

• 1 Gijn J van, Dongen K J van, Vermeulen M, Hijdra A. Perimesencephalic hemorrhage: A nonaneurysmal and benign form of subarachnoid hemorrhage.  Neurology. 1985;  35 493-497
  CrossrefPubMedGoogle Scholar
• 2 Kallmes D F, Clark H P, Dix J E, Cloft H J, Evans A J, Dion J E, Kassel N F. Ruptured vertebrobasilar aneurysms: Frequency of the nonaneurysmal perimesencephalic pattern of hemorrhage on CT scans.  Radiology. 1996;  201 657-660
  CrossrefPubMedGoogle Scholar
• 3 Rinkel G JE, Wijdicks E FM, Vermeulen M, Hageman L M, Tans J ThJ, Gijn J van. Outcome in perimesencephalic (nonaneurysmal) subarachnoid hemorrhage: A follow-up study in 37 patients.  Neurology. 1990;  40 1130-1132
  CrossrefPubMedGoogle Scholar
• 4 Rinkel G JE, Wijdicks E FM, Kasan D, Kienstra G EM, Franke C L, Hageman L M, Vermeulen M, Gijn J van. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage an computed tomography.  Lancet. 1991;  338 964-968
  CrossrefPubMedGoogle Scholar
• 5 Rinkel G JE, Gijn J van, Wijdicks E FM. Subarachnoid hemorrhage without detectable aneurysm. A review of the causes.  Stroke. 1993;  24 1403-1409
  CrossrefPubMedGoogle Scholar
• 6 Alexander M SM, Dias P S, Uttley D. Spontaneous subarachnoid hemorrhage and negative cerebral panangiography.  J Neurosurg. 1986;  64 359-362
  PubMedGoogle Scholar
• 7 Andrioli G C, Salar G, Rigobello L, Mingrino S. Subarachnoid haemorrhage of unknown aetiology.  Acta Neurochir. 1979;  48 217-221
  CrossrefPubMedGoogle Scholar
• 8 Hayward R D. Subarachnoid haemorrhage of unknown aetiology.  J Neurol Neurosurg Psych. 1977;  40 926-931
  PubMedGoogle Scholar
• 9 Schievink W I, Wijdicks E FM. Pretruncal subarachnoid hemorrhage: An anatomically correct description of the perimesencephalic subarachnoid hemorrhage (Letter).  Stroke. 1997;  28 2572
  PubMedGoogle Scholar
• 10 Spallone A, Ferrante L, Palatinsky E, Santoro A, Acqui M. Subarachnoid haemorrhage of unknown origin.  Acta Neurochir. 1986;  80 12-17
  CrossrefPubMedGoogle Scholar
• 11 Wijdicks E FM, Schievink W I. Perimesencephalic nonaneurysmal subarachnoid hemorrhage: First hint of a cause?.  Neurology. 1997;  49 (2) 634-636
  CrossrefPubMedGoogle Scholar
• 12 Bonita R, Beaglehole R, Norm J DK. Subarachnoid hemorrhage in New Zealand: An epidemiological study.  Stroke. 1983;  14 342-347
  PubMedGoogle Scholar
• 13 Knekt P, Reunanen A, Aho K, Heliövaara M, Rissanen A, Aromaa A, Impivaara O. Risk factors for subarachnoid hemorrhage in a longitudinal population study.  J Clin Epidem. 1991;  44 933-938
  CrossrefPubMedGoogle Scholar
• 14 Longstreth W T, Koepsell T D, Yerby M S, Belle G van. Risk factors for subarachnoid hemorrhage.  Stroke. 1985;  16 377-385
  PubMedGoogle Scholar
• 15 Monte S M de la, Moore G W, Monk M A, Hutchins G M. Risk factors for the development and rupture of intracranial berry aneurysms.  Am J Med. 1985;  78 957-964
  CrossrefPubMedGoogle Scholar
• 16 Teunissen L L, Kinkel G JE, Algra A, Gijn J van. Risk factors for subarachnoid hemorrhage. A systematic review.  Stroke. 1996;  27 544-549
  CrossrefPubMedGoogle Scholar
• 17 Canhao P, Ferro J M, Pinto A N, Melo T P, Carapos J G. Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms.  Acta Neurochir. 1995;  132 14-19
  CrossrefPubMedGoogle Scholar
• 18 Dyken M L, Wolf P A, Barnett H JM, Bergan J J, Hass W K, Kannel W B, Kuller L, Kurtzke J F, Sundt T M. Risk factors in stroke. A statement for physicians by the Subcommittee on Risk Factors and Stroke of the Stroke Council.  Stroke. 1984;  15 1105-1111
  PubMedGoogle Scholar
• 19 Kannel W B, Wolf P A, McGee D L, Dawber T R, McNamara P, Castelli W P. Systolic blood pressure, arterial rigidity, and risk of stroke. The Framingham Study.  JAMA. 1981;  245 1225-1229
  CrossrefPubMedGoogle Scholar
• 20 Lechner H, Schmidt R, Reinhart B, Grieshofer P, Eber B, Fazekas F, Schumacher M, Horner S, Freidl W, Niederkorn K, Koch M. Cerebrovascular risk factors in an elderly Austrian population: First year results of the Austrian Stroke Prevention Study (ASPS).  Wien Klin Wochenschr. 1993;  105/14 398-403
  PubMedGoogle Scholar
• 21 Shinton R, Beevers G. Meta-analysis of relation between cigarette smoking and stroke.  BMJ. 1989;  298 789-794
  CrossrefPubMedGoogle Scholar
• 22 Andrews R A, Spiegel P K. Intracranial aneurysms. Age, sex, blood pressure, and multiplicity in an unselected series of patients.  J Neurosurg. 1979;  51 27-32
  PubMedGoogle Scholar
• 23 Bonita R. Cigarette smoking, hypertension and the risk of subarachnoid hemorrhage: A population-based case control study.  Stroke. 1986;  17 831-835
  CrossrefPubMedGoogle Scholar
• 24 Lasner T M, Weil R W, Riina H A, King J T, Zager E L, Raps E C, Flamm E S. Cigarette smoking-induced increase in the risk of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage.  J Neurosurg. 1997;  87 381-384
  CrossrefPubMedGoogle Scholar
• 25 Longstreth W T, Nelson L N, Koepsell T D, Belle G van. Cigarette smoking, alcohol use, and subarachnoid hemorrhage.  Stroke. 1992;  23 1242-1249
  CrossrefPubMedGoogle Scholar
• 26 Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Koike T, Tanaka R. Hemostasis in spontaneous subarachnoid hemorrhage.  Neurosurgery. 1995;  37 226-234
  PubMedGoogle Scholar
• 27 Peltonen S, Juvela S, Kaste M, Lassila R. Hemostasis and fibrinolysis activation after subarachnoid hemorrhage.  J Neurosurg. 1997;  87 207-214
  PubMedGoogle Scholar
• 28 Beguelin C, Seiler R. Subarachnoid hemorrhage with normal cerebral panangiography.  Neurosurgery. 1983;  13 409-411
  PubMedGoogle Scholar
• 29 af Björkesten G, Troupp H. Prognosis of subarachnoid hemorrhage. A comparison between patients with verified aneurysms and patients with normal angiograms.  J Neurosurg. 1957;  14 434-441
  PubMedGoogle Scholar
• 30 Brismar J, Sundbärg G. Subarachnoid hemorrhage of unknown origin: prognosis and prognostic factors.  J Neurosurg. 1985;  63 349-354
  PubMedGoogle Scholar
• 31 Cohen M M. Cerebrovascular accidents.  Arch Patholog. 1955;  60 296-307
  PubMedGoogle Scholar
• 32 Eskesen V, Sørensen E B, Rosenørn J, Schmidt K. The prognosis in subarachnoid hemorrhage of unknown etiology.  J Neurosurg. 1984;  61 1029-1031
  PubMedGoogle Scholar
• 33 Jain V K, Hedge T, Easwaran R K, Das B S, Reddy G NN. Benign subarachnoid haemorrhage (subarachnoid haemorrhage of unexplained aetiology).  Acta Neurochir. 1987;  86 89-92
  CrossrefPubMedGoogle Scholar
• 34 Juul R, Fredriksen T A, Ringkjob R. Prognosis in subarachnoid hemorrhage of unknown etiology.  J Neurosurg. 1986;  64 537-542
  PubMedGoogle Scholar
• 35 Kawamura S, Yasui N. Clinical and long-term follow-up study in patients with spontaneous subarachnoid haemorrhage of unknown aetiology.  Acta Neurochir. 1990;  106 110-114
  CrossrefPubMedGoogle Scholar
• 36 Mehdorn H M, Dietrich U, Kalff R, Hoffmann B, Rauhut F, Grote W. Subarachnoid hemorrhage of unknown origin. Longterm prognosis.  Neurosurg Rev. 1992;  15 27-31
  PubMedGoogle Scholar
• 37 Nishioka H, Torner J C, Graf C J, Kassel N F, Sahs A L, Goettler L C. Cooperative study of intracranial aneurysms and subarachnoid hemorrhage: A long-term prognostic study. III. Subarachnoid hemorrhage of undetermined etiology.  Arch Neurol. 1984;  41 1147-1151
  CrossrefPubMedGoogle Scholar
• 38 Oder W, Kollegger H, Zeiler K, Dal-Bianco P, Wessely P, Deecke L. Subarachnoid hemorrhage of unknown etiology: early prognostic factors for long-term functional capacity.  J Neurosurgery. 1991;  76 601-605
  PubMedGoogle Scholar
• 39 Drake C G. Report of World Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale.  J Neurosurg. 1988;  68 985-986
  PubMedGoogle Scholar
• 40 Fisher C M, Kistler J P, Davis J M. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning.  Neurosurgery. 1980;  6 1-9
  CrossrefPubMedGoogle Scholar
• 41 Jennett B, Bond M. Assessment of outcome after severe brain damage.  Lancet. 1975;  1 480-489
  Google Scholar
• 42 Shephard R H. Prognosis of spontaneous (non traumatic) subarachnoid haemorrhage of unknown cause.  Lancet. 1984;  1 777-778
  PubMedGoogle Scholar
• 43 Levy L F. Subarachnoid haemorrhage without arteriographic vascular abnormality.  J Neurosurg. 1960;  17 252-258
  PubMedGoogle Scholar
• 44 Cioffi F, Pasqualin A, Cavazzani P, Pian R da. Subarachnoid haemorrhage of unknown origin: Clinical and tomographical aspects.  Acta Neurochir. 1989;  97 31-39
  CrossrefPubMedGoogle Scholar
• 45 Ferbert A, Hubo I, Biniek R. Non-traumatic subarachnoid hemorrhage with normal angiogram. Long-term follow-up and CT predictors of complication.  J Neurolog Sci. 1992;  107 14-18
  PubMedGoogle Scholar
• 46 Giombini S, Bruzzone M G, Pluchino F. Subarachnoid hemorrhage of unexplained cause.  Neurosurgery. 1988;  22 313-316
  CrossrefPubMedGoogle Scholar
• 47 Rinkel G JE, Wijdicks E FM, Vermeulen M, Hasan D, Brouwers P JAM, Gijn J van. The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage.  Ann Neurol. 1991;  29 463-468
  CrossrefPubMedGoogle Scholar
• 48 Ronkainen A, Hernesniemi J. Subarachnoid haemorrhage of unknown aetiology.  Acta Neurochir. 1992;  119 29-34
  CrossrefPubMedGoogle Scholar
• 49 Lanzino G, Kassell N F, Germanson T, Kongable G L, Truskowski L L, Torner J C, Jane J A. Age and outcome after aneurysmal subarachnoid hemorrhage: Why do older patients far worse?.  J Neurosurg. 1996;  85 410-418
  CrossrefPubMedGoogle Scholar
• 50 Taylor C L, Yuan Z, Selman W R, Ratcheson R A, Rimm A A. Cerebral arterial aneurysm formation and rupture in 20 767 elderly patients: Hypertension and other risk factors.  J Neurosurg. 1995;  83 812-819
  PubMedGoogle Scholar
• 51 McCormick W F, Schmalstieg E J. The relationship of arterial hypertension to intracranial aneurysms.  Arch Neurol. 1977;  34 258-287
  PubMedGoogle Scholar
• 52 Juvela S, Hillbom M, Numminen H, Koskinen P. Cigarette smoking and alcohol consumption as risk factors for aneurysmal subarachnoid hemorrhage.  Stroke. 1993;  24 639-646
  CrossrefPubMedGoogle Scholar
• 53 Ostergaard J R. Risk factors in intracranial saccular aneurysms. Aspect on the formation and rupture of aneurysms, and development of cerebral vasospasm.  Acta Neurol Scand. 1989;  80 81-98
  PubMedGoogle Scholar
• 54 Simpson R K, Contant C F, Fischer D K, Cech D A, Robertson C S, Narayan R K. Epidemiological characteristics of subarachnoid hemorrhage in an urban population.  J Clin Epidem. 1991;  44 641-648
  PubMedGoogle Scholar
• 55 Bell B A, Symon L. Smoking and subarachnoid haemorrhage.  Brit Med J. 1979;  1 577-578
  PubMedGoogle Scholar
• 56 Sacco R L, Wolf P A, Bharucha N E, Meeks S L, Kannel W B, Charette L J, McNamara P M, Palmer E P, D'Agostino R. Subarachnoid and intracerebral hemorrhage: Natural history, prognosis, and precursive factors in the Framingham Study.  Neurology. 1984;  34 847-854
  CrossrefPubMedGoogle Scholar
• 57 Giroud M, Creisson E, Fayolle H, Andre N, Becker F, Martin D, Dumas R. Risk factors for primary cerebral hemorrhage: a population-based-study in the Stroke Registry of Dijon.  Neuroepidemiology. 1995;  14 20-26
  PubMedGoogle Scholar
• 58 Wood J H, Kee D B. Hemorheology of the cerebral circulation in stroke.  Stroke. 1985;  16 765-772
  PubMedGoogle Scholar
• 59 Ernst E. Haemorheological consequences of chronic cigarette smoking.  J Cardiovasc Risk. 1995;  2 435-439
  PubMedGoogle Scholar
• 60 Lowe G D. Etiopathogenesis of cardiovascular disease: hemostasis, thrombosis, and vascular medicine.  Ann Periodontol. 1998;  3 121-126
  PubMedGoogle Scholar
• 61 Neil-Dwyer G, Cruickshank J. The blood leucocyte count and its prognostic significance in subarachnoid hemorrhage.  Brain. 1974;  97 79-86
  PubMedGoogle Scholar
• 62 Nishiuma S, Kario K, Yakushijin K, Maeda M, Murai R, Matsuo T, Ikeda U, Shimada K, Matsou M. Genetic variation in the promoter region of the beta-fibrinogen gene is associated with ischemic stroke in a Japanese population.  Blood Coagul Fibrinolysis. 1998;  9 373-379
  PubMedGoogle Scholar
• 63 Tsuda Y, Satoh K, Kitadai M, Takahashi T. Hemorheologic profiles of plasma fibrinogen and blood viscosity from silent to acute and chronic cerebral infarctions.  J Neurol Sci. 1997;  147 49-54
  CrossrefPubMedGoogle Scholar
• 64 Schwarz B, Bischof H, Kunze M. Hyperglycemia and coronary risk factors, results from western Austria.  Eur J Epidem. 1992;  8 40-47
  PubMedGoogle Scholar
• 65 Duong H, Melancon D, Tampieri D, Ethier R. The negative angiogram in subarachnoid haemorrhage.  Neuroradiology. 1996;  38 15-19
  CrossrefPubMedGoogle Scholar
• 66 Farrés M T, Ferras-Leite H, Schindler E, Mühlbauer M. Spontaneous subarachnoid hemorrhage with negative angiography: CT findings.  J Comput Assist Tomogr. 1992;  16 (4) 534-537
  CrossrefPubMedGoogle Scholar
• 67 Forster D MC, Steiner L, Hakanson S, Bergvall U. The value of repeat pan-angiography in cases of unexplained subarachnoid hemorrhage.  J Neurosurg. 1978;  48 712-716
  PubMedGoogle Scholar
• 68 Pinto A N, Ferro T M, Canhao P, Campos J. How often is a perimesencephalic subarachnoid haemorrhage CT pattern caused by ruptured aneurysms?.  Acta Neurochir. 1993;  124 78-81
  PubMedGoogle Scholar
• 69 Rinkel G JE, Wijdicks E FM, Vermeulen M, Ramos L MP, Tanghe H LJ, Kasan D, Meiners L C, Gijn J van. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture.  AJNR. 1991;  12 829-834
  PubMedGoogle Scholar
• 70 Schwartz T H, Mayer S A. Quadrigeminal variant of perimesencephalic nonaneurysmal subarachnoid hemorrhage.  Neurosurgery. 2000;  46 584-588
  CrossrefPubMedGoogle Scholar
• 71 Sheehan J M, Cloft H, Kassel N F. Symptomatic delayed arterial spasm following non-aneurysmal perimesencephalic subarachnoid hemorrhage: A case report and review of literature.  Acta Neurochir (Wien). 2000;  142 709-712
  CrossrefPubMedGoogle Scholar

Dr. Günther Kleinpeter

Neurochirurgie · Donauspital

Langobardenstraße 122

1220 Wien

Austria

Phone: +43-1-28802 3602

Fax: +43-1-28802 3680

Email: g.kleinpeter@billrothhaus.at