J Neurol Surg A Cent Eur Neurosurg 2015; 76(02): 126-132
DOI: 10.1055/s-0034-1394189
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Intraventricular Hemorrhage Is Associated with Early Hydrocephalus, Symptomatic Vasospasm, and Poor Outcome in Aneurysmal Subarachnoid Hemorrhage

Thomas J. Wilson
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
William R. Stetler Jr.
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
Matthew C. Davis
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
David A. Giles
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
Adam Khan
2   Department of Radiology, University of Michigan, Ann Arbor, Michigan, United States
Neeraj Chaudhary
2   Department of Radiology, University of Michigan, Ann Arbor, Michigan, United States
Joseph J. Gemmete
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
Guohua Xi
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
B. Gregory Thompson
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
Aditya S. Pandey
1   Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan, United States
› Author Affiliations
Further Information

Publication History

16 October 2013

23 May 2014

Publication Date:
29 December 2014 (online)


Objective We hypothesized that the subset of patients with early hydrocephalus following aneurysmal subarachnoid hemorrhage may represent a subset of patients with a more vehement inflammatory reaction to blood products in the subarachnoid space. We thus examined risk factors for early hydrocephalus and examined the relationship between early hydrocephalus and symptomatic vasospasm as well as clinical outcome.

Methods We retrospectively analyzed all patients presenting to our institution with subarachnoid hemorrhage over a 7-year period. We examined for risk factors, including early hydrocephalus, for poor clinical outcome and symptomatic vasospasm.

Results We found intraventricular hemorrhage to be strongly associated with the development of early hydrocephalus. In univariate analysis, early hydrocephalus was strongly associated with both poor functional outcome and symptomatic vasospasm. In multivariate analysis, intraventricular hemorrhage and tobacco use were associated with symptomatic vasospasm; intraventricular hemorrhage, intraparenchymal hemorrhage, and symptomatic vasospasm were associated with poor functional outcome.

Conclusions We found that intraventricular hemorrhage was strongly associated with early hydrocephalus. Further exploration of the mechanistic explanation is needed, but we suggest this may be from a combination of obstruction of cerebrospinal fluid pathways by blood products and inflammation in the choroid plexus resulting in increased cerebrospinal fluid production. Further, we suggest that both early hydrocephalus and cerebral vasospasm may be parts of the overall inflammatory cascade that occurs with intraventricular hemorrhage and ultimately results in a poorer clinical outcome.

  • References

  • 1 Kusske JA, Turner PT, Ojemann GA, Harris AB. Ventriculostomy for the treatment of acute hydrocephalus following subarachnoid hemorrhage. J Neurosurg 1973; 38 (5) 591-595
  • 2 Pertuiset B, Houtteville JP, George B, Margent P. Early ventricular dilatation and hydrocephalus following rupture of supratentorial arterial aneurysms [in French]. Neurochirurgia (Stuttg) 1972; 15 (4) 113-126
  • 3 Raimondi AJ, Torres H. Acute hydrocephalus as a complication of subarachnoid hemorrhage. Surg Neurol 1973; 1 (1) 23-26
  • 4 Vassilouthis J, Richardson AE. Ventricular dilatation and communicating hydrocephalus following spontaneous subarachnoid hemorrhage. J Neurosurg 1979; 51 (3) 341-351
  • 5 Hasan D, Vermeulen M, Wijdicks EF, Hijdra A, van Gijn J. Management problems in acute hydrocephalus after subarachnoid hemorrhage. Stroke 1989; 20 (6) 747-753
  • 6 Graff-Radford NR, Torner J, Adams Jr HP, Kassell NF. Factors associated with hydrocephalus after subarachnoid hemorrhage. A report of the Cooperative Aneurysm Study. Arch Neurol 1989; 46 (7) 744-752
  • 7 Shah AH, Komotar RJ. Pathophysiology of acute hydrocephalus after subarachnoid hemorrhage. World Neurosurg 2013; 80 (3–4) 304-306
  • 8 Dóczi T, Szerdahelyi P, Gulya K, Kiss J. Brain water accumulation after the central administration of vasopressin. Neurosurgery 1982; 11 (3) 402-407
  • 9 Hasan D, Tanghe HL. Distribution of cisternal blood in patients with acute hydrocephalus after subarachnoid hemorrhage. Ann Neurol 1992; 31 (4) 374-378
  • 10 Kanat A, Turkmenoglu O, Aydin MD , et al. Toward changing of the pathophysiologic basis of acute hydrocephalus after subarachnoid hemorrhage: a preliminary experimental study. World Neurosurg 2013; 80 (3–4) 390-395
  • 11 Barkovich AJ, Edwards MS. Applications of neuroimaging in hydrocephalus. Pediatr Neurosurg 1992; 18 (2) 65-83
  • 12 Diringer MN, Edwards DF, Zazulia AR. Hydrocephalus: a previously unrecognized predictor of poor outcome from supratentorial intracerebral hemorrhage. Stroke 1998; 29 (7) 1352-1357
  • 13 Connolly Jr ES, Rabinstein AA, Carhuapoma JR , et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. 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) 1711-1737
  • 14 Komotar RJ, Hahn DK, Kim GH , et al. The impact of microsurgical fenestration of the lamina terminalis on shunt-dependent hydrocephalus and vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 2008; 62 (1) 123-132 ; discussion 132–134
  • 15 Little AS, Zabramski JM, Peterson M , et al. Ventriculoperitoneal shunting after aneurysmal subarachnoid hemorrhage: analysis of the indications, complications, and outcome with a focus on patients with borderline ventriculomegaly. Neurosurgery 2008; 62 (3) 618-627 ; discussion 618–627
  • 16 de Oliveira JG, Beck J, Setzer M , et al. Risk of shunt-dependent hydrocephalus after occlusion of ruptured intracranial aneurysms by surgical clipping or endovascular coiling: a single-institution series and meta-analysis. Neurosurgery 2007; 61 (5) 924-933 ; discussion 933–934
  • 17 Mura J, Rojas-Zalazar D, Ruíz A, Vintimilla LC, Marengo JJ. Improved outcome in high-grade aneurysmal subarachnoid hemorrhage by enhancement of endogenous clearance of cisternal blood clots: a prospective study that demonstrates the role of lamina terminalis fenestration combined with modern microsurgical cisternal blood evacuation. Minim Invasive Neurosurg 2007; 50 (6) 355-362
  • 18 Kwon JH, Sung SK, Song YJ, Choi HJ, Huh JT, Kim HD. Predisposing factors related to shunt-dependent chronic hydrocephalus after aneurysmal subarachnoid hemorrhage. J Korean Neurosurg Soc 2008; 43 (4) 177-181
  • 19 Hellingman CA, van den Bergh WM, Beijer IS , et al. Risk of rebleeding after treatment of acute hydrocephalus in patients with aneurysmal subarachnoid hemorrhage. Stroke 2007; 38 (1) 96-99
  • 20 Rincon F, Gordon E, Starke RM , et al. Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 2010; 113 (4) 774-780
  • 21 Levi B, Sugg KB, Lien SC , et al. Outcomes of tethered cord repair with a layered soft tissue closure. Ann Plast Surg 2013; 70 (1) 74-78
  • 22 Breeze RE, McComb JG, Hyman S, Gilles FH. CSF production in acute ventriculitis. J Neurosurg 1989; 70 (4) 619-622
  • 23 Kaestner S, Dimitriou I. TGF beta1 and TGF beta2 and their role in posthemorrhagic hydrocephalus following SAH and IVH. J Neurol Surg A Cent Eur Neurosurg 2013; 74 (5) 279-284
  • 24 Dietrich HH, Dacey Jr RG. Molecular keys to the problems of cerebral vasospasm. Neurosurgery 2000; 46 (3) 517-530
  • 25 Sonobe M, Suzuki J. Vasospasmogenic substance produced following subarachnoid haemorrhage, and its fate. Acta Neurochir (Wien) 1978; 44 (1–2) 97-106
  • 26 Ladner TR, Zuckerman SL, Mocco J. Genetics of cerebral vasospasm. Neurol Res Int 2013; 2013: 291895
  • 27 Chaichana KL, Pradilla G, Huang J, Tamargo RJ. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg 2010; 73 (1) 22-41
  • 28 Edwards DH, Griffith TM, Ryley HC, Henderson AH. Haptoglobin-haemoglobin complex in human plasma inhibits endothelium dependent relaxation: evidence that endothelium derived relaxing factor acts as a local autocoid. Cardiovasc Res 1986; 20 (8) 549-556
  • 29 Saeed SA, Ahmad N, Ahmed S. Dual inhibition of cyclooxygenase and lipoxygenase by human haptoglobin: its polymorphism and relation to hemoglobin binding. Biochem Biophys Res Commun 2007; 353 (4) 915-920
  • 30 Agil A, Fuller CJ, Jialal I. Susceptibility of plasma to ferrous iron/hydrogen peroxide-mediated oxidation: demonstration of a possible Fenton reaction. Clin Chem 1995; 41 (2) 220-225
  • 31 Kumar A, Brown R, Dhar R , et al. Early vs. delayed cerebral infarction following aneurysm repair after subarachnoid hemorrhage. Neurosurgery 2013; 73 (4) 617-623
  • 32 Güresir E, Beck J, Vatter H , et al. Subarachnoid hemorrhage and intracerebral hematoma: incidence, prognostic factors, and outcome. Neurosurgery 2008; 63 (6) 1088-1093 ; discussion 1093–1094