Predictors of Ventriculoperitoneal shunting following Subarachnoid Hemorrhage treated with External Ventricular Drainage

Abstract

Background/Objectives

Aneurysmal subarachnoid hemorrhage (aSAH) is commonly associated with hydrocephalus due to subarachnoid hemorrhage blood products obstructing cerebrospinal fluid outflow. Hydrocephalus after aSAH is routinely managed with temporary external ventricular drainage (EVD) followed by standard EVD weaning protocols, which determine the need for ventriculoperitoneal shunting (VPS). We sought to investigate aSAH patients who initially passed EVD weaning trials and had EVD removal, but later presented with recurrent, delayed, symptomatic hydrocephalus requiring a VPS.

Methods

We conducted a retrospective review of all patients at our tertiary care medical center who presented with aSAH, requiring an EVD. We analyzed variables associated with ultimate VPS dependency during hospitalization.

Results

We reviewed 489 patients with aSAH over a 6-year period (2008–2014). One hundred and thirty-eight (28.2%) developed hydrocephalus requiring a temporary EVD. Forty-four (31.9%) of these patients died or had withdrawal of care during admission, and were excluded from final analysis. Of the remaining 94 patients, 29 (30.9%) failed their clamp trial and required VPS. Sixty-five (69.1%) patients passed their clamp trial and were discharged without a VPS. However, 10 (15.4%) of these patients developed delayed hydrocephalus after discharge and ultimately required VPS [mean (range) days after discharge, 97.2 (35–188)]. Compared to early VPS, the delayed VPS group had a higher incidence of symptomatic vasospasm (90.0% vs 51.7%; P = 0.03). When comparing patients discharged from the hospital without VPS, delayed VPS patients also had higher 6- and 12-month mortality (P = 0.02) and longer EVD clamp trials (P < 0.01) than patients who never required VPS but had an EVD during hospitalization. Delayed hydrocephalus occurred in only 7.8% of patients who passed the initial EVD clamp trial, compared to 14.3% who failed the initial trial and 80.0% who failed 2 or more trials.

Conclusion

Patients who failed their initial or subsequent EVD clamp trials had a small, but increased risk of developing delayed hydrocephalus ultimately requiring VPS. Additionally, the majority of patients who presented with delayed hydrocephalus also suffered symptomatic vasospasm. These associations should be further explored and validated in a larger prospective study.

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References

  1. 1.

    Adams H, Ban VS, Leinonen V, et al. Risk of shunting after aneurysmal subarachnoid hemorrhage: a collaborative study and initiation of a consortium. Stroke. 2016;47:2488–96.

    Article  Google Scholar 

  2. 2.

    Chan M, Alaraj A, Calderon M, et al. Prediction of ventriculoperitoneal shunt dependency in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2009;110:44–9.

    Article  Google Scholar 

  3. 3.

    Chen Z, Chen G, Song W, Liu L, Yang Y, Ling F. Rehabilitation combined with ventriculoperitoneal shunt for patients with chronic normal pressure hydrocephalus due to aneurysm subarachnoid haemorrhage: a preliminary study. J Rehabil Med. 2009;41:1096–9.

    Article  Google Scholar 

  4. 4.

    Erixon HO, Sorteberg A, Sorteberg W, Eide PK. Predictors of shunt dependency after aneurysmal subarachnoid hemorrhage: results of a single-center clinical trial. Acta Neurochir (Wien). 2014;156:2059–69.

    Article  Google Scholar 

  5. 5.

    Yamada S, Nakase H, Park YS, Nishimura F, Nakagawa I. Discriminant analysis prediction of the need for ventriculoperitoneal shunt after subarachnoid hemorrhage. J Stroke Cerebrovasc Dis. 2012;21:493–7.

    Article  Google Scholar 

  6. 6.

    Czorlich P, Ricklefs F, Reitz M, et al. Impact of intraventricular hemorrhage measured by Graeb and LeRoux score on case fatality risk and chronic hydrocephalus in aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2015;157:409–15.

    Article  Google Scholar 

  7. 7.

    Lewis A, Irvine H, Ogilvy C, Kimberly WT. Predictors for delayed ventriculoperitoneal shunt placement after external ventricular drain removal in patients with subarachnoid hemorrhage. Br J Neurosurg. 2015;29:219–24.

    Article  Google Scholar 

  8. 8.

    Wilson CD, Safavi-Abbasi S, Sun H, et al. Meta-analysis and systematic review of risk factors for shunt dependency after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2017;126:586–95.

    Article  Google Scholar 

  9. 9.

    Paisan GM, Ding D, Starke RM, Crowley RW, Liu KC. Shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: predictors and long-term functional outcomes. Neurosurgery. 2017;83:393–402.

    Article  Google Scholar 

  10. 10.

    Pinggera D, Kerschbaumer J, Petr O, Ortler M, Thome C, Freyschlag CF. The volume of the third ventricle as a prognostic marker for shunt dependency after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2017;108:107–11.

    Article  Google Scholar 

  11. 11.

    Walcott BP, Iorgulescu JB, Stapleton CJ, Kamel H. Incidence, timing, and predictors of delayed shunting for hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2015;23:54–8.

    Article  Google Scholar 

  12. 12.

    von Elm E, Altman DG, Egger M, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370:1453–7.

    Article  Google Scholar 

  13. 13.

    Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2012;43:1711–37.

    Article  Google Scholar 

  14. 14.

    Moher D, Schulz KF, Altman D. The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomized trials. JAMA. 2001;285:1987–91.

    CAS  Article  Google Scholar 

  15. 15.

    Moher D, Schulz KF, Altman DG. The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomized trials. Ann Intern Med. 2001;134:657–62.

    CAS  Article  Google Scholar 

  16. 16.

    Moher D, Schulz KF, Altman DG. The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomised trials. Lancet. 2001;357:1191–4.

    CAS  Article  Google Scholar 

  17. 17.

    Chen S, Feng H, Sherchan P, et al. Controversies and evolving new mechanisms in subarachnoid hemorrhage. Prog Neurobiol. 2014;115:64–91.

    Article  Google Scholar 

  18. 18.

    Massicotte EM, Del Bigio MR. Human arachnoid villi response to subarachnoid hemorrhage: possible relationship to chronic hydrocephalus. J Neurosurg. 1999;91:80–4.

    CAS  Article  Google Scholar 

  19. 19.

    Suzuki H, Kinoshita N, Imanaka-Yoshida K, Yoshida T, Taki W. Cerebrospinal fluid tenascin-C increases preceding the development of chronic shunt-dependent hydrocephalus after subarachnoid hemorrhage. Stroke. 2008;39:1610–2.

    CAS  Article  Google Scholar 

  20. 20.

    Klopfenstein JD, Kim LJ, Feiz-Erfan I, et al. Comparison of rapid and gradual weaning from external ventricular drainage in patients with aneurysmal subarachnoid hemorrhage: a prospective randomized trial. J Neurosurg. 2004;100:225–9.

    Article  Google Scholar 

  21. 21.

    Lai L, Morgan MK. Predictors of in-hospital shunt-dependent hydrocephalus following rupture of cerebral aneurysms. J Clin Neurosci. 2013;20:1134–8.

    Article  Google Scholar 

  22. 22.

    Dorai Z, Hynan LS, Kopitnik TA, Samson D. Factors related to hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2003;52:763–9 (discussion 9–71).

    Article  Google Scholar 

  23. 23.

    Graff-Radford NR, Torner J, Adams HP Jr, Kassell NF. Factors associated with hydrocephalus after subarachnoid hemorrhage. A report of the Cooperative Aneurysm Study. Arch Neurol. 1989;46:744–52.

    CAS  Article  Google Scholar 

  24. 24.

    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;43:177–81.

    Article  Google Scholar 

  25. 25.

    Nissen JJ, Mantle D, Blackburn A, et al. The selectin superfamily: the role of selectin adhesion molecules in delayed cerebral ischaemia after aneurysmal subarachnoid haemorrhage. Acta Neurochir Suppl. 2000;76:55–60.

    CAS  PubMed  Google Scholar 

  26. 26.

    Polin RS, Bavbek M, Shaffrey ME, et al. Detection of soluble E-selectin, ICAM-1, VCAM-1, and L-selectin in the cerebrospinal fluid of patients after subarachnoid hemorrhage. J Neurosurg. 1998;89:559–67.

    CAS  Article  Google Scholar 

  27. 27.

    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;61:924–33 (discussion 33–34).

    Article  Google Scholar 

  28. 28.

    Rincon F, Gordon E, Starke RM, et al. Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg. 2010;113:774–80.

    Article  Google Scholar 

  29. 29.

    Miranda-Neto MH, Brancalhao RM, Chopard RP, Molinari SL. Morphological study of human arachnoid granulations with reference to their classification. Arq Neuropsiquiatr. 1994;52:41–5.

    CAS  Article  Google Scholar 

  30. 30.

    Kang DH, Park J, Park SH, Kim YS, Hwang SK, Hamm IS. Early ventriculoperitoneal shunt placement after severe aneurysmal subarachnoid hemorrhage: role of intraventricular hemorrhage and shunt function. Neurosurgery. 2010;66:904–8 (discussion 8–9).

    Article  Google Scholar 

  31. 31.

    Rammos S, Klopfenstein J, Augspurger L, et al. Conversion of external ventricular drains to ventriculoperitoneal shunts after aneurysmal subarachnoid hemorrhage: effects of site and protein/red blood cell counts on shunt infection and malfunction. J Neurosurg. 2008;109:1001–4.

    Article  Google Scholar 

  32. 32.

    Ikushima I, Korogi Y, Makita O, et al. MRI of arachnoid granulations within the dural sinuses using a FLAIR pulse sequence. Br J Radiol. 1999;72:1046–51.

    CAS  Article  Google Scholar 

  33. 33.

    Koshikawa T, Naganawa S, Fukatsu H, Ishiguchi T, Ishigaki T. Arachnoid granulations on high-resolution MR images and diffusion-weighted MR images: normal appearance and frequency. Radiat Med. 2000;18:187–91.

    CAS  PubMed  Google Scholar 

  34. 34.

    Leach JL, Jones BV, Tomsick TA, Stewart CA, Balko MG. Normal appearance of arachnoid granulations on contrast-enhanced CT and MR of the brain: differentiation from dural sinus disease. AJNR Am J Neuroradiol. 1996;17:1523–32.

    CAS  PubMed  Google Scholar 

  35. 35.

    Roche J, Warner D. Arachnoid granulations in the transverse and sigmoid sinuses: CT, MR, and MR angiographic appearance of a normal anatomic variation. AJNR Am J Neuroradiol. 1996;17:677–83.

    CAS  PubMed  Google Scholar 

  36. 36.

    Abe K, Ono Y, Yoneyama H, et al. Assessment of cerebrospinal fluid flow patterns using the time-spatial labeling inversion pulse technique with 3T MRI: early clinical experiences. Neuroradiol J. 2014;27:268–79.

    Article  Google Scholar 

  37. 37.

    Forner Giner J, Sanz-Requena R, Florez N, et al. Quantitative phase-contrast MRI study of cerebrospinal fluid flow: a method for identifying patients with normal-pressure hydrocephalus. Neurologia. 2014;29:68–75.

    CAS  Article  Google Scholar 

  38. 38.

    Hasiloglu ZI, Albayram S, Gorucu Y, et al. Assessment of CSF flow dynamics using PC-MRI in spontaneous intracranial hypotension. Headache. 2012;52:808–19.

    Article  Google Scholar 

  39. 39.

    Hodel J, Rahmouni A, Zins M, Vignaud A, Decq P. Magnetic resonance imaging of noncommunicating hydrocephalus. World Neurosurg. 2013;79(S21):e9–12.

    Google Scholar 

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OOA contributed to conception/design, data collection/analysis/interpretation, manuscript writing/critical revision, tables/figures. TGV-B contributed to data collection, tables/figures. NH contributed to manuscript writing/critical revision. SG contributed to data collection. NM contributed to data collection. RGT and MTT contributed to manuscript critical revision. WDF contributed to conception/design, manuscript critical revision. All authors approved the final article.

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Correspondence to William D. Freeman.

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Akinduro, O.O., Vivas-Buitrago, T.G., Haranhalli, N. et al. Predictors of Ventriculoperitoneal shunting following Subarachnoid Hemorrhage treated with External Ventricular Drainage. Neurocrit Care 32, 755–764 (2020). https://doi.org/10.1007/s12028-019-00802-8

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Keywords

  • Aneurysm
  • Subarachnoid hemorrhage
  • Arachnoid granulations
  • Chronic hydrocephalus
  • Vasospasm