A sustained systemic inflammatory response syndrome is associated with shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage

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OBJECTIVE

The authors sought to evaluate whether a sustained systemic inflammatory response was associated with shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage.

METHODS

A retrospective analysis of 193 consecutive patients with aneurysmal subarachnoid hemorrhage was performed. Management of hydrocephalus followed a stepwise algorithm to determine the need for external CSF drainage and subsequent shunt placement. Systemic inflammatory response syndrome (SIRS) data were collected for all patients during the first 7 days of hospitalization. Patients who met the SIRS criteria every day for the first 7 days of hospitalization were considered as having a sustained SIRS. Univariate and multivariate regression analyses were used to determine predictors of shunt dependence.

RESULTS

Sixteen percent of patients required shunt placement. Sustained SIRS was observed in 35% of shunt-dependent patients compared to 14% in non–shunt-dependent patients (p = 0.004). On multivariate logistic regression, female sex (OR 0.35, 95% CI 0.142–0.885), moderate to severe vasospasm (OR 3.78, 95% CI 1.333–10.745), acute hydrocephalus (OR 21.39, 95% CI 2.260–202.417), and sustained SIRS (OR 2.94, 95% CI 1.125–7.689) were significantly associated with shunt dependence after aneurysmal subarachnoid hemorrhage. Receiver operating characteristic analysis revealed an area under the curve of 0.83 for the final regression model.

CONCLUSIONS

Sustained SIRS was a predictor of shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage even after adjustment for potential confounding variables in a multivariate logistic regression model.

ABBREVIATIONS AUC = area under the curve; CTA = CT angiography; DND = delayed neurological deficit; DSA = digital subtraction angiography; EVD = external ventricular drain; MFS = modified Fisher scale; NF = nuclear factor; ROC = receiver operating characteristic; SIRS = systemic inflammatory response syndrome; TGF = transforming growth factor; WFNS = World Federation of Neurosurgical Societies.

Article Information

Correspondence Aaron P. Wessell: University of Maryland School of Medicine, Baltimore, MD. awessell@som.umaryland.edu.

INCLUDE WHEN CITING Published online June 29, 2018; DOI: 10.3171/2018.1.JNS172925.

Disclosures Dr. Jindal reports receiving research grant funding from Stryker Neurovascular.

© AANS, except where prohibited by US copyright law.

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Figures

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    Flow chart outlining patient selection criteria leading to 193 included study patients.

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    ROC curve for final regression model predicting shunt dependence (AUC = 0.8344). Figure is available in color online only.

References

  • 1

    Banizs BPike MMMillican CLFerguson WBKomlosi PSheetz J: Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 132:532953392005

  • 2

    Bartlett JGGerding DN: Clinical recognition and diagnosis of Clostridium difficile infection. Clin Infect Dis 46 (Suppl 1):S12S182008

  • 3

    Connolly ES JrRabinstein AACarhuapoma JRDerdeyn CPDion JHigashida RT: Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43:171117372012

  • 4

    Dhar RDiringer MN: The burden of the systemic inflammatory response predicts vasospasm and outcome after subarachnoid hemorrhage. Neurocrit Care 8:4044122008

  • 5

    Erixon HOSorteberg ASorteberg WEide PK: Predictors of shunt dependency after aneurysmal subarachnoid hemorrhage: results of a single-center clinical trial. Acta Neurochir (Wien) 156:205920692014

  • 6

    Frontera JAClaassen JSchmidt JMWartenberg KETemes RConnolly ES Jr: Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery 59:21272006

  • 7

    Frontera JAFernandez ASchmidt JMClaassen JWartenberg KEBadjatia N: Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke 40:196319682009

  • 8

    Gruber AReinprecht AIllievich UMFitzgerald RDietrich WCzech T: Extracerebral organ dysfunction and neurologic outcome after aneurysmal subarachnoid hemorrhage. Crit Care Med 27:5055141999

  • 9

    Gruber ARössler KGraninger WDonner AIllievich MUCzech T: Ventricular cerebrospinal fluid and serum concentrations of sTNFR-I, IL-1ra, and IL-6 after aneurysmal subarachnoid hemorrhage. J Neurosurg Anesthesiol 12:2973062000

  • 10

    Güresir ESchuss PBorger VVatter H: Experimental subarachnoid hemorrhage: double cisterna magna injection rat model—assessment of delayed pathological effects of cerebral vasospasm. Transl Stroke Res 6:2422512015

  • 11

    Hirashima YNakamura SEndo SKuwayama NNaruse YTakaku A: Elevation of platelet activating factor, inflammatory cytokines, and coagulation factors in the internal jugular vein of patients with subarachnoid hemorrhage. Neurochem Res 22:124912551997

  • 12

    Hooton TMBradley SFCardenas DDColgan RGeerlings SERice JC: Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin Infect Dis 50:6256632010

  • 13

    Howell MDDavis AM: Management of sepsis and septic shock. JAMA 317:8478482017

  • 14

    Jabbarli RBohrer AMPierscianek DMüller DWrede KHDammann P: The CHESS score: a simple tool for early prediction of shunt dependency after aneurysmal subarachnoid hemorrhage. Eur J Neurol 23:9129182016

  • 15

    Kalil ACMetersky MLKlompas MMuscedere JSweeney DAPalmer LB: Management of adults with hospital-acquired and ventilator-associated pneumonia: 2016 clinical practice guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis 63:e61e1112016

  • 16

    Kanat ATurkmenoglu OAydin MDYolas CAydin NGursan N: Toward changing of the pathophysiologic basis of acute hydrocephalus after subarachnoid hemorrhage: a preliminary experimental study. World Neurosurg 80:3903952013

  • 17

    Kanev PMSheehan JM: Reflections on shunt infection. Pediatr Neurosurg 39:2852902003

  • 18

    Karimy JKDuran DHu JKGavankar CGaillard JRBayri Y: Cerebrospinal fluid hypersecretion in pediatric hydrocephalus. Neurosurg Focus 41(5):E102016

  • 19

    Karimy JKZhang JKurland DBTheriault BCDuran DStokum JA: Inflammation-dependent cerebrospinal fluid hypersecretion by the choroid plexus epithelium in posthemorrhagic hydrocephalus. Nat Med 23:99710032017

  • 20

    Kassell NFTorner JCHaley EC JrJane JAAdams HPKongable GL: The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg 73:18361990

  • 21

    Lai LMorgan MK: Predictors of in-hospital shunt-dependent hydrocephalus following rupture of cerebral aneurysms. J Clin Neurosci 20:113411382013

  • 22

    Lattke MMagnutzki AWalther PWirth TBaumann B: Nuclear factor κB activation impairs ependymal ciliogenesis and links neuroinflammation to hydrocephalus formation. J Neurosci 32:11511115232012

  • 23

    Li TZhang PYuan BZhao DChen YZhang X: Thrombin-induced TGF-β1 pathway: a cause of communicating hydrocephalus post subarachnoid hemorrhage. Int J Mol Med 31:6606662013

  • 24

    Little ASZabramski JMPeterson MGoslar PWWait SDAlbuquerque FC: Ventriculoperitoneal shunting after aneurysmal subarachnoid hemorrhage: analysis of the indications, complications, and outcome with a focus on patients with borderline ventriculomegaly. Neurosurgery 62:6186272008

  • 25

    Lu QElston RC: Using the optimal receiver operating characteristic curve to design a predictive genetic test, exemplified with type 2 diabetes. Am J Hum Genet 82:6416512008

  • 26

    Mathiesen TLefvert AK: Cerebrospinal fluid and blood lymphocyte subpopulations following subarachnoid haemorrhage. Br J Neurosurg 10:89921996

  • 27

    McKeating EGAndrews PJSignorini DFMascia L: Transcranial cytokine gradients in patients requiring intensive care after acute brain injury. Br J Anaesth 78:5205231997

  • 28

    O’Kelly CJKulkarni AVAustin PCUrbach DWallace MC: Shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: incidence, predictors, and revision rates. Clinical article. J Neurosurg 111:102910352009

  • 29

    Rincon FGordon EStarke RMBuitrago MMFernandez ASchmidt JM: Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 113:7747802010

  • 30

    Saliou GBalédent OLehmann PParadot GGondry-Jouet CBouzerar R: [Acute CSF changes in the mesencephalon aqueduct after subarachnoid hemorrhage as measured by PC-MRI.] J Neuroradiol 36:41472009 (Fr)

  • 31

    Saliou GParadot GGondry CBouzerar RLehmann PMeyers ME: A phase-contrast MRI study of acute and chronic hydrodynamic alterations after hydrocephalus induced by subarachnoid hemorrhage. J Neuroimaging 22:3433502012

  • 32

    Simard PFTosun CMelnichenko LIvanova SGerzanich VSimard JM: Inflammation of the choroid plexus and ependymal layer of the ventricle following intraventricular hemorrhage. Transl Stroke Res 2:2272312011

  • 33

    Tam AKIlodigwe DMocco JMayer SKassell NRuefenacht D: Impact of systemic inflammatory response syndrome on vasospasm, cerebral infarction, and outcome after subarachnoid hemorrhage: exploratory analysis of CONSCIOUS-1 database. Neurocrit Care 13:1821892010

  • 34

    Tan QChen QFeng ZShi XTang JTao Y: Cannabinoid receptor 2 activation restricts fibrosis and alleviates hydrocephalus after intraventricular hemorrhage. Brain Res 1654 (Pt A):24332017

  • 35

    Teasdale GMDrake CGHunt WKassell NSano KPertuiset B: A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry 51:14571988

  • 36

    Tso MKIbrahim GMMacdonald RL: Predictors of shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage. World Neurosurg 86:2262322016

  • 37

    Tunkel ARHasbun RBhimraj AByers KKaplan SLScheld WM: 2017 Infectious Diseases Society of America’s clinical practice guidelines for healthcare-associated ventriculitis and meningitis. Clin Infect Dis 64:e34e652017

  • 38

    Varatharaj AGalea I: The blood-brain barrier in systemic inflammation. Brain Behav Immun 60:1122017

  • 39

    Walcott BPIorgulescu JBStapleton CJKamel H: Incidence, timing, and predictors of delayed shunting for hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurocrit Care 23:54582015

  • 40

    Wang YMLin YJChuang MJLee THTsai NWCheng BC: Predictors and outcomes of shunt-dependent hydrocephalus in patients with aneurysmal sub-arachnoid hemorrhage. BMC Surg 12:122012

  • 41

    Weidauer SLanfermann HRaabe AZanella FSeifert VBeck J: Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 38:183118362007

  • 42

    Wostrack MReeb TMartin JKehl VShiban EPreuss A: Shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: the role of intrathecal interleukin-6. Neurocrit Care 21:78842014

  • 43

    Yan HChen YLi LJiang JWu GZuo Y: Decorin alleviated chronic hydrocephalus via inhibiting TGF-β1/Smad/CTGF pathway after subarachnoid hemorrhage in rats. Brain Res 1630:2412532016

  • 44

    Yoshimoto YTanaka YHoya K: Acute systemic inflammatory response syndrome in subarachnoid hemorrhage. Stroke 32:198919932001

  • 45

    Zaidi HAMontoure AElhadi ANakaji PMcDougall CGAlbuquerque FC: Long-term functional outcomes and predictors of shunt-dependent hydrocephalus after treatment of ruptured intracranial aneurysms in the BRAT trial: revisiting the clip vs coil debate. Neurosurgery 76:6086142015

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