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Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy
Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy Eric W. Sankey a, Ignacio Jusué-Torres a, Benjamin D. Elder a,⇑, C. Rory Goodwin a, Sachin Batra a, Jamie Hoffberger a, Jennifer Lu a, Ari M. Blitz b, Daniele Rigamonti a a b
Department of Neurosurgery, The Johns Hopkins Hospital, 600 N Wolfe Street, Phipps 126, Baltimore, MD, USA Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA
a r t i c l e
i n f o
Article history: Received 9 February 2015 Accepted 14 February 2015 Available online xxxx Keywords: Endoscopic third ventriculostomy Idiopathic normal pressure hydrocephalus Timed up and go Tinetti performance oriented mobility assessment
a b s t r a c t We evaluated if patients with idiopathic normal pressure hydrocephalus (iNPH) showed functional improvement after primary endoscopic third ventriculostomy (ETV). The efficacy of ETV for iNPH remains controversial. We retrospectively reviewed 10 consecutive patients treated between 2009 and 2011 with ETV for iNPH. Seven patients with a median age of 73 years (range: 60–80) who underwent a primary ETV for iNPH were included for analysis. Median follow-up was 39 months (range: 26–46). Post-ETV stoma and aqueductal and cisternal flows were confirmed via high resolution, gradient echo and phase contrast MRI. Post-ETV timed up and go (TUG) and Tinetti performance oriented mobility assessment scores were compared to pre- and post-lumbar puncture (LP) values. A second LP was performed if ETV failed to sustain the observed improvement after initial LP. Patients who demonstrated ETV failure were subsequently shunted. Compared to pre-LP TUG and Tinetti values of 14.00 seconds (range: 12.00–23.00) and 22 (range: 16–24), post-LP scores improved to 11.00 seconds (range: 8.64–15.00; p = 0.06) and 25 (range: 24–28; p = 0.02), respectively. ETV failed to sustain this improvement with slight worsening between pre-LP and post-ETV TUG and Tinetti scores. Improvement from pre-LP assessment was regained after shunting and at last follow-up with TUG and Tinetti scores of 12.97 seconds (range: 9.00–18.00; p = 0.250) and 25 (range: 18–27; p = 0.07), and 11.87 seconds (range: 8.27–18.50; p = 0.152) and 23 (range: 18–26; p = 0.382), respectively. Despite stoma patency, ETV failed to sustain functional improvement seen after LP, however, improvement was regained after subsequent shunting suggesting that shunt placement remains the preferred treatment for iNPH. Published by Elsevier Ltd.
1. Introduction Idiopathic normal pressure hydrocephalus (iNPH) is a common and treatable neurological disorder that occurs in the elderly, and most often results in progressive gait impairment, urinary incontinence and cognitive deterioration [1,2]. Surgery is warranted in the majority of patients with symptomatic iNPH as cerebrospinal fluid (CSF) diversion results in symptomatic improvement in up to 80– 90% of individuals [1]. Potential options for CSF diversion in iNPH patients include ventriculoperitoneal (VP) shunt placement and endoscopic third ventriculostomy (ETV). Although ETV is considered a preferred treatment for obstructive hydrocephalus [3], its use in iNPH remains controversial with studies displaying contradictory outcomes [4]. Likewise, while the
⇑ Corresponding author. Tel.: +1 14109555000. E-mail address: [email protected] (B.D. Elder).
efficacy of ETV for obstructive hydrocephalus is easily understood as a means to bypass an obstructive lesion, the mechanism by which ETV may work in iNPH is not well understood. ETV is considered to be a safe and relatively simple procedure [5] with a lower risk of infection and delayed failure compared to VP shunts [6–8], however, careful consideration of the risk-benefit ratio related to each treatment option must be performed to determine the most appropriate modality for hydrocephalus management. As such, more data is needed regarding the outcomes in patients with iNPH following ETV compared to VP shunt placement. Previous studies regarding the success of ETV in patients with iNPH were limited by the fact that often CT scan instead of MRI was used as the imaging modality and by the fact that third ventricle morphology was not used as inclusion/exclusion criteria [9–11] despite the significant association between third ventricle morphology and outcomes after ETV [12]. As a result, the majority of these studies likely included patients with obstructive etiologies with either triventricular enlargement (unrecognized aqueductal
http://dx.doi.org/10.1016/j.jocn.2015.02.019 0967-5868/Published by Elsevier Ltd.
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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E.W. Sankey et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
obstruction on CT scan) or tetraventricular enlargement such as infratentorial intracisternal obstructive hydrocephalus [13,14]. Therefore, prior studies have potentially included better results that are not applicable to patients with iNPH. It is essential, therefore, to ensure that only patients with clinically and radiographically confirmed iNPH are included in studies evaluating the efficacy of ETV for iNPH. In the present study, we evaluated functional gait outcomes (as indicated by the change in timed up and go [TUG] and Tinetti performance oriented mobility assessment scores during follow-up) after primary ETV in patients with a confirmed diagnosis of iNPH and normal third ventricle morphology. 2. Materials and methods 2.1. Patients Under an active Institutional Review Board approved protocol, the medical records of 10 consecutive patients treated with ETV for iNPH by the senior author between 2009 and 2011, were retrospectively reviewed. Of note, 107 new shunts were placed by the senior author for the treatment of obstructive hydrocephalus presenting as iNPH during the same time period. After discussion regarding the known treatment options for iNPH, 10 patients chose to undergo ETV instead of shunting. All patients were adults (>21 years of age). Seven patients (70%) with iNPH who received an ETV as their primary treatment were included for analysis (Table 1). A total of three patients (30%) were excluded, one (10%) because of secondary iNPH resulting from an intracranial infection, one (10%) with iNPH who had a history of previous shunt placement, and one (10%) with iNPH who was lost to follow-up after discharge. Preoperative high resolution, gradient echo MRI sequences were obtained to confirm the absence of an obstructive etiology, and displayed a normal third ventricle morphology in all patients (Fig. 1). All patients received a lumbar puncture (LP) prior
Table 1 Idiopathic normal pressure hydrocephalus patient characteristics Characteristics
iNPH patients (n = 7)
Age, years, median (range) Sex, female, n (%) Race, n (%) Caucasian Symptoms at presentation, n (%) Gait impairment Urinary incontinence Cognitive dysfunction Vision deficit Headaches Nausea Dizziness Duration of symptoms prior to ETV, months, median (range) Complications, n (%) Intraoperative Postoperative Follow-up duration, months, median (range)
73 (60–80) 3 (43) 7 (100) 7 (100) 7 (100) 5 (71) 0 (0) 1 (14) 0 (0) 3 (43) 24 (5–60)
0 (0) 0 (0) 39 (26–46)
Pre-LP quantitative tests
iNPH patients (n = 7)
MMSE, median (range) TUG, seconds, median (range)
27 (25–29) 14.00 (12.00– 23.00) 22 (16–24) 0.36 (0.33–0.39)
Tinetti, median (range) Evan’s index, median (range)
ETV = endoscopic third ventriculostomy, iNPH = idiopathic normal pressure hydrocephalus, LP = lumbar puncture, MMSE = mini-mental state examination, Tinetti = Tinetti performance oriented mobility score, TUG = timed up and go.
to ETV and had a preoperative opening pressure <25 cm H2O, supporting the diagnosis of iNPH. Demographic information concerning sex, race, age at treatment, and previous shunting were collected. Baseline data concerning the duration of symptoms prior to ETV, Evan’s index, and presenting symptoms were obtained. Baseline and post-LP TUG and Tinetti scores were reviewed prior to ETV. Quantitative, continuous data are expressed in median (range) for non-parametric variables, and categorical data are expressed as frequency (percentage). 2.2. Clinical and radiologic follow-up All intraoperative and postoperative complications that occurred within 6 weeks postoperatively were recorded. Post-ETV TUG and Tinetti scores were compared to pre- and post-LP values prior to ETV. Higher values of mini–mental state examination (MMSE; 30 points) and Tinetti (28 points) and lower values of TUG indicate better performance. Recurrence free probability was determined by the time to symptom recurrence after ETV (Fig. 2). A second LP was performed if the ETV failed to sustain the observed improvement after initial LP, despite stoma patency. After ETV failure, patients who demonstrated improvement after a second LP were considered for repeat ETV or VP shunting. Postoperative ETV patency and aqueductal and cisternal flow were assessed by high resolution, gradient echo MRI and flow pulsatility through the stoma on phase contrast MRI. 3. Results Three Caucasian women (43%) and four men (57%) with iNPH underwent ETV as their primary treatment modality. The median age at treatment was 73 years (range: 60–80). The median duration of symptoms prior to ETV was 24 months (range: 5–60). Preoperative Evan’s index was 0.36 (range: 0.33–0.38). All patients presented with gait impairment and urinary incontinence and five (71%) displayed signs of cognitive dysfunction. Median baseline pre-LP MMSE, TUG, and Tinetti scores were 27 (range: 25–29), 14.00 seconds (range: 12.00–23.00) and 22 (range: 16–24), respectively. No intraoperative or postoperative complications occurred during the primary ETV or subsequent shunt placement. After an initial LP, the TUG and Tinetti scores improved to 11.00 seconds (range: 8.64–15.00; p = 0.06) and 25 (range: 24– 28; p = 0.02), respectively (Fig. 3). However, this improvement was not sustained after ETV with slight worsening observed between pre-LP and post-ETV TUG and Tinetti scores (Fig. 4). All patients also showed symptomatic ETV failure after a median of 9 months (range: 0–24; Fig. 2) despite evidence of a patent stoma on imaging. Patients were re-evaluated with a new LP after ETV failure and subsequently shunted after displaying improvement from pre-LP values following the second-LP. Improvement from pre-LP assessment was regained after shunting and at last follow-up with TUG and Tinetti scores of 12.97 seconds (range: 9.00–18.00; p = 0.250) and 25 (range: 18–27; p = 0.07), and 11.87 seconds (range: 8.27–18.50; p = 0.152) and 23 (range: 18– 26; p = 0.382), respectively (Fig. 4). Follow-up duration was a median of 39 months (range: 26–46). 4. Discussion Data from the present study suggests that primary ETV fails to improve mobility, assessed by TUG and Tinetti, in patients with confirmed iNPH and normal third ventricle morphology while subsequent shunt placement regained the improvement seen after a trial of CSF drainage via LP. As prior studies describing ETV use in
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
E.W. Sankey et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
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Fig. 1. Baseline sagittal high resolution, gradient echo MRI showing a concave lamina terminalis and third ventricular floor, indicated by arrows, in a patient with idiopathic normal pressure hydrocephalus.
Fig. 2. Kaplan–Meier curve showing recurrence free probability for the time to symptom recurrence post-endoscopic third ventriculostomy. All patients showed symptomatic endoscopic third ventriculostomy failure after a median of 9 months (range 0–24).
iNPH did not use third ventricle morphology as an inclusion/exclusion criterion or they included patient cohorts with both idiopathic and secondary NPH, our results are unique; we analyzed a homogenous cohort with both radiographically and clinically confirmed iNPH. In addition, ETV was performed as a primary treatment for iNPH after improvement with a CSF drainage trial, predicting potential success with CSF diversion irrespective of the method of treatment. Our data supports the use of VP shunting as the treatment of choice for iNPH and suggests that ETV is an ineffective treatment modality for the management of this challenging condition. The most common presenting symptom in patients with iNPH is gait impairment [15]. Functional outcomes related to gait can be accurately assessed using reliable and validated performance measures such as the TUG test and Tinetti performance oriented mobility assessment. These assessments often allow clinicians to objectively monitor the change in mobility in patients with suspected iNPH during treatment [16]. However, our anecdotal experience suggests that these measures may not be sensitive enough to detect small changes in gait with patients often reporting a subjective worsening with ambulation despite favorable TUG and Tinetti scores. ETV is a highly effective treatment for patients with obstructive hydrocephalus and it has also been used in several studies to treat
communicating hydrocephalus with contradictory results [4]. For example, ETV has been considered as a viable treatment option in select patients with communicating hydrocephalus such as those with mild impairment and aged under 65 years [10]. Since the etiology of communicating hydrocephalus remains unclear, the mechanism by which ETV is proposed to work in patients with iNPH is also not well understood. Yet, studies using magnetic resonance elastography have shown that there is clear evidence of tissue degradation associated with iNPH leading to altered viscoelastic properties of brain tissue during disease progression and tissue repair [17,18]. One potential explanation is that communicating hydrocephalus results in decreased intracranial compliance leading to increased intracranial systolic pulse pressure and ultimately to a decrease in cerebral blood flow. As such, ETV may exert its effect in these patients by effectively decreasing intracranial systolic pulse pressure via CSF diversion through the third ventricular floor, ultimately improving cerebral blood flow and perfusion pressure and eliminating transependymal resorption of CSF [4]. Another potential explanation by Longatti et al. is that iNPH may cause an intermittent functional aqueductal stenosis stemming from continuous systolic pulsations in the context of decreased intracranial compliance [19]. Thus, ETV may provide a conduit to bypass this functional obstruction similar to its effect in obstructive hydrocephalus. However, the results of most studies endorse substantially better outcomes after ETV in the management of obstructive hydrocephalus as compared to communicating hydrocephalus with success rates ranging from 66–88% compared to 21–75%, respectively [3,20,21]. Despite some studies showing positive outcomes after ETV for communicating hydrocephalus [9,10], it is important to note that many authors utilized radiographic evidence of tetraventricular enlargement without assessment of third ventricle morphology as evidence for the diagnosis of communicating hydrocephalus. As a result, these studies likely included patients with other etiologies of hydrocephalus that clearly benefit from ETV such as suprasellar arachnoidal cyst or prepontine subarachnoidal obstruction [12,13], among patients with iNPH. These obstructive etiologies may be mistaken for a communicating hydrocephalus due to the presence of dilation seen in all ventricles without an obvious source of obstruction. For example, Kehler et al. found that 12.7% of patients with a presumed diagnosis of iNPH were found to have infratentorial intracisternal obstructive hydrocephalus on MRI [14]. Moreover, in certain instances, patients may display a combination of both communicating and obstructive hydrocephalus,
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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E.W. Sankey et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Fig. 3. Change in timed up and go (TUG; A) and Tinetti performance oriented mobility (B) scores of idiopathic normal pressure hydrocephalus patients before and after endoscopic third ventriculostomy (ETV) and cerebrospinal fluid drainage trial via lumbar puncture (LP), predicting clinical improvement with cerebrospinal fluid diversion. Median pre-drainage TUG (A) improved from 14.00 to 11.00 seconds (p = 0.06) after initial LP. Median pre-drainage Tinetti (B) significantly improved from 22 to 25 after preETV LP (p = 0.02), and significant improvement was regained at 24.5 after post-ETV failure LP (p = 0.03). Error bars depict ranges.
Fig. 4. Change in timed up and go (TUG; A) and Tinetti performance oriented mobility (B) scores of idiopathic normal pressure hydrocephalus patients showing slight worsening after primary endoscopic third ventriculostomy (ETV) and subsequent improvement after secondary VP shunting. Median baseline (pre-drainage) TUG (A) worsened from 14.00 to 15.00 seconds after ETV and subsequently improved to 12.97 seconds after shunting. Median baseline (pre-drainage) Tinetti worsened from 22 to 21 after ETV, and subsequently improved to 25 after shunting (p = 0.07). Error bars depict ranges.
further complicating prediction of ETV success [22]. In situations where the obstructive lesion is not visualized directly, the pressure difference between the third ventricle and surrounding subarachnoid space can be indicated by downward bulging of the third ventricular floor and an anteriorly displaced lamina terminalis. Therefore, bowing of the third ventricular floor, which implies aqueductal or infratentorial intracisternal obstruction with a retrograde increased intraventricular pressure gradient, may be one of the most highly predictive factors of ETV success [12,23,24]. Our results are similar to those found by Edwards et al., who terminated their prospective randomized controlled trial after interim analysis failed to show a benefit in functional outcomes
after ETV in patients with iNPH while patients who received shunts had significant improvements in both gait (p = 0.04) and modified Rankin score (p = 0.001) at 3 months post-shunt [25]. Likewise, Pinto et al. also found that patients who underwent an ETV for iNPH failed to maintain the improved TUG scores seen immediately post-ETV after 12 months of follow-up, while patients who received a VP shunt maintained better TUG scores after 12 months than prior to their initial LP [11]. Even though the authors concluded that shunting is superior to ETV for the management of iNPH, at least 50% of patients in the ETV group experienced functional improvement in their study. However, the authors utilized radiographic evidence of ventricular dilation confirmed by brain
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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CT scan and MRI showing only the communicating hydrocephalus and an Evans index of 0.30% as diagnostic criteria for iNPH [11]. One significant limitation of many previous studies regarding hydrocephalus management is the inadequate resolution of routine MRI sequences [12,23,24], potentially resulting in misclassification and heterogeneous cohorts as discussed above. High resolution, gradient echo MRI sequences are more versatile than traditional spin echo MRI sequences. These imaging modalities allow visualization of subtle anatomic information that may be missed on routine MRI. The T2/T1-weighted ratio between structures under gradient echo MRI determines the contrast achieved by this technique. As such, high resolution gradient echo MRI is especially useful for evaluating the ventricular system based on the large degree of difference in T2-weighted values between the CSF and nearby anatomic structures [26]. In particular, it is highly sensitive to the detection of membranes within the cerebral cisterns and can reliably determine the etiology of hydrocephalus in the majority of patients [27]. Such characterization can help physicians determine the most appropriate method of treatment in patients with hydrocephalus. Though 50 years have passed since the first description of iNPH by Hakim and Adams in 1965 [1], limited Class I evidence exists regarding the best treatment modality for affected patients. Thankfully, an ongoing multicenter, randomized crossover study for iNPH may provide clinicians with the evidence needed to determine the true efficacy of shunt placement for the treatment of iNPH and to identify the most sensitive criteria to appropriately select patients for surgery [28]. While this study includes a homogenous cohort of patients with clinically and radiographically confirmed iNPH, several limitations should be considered. Important limitations include a small sample size, relatively long duration of symptoms prior to initial treatment and retrospective data collection. Due to the progressive deterioration seen in iNPH, patients who have a long duration of symptoms prior to treatment are much less likely to achieve a significant benefit in functional outcomes compared to patients who receive early intervention [29]. Moreover, patients with minor impairment and chronic ventriculomegaly may experience a marginal degree of clinical improvement [3]. The complete clinical triad of gait impairment, urinary incontinence and cognitive deficit in iNPH was observed in the majority of the patients in this series. It is a late phenomenon in the natural history of the disease [29,30], so the functional improvement seen in our patient population may have not been substantial enough to observe a significant improvement in gait after treatment. As such, additional large, prospective randomized clinical trials with confirmation of hydrocephalus etiology via high resolution gradient echo MRI are needed to appropriately guide surgeons regarding the optimal management strategy for symptomatic iNPH patients. Despite these limitations, the results of our study suggest that ETV is not an effective primary treatment option for iNPH and shunting should still be considered as the treatment of choice for communicating hydrocephalus.
5. Conclusion Patients with iNPH failed to maintain functional gait improvement after primary ETV despite evidence of a patent stoma. However, the improvement observed after both initial and second CSF drainage trials via LP was maintained after subsequent shunt placement. Our data supports the use of VP shunt placement as the treatment of choice for iNPH and suggests that ETV is an ineffective treatment modality for the management of this challenging condition.
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Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Hakim S, Adams RD. The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci 1965;2:307–27. [2] Adams RD, Fisher CM, Hakim S, et al. Symptomatic Occult Hydrocephalus with ‘‘normal’’ cerebrospinal-fluid pressure: a treatable syndrome. N Engl J Med 1965;273:117–26. [3] Dusick JR, McArthur DL, Bergsneider M. Success and complication rates of endoscopic third ventriculostomy for adult hydrocephalus: a series of 108 patients. Surg Neurol 2008;69:5–15. [4] Fleck S, Baldauf J, Schroeder H. Endoscopic third ventriculostomy: indications, technique, outcome, and complications. Cambridge, England: Cambridge University Press; 2014. [5] Schroeder HW, Niendorf WR, Gaab MR. Complications of endoscopic third ventriculostomy. J Neurosurg 2002;96:1032–40. [6] Drake JM, Kestle JR, Milner R, et al. Randomized trial of cerebrospinal fluid shunt valve design in pediatric hydrocephalus. Neurosurgery 1998;43:294–303 [discussion 303–5]. [7] Aquilina K, Edwards RJ, Pople IK. Routine placement of a ventricular reservoir at endoscopic third ventriculostomy. Neurosurgery 2003;53:91–6 [discussion 96–7]. [8] O’Brien DF, Javadpour M, Collins DR, et al. Endoscopic third ventriculostomy: an outcome analysis of primary cases and procedures performed after ventriculoperitoneal shunt malfunction. J Neurosurg 2005;103:393–400. [9] Gangemi M, Maiuri F, Naddeo M, et al. Endoscopic third ventriculostomy in idiopathic normal pressure hydrocephalus: an Italian multicenter study. Neurosurgery 2008;63:62–7 [discussion 67–9]. [10] Hailong F, Guangfu H, Haibin T, et al. Endoscopic third ventriculostomy in the management of communicating hydrocephalus: a preliminary study. J Neurosurg 2008;109:923–30. [11] Pinto FC, Saad F, Oliveira MF, et al. Role of endoscopic third ventriculostomy and ventriculoperitoneal shunt in idiopathic normal pressure hydrocephalus: preliminary results of a randomized clinical trial. Neurosurgery 2013;72:845–53 [discussion 853–4]. [12] Dlouhy BJ, Capuano AW, Madhavan K, et al. Preoperative third ventricular bowing as a predictor of endoscopic third ventriculostomy success. J Neurosurg Pediatr 2012;9:182–90. [13] Kehler U, Gliemroth J. Extraventricular intracisternal obstructive hydrocephalus – a hypothesis to explain successful 3rd ventriculostomy in communicating hydrocephalus. Pediatr Neurosurg 2003;38:98–101. [14] Kehler U, Herzog J. Intratentorial intracisternal obstructive hydrocephalus (InfinOH): how often is this subtype, which can be treated endoscopically, among idiopathic normal pressure hydrocephalus (iNPH)? IFNE Interim Meeting, Tokyo, Dec. 12–13, 2011. http://wah.kenkyuukai.jp/images/sys/ information/20110209180757-F0F3F14F73D3A12D6DDE0FBFD6E8922601E0 82C6443314C34FBB740322D59038.pdf. [15] Fisher CM. Hydrocephalus as a cause of disturbances of gait in the elderly. Neurology 1982;32:1358–63. [16] Feick D, Sickmond J, Liu L, et al. Sensitivity and predictive value of occupational and physical therapy assessments in the functional evaluation of patients with suspected normal pressure hydrocephalus. J Rehabil Med 2008;40:715–20. [17] Streitberger KJ, Wiener E, Hoffmann J, et al. In vivo viscoelastic properties of the brain in normal pressure hydrocephalus. NMR Biomed 2011;24: 385–92. [18] Freimann FB, Streitberger KJ, Klatt D, et al. Alteration of brain viscoelasticity after shunt treatment in normal pressure hydrocephalus. Neuroradiology 2012;54:189–96. [19] Longatti PL, Fiorindi A, Martinuzzi A. Failure of endoscopic third ventriculostomy in the treatment of idiopathic normal pressure hydrocephalus. Minim Invasive Neurosurg 2004;47:342–5. [20] Aquilina K, Pople IK, Sacree J, et al. The constant flow ventricular infusion test: a simple and useful study in the diagnosis of third ventriculostomy failure. J Neurosurg 2012;116:445–52. [21] Kandasamy J, Yousaf J, Mallucci C. Third ventriculostomy in normal pressure hydrocephalus. World Neurosurg 2013;79. S22.e21–27. [22] Yadav YR, Mukerji G, Parihar V, et al. Complex hydrocephalus (combination of communicating and obstructive type): an important cause of failed endoscopic third ventriculostomy. BMC Res Notes 2009;2:137. [23] Kehler U, Regelsberger J, Gliemroth J, et al. Outcome prediction of third ventriculostomy: a proposed hydrocephalus grading system. Minim Invasive Neurosurg 2006;49:238–43. [24] Foroughi M, Wong A, Steinbok P, et al. Third ventricular shape: a predictor of endoscopic third ventriculostomy success in pediatric patients. J Neurosurg Pediatr 2011;7:389–96. [25] Edwards RJ, Aquilina K, Bunnage M, Pople IK. A Prospective, Randomized, Controlled Trial of the Neuroendoscopic Treatment of Idiopathic Normal Pressure Hydrocephalus (ISRCTN29863839). IFNE Interim Meeting, Tokyo,
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Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy Eric W. Sankey a, Ignacio Jusué-Torres a, Benjamin D. Elder a,⇑, C. Rory Goodwin a, Sachin Batra a, Jamie Hoffberger a, Jennifer Lu a, Ari M. Blitz b, Daniele Rigamonti a a b
Department of Neurosurgery, The Johns Hopkins Hospital, 600 N Wolfe Street, Phipps 126, Baltimore, MD, USA Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA
a r t i c l e
i n f o
Article history: Received 9 February 2015 Accepted 14 February 2015 Available online xxxx Keywords: Endoscopic third ventriculostomy Idiopathic normal pressure hydrocephalus Timed up and go Tinetti performance oriented mobility assessment
a b s t r a c t We evaluated if patients with idiopathic normal pressure hydrocephalus (iNPH) showed functional improvement after primary endoscopic third ventriculostomy (ETV). The efficacy of ETV for iNPH remains controversial. We retrospectively reviewed 10 consecutive patients treated between 2009 and 2011 with ETV for iNPH. Seven patients with a median age of 73 years (range: 60–80) who underwent a primary ETV for iNPH were included for analysis. Median follow-up was 39 months (range: 26–46). Post-ETV stoma and aqueductal and cisternal flows were confirmed via high resolution, gradient echo and phase contrast MRI. Post-ETV timed up and go (TUG) and Tinetti performance oriented mobility assessment scores were compared to pre- and post-lumbar puncture (LP) values. A second LP was performed if ETV failed to sustain the observed improvement after initial LP. Patients who demonstrated ETV failure were subsequently shunted. Compared to pre-LP TUG and Tinetti values of 14.00 seconds (range: 12.00–23.00) and 22 (range: 16–24), post-LP scores improved to 11.00 seconds (range: 8.64–15.00; p = 0.06) and 25 (range: 24–28; p = 0.02), respectively. ETV failed to sustain this improvement with slight worsening between pre-LP and post-ETV TUG and Tinetti scores. Improvement from pre-LP assessment was regained after shunting and at last follow-up with TUG and Tinetti scores of 12.97 seconds (range: 9.00–18.00; p = 0.250) and 25 (range: 18–27; p = 0.07), and 11.87 seconds (range: 8.27–18.50; p = 0.152) and 23 (range: 18–26; p = 0.382), respectively. Despite stoma patency, ETV failed to sustain functional improvement seen after LP, however, improvement was regained after subsequent shunting suggesting that shunt placement remains the preferred treatment for iNPH. Published by Elsevier Ltd.
1. Introduction Idiopathic normal pressure hydrocephalus (iNPH) is a common and treatable neurological disorder that occurs in the elderly, and most often results in progressive gait impairment, urinary incontinence and cognitive deterioration [1,2]. Surgery is warranted in the majority of patients with symptomatic iNPH as cerebrospinal fluid (CSF) diversion results in symptomatic improvement in up to 80– 90% of individuals [1]. Potential options for CSF diversion in iNPH patients include ventriculoperitoneal (VP) shunt placement and endoscopic third ventriculostomy (ETV). Although ETV is considered a preferred treatment for obstructive hydrocephalus [3], its use in iNPH remains controversial with studies displaying contradictory outcomes [4]. Likewise, while the
⇑ Corresponding author. Tel.: +1 14109555000. E-mail address: [email protected] (B.D. Elder).
efficacy of ETV for obstructive hydrocephalus is easily understood as a means to bypass an obstructive lesion, the mechanism by which ETV may work in iNPH is not well understood. ETV is considered to be a safe and relatively simple procedure [5] with a lower risk of infection and delayed failure compared to VP shunts [6–8], however, careful consideration of the risk-benefit ratio related to each treatment option must be performed to determine the most appropriate modality for hydrocephalus management. As such, more data is needed regarding the outcomes in patients with iNPH following ETV compared to VP shunt placement. Previous studies regarding the success of ETV in patients with iNPH were limited by the fact that often CT scan instead of MRI was used as the imaging modality and by the fact that third ventricle morphology was not used as inclusion/exclusion criteria [9–11] despite the significant association between third ventricle morphology and outcomes after ETV [12]. As a result, the majority of these studies likely included patients with obstructive etiologies with either triventricular enlargement (unrecognized aqueductal
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Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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E.W. Sankey et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
obstruction on CT scan) or tetraventricular enlargement such as infratentorial intracisternal obstructive hydrocephalus [13,14]. Therefore, prior studies have potentially included better results that are not applicable to patients with iNPH. It is essential, therefore, to ensure that only patients with clinically and radiographically confirmed iNPH are included in studies evaluating the efficacy of ETV for iNPH. In the present study, we evaluated functional gait outcomes (as indicated by the change in timed up and go [TUG] and Tinetti performance oriented mobility assessment scores during follow-up) after primary ETV in patients with a confirmed diagnosis of iNPH and normal third ventricle morphology. 2. Materials and methods 2.1. Patients Under an active Institutional Review Board approved protocol, the medical records of 10 consecutive patients treated with ETV for iNPH by the senior author between 2009 and 2011, were retrospectively reviewed. Of note, 107 new shunts were placed by the senior author for the treatment of obstructive hydrocephalus presenting as iNPH during the same time period. After discussion regarding the known treatment options for iNPH, 10 patients chose to undergo ETV instead of shunting. All patients were adults (>21 years of age). Seven patients (70%) with iNPH who received an ETV as their primary treatment were included for analysis (Table 1). A total of three patients (30%) were excluded, one (10%) because of secondary iNPH resulting from an intracranial infection, one (10%) with iNPH who had a history of previous shunt placement, and one (10%) with iNPH who was lost to follow-up after discharge. Preoperative high resolution, gradient echo MRI sequences were obtained to confirm the absence of an obstructive etiology, and displayed a normal third ventricle morphology in all patients (Fig. 1). All patients received a lumbar puncture (LP) prior
Table 1 Idiopathic normal pressure hydrocephalus patient characteristics Characteristics
iNPH patients (n = 7)
Age, years, median (range) Sex, female, n (%) Race, n (%) Caucasian Symptoms at presentation, n (%) Gait impairment Urinary incontinence Cognitive dysfunction Vision deficit Headaches Nausea Dizziness Duration of symptoms prior to ETV, months, median (range) Complications, n (%) Intraoperative Postoperative Follow-up duration, months, median (range)
73 (60–80) 3 (43) 7 (100) 7 (100) 7 (100) 5 (71) 0 (0) 1 (14) 0 (0) 3 (43) 24 (5–60)
0 (0) 0 (0) 39 (26–46)
Pre-LP quantitative tests
iNPH patients (n = 7)
MMSE, median (range) TUG, seconds, median (range)
27 (25–29) 14.00 (12.00– 23.00) 22 (16–24) 0.36 (0.33–0.39)
Tinetti, median (range) Evan’s index, median (range)
ETV = endoscopic third ventriculostomy, iNPH = idiopathic normal pressure hydrocephalus, LP = lumbar puncture, MMSE = mini-mental state examination, Tinetti = Tinetti performance oriented mobility score, TUG = timed up and go.
to ETV and had a preoperative opening pressure <25 cm H2O, supporting the diagnosis of iNPH. Demographic information concerning sex, race, age at treatment, and previous shunting were collected. Baseline data concerning the duration of symptoms prior to ETV, Evan’s index, and presenting symptoms were obtained. Baseline and post-LP TUG and Tinetti scores were reviewed prior to ETV. Quantitative, continuous data are expressed in median (range) for non-parametric variables, and categorical data are expressed as frequency (percentage). 2.2. Clinical and radiologic follow-up All intraoperative and postoperative complications that occurred within 6 weeks postoperatively were recorded. Post-ETV TUG and Tinetti scores were compared to pre- and post-LP values prior to ETV. Higher values of mini–mental state examination (MMSE; 30 points) and Tinetti (28 points) and lower values of TUG indicate better performance. Recurrence free probability was determined by the time to symptom recurrence after ETV (Fig. 2). A second LP was performed if the ETV failed to sustain the observed improvement after initial LP, despite stoma patency. After ETV failure, patients who demonstrated improvement after a second LP were considered for repeat ETV or VP shunting. Postoperative ETV patency and aqueductal and cisternal flow were assessed by high resolution, gradient echo MRI and flow pulsatility through the stoma on phase contrast MRI. 3. Results Three Caucasian women (43%) and four men (57%) with iNPH underwent ETV as their primary treatment modality. The median age at treatment was 73 years (range: 60–80). The median duration of symptoms prior to ETV was 24 months (range: 5–60). Preoperative Evan’s index was 0.36 (range: 0.33–0.38). All patients presented with gait impairment and urinary incontinence and five (71%) displayed signs of cognitive dysfunction. Median baseline pre-LP MMSE, TUG, and Tinetti scores were 27 (range: 25–29), 14.00 seconds (range: 12.00–23.00) and 22 (range: 16–24), respectively. No intraoperative or postoperative complications occurred during the primary ETV or subsequent shunt placement. After an initial LP, the TUG and Tinetti scores improved to 11.00 seconds (range: 8.64–15.00; p = 0.06) and 25 (range: 24– 28; p = 0.02), respectively (Fig. 3). However, this improvement was not sustained after ETV with slight worsening observed between pre-LP and post-ETV TUG and Tinetti scores (Fig. 4). All patients also showed symptomatic ETV failure after a median of 9 months (range: 0–24; Fig. 2) despite evidence of a patent stoma on imaging. Patients were re-evaluated with a new LP after ETV failure and subsequently shunted after displaying improvement from pre-LP values following the second-LP. Improvement from pre-LP assessment was regained after shunting and at last follow-up with TUG and Tinetti scores of 12.97 seconds (range: 9.00–18.00; p = 0.250) and 25 (range: 18–27; p = 0.07), and 11.87 seconds (range: 8.27–18.50; p = 0.152) and 23 (range: 18– 26; p = 0.382), respectively (Fig. 4). Follow-up duration was a median of 39 months (range: 26–46). 4. Discussion Data from the present study suggests that primary ETV fails to improve mobility, assessed by TUG and Tinetti, in patients with confirmed iNPH and normal third ventricle morphology while subsequent shunt placement regained the improvement seen after a trial of CSF drainage via LP. As prior studies describing ETV use in
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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Fig. 1. Baseline sagittal high resolution, gradient echo MRI showing a concave lamina terminalis and third ventricular floor, indicated by arrows, in a patient with idiopathic normal pressure hydrocephalus.
Fig. 2. Kaplan–Meier curve showing recurrence free probability for the time to symptom recurrence post-endoscopic third ventriculostomy. All patients showed symptomatic endoscopic third ventriculostomy failure after a median of 9 months (range 0–24).
iNPH did not use third ventricle morphology as an inclusion/exclusion criterion or they included patient cohorts with both idiopathic and secondary NPH, our results are unique; we analyzed a homogenous cohort with both radiographically and clinically confirmed iNPH. In addition, ETV was performed as a primary treatment for iNPH after improvement with a CSF drainage trial, predicting potential success with CSF diversion irrespective of the method of treatment. Our data supports the use of VP shunting as the treatment of choice for iNPH and suggests that ETV is an ineffective treatment modality for the management of this challenging condition. The most common presenting symptom in patients with iNPH is gait impairment [15]. Functional outcomes related to gait can be accurately assessed using reliable and validated performance measures such as the TUG test and Tinetti performance oriented mobility assessment. These assessments often allow clinicians to objectively monitor the change in mobility in patients with suspected iNPH during treatment [16]. However, our anecdotal experience suggests that these measures may not be sensitive enough to detect small changes in gait with patients often reporting a subjective worsening with ambulation despite favorable TUG and Tinetti scores. ETV is a highly effective treatment for patients with obstructive hydrocephalus and it has also been used in several studies to treat
communicating hydrocephalus with contradictory results [4]. For example, ETV has been considered as a viable treatment option in select patients with communicating hydrocephalus such as those with mild impairment and aged under 65 years [10]. Since the etiology of communicating hydrocephalus remains unclear, the mechanism by which ETV is proposed to work in patients with iNPH is also not well understood. Yet, studies using magnetic resonance elastography have shown that there is clear evidence of tissue degradation associated with iNPH leading to altered viscoelastic properties of brain tissue during disease progression and tissue repair [17,18]. One potential explanation is that communicating hydrocephalus results in decreased intracranial compliance leading to increased intracranial systolic pulse pressure and ultimately to a decrease in cerebral blood flow. As such, ETV may exert its effect in these patients by effectively decreasing intracranial systolic pulse pressure via CSF diversion through the third ventricular floor, ultimately improving cerebral blood flow and perfusion pressure and eliminating transependymal resorption of CSF [4]. Another potential explanation by Longatti et al. is that iNPH may cause an intermittent functional aqueductal stenosis stemming from continuous systolic pulsations in the context of decreased intracranial compliance [19]. Thus, ETV may provide a conduit to bypass this functional obstruction similar to its effect in obstructive hydrocephalus. However, the results of most studies endorse substantially better outcomes after ETV in the management of obstructive hydrocephalus as compared to communicating hydrocephalus with success rates ranging from 66–88% compared to 21–75%, respectively [3,20,21]. Despite some studies showing positive outcomes after ETV for communicating hydrocephalus [9,10], it is important to note that many authors utilized radiographic evidence of tetraventricular enlargement without assessment of third ventricle morphology as evidence for the diagnosis of communicating hydrocephalus. As a result, these studies likely included patients with other etiologies of hydrocephalus that clearly benefit from ETV such as suprasellar arachnoidal cyst or prepontine subarachnoidal obstruction [12,13], among patients with iNPH. These obstructive etiologies may be mistaken for a communicating hydrocephalus due to the presence of dilation seen in all ventricles without an obvious source of obstruction. For example, Kehler et al. found that 12.7% of patients with a presumed diagnosis of iNPH were found to have infratentorial intracisternal obstructive hydrocephalus on MRI [14]. Moreover, in certain instances, patients may display a combination of both communicating and obstructive hydrocephalus,
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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Fig. 3. Change in timed up and go (TUG; A) and Tinetti performance oriented mobility (B) scores of idiopathic normal pressure hydrocephalus patients before and after endoscopic third ventriculostomy (ETV) and cerebrospinal fluid drainage trial via lumbar puncture (LP), predicting clinical improvement with cerebrospinal fluid diversion. Median pre-drainage TUG (A) improved from 14.00 to 11.00 seconds (p = 0.06) after initial LP. Median pre-drainage Tinetti (B) significantly improved from 22 to 25 after preETV LP (p = 0.02), and significant improvement was regained at 24.5 after post-ETV failure LP (p = 0.03). Error bars depict ranges.
Fig. 4. Change in timed up and go (TUG; A) and Tinetti performance oriented mobility (B) scores of idiopathic normal pressure hydrocephalus patients showing slight worsening after primary endoscopic third ventriculostomy (ETV) and subsequent improvement after secondary VP shunting. Median baseline (pre-drainage) TUG (A) worsened from 14.00 to 15.00 seconds after ETV and subsequently improved to 12.97 seconds after shunting. Median baseline (pre-drainage) Tinetti worsened from 22 to 21 after ETV, and subsequently improved to 25 after shunting (p = 0.07). Error bars depict ranges.
further complicating prediction of ETV success [22]. In situations where the obstructive lesion is not visualized directly, the pressure difference between the third ventricle and surrounding subarachnoid space can be indicated by downward bulging of the third ventricular floor and an anteriorly displaced lamina terminalis. Therefore, bowing of the third ventricular floor, which implies aqueductal or infratentorial intracisternal obstruction with a retrograde increased intraventricular pressure gradient, may be one of the most highly predictive factors of ETV success [12,23,24]. Our results are similar to those found by Edwards et al., who terminated their prospective randomized controlled trial after interim analysis failed to show a benefit in functional outcomes
after ETV in patients with iNPH while patients who received shunts had significant improvements in both gait (p = 0.04) and modified Rankin score (p = 0.001) at 3 months post-shunt [25]. Likewise, Pinto et al. also found that patients who underwent an ETV for iNPH failed to maintain the improved TUG scores seen immediately post-ETV after 12 months of follow-up, while patients who received a VP shunt maintained better TUG scores after 12 months than prior to their initial LP [11]. Even though the authors concluded that shunting is superior to ETV for the management of iNPH, at least 50% of patients in the ETV group experienced functional improvement in their study. However, the authors utilized radiographic evidence of ventricular dilation confirmed by brain
Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019
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CT scan and MRI showing only the communicating hydrocephalus and an Evans index of 0.30% as diagnostic criteria for iNPH [11]. One significant limitation of many previous studies regarding hydrocephalus management is the inadequate resolution of routine MRI sequences [12,23,24], potentially resulting in misclassification and heterogeneous cohorts as discussed above. High resolution, gradient echo MRI sequences are more versatile than traditional spin echo MRI sequences. These imaging modalities allow visualization of subtle anatomic information that may be missed on routine MRI. The T2/T1-weighted ratio between structures under gradient echo MRI determines the contrast achieved by this technique. As such, high resolution gradient echo MRI is especially useful for evaluating the ventricular system based on the large degree of difference in T2-weighted values between the CSF and nearby anatomic structures [26]. In particular, it is highly sensitive to the detection of membranes within the cerebral cisterns and can reliably determine the etiology of hydrocephalus in the majority of patients [27]. Such characterization can help physicians determine the most appropriate method of treatment in patients with hydrocephalus. Though 50 years have passed since the first description of iNPH by Hakim and Adams in 1965 [1], limited Class I evidence exists regarding the best treatment modality for affected patients. Thankfully, an ongoing multicenter, randomized crossover study for iNPH may provide clinicians with the evidence needed to determine the true efficacy of shunt placement for the treatment of iNPH and to identify the most sensitive criteria to appropriately select patients for surgery [28]. While this study includes a homogenous cohort of patients with clinically and radiographically confirmed iNPH, several limitations should be considered. Important limitations include a small sample size, relatively long duration of symptoms prior to initial treatment and retrospective data collection. Due to the progressive deterioration seen in iNPH, patients who have a long duration of symptoms prior to treatment are much less likely to achieve a significant benefit in functional outcomes compared to patients who receive early intervention [29]. Moreover, patients with minor impairment and chronic ventriculomegaly may experience a marginal degree of clinical improvement [3]. The complete clinical triad of gait impairment, urinary incontinence and cognitive deficit in iNPH was observed in the majority of the patients in this series. It is a late phenomenon in the natural history of the disease [29,30], so the functional improvement seen in our patient population may have not been substantial enough to observe a significant improvement in gait after treatment. As such, additional large, prospective randomized clinical trials with confirmation of hydrocephalus etiology via high resolution gradient echo MRI are needed to appropriately guide surgeons regarding the optimal management strategy for symptomatic iNPH patients. Despite these limitations, the results of our study suggest that ETV is not an effective primary treatment option for iNPH and shunting should still be considered as the treatment of choice for communicating hydrocephalus.
5. Conclusion Patients with iNPH failed to maintain functional gait improvement after primary ETV despite evidence of a patent stoma. However, the improvement observed after both initial and second CSF drainage trials via LP was maintained after subsequent shunt placement. Our data supports the use of VP shunt placement as the treatment of choice for iNPH and suggests that ETV is an ineffective treatment modality for the management of this challenging condition.
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Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Hakim S, Adams RD. The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci 1965;2:307–27. [2] Adams RD, Fisher CM, Hakim S, et al. Symptomatic Occult Hydrocephalus with ‘‘normal’’ cerebrospinal-fluid pressure: a treatable syndrome. N Engl J Med 1965;273:117–26. [3] Dusick JR, McArthur DL, Bergsneider M. Success and complication rates of endoscopic third ventriculostomy for adult hydrocephalus: a series of 108 patients. Surg Neurol 2008;69:5–15. [4] Fleck S, Baldauf J, Schroeder H. Endoscopic third ventriculostomy: indications, technique, outcome, and complications. Cambridge, England: Cambridge University Press; 2014. [5] Schroeder HW, Niendorf WR, Gaab MR. Complications of endoscopic third ventriculostomy. J Neurosurg 2002;96:1032–40. [6] Drake JM, Kestle JR, Milner R, et al. Randomized trial of cerebrospinal fluid shunt valve design in pediatric hydrocephalus. Neurosurgery 1998;43:294–303 [discussion 303–5]. [7] Aquilina K, Edwards RJ, Pople IK. Routine placement of a ventricular reservoir at endoscopic third ventriculostomy. Neurosurgery 2003;53:91–6 [discussion 96–7]. [8] O’Brien DF, Javadpour M, Collins DR, et al. Endoscopic third ventriculostomy: an outcome analysis of primary cases and procedures performed after ventriculoperitoneal shunt malfunction. J Neurosurg 2005;103:393–400. [9] Gangemi M, Maiuri F, Naddeo M, et al. Endoscopic third ventriculostomy in idiopathic normal pressure hydrocephalus: an Italian multicenter study. Neurosurgery 2008;63:62–7 [discussion 67–9]. [10] Hailong F, Guangfu H, Haibin T, et al. Endoscopic third ventriculostomy in the management of communicating hydrocephalus: a preliminary study. J Neurosurg 2008;109:923–30. [11] Pinto FC, Saad F, Oliveira MF, et al. Role of endoscopic third ventriculostomy and ventriculoperitoneal shunt in idiopathic normal pressure hydrocephalus: preliminary results of a randomized clinical trial. Neurosurgery 2013;72:845–53 [discussion 853–4]. [12] Dlouhy BJ, Capuano AW, Madhavan K, et al. Preoperative third ventricular bowing as a predictor of endoscopic third ventriculostomy success. J Neurosurg Pediatr 2012;9:182–90. [13] Kehler U, Gliemroth J. Extraventricular intracisternal obstructive hydrocephalus – a hypothesis to explain successful 3rd ventriculostomy in communicating hydrocephalus. Pediatr Neurosurg 2003;38:98–101. [14] Kehler U, Herzog J. Intratentorial intracisternal obstructive hydrocephalus (InfinOH): how often is this subtype, which can be treated endoscopically, among idiopathic normal pressure hydrocephalus (iNPH)? IFNE Interim Meeting, Tokyo, Dec. 12–13, 2011. http://wah.kenkyuukai.jp/images/sys/ information/20110209180757-F0F3F14F73D3A12D6DDE0FBFD6E8922601E0 82C6443314C34FBB740322D59038.pdf. [15] Fisher CM. Hydrocephalus as a cause of disturbances of gait in the elderly. Neurology 1982;32:1358–63. [16] Feick D, Sickmond J, Liu L, et al. Sensitivity and predictive value of occupational and physical therapy assessments in the functional evaluation of patients with suspected normal pressure hydrocephalus. J Rehabil Med 2008;40:715–20. [17] Streitberger KJ, Wiener E, Hoffmann J, et al. In vivo viscoelastic properties of the brain in normal pressure hydrocephalus. NMR Biomed 2011;24: 385–92. [18] Freimann FB, Streitberger KJ, Klatt D, et al. Alteration of brain viscoelasticity after shunt treatment in normal pressure hydrocephalus. Neuroradiology 2012;54:189–96. [19] Longatti PL, Fiorindi A, Martinuzzi A. Failure of endoscopic third ventriculostomy in the treatment of idiopathic normal pressure hydrocephalus. Minim Invasive Neurosurg 2004;47:342–5. [20] Aquilina K, Pople IK, Sacree J, et al. The constant flow ventricular infusion test: a simple and useful study in the diagnosis of third ventriculostomy failure. J Neurosurg 2012;116:445–52. [21] Kandasamy J, Yousaf J, Mallucci C. Third ventriculostomy in normal pressure hydrocephalus. World Neurosurg 2013;79. S22.e21–27. [22] Yadav YR, Mukerji G, Parihar V, et al. Complex hydrocephalus (combination of communicating and obstructive type): an important cause of failed endoscopic third ventriculostomy. BMC Res Notes 2009;2:137. [23] Kehler U, Regelsberger J, Gliemroth J, et al. Outcome prediction of third ventriculostomy: a proposed hydrocephalus grading system. Minim Invasive Neurosurg 2006;49:238–43. [24] Foroughi M, Wong A, Steinbok P, et al. Third ventricular shape: a predictor of endoscopic third ventriculostomy success in pediatric patients. J Neurosurg Pediatr 2011;7:389–96. [25] Edwards RJ, Aquilina K, Bunnage M, Pople IK. A Prospective, Randomized, Controlled Trial of the Neuroendoscopic Treatment of Idiopathic Normal Pressure Hydrocephalus (ISRCTN29863839). IFNE Interim Meeting, Tokyo,
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Please cite this article in press as: Sankey EW et al. Functional gait outcomes for idiopathic normal pressure hydrocephalus after primary endoscopic third ventriculostomy. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.02.019