- Email: [email protected]
Comparison of Complication and Revision Rates After Frontal Versus Parietal Approach for Ventricular Shunt Placement in Idiopathic Normal Pressure Hydrocephalus
Original Article
Comparison of Complication and Revision Rates After Frontal Versus Parietal Approach for Ventricular Shunt Placement in Idiopathic Normal Pressure Hydrocephalus Adip G. Bhargav1, Lorenzo Rinaldo2, Giuseppe Lanzino2,3, Benjamin D. Elder2,4,5
-
BACKGROUND: Ventricular shunts are most commonly placed via a frontal or parietal approach. However, there is a paucity of data comparing complication and revision rates associated with these approaches in the idiopathic normal pressure hydrocephalus (iNPH) population.
complication and revision rates in patients with iNPH, and either approach is a reasonable first-line option.
METHODS: Patients with iNPH treated with ventricular shunting between 2001 and 2017 at our institution were included for analysis. Patient characteristics, catheter accuracy, and incidence of revision were determined from the medical record. Catheter accuracy was determined using axial computed tomography imaging and classified as grade 1, 2, or 3 based on location of the catheter tip.
INTRODUCTION
-
RESULTS: There were 348 patients included for analysis with 266 (76.4%) and 82 (23.6%) receiving a frontal versus parietal shunt, respectively. Patients undergoing the parietal approach were more likely to receive a programmable valve (37.8% vs. 25.2%; P [ 0.026). Neuronavigation was used more frequently for patients undergoing the parietal approach (26.8% vs. 4.1%; P < 0.001); however, a minority of cases used neuronavigation in general (9.5%). There was no difference in catheter accuracy between the 2 approaches and no difference in catheter accuracy with the use of neuronavigation. The overall revision rate was 21.0%, and there were no differences in the incidence of revisions between the frontal and parietal approaches (21.8% vs. 18.3%, respectively; P [ 0.495). There were no differences in revision subtypes between the approaches.
-
CONCLUSIONS: These results suggest that the type of approach for shunting may not have a significant impact on
-
Key words Hydrocephalus - Revision surgery - Shunt malfunction - Technique - Ventriculoperitoneal shunt -
Abbreviations and Acronyms CSF: Cerebrospinal fluid CT: Computed tomography iNPH: Idiopathic normal pressure hydrocephalus
WORLD NEUROSURGERY -: e1-e6, - 2019
V
entricular shunting to divert cerebrospinal fluid (CSF) is an effective therapy for idiopathic normal pressure hydrocephalus (iNPH).1,2 The 2 most common approaches for the placement of the ventricular catheter are via a frontal or parietal burr hole.3 There has been limited analysis of the complication and revision rates after shunt placement using different ventricular approaches in the iNPH population. To address this issue, the complication and revision rates associated with frontal versus parietal shunt placement in a large series of patients with iNPH were investigated. METHODS Patient Selection Institutional review board approval (18-000051) was obtained prior to the initiation of this study. We retrospectively reviewed our institution’s medical records for patients with iNPH treated with ventricular shunting between 2000 and 2017. Patients included for analysis had an established diagnosis of iNPH as determined by a neurologist. The diagnosis of iNPH was made according to clinical symptoms, radiographic ventriculomegaly, and opening pressure <25 cm H2O on lumbar puncture, along with improvement after a high-volume lumbar puncture.4 We excluded patients with a prior shunt placement on initial evaluation at our institution. The choice of approach was dependent on staff surgeon preference, facilitating a comparison of frontal and parietal in a relatively
From the 1Mayo Clinic School of Medicine and Departments of 2Neurosurgery, 3Radiology, 4 Bioengineering, and 5Orthopedics, Mayo Clinic, Rochester, Minnesota, USA To whom correspondence should be addressed: Benjamin D. Elder, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.027 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e1
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Figure 1. Grading of catheter placement using axial computed tomography imaging. (A) Grade 1 catheter placement with tip of catheter surrounded by cerebrospinal fluid. (B) Grade 2 placement with tip in
unselected population. Outcomes and follow-up time between shunt surgery and last appointment were recorded for each patient. Incidence of Revision Surgery and Determination of Shunt Malfunction Etiology The primary outcome of interest was the incidence of shunt revision surgery and revision surgery because of specific indications. The indication for revision was classified as one of the following: persistent symptoms without obstruction, proximal or distal obstruction, infection, overdrainage, or subdural collection. We defined shunt infection as symptomatology suggestive of infection with positive cultures for microbial growth or a positive CSF gram stain. Patients were suspected of having a shunt obstruction based on clinical presentation, mainly minimal to no clinical improvement after shunt placement or neurologic decline after initial improvement after shunt placement. Routine noninvasive evaluation to assess for shunt obstruction included palpation of shunt valve reservoir to evaluate refilling and radiographic evaluation in the form of radiographic shunt series and head computed tomography (CT) imaging. Given the low likelihood of proximal obstruction in this patient population and risk of iatrogenic shunt infection, shunt tapping was not routinely performed to assess for proximal obstruction. Additional ancillary tests such as radionuclide studies were also not routinely performed and obtained only at the discretion of the treating neurosurgeon in isolated cases. To classify obstruction because of a proximal versus distal cause, the operative record was reviewed. Shunt components were interrogated to determine the cause of malfunction in all patients undergoing revision surgery because of suspected shunt obstruction. Proximal obstruction was defined as a lack of flow through the ventricular catheter or as a visibly malpositioned ventricular catheter on imaging studies, with no catheter holes within the ventricular space. Distal obstruction was defined as little to no flow through the distal catheter using a manometer or on direct observation. Kinking of the distal catheter was also classified as a distal obstruction, as were peritoneal catheters
e2
www.SCIENCEDIRECT.com
contact with the ependymal lining of the ventricle. (C) Grade 3 placement with tip of catheter in brain parenchyma.
located in the preperitoneal space or within a loculated intraperitoneal fluid collection. Patients were classified as having persistent symptoms without obstruction if intraoperative interrogation revealed functional shunt components. The incidence of multiple revision surgeries, subdural fluid collections, and need for subdural collection evacuation was also noted. Noninvasive manipulation of shunt parameters was not classified as a surgical revision. Invasive procedures to decrease overdrainage in patients with clinical or radiographic signs of ventricular overdrainage— subdural collection or pachymeningeal enhancement—were considered to be surgical revisions. These included interventions such as clavicular incision to tie off a distal shunt or complete shunt removal. Patient Variables of Interest The primary variable of interest was the type of anatomic approach selected for shunt placement, specifically the frontal versus parietal approach. Additional variables including age, sex, body mass index, use of neuronavigation, valve type, and distal catheter location were recorded. Distal catheter location was classified as in the peritoneum, pleural space, or atrium. Catheter Accuracy To compare the accuracy of the frontal and parietal approach in ventricular shunt placement, all of the patients’ postoperative head CT scans were examined and the catheter placement was graded according to the methodology proposed by Hayhurst et al.5 Grade 1 was defined as the catheter tip being completely surrounded by CSF without contact with ependymal lining. Grade 2 was defined as the catheter tip touching the ependymal lining of the ventricle. Grade 3 was assigned when there was complete misplacement of the catheter outside of the ventricle or if a portion of the catheter was intraparenchymal (Figure 1). Temporal Trends Given the extended time period of our study, changes in the utilization of frontal versus parietal approach, fixed-setting versus
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.027
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Table 1. Comparison of Patients Undergoing Frontal versus Parietal Approach Frontal Approach (n [ 266)
Parietal Approach (n [ 82)
Total (N [ 348)
P Value
73.1 8.3
73.5 8.4
73.2 8.3
0.693
Male
174 (65.4)
50 (61.0)
224 (64.4)
Female
92 (34.6)
32 (39.0)
124 (35.6)
29.4 4.9
28.4 4.9
29.2 4.9
0.114
11 (4.1)
22 (26.8)
33 (9.5)
<0.0001y
Fixed
199 (74.8)
51 (62.2)
250 (71.8)
Programmable
67 (25.2)
31 (37.8)
98 (28.2)
0.026y
260 (97.7)
81 (98.8)
341 (98.0)
0.559
Atrium
5 (1.9)
1 (1.2)
6 (1.7)
0.688
Pleural space
1 (0.4)
0 (0)
1 (0.3)
0.578
58 (21.8)
15 (18.3)
73 (21.0)
0.495
0.3 0.6
0.2 0.6
0.3 0.6
0.692
0e4
0e3
0e4
15.2 23.5
21.3 38.8
16.5 27.1
Variable Age (years) Sex
BMI* Use of neuronavigation
0.463
Valve type
Distal catheter location Peritoneum
Revision surgery Revisions per patient Range Time to initial revision (months) Median Follow-up time (months) Median
5.3
1.5
4
25.7 31.7
33.6 42.6
27.6 34.7
12.1
12.8
12.3
0.569
0.127
Values are mean SD, number of patients (%), or as otherwise indicated. BMI, body mass index. *BMI unavailable for 17 patients. yStatistical significance.
programmable valve, and incidence of revision surgery over time were assessed using linear regression analysis. The independent variable was the year of shunt placement (2000e2017). Separate regression models were constructed for catheter approach, valve type, and incidence of revision, with the yearly percentage of cases using a parietal approach, a programmable valve, or requiring revision surgery serving as the dependent variable, respectively. Models were weighted according to the total number of cases performed during each year of the study. Results were presented as a b coefficient, representing the change in the dependent variable per unit change in the independent variable, correlation coefficient (r2), and P value. Statistical Analysis Descriptive statistics were performed for continuous and categorical variables. Mean and SD were reported for continuous variables, whereas frequency and percentage were reported for categorical variables. Student t test, Pearson c2 test, and analysis of variance were used where appropriate to perform comparative statistics for continuous and categorical variables. Multivariate analysis was performed using a Cox proportional hazards model.
WORLD NEUROSURGERY -: e1-e6, - 2019
Alpha levels for statistical significance were set at 0.05. Commercially available software (JMP 10.0.0 [SAS Institute Inc., Cary, North Carolina, USA]) was used to perform the analysis. RESULTS Patient Characteristics and Outcomes There were 348 patients included for analysis. The mean age of the cohort was 73.2 8.3 years, with most patients being men (64.4%). Most patients had their shunt placed via a frontal approach (n ¼ 266, 76.4%), with a relative minority of patients receiving parietal shunts (n ¼ 82, 23.6%). Patients undergoing a parietal approach were more likely to receive a programmable valve than a fixed valve (37.8% vs. 25.2%, respectively; P ¼ 0.026). The most common distal catheter location was the peritoneum (n ¼ 341, 98.0%) followed by the atrium (n ¼ 6, 1.7%) and pleural space (n ¼ 1, 0.3%). Baseline characteristics of patients receiving the frontal versus parietal approach are shown in Table 1. There were 73 patients (21.0%) who required revision surgery, with 12 patients (3.4%) undergoing multiple revisions. The mean time to revision was 16.5 27.1 months. In 24 patients (6.9%), no
www.journals.elsevier.com/world-neurosurgery
e3
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Table 2. Incidence of Revision Subtypes in Patients Undergoing Frontal versus Parietal Approach Variable
Frontal Approach (n [ 266)
Parietal Approach (n [ 82)
Total (N [ 348)
P Value
58 (21.8)
15 (18.3)
73 (21.0)
0.495
Any revision Multiple revisions
8 (3.0)
4 (4.9)
12 (3.4)
0.417
Persistent symptoms without obstruction
18 (6.8)
6 (7.3)
24 (6.9)
0.864
Distal obstruction
16 (6.0)
2 (2.4)
18 (5.2)
0.201
Proximal obstruction
3 (1.1)
3 (3.7)
6 (1.7)
0.124
Infection
10 (3.7)
3 (3.7)
13 (3.7)
0.966
Overdrainage requiring revision
12 (4.5)
2 (2.4)
14 (4.0)
0.404
Intracranial hemorrhage
3 (1.1)
3 (3.7)
6 (1.7)
0.124
Subdural collection
47 (17.7)
22 (26.8)
69 (19.9)
0.071
Evacuated subdural
15 (5.6)
5 (6.1)
20 (5.7)
0.876
Values are number of patients (%) or as otherwise indicated.
definite obstruction was observed despite persistent patient symptomatology. Eighteen patients (5.2%) underwent revision surgery for distal obstruction, whereas 6 patients (1.7%) underwent revision surgery for proximal obstruction. Thirteen patients (3.7%) underwent revision surgery because of infection, and 14 patients (4.0%) received revision surgery for overdrainage. Sixtynine patients (19.9%) developed a subdural collection, with 20 of these patients (5.7%) requiring surgical evacuation. Among the patients who developed a subdural collection, 22 patients (31.9%) had a programmable valve, with valve reprogramming to a higher setting performed in 18 patients (81.8%). In the remaining 4 patients, the subdural collection was found to be asymptomatic and stable on serial imaging; therefore, the valve was not adjusted. Of the 14 patients requiring revision surgery for overdrainage, 3 (21.4%) had a programmable valve. Prior to revision surgery, shunt reprogramming was initially attempted; however, the patients either remained symptomatic or the subdural collection was noted to enlarge, ultimately leading to surgical shunt ligation. There were no statistically significant differences in the rate of overall revision surgery (21.8% vs. 18.3%, respectively; P ¼ 0.495)
or revision subtypes after shunt placement via the frontal versus parietal approach (Table 2). We did observe that patients receiving a fixed-setting valve were more likely to undergo revision surgery relative to those receiving a programmable valve (24.0% vs. 13.3%, respectively; P ¼ 0.027). Using a Cox proportional hazards model, when adjusting for valve type, catheter approach was still not associated with increased risk of revision surgery (relative risk for frontal vs. parietal approach: 1.33; 95% confidence interval, 0.74e2.38; P ¼ 0.335). Comparison of Catheter Placement with the Frontal and Parietal Approach The frequency of grade 1, 2, and 3 catheter accuracy was 26.1% (n ¼ 81), 69.4% (n ¼ 215), and 4.5% (n ¼ 14). There were no statistically significant differences in catheter accuracy when placed via a frontal versus parietal approach (Table 3). The use of neuronavigation was more common in patients receiving the parietal approach (26.8% vs. 4.1%, respectively; P < 0.001) (Table 1); however, the use of neuronavigation did not have a significant impact on catheter accuracy (Table 4).
Table 3. Catheter Accuracy in Patients Undergoing Frontal versus Parietal Approach
Variable
Frontal Approach (n [ 266)
Table 4. Effect of Neuronavigation on Catheter Accuracy
Parietal Approach (n [ 82)
Total (N [ 348)
P Value
Catheter accuracy*
Neuronavigation (n [ 33)
No Navigation (n [ 315)
Total (N [ 348)
P Value
Catheter accuracy with neuronavigation*
Grade 1
66 (27.8)
15 (20.5)
81 (26.1)
0.215
Grade 1
8 (24.2)
73 (26.4)
81 (26.1)
0.794
Grade 2
160 (67.5)
55 (75.3)
215 (69.4)
0.204
Grade 2
23 (69.7)
192 (69.3)
215 (69.4)
0.964
Grade 3
11 (4.6)
3 (4.1)
14 (4.5)
0.848
Grade 3
2 (6.1)
12 (4.3)
14 (4.5)
0.651
Values are number of patients (%) or as otherwise indicated. *Thirty-eight patients did not have postoperative head computed tomography scan.
e4
Variable
www.SCIENCEDIRECT.com
Values are number of patients (%) or as otherwise indicated. *Thirty-eight patients did not have postoperative head computed tomography scan.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.027
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Temporal Trends in Catheter Approach, Valve Type, and Revision Rate The utilization of the parietal approach (versus the frontal approach) was found to decrease over the study period (b ¼ 1.083, r2 ¼ 0.237, P ¼ 0.040) (Figure 2A), whereas the utilization of programmable valves was found to increase (b ¼ 1.279, r2 ¼ 0.265, P ¼ 0.029) (Figure 2B). The rate of revision surgery because of all causes was found to decrease over the study period (b ¼ 1.208, r2 ¼ 0.413, P ¼ 0.004) (Figure 2C). DISCUSSION
Figure 2. Temporal trends in the selection of anatomic approach, valve type, and revision rates. (A) Rates of parietal versus frontal approach selection from 2000 to 2017. (B) Rates of programmable versus fixed valve use from 2000 to 2017. (C) Rates of all cause revision rates from 2000 to 2017. The r2 and P values were obtained through linear regression analysis and weighted by number of cases per year. The shaded pink areas denote the 95% confidence interval. The red line represents the linear regression line. The blue line represents the mean of the residuals for the rate of parietal approach at each time point.
WORLD NEUROSURGERY -: e1-e6, - 2019
In this study, the outcomes of ventricular shunting using a frontal or parietal approach for the treatment of iNPH performed at our institution over the last 2 decades were retrospectively reviewed, focusing on the effect of approach on the incidence of revision surgery. To our knowledge, this is the largest series comparing outcomes of these approaches in patients with iNPH. Although there are data primarily in the pediatric population suggesting that shunt function is more sustained and robust for frontal versus parietally inserted shunts, our results do not suggest a similar association in the iNPH population.6,7 Catheter approach may be most relevant to the incidence of proximal obstruction; therefore, choice of approach is potentially less important in the iNPH population in which proximal obstruction is less common. In our cohort, only 6 patients were observed to have proximal shunt malfunction, with no difference in incidence between patients receiving a frontal versus parietal shunt (Table 2). These data are consistent with prior studies suggesting that distal malfunction is the primary mode of shunt obstruction in the iNPH population.8 Lower rates of proximal obstruction in this population may be related to factors such as relative dilation of the ventricular system and a smaller choroid plexus in older adults when compared with the pediatric population, leading to a lower likelihood of the catheter tip penetrating the choroid plexus.9,10 Although differences in the risk of proximal shunt failure may exist for frontal and parietal shunts, an even larger cohort of patients with iNPH may be needed to address this question given the relative rarity of this complication in this population. The results suggest that anatomic approach may not have a significant impact on incidence of revision surgery in general and associated complications. As noted in the literature, there is not a standard, optimal approach for ventricular catheter placement in the iNPH population, and the results of this study support that either the frontal or parietal approach is a reasonable option for ventricular shunting.8,11,12 It would be of interest to determine whether there are any differences in functional outcomes after frontal versus parietal shunt placement. However, in the absence of such evidence, it seems appropriate to select catheter approach according to surgeon preference. There was no evidence that neuronavigation affects catheter accuracy in our cohort. Other studies in the literature report significant improvements in catheter accuracy with the use of neuronavigation and reduction in subsequent revision rates, particularly in the pediatric population.5,13-16 However, there is no consensus on the use of neuronavigation and prospective studies
www.journals.elsevier.com/world-neurosurgery
e5
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
addressing this issue are lacking. Given the selection bias inherent in our study, our findings on the utility of neuronavigation are inconclusive and additional studies are needed to investigate the effect of neuronavigation on catheter placement regarding accuracy, cost-effectiveness, and long-term outcomes. We observed a decrease in the incidence of revision surgery across the study period. This decrease occurred in tandem with an increase in utilization of programmable valves, which may account for part of the observed increase in shunt survival.17 Interestingly, we also observed a decline in utilization of parietal catheter placement during the study period, likely because of changes in surgeon preference over time.
those of prior studies suggests our results are generalizable.2 The analysis of the effect of neuronavigation on accuracy of catheter placement is also likely limited by selection bias. Additionally, there were differences in the usage of fixed-setting versus programmable valves between patients undergoing frontal versus parietal shunt placement (Table 1). Valve type may influence the need for subsequent revision surgery, particularly in patients who do not clinically respond to initial shunt placement, highlighting the need for prospective studies in which revision rates after frontal versus parietal shunt placement are examined in a controlled fashion.
Limitations This study is limited by the single-center, retrospective methodology. The observed rate of revision surgery may be erroneously low if patients underwent revision surgery after last follow-up at our institution; however, the comparability of our revision rates to
CONCLUSIONS
REFERENCES 1. Pujari S, Kharkar S, Metellus P, Shuck J, Williams MA, Rigamonti D. Normal pressure hydrocephalus: long-term outcome after shunt surgery. J Neurol Neurosurg Psychiatry. 2008;79: 1282-1286. 2. Hebb AO, Cusimano MD. Idiopathic normal pressure hydrocephalus: a systematic review of diagnosis and outcome. Neurosurgery. 2001;49: 1166-1184 [discussion: 1184-1186]. 3. Lind CR, Correia JA, Law AJ, Kejriwal R. A survey of surgical techniques for catheterising the cerebral lateral ventricles. J Clin Neurosci. 2008;15: 886-890. 4. Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3 suppl): S4-S16 [discussion: ii-v]. 5. Hayhurst C, Beems T, Jenkinson MD, et al. Effect of electromagnetic-navigated shunt placement on failure rates: a prospective multicenter study. J Neurosurg. 2010;113:1273-1278. 6. Albright AL, Haines SJ, Taylor FH. Function of parietal and frontal shunts in childhood hydrocephalus. J Neurosurg. 1988;69:883-886. 7. Whitehead WE, Riva-Cambrin J, Kulkarni AV, et al. Ventricular catheter entry site and not catheter tip location predicts shunt survival: a secondary analysis of 3 large pediatric
e6
www.SCIENCEDIRECT.com
We report no difference in rate of shunt revision between the frontal and parietal approach in the treatment of patients with iNPH. These findings may help guide surgeon selection of anatomic approach to ventricular shunting in patients with iNPH.
hydrocephalus studies. J Neurosurg Pediatr. 2017;19: 157-167. 8. Dickerman RD, McConathy WJ, Morgan J, et al. Failure rate of frontal versus parietal approaches for proximal catheter placement in ventriculoperitoneal shunts: revisited. J Clin Neurosci. 2005;12:781-783. 9. Meier U, Mutze S. Correlation between decreased ventricular size and positive clinical outcome following shunt placement in patients with normal-pressure hydrocephalus. J Neurosurg. 2004; 100:1036-1040. 10. Silverberg GD, Huhn S, Jaffe RA, et al. Downregulation of cerebrospinal fluid production in patients with chronic hydrocephalus. J Neurosurg. 2002;97:1271-1275. 11. Wan KR, Toy JA, Wolfe R, Danks A. Factors affecting the accuracy of ventricular catheter placement. J Clin Neurosci. 2011;18:485-488. 12. Lind CR, Tsai AM, Lind CJ, Law AJ. Ventricular catheter placement accuracy in non-stereotactic shunt surgery for hydrocephalus. J Clin Neurosci. 2009;16:918-920. 13. Azeem SS, Origitano TC. Ventricular catheter placement with a frameless neuronavigational system: a 1-year experience. Neurosurgery. 2007; 60(4 suppl 2):243-247 [discussion: 247-248].
children with hydrocephalus and small ventricles: the use of a frameless neuronavigation system. Childs Nerv Syst. 2002;18:26-29. 15. Wilson TJ, Stetler WR Jr, Al-Holou WN, Sullivan SE. Comparison of the accuracy of ventricular catheter placement using freehand placement, ultrasonic guidance, and stereotactic neuronavigation. J Neurosurg. 2013;119:66-70. 16. Kestle JR. Shunt insertion. J Neurosurg. 2013;119: 64. 17. Li M, Wang H, Ouyang Y, Yin M, Yin X. Efficacy and safety of programmable shunt valves for hydrocephalus: a meta-analysis. Int J Surg. 2017;44: 139-146.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 14 January 2019; accepted 4 March 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.027 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
14. Gil Z, Siomin V, Beni-Adani L, Sira B, Constantini S. Ventricular catheter placement in
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.027
Comparison of Complication and Revision Rates After Frontal Versus Parietal Approach for Ventricular Shunt Placement in Idiopathic Normal Pressure Hydrocephalus Adip G. Bhargav1, Lorenzo Rinaldo2, Giuseppe Lanzino2,3, Benjamin D. Elder2,4,5
-
BACKGROUND: Ventricular shunts are most commonly placed via a frontal or parietal approach. However, there is a paucity of data comparing complication and revision rates associated with these approaches in the idiopathic normal pressure hydrocephalus (iNPH) population.
complication and revision rates in patients with iNPH, and either approach is a reasonable first-line option.
METHODS: Patients with iNPH treated with ventricular shunting between 2001 and 2017 at our institution were included for analysis. Patient characteristics, catheter accuracy, and incidence of revision were determined from the medical record. Catheter accuracy was determined using axial computed tomography imaging and classified as grade 1, 2, or 3 based on location of the catheter tip.
INTRODUCTION
-
RESULTS: There were 348 patients included for analysis with 266 (76.4%) and 82 (23.6%) receiving a frontal versus parietal shunt, respectively. Patients undergoing the parietal approach were more likely to receive a programmable valve (37.8% vs. 25.2%; P [ 0.026). Neuronavigation was used more frequently for patients undergoing the parietal approach (26.8% vs. 4.1%; P < 0.001); however, a minority of cases used neuronavigation in general (9.5%). There was no difference in catheter accuracy between the 2 approaches and no difference in catheter accuracy with the use of neuronavigation. The overall revision rate was 21.0%, and there were no differences in the incidence of revisions between the frontal and parietal approaches (21.8% vs. 18.3%, respectively; P [ 0.495). There were no differences in revision subtypes between the approaches.
-
CONCLUSIONS: These results suggest that the type of approach for shunting may not have a significant impact on
-
Key words Hydrocephalus - Revision surgery - Shunt malfunction - Technique - Ventriculoperitoneal shunt -
Abbreviations and Acronyms CSF: Cerebrospinal fluid CT: Computed tomography iNPH: Idiopathic normal pressure hydrocephalus
WORLD NEUROSURGERY -: e1-e6, - 2019
V
entricular shunting to divert cerebrospinal fluid (CSF) is an effective therapy for idiopathic normal pressure hydrocephalus (iNPH).1,2 The 2 most common approaches for the placement of the ventricular catheter are via a frontal or parietal burr hole.3 There has been limited analysis of the complication and revision rates after shunt placement using different ventricular approaches in the iNPH population. To address this issue, the complication and revision rates associated with frontal versus parietal shunt placement in a large series of patients with iNPH were investigated. METHODS Patient Selection Institutional review board approval (18-000051) was obtained prior to the initiation of this study. We retrospectively reviewed our institution’s medical records for patients with iNPH treated with ventricular shunting between 2000 and 2017. Patients included for analysis had an established diagnosis of iNPH as determined by a neurologist. The diagnosis of iNPH was made according to clinical symptoms, radiographic ventriculomegaly, and opening pressure <25 cm H2O on lumbar puncture, along with improvement after a high-volume lumbar puncture.4 We excluded patients with a prior shunt placement on initial evaluation at our institution. The choice of approach was dependent on staff surgeon preference, facilitating a comparison of frontal and parietal in a relatively
From the 1Mayo Clinic School of Medicine and Departments of 2Neurosurgery, 3Radiology, 4 Bioengineering, and 5Orthopedics, Mayo Clinic, Rochester, Minnesota, USA To whom correspondence should be addressed: Benjamin D. Elder, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.027 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
www.journals.elsevier.com/world-neurosurgery
e1
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Figure 1. Grading of catheter placement using axial computed tomography imaging. (A) Grade 1 catheter placement with tip of catheter surrounded by cerebrospinal fluid. (B) Grade 2 placement with tip in
unselected population. Outcomes and follow-up time between shunt surgery and last appointment were recorded for each patient. Incidence of Revision Surgery and Determination of Shunt Malfunction Etiology The primary outcome of interest was the incidence of shunt revision surgery and revision surgery because of specific indications. The indication for revision was classified as one of the following: persistent symptoms without obstruction, proximal or distal obstruction, infection, overdrainage, or subdural collection. We defined shunt infection as symptomatology suggestive of infection with positive cultures for microbial growth or a positive CSF gram stain. Patients were suspected of having a shunt obstruction based on clinical presentation, mainly minimal to no clinical improvement after shunt placement or neurologic decline after initial improvement after shunt placement. Routine noninvasive evaluation to assess for shunt obstruction included palpation of shunt valve reservoir to evaluate refilling and radiographic evaluation in the form of radiographic shunt series and head computed tomography (CT) imaging. Given the low likelihood of proximal obstruction in this patient population and risk of iatrogenic shunt infection, shunt tapping was not routinely performed to assess for proximal obstruction. Additional ancillary tests such as radionuclide studies were also not routinely performed and obtained only at the discretion of the treating neurosurgeon in isolated cases. To classify obstruction because of a proximal versus distal cause, the operative record was reviewed. Shunt components were interrogated to determine the cause of malfunction in all patients undergoing revision surgery because of suspected shunt obstruction. Proximal obstruction was defined as a lack of flow through the ventricular catheter or as a visibly malpositioned ventricular catheter on imaging studies, with no catheter holes within the ventricular space. Distal obstruction was defined as little to no flow through the distal catheter using a manometer or on direct observation. Kinking of the distal catheter was also classified as a distal obstruction, as were peritoneal catheters
e2
www.SCIENCEDIRECT.com
contact with the ependymal lining of the ventricle. (C) Grade 3 placement with tip of catheter in brain parenchyma.
located in the preperitoneal space or within a loculated intraperitoneal fluid collection. Patients were classified as having persistent symptoms without obstruction if intraoperative interrogation revealed functional shunt components. The incidence of multiple revision surgeries, subdural fluid collections, and need for subdural collection evacuation was also noted. Noninvasive manipulation of shunt parameters was not classified as a surgical revision. Invasive procedures to decrease overdrainage in patients with clinical or radiographic signs of ventricular overdrainage— subdural collection or pachymeningeal enhancement—were considered to be surgical revisions. These included interventions such as clavicular incision to tie off a distal shunt or complete shunt removal. Patient Variables of Interest The primary variable of interest was the type of anatomic approach selected for shunt placement, specifically the frontal versus parietal approach. Additional variables including age, sex, body mass index, use of neuronavigation, valve type, and distal catheter location were recorded. Distal catheter location was classified as in the peritoneum, pleural space, or atrium. Catheter Accuracy To compare the accuracy of the frontal and parietal approach in ventricular shunt placement, all of the patients’ postoperative head CT scans were examined and the catheter placement was graded according to the methodology proposed by Hayhurst et al.5 Grade 1 was defined as the catheter tip being completely surrounded by CSF without contact with ependymal lining. Grade 2 was defined as the catheter tip touching the ependymal lining of the ventricle. Grade 3 was assigned when there was complete misplacement of the catheter outside of the ventricle or if a portion of the catheter was intraparenchymal (Figure 1). Temporal Trends Given the extended time period of our study, changes in the utilization of frontal versus parietal approach, fixed-setting versus
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.027
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Table 1. Comparison of Patients Undergoing Frontal versus Parietal Approach Frontal Approach (n [ 266)
Parietal Approach (n [ 82)
Total (N [ 348)
P Value
73.1 8.3
73.5 8.4
73.2 8.3
0.693
Male
174 (65.4)
50 (61.0)
224 (64.4)
Female
92 (34.6)
32 (39.0)
124 (35.6)
29.4 4.9
28.4 4.9
29.2 4.9
0.114
11 (4.1)
22 (26.8)
33 (9.5)
<0.0001y
Fixed
199 (74.8)
51 (62.2)
250 (71.8)
Programmable
67 (25.2)
31 (37.8)
98 (28.2)
0.026y
260 (97.7)
81 (98.8)
341 (98.0)
0.559
Atrium
5 (1.9)
1 (1.2)
6 (1.7)
0.688
Pleural space
1 (0.4)
0 (0)
1 (0.3)
0.578
58 (21.8)
15 (18.3)
73 (21.0)
0.495
0.3 0.6
0.2 0.6
0.3 0.6
0.692
0e4
0e3
0e4
15.2 23.5
21.3 38.8
16.5 27.1
Variable Age (years) Sex
BMI* Use of neuronavigation
0.463
Valve type
Distal catheter location Peritoneum
Revision surgery Revisions per patient Range Time to initial revision (months) Median Follow-up time (months) Median
5.3
1.5
4
25.7 31.7
33.6 42.6
27.6 34.7
12.1
12.8
12.3
0.569
0.127
Values are mean SD, number of patients (%), or as otherwise indicated. BMI, body mass index. *BMI unavailable for 17 patients. yStatistical significance.
programmable valve, and incidence of revision surgery over time were assessed using linear regression analysis. The independent variable was the year of shunt placement (2000e2017). Separate regression models were constructed for catheter approach, valve type, and incidence of revision, with the yearly percentage of cases using a parietal approach, a programmable valve, or requiring revision surgery serving as the dependent variable, respectively. Models were weighted according to the total number of cases performed during each year of the study. Results were presented as a b coefficient, representing the change in the dependent variable per unit change in the independent variable, correlation coefficient (r2), and P value. Statistical Analysis Descriptive statistics were performed for continuous and categorical variables. Mean and SD were reported for continuous variables, whereas frequency and percentage were reported for categorical variables. Student t test, Pearson c2 test, and analysis of variance were used where appropriate to perform comparative statistics for continuous and categorical variables. Multivariate analysis was performed using a Cox proportional hazards model.
WORLD NEUROSURGERY -: e1-e6, - 2019
Alpha levels for statistical significance were set at 0.05. Commercially available software (JMP 10.0.0 [SAS Institute Inc., Cary, North Carolina, USA]) was used to perform the analysis. RESULTS Patient Characteristics and Outcomes There were 348 patients included for analysis. The mean age of the cohort was 73.2 8.3 years, with most patients being men (64.4%). Most patients had their shunt placed via a frontal approach (n ¼ 266, 76.4%), with a relative minority of patients receiving parietal shunts (n ¼ 82, 23.6%). Patients undergoing a parietal approach were more likely to receive a programmable valve than a fixed valve (37.8% vs. 25.2%, respectively; P ¼ 0.026). The most common distal catheter location was the peritoneum (n ¼ 341, 98.0%) followed by the atrium (n ¼ 6, 1.7%) and pleural space (n ¼ 1, 0.3%). Baseline characteristics of patients receiving the frontal versus parietal approach are shown in Table 1. There were 73 patients (21.0%) who required revision surgery, with 12 patients (3.4%) undergoing multiple revisions. The mean time to revision was 16.5 27.1 months. In 24 patients (6.9%), no
www.journals.elsevier.com/world-neurosurgery
e3
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Table 2. Incidence of Revision Subtypes in Patients Undergoing Frontal versus Parietal Approach Variable
Frontal Approach (n [ 266)
Parietal Approach (n [ 82)
Total (N [ 348)
P Value
58 (21.8)
15 (18.3)
73 (21.0)
0.495
Any revision Multiple revisions
8 (3.0)
4 (4.9)
12 (3.4)
0.417
Persistent symptoms without obstruction
18 (6.8)
6 (7.3)
24 (6.9)
0.864
Distal obstruction
16 (6.0)
2 (2.4)
18 (5.2)
0.201
Proximal obstruction
3 (1.1)
3 (3.7)
6 (1.7)
0.124
Infection
10 (3.7)
3 (3.7)
13 (3.7)
0.966
Overdrainage requiring revision
12 (4.5)
2 (2.4)
14 (4.0)
0.404
Intracranial hemorrhage
3 (1.1)
3 (3.7)
6 (1.7)
0.124
Subdural collection
47 (17.7)
22 (26.8)
69 (19.9)
0.071
Evacuated subdural
15 (5.6)
5 (6.1)
20 (5.7)
0.876
Values are number of patients (%) or as otherwise indicated.
definite obstruction was observed despite persistent patient symptomatology. Eighteen patients (5.2%) underwent revision surgery for distal obstruction, whereas 6 patients (1.7%) underwent revision surgery for proximal obstruction. Thirteen patients (3.7%) underwent revision surgery because of infection, and 14 patients (4.0%) received revision surgery for overdrainage. Sixtynine patients (19.9%) developed a subdural collection, with 20 of these patients (5.7%) requiring surgical evacuation. Among the patients who developed a subdural collection, 22 patients (31.9%) had a programmable valve, with valve reprogramming to a higher setting performed in 18 patients (81.8%). In the remaining 4 patients, the subdural collection was found to be asymptomatic and stable on serial imaging; therefore, the valve was not adjusted. Of the 14 patients requiring revision surgery for overdrainage, 3 (21.4%) had a programmable valve. Prior to revision surgery, shunt reprogramming was initially attempted; however, the patients either remained symptomatic or the subdural collection was noted to enlarge, ultimately leading to surgical shunt ligation. There were no statistically significant differences in the rate of overall revision surgery (21.8% vs. 18.3%, respectively; P ¼ 0.495)
or revision subtypes after shunt placement via the frontal versus parietal approach (Table 2). We did observe that patients receiving a fixed-setting valve were more likely to undergo revision surgery relative to those receiving a programmable valve (24.0% vs. 13.3%, respectively; P ¼ 0.027). Using a Cox proportional hazards model, when adjusting for valve type, catheter approach was still not associated with increased risk of revision surgery (relative risk for frontal vs. parietal approach: 1.33; 95% confidence interval, 0.74e2.38; P ¼ 0.335). Comparison of Catheter Placement with the Frontal and Parietal Approach The frequency of grade 1, 2, and 3 catheter accuracy was 26.1% (n ¼ 81), 69.4% (n ¼ 215), and 4.5% (n ¼ 14). There were no statistically significant differences in catheter accuracy when placed via a frontal versus parietal approach (Table 3). The use of neuronavigation was more common in patients receiving the parietal approach (26.8% vs. 4.1%, respectively; P < 0.001) (Table 1); however, the use of neuronavigation did not have a significant impact on catheter accuracy (Table 4).
Table 3. Catheter Accuracy in Patients Undergoing Frontal versus Parietal Approach
Variable
Frontal Approach (n [ 266)
Table 4. Effect of Neuronavigation on Catheter Accuracy
Parietal Approach (n [ 82)
Total (N [ 348)
P Value
Catheter accuracy*
Neuronavigation (n [ 33)
No Navigation (n [ 315)
Total (N [ 348)
P Value
Catheter accuracy with neuronavigation*
Grade 1
66 (27.8)
15 (20.5)
81 (26.1)
0.215
Grade 1
8 (24.2)
73 (26.4)
81 (26.1)
0.794
Grade 2
160 (67.5)
55 (75.3)
215 (69.4)
0.204
Grade 2
23 (69.7)
192 (69.3)
215 (69.4)
0.964
Grade 3
11 (4.6)
3 (4.1)
14 (4.5)
0.848
Grade 3
2 (6.1)
12 (4.3)
14 (4.5)
0.651
Values are number of patients (%) or as otherwise indicated. *Thirty-eight patients did not have postoperative head computed tomography scan.
e4
Variable
www.SCIENCEDIRECT.com
Values are number of patients (%) or as otherwise indicated. *Thirty-eight patients did not have postoperative head computed tomography scan.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.027
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
Temporal Trends in Catheter Approach, Valve Type, and Revision Rate The utilization of the parietal approach (versus the frontal approach) was found to decrease over the study period (b ¼ 1.083, r2 ¼ 0.237, P ¼ 0.040) (Figure 2A), whereas the utilization of programmable valves was found to increase (b ¼ 1.279, r2 ¼ 0.265, P ¼ 0.029) (Figure 2B). The rate of revision surgery because of all causes was found to decrease over the study period (b ¼ 1.208, r2 ¼ 0.413, P ¼ 0.004) (Figure 2C). DISCUSSION
Figure 2. Temporal trends in the selection of anatomic approach, valve type, and revision rates. (A) Rates of parietal versus frontal approach selection from 2000 to 2017. (B) Rates of programmable versus fixed valve use from 2000 to 2017. (C) Rates of all cause revision rates from 2000 to 2017. The r2 and P values were obtained through linear regression analysis and weighted by number of cases per year. The shaded pink areas denote the 95% confidence interval. The red line represents the linear regression line. The blue line represents the mean of the residuals for the rate of parietal approach at each time point.
WORLD NEUROSURGERY -: e1-e6, - 2019
In this study, the outcomes of ventricular shunting using a frontal or parietal approach for the treatment of iNPH performed at our institution over the last 2 decades were retrospectively reviewed, focusing on the effect of approach on the incidence of revision surgery. To our knowledge, this is the largest series comparing outcomes of these approaches in patients with iNPH. Although there are data primarily in the pediatric population suggesting that shunt function is more sustained and robust for frontal versus parietally inserted shunts, our results do not suggest a similar association in the iNPH population.6,7 Catheter approach may be most relevant to the incidence of proximal obstruction; therefore, choice of approach is potentially less important in the iNPH population in which proximal obstruction is less common. In our cohort, only 6 patients were observed to have proximal shunt malfunction, with no difference in incidence between patients receiving a frontal versus parietal shunt (Table 2). These data are consistent with prior studies suggesting that distal malfunction is the primary mode of shunt obstruction in the iNPH population.8 Lower rates of proximal obstruction in this population may be related to factors such as relative dilation of the ventricular system and a smaller choroid plexus in older adults when compared with the pediatric population, leading to a lower likelihood of the catheter tip penetrating the choroid plexus.9,10 Although differences in the risk of proximal shunt failure may exist for frontal and parietal shunts, an even larger cohort of patients with iNPH may be needed to address this question given the relative rarity of this complication in this population. The results suggest that anatomic approach may not have a significant impact on incidence of revision surgery in general and associated complications. As noted in the literature, there is not a standard, optimal approach for ventricular catheter placement in the iNPH population, and the results of this study support that either the frontal or parietal approach is a reasonable option for ventricular shunting.8,11,12 It would be of interest to determine whether there are any differences in functional outcomes after frontal versus parietal shunt placement. However, in the absence of such evidence, it seems appropriate to select catheter approach according to surgeon preference. There was no evidence that neuronavigation affects catheter accuracy in our cohort. Other studies in the literature report significant improvements in catheter accuracy with the use of neuronavigation and reduction in subsequent revision rates, particularly in the pediatric population.5,13-16 However, there is no consensus on the use of neuronavigation and prospective studies
www.journals.elsevier.com/world-neurosurgery
e5
ORIGINAL ARTICLE ADIP G. BHARGAV ET AL.
COMPARISON OF FRONTAL VERSUS PARIETAL SHUNT PLACEMENT FOR INPH
addressing this issue are lacking. Given the selection bias inherent in our study, our findings on the utility of neuronavigation are inconclusive and additional studies are needed to investigate the effect of neuronavigation on catheter placement regarding accuracy, cost-effectiveness, and long-term outcomes. We observed a decrease in the incidence of revision surgery across the study period. This decrease occurred in tandem with an increase in utilization of programmable valves, which may account for part of the observed increase in shunt survival.17 Interestingly, we also observed a decline in utilization of parietal catheter placement during the study period, likely because of changes in surgeon preference over time.
those of prior studies suggests our results are generalizable.2 The analysis of the effect of neuronavigation on accuracy of catheter placement is also likely limited by selection bias. Additionally, there were differences in the usage of fixed-setting versus programmable valves between patients undergoing frontal versus parietal shunt placement (Table 1). Valve type may influence the need for subsequent revision surgery, particularly in patients who do not clinically respond to initial shunt placement, highlighting the need for prospective studies in which revision rates after frontal versus parietal shunt placement are examined in a controlled fashion.
Limitations This study is limited by the single-center, retrospective methodology. The observed rate of revision surgery may be erroneously low if patients underwent revision surgery after last follow-up at our institution; however, the comparability of our revision rates to
CONCLUSIONS
REFERENCES 1. Pujari S, Kharkar S, Metellus P, Shuck J, Williams MA, Rigamonti D. Normal pressure hydrocephalus: long-term outcome after shunt surgery. J Neurol Neurosurg Psychiatry. 2008;79: 1282-1286. 2. Hebb AO, Cusimano MD. Idiopathic normal pressure hydrocephalus: a systematic review of diagnosis and outcome. Neurosurgery. 2001;49: 1166-1184 [discussion: 1184-1186]. 3. Lind CR, Correia JA, Law AJ, Kejriwal R. A survey of surgical techniques for catheterising the cerebral lateral ventricles. J Clin Neurosci. 2008;15: 886-890. 4. Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005;57(3 suppl): S4-S16 [discussion: ii-v]. 5. Hayhurst C, Beems T, Jenkinson MD, et al. Effect of electromagnetic-navigated shunt placement on failure rates: a prospective multicenter study. J Neurosurg. 2010;113:1273-1278. 6. Albright AL, Haines SJ, Taylor FH. Function of parietal and frontal shunts in childhood hydrocephalus. J Neurosurg. 1988;69:883-886. 7. Whitehead WE, Riva-Cambrin J, Kulkarni AV, et al. Ventricular catheter entry site and not catheter tip location predicts shunt survival: a secondary analysis of 3 large pediatric
e6
www.SCIENCEDIRECT.com
We report no difference in rate of shunt revision between the frontal and parietal approach in the treatment of patients with iNPH. These findings may help guide surgeon selection of anatomic approach to ventricular shunting in patients with iNPH.
hydrocephalus studies. J Neurosurg Pediatr. 2017;19: 157-167. 8. Dickerman RD, McConathy WJ, Morgan J, et al. Failure rate of frontal versus parietal approaches for proximal catheter placement in ventriculoperitoneal shunts: revisited. J Clin Neurosci. 2005;12:781-783. 9. Meier U, Mutze S. Correlation between decreased ventricular size and positive clinical outcome following shunt placement in patients with normal-pressure hydrocephalus. J Neurosurg. 2004; 100:1036-1040. 10. Silverberg GD, Huhn S, Jaffe RA, et al. Downregulation of cerebrospinal fluid production in patients with chronic hydrocephalus. J Neurosurg. 2002;97:1271-1275. 11. Wan KR, Toy JA, Wolfe R, Danks A. Factors affecting the accuracy of ventricular catheter placement. J Clin Neurosci. 2011;18:485-488. 12. Lind CR, Tsai AM, Lind CJ, Law AJ. Ventricular catheter placement accuracy in non-stereotactic shunt surgery for hydrocephalus. J Clin Neurosci. 2009;16:918-920. 13. Azeem SS, Origitano TC. Ventricular catheter placement with a frameless neuronavigational system: a 1-year experience. Neurosurgery. 2007; 60(4 suppl 2):243-247 [discussion: 247-248].
children with hydrocephalus and small ventricles: the use of a frameless neuronavigation system. Childs Nerv Syst. 2002;18:26-29. 15. Wilson TJ, Stetler WR Jr, Al-Holou WN, Sullivan SE. Comparison of the accuracy of ventricular catheter placement using freehand placement, ultrasonic guidance, and stereotactic neuronavigation. J Neurosurg. 2013;119:66-70. 16. Kestle JR. Shunt insertion. J Neurosurg. 2013;119: 64. 17. Li M, Wang H, Ouyang Y, Yin M, Yin X. Efficacy and safety of programmable shunt valves for hydrocephalus: a meta-analysis. Int J Surg. 2017;44: 139-146.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 14 January 2019; accepted 4 March 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.03.027 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
14. Gil Z, Siomin V, Beni-Adani L, Sira B, Constantini S. Ventricular catheter placement in
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.03.027