Scholarly article on topic 'Shunt revision requirements after posthemorrhagic hydrocephalus of prematurity: insight into the time course of shunt dependency'

Shunt revision requirements after posthemorrhagic hydrocephalus of prematurity: insight into the time course of shunt dependency Academic research paper on "Clinical medicine"

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Academic research paper on topic "Shunt revision requirements after posthemorrhagic hydrocephalus of prematurity: insight into the time course of shunt dependency"

Childs Nerv Syst

DOI 10.1007/s00381-015-2865-5

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ORIGINAL PAPER

Shunt revision requirements after posthemorrhagic hydrocephalus of prematurity: insight into the time course of shunt dependency

Joanna Y. Wang1 • Eric M. Jackson1 • George I. Jallo1 • Edward S. Ahn1

Received: 24 July 2015 / Accepted: 29 July 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract

Purpose Intraventricular hemorrhage (IVH) is a common affliction of preterm infants and often results in posthemorrhagic hydrocephalus (PHH). These patients typically eventually require permanent CSF diversion and are presumed to be indefinitely shunt-dependent. To date, however, there has been no study of long-term shunt revision requirements in patients with PHH.

Methods We analyzed retrospectively collected data for 89 preterm patients diagnosed with grades III and IV IVH and PHH at our institution from 1998 to 2011. Results Sixty-nine out of 89 patients (77.5 %) underwent ventriculoperitoneal (VP) shunt placement, and 33 (47.8 %) required at least one shunt revision and 18 (26.1 %) required multiple revisions. The mean ± standard deviation follow-up time for shunted patients was 5.0 ± 3.3 years. The majority of early failures were due to proximal catheter malfunction, while later failures were mostly due to distal catheter problems. There was a significant difference in the number of patients requiring revisions in the first 3 years following initial VP shunt insertion compared after 3 years, with 28 revisions versus 10 (p < 0.004). In 8 out of 10 patients who underwent shunt revisions after 3 years, evidence of obstructive hydro-cephalus was found on imaging either in the form of an isolated fourth ventricular cyst or aqueductal stenosis. Conclusions Our results suggest that in a distinct subset of patients with PHH, obstructive hydrocephalus may develop,

* Edward S. Ahn eahn4@jhmi.edu

1 Division of Pediatric Neurosurgery, Johns Hopkins University School of Medicine, 600 North Wolfe Street, Phipps 560A, Baltimore, MD 21287, USA

resulting in long-term dependence on CSF diversion. Further study on the factors associated with long-term shunt dependence and revision requirements within the PHH group is warranted.

Keywords Hydrocephalus . Intraventricular hemorrhage . Posthemorrhagic hydrocephalus . Revision . Shunt

Introduction

Severe intraventricular hemorrhage (IVH) portends a poor prognosis in premature infants. In addition to neurodevelopmental impairment, which is seen in 7.4 to 48.7 % of patients with grade III or IV IVH, a significant proportion of patients develop posthemorrhagic hydrocephalus (PHH) [4, 5]. While there is no standard treatment paradigm for the management of PHH, many patients will initially undergo placement of a temporizing device such as a ventricular reservoir or a ventriculosubgaleal shunt (VSGS), with the majority of these patients going on to require permanent shunting [17, 29]. These patients are assumed to experience long-term shunt-dependent hydrocephalus and to be at lifelong risk for shunt failure and related complications.

The long-term care of a ventricular shunt can be burdensome for both the patient and their family as well as the health care system, irrespective of hydrocephalus etiology. In 1998 to 2000, pediatric data from the Nationwide Inpatient Sample revealed the mortality associated with ventriculoperitoneal (VP) shunt insertion or revision to range from 0.3 to 0.8 % [23]. Annually, the cost of ventricular shunt-related procedures in the USA is over $1 billion, mostly from shunt complications and revisions [14, 21, 25]. Shunt failure can be due to proximal or distal catheter obstruction, disconnection, or migration; valve malfunction; or infection. In the pediatric

Published online: 07 August 2015

Ö Springer

population, 20 to 70 % of patients with shunts will ultimately require revision at median cost of each revision at $19,485, with some patients requiring more than 20 revisions over 5 years [ 14, 20]. Patients with PHH appear to be at higher risk for shunt failure and also have significantly decreased shunt survival times [12, 22].

Even though long-term shunt dependency is presumed in most pediatric hydrocephalus patients, little data on long-term shunt revision rates exist. Stone and colleagues examined shunt revision rates in a pediatric hydrocephalus of all causes cohort with over 15 years of follow-up, reporting that 12.5 % of patients required their first shunt revision more than 10 years after initial shunt insertion [25]. Previous studies have investigated time to first shunt revision, but none have examined the rates of shunt revision per year over the course of follow-up. In this study, a retrospective review of preterm infants treated for severe IVH and PHH at a single institution was performed to study changes in rates of shunt failure over time and to gain insight into long-term shunt dependence.

Methods

Data collection and outcome measures

A retrospective review of 89 preterm infants who were diagnosed with and treated for IVH and PHH at our institution between 1998 and 2011 was conducted. All research protocols were approved by our Institutional Review Board for Human Research. The diagnosis of IVH and PHH was established by cranial ultrasonography. The medical records of these patients were reviewed for information on patient demographics, birth history, IVH Papile grade, temporizing device insertion rates (ventricular reservoir and VSGS), VP shunt insertion, VP shunt failure and revision, and clinical follow-up visits. Prematurity was defined as an estimated gestational age (EGA) at birth of less than 37 weeks, with patients with an EGA at birth between 28 and 32 weeks defined as very pre-term and those born at less than 28 weeks defined as extremely preterm. Birth weight was stratified into very low birth weight (VLBW; <1500 g) and extremely low birth weight (ELBW; <1000 g). Primary outcomes included VP shunt insertion, VP shunt revision, and multiple VP shunt revisions. Computed tomography (CT) and magnetic resonance imaging (MRI) scans obtained in patients at the time of shunt revision was reviewed.

Treatment techniques

In the 43 patients who underwent reservoir placement, a Medtronic CSF-Neonate reservoir (Minneapolis, MN), 10 mm, with integrated 3-4 cm right angle ventricular catheter was inserted in the right frontal region, adjacent to the anterior

fontanelle, through a curvilinear incision. For the 46 patients who underwent VSGS insertion, a large subgaleal pocket was created adjacent to the neonatal reservoir. The dome of the reservoir had cross-hair slits cut into it to allow for CSF egress. Minimal criteria for insertion of a VP shunt were progressive ventricular dilation, rapid increase in head circumference, and weight greater than 2 kg. The majority of VP shunts were inserted via an occipital approach. The reservoirs were removed at the time of shunt insertion. Valves utilized included the DePuy Synthes Codman Hakim (Raynham, MA), Medtronic Strata (Minneapolis, MN), Medtronic Delta (Minneapolis, MN), and Aesculap proGAV (Tuttlingen, Germany).

Data analysis

Comparisons of patient demographics and outcome data were performed using Pearson's x2 test and Student's t test for parametric data. Kaplan-Meier survival analysis was used to examine time to shunt failure. Cox proportional hazards regression analysis was used to identify factors predictive of time to VP shunt revision. Data is given as mean ± standard deviation, median with range, or with 95 % confidence intervals (CI). Statistical significance was defined asp < 0.05. All statistical analyses were performed using Stata/IC 12 (StataCorp LP, College Station, TX).

Results

Patient population

For the 89 patients in our complete cohort, all were preterm and had low birth weights. The mean EGA at birth was 26 4/7 ± 2 1/7 weeks, with 64 (71.9 %) patients classified as extremely preterm. The mean weight at birth was 922 ± 291 g, with 58 (65.2 %) ELBW infants. Thirty-three (42.3 %) patients were male, and the majority of patients were African-American (47, 52.8 %), while 38 (42.7 %) were Caucasian. All had severe IVH, with 45 (51.1 %) grade III and 43 (48.9 %) grade IV. All 89 patients were initially managed with a temporizing device, with 43 (48.3 %) undergoing ventricular reservoir placement and 46 (51.7 %) undergoing VSGS insertion. Sixty-nine (77.5 %) of the patients eventually underwent VP shunt insertion, at an EGA of 40 1/7 ± 7 4/7 weeks. The mean duration of clinical follow-up was 5.0 ± 3.3 years (range 0.03 to 13.13 years) (Table 1).

Shunt failure outcomes

Thirty-three (47.8 %) of these patients ultimately required at least one shunt revision, and 18 (26.1 %) required multiple revisions, for a total of 66 shunt revisions. No patient factors were found to be significantly associated with permanent

Table 1 Patient demographics and baseline characteristics Table 2 Shunt failure outcomes

Characteristic Value (n = 89) Characteristics Number of revisions per patient, median with range Value 2, 1-9

EGA at birth, weeks 26 4/7 ± 2 1/7 Cause of malfunction

Male 33 (42.3) Proximal catheter occlusion 31

Weight at birth, grams 922 ± 291 Valve malfunction 6

Race/ethnicity Distal catheter occlusion or disconnection 14

Caucasian 38 (42.7) Shunt infection 10

African-American 47 (52.8) Other 5

Other 4 (4.5) Shunt components replaced at the time of revision

IVH grade Proximal catheter only 24

III 45 (51.1) Proximal catheter and valve 8

IV 43 (48.9) Valve only 5

Temporizing device Distal catheter and valve 1

Ventricular reservoir 43 (48.3) Distal catheter only 11

VSGS 46(51.7) Complete system 17

Initial VP shunt insertion

Patients undergoing shunting 69 (77.5) 66 shunt revision procedures were performed. Data given as values unless

otherwise indicated

EGA at initial shunt insertion 40 1/7 ± 7 4/7

Approach

Frontal 7 (10.9) Shunt revisions over time

Parieto-occipital 57(89.1)

Patients requiring shunt revision 33 (47.8)

Clinical follow-up time from initial shunt insertion, years 5.0 ± 3.3

Data given as mean ± standard deviation or values with (%)

EGA estimated gestational age, VP ventriculoperitoneal, VSGS

ventriculosubgaleal shunt

shunting, including patient age and weight at birth and at surgery, IVH grade, and temporizing device. Additionally, none of these patient factors were predictive of shunt revision. The median number of revision procedures experienced by each patient was 2 (range 1 to 9); 15 (45.5 %) of the patients had one revision; 13 (39.4 %) had two; 2 (6.1 %) had three; and 1 each (3.0%) had four, six, and nine revisions. Only ELBW was significantly predictive of multiple (>2) shunt revisions, which was not associated with patient demographics, initial shunt insertion approach, initial valve used, or duration of clinical follow-up (p = 0.02). Of the 66 revisions performed, 31 (47.0 %) were for proximal catheter occlusion, 6 (9.1 %) for valve malfunction, 14 (21.2 %) for distal catheter occlusion or disconnection, and 10 (15.2 %) for shunt infection (Table 2). Of the revisions for shunt infection, nine occurred in the first year after shunt insertion and one in the second year. The cause of the proximal shunt malfunctions were true mechanical obstructions that were not in the setting of CSF infections. As such, 24 (36.4 %) revisions involved replacement of the proximal catheter only, 8 (12.1 %) replacement of the proximal catheter and valve, 5 (7.6 %) of the valve only, 1 (1.5 %) of the distal catheter and valve, 11 (16.7 %) of the distal catheter only, and 17 (25.8 %) of the entire shunt system (Table 2).

Time to shunt failure is depicted in the Kaplan-Meier curve in Fig. 1; at 1 year, 73.6 % (95 % CI 61.0-82.7 %) remained malfunction-free, which declined to 44.1 % (95 % CI 30.257.1 %) at 5 years and 36.7 % (95 % CI 20.1-52.6 %) at 10 years. No factors were significantly associated with time to shunt failure. To investigate shunt dependence over time, the number of revision procedures over time was examined. In the first year following VP shunt insertion, of the 58 patients with at least 1 year of clinical follow-up, 17 (29.3 %) required revisions. Fifty-five patients had at least 2 years of follow-up, and 12 (21.8 %) underwent revision; of 51 patients with follow-up in the third year, 5 (9.8 %) underwent revision. Patients requiring revisions per year of follow-up was 4 (9.8 %) in the fourth year, 3 (11.1 %) in the fifth year, 1 (4.5 %) in the sixth, 0 in the seventh, 1 (6.3 %) in the eighth, and 2 (18.2 %) in the ninth; no patients required revisions in the tenth and eleventh years (Fig. 2). There was a significant difference in the number of revisions performed in the first

3 years following initial VP shunt insertion compared to revisions performed after three years, with 28 patients requiring revisions in the first 3 years versus 10 after (p < 0.004).

The type of malfunction varied with time from initial VP shunt insertion, with the majority of revisions in the first

4 years following insertion due to proximal occlusion (Fig. 3). In the first year of follow-up, 33 shunt failures occurred, of which 15 (45.5 %) were due to proximal occlusions, 3 (9.1 %) were due to valve failure, and 4(12.1%) were due to distal obstruction. Later malfunction was due to distal malfunction in the majority of cases, and in the two patients requiring shunt revision in the ninth year, both experienced

Fig. 1 Kaplan-Meier shunt survival curve from time of initial VP shunt insertion. At 1 year, 73.6 % (95 % CI 61.0-82.7 %) ofpatients remained shunt failure-free; at 5 years, 44.1 % (95 % CI 30.2-57.1 %); at 10 years, 36.7 % (95 % CI 20.1-52.6 %). The median shunt survival time was 3.6 years

distal disconnection of their shunt. One of these patients had previously experienced no shunt malfunctions, and the other had only experienced one prior revision.

Late shunt revisions

Overall, 10 patients underwent late revisions, or shunt failure more 3 years from the date of initial shunt insertion. Two (20 %) of these patients underwent revision in the fourth year due to shortened distal ventriculoatrial catheters noted on imaging, but were both asymptomatic and without evidence of interval ventricular enlargement on imaging. Four (40 %) patients developed isolated fourth ventricular cysts; in one patient who presented with lethargy and vomiting in the eighth

Fig. 2 Number of revisions per year of follow-up; 58 patients had at least 1 year of follow-up, in which 33 revisions were performed in 17 patients; 27 patients had at least 5 years of follow-up, in which 3 patients underwent 3 revisions; 11 patients had at least 10 years of follow-up, in which 2 patients underwent 1 revision each

year after initial insertion, MRI2 years prior had demonstrated obstruction from a large isolated fourth ventricular cyst (Fig. 4a). The remaining four (40 %) patients, including the two who underwent revisions in the ninth year, had imaging during the course of their care revealing blocked communication between the third and fourth ventricles, indicative of obstruction at the cerebral aqueduct (Fig. 4b).

Discussion Key results

A significant proportion ofpatients with IVH and PHH go on to require permanent CSF diversion and have been assumed to be shunt-dependent and at lifelong risk for shunt failure and related complications. However, little data on the long-term durability of VP shunting and shunt revision rates exist to support this idea. While previous studies have almost exclusively examined shunt survival and time to first shunt failure, the change in rates of shunt revision is a unique method of investigating shunt dependency. While we did not find any predictors of VP shunt insertion, ELBW was a predictor of multiple shunt revisions. While the majority of early failures were due to proximal catheter obstruction, most late failures were due to distal shunt disconnection. The rate of shunt failure and revision declined significantly after the third year after VP shunt insertion.

Shunt outcomes

The incidence of IVH and PHH appears to be on the decline, likely as a result of improvements in obstetrical and neonatal

0 2 4 6 8 10 12

Time from VP shunt insertion (years)

Fig. 3 Type of shunt malfunction over time from VP shunt insertion; 66 shunt revisions were performed in total. In the first year of follow-up, 33 shunt failures occurred, of which 15 (45.5 %) were due to proximal occlusions, 3 (9.1 %) were due to valve failure, and 4 (12.1 %) were due to distal obstruction. In the eighth and ninth years of follow-up, one and two shunt failures occurred due to distal disconnection, respectively

care [1]. Although most previous reports have cited rates of permanent CSF diversion in the range of 0 to 25 % in these patients, a recent study by Chittiboina et al. noted that 95.4 % of their cohort of 109 patients with PHH underwent shunt placement [6, 8, 10, 17, 29, 31, 32]. However, Alan and colleagues found that the percentage of patients with PHH requiring surgical intervention was, for the first time at their institution, on the decline [1]. Rates of permanent shunting in patients with PHH appear highly variable and can likely be attributed to the lack of standard guidelines for the management of PHH.

While it is relatively well-established that PHH itself is associated with poorer neurodevelopmental outcomes, the direct relationship between permanent shunting and outcomes in pediatric hydrocephalus remains incompletely understood, especially in preterm infants who often have other neurologic conditions. Patients who require permanent CSF diversion often carry more morbidity than patients who never undergo

shunting, and their poorer outcomes is most likely due more to the severity of the initial neurologic insult rather than complications of shunting [1, 17]. Older studies have found that in addition to IVH severity, the number of shunt revisions is also predictive of long-term survival, but shunt complications have not consistently been found to be associated with neurologic outcomes [9, 16].

Many studies have been conducted in pediatric patients with hydrocephalus to find risk factors for shunt failure and have identified earlier age at initial shunt placement, hydro-cephalus etiology, shunt components replaced during first revision (partial vs. total), and lower hospital volume as predictive of shunt revisions [3, 11, 19, 28]. Patients with PHH appear to experience a higher risk of shunt malfunction and decreased shunt survival [12, 22]. Reports of revision rates range from 63.8 to 84.1 %, while we found a lower rate of 47.8 % [6, 10, 12]. Chittiboina et al. described a median time to first shunt revision of 1.1 years compared to the 0.25 years

Fig. 4 Late shunt revisions. a Representative MRI of a patient with an isolated fourth ventricular cyst who required a late distal shunt revision performed 8 years after initial shunt insertion. b Representative MRI that demonstrates aqueductal stenosis in a patient who required a late distal shunt revision 6 years after initial shunt insertion

found by Notarianni et al. In our cohort, the median time was greater, at 3.6 years [6,12]. Few studies have investigated risk factors for shunt revision in only patients with PHH, but lower EGA was predictive of earlier revision in two studies, and lower EGA and the presence of obstructive hydrocephalus were associated with multiple revisions in one report [6, 7].

Many strategies to decrease the rates of shunt failure and revision have been proposed. The use of temporizing devices has variable success in reducing shunt placement, as in most studies of reservoirs and VSGSs, the majority of patients go on to permanent shunt insertion [10, 29, 31, 32]. Antibiotic-impregnated shunts may be capable of reducing the rates of shunt infection in pediatric hydrocephalus, but do not address the most common cause of shunt failure, proximal obstruction [13, 18]. Awide variety of shunt systems are currently available to clinicians, but their impact on shunt failures rates is unclear. Notarianni et al. did not find a difference in the rates of shunt failure in comparing programmable systems with pressure-controlled or valveless shunts, and recent studies with newer valves have not found a difference in revision rates by valve type [2, 12]. However, the rates of shunt failure remain high, and new methods are needed to ensure shunt survival [24]. Other techniques for managing hydrocephalus, such as endoscopic third ventriculostomy, have been used in select patients with PHH, but the mainstay of treatment for PHH remains VP shunt insertion [26, 30].

While it is clear that many patients with PHH experience early shunt failure, late revision rates have not been reported. While variability in follow-up time limits the conclusions that can be drawn from our data, the rate of shunt malfunction and revision significantly declined after the third year after VP shunt insertion. There is the possibility that shunts are less prone to mechanical failure in older children. However, another consideration is that some PHH patients may achieve shunt independence where even a mechanical failure of the shunt remains subclinical. Interestingly, in patients with myelomeningocele, the rate of shunt revisions within 3 years of initial shunt insertion and the rate after 3 years appears roughly equivalent [27]. This comparison suggests that the pattern of revision requirement we observed may be unique to patients with PHH. It would be worthwhile to examine the long-term shunt performance in infants with other etiologies of hydrocephalus.

This study also reveals an age-dependent pattern in that the percentage of revisions due to proximal catheter occlusion drops to 0 % from being the most common cause of failures in the first and second years. Previous studies have also found that proximal shunt malfunctions are the most common cause of shunt failure, with approximately half of all revisions performed for proximal catheter failure, but none to date had examined changes in the distribution of cause of shunt failure over time [6]. Interestingly, in the patients who underwent shunt revisions more than 3 years after the placement of their

initial shunt, other than two asymptomatic patients with shortened distal catheters, evidence of obstruction of CSF flow within the ventricles was found, either due to an isolated fourth ventricular cyst or aqueductal stenosis. This finding suggests that in a distinct subset of patients with PHH, obstructive or non-communicating hydrocephalus may develop, resulting in long-term dependence on CSF diversion. In these patients with late shunt failures, further imaging may be indicated to identify an obstructive cause for their presentation. If present, these patients may be candidates for endoscopic third ventriculostomy or related procedures.

In a study of patients with pediatric hydrocephalus, Stone et al. found that 8 (12.5 %) out of 64 patients required their first shunt revision more than 10 years after insertion of their initial VP shunts. Two of these patients had hydrocephalus secondary to IVH, but their cause of shunt failure whether there was obstruction at the aqueduct or fourth ventricle is unknown [26]. While this report may suggest that no pediatric patients with hydrocephalus can be assumed have attained shunt independence at any time, the results may be biased by the fact that this was a retrospective review of only patients with at least 15 years of follow-up. The baseline characteristics of this cohort may be significantly different from their complete patient population with less regular follow-up. Reddy and colleagues studied the shunt failure rates in a long-term cohort of adult patients who were treated with VP shunts as children for hydrocephalus and found that 39 (37.1 %) of 105 patients had their first shunt revision after age 17. However, the age at initial shunt insertion ranged from 0 to 17 years, and the number of patients with PHH included was not specified [15].

Limitations

The primary limitation of this study is its single-institution retrospective design. While infants with PHH at our institution are chosen to undergo VP shunt insertion for progressive hy-drocephalus and weight-based criteria, this practice may be different from other centers where shunting may be deferred for longer periods of time. The number of late shunt failures captured is also dependent on the length of follow-up. However, our study remains the only long-term follow-up study of VP shunting in PHH which examines changes in rates of shunt revision over time, which may have important implications for patient care. A long-term prospective trial is needed to further examine signs of shunt independence for patients with PHH.

Conclusions

A significant proportion of patients with IVH and PHH eventually require permanent CSF diversion and are presumed to

experience lifelong shunt-dependent hydrocephalus, but little data exists to support this conclusion. In our cohort of 89 preterm infants with severe IVH and resultant PHH, the rate of shunt failure and revision significantly declined after the third year after initial VP shunt insertion. The majority of shunt revisions in the first 4 years of follow-up was due to proximal catheter occlusion, but later revisions were most often due to distal catheter failures. Additionally, in all eight patients with symptomatic late shunt failures, an obstructive cause of their presentation was identified on imaging, which suggests that in a subset of patients with PHH, non-communicating hydrocephalus may develop and result in long-term dependence on CSF diversion. These results also raise the possibility that PHH may not result in inevitable long-term shunt dependence. A prospective study of VP shunt revision rates in patients with PHH is warranted to assess rates of shunt dependence over time.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Financial support None.

References

1. Alan N, Manjila S, Minich N, Bass N, Cohen AR, Walsh M, et al. (2012) Reduced ventricular shunt rate in very preterm infants with severe intraventricular hemorrhage: an institutional experience. J Neurosurg Pediatr 10:357-364

2. Beez T, Sarikaya-Seiwert S, Bellstadt L, Muhmer M, Steiger HJ (2014) Role of ventriculoperitoneal shunt valve design in the treatment of pediatric hydrocephalus—a single center study of valve performance in the clinical setting. Childs Nerv Syst 30:293-297

3. Berry JG, Hall MA, Sharma V, Goumnerova L, Slonim AD, Shah SS (2008) A multi-institutional, 5-year analysis of initial and multiple ventricular shunt revisions in children. Neurosurgery 62:445453 discussion 453-444

4. Brouwer A, Groenendaal F, van Haastert IL, Rademaker K, Hanlo P, de Vries L (2008) Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for posthemorrhagic ventricular dilatation. J Pediatr 152:648-654

5. Brouwer AJ, van Stam C, Uniken Venema M, Koopman C, Groenendaal F, de Vries LS (2012) Cognitive and neurological outcome at the age of 5-8 years of preterm infants with posthemorrhagic ventricular dilatation requiring neurosurgical intervention. Neonatology 101:210-216

6. Chittiboina P, Pasieka H, Sonig A, Bollam P, Notarianni C, Willis BK, et al. (2013) Posthemorrhagic hydrocephalus and shunts: what are the predictors of multiple revision surgeries? J Neurosurg Pediatr 11:37-42

7. Lazareff JA, Peacock W, Holly L, Ver Halen J, Wong A, Olmstead C (1998) Multiple shunt failures: an analysis of relevant factors. Childs Nerv Syst 14:271-275

8. Lee IC, Lee HS, Su PH, Liao WJ, Hu JM, Chen JY (2009) Posthemorrhagic hydrocephalus in newborns: clinical characteristics and role of ventriculoperitoneal shunts. Pediatr Neonatol 50: 26-32

9. Levy ML, Masri LS, McComb JG (1997) Outcome for preterm infants with germinal matrix hemorrhage and progressive hydrocephalus. Neurosurgery 41:1111-1117 discussion 1117-1118

10. Limbrick Jr DD, Mathur A, Johnston JM, Munro R, Sagar J, Inder T, et al. (2010) Neurosurgical treatment of progressive posthemor-rhagic ventricular dilation in preterm infants: a 10-year single-institution study J Neurosurg Pediatr 6:224-230

11. McGirt MJ, Wellons 3rd JC, Nimjee SM, Bulsara KR Fuchs HE, George TM (2003) Comparison oftotal versus partial revision ofinitial ventriculoperitoneal shunt failures. Pediatr Neurosurg 38:34-40

12. Notarianni C, Vannemreddy P, Caldito G, Bollam P, Wylen E, Willis B, et al. (2009) Congenital hydrocephalus and ventriculoperitoneal shunts: influence of etiology and programmable shunts on revisions. J Neurosurg Pediatr 4:547-552

13. Parker SL, Attenello FJ, Sciubba DM, Garces-Ambrossi GL, Ahn E, Weingart J, et al. (2009) Comparison of shunt infection incidence in high-risk subgroups receiving antibiotic-impregnated versus standard shunts. Childs Nerv Syst 25:77-83 discussion 85

14. Patwardhan RV, Nanda A (2005) Implanted ventricular shunts in the United States: the billion-dollar-a-year cost of hydrocephalus treatment. Neurosurg 56:139-144 discussion 144—135

15. Reddy GK, Bollam P, Caldito G (2014) Long-term outcomes of ventriculoperitoneal shunt surgery in patients with hydrocephalus. World Neurosurg 81:404-410

16. Reinprecht A, Dietrich W, Berger A, Bavinzski G, Weninger M, Czech T (2001) Posthemorrhagic hydrocephalus in preterm infants: long-term follow-up and shunt-related complications. Childs Nerv Syst 17:663-669

17. Robinson S (2012) Neonatal posthemorrhagic hydrocephalus from prematurity: pathophysiology and current treatment concepts. J Neurosurg Pediatr 9:242-258

18. Sciubba DM, Noggle JC, Carson BS, Jallo GI (2008) Antibiotic-impregnated shunt catheters for the treatment of infantile hydro-cephalus. Pediatr Neurosurg 44:91-96

19. Shah SS, Hall M, Slonim AD, Hornig GW, Berry JG, Sharma V (2008) A multicenter study of factors influencing cerebrospinal fluid shunt survival in infants and children. Neurosurgery 62: 1095-1102 discussion 1102-1093

20. Shannon CN, Simon TD, Reed GT, Franklin FA, Kirby RS, Kilgore ML, et al. (2011) The economic impact of ventriculoperitoneal shunt failure. J Neurosurg Pediatr 8:593-599

21. Simon TD, Riva-Cambrin J, Srivastava R, Bratton SL, Dean JM, Kestle JR (2008) Hospital care for children with hydrocephalus in the United States: utilization, charges, comorbidities, and deaths. J Neurosurg Pediatr 1:131-137

22. Simon TD, Whitlock KB, Riva-Cambrin J, Kestle JR, Rosenfeld M, Dean JM, et al. (2012) Association of intraventricular hemorrhage secondary to prematurity with cerebrospinal fluid shunt surgery in the first year following initial shunt placement. J Neurosurg Pediatr 9:54-63

23. Smith ER, Butler WE, Barker 2nd FG (2004) In-hospital mortality rates after ventriculoperitoneal shunt procedures in the United States, 1998 to 2000: relation to hospital and surgeon volume of care. J Neurosurg 100:90-97

24. Stein SC, Guo W (2008) Have we made progress in preventing shunt failure? A critical analysis. J Neurosurg Pediatr 1:40-47

25. Stone JJ, Walker CT, Jacobson M, Phillips V, Silberstein HJ (2013) Revision rate of pediatric ventriculoperitoneal shunts after 15 years. J Neurosurg Pediatr 11:15-19

26. Stone SS, Warf BC (2014) Combined endoscopic third ventriculostomy and choroid plexus cauterization as primary treatment for infant hydrocephalus: a prospective North American series. J Neurosurg Pediatr 14:439-446

27. Talamonti G, D'Aliberti G, Collice M (2007) Myelomeningocele: long-term neurosurgical treatment and follow-up in 202 patients. J Neurosurg 107:368-386

28. Tuli S, Drake J, Lawless J, Wigg M, Lamberti-Pasculli M (2000) Risk factors for repeated cerebrospinal shunt failures in pediatric patients with hydrocephalus. JNeurosurg 92:31-38

29. Wang JY, Amin AG, Jallo GI, Ahn ES (2014) Ventricular reservoir versus ventriculosubgaleal shunt for posthemorrhagic hydrocepha-lus in preterm infants: infection risks and ventriculoperitoneal shunt rate. J Neurosurg Pediatr 14:447-454

30. Warf BC, Campbell JW, Riddle E (2011) Initial experience with combined endoscopic third ventriculostomy and choroid plexus cauterization for post-hemorrhagic hydrocephalus of prematurity: the importance of prepontine cistern status and the predictive value of FIESTA MRI imaging. Childs Nerv Syst 27:1063-1071

31. Wellons JC, Shannon CN, Kulkarni AV, Simon TD, Riva-Cambrin J, Whitehead WE, et al. (2009) A multicenter retrospective comparison of conversion from temporary to permanent cerebrospinal fluid diversion in very low birth weight infants with posthemor-rhagic hydrocephalus. J Neurosurg Pediatr 4:50-55

32. Willis B, Javalkar V, Vannemreddy P, Caldito G, Matsuyama J, Guthikonda B, et al. (2009) Ventricular reservoirs and ventriculoperitoneal shunts for premature infants with posthemor-rhagic hydrocephalus: an institutional experience. J Neurosurg Pediatr 3:94-100