Calgary Shunt Protocol, an adaptation of the Hydrocephalus Clinical Research Network shunt protocol, reduces shunt infections in children

Michael M. H. Yang Section of Pediatric Neurosurgery, Division of Neurosurgery, Department of Clinical Neurosciences; and

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Walter Hader Section of Pediatric Neurosurgery, Division of Neurosurgery, Department of Clinical Neurosciences; and

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Kelly Bullivant Section of Pediatric Neurosurgery, Division of Neurosurgery, Department of Clinical Neurosciences; and

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Mary Brindle Section of Pediatric Surgery, Department of Surgery, University of Calgary, Calgary, Alberta, Canada

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Jay Riva-Cambrin Section of Pediatric Neurosurgery, Division of Neurosurgery, Department of Clinical Neurosciences; and

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OBJECTIVE

The shunt protocol developed by the Hydrocephalus Clinical Research Network (HCRN) was shown to significantly reduce shunt infections in children. However, its effectiveness had not been validated in a non-HCRN, small- to medium-volume pediatric neurosurgery center. The present study evaluated whether the 9-step Calgary Shunt Protocol, closely adapted from the HCRN shunt protocol, reduced shunt infections in children.

METHODS

The Calgary Shunt Protocol was prospectively applied at Alberta Children’s Hospital from May 23, 2013, to all children undergoing any shunt procedure. The control cohort consisted of children undergoing shunt surgery between January 1, 2009, and the implementation of the Calgary Shunt Protocol. The primary outcome was the strict HCRN definition of shunt infection. Univariate analyses of the protocol, individual elements within, and known confounders were performed using Student t-test for measured variables and chi-square tests for categorical variables. Multivariable logistic regression was performed using stepwise analysis.

RESULTS

Two-hundred sixty-eight shunt procedures were performed. The median age of patients was 14 months (IQR 3–61), and 148 (55.2%) were male. There was a significant absolute risk reduction of 10.0% (95% CI 3.9%–15.9%) in shunt infections (12.7% vs 2.7%, p = 0.004) after implementation of the Calgary Shunt Protocol. In univariate analyses, chlorhexidine was associated with fewer shunt infections than iodine-based skin preparation solution (4.1% vs 12.3%, p = 0.02). Waiting ≥ 20 minutes between receiving preoperative antibiotics and skin incision was also associated with a reduction in shunt infection (4.5% vs 14.2%, p = 0.007). In the multivariable analysis, only the overall protocol independently reduced shunt infections (OR 0.19 [95% CI 0.06–0.67], p = 0.009), while age, etiology, procedure type, ventricular catheter type, skin preparation solution, and time from preoperative antibiotics to skin incision were not significant.

CONCLUSIONS

This study externally validates the published HCRN protocol for reducing shunt infection in an independent, non-HCRN, and small- to medium-volume pediatric neurosurgery setting. Implementation of the Calgary Shunt Protocol independently reduced shunt infection risk. Chlorhexidine skin preparation and waiting ≥ 20 minutes between administration of preoperative antibiotic and skin incision may have contributed to the protocol’s quality improvement success.

ABBREVIATIONS

ACH = Alberta Children’s Hospital; CSP = Calgary Shunt Protocol; EVD = external ventricular drain; HCRN = Hydrocephalus Clinical Research Network; IVH = intraventricular hemorrhage.

OBJECTIVE

The shunt protocol developed by the Hydrocephalus Clinical Research Network (HCRN) was shown to significantly reduce shunt infections in children. However, its effectiveness had not been validated in a non-HCRN, small- to medium-volume pediatric neurosurgery center. The present study evaluated whether the 9-step Calgary Shunt Protocol, closely adapted from the HCRN shunt protocol, reduced shunt infections in children.

METHODS

The Calgary Shunt Protocol was prospectively applied at Alberta Children’s Hospital from May 23, 2013, to all children undergoing any shunt procedure. The control cohort consisted of children undergoing shunt surgery between January 1, 2009, and the implementation of the Calgary Shunt Protocol. The primary outcome was the strict HCRN definition of shunt infection. Univariate analyses of the protocol, individual elements within, and known confounders were performed using Student t-test for measured variables and chi-square tests for categorical variables. Multivariable logistic regression was performed using stepwise analysis.

RESULTS

Two-hundred sixty-eight shunt procedures were performed. The median age of patients was 14 months (IQR 3–61), and 148 (55.2%) were male. There was a significant absolute risk reduction of 10.0% (95% CI 3.9%–15.9%) in shunt infections (12.7% vs 2.7%, p = 0.004) after implementation of the Calgary Shunt Protocol. In univariate analyses, chlorhexidine was associated with fewer shunt infections than iodine-based skin preparation solution (4.1% vs 12.3%, p = 0.02). Waiting ≥ 20 minutes between receiving preoperative antibiotics and skin incision was also associated with a reduction in shunt infection (4.5% vs 14.2%, p = 0.007). In the multivariable analysis, only the overall protocol independently reduced shunt infections (OR 0.19 [95% CI 0.06–0.67], p = 0.009), while age, etiology, procedure type, ventricular catheter type, skin preparation solution, and time from preoperative antibiotics to skin incision were not significant.

CONCLUSIONS

This study externally validates the published HCRN protocol for reducing shunt infection in an independent, non-HCRN, and small- to medium-volume pediatric neurosurgery setting. Implementation of the Calgary Shunt Protocol independently reduced shunt infection risk. Chlorhexidine skin preparation and waiting ≥ 20 minutes between administration of preoperative antibiotic and skin incision may have contributed to the protocol’s quality improvement success.

In Brief

The authors implemented a 9-step shunt protocol at their institution that resulted in a significant reduction in cerebral shunt infections.

Shunt infections continue to be a common complication of CSF shunts for children with hydrocephalus.13 In large database studies, the procedural infection rate has been reported between 5% and 10%.10,11,15 Shunt infections are associated with significant morbidity, including lower IQ scores and worse long-term quality of life.27 Moreover, shunt infection is an important contributor to the cost in the management of pediatric hydrocephalus, including hospital admissions, antibiotics, shunt removals, and implantations of new hardware. The mean cost to manage a shunt infection is estimated to be $30,000, leading to $259 million in hospital charges in 2003.23

Efforts have been made to identify modifiable risk factors and create standardize protocols to help reduce shunt infections in children.10,12–14,21 Kestle et al.14 published a paper for the Hydrocephalus Clinical Research Network (HCRN), presenting a standardized protocol for shunt insertions that led to a 36% relative risk reduction and a 3.2% absolute risk reduction in the number of shunt infections across 4 centers. Despite their study being a multicenter international study, generalizability to independent, small- to medium-volume children’s hospitals has not been established.

After learning about the effectiveness of the HCRN shunt protocol in 2012, the authors at the University of Calgary, Alberta Children’s Hospital (ACH), set out to implement a similar protocol as part of a quality improvement initiative. The 9-step Calgary Shunt Protocol (CSP) was created around the 2011 HCRN protocol14 and was implemented beginning on May 23, 2013. The goals for the current study were as follows: 1) to determine whether a small- to medium-volume, non-HCRN center was able to effectively reduce shunt infection rates by implementing a closely adapted protocol and 2) to explore which variables within the CSP could explain those effects.

Methods

Calgary Shunt Protocol

Institutional approval was obtained from the Conjoint Health Research Ethics Board at the University of Calgary. ACH (during the study timeline) was a non-HCRN, small- to medium-volume tertiary pediatric neurosurgery center (40–50 shunt cases a year). Prior to the implementation of the CSP, our neurosurgery service did not have (nor did the hospital dictate) a standardized way to perform shunt surgeries, except for the administration of preoperative antibiotics as recommended by the WHO.17 The CSP (Fig. 1) was modeled on HCRN’s 201114 published standardized protocol to reduce CSF shunt infection, with a few exceptions. Specifically, the CSP excluded positioning the head away from the main operating room door, injecting vancomycin/gentamicin into the shunt reservoir, and applying a mandatory dressing. Logistical challenges between hospital pharmacy and the operating theater in combination with a lack of specific efficacy of this variable in Kestle et al.’s article14 prevented the inclusion of intrareservoir antibiotic injection. The CSP included two additional steps that were not in the original HCRN protocol: waiting at least 30 minutes after preoperative antibiotics administration before skin incision and mandating normothermia throughout the case.

FIG. 1.
FIG. 1.

Calgary Shunt Protocol. The CSP was adapted from the 2011 Kestle et al. HCRN protocol. OR = operating room.

We hypothesized that waiting at least 30 minutes after preoperative administration of antibiotics before skin incision would have a positive impact on shunt infections for two reasons. Studies have shown that it takes at least 30 minutes before cefazolin (the most common preoperative antibiotics administered for neurosurgical procedures) will reach minimum inhibitory concentrations.5 Also, by setting a precise time interval, this ensured that preoperative antibiotics were always given before skin incision, which has been shown to improve surgical site infections.17 Perioperative hypothermia has also been associated with increased surgical site infection risk.16,26 In a study evaluating mild intraoperative hypothermia during surgery for intracranial aneurysms, Todd et al.26 showed that postoperative bacteremia was more common in the hypothermia group than the normothermia group (p = 0.05). In the colorectal population, mild intraoperative hypothermia has also been associated with 15% more infections compared to a normothermia group (p = 0.009).16

Protocol Development and Implementation

An internal quality assurance audit showed the shunt infection rates at ACH were between 12% and 15% in 2011. These results prompted an interdisciplinary meeting between neurosurgery and infectious disease to evaluate strategies to reduce shunt infections in November 2012. Neurosurgery leadership hosted meetings and in-services with key stakeholders (e.g., nursing and anesthesia), where we described the morbidity and cost associated with shunt infections and the result of the quality assurance audit. Buy-in was established from these various stakeholders, which acknowledged the need to reduce shunt infection rates at the hospital. Furthermore, an operating room nurse champion was identified who aided in education and enforcement of the shunt protocol among nurses. The CSP was successfully implemented beginning on May 23, 2013, without a trial phase.

Entry Criteria

To maintain maximal comparability, the entry criteria into the study were the same as the standardized protocol published by Kestle et al.14 Specifically, the entry criteria included age less than 19 years and patients undergoing shunt insertion or revision involving any ventriculoperitoneal, ventriculoatrial, ventriculopleural, cystoperitoneal, subduroperitoneal, or lumboperitoneal shunts. Patients who underwent a shunt procedure to treat a shunt infection after appropriate antibiotic treatment were also included. Children who underwent surgery for the insertion or revision of ventricular access devices or subgaleal shunts were excluded at the time of those procedures but were potentially eligible if they later underwent a permanent CSF shunt procedure.

Shunt procedures were classified into 4 different categories: 1) primary shunt insertions (patients who underwent their first CSF shunt implantation), 2) shunt revision (surgery in which a child entered the operating room with all shunt equipment previously implanted and left the operating room with all shunt equipment implanted), 3) shunt insertion after placement of an external ventricular drain (EVD; not infected), and 4) shunt insertion after treatment for shunt infection.

Outcome Variables

Each shunt procedure was monitored for infection for a minimum of 6 months unless a shunt revision occurred or the patients died within 6 months of their procedure. Surveillance for shunt infections was conducted during routine clinic visits, emergency room visits, and hospital admissions, and supplemented by screening laboratory findings (e.g., CSF Gram stains) prospectively in the postimplementation cohort and using electronic and paper medical records for the retrospective preimplementation cohort. The primary outcome was the HCRN definition of shunt infection, which included one of the following: 1) identification of organisms on culture or Gram stain from CSF, wound swab, or abdominal pseudocyst fluid; 2) shunt erosion with exposed hardware; 3) abdominal pseudocyst (regardless of culture positivity); or 4) positive blood culture in patients with a ventriculoatrial shunt. The overall center infection rates before and after the implementation of the CSP were summated.

Data Collection

The CSP was implemented at the ACH on May 23, 2013, for all children undergoing CSF shunt surgery. Patients included in the prospective postprotocol implementation cohort had their shunt surgery between May 23, 2013, and December 31, 2016. Children undergoing shunt surgery between Jan 1, 2009, and prior to the implementation of the CSP were used as the retrospective control cohort. Data were collected prospectively from the CSP start date and retrospectively back to January 2009. Compliance for each step of the protocol was prospectively recorded by a participating member of the surgical team (attending surgeon, residents, fellows, or nurse practitioner) at the end of each operation using a physical checklist. The handwashing technique was recorded as compliant only if all personnel involved in the operation performed a formal scrub. The use of antiseptic cream (in lieu of a formal hand scrub) was considered noncompliant. Normothermia was defined as maintaining core temperature between 36°C and 38°C at all times from induction of anesthesia to the removal of intraoperative monitors. To ensure the validity of the physical checklist, the time between preoperative antibiotics and skin incision and whether postoperative antibiotics were given were retrospectively cross-checked against anesthesia electronic and paper charting (exact times were reported by anesthesia and nursing staff). Perfect and near-perfect compliance (one deviation in protocol) to the CSP was also recorded.

For the preimplementation cohort, other clinical variables that could potentially affect shunt infection rates were also collected retrospectively through electronic and paper charts. Skin preparation solution, type of catheter (e.g., antibiotic impregnated, barium, or Bioglide), shunt valve, surgeon, patient age at surgery, specific preoperative and postoperative antibiotic agents given, and etiology of hydrocephalus were identified and documented.

Statistical Analysis

Univariate analyses of outcomes associated with the protocol itself, the individual elements within the protocol, and potential confounders (e.g., age, hydrocephalus etiology, etc.) were performed using Student t-tests for continuous variables and chi-square tests for categorical variables. The Mann-Whitney U-test was used to compare age and time between preoperative antibiotics administration and skin incision due to unequal variances between groups. Variables on univariate analysis that had a p value less than 0.10 and potential confounders (e.g., age and etiology) were included in the multivariable logistic regression analysis. Multivariable logistic regression was performed using the stepwise variable selection method with shunt infection at 6 months as the outcome variable. The robustness of the model was evaluated by repeating the multivariable logistic regression by using forward and backward variable selection methods. Evaluation for interactions was not performed due to limited sample size. Variables included in the multivariable logistic regression included age, etiology of hydrocephalus, procedure type, implementation of the CSP, ventricular catheter type, type of skin preparation, and waiting at least 30 minutes between administration of preoperative antibiotics and skin incision. Level of significance was set at alpha = 0.05. All statistical analyses were performed on SAS version 9.4.

Results

Description of Enrolled Cohort

Two-hundred sixty-eight unique shunt procedures were performed between January 2009 and December 2016 (158 in the preprotocol era and 110 in the postprotocol era). The median age of patients was 14 months (range 0–213 months), and 148 patients (55.2%) were male. The most common etiologies of hydrocephalus were intraventricular hemorrhage (IVH) secondary to prematurity (22.4%), aqueductal stenosis (11.9%), and myelomeningocele (9.7%). New shunt insertions represented 46% of the procedures, while shunt revisions (43%), insertions following noninfected EVDs (4%), and reinsertions following shunt infections (6%) were the remainder. The vast majority of shunt insertions performed were ventriculoperitoneal shunts (87%). The majority of patients received intravenous cefazolin as their preoperative antibiotics (89%). Table 1 summarizes the baseline characteristic of all patients included in the study. As to shunt procedures, 158 and 110 surgeries were performed in the preprotocol and postprotocol eras, respectively. Baseline demographics between the preprotocol and the postprotocol eras were similar except for the individual steps within the CSP and procedure type. Specifically, the postprotocol era included more revisions and fewer postinfection procedures (Table 2). Ventricular catheter type also differed between eras (p < 0.001), with significantly diminished use of Bioglide and antibiotic-impregnated catheters in the postprotocol era.

TABLE 1.

Baseline characteristics of all patients and 268 shunt procedures in study

VariableValue
Median age at op in mos14 (3–61)
Male sex148 (55.2)
Etiology
 IVH due to prematurity60 (22.4)
 Aqueductal stenosis32 (11.9)
 Myelomeningocele26 (9.7)
 Arachnoid cysts25 (9.3)
 Brain tumor24 (9)
 Congenital communicating23 (8.6)
 Postinfection18 (6.7)
 Other60 (22.4)
Procedure type
 New insertion124 (46.3)
 Revision116 (43.3)
 Replacement shunt after infection17 (6.3)
 New shunt after EVD11 (4.1)
Shunt configuration
 Ventriculoperitoneal234 (87.3)
 Subduroperitoneal19 (7.1)
 Cystoperitoneal12 (4.5)
 Ventriculoatrial2 (0.7)
 Lumboperitoneal1 (0.4)
Valve type
 Fixed differential pressure154 (57.5)
 Programmable71 (26.5)
 Delta2 (0.7)
 Flow regulating1 (0.4)
 Not replaced & unknown40 (14.9)
Ventricular catheter
 Bioglide105 (39.2)
 Barium impregnated77 (28.7)
 Antibiotic impregnated32 (11.9)
 Not replaced & unknown54 (20.1)

Values are presented as the number (%) of procedures or as the median (IQR).

TABLE 2.

Comparison of baseline characteristics by protocol implementation

VariablePreprotocol (n = 158)Postprotocol (n = 110)p Value
Median age at op in mos16 (4–54)8 (3–66)0.66
Male sex86 (54.4)62 (56.4)0.80
Etiology
 IVH due to prematurity27 (17.1)33 (30)
 Aqueductal stenosis20 (12.7)12 (10.9)
 Myelomeningocele12 (7.6)14 (12.7)
 Arachnoid cysts16 (10.1)9 (8.2)
 Brain tumor15 (9.5)9 (8.2)
 Congenital communicating15 (9.5)8 (7.3)
 Postinfection12 (7.6)6 (5.5)
 Other41 (26)19 (17.3)0.18
Procedure type
 New insertion75 (47.5)49 (44.6)0.01
 Revision60 (38.0)56 (50.9)
 Replacement shunt after infection16 (10.1)1 (0.9)
 New shunt after EVD7 (4.4)4 (3.6)
Shunt configuration
 Ventriculoperitoneal136 (86.1)98 (89.1)0.51
 Subduroperitoneal14 (8.9)5 (4.6)
 Cystoperitoneal7 (4.4)5 (4.6)
 Ventriculoatrial1 (0.6)1 (0.9)
 Lumboperitoneal0 (0)1 (0.9)
Ventricular catheter
 Bioglide96 (60.8)9 (8.2)<0.001
 Barium impregnated3 (1.9)74 (67.3)
 Antibiotic impregnated25 (15.8)7 (6.4)
 Not replaced & unknown34 (21.5)20 (18.2)
Shunt infection20 (12.7)3 (2.7)0.004
Perfect protocol compliance0 (0)77 (70)<0.001
Skin preparation
 Chlorhexidine13 (8.2)109 (99.1)<0.001
Antibiotics given ≥30 mins prior to incision24 (15.2)93 (84.6)<0.001
Postop antibiotics given136 (86.1)106 (96.4)0.005

Values are presented as the number (%) of procedures or as the median (IQR). Boldface type indicates statistical significance.

Shunt Infections

There were a total of 23 shunt infections in the study, of which 20 (representing a 12.7% infection rate) were in the preprotocol era and 3 (representing a 2.7% infection rate) in the postprotocol era. This represented a significant absolute risk reduction of 10% (95% CI 3.9%–15.9%, p = 0.004) and a 79% relative risk reduction in shunt infections after the implementation of the CSP (Fig. 2). Table 3 compares patient and surgical characteristic between infected and noninfected groups. Age (p = 0.45), sex (p = 0.13), etiology of hydrocephalus (p = 0.16), procedure type (p = 0.08), shunt configuration (p = 0.76), surgeon (p = 0.56), and type of valve (p = 0.94) were not significantly associated with shunt infection. Ventricular catheter type was associated with shunt infection (p = 0.03), with Bioglide ventricular catheters having higher and barium-impregnated catheters having lower infection rates. Table 4 outlines the organisms identified in the shunt infection cohort.

FIG. 2.
FIG. 2.

Line graph comparing shunt infection rates before and after protocol implementation. The pre- and postimplementation infection rates were 12.7% (red line) and 2.7% (green line), respectively (p = 0.004). ARR = absolute risk reduction. Figure is available in color online only.

TABLE 3.

Univariate analyses of patient and procedural characteristics

VariableShunt Infection (n = 23)No Shunt Infection (n = 245)p Value
Median age at op in mos10 (4–25)16 (3–63)0.45
Male sex9 (39.1)139 (56.7)0.13
Etiology
 IVH due to prematurity3 (13)57 (23.3)0.16
 Aqueductal stenosis1 (4.4)31 (12.7)
 Myelomeningocele2 (8.7)24 (9.8)
 Arachnoid cysts0 (0)25 (10.2)
 Brain tumor4 (17.4)20 (8.2)
 Congenital communicating4 (17.4)19 (7.8)
 Postinfection3 (13)15 (6.1)
 Other6 (26.1)54 (22)
Procedure type
 New insertion9 (39.1)115 (46.9)0.08
 Revision8 (34.8)108 (44.1)
 Replacement shunt after infection4 (17.4)13 (5.3)
 New shunt after EVD2 (8.7)9 (3.7)
Shunt configuration
 Ventriculoperitoneal22 (95.7)212 (86.5)0.76
 Subduroperitoneal1 (4.4)18 (7.4)
 Cystoperitoneal0 (0)12 (4.9)
 Ventriculoatrial0 (0)2 (0.8)
 Lumboperitoneal0 (0)1 (0.4)
Valve type
 Fixed differential pressure15 (65.2)139 (56.7)0.94
 Programmable6 (26.1)65 (26.5)
 Delta0 (0)2 (0.8)
 Flow regulating0 (0)1 (0.4)
 Not replaced & unknown2 (8.7)38 (15.5)
Ventricular catheter
 Bioglide4 (17.4)28 (11.4)0.03
 Barium impregnated1 (4.4)76 (31.0)
 Antibiotic impregnated14 (60.9)91 (37.1)
 Not replaced & unknown4 (17.4)50 (20.4)

Values are presented as the number (%) of procedures or as the median (IQR). Boldface type indicates statistical significance.

TABLE 4.

Organisms identified in the shunt infection cohort

OrganismPreprotocolPostprotocol
Staphylococcus epidermidis4 (20)2 (67)
Methicillin-sensitive Staphylococcus aureus4 (20)0 (0)
Cutibacterium acnes*4 (20)0 (0)
Methicillin-resistant S. aureus1 (5)0 (0)
Staphylococcus lugdunesis1 (5)0 (0)
Streptococcus pneumonia0 (0)1 (33)
Enterococcus faecalis1 (5)0 (0)
Staphylococcus schleiferi1 (5)0 (0)
Neisseria lactamica1 (5)0 (0)
Candida albicans1 (5)0 (0)
Multiorganism2 (10)0 (0)
Total20 (100)3 (100)

Values are presented as the number (%) of cases of infection.

Formerly known as Propionibacterium acnes.

Cutibacterium acnes and methicillin-sensitive S. aureus.

Table 5 compares the overall CSP, as well as each of its individual steps, by infection group. The CSP items that could not be reliably collected retrospectively in the preimplementation cohort (which included the sign on the door, allowing the skin preparation to sit for at least 3 minutes, and double gloving) were excluded for the analysis. The use of chlorhexidine-containing skin preparation solution compared to iodine-based solution was associated with diminished shunt infections (OR 0.30 [95% CI 0.11–0.85], p = 0.02). The protocol required at least 30 minutes between preoperative antibiotic administration and skin incision; however, on univariate analysis, this step in the protocol was not associated with a reduction in shunt infections (OR 0.43 [95% CI 0.16–1.12], p = 0.08). However, an exploratory subanalysis (including both pre- and postprotocol patients) found a significant protective association with shunt infection when the threshold was set at ≥ 20 minutes (OR 0.29 [95% CI 0.11–0.72], p = 0.007). More broadly, the median time between preoperative antibiotics and skin incision in the infection versus the no-infection group was 11.5 minutes and 29 minutes, respectively (p = 0.01). Perfect compliance with the protocol was recorded in 77/110 (70%), while the near-perfect (not more than 1 protocol step not followed) compliance rate was 73.6% (81/110) (Table 6). After CSP implementation, perfect compliance was associated with a 2.6% infection rate versus a 3.7% rate for noncompliant cases.

TABLE 5.

Univariate analyses of the CSP and its individual steps

VariableShunt Infection (n = 23)No Shunt Infection (n = 245)p Value
Preimplementation*20 (87.0)138 (56.3)0.004
Postimplementation3 (13.0)107 (43.7)
Skin preparation solution
 Chlorhexidine5 (21.7)117 (47.8)0.02
 Iodine18 (78.3)128 (52.2)
Preop antibiotics given
 Yes18 (78.3)219 (89.4)0.16
 Never4 (17.4)16 (6.5)
 After skin incision1 (4.4)10 (4.1)
Antibiotics given
 ≥30 mins prior to incision6 (26.1)111 (45.3)0.08
 ≥20 mins prior to incision7 (30.4)148 (60.4)0.007
Postop antibiotics given
 Yes19 (82.6)223 (91)0.26

Values are presented as the number (%) of procedures with and without associated shunt infections. Boldface type indicates statistical significance.

Before May 23, 2013.

On or after May 23, 2013.

TABLE 6.

Perfect compliance rates for each protocol item

Protocol ItemPerfect Compliance Rate (n = 110)
1) Sign on OR door to minimize traffic89 (80.9)
2) Preop antibiotics ≥30 mins prior to skin incision93 (84.5)
3) Chloraprep applied to surgical field & not washed off109 (99.1)
4) Allowed Chloraprep to sit for at least 3 mins97 (88.2)
5) Hand scrubbed w/ Betadine or chlorhexidine96 (87.3)
6) Double glove used91 (82.7)
7) Ioban drape used97 (88.2)
8) Maintained normothermia throughout op95 (86.4)
9) Postop antibiotics given (at least 1 dose)106 (96.4)
All 9 steps of protocol followed77 (70%)

OR = operating room.

Values are presented as the number (%) of cases that have perfect compliance with the CSP.

Multivariable Analysis

The multivariable model showed that the implementation of the CSP was independently predictive of reducing shunt infection (adjusted OR 0.19 [95% CI 0.06–0.67], p = 0.009). The model accuracy (c-statistic) was 0.65. Backward and forward logistic regression analyses were also performed and yielded the same result as the stepwise analysis, suggesting robustness of the model. Age at surgery, hydrocephalus etiology, procedure type, ventricular catheter type, type of skin preparation, and waiting at least 30 minutes between preoperative antibiotics and skin incision were not found to be independently associated with shunt infection in our sample.

Discussion

Since the publication of the HCRN’s multicenter study demonstrating that the implementation of an 11-step protocol significantly reduced shunt infections, the generalizability of this success to smaller non-HCRN centers has been questioned.14,21 Our study, using a closely adapted HCRN shunt protocol, validated the HCRN’s results at a non-HCRN, small- to medium-volume pediatric neurosurgery center by reducing CSF shunt infection rates by 10%. In addition, waiting at least 20 minutes after preoperative antibiotic administration before skin incision and using chlorhexidine-containing preparation solution compared to iodine-based solution significantly reduced shunt infections on univariate analysis. However, only the implementation of the overall CSP was independently predictive of reducing shunt infections.

Our findings are consistent with, and extend those of, previous studies. Given the significant morbidity shunt infection imposes on patients, numerous standardized protocols have been developed to reduce shunt infection rates in children.2,6,13,14,20,22,24 In 1992 Choux et al.2 published the first shunt protocol involving standardization of both perioperative and postoperative steps, such as the mandatory use of skin preparation (with iodine- or chlorhexidine-based solution), limiting length of the operation to between 20 and 40 minutes, and opening of sterile packaging at the last moment. The authors were able to show a significant reduction in infection from 7.75% to 0.17% after implementation of the protocol. Pirotte et al.20 also showed that applying a strict protocol, including minimal implant and skin-edge manipulation, minimal staff in the operating room, using systemic antibiotics prophylaxis for 24 hours, and double gloving of surgeons, resulted in no shunt infections after 115 procedures. These studies demonstrate that the act of implementing a protocol will have a positive impact on reducing shunt infection rates, irrespective of the components within the protocol. Similarly, our study showed that only the implementation of the CSP was independently associated with improvement in shunt infection rates. The magnitude of the reduction in shunt infection (10% absolute risk reduction) was large compared to the HCRN protocol of 3.2% but is still comparable to what has been described in the literature.2,6,13,14,20,22 The compliance rate to the CSP was 70% and 74% for perfect and near-perfect compliance, respectively, which is also comparable to 74% and 95% rates reported by the HCRN and to other literature.13,14,20

Interestingly, barium-impregnated ventricular catheters had a protective effect against shunt infections in the univariate analysis, which has not been previously reported. In contrast, Bioglide ventricular catheters were associated with higher rates of infection. This is consistent with the study by Kestle et al.,14 which demonstrated a twofold increase in infection odds when Bioglide catheters were used (p = 0.002). This result strongly discouraged Bioglide catheter use at our institution and resulted in the eventual removal of this catheter type from our hospital inventory in the postprotocol era. Similar to previous studies, our study did not find that age, sex, etiology, type of procedure, and type of shunt used were associated with shunt infection rates.14 Furthermore, the administration of preoperative antibiotics before skin incision was not independently associated with a reduction in shunt infection. Contrarily, a recent meta-analysis by Xu et al.28 showed that administrating prophylactic antibiotic was able to reduce shunt infections (relative risk 0.59 [95% CI 0.38–0.90], p = 0.02) compared to placebo. The difference in our study was likely due to the relative small sample size represented by the group of patients who did not receive antibiotics, leading to an insufficient power to detect an association.

Chlorhexidine-containing skin preparation solution has been shown to be superior to iodine-based solutions in reducing surgical site infection in a myriad of surgical disciplines.4 Previous studies could not evaluate the impact of preoperative skin preparation solution on shunt infection due to the lack of variability in skin preparation solution used in the HCRN centers. However, iodine-based skin preparation solution has been historically used at ACH due to the theoretical neurotoxic risk of chlorhexidine in direct contact with neural tissues or meninges.8,9,25 Since the implementation of the CSP, there has been a shift to using chlorhexidine-based skin preparation solutions for shunt procedures. This study shows for the first-time that chlorhexidine-containing skin preparation solution was able to reduce shunt infections (OR 0.30 [95% CI 0.11–0.85], p = 0.02) on univariate analysis. Both chlorhexidine and iodine possess broad-spectrum antimicrobial activity;19 however, the superior clinical protection provided by chlorhexidine is probably related to its more rapid action, persistent activity despite exposure to bodily fluids, and residual bactericidal effect.4 Even though the use of flammable alcohol-based product poses the risk of chemical or fire skin burn, the HCRN protocol and the CSP require surgeons to wait at least 3 minutes to allow the chlorhexidine skin preparation solution to dry, which may reduce this risk. Based on the findings in this study, chlorhexidine-containing skin preparation solutions should be strongly considered for all shunt procedures in children.

The administration of preoperative antibiotics has been extensively studied and has been shown to reduce postoperative surgical site infections.3 Additionally, the WHO surgical safety checklist7 requires prophylactic antibiotics to be given within 60 minutes of skin incision. During the development of the CSP, it was hypothesized that the time between preoperative antibiotic administration and skin incision had an impact on shunt infection rates. The most effective preoperative antibiotics for shunt surgeries remains controversial due to a paucity of studies on this subject, but the most common antibiotic given in neurosurgery remains to be intravenous cefazolin.1 Since peak plasma concentration of intravenous cefazolin is estimated to take approximately 30 minutes,18 the CSP required preoperative antibiotics to be given at least 30 minutes before skin incision. On univariate analysis, there was no significant difference in infection rates from the a priori determined 30-minute cutoff (OR 0.43 [95% CI 0.16–1.12], p = 0.08). However, exploratory analysis revealed that the 20-minute cutoff was significant (OR 0.29 [95% CI 0.11–0.72], p = 0.007). Furthermore, waiting longer between preoperative antibiotic administration and skin incision (11.5 minutes in the infection group vs 29 minutes in the no-infection group) may have contributed to an improvement in shunt infections. This is the first study to allude to a possible association between the timing of preoperative antibiotics and skin incision. However, given this signal was detected during exploratory analysis, future studies should attempt to reproduce these results.

A major strength of this study was the prospective nature in which compliance to the CSP and shunt infection rates was recorded in the postimplementation cohort. This forward directionality provides the ability to clarify the timing of exposure in relation to disease and is therefore more capable of identifying casual effects compared to other study designs. Since ACH is the only center in Southern Alberta capable of managing pediatric shunts, there was negligible selection bias secondary to patient attrition. Furthermore, since ACH was a non-HCRN center at the time of study, the results may be generalizable to other small- to medium-volume non-HCRN pediatric centers. However, the findings should be interpreted in the context of the study design. Because the control cohort used in this study was collected in a retrospective manner, a few steps within the CSP were not collected and individually analyzed (e.g., whether the team double gloved and waited 3 minutes after skin preparation before skin incision). This prevented the comparison of the impact of many CSP steps on shunt infection rates. As in any nonrandomized controlled study, important unidentified or uncollected confounding variables may have biased the findings. Furthermore, the outcome of interest in this study was rare (23 shunt infections), leading to a lack of precision in the effect estimates and power in the regression analysis.

Conclusions

This study showed that a small- to medium-volume non-HCRN center using a closely adapted HCRN shunt protocol was able to significantly reduce shunt infections from 12.7% to 2.7% with a perfect compliance rate of 70%. The implementation of the shunt protocol was the only variable that independently predicted a reduction in shunt infection. However, the use of chlorhexidine-based skin preparation and waiting for at least 20 minutes between preoperative antibiotic administration and skin incision may have contributed to the protocol’s quality improvement success.

Acknowledgments

M.M.Y. was supported by the Clinical Investigator Program, University of Calgary and the Canadian Institute of Health Research. This project was supported by the Alberta Children’s Hospital Research Institute Trainee Small Research Grant, University of Calgary.

We would like to thank Salim Ahmed and Cara McDiarmid for their assistance in providing administrative support to this project.

Disclosures

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

Author Contributions

Conception and design: Riva-Cambrin, Yang, Hader, Bullivant. Acquisition of data: Yang, Hader, Bullivant. Analysis and interpretation of data: Riva-Cambrin, Yang, Hader, Brindle. Drafting the article: Riva-Cambrin, Yang. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Riva-Cambrin. Statistical analysis: Riva-Cambrin, Yang. Administrative/technical/material support: Brindle. Study supervision: Riva-Cambrin.

References

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    Brown EM: Antimicrobial prophylaxis in neurosurgery. J Antimicrob Chemother 31 (Suppl B):4963, 1993

  • 2

    Choux M, Genitori L, Lang D, Lena G: Shunt implantation: reducing the incidence of shunt infection. J Neurosurg 77:875880, 1992

  • 3

    Classen DC, Evans RS, Pestotnik SL, Horn SD, Menlove RL, Burke JP: The timing of prophylactic administration of antibiotics and the risk of surgical-wound infection. N Engl J Med 326:281286, 1992

    • Crossref
    • PubMed
    • Search Google Scholar
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  • 4

    Darouiche RO, Wall MJ Jr, Itani KM, Otterson MF, Webb AL, Carrick MM, et al.: Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. N Engl J Med 362:1826, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Douglas A, Udy AA, Wallis SC, Jarrett P, Stuart J, Lassig-Smith M, et al.: Plasma and tissue pharmacokinetics of cefazolin in patients undergoing elective and semielective abdominal aortic aneurysm open repair surgery. Antimicrob Agents Chemother 55:52385242, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Faillace WJ: A no-touch technique protocol to diminish cerebrospinal fluid shunt infection. Surg Neurol 43:344350, 1995

  • 7

    Haynes AB, Weiser TG, Berry WR, Lipsitz SR, Breizat AH, Dellinger EP, et al.: A surgical safety checklist to reduce morbidity and mortality in a global population. N Engl J Med 360:491499, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Henschen A, Olson L: Chlorhexidine-induced degeneration of adrenergic nerves. Acta Neuropathol 63:1823, 1984

  • 9

    Hurst EW: Adhesive arachnoiditis and vascular blockage caused by detergents and other chemical irritants: an experimental study. J Pathol Bacteriol 70:167178, 1955

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kestle J, Drake J, Milner R, Sainte-Rose C, Cinalli G, Boop F, et al.: Long-term follow-up data from the Shunt Design Trial. Pediatr Neurosurg 33:230236, 2000

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    Kestle JR, Drake JM, Cochrane DD, Milner R, Walker ML, Abbott R III, et al.: Lack of benefit of endoscopic ventriculoperitoneal shunt insertion: a multicenter randomized trial. J Neurosurg 98:284290, 2003

    • Crossref
    • PubMed
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    • Export Citation
  • 12

    Kestle JR, Garton HJ, Whitehead WE, Drake JM, Kulkarni AV, Cochrane DD, et al.: Management of shunt infections: a multicenter pilot study. J Neurosurg 105 (3 Suppl):177181, 2006

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Kestle JR, Holubkov R, Douglas Cochrane D, Kulkarni AV, Limbrick DD Jr, Luerssen TG, et al.: A new Hydrocephalus Clinical Research Network protocol to reduce cerebrospinal fluid shunt infection. J Neurosurg Pediatr 17:391396, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Kestle JR, Riva-Cambrin J, Wellons JC III, Kulkarni AV, Whitehead WE, Walker ML, et al.: A standardized protocol to reduce cerebrospinal fluid shunt infection: the Hydrocephalus Clinical Research Network Quality Improvement Initiative. J Neurosurg Pediatr 8:2229, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Kulkarni AV, Rabin D, Lamberti-Pasculli M, Drake JM: Repeat cerebrospinal fluid shunt infection in children. Pediatr Neurosurg 35:6671, 2001

  • 16

    Kurz A, Sessler DI, Lenhardt R: Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. N Engl J Med 334:12091215, 1996

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Leaper DJ, Edmiston CE: World Health Organization: global guidelines for the prevention of surgical site infection. J Hosp Infect 95:135136, 2017

  • 18

    Lee FH, Pfeffer M, Van Harken DR, Smyth RD, Hottendorf GH: Comparative pharmacokinetics of ceforanide (BL-S786R) and cefazolin in laboratory animals and humans. Antimicrob Agents Chemother 17:188192, 1980

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR: Guideline for prevention of surgical site infection, 1999. Infect Control Hosp Epidemiol 20:250280, 1999

  • 20

    Pirotte BJ, Lubansu A, Bruneau M, Loqa C, Van Cutsem N, Brotchi J: Sterile surgical technique for shunt placement reduces the shunt infection rate in children: preliminary analysis of a prospective protocol in 115 consecutive procedures. Childs Nerv Syst 23:12511261, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Riva-Cambrin J, Kestle JR, Holubkov R, Butler J, Kulkarni AV, Drake J, et al.: Risk factors for shunt malfunction in pediatric hydrocephalus: a multicenter prospective cohort study. J Neurosurg Pediatr 17:382390, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Rotim K, Miklic P, Paladino J, Melada A, Marcikic M, Scap M: Reducing the incidence of infection in pediatric cerebrospinal fluid shunt operations. Childs Nerv Syst 13:584587, 1997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Simon TD, Riva-Cambrin J, Srivastava R, Bratton SL, Dean JM, Kestle JR: Hospital care for children with hydrocephalus in the United States: utilization, charges, comorbidities, and deaths. J Neurosurg Pediatr 1:131137, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Spader HS, Hertzler DA, Kestle JR, Riva-Cambrin J: Risk factors for infection and the effect of an institutional shunt protocol on the incidence of ventricular access device infections in preterm infants. J Neurosurg Pediatr 15:156160, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Sviggum HP, Jacob AK, Arendt KW, Mauermann ML, Horlocker TT, Hebl JR: Neurologic complications after chlorhexidine antisepsis for spinal anesthesia. Reg Anesth Pain Med 37:139144, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Todd MM, Hindman BJ, Clarke WR, Torner JC: Mild intraoperative hypothermia during surgery for intracranial aneurysm. N Engl J Med 352:135145, 2005

  • 27

    Vinchon M, Dhellemmes P: Cerebrospinal fluid shunt infection: risk factors and long-term follow-up. Childs Nerv Syst 22:692697, 2006

  • 28

    Xu H, Hu F, Hu H, Sun W, Jiao W, Li R, et al.: Antibiotic prophylaxis for shunt surgery of children: a systematic review. Childs Nerv Syst 32:253258, 2016

  • Collapse
  • Expand
  • Calgary Shunt Protocol. The CSP was adapted from the 2011 Kestle et al. HCRN protocol. OR = operating room.

  • Line graph comparing shunt infection rates before and after protocol implementation. The pre- and postimplementation infection rates were 12.7% (red line) and 2.7% (green line), respectively (p = 0.004). ARR = absolute risk reduction. Figure is available in color online only.

  • 1

    Brown EM: Antimicrobial prophylaxis in neurosurgery. J Antimicrob Chemother 31 (Suppl B):4963, 1993

  • 2

    Choux M, Genitori L, Lang D, Lena G: Shunt implantation: reducing the incidence of shunt infection. J Neurosurg 77:875880, 1992

  • 3

    Classen DC, Evans RS, Pestotnik SL, Horn SD, Menlove RL, Burke JP: The timing of prophylactic administration of antibiotics and the risk of surgical-wound infection. N Engl J Med 326:281286, 1992

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Darouiche RO, Wall MJ Jr, Itani KM, Otterson MF, Webb AL, Carrick MM, et al.: Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. N Engl J Med 362:1826, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Douglas A, Udy AA, Wallis SC, Jarrett P, Stuart J, Lassig-Smith M, et al.: Plasma and tissue pharmacokinetics of cefazolin in patients undergoing elective and semielective abdominal aortic aneurysm open repair surgery. Antimicrob Agents Chemother 55:52385242, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Faillace WJ: A no-touch technique protocol to diminish cerebrospinal fluid shunt infection. Surg Neurol 43:344350, 1995

  • 7

    Haynes AB, Weiser TG, Berry WR, Lipsitz SR, Breizat AH, Dellinger EP, et al.: A surgical safety checklist to reduce morbidity and mortality in a global population. N Engl J Med 360:491499, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Henschen A, Olson L: Chlorhexidine-induced degeneration of adrenergic nerves. Acta Neuropathol 63:1823, 1984

  • 9

    Hurst EW: Adhesive arachnoiditis and vascular blockage caused by detergents and other chemical irritants: an experimental study. J Pathol Bacteriol 70:167178, 1955

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kestle J, Drake J, Milner R, Sainte-Rose C, Cinalli G, Boop F, et al.: Long-term follow-up data from the Shunt Design Trial. Pediatr Neurosurg 33:230236, 2000

  • 11

    Kestle JR, Drake JM, Cochrane DD, Milner R, Walker ML, Abbott R III, et al.: Lack of benefit of endoscopic ventriculoperitoneal shunt insertion: a multicenter randomized trial. J Neurosurg 98:284290, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Kestle JR, Garton HJ, Whitehead WE, Drake JM, Kulkarni AV, Cochrane DD, et al.: Management of shunt infections: a multicenter pilot study. J Neurosurg 105 (3 Suppl):177181, 2006

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Kestle JR, Holubkov R, Douglas Cochrane D, Kulkarni AV, Limbrick DD Jr, Luerssen TG, et al.: A new Hydrocephalus Clinical Research Network protocol to reduce cerebrospinal fluid shunt infection. J Neurosurg Pediatr 17:391396, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Kestle JR, Riva-Cambrin J, Wellons JC III, Kulkarni AV, Whitehead WE, Walker ML, et al.: A standardized protocol to reduce cerebrospinal fluid shunt infection: the Hydrocephalus Clinical Research Network Quality Improvement Initiative. J Neurosurg Pediatr 8:2229, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Kulkarni AV, Rabin D, Lamberti-Pasculli M, Drake JM: Repeat cerebrospinal fluid shunt infection in children. Pediatr Neurosurg 35:6671, 2001

  • 16

    Kurz A, Sessler DI, Lenhardt R: Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. N Engl J Med 334:12091215, 1996

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Leaper DJ, Edmiston CE: World Health Organization: global guidelines for the prevention of surgical site infection. J Hosp Infect 95:135136, 2017

  • 18

    Lee FH, Pfeffer M, Van Harken DR, Smyth RD, Hottendorf GH: Comparative pharmacokinetics of ceforanide (BL-S786R) and cefazolin in laboratory animals and humans. Antimicrob Agents Chemother 17:188192, 1980

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR: Guideline for prevention of surgical site infection, 1999. Infect Control Hosp Epidemiol 20:250280, 1999

  • 20

    Pirotte BJ, Lubansu A, Bruneau M, Loqa C, Van Cutsem N, Brotchi J: Sterile surgical technique for shunt placement reduces the shunt infection rate in children: preliminary analysis of a prospective protocol in 115 consecutive procedures. Childs Nerv Syst 23:12511261, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Riva-Cambrin J, Kestle JR, Holubkov R, Butler J, Kulkarni AV, Drake J, et al.: Risk factors for shunt malfunction in pediatric hydrocephalus: a multicenter prospective cohort study. J Neurosurg Pediatr 17:382390, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Rotim K, Miklic P, Paladino J, Melada A, Marcikic M, Scap M: Reducing the incidence of infection in pediatric cerebrospinal fluid shunt operations. Childs Nerv Syst 13:584587, 1997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Simon TD, Riva-Cambrin J, Srivastava R, Bratton SL, Dean JM, Kestle JR: Hospital care for children with hydrocephalus in the United States: utilization, charges, comorbidities, and deaths. J Neurosurg Pediatr 1:131137, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Spader HS, Hertzler DA, Kestle JR, Riva-Cambrin J: Risk factors for infection and the effect of an institutional shunt protocol on the incidence of ventricular access device infections in preterm infants. J Neurosurg Pediatr 15:156160, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Sviggum HP, Jacob AK, Arendt KW, Mauermann ML, Horlocker TT, Hebl JR: Neurologic complications after chlorhexidine antisepsis for spinal anesthesia. Reg Anesth Pain Med 37:139144, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Todd MM, Hindman BJ, Clarke WR, Torner JC: Mild intraoperative hypothermia during surgery for intracranial aneurysm. N Engl J Med 352:135145, 2005

  • 27

    Vinchon M, Dhellemmes P: Cerebrospinal fluid shunt infection: risk factors and long-term follow-up. Childs Nerv Syst 22:692697, 2006

  • 28

    Xu H, Hu F, Hu H, Sun W, Jiao W, Li R, et al.: Antibiotic prophylaxis for shunt surgery of children: a systematic review. Childs Nerv Syst 32:253258, 2016

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