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Publication Record


Inflammation-dependent cerebrospinal fluid hypersecretion by the choroid plexus epithelium in posthemorrhagic hydrocephalus.
Karimy JK, Zhang J, Kurland DB, Theriault BC, Duran D, Stokum JA, Furey CG, Zhou X, Mansuri MS, Montejo J, Vera A, DiLuna ML, Delpire E, Alper SL, Gunel M, Gerzanich V, Medzhitov R, Simard JM, Kahle KT
(2017) Nat Med 23: 997-1003
MeSH Terms: Acetazolamide, Animals, Antioxidants, Blotting, Western, Bumetanide, Cerebral Hemorrhage, Cerebral Ventricles, Cerebrospinal Fluid, Choroid Plexus, Diuretics, Gene Knockdown Techniques, Gene Knockout Techniques, Hydrocephalus, Immunoblotting, Immunohistochemistry, Immunoprecipitation, Inflammation, NF-kappa B, Proline, Protein-Serine-Threonine Kinases, Rats, Rats, Wistar, Salicylanilides, Solute Carrier Family 12, Member 2, Sulfonamides, Thiocarbamates, Toll-Like Receptor 4
Show Abstract · Added April 3, 2018
The choroid plexus epithelium (CPE) secretes higher volumes of fluid (cerebrospinal fluid, CSF) than any other epithelium and simultaneously functions as the blood-CSF barrier to gate immune cell entry into the central nervous system. Posthemorrhagic hydrocephalus (PHH), an expansion of the cerebral ventricles due to CSF accumulation following intraventricular hemorrhage (IVH), is a common disease usually treated by suboptimal CSF shunting techniques. PHH is classically attributed to primary impairments in CSF reabsorption, but little experimental evidence supports this concept. In contrast, the potential contribution of CSF secretion to PHH has received little attention. In a rat model of PHH, we demonstrate that IVH causes a Toll-like receptor 4 (TLR4)- and NF-κB-dependent inflammatory response in the CPE that is associated with a ∼3-fold increase in bumetanide-sensitive CSF secretion. IVH-induced hypersecretion of CSF is mediated by TLR4-dependent activation of the Ste20-type stress kinase SPAK, which binds, phosphorylates, and stimulates the NKCC1 co-transporter at the CPE apical membrane. Genetic depletion of TLR4 or SPAK normalizes hyperactive CSF secretion rates and reduces PHH symptoms, as does treatment with drugs that antagonize TLR4-NF-κB signaling or the SPAK-NKCC1 co-transporter complex. These data uncover a previously unrecognized contribution of CSF hypersecretion to the pathogenesis of PHH, demonstrate a new role for TLRs in regulation of the internal brain milieu, and identify a kinase-regulated mechanism of CSF secretion that could be targeted by repurposed US Food and Drug Administration (FDA)-approved drugs to treat hydrocephalus.
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MeSH Terms
Glycan engagement dictates hydrocephalus induction by serotype 1 reovirus.
Stencel-Baerenwald J, Reiss K, Blaum BS, Colvin D, Li XN, Abel T, Boyd K, Stehle T, Dermody TS
(2015) MBio 6: e02356
MeSH Terms: Animals, Animals, Newborn, Cells, Cultured, Disease Models, Animal, G(M2) Ganglioside, Hydrocephalus, Mice, Receptors, Virus, Reoviridae, Reoviridae Infections, Serogroup, Virus Attachment
Show Abstract · Added February 4, 2016
UNLABELLED - Receptors expressed on the host cell surface adhere viruses to target cells and serve as determinants of viral tropism. Several viruses bind cell surface glycans to facilitate entry, but the contribution of specific glycan moieties to viral disease is incompletely understood. Reovirus provides a tractable experimental model for studies of viral neuropathogenesis. In newborn mice, serotype 1 (T1) reovirus causes hydrocephalus, whereas serotype 3 (T3) reovirus causes encephalitis. T1 and T3 reoviruses engage distinct glycans, suggesting that glycan-binding capacity contributes to these differences in pathogenesis. Using structure-guided mutagenesis, we engineered a mutant T1 reovirus incapable of binding the T1 reovirus-specific glycan receptor, GM2. The mutant virus induced substantially less hydrocephalus than wild-type virus, an effect phenocopied by wild-type virus infection of GM2-deficient mice. In comparison to wild-type virus, yields of mutant virus were diminished in cultured ependymal cells, the cell type that lines the brain ventricles. These findings suggest that GM2 engagement targets reovirus to ependymal cells in mice and illuminate the function of glycan engagement in reovirus serotype-dependent disease.
IMPORTANCE - Receptor utilization strongly influences viral disease, often dictating host range and target cell selection. Different reovirus serotypes bind to different glycans, but a precise function for these molecules in pathogenesis is unknown. We used type 1 (T1) reovirus deficient in binding the GM2 glycan and mice lacking GM2 to pinpoint a role for glycan engagement in hydrocephalus caused by T1 reovirus. This work indicates that engagement of a specific glycan can lead to infection of specific cells in the host and consequent disease at that site. Since reovirus is being developed as a vaccine vector and oncolytic agent, understanding reovirus-glycan interactions may allow manipulation of reovirus glycan-binding properties for therapeutic applications.
Copyright © 2015 Stencel-Baerenwald et al.
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12 MeSH Terms
Cole-Carpenter syndrome is caused by a heterozygous missense mutation in P4HB.
Rauch F, Fahiminiya S, Majewski J, Carrot-Zhang J, Boudko S, Glorieux F, Mort JS, Bächinger HP, Moffatt P
(2015) Am J Hum Genet 96: 425-31
MeSH Terms: Child, Preschool, Craniosynostoses, Eye Abnormalities, Female, Gene Frequency, Heterozygote, Humans, Hydrocephalus, Infant, Male, Mutation, Missense, Osteogenesis Imperfecta, Pedigree, Procollagen-Proline Dioxygenase, Protein Conformation, Protein Disulfide-Isomerases, Protein Folding, Sequence Analysis, DNA
Show Abstract · Added November 2, 2017
Cole-Carpenter syndrome is a severe bone fragility disorder that is characterized by frequent fractures, craniosynostosis, ocular proptosis, hydrocephalus, and distinctive facial features. To identify the cause of Cole-Carpenter syndrome in the two individuals whose clinical results were presented in the original description of this disorder, we performed whole-exome sequencing of genomic DNA samples from both individuals. The two unrelated individuals had the same heterozygous missense mutation in exon 9 of P4HB (NM_000918.3: c.1178A>G [p.Tyr393Cys]), the gene that encodes protein disulfide isomerase (PDI). In one individual, the P4HB mutation had arisen de novo, whereas in the other the mutation was transmitted from the clinically unaffected father who was a mosaic carrier of the variant. The mutation was located in the C-terminal disulfide isomerase domain of PDI, sterically close to the enzymatic center, and affected disulfide isomerase activity in vitro. Skin fibroblasts showed signs of increased endoplasmic reticulum stress, but despite the reported importance of PDI for collagen type I production, the rate of collagen type I secretion appeared normal. In conclusion, Cole-Carpenter syndrome is caused by a specific de novo mutation in P4HB that impairs the disulfide isomerase activity of PDI.
Copyright © 2015 The American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.
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18 MeSH Terms
Pediatric posterior reversible encephalopathy syndrome presenting with isolated cerebellar edema and obstructive hydrocephalus.
Ettinger N, Pearson M, Lamb FS, Wellons JC
(2014) J Neurosurg Pediatr 14: 344-7
MeSH Terms: Adolescent, Antihypertensive Agents, Brain Edema, Cerebellum, Drainage, Fourth Ventricle, Humans, Hydrocephalus, Hypertension, Hypertrophy, Left Ventricular, Magnetic Resonance Imaging, Male, Posterior Leukoencephalopathy Syndrome, Tomography, X-Ray Computed
Show Abstract · Added February 22, 2016
In this report, the authors describe the case of a teenage boy who presented with hypertensive emergency, posterior reversible encephalopathy syndrome, and hydrocephalus due to fourth ventricle outlet obstruction. Posterior reversible encephalopathy syndrome is a well-characterized but uncommon syndrome in children that is generally triggered by severe hypertension. The unusual clinical picture of this patient, who had isolated cerebellar edema leading to obstructive hydrocephalus, has been rarely described in children.
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14 MeSH Terms
DIPA-family coiled-coils bind conserved isoform-specific head domain of p120-catenin family: potential roles in hydrocephalus and heterotopia.
Markham NO, Doll CA, Dohn MR, Miller RK, Yu H, Coffey RJ, McCrea PD, Gamse JT, Reynolds AB
(2014) Mol Biol Cell 25: 2592-603
MeSH Terms: Adherens Junctions, Amino Acid Sequence, Animals, Cadherins, Catenins, Cell Line, Tumor, Conserved Sequence, Dogs, Gene Knockdown Techniques, HEK293 Cells, Humans, Hydrocephalus, Madin Darby Canine Kidney Cells, Molecular Sequence Data, Neural Tube Defects, Protein Isoforms, Protein Structure, Tertiary, Sequence Alignment, Zebrafish
Show Abstract · Added February 19, 2015
p120-catenin (p120) modulates adherens junction (AJ) dynamics by controlling the stability of classical cadherins. Among all p120 isoforms, p120-3A and p120-1A are the most prevalent. Both stabilize cadherins, but p120-3A is preferred in epithelia, whereas p120-1A takes precedence in neurons, fibroblasts, and macrophages. During epithelial-to-mesenchymal transition, E- to N-cadherin switching coincides with p120-3A to -1A alternative splicing. These isoforms differ by a 101-amino acid "head domain" comprising the p120-1A N-terminus. Although its exact role is unknown, the head domain likely mediates developmental and cancer-associated events linked to p120-1A expression (e.g., motility, invasion, metastasis). Here we identified delta-interacting protein A (DIPA) as the first head domain-specific binding partner and candidate mediator of isoform 1A activity. DIPA colocalizes with AJs in a p120-1A- but not 3A-dependent manner. Moreover, all DIPA family members (Ccdc85a, Ccdc85b/DIPA, and Ccdc85c) interact reciprocally with p120 family members (p120, δ-catenin, p0071, and ARVCF), suggesting significant functional overlap. During zebrafish neural tube development, both knockdown and overexpression of DIPA phenocopy N-cadherin mutations, an effect bearing functional ties to a reported mouse hydrocephalus phenotype associated with Ccdc85c. These studies identify a novel, highly conserved interaction between two protein families that may participate either individually or collectively in N-cadherin-mediated development.
© 2014 Markham et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0).
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No significant improvement in the rate of accurate ventricular catheter location using ultrasound-guided CSF shunt insertion: a prospective, controlled study by the Hydrocephalus Clinical Research Network.
Whitehead WE, Riva-Cambrin J, Wellons JC, Kulkarni AV, Holubkov R, Illner A, Oakes WJ, Luerssen TG, Walker ML, Drake JM, Kestle JR, Hydrocephalus Clinical Research Network
(2013) J Neurosurg Pediatr 12: 565-74
MeSH Terms: Adolescent, Child, Child, Preschool, Clinical Competence, Echoencephalography, Equipment Failure, Female, Foreign-Body Migration, Humans, Hydrocephalus, Infant, Infant, Newborn, Kaplan-Meier Estimate, Male, Prospective Studies, Sample Size, Time Factors, Treatment Outcome, Ultrasonography, Interventional, Ventriculoperitoneal Shunt
Show Abstract · Added March 7, 2014
OBJECT - Cerebrospinal fluid shunt ventricular catheters inserted into the frontal horn or trigone are associated with prolonged shunt survival. Developing surgical techniques for accurate catheter insertion could, therefore, be beneficial to patients. This study was conducted to determine if the rate of accurate catheter location with intraoperative ultrasound guidance could exceed 80%.
METHODS - The authors conducted a prospective, multicenter study of children (< 18 years) requiring first-time treatment for hydrocephalus with a ventriculoperitoneal shunt. Using intraoperative ultrasound, surgeons were required to target the frontal horn or trigone for catheter tip placement. An intraoperative ultrasound image was obtained at the time of catheter insertion. Ventricular catheter location, the primary outcome measure, was determined from the first postoperative image. A control group of patients treated by nonultrasound surgeons (conventional surgeons) were enrolled using the same study criteria. Conventional shunt surgeons also agreed to target the frontal horn or trigone for all catheter insertions. Patients were triaged to participating surgeons based on call schedules at each center. A pediatric neuroradiologist blinded to method of insertion, center, and surgeon determined ventricular catheter tip location.
RESULTS - Eleven surgeons enrolled as ultrasound surgeons and 6 as conventional surgeons. Between February 2009 and February 2010, 121 patients were enrolled at 4 Hydrocephalus Clinical Research Network centers. Experienced ultrasound surgeons (> 15 cases prior to study) operated on 67 patients; conventional surgeons operated on 52 patients. Experienced ultrasound surgeons achieved accurate catheter location in 39 (59%) of 66 patients, 95% CI (46%-71%). Intraoperative ultrasound images were compared with postoperative scans. In 32.7% of cases, the catheter tip moved from an accurate location on the intraoperative ultrasound image to an inaccurate location on the postoperative study. This was the most significant factor affecting accuracy. In comparison, conventional surgeons achieved accurate location in 24 (49.0%) of 49 cases (95% CI [34%-64%]). The shunt survival rate at 1 year was 70.8% in the experienced ultrasound group and 66.9% in the conventional group (p = 0.66). Ultrasound surgeons had more catheters surrounded by CSF (30.8% vs 6.1%, p = 0.0012) and away from the choroid plexus (72.3% vs 58.3%, p = 0.12), and fewer catheters in the brain (3% vs 22.4%, p = 0.0011) and crossing the midline (4.5% vs 34.7%, p < 0.001), but they had a higher proportion of postoperative pseudomeningocele (10.1% vs 3.8%, p = 0.30), wound dehiscence (5.8% vs 0%, p = 0.13), CSF leak (10.1% vs 1.9%, p = 0.14), and shunt infection (11.6% vs 5.8%, p = 0.35).
CONCLUSIONS - Ultrasound-guided shunt insertion as performed in this study was unable to consistently place catheters into the frontal horn or trigone. The technique is safe and achieves outcomes similar to other conventional shunt insertion techniques. Further efforts to improve accurate catheter location should focus on prevention of catheter migration that occurs between intraoperative placement and postoperative imaging. Clinical trial registration no.: NCT01007786 ( ClinicalTrials.gov ).
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20 MeSH Terms
Outcomes of CSF shunting in children: comparison of Hydrocephalus Clinical Research Network cohort with historical controls: clinical article.
Kulkarni AV, Riva-Cambrin J, Butler J, Browd SR, Drake JM, Holubkov R, Kestle JR, Limbrick DD, Simon TD, Tamber MS, Wellons JC, Whitehead WE, Hydrocephalus Clinical Research Network
(2013) J Neurosurg Pediatr 12: 334-8
MeSH Terms: Adolescent, Cerebrospinal Fluid Shunts, Child, Child, Preschool, Clinical Trials as Topic, Cohort Studies, Equipment Failure, Female, Humans, Hydrocephalus, Infant, Kaplan-Meier Estimate, Male, Multicenter Studies as Topic, Neuroendoscopy, Prognosis, Proportional Hazards Models, Prospective Studies, Reoperation, Survival Analysis, Treatment Outcome
Show Abstract · Added March 7, 2014
OBJECT - The Hydrocephalus Clinical Research Network (HCRN), which comprises 7 pediatric neurosurgical centers in North America, provides a unique multicenter assessment of the current outcomes of CSF shunting in nonselected patients. The authors present the initial results for this cohort and compare them with results from prospective multicenter trials performed in the 1990s.
METHODS - Analysis was restricted to patients with newly diagnosed hydrocephalus undergoing shunting for the first time. Detailed perioperative data from 2008 through 2012 for all HCRN centers were prospectively collected and centrally stored by trained research coordinators. Historical control data were obtained from the Shunt Design Trial (1993-1995) and the Endoscopic Shunt Insertion Trial (1996-1999). The primary outcome was time to first shunt failure, which was determined by using Cox regression survival analysis.
RESULTS - Mean age of the 1184 patients in the HCRN cohort was older than mean age of the 720 patients in the historical cohort (2.51 years vs 1.60 years, p < 0.0001). The distribution of etiologies differed (p < 0.0001, chi-square test); more tumors and fewer myelomeningoceles caused the hydrocephalus in the HCRN cohort patients. The hazard ratio for first shunt failure significantly favored the HCRN cohort, even after the model was adjusted for the prognostic effects of age and etiology (adjusted HR 0.82, 95% CI 0.69-0.96).
CONCLUSIONS - Current outcomes of shunting in general pediatric neurosurgery practice have improved over those from the 1990s, although the reasons remain unclear.
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21 MeSH Terms
Validation and modification of a predictive model of postresection hydrocephalus in pediatric patients with posterior fossa tumors.
Foreman P, McClugage S, Naftel R, Griessenauer CJ, Ditty BJ, Agee BS, Riva-Cambrin J, Wellons J
(2013) J Neurosurg Pediatr 12: 220-6
MeSH Terms: Adolescent, Age Factors, Canada, Cerebrospinal Fluid Shunts, Child, Child, Preschool, Edema, Ependyma, Female, Humans, Hydrocephalus, Infant, Infratentorial Neoplasms, Male, Medical Records, Models, Statistical, Odds Ratio, Predictive Value of Tests, Retrospective Studies, Risk Assessment, Risk Factors, Severity of Illness Index, Treatment Outcome
Show Abstract · Added March 7, 2014
OBJECT - Postresection hydrocephalus is observed in approximately 30% of pediatric patients with posterior fossa tumors. However, which patients will develop postresection hydrocephalus is not known. The Canadian Preoperative Prediction Rule for Hydrocephalus (CPPRH) was developed in an attempt to identify this subset of patients, allowing for the optimization of their care. The authors sought to validate and critically appraise the CPPRH.
METHODS - The authors conducted a retrospective chart review of 99 consecutive pediatric patients who presented between 2002 and 2010 with posterior fossa tumors and who subsequently underwent resection. The data were then analyzed using bivariate and multivariate analyses, and a modified CPPRH (mCPPRH) was applied.
RESULTS - Seventy-six patients were evaluated. Four variables were found to be significant in predicting postresection hydrocephalus: age younger than 2 years, moderate/severe hydrocephalus, preoperative tumor diagnosis, and transependymal edema. The mCPPRH produced observed likelihood ratios of 0.737 (95% CI 0.526-1.032) and 4.688 (95% CI 1.421-15.463) for low- and high-risk groups, respectively.
CONCLUSIONS - The mCPPRH utilizes readily obtainable and reliable preoperative variables that together stratify children with posterior fossa tumors into high- and low-risk categories for the development of postresection hydrocephalus. This new predictive model will aid patient counseling and tailor the intensity of postoperative clinical and radiographic monitoring for hydrocephalus, as well as provide evidence-based guidance for the use of prophylactic CSF diversion.
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23 MeSH Terms
Long-term change in ventricular size following endoscopic third ventriculostomy for hydrocephalus due to tectal plate gliomas.
Romeo A, Naftel RP, Griessenauer CJ, Reed GT, Martin R, Shannon CN, Grabb PA, Tubbs RS, Wellons JC
(2013) J Neurosurg Pediatr 11: 20-5
MeSH Terms: Adolescent, Anesthesia, General, Brain Stem Neoplasms, Cerebral Ventricles, Child, Child, Preschool, Endoscopy, Female, Follow-Up Studies, Glioma, Humans, Hydrocephalus, Intracranial Hypertension, Male, Postoperative Complications, Radiography, Reoperation, Retrospective Studies, Treatment Failure, Treatment Outcome, Ventriculostomy
Show Abstract · Added March 20, 2014
OBJECT - Endoscopic third ventriculostomy (ETV) is an alternative to shunt placement in children with hydrocephalus due to tectal plate gliomas (TPGs). However, controversy remains regarding the amount of ventricular size reduction that should be expected after ETV. This study investigates ventricular size change after ETV for TPGs.
METHODS - Twenty-two children were identified from a 15-year retrospective database of neuroendoscopic procedures performed at the authors' institution, Children's Hospital of Alabama, in patients with a minimum of 1 year of follow-up. Clinical outcomes, including the need for further CSF diversion and symptom resolution, were recorded. The frontal and occipital horn ratio (FOR) was measured on pre- and postoperative, 1-year, and last follow-up imaging studies.
RESULTS - In 17 (77%) of 22 children no additional procedure for CSF diversion was required. Of those in whom CSF diversion failed, 4 underwent successful repeat ETV and 1 required shunt replacement. Therefore, in 21 (96%) of 22 patients, CSF diversion was accomplished with ETV. Preoperative and postoperative imaging was available for 18 (82%) of 22 patients. The FOR decreased in 89% of children who underwent ETV. The FOR progressively decreased 1.7%, 11.2%, and 12.7% on the initial postoperative, 1-year, and last follow-up images, respectively. The mean radiological follow-up duration for 18 patients was 5.4 years. When ETV failed, the FOR increased at the time of failure in all patients. Failure occurred 1.6 years after initial ETV on average. The mean clinical follow-up period for all 22 patients was 5.3 years. In all cases clinical improvement was demonstrated at the last follow-up.
CONCLUSIONS - Endoscopic third ventriculostomy successfully treated hydrocephalus in the extended follow-up period of patients with TPGs. The most significant reduction in ventricular size was observed at the the 1-year followup, with only modest reduction thereafter.
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Technology preferences among caregivers of children with hydrocephalus.
Naftel RP, Safiano NA, Falola MI, Shannon CN, Wellons JC, Johnston JM
(2013) J Neurosurg Pediatr 11: 26-36
MeSH Terms: Adult, Biomedical Technology, Caregivers, Child, Data Collection, Female, Health Care Surveys, Humans, Hydrocephalus, Information Seeking Behavior, Internet, Male, Patient Education as Topic, Patient Preference, Population, Prospective Studies, Self-Help Groups, Social Media, Socioeconomic Factors
Show Abstract · Added March 20, 2014
OBJECT - The Internet and social media are powerful disseminators of medical information, providing new portals for patient care. The authors of this study evaluated current technology hardware, Internet, and social media use and their socioeconomic relationships among caregivers of children with hydrocephalus.
METHODS - A written survey was completed in the neurosurgical clinics at the University of Alabama at Birmingham by 300 parents of children with shunted hydrocephalus between October 26, 2010, and July 26, 2011.
RESULTS - Computer use (94.6%), Internet use (91.7%), smartphone use (56.9%), and Internet research on hydrocephalus (81.9%) were prevalent. However, for each of these four utilizations there was significantly lower access by caregivers of minority races (p = 0.04, 0.03, 0.002, and < 0.0001, respectively), lower income (p = 0.02, 0.01, < 0.0001, and < 0.0001, respectively), and lower level of education (p = 0.001, 0.002, < 0.0001, and 0.001, respectively). Personal use of social media was prevalent (95.1% of all Internet users) with use being more prevalent among less-educated than higher-educated caregivers (p = 0.017). Hydrocephalus-related social media use (59.5% of Internet users) was not associated with socioeconomic factors. For hydrocephalus education on the Internet, caregivers chose information websites such as Wikipedia or the Hydrocephalus Association as preferred platforms; these preferences were followed by use of social media websites. Facebook and YouTube were the preferred social media platforms for personal and hydrocephalus-related use. Parents indicate moderate skepticism about the trustworthiness of the Internet; only 21.7% always trust the online sources. Most parents (89.8%) say that they would visit neurosurgeon-recommended websites. Of Internet-using caregivers, 28.6% use the Internet or social media to find hydrocephalus support groups, and 34.8% have used the Internet to communicate with other caregivers who have children with similar conditions.
CONCLUSIONS - Technology hardware, the Internet, and social media are widely used with some skepticism by parents of children with shunted hydrocephalus. Caregivers are interested in physician-recommended Internet resources. Socioeconomic factors including race, income, and level of education reveal a disparity in access to some of these resources, although all groups have relatively high use. Unlike typical technology use, social media use is breaking down the digital divide among ethnic and socioeconomic groups.
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