A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus

Abstract Background Implantation of ventricular catheters (VCs) to drain cerebrospinal fluid (CSF) is a standard approach to treat hydrocephalus. VCs fail frequently due to tissue obstructing the lumen via the drainage holes. Mechanisms driving obstruction are poorly understood. This study aimed to...

Full description

Bibliographic Details
Main Authors: Prashant Hariharan, Jeffrey Sondheimer, Alexandra Petroj, Jacob Gluski, Andrew Jea, William E. Whitehead, Sandeep Sood, Steven D. Ham, Brandon G. Rocque, Neena I. Marupudi, James P. McAllister, David Limbrick, Marc R. Del Bigio, Carolyn A. Harris
Format: Article
Language:English
Published: BMC 2021-07-01
Series:Fluids and Barriers of the CNS
Subjects:
Online Access:https://doi.org/10.1186/s12987-021-00262-3
_version_ 1818453831276560384
author Prashant Hariharan
Jeffrey Sondheimer
Alexandra Petroj
Jacob Gluski
Andrew Jea
William E. Whitehead
Sandeep Sood
Steven D. Ham
Brandon G. Rocque
Neena I. Marupudi
James P. McAllister
David Limbrick
Marc R. Del Bigio
Carolyn A. Harris
author_facet Prashant Hariharan
Jeffrey Sondheimer
Alexandra Petroj
Jacob Gluski
Andrew Jea
William E. Whitehead
Sandeep Sood
Steven D. Ham
Brandon G. Rocque
Neena I. Marupudi
James P. McAllister
David Limbrick
Marc R. Del Bigio
Carolyn A. Harris
author_sort Prashant Hariharan
collection DOAJ
description Abstract Background Implantation of ventricular catheters (VCs) to drain cerebrospinal fluid (CSF) is a standard approach to treat hydrocephalus. VCs fail frequently due to tissue obstructing the lumen via the drainage holes. Mechanisms driving obstruction are poorly understood. This study aimed to characterize the histological features of VC obstructions and identify links to clinical factors. Methods 343 VCs with relevant clinical data were collected from five centers. Each hole on the VCs was classified by degree of tissue obstruction after macroscopic analysis. A subgroup of 54 samples was analyzed using immunofluorescent labelling, histology and immunohistochemistry. Results 61.5% of the 343 VCs analyzed had tissue aggregates occluding at least one hole (n = 211) however the vast majority of the holes (70%) showed no tissue aggregates. Mean age at which patients with occluded VCs had their first surgeries (3.25 yrs) was lower than in patients with non-occluded VCs (5.29 yrs, p < 0.02). Mean length of time of implantation of occluded VCs, 33.22 months was greater than for non-occluded VCs, 23.8 months (p = 0.02). Patients with myelomeningocele had a greater probability of having an occluded VC (p = 0.0426). VCs with occlusions had greater numbers of macrophages and astrocytes in comparison to non-occluded VCs (p < 0.01). Microglia comprised only 2–6% of the VC-obstructing tissue aggregates. Histologic analysis showed choroid plexus occlusion in 24%, vascularized glial tissue occlusion in 24%, prevalent lymphocytic inflammation in 29%, and foreign body giant cell reactions in 5% and no ependyma. Conclusion Our data show that age of the first surgery and length of time a VC is implanted are factors that influence the degree of VC obstruction. The tissue aggregates obstructing VCs are composed predominantly of astrocytes and macrophages; microglia have a relatively small presence.
first_indexed 2024-12-14T21:45:14Z
format Article
id doaj.art-38e2917193ac4764999c8175445c5ce2
institution Directory Open Access Journal
issn 2045-8118
language English
last_indexed 2024-12-14T21:45:14Z
publishDate 2021-07-01
publisher BMC
record_format Article
series Fluids and Barriers of the CNS
spelling doaj.art-38e2917193ac4764999c8175445c5ce22022-12-21T22:46:22ZengBMCFluids and Barriers of the CNS2045-81182021-07-0118111210.1186/s12987-021-00262-3A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalusPrashant Hariharan0Jeffrey Sondheimer1Alexandra Petroj2Jacob Gluski3Andrew Jea4William E. Whitehead5Sandeep Sood6Steven D. Ham7Brandon G. Rocque8Neena I. Marupudi9James P. McAllister10David Limbrick11Marc R. Del Bigio12Carolyn A. Harris13Wayne State University Dept. of Biomedical EngineeringWayne State University Dept. of Chemical Engineering and Materials ScienceWayne State University Dept. of Chemical Engineering and Materials ScienceDept. of Neurosurgery, Wayne State University School of MedicineRiley Hospital for Children at IU HealthTexas Children’sDepartments of Neurosurgery and Pediatric Neurosurgery, Wayne State University School of Medicine and Children’s Hospital of MichiganDepartments of Neurosurgery and Pediatric Neurosurgery, Wayne State University School of Medicine and Children’s Hospital of MichiganDepartment of Neurosurgery, University of Alabama At BirminghamChildren’s Hospital of Michigan Dept. of NeurosurgerySchool of Medicine Dept. of Neurological Surgery, Washington UniversitySchool of Medicine Dept. of Neurological Surgery, Washington UniversityDepartment of Pathology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of ManitobaWayne State University Dept. of Chemical Engineering and Materials ScienceAbstract Background Implantation of ventricular catheters (VCs) to drain cerebrospinal fluid (CSF) is a standard approach to treat hydrocephalus. VCs fail frequently due to tissue obstructing the lumen via the drainage holes. Mechanisms driving obstruction are poorly understood. This study aimed to characterize the histological features of VC obstructions and identify links to clinical factors. Methods 343 VCs with relevant clinical data were collected from five centers. Each hole on the VCs was classified by degree of tissue obstruction after macroscopic analysis. A subgroup of 54 samples was analyzed using immunofluorescent labelling, histology and immunohistochemistry. Results 61.5% of the 343 VCs analyzed had tissue aggregates occluding at least one hole (n = 211) however the vast majority of the holes (70%) showed no tissue aggregates. Mean age at which patients with occluded VCs had their first surgeries (3.25 yrs) was lower than in patients with non-occluded VCs (5.29 yrs, p < 0.02). Mean length of time of implantation of occluded VCs, 33.22 months was greater than for non-occluded VCs, 23.8 months (p = 0.02). Patients with myelomeningocele had a greater probability of having an occluded VC (p = 0.0426). VCs with occlusions had greater numbers of macrophages and astrocytes in comparison to non-occluded VCs (p < 0.01). Microglia comprised only 2–6% of the VC-obstructing tissue aggregates. Histologic analysis showed choroid plexus occlusion in 24%, vascularized glial tissue occlusion in 24%, prevalent lymphocytic inflammation in 29%, and foreign body giant cell reactions in 5% and no ependyma. Conclusion Our data show that age of the first surgery and length of time a VC is implanted are factors that influence the degree of VC obstruction. The tissue aggregates obstructing VCs are composed predominantly of astrocytes and macrophages; microglia have a relatively small presence.https://doi.org/10.1186/s12987-021-00262-3HydrocephalusBiobankVentriculoperitoneal shuntShunt failureShunt obstructionRetrospective cohort
spellingShingle Prashant Hariharan
Jeffrey Sondheimer
Alexandra Petroj
Jacob Gluski
Andrew Jea
William E. Whitehead
Sandeep Sood
Steven D. Ham
Brandon G. Rocque
Neena I. Marupudi
James P. McAllister
David Limbrick
Marc R. Del Bigio
Carolyn A. Harris
A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
Fluids and Barriers of the CNS
Hydrocephalus
Biobank
Ventriculoperitoneal shunt
Shunt failure
Shunt obstruction
Retrospective cohort
title A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
title_full A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
title_fullStr A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
title_full_unstemmed A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
title_short A multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
title_sort multicenter retrospective study of heterogeneous tissue aggregates obstructing ventricular catheters explanted from patients with hydrocephalus
topic Hydrocephalus
Biobank
Ventriculoperitoneal shunt
Shunt failure
Shunt obstruction
Retrospective cohort
url https://doi.org/10.1186/s12987-021-00262-3
work_keys_str_mv AT prashanthariharan amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT jeffreysondheimer amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT alexandrapetroj amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT jacobgluski amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT andrewjea amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT williamewhitehead amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT sandeepsood amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT stevendham amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT brandongrocque amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT neenaimarupudi amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT jamespmcallister amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT davidlimbrick amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT marcrdelbigio amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT carolynaharris amulticenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT prashanthariharan multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT jeffreysondheimer multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT alexandrapetroj multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT jacobgluski multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT andrewjea multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT williamewhitehead multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT sandeepsood multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT stevendham multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT brandongrocque multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT neenaimarupudi multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT jamespmcallister multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT davidlimbrick multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT marcrdelbigio multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus
AT carolynaharris multicenterretrospectivestudyofheterogeneoustissueaggregatesobstructingventricularcathetersexplantedfrompatientswithhydrocephalus