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Published in: Acta Neurochirurgica 11/2023

29-08-2023 | Hydrocephalus | Review Article

CSF hypersecretion versus impaired CSF absorption in posthemorrhagic hydrocephalus: a systematic review

Authors: Shai David Ben-Shoshan, Sara Diana Lolansen, Tiit Illimar Mathiesen, Nanna MacAulay

Published in: Acta Neurochirurgica | Issue 11/2023

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Abstract

Background

The molecular mechanisms underlying development of posthemorrhagic hydrocephalus (PHH) remain elusive. The aim of this systematic review was to evaluate existing literature on increased CSF secretion and impaired CSF absorption as pathogenic contributors to CSF accumulation in neonatal and adult PHH.

Methods

The systematic review was conducted in accordance with the PRISMA guidelines. Relevant studies published before March 11th, 2023, were identified from PubMed and reference lists. Studies were screened for eligibility using predefined inclusion and exclusion criteria. Data from eligible studies were extracted and potential sources of bias were evaluated.

Results

Nineteen studies quantified CSF production rates and/or CSF absorption capacity in human patients with PHH or animals with experimentally induced PHH. Increased CSF production was reported as early as 24 h and as late as 28 days post ictus in six out of eight studies quantifying CSF production rates in animals with experimentally induced PHH. Impaired CSF absorption was reported in all four studies quantifying CSF absorption capacity in human patients with PHH and in seven out of nine studies quantifying CSF absorption capacity in animals with experimentally induced PHH. Impaired CSF absorption was reported as early as 30 min and as late as 10 months post ictus.

Conclusions

The pathological CSF accumulation in PHH likely arises from a combination of increased CSF secretion and impaired CSF absorption, which may manifest at different time scales following a hemorrhagic event. Emergent evidence on increased CSF secretion by the choroid plexus may herald a paradigm shift in our understanding of PHH.
Literature
12.
14.
go back to reference Chaudhry SR, Stoffel-Wagner B, Kinfe TM, Güresir E, Vatter H, Dietrich D, Lamprecht A, Muhammad S (2017) Elevated systemic IL-6 levels in patients with aneurysmal subarachnoid hemorrhage is an unspecific marker for post-SAH complications. Int J Mol Sci 18. https://doi.org/10.3390/ijms18122580 Chaudhry SR, Stoffel-Wagner B, Kinfe TM, Güresir E, Vatter H, Dietrich D, Lamprecht A, Muhammad S (2017) Elevated systemic IL-6 levels in patients with aneurysmal subarachnoid hemorrhage is an unspecific marker for post-SAH complications. Int J Mol Sci 18. https://​doi.​org/​10.​3390/​ijms18122580
28.
go back to reference Fejes Z, Pócsi M, Takai J, Erdei J, Tóth A, Balogh E, Rusznyák Á, Fenyvesi F, Nagy A, Kappelmayer J, Jeney V, Nagy B Jr (2021) Preterm intraventricular hemorrhage-induced inflammatory response in human choroid plexus epithelial cells. Int J Mol Sci 22:–8648. https://doi.org/10.3390/ijms22168648 Fejes Z, Pócsi M, Takai J, Erdei J, Tóth A, Balogh E, Rusznyák Á, Fenyvesi F, Nagy A, Kappelmayer J, Jeney V, Nagy B Jr (2021) Preterm intraventricular hemorrhage-induced inflammatory response in human choroid plexus epithelial cells. Int J Mol Sci 22:–8648. https://​doi.​org/​10.​3390/​ijms22168648
31.
go back to reference Giray S, Sen O, Sarica FB, Tufan K, Karatas M, Goksel BK, Yerdelen D, Cekinmez M, Can U (2009) Spontaneous primary intraventricular hemorrhage in adults: clinical data, etiology and outcome. Turk Neurosurg 19:338–344PubMed Giray S, Sen O, Sarica FB, Tufan K, Karatas M, Goksel BK, Yerdelen D, Cekinmez M, Can U (2009) Spontaneous primary intraventricular hemorrhage in adults: clinical data, etiology and outcome. Turk Neurosurg 19:338–344PubMed
37.
go back to reference Hill A, Shackelford GD, Volpe JJ (1984) A potential mechanism of pathogenesis for early posthemorrhagic hydrocephalus in the premature newborn. Pediatrics 73:19–21CrossRefPubMed Hill A, Shackelford GD, Volpe JJ (1984) A potential mechanism of pathogenesis for early posthemorrhagic hydrocephalus in the premature newborn. Pediatrics 73:19–21CrossRefPubMed
40.
go back to reference Hydrocephalus A (1841) or water in the head, an inflammatory disease, and curable equally and by the same means with other diseases of inflammation. Br Foreign Med Rev 11:151–158 Hydrocephalus A (1841) or water in the head, an inflammatory disease, and curable equally and by the same means with other diseases of inflammation. Br Foreign Med Rev 11:151–158
46.
go back to reference 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) Inflammation-dependent cerebrospinal fluid hypersecretion by the choroid plexus epithelium in posthemorrhagic hydrocephalus. Nat Med 23:997–1003. https://doi.org/10.1038/nm.4361CrossRefPubMed 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) Inflammation-dependent cerebrospinal fluid hypersecretion by the choroid plexus epithelium in posthemorrhagic hydrocephalus. Nat Med 23:997–1003. https://​doi.​org/​10.​1038/​nm.​4361CrossRefPubMed
53.
go back to reference Li Q, Ding Y, Krafft P, Wan W, Yan F, Wu G, Zhang Y, Zhan Q, Zhang JH (2018) Targeting germinal matrix hemorrhage-induced overexpression of sodium-coupled bicarbonate exchanger reduces posthemorrhagic hydrocephalus formation in neonatal rats. J Am Heart Assoc 7. https://doi.org/10.1161/jaha.117.007192 Li Q, Ding Y, Krafft P, Wan W, Yan F, Wu G, Zhang Y, Zhan Q, Zhang JH (2018) Targeting germinal matrix hemorrhage-induced overexpression of sodium-coupled bicarbonate exchanger reduces posthemorrhagic hydrocephalus formation in neonatal rats. J Am Heart Assoc 7. https://​doi.​org/​10.​1161/​jaha.​117.​007192
64.
go back to reference McAllister JP 2nd, Williams MA, Walker ML, Kestle JR, Relkin NR, Anderson AM, Gross PH, Browd SR (2015) An update on research priorities in hydrocephalus: overview of the third National Institutes of Health-sponsored symposium "Opportunities for Hydrocephalus Research: Pathways to Better Outcomes". J Neurosurg 123:1427–1438. https://doi.org/10.3171/2014.12.Jns132352CrossRefPubMed McAllister JP 2nd, Williams MA, Walker ML, Kestle JR, Relkin NR, Anderson AM, Gross PH, Browd SR (2015) An update on research priorities in hydrocephalus: overview of the third National Institutes of Health-sponsored symposium "Opportunities for Hydrocephalus Research: Pathways to Better Outcomes". J Neurosurg 123:1427–1438. https://​doi.​org/​10.​3171/​2014.​12.​Jns132352CrossRefPubMed
69.
go back to reference Oernbo EK, Steffensen AB, Razzaghi Khamesi P, Toft-Bertelsen TL, Barbuskaite D, Vilhardt F, Gerkau NJ, Tritsaris K, Simonsen AH, Lolansen SD, Andreassen SN, Hasselbalch SG, Zeuthen T, Rose CR, Kurtcuoglu V, MacAulay N (2022) Membrane transporters control cerebrospinal fluid formation independently of conventional osmosis to modulate intracranial pressure. Fluids Barriers CNS 19:65. https://doi.org/10.1186/s12987-022-00358-4CrossRefPubMedPubMedCentral Oernbo EK, Steffensen AB, Razzaghi Khamesi P, Toft-Bertelsen TL, Barbuskaite D, Vilhardt F, Gerkau NJ, Tritsaris K, Simonsen AH, Lolansen SD, Andreassen SN, Hasselbalch SG, Zeuthen T, Rose CR, Kurtcuoglu V, MacAulay N (2022) Membrane transporters control cerebrospinal fluid formation independently of conventional osmosis to modulate intracranial pressure. Fluids Barriers CNS 19:65. https://​doi.​org/​10.​1186/​s12987-022-00358-4CrossRefPubMedPubMedCentral
72.
go back to reference Oreskovic D, Klarica M, Vukic M, Marakovic J (2003) Evaluation of ventriculo-cisternal perfusion model as a method to study cerebrospinal fluid formation. Croat Med J 44:161–164PubMed Oreskovic D, Klarica M, Vukic M, Marakovic J (2003) Evaluation of ventriculo-cisternal perfusion model as a method to study cerebrospinal fluid formation. Croat Med J 44:161–164PubMed
73.
go back to reference Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Bmj 372:n71. https://doi.org/10.1136/bmj.n71CrossRefPubMedPubMedCentral Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Bmj 372:n71. https://​doi.​org/​10.​1136/​bmj.​n71CrossRefPubMedPubMedCentral
80.
go back to reference Riva-Cambrin J, Kestle JRW, Rozzelle CJ, Naftel RP, Alvey JS, Reeder RW, Holubkov R, Browd SR, Cochrane DD, Limbrick DD, Shannon CN, Simon TD, Tamber MS, Wellons JC, Whitehead WE, Kulkarni AV (2019) Predictors of success for combined endoscopic third ventriculostomy and choroid plexus cauterization in a North American setting: a Hydrocephalus Clinical Research Network study. J Neurosurg Pediatr 24:128–138. https://doi.org/10.3171/2019.3.Peds18532CrossRefPubMed Riva-Cambrin J, Kestle JRW, Rozzelle CJ, Naftel RP, Alvey JS, Reeder RW, Holubkov R, Browd SR, Cochrane DD, Limbrick DD, Shannon CN, Simon TD, Tamber MS, Wellons JC, Whitehead WE, Kulkarni AV (2019) Predictors of success for combined endoscopic third ventriculostomy and choroid plexus cauterization in a North American setting: a Hydrocephalus Clinical Research Network study. J Neurosurg Pediatr 24:128–138. https://​doi.​org/​10.​3171/​2019.​3.​Peds18532CrossRefPubMed
81.
go back to reference Robert SM, Reeves BC, Kiziltug E, Duy PQ, Karimy JK, Mansuri MS, Marlier A, Allington G, Greenberg ABW, DeSpenza T Jr, Singh AK, Zeng X, Mekbib KY, Kundishora AJ, Nelson-Williams C, Hao LT, Zhang J, Lam TT, Wilson R et al (2023) The choroid plexus links innate immunity to CSF dysregulation in hydrocephalus. Cell 186:764–785.e721. https://doi.org/10.1016/j.cell.2023.01.017CrossRefPubMed Robert SM, Reeves BC, Kiziltug E, Duy PQ, Karimy JK, Mansuri MS, Marlier A, Allington G, Greenberg ABW, DeSpenza T Jr, Singh AK, Zeng X, Mekbib KY, Kundishora AJ, Nelson-Williams C, Hao LT, Zhang J, Lam TT, Wilson R et al (2023) The choroid plexus links innate immunity to CSF dysregulation in hydrocephalus. Cell 186:764–785.e721. https://​doi.​org/​10.​1016/​j.​cell.​2023.​01.​017CrossRefPubMed
82.
go back to reference Sadegh C, Xu H, Sutin J, Fatou B, Gupta S, Pragana A, Taylor M, Kalugin PN, Zawadzki ME, Alturkistani O, Shipley FB, Dani N, Fame RM, Wurie Z, Talati P, Schleicher RL, Klein EM, Zhang Y, Holtzman MJ et al (2023) Choroid plexus-targeted NKCC1 overexpression to treat post-hemorrhagic hydrocephalus. Neuron. https://doi.org/10.1016/j.neuron.2023.02.020 Sadegh C, Xu H, Sutin J, Fatou B, Gupta S, Pragana A, Taylor M, Kalugin PN, Zawadzki ME, Alturkistani O, Shipley FB, Dani N, Fame RM, Wurie Z, Talati P, Schleicher RL, Klein EM, Zhang Y, Holtzman MJ et al (2023) Choroid plexus-targeted NKCC1 overexpression to treat post-hemorrhagic hydrocephalus. Neuron. https://​doi.​org/​10.​1016/​j.​neuron.​2023.​02.​020
94.
go back to reference Weed LH (1914) Studies on cerebro-spinal fluid. No. III : the pathways of escape from the Subarachnoid Spaces with particular reference to the Arachnoid Villi. J Med Res 31:51–91PubMedPubMedCentral Weed LH (1914) Studies on cerebro-spinal fluid. No. III : the pathways of escape from the Subarachnoid Spaces with particular reference to the Arachnoid Villi. J Med Res 31:51–91PubMedPubMedCentral
99.
go back to reference Wyss-Coray T, Feng L, Masliah E, Ruppe MD, Lee HS, Toggas SM, Rockenstein EM, Mucke L (1995) Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol 147:53–67PubMedPubMedCentral Wyss-Coray T, Feng L, Masliah E, Ruppe MD, Lee HS, Toggas SM, Rockenstein EM, Mucke L (1995) Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol 147:53–67PubMedPubMedCentral
Metadata
Title
CSF hypersecretion versus impaired CSF absorption in posthemorrhagic hydrocephalus: a systematic review
Authors
Shai David Ben-Shoshan
Sara Diana Lolansen
Tiit Illimar Mathiesen
Nanna MacAulay
Publication date
29-08-2023
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 11/2023
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-023-05746-9

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