Pro-inflammatory cerebrospinal fluid profile of neonates with intraventricular hemorrhage: clinical relevance and contrast with CNS infection.

Bacterial Meningitis CNS infection Cerebrospinal fluid Intraventricular hemorrhage Post-hemorrhagic hydrocephalus Prematurity Viral meningitis

Journal

Fluids and barriers of the CNS
ISSN: 2045-8118
Titre abrégé: Fluids Barriers CNS
Pays: England
ID NLM: 101553157

Informations de publication

Date de publication:
21 Feb 2024
Historique:
received: 16 07 2023
accepted: 16 01 2024
medline: 22 2 2024
pubmed: 22 2 2024
entrez: 21 2 2024
Statut: epublish

Résumé

Interpretation of cerebrospinal fluid (CSF) studies can be challenging in preterm infants. We hypothesized that intraventricular hemorrhage (IVH), post-hemorrhagic hydrocephalus (PHH), and infection (meningitis) promote pro-inflammatory CSF conditions reflected in CSF parameters. Biochemical and cytological profiles of lumbar CSF and peripheral blood samples were analyzed for 81 control, 29 IVH grade 1/2 (IVH PHH infants had higher (p < 0.02) CSF total cell and red blood cell (RBC) counts compared to control, IVH Similarities in CSF parameters may reflect common pathological processes in the inflammatory response and show the complexity associated with interpreting CSF profiles, especially in PHH and meningitis/ventriculitis.

Sections du résumé

BACKGROUND BACKGROUND
Interpretation of cerebrospinal fluid (CSF) studies can be challenging in preterm infants. We hypothesized that intraventricular hemorrhage (IVH), post-hemorrhagic hydrocephalus (PHH), and infection (meningitis) promote pro-inflammatory CSF conditions reflected in CSF parameters.
METHODS METHODS
Biochemical and cytological profiles of lumbar CSF and peripheral blood samples were analyzed for 81 control, 29 IVH grade 1/2 (IVH
RESULTS RESULTS
PHH infants had higher (p < 0.02) CSF total cell and red blood cell (RBC) counts compared to control, IVH
CONCLUSIONS CONCLUSIONS
Similarities in CSF parameters may reflect common pathological processes in the inflammatory response and show the complexity associated with interpreting CSF profiles, especially in PHH and meningitis/ventriculitis.

Identifiants

pubmed: 38383424
doi: 10.1186/s12987-024-00512-0
pii: 10.1186/s12987-024-00512-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

17

Informations de copyright

© 2024. The Author(s).

Références

Majumdar A, Jana A, Jana A, Biswas S, Bhatacharyya S, Bannerjee S. Importance of normal values of CSF parameters in term versus preterm neonates. J Clin Neonatol. 2013;2:166–8.
pubmed: 24404527 pmcid: 3883210 doi: 10.4103/2249-4847.123089
Thomson J, Sucharew H, Cruz AT, et al. Cerebrospinal fluid reference values for young infants undergoing lumbar puncture. Pediatrics. 2018. https://doi.org/10.1542/peds.2017-3405 .
doi: 10.1542/peds.2017-3405 pubmed: 29437883 pmcid: 5803891
Melville JM, Moss TJ. The immune consequences of preterm birth. Front Neurosci. 2013;7:79.
pubmed: 23734091 pmcid: 3659282 doi: 10.3389/fnins.2013.00079
Cuenca AG, Wynn JL, Moldawer LL, Levy O. Role of innate immunity in neonatal infection. Am J Perinatol. 2013;30:105–12.
pubmed: 23297181 pmcid: 3959733 doi: 10.1055/s-0032-1333412
Wellons JC 3rd, Shannon CN, Holubkov R, et al. Shunting outcomes in posthemorrhagic hydrocephalus: results of a hydrocephalus clinical research network prospective cohort study. J Neurosurg Pediatr. 2017;20:19–29.
pubmed: 28452657 doi: 10.3171/2017.1.PEDS16496
Mathews TJ, Miniño AM, Osterman MJ, Strobino DM, Guyer B. Annual summary of vital statistics: 2008. Pediatrics. 2011;127:146–57.
pubmed: 21173001 doi: 10.1542/peds.2010-3175
Strahle J, Garton HJ, Maher CO, Muraszko KM, Keep RF, Xi G. Mechanisms of hydrocephalus after neonatal and adult intraventricular hemorrhage. Transl Stroke Res. 2012;3:25–38.
pubmed: 23976902 pmcid: 3750748 doi: 10.1007/s12975-012-0182-9
Sävman K, Blennow M, Hagberg H, Tarkowski E, Thoresen M, Whitelaw A. Cytokine response in cerebrospinal fluid from preterm infants with posthaemorrhagic ventricular dilatation. Acta Paediatr. 2002;91:1357–63.
pubmed: 12578295 doi: 10.1111/j.1651-2227.2002.tb02834.x
Baumeister FA, Pohl-Koppe A, Hofer M, Kim JO, Weiss M. IL-6 in CSF during ventriculitis in preterm infants with posthemorrhagic hydrocephalus. Infection. 2000;28:234–6.
pubmed: 10961531 doi: 10.1007/s150100070043
Schmitz T, Heep A, Groenendaal F, et al. Interleukin-1beta, interleukin-18, and interferon-gamma expression in the cerebrospinal fluid of premature infants with posthemorrhagic hydrocephalus–markers of white matter damage? Pediatr Res. 2007;61:722–6.
pubmed: 17426654 doi: 10.1203/pdr.0b013e31805341f1
Sival DA, Felderhoff-Müser U, Schmitz T, Hoving EW, Schaller C, Heep A. Neonatal high pressure hydrocephalus is associated with elevation of pro-inflammatory cytokines IL-18 and IFNgamma in cerebrospinal fluid. Cerebrospinal Fluid Res. 2008;5:21.
pubmed: 19117508 pmcid: 2648939 doi: 10.1186/1743-8454-5-21
Habiyaremye G, Morales DM, Morgan CD, et al. Chemokine and cytokine levels in the lumbar cerebrospinal fluid of preterm infants with post-hemorrhagic hydrocephalus. Fluids Barriers CNS. 2017;14:35.
pubmed: 29228970 pmcid: 5725948 doi: 10.1186/s12987-017-0083-0
Cizmeci MN, Groenendaal F, Liem KD, et al. Randomized controlled early versus late ventricular intervention study in posthemorrhagic ventricular dilatation: outcome at 2 years. J Pediatr. 2020;226:28-35.e23.
pubmed: 32800815 doi: 10.1016/j.jpeds.2020.08.014
de Vries LS, Groenendaal F, Liem KD, et al. Treatment thresholds for intervention in posthaemorrhagic ventricular dilation: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2019;104:F70-f75.
pubmed: 29440132 doi: 10.1136/archdischild-2017-314206
Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1500 gm. J Pediatr. 1978;92:529–34.
pubmed: 305471 doi: 10.1016/S0022-3476(78)80282-0
Patra K, Wilson-Costello D, Taylor HG, Mercuri-Minich N, Hack M. Grades I-II intraventricular hemorrhage in extremely low birth weight infants: effects on neurodevelopment. J Pediatr. 2006;149:169–73.
pubmed: 16887428 doi: 10.1016/j.jpeds.2006.04.002
Wellons JC 3rd, Holubkov R, Browd SR, et al. The assessment of bulging fontanel and splitting of sutures in premature infants: an interrater reliability study by the hydrocephalus clinical research network. J Neurosurg Pediatr. 2013;11:12–4.
pubmed: 23121114 doi: 10.3171/2012.10.PEDS12329
El Bashir H, Laundy M, Booy R. Diagnosis and treatment of bacterial meningitis. Arch Dis Child. 2003;88:615–20.
pubmed: 12818910 pmcid: 1763168 doi: 10.1136/adc.88.7.615
Franco-Paredes C, Lammoglia L, Hernández I, Santos-Preciado JI. Epidemiology and outcomes of bacterial meningitis in Mexican children: 10-year experience (1993–2003). Int J Infect Dis. 2008;12:380–6.
pubmed: 18068385 doi: 10.1016/j.ijid.2007.09.012
Sáez-Llorens X, McCracken GH Jr. Bacterial meningitis in children. Lancet. 2003;361:2139–48.
pubmed: 12826449 doi: 10.1016/S0140-6736(03)13693-8
McGill F, Griffiths MJ, Solomon T. Viral meningitis: current issues in diagnosis and treatment. Curr Opin Infect Dis. 2017;30:248–56.
pubmed: 28118219 doi: 10.1097/QCO.0000000000000355
Brouwer MC, Tunkel AR, van de Beek D. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clin Microbiol Rev. 2010;23:467–92.
pubmed: 20610819 pmcid: 2901656 doi: 10.1128/CMR.00070-09
Morales DM, Silver SA, Morgan CD, et al. Lumbar cerebrospinal fluid biomarkers of posthemorrhagic hydrocephalus of prematurity: amyloid precursor protein, soluble amyloid precursor protein α, and L1 cell adhesion molecule. Neurosurgery. 2017;80:82–90.
pubmed: 27571524 doi: 10.1227/NEU.0000000000001415
Novak RW. Lack of validity of standard corrections for white blood cell counts of blood-contaminated cerebrospinal fluid in infants. Am J Clin Pathol. 1984;82:95–7.
pubmed: 6741880 doi: 10.1093/ajcp/82.1.95
The International Neonatal Network. The CRIB (clinical risk index for babies) score: a tool for assessing initial neonatal risk and comparing performance of neonatal intensive care units. Lancet. 1993;342:193–8.
doi: 10.1016/0140-6736(93)92296-6
Parry G, Tucker J, Tarnow-Mordi W. CRIB II: an update of the clinical risk index for babies score. Lancet. 2003;361:1789–91.
pubmed: 12781540 doi: 10.1016/S0140-6736(03)13397-1
Kinoshita M, Hawkes CP, Ryan CA, Dempsey EM. Perfusion index in the very preterm infant. Acta Paediatr. 2013;102:e398–401.
pubmed: 23772960 doi: 10.1111/apa.12322
Akima S, Kent A, Reynolds GJ, Gallagher M, Falk MC. Indomethacin and renal impairment in neonates. Pediatr Nephrol. 2004;19:490–3.
pubmed: 15007713 doi: 10.1007/s00467-003-1402-z
Tunkel AR, Hasbun R, Bhimraj A, et al. 2017 infectious diseases society of America’s clinical practice guidelines for healthcare-associated ventriculitis and meningitis. Clin Infect Dis. 2017;64:e34–65.
pubmed: 28203777 pmcid: 5848239 doi: 10.1093/cid/ciw861
Esaiassen E, Fjalstad JW, Juvet LK, van den Anker JN, Klingenberg C. Antibiotic exposure in neonates and early adverse outcomes: a systematic review and meta-analysis. J Antimicrob Chemother. 2017;72:1858–70.
pubmed: 28369594 doi: 10.1093/jac/dkx088
Mukhopadhyay S, Sengupta S, Puopolo KM. Challenges and opportunities for antibiotic stewardship among preterm infants. Arch Dis Child Fetal Neonatal Ed. 2019;104:F327-f332.
pubmed: 30425110 doi: 10.1136/archdischild-2018-315412
Ku LC, Boggess KA, Cohen-Wolkowiez M. Bacterial meningitis in infants. Clin Perinatol. 2015;42:29–45.
pubmed: 25677995 doi: 10.1016/j.clp.2014.10.004
van Furth AM, Roord JJ, van Furth R. Roles of proinflammatory and anti-inflammatory cytokines in pathophysiology of bacterial meningitis and effect of adjunctive therapy. Infect Immun. 1996;64:4883–90.
pubmed: 8945522 pmcid: 174464 doi: 10.1128/iai.64.12.4883-4890.1996
Mustafa MM, Ramilo O, Sáez-Llorens X, Olsen KD, Magness RR, McCracken GH Jr. Cerebrospinal fluid prostaglandins, interleukin 1 beta, and tumor necrosis factor in bacterial meningitis. Clinical and laboratory correlations in placebo-treated and dexamethasone-treated patients. Am J Dis Child. 1990;144:883–7.
pubmed: 2116086 doi: 10.1001/archpedi.1990.02150320047024
Srinivasan L, Kilpatrick L, Shah SS, Abbasi S, Harris MC. Cerebrospinal fluid cytokines in the diagnosis of bacterial meningitis in infants. Pediatr Res. 2016;80:566–72.
pubmed: 27486702 doi: 10.1038/pr.2016.117
Chadwick DR. Viral meningitis. Br Med Bull. 2005;75–76:1–14.
pubmed: 16474042 doi: 10.1093/bmb/ldh057
Kadry H, Noorani B, Cucullo L. A blood–brain barrier overview on structure, function, impairment, and biomarkers of integrity. Fluids Barriers CNS. 2020;17:69.
pubmed: 33208141 pmcid: 7672931 doi: 10.1186/s12987-020-00230-3
Bajaj M, Lulic-Botica M, Natarajan G. Evaluation of cerebrospinal fluid parameters in preterm infants with intraventricular reservoirs. J Perinatol. 2012;32:786–90.
pubmed: 22301529 doi: 10.1038/jp.2011.190
Lenfestey RW, Smith PB, Moody MA, et al. Predictive value of cerebrospinal fluid parameters in neonates with intraventricular drainage devices. J Neurosurg. 2007;107:209–12.
pubmed: 17918526
Verbeek MM, Leen WG, Willemsen MA, Slats D, Claassen JA. Hourly analysis of cerebrospinal fluid glucose shows large diurnal fluctuations. J Cereb Blood Flow Metab. 2016;36:899–902.
pubmed: 26945018 pmcid: 4853846 doi: 10.1177/0271678X16637612
Tan QC, Xing XW, Zhang JT, et al. Correlation between blood glucose and cerebrospinal fluid glucose levels in patients with differences in glucose metabolism. Front Neurol. 2023;14:1103026.
pubmed: 37181574 pmcid: 10174426 doi: 10.3389/fneur.2023.1103026
Karimy JK, Zhang J, Kurland DB, et al. Inflammation-dependent cerebrospinal fluid hypersecretion by the choroid plexus epithelium in posthemorrhagic hydrocephalus. Nat Med. 2017;23:997–1003.
pubmed: 28692063 doi: 10.1038/nm.4361
Karimy JK, Reeves BC, Damisah E, et al. Inflammation in acquired hydrocephalus: pathogenic mechanisms and therapeutic targets. Nat Rev Neurol. 2020;16:285–96.
pubmed: 32152460 pmcid: 7375440 doi: 10.1038/s41582-020-0321-y
Pasquier JC, Picaud JC, Rabilloud M, et al. Neonatal outcomes after elective delivery management of preterm premature rupture of the membranes before 34 weeks’ gestation (DOMINOS study). Eur J Obstet Gynecol Reprod Biol. 2009;143:18–23.
pubmed: 19167805 doi: 10.1016/j.ejogrb.2008.10.017
Ernest JM. Neonatal consequences of preterm PROM. Clin Obstet Gynecol. 1998;41:827–31.
pubmed: 9917937 doi: 10.1097/00003081-199812000-00006
Velemínský M Jr, Stránský P, Velemínský M Sr, Tosner J. Relationship of IL-6, IL-8, TNF and sICAM-1 levels to PROM, pPROM, and the risk of early-onset neonatal sepsis. Neuro Endocrinol Lett. 2008;29:303–11.
pubmed: 18580842
Srinivasan L, Shah SS, Padula MA, Abbasi S, McGowan KL, Harris MC. Cerebrospinal fluid reference ranges in term and preterm infants in the neonatal intensive care unit. J Pediatr. 2012;161:729–34.
pubmed: 22575245 pmcid: 4593309 doi: 10.1016/j.jpeds.2012.03.051
Nigrovic LE, Malley R, Macias CG, et al. Effect of antibiotic pretreatment on cerebrospinal fluid profiles of children with bacterial meningitis. Pediatrics. 2008;122:726–30.
pubmed: 18829794 doi: 10.1542/peds.2007-3275

Auteurs

Maria Garcia-Bonilla (M)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA. mariag@wustl.edu.
Department of Neurosurgery, Virginia Commonwealth University School of Medicine, Richmond, VA, USA. mariag@wustl.edu.

Alexander T Yahanda (AT)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA.

Albert M Isaacs (AM)

Department of Neurosurgery, Nationwide Children's Hospital, Ohio State University, Columbus, OH, USA.

Brandon Baksh (B)

University of Miami Miller School of Medicine, Miami, FL, USA.

S Hassan A Akbari (SHA)

John Hopkins University School of Medicine, Johns Hopkins All Children's Hospital, St. Petersburg,, FL, USA.

Haley Botteron (H)

Medical School, University of Kansas, Kansas City, KS, USA.

Diego M Morales (DM)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA.

Rowland H Han (RH)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA.

James P McAllister Ii (JP)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA.

Amit M Mathur (AM)

Department of Pediatrics, Saint Louis University School of Medicine, St. Louis, MO, USA.

Jennifer M Strahle (JM)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA.
Department of Pediatrics, Washington University School of Medicine, St. Louis, MO, USA.

Christopher D Smyser (CD)

Department of Pediatrics, Washington University School of Medicine, St. Louis, MO, USA.
Department of Neurology, Washington University School of Medicine, St. Louis, MO, USA.
Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, MO, USA.

David D Limbrick (DD)

Department of Neurosurgery, Washington University School of Medicine, One Children's Place, Suite 420, St. Louis, MO, USA.
Department of Neurosurgery, Virginia Commonwealth University School of Medicine, Richmond, VA, USA.

Classifications MeSH