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Open Access 01-12-2024 | Hydrocephalus | Review

Volumes and velocities: Meta-analysis of PC-MRI studies in normal pressure hydrocephalus

Authors: Helen Whitley, Petr Skalický, Awista Zazay, Adéla Bubeníková, Ondrej Bradáč

Published in: Acta Neurochirurgica | Issue 1/2024

Abstract

Purpose

Phase contrast magnetic resonance imaging (PC-MRI) represents an opportunity to non-invasively investigate cerebral spinal fluid (CSF) flow in patients with idiopathic normal pressure hydrocephalus (iNPH). Studies in recent years have explored the diagnostic and prognostic value of PC-MRI derived parameters. This review aims to identify all PC-MRI studies of iNPH published since 2010, synthesise a review based on collated results, and analyse specific flow parameters identified in the selected studies.

Methods

Our protocol was prospectively registered on PROSPERO [CRD42020180826]. We systematically searched four databases: Pubmed, Web of Science, Ovid, and Cochrane library to identify all eligible studies. Quality assessment was performed using a modified Newcastle–Ottawa Scale [19]. Systematic review was conducted according to Prisma guidelines. A random-effects model was used to perform meta-analysis on the available flow parameters.

Results

Eighteen records were identified for inclusion. Five studies were eligible for meta-analysis, representing 107 iNPH patients and 82 controls. CSF flow parameters available for analysis were stroke volume and peak velocity. Both were significantly higher than controls (p = 0.0007 and p = 0.0045 respectively) according to our random-effects analysis, consistent with a model of hyper-dynamic CSF in iNPH. Our systematic review revealed average stroke volumes in iNPH ranging from 43uL to over 200uL. Peak velocity values ranged from 5.9 cm/s to 12.8 cm/s.

Conclusion

Significant increases in stroke volume and peak velocity values in iNPH patients suggest a place for PC-MRI as supplementary evidence in the diagnostic work-up of iNPH. Although shunting reduces aqueductal stroke volume and peak velocity, the ability of pre-shunt values to reliably predict treatment response remains complicated. We suggest that it may be more appropriate to consider a range of values that reflect varying probabilities of shunt success. We recommend that future studies should prioritise standardising PC-MRI protocols, and before then PC-MRI findings should be considered supportive rather than determinative.

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Algin O, Hakyemez B, Parlak M (2010) The efficiency of PC-MRI in diagnosis of normal pressure hydrocephalus and prediction of shunt response. Acad Radiol 17(2):181–187. https://doi.org/10.1016/j.acra.2009.08.011CrossRefPubMed

Alperin N (2004) MR-intracranial compliance and pressure: a method for noninvasive measurement of important neurophysiologic parameters. Methods Enzymol 386:323–349. https://doi.org/10.1016/S0076-6879(04)86016-6CrossRefPubMed

Andersson J, Rosell M, Kockum K, Lilja-Lund O, Söderstr L (2019) Prevalence of idiopathic normal pressure hydrocephalus: A prospective, population-based study. PLoS One 14(5):e0217705. https://doi.org/10.1371/journal.pone.0217705CrossRefPubMedPubMedCentral

ASCI Cct and CMR Guideline Working Group, Chan CW, Choi BW, ASCI, et al (2010) standardised practice protocol for cardiac magnetic resonance imaging: a report of the Asian society of cardiovascular imaging cardiac computed tomography and cardiac magnetic resonance imaging guideline working group. Int J Cardiovasc Imaging 2010:26. https://doi.org/10.1007/s10554-010-9708-yCrossRef

Balédent O, Henry-Feugeas MC, Idy-Peretti I (2001) Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest Radiol 36(7):368–377. https://doi.org/10.1097/00004424-200107000-00003CrossRefPubMed

Balédent O, Gondry-Jouet C, Meyer ME et al (2004) Relationship between cerebrospinal fluid and blood dynamics in healthy volunteers and patients with communicating hydrocephalus. Invest Radiol 39(1):45–55. https://doi.org/10.1097/01.rli.0000100892.87214.49CrossRefPubMed

Balédent O, Czosnyka Z, Czosnyka M (2019) “Bucket” cerebrospinal fluid bulk flow-is it a fact or a fiction? Acta Neurochir (Wien) 161(2):257–258. https://doi.org/10.1007/s00701-018-3731-5CrossRefPubMed

Bateman GA (2000) Vascular compliance in normal pressure hydrocephalus. AJNR Am J Neuroradiol 21(9):1574–1585PubMedPubMedCentral

Borzage M, Ponrartana S, Tamrazi B, Gibbs W, Nelson MD, McComb JG, Blüml S (2018) A new MRI tag-based method to non-invasively visualize cerebrospinal fluid flow. Childs Nerv Syst 34(9):1677–1682. https://doi.org/10.1007/s00381-018-3845-3CrossRefPubMed

10.

Bradley WG Jr, Scalzo D, Queralt J, Nitz WN, Atkinson DJ, Wong P (1996) Normal-pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 198(2):523–529CrossRefPubMed

11.

Chen CH, Cheng YC, Huang CY, Chen HC, Chen WH, Chai JW (2022) Accuracy of MRI derived cerebral aqueduct flow parameters in the diagnosis of idiopathic normal pressure hydrocephalus. J Clin Neurosci 105:9–15CrossRefPubMed

12.

Daouk J, Chaarani B, Zmudka J et al (2014) Relationship between cerebrospinal fluid flow, ventricles morphology, and DTI properties in internal capsules: differences between Alzheimer’s disease and normal-pressure hydrocephalus. Acta Radiol 55(8):992–999. https://doi.org/10.1177/0284185113508112CrossRefPubMed

13.

Enzmann DR, Pelc NJ (1991) Normal flow patterns of intracranial and spinal cerebrospinal fluid defined with phase-contrast cine MR imaging. Radiology 178:467–474CrossRefPubMed

14.

Feinberg DA, Mark AS (1987) Human brain motion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. Radiology 163(3):793–799. https://doi.org/10.1148/radiology.163.3.3575734CrossRefPubMed

15.

Greitz D, Greitz T (1997) The pathogenesis and hemodynamics of hydrocephalus. A proposal for a new understanding. Int J Neuroradiol 3:367–375

16.

Greitz D, Franck A, Nordell B (1993Jul) On the pulsatile nature of intracranial and spinal CSF-circulation demonstrated by MR imaging. Acta Radiol 34(4):321–328CrossRefPubMed

17.

Halperin J et al (2015) Practice guideline: Idiopathic normal pressure hydrocephalus: Response to shunting and predictors of response: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology. Neurology 85(23):2063–2071CrossRefPubMedPubMedCentral

18.

Hamilton RB, Scalzo F, Baldwin K et al (2019) Opposing CSF hydrodynamic trends found in the cerebral aqueduct and prepontine cistern following shunt treatment in patients with normal pressure hydrocephalus. Fluids Barriers CNS 16(1):2. https://doi.org/10.1186/s12987-019-0122-0CrossRefPubMedPubMedCentral

19.

He WJ, Zhang XJ, Xu QZ et al (2022) Are preoperative phase-contrast CSF flow parameters ideal for predicting the outcome of shunt surgery in patients with idiopathic normal pressure hydrocephalus? Front Neurol 13:959450 Published 2022 Sep 27 https://doi.org/10.3389/fneur.2022.959450CrossRefPubMedPubMedCentral

20.

Iseki C, Takahashi Y, Wada M, Kawanami T, Adachi M, Kato T (2014) Incidence of idiopathic normal pressure hydrocephalus (iNPH): a 10-year follow-up study of a rural community in Japan. J Neurol Sci 339:108–112CrossRefPubMed

21.

Jaraj D, Rabiei K, Marlow T et al (2014) Prevalence of idiopathic normal pressure hydrocephalus. Neurology 82(16):1449–1454. https://doi.org/10.1212/WNL.0000000000000342CrossRefPubMedPubMedCentral

22.

Klarica M, Radoš M, Vukić M, Orešković D (2021) The physiology and pathophysiology of cerebrospinal fluid: new evidence. Croat Med J 62(4):307–309. https://doi.org/10.3325/cmj.2021.62.307CrossRefPubMedPubMedCentral

23.

Kondziella D, Sonnewald U, Tullberg M, Wikkelso C (2008) Brain metabolism in adult chronic hydrocephalus. J Neurochem 106:1515–1524. https://doi.org/10.1111/j.1471-4159.2008.05422.xCrossRefPubMed

24.

Korbecki A, Zimny A, Podgórski P, Sąsiadek M, Bladowska J (2019) Imaging of cerebrospinal fluid flow: fundamentals, techniques, and clinical applications of phase-contrast magnetic resonance imaging. Pol J Radiol 84:e240–e250. https://doi.org/10.5114/pjr.2019.86881. Published 2019 May 13CrossRefPubMedPubMedCentral

25.

Lindstrøm EK, Ringstad G, Mardal K-A, Eide PK (2018) Cerebrospinal fluid volumetric net flow rate and direction in idiopathic normal pressure hydrocephalus, NeuroImage: Clinical, 20. ISSN 731–741:2213–1582. https://doi.org/10.1016/j.nicl.2018.09.006CrossRef

26.

Luetmer PH, Huston J, Friedman JA et al (2002) Measurement of cerebrospinal fluid flow at the cerebral aqueduct by use of phase-contrast magnetic resonance imaging: technique validation and utility in diagnosing idiopathic normal pressure hydrocephalus. Neurosurgery 50(3):534–544. https://doi.org/10.1097/00006123-200203000-00020CrossRefPubMed

27.

Miskin N, Serulle Y, Wu W et al (2015) Post-Shunt Gait Improvement Correlates with Increased Cerebrospinal Fluid Peak Velocity in Normal Pressure Hydrocephalus: A Retrospective Observational Phase-Contrast Magnetic Resonance Imaging Study Int J Sci Study 3(8):48–54

28.

Moran PR, Moran RA, Karstaedt N (1985) Verification and evaluation of internal flow and motion. True magnetic resonance imaging by the phase gradient modulation method. Radiology 154(2):433–441. https://doi.org/10.1148/radiology.154.2.3966130CrossRefPubMed

29.

Naidich TP, Altman NR, Gonzalez-Arias SM, Imaging PCCMR (1993) Normal Cerebrospinal Fluid Oscillation and Applications to Hydrocephalus. Neurosurg Clin N Am 4(4):677–705. https://doi.org/10.1016/S1042-3680(18)30559-XCrossRefPubMed

30.

Panman JL, To YY, van der Ende EL et al (2019) Bias Introduced by Multiple Head Coils in MRI Research: An 8 Channel and 32 Channel Coil Comparison. Front Neurosci 13:729. https://doi.org/10.3389/fnins.2019.00729CrossRefPubMedPubMedCentral

31.

Qvarlander S, Ambarki K, Wåhlin A et al (2017) Cerebrospinal fluid and blood flow patterns in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 135(5):576–584. https://doi.org/10.1111/ane.12636CrossRefPubMed

32.

Reeves BC, Karimy JK, Kundishora AJ et al (2020) Glymphatic System Impairment in Alzheimer’s Disease and Idiopathic Normal Pressure Hydrocephalus. Trends Mol Med 26(3):285–295. https://doi.org/10.1016/j.molmed.2019.11.00847]CrossRefPubMedPubMedCentral

33.

Relkin N, Marmarou A, Klinge P et al (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S4-16. https://doi.org/10.1227/01.neu.0000168185.29659.c5CrossRefPubMed

34.

Ringstad G, Emblem KE, Eide PK (2016) Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg 124(6):1850–1857. https://doi.org/10.3171/2015.6.JNS15496CrossRefPubMed

35.

Shanks J, Markenroth Bloch K, Laurell K et al (2019) Aqueductal CSF Stroke Volume Is Increased in Patients with Idiopathic Normal Pressure Hydrocephalus and Decreases after Shunt Surgery. Am J Neuroradiol 40(3):453–459. https://doi.org/10.3174/ajnr.A5972CrossRefPubMedPubMedCentral

36.

Stankovic Z, Allen BD, Garcia J, Jarvis KB, Markl M (2014) 4D flow imaging with MRI. Cardiovasc Diagn Ther 4(2):173–192. https://doi.org/10.3978/j.issn.2223-3652.2014.01.02CrossRefPubMedPubMedCentral

37.

Stecco A, Cassarà A, Zuccalà A, Anoaica, M., Genovese E, Car P, Panzarasa G, Guzzardi G, Carriero A. (2017). Quantitative analysis of cerebrospinal fluid dynamics at phase contrast cine-MRI: predictivity of neurosurgical "Shunt" responsiveness in patients with idiopathic normal pressure hydrocephalus. Journal of neurosurgical sciences. 64. https://doi.org/10.23736/S0390-5616.17.04092-9.

38.

Tawfik AM, Elsorogy L, Abdelghaffar R, Naby AA, Elmenshawi I (2017) Phase-Contrast MRI CSF Flow Measurements for the Diagnosis of Normal-Pressure Hydrocephalus: Observer Agreement of Velocity Versus Volume Parameters. Am J Roentgenol 208(4):838–843CrossRef

39.

Tan C, Wang X, Wang Y et al (2021) The Pathogenesis Based on the Glymphatic System, Diagnosis, and Treatment of Idiopathic Normal Pressure Hydrocephalus. Clin Interv Aging 16:139–153. https://doi.org/10.2147/CIA.S290709. Published 2021 Jan 15CrossRefPubMedPubMedCentral

40.

Tsou CH, Cheng YC, Huang CY et al (2021) Using deep learning convolutional neural networks to automatically perform cerebral aqueduct CSF flow analysis. J Clin Neurosci 90:60–67. https://doi.org/10.1016/j.jocn.2021.05.010CrossRefPubMed

41.

Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36(3):1–48. https://doi.org/10.18637/jss.v036.i03CrossRef

42.

Vlasák A, Gerla V, Skalický P et al (2022) Boosting phase-contrast MRI performance in idiopathic normal pressure hydrocephalus diagnostics by means of machine learning approach. Neurosurg Focus 52(4):E6. https://doi.org/10.3171/2022.1.FOCUS21733CrossRefPubMed

43.

Wells G A, Shea B, O’Connell D et al. (2013) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp, Accessed 14th May 2022

44.

Wentland AL, Wieben O, Korosec FR, Haughton VM (2010) Accuracy and reproducibility of phase-contrast MR imaging measurements for CSF flow. Am J Neuroradiol 31(7):1331–1336. https://doi.org/10.3174/ajnr.A2039CrossRefPubMedPubMedCentral

45.

Witthiwej T, Sathira-ankul P, Chawalparit O et al (2012) MRI study of intracranial hydrodynamics and ventriculoperitoneal shunt responsiveness in patient with normal pressure hydrocephalus. J Med Assoc Thailand 95(12):1556–1562

46.

Yamada S (2021Aug 31) Cerebrospinal fluid dynamics. Croat Med J 62(4):399–410. https://doi.org/10.3325/cmj.2021.62.399CrossRefPubMed

47.

Yamada S, Ishikawa M, Ito H et al (2020) Cerebrospinal fluid dynamics in idiopathic normal pressure hydrocephalus on four-dimensional flow imaging. Eur Radiol 30(8):4454–4465. https://doi.org/10.1007/s00330-020-06825-6CrossRefPubMed

48.

Yin LK, Zheng JJ, Zhao L et al (2017) Reversed aqueductal cerebrospinal fluid net flow in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 136(5):434–439. https://doi.org/10.1111/ane.12750CrossRefPubMed

49.

Yousef MI, Abd El Mageed AE, Yassin AEN, Shaaban MH (2016) Use of cerebrospinal fluid flow rates measured by phase-contrast MR to differentiate normal pressure hydrocephalus from involutional brain changes. Egypt J of Radiol Nucl Med 47(3):999–1008CrossRef

Title: Volumes and velocities: Meta-analysis of PC-MRI studies in normal pressure hydrocephalus
Authors: Helen Whitley
Petr Skalický
Awista Zazay
Adéla Bubeníková
Ondrej Bradáč
Publication date: 01-12-2024
Publisher: Springer Vienna
Keywords: Hydrocephalus
Hydrocephalus
Hydrocephalus
Magnetic Resonance Imaging
Magnetic Resonance Imaging
Published in: Acta Neurochirurgica / Issue 1/2024
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-024-06333-2

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Volumes and velocities: Meta-analysis of PC-MRI studies in normal pressure hydrocephalus

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