UNLABELLED: 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.

1st Faculty of Medicine Charles University Nové Město Czech Republic

Charing Cross Hospital Imperial College Healthcare London UK

Department of Neurosurgery 2nd Faculty of Medicine Charles University Prague and Motol University Hospital Prague Czech Republic

Department of Neurosurgery and Neurooncology Military University Hospital and Charles University U Vojenské Nemocnice 1200 1 162 00 Prague 6 Czech Republic

Zobrazit více v PubMed

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. 10.1016/j.acra.2009.08.011 PubMed

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

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. 10.1371/journal.pone.0217705 PubMed PMC

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. 10.1007/s10554-010-9708-y PubMed PMC

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. 10.1097/00004424-200107000-00003 PubMed

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. 10.1097/01.rli.0000100892.87214.49 PubMed

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. 10.1007/s00701-018-3731-5 PubMed

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

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. 10.1007/s00381-018-3845-3 PubMed

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):523–529 PubMed

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 105:9–15 PubMed

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. 10.1177/0284185113508112 PubMed

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

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

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

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):321–328 PubMed

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):2063–2071 PubMed PMC

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. 10.1186/s12987-019-0122-0 PubMed PMC

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 10.3389/fneur.2022.959450 PubMed PMC

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 339:108–112 PubMed

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

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. 10.3325/cmj.2021.62.307 PubMed PMC

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

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. 10.5114/pjr.2019.86881. Published 2019 May 13 PubMed PMC

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. 10.1016/j.nicl.2018.09.006 PubMed PMC

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. 10.1097/00006123-200203000-00020 PubMed

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

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. 10.1148/radiology.154.2.3966130 PubMed

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. 10.1016/S1042-3680(18)30559-X PubMed

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. 10.3389/fnins.2019.00729 PubMed PMC

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. 10.1111/ane.12636 PubMed

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. 10.1016/j.molmed.2019.11.00847] PubMed PMC

Relkin N, Marmarou A, Klinge P et al (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S4-16. 10.1227/01.neu.0000168185.29659.c5 PubMed

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. 10.3171/2015.6.JNS15496 PubMed

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. 10.3174/ajnr.A5972 PubMed PMC

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

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. 10.23736/S0390-5616.17.04092-9. PubMed

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):838–843 PubMed

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. 10.2147/CIA.S290709. Published 2021 Jan 15 PubMed PMC

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. 10.1016/j.jocn.2021.05.010 PubMed

Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36(3):1–48. 10.18637/jss.v036.i03

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. 10.3171/2022.1.FOCUS21733 PubMed

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

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. 10.3174/ajnr.A2039 PubMed PMC

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 PubMed

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

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. 10.1007/s00330-020-06825-6 PubMed

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. 10.1111/ane.12750 PubMed

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):999–1008