This report describes the data related to the article entitiled: “Relationship between inferior frontal sulcal hyperintensities on brain MRI, ageing and cerebral small vessel disease”. This systematic review was conducted to assess possible causes for sulcal hyperintensities on fluid-attenuated inversion recovery (FLAIR) images on brain MRI

Lim, Hwee Fang

Valdés Hernández, Maria C

Wardlaw, Joanna M.

Wu, Yun-cheng

Zhang, Jun-fang

English

zhang, J

NARCIS 

The possible causes for sulcal hyperintensities on FLAIR images on brain MRI: the dataset derived from a systematic review

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     Edinburgh Research Explorer                                      The possible causes for sulcal hyperintensities on FLAIR imageson brain MRI: the dataset derived from a systematic reviewCitation for published version:Lim, HF, Zhang, J, Valdés Hernández, MC, Wu, Y & Wardlaw, JM, The possible causes for sulcalhyperintensities on FLAIR images on brain MRI: the dataset derived from a systematic review, 2021, Dataset/Database. https://doi.org/10.17632/pskc7cfmrt.1Digital Object Identifier (DOI):10.17632/pskc7cfmrt.1Link:Link to publication record in Edinburgh Research ExplorerGeneral rightsCopyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s)and / or other copyright owners and it is a condition of accessing these publications that users recognise andabide by the legal requirements associated with these rights.Take down policyThe University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorercontent complies with UK legislation. If you believe that the public display of this file breaches copyright pleasecontact openaccess@ed.ac.uk providing details, and we will remove access to the work immediately andinvestigate your claim.Download date: 23. Feb. 2022The possible causes for sulcal hyperintensities on FLAIR images on brain MRI: the dataset derived from a systematic review   Cerebrospinal fluid (CSF) is normally dark with low signal on magnetic resonance imaging (MRI) fluid-attenuated inversion recovery (FLAIR) images, but the signal may increase (become whiter) if there is protein or gadolinium compounds or other materials in the CSF. We performed a systematic review to document all causes of increase in CSF signal on FLAIR MRI.  A systematic literature search was conducted in PubMed and EMBASE (from inception to June 2020) in line with the PRISMA Statement (Preferred Reporting Items for Systematic Reviews and Meta-Analyses). We searched for relevant articles reporting sulcal FLAIR hyperintensities using Boolean operator terms and restricted the search to MR imaging in humans. Various combinations of the following search terms were employed: “inferior frontal sulci”, “inferior frontal sulcus”, “sulcal”, “CSF”, “cerebrospinal fluid”, “FLAIR”, “hyperintensity” and “hyperintensities”.   Initial search specifically relating IFSH on FLAIR on 3T MRI sequences yielded no relevant results on PubMed and EMBASE (search syntax entered on PUBMED listed as Figure I). Hence, the search was subsequently expanded to look more generally at causes for sulcal hyperintensities on FLAIR images which yielded more results (search syntax used on PubMed is listed in Figure II). Additional papers were also reviewed by hand-searching the references of the relevant papers found. We excluded non-English articles, animal-based studies and articles that were not available via full-text.   Results of literature review  A summary of the number of papers found is shown as below in Figure III with the corresponding flow-chart summarizing the search. Out of the initial 83 potentially relevant papers identified, after de-duplication, 64 were screened and 39 full papers assessed for relevance. Of 25 records removed, 24 papers were excluded as they were not available as full articles, and one was excluded as it was not in English language. Fifteen full-text articles were subsequently excluded as they were deemed not relevant to the focus of the study. Overall, only 24 articles were deemed relevant.     Figure I: Search syntax on PubMed regarding inferior frontal sulci hyperintensities on FLAIR on 3T MRI sequences      Figure II: PubMed search syntax         Figure III: Flow-chart of the systematic literature search         A summary of the various papers is shown in Table I which includes the field strength of the scanner used, number of patients, age ranges, gender demographic, disease association with sulcal hyperintensity on FLAIR and proposed pathological process behind sulcal hyperintensity.  Of the 24 included papers, 2 concerned acute stroke, 3 were on haemorrhage, 4 on meningitis, 2 on malignancies, 4 post-interventions (CSF drainage, oxygen administration), 3 on migraine with aura and the remaining 6 on a number of other topics. Though there were varied causes of increased cerebrospinal fluid (CSF) signal on FLAIR, a number of studies attributed sulcal hyperintensity to blood brain barrier (BBB) disruption or increased CSF protein concentration/leakage, eg due to blood products. Specifically, increased CSF protein concentration was mentioned in association with conditions such as meningitis, cryptococcal meningoencephalitis and intracranial meningeal carcinomatosis (tumour cells thought to induce increased CSF protein). BBB breakdown was mentioned in association with conditions such as stroke and central nervous system (CNS) haemorrhage. The increased CSF signal on FLAIR was usually located at the site of the brain pathology and therefore could relate to any sulci.  Most studies used 1.5T scanners. The range of total number of participants across the studies is from 1 – 578 (1 being a case report). Age range of participants across studies range from 3 months – 88 years.           Table I: Literature review summary table by diseases  First Author and paper title Field strength No of patients Age range (years) Gender (Male/ Female) Postulated underlying pathology for sulcal hyperintensity  Stroke Lee H et al. Clinical Implications of Sulcal Enhancement on Postcontrast Fluid Attenuated Inversion Recovery Images in Patients with Acute Stroke Symptoms1  1.5T, 3T 578 - - Hyperintense acute reperfusion marker is thought to be a useful marker for indicating BBB disruption in an acute stroke, because gadolinium does not cross the intact BBB. The contrast medium is believed to cross the BBB injury site after reperfusion, enter the perivascular space, and then diffuse into the CSF via a perivascular pathway. Kim et al. Sulcal Hyperintensity on Fluid-Attenuated Inversion Recovery Imaging in Acute Ischemic Stroke Patients Treated With Intra-Arterial Thrombolysis: Iodinated Contrast Media as Its Possible Cause and the Association With Hemorrhagic Transformation2 1.5 T 14 43-75  7 /7 May be caused by disruption of the BBB, which may result in leakage of contrast medium as well as protein into the CSF space.  Haemorrhage Noguchi et al. MR of Acute Subarachnoid Hemorrhage: A Preliminary Report of Fluid- Attenuated Inversion-Recovery Pulse Sequences3 0.5 T 3 30-68  1/2 Increased signal from bloody CSF because of shortening of the Tl relaxation time. Thus, acute subarachnoid haemorrhage is seen as hyperintense relative to normal CSF. Kidwell et al. Hyperacute injury marker (HARM) in primary hemorrhage: a distinct form of CNS barrier disruption.4 1.5T, 3T 46 Mean age = 65 - Likely involves a combination of BBB and B-CSF-B disruption.   Oshida et al. A Case of Chronic Subdural Hematoma Demonstrating the Epileptic Focus at the Area With Sulcal Hyperintensity on Fluid-Attenuated Inversion Recovery Image5 - 1 (case report) 77 1/- The epileptogenic area corresponding to that with sulcal hyperintensity on FLAIR might be in an activated electrophysiological state, with the activated area exhibiting a hypermetabolic state, thereby causing compensatory regional hyperperfusion. Meningitis Kamran et al. Role of fluid-attenuated inversion recovery in the diagnosis of meningitis: comparison with contrast-enhanced magnetic resonance imaging.6 1.5 T 28 1 month to 69 years  20/8  FLAIR high signal may be seen in meningitis due to increased CSF protein concentration. Kuwahara et al. Cryptococcal meningoencephalitis presenting with an unusual magnetic resonance imaging appearance--case report.7 Not stated 1 (case report) 61 - /1 Increased CSF protein concentration from inflammation in localised subarachnoid space  Boban et al. Leptomeningeal form of Immunoglobulin G4-related hypertrophic meningitis with perivascular spread: a case report and review of the literature.8 - 1 (case report) 58 1/- These changes probably represented vasogenic edema (no signs of restricted diffusion were present), due to venous congestion and deprived venous outflow.  Melhem et al. Fluid-attenuated inversion recovery MR imaging: identification of protein concentration thresholds for CSF hyperintensity. 24 1.5 T 1 (case report) 60 - /1 FLAIR high signal may be seen in acute meningitis due to increased CSF protein concentration. Malignancies Yasuyuki et al. Epithelial Ovarian Carcinoma Associated with Metastases to Central Nervous System: Two Case Reports9  - 2 case reports 55 and 63 - / 1 - Tsuchiya et al. FLAIR MR imaging for diagnosing intracranial meningeal carcinomatosis10 1.5 T, 0.5T 9 21- 73  4/5 Tumour cells in meningeal carcinomatosis thought to induce an increase in cerebrospinal fluid proteins. CSF removal and oxygen administration Yazdani et al. Sulcal FLAIR hyperintensity after CSF removal in two patients with intracranial hypertension11  - 2 (case reports) 27 and 28 - / 2 Proposed mechanism of sulcal FLAIR hyperintensity is possibly due to decrease in CSF to blood pool ratio in the involved voxels from decrease in sulcal CSF space hence the blood pool becomes the dominant contributor to sulcal FLAIR signal rather than CSF, and the blood pool is not attenuated by the inversion recovery.  Anzai et al. Paramagnetic Effect of Supplemental Oxygen on CSF Hyperintensity on Fluid-Attenuated Inversion Recovery MR Images12 1.5 T 6 34-40  3/3 Oxygen has a known paramagnetic effect and increases CSF signal intensity on fluid-attenuated inversion recovery (FLAIR) MR images Frigon et al. Fraction of Inspired Oxygen in Relation to Cerebrospinal Fluid Hyperintensity on FLAIR MR Imaging of the Brain in Children and Young Adults Undergoing Anesthesia13 1.5 T 70 - - Likely related to the fact that oxygen, being slightly paramagnetic, also produces a mild shortening in T1.   Goetz et al. Hyperintense Cerebrospinal Fluid on FLAIR Images Induced by Ventilation with 100% Oxygen14  1.5 T 40 3 months to 8 years  27 /13 Increased CSF signal intensity changes thought to be caused by paramagnetic effects of supplemental oxygen. Migraine with aura de Oliveira et al.Reversible Sulcal FLAIR Hyperintensity on MRI in a Migraine Patient With Aura15  1.5T 1 (case report) 66 - / 1 Changes in the occipital lobe possibly related to a hyper excitable visual cortex as trigger for the headache and also vasodilatation with tissue hyperoxygenation and decreased energy reserves as part of the central pain process pathway. A suggested mechanism is increased leptomeningeal vascularity leading to plasma extravasation and increased local protein concentration in the sulci. Gómez et al. Migraine with Aura Associated with Reversible Sulcal Hyperintensity in FLAIR16  - 1 (case report) 22 - / 1 Transient increase of leptomeningeal vascular permeability during the aura phase might have led to gadolinium leakage during the first/prior MR head examination. It would accumulate within the pia mater and arachnoid membrane in sufficient concentration to cause the signal changes observed during the second MRI study.  Kang et al. Transient Sulcal Hyperintensities on Fluid-Attenuated Inversion Recovery in Migraine With Aura: Transient Sulcal Hyperintensities in Migraine17 - 1 (case report) 33 - / 1 It is suggested that sulcal hyperintensities on FLAIR images could be caused by a slow flow of the pial artery which transiently occludes the microcirculation from micro- emboli via PFO. Others Taoka et al. Sulcal hyperintensity on fluid-attenuated inversion recovery mr images in patients without apparent cerebrospinal fluid abnormality18 1.5 T 291 2- 88    - Protein leakage, alteration of vascular haemodynamic and increased blood pool. Hacein-Bey et al. Hyperintense ipsilateral cortical sulci on FLAIR imaging in carotid stenosis: ivy sign equivalent from enlarged leptomeningeal collaterals19 Not stated 1 (case report) 69 - / 1 Slow flow within enlarged leptomeningeal collaterals.  Bozzao et al. Cerebrospinal fluid changes after intravenous injection of gadolinium chelate: assessment by FLAIR MR imaging20 1.5 T 33 - - In pathological conditions with BBB breakdown or neovascularisation, gadolinium can leak in the subarachnoid spaces and cause CSF signal changes. Liu et al. MRI Abnormalities Predominate in the Bottom Part of the Sulcus with Type II Focal Cortical Dysplasia: A Quantitative Study21 3T 58 - 35/23 Cortical FLAIR hyperintensity, which predominate in the bottom part of the sulcus, seen in Type II focal cortical dysplasia.  van Veluw et al. Hippocampal T2 hyperintensities on 7 Tesla MRI22 7T 58 43-78  31/37  Study done in patients with no known neurological disease. Found that hippocampal T2 hyperintensities are extremely common. Stephen et al. Hyperintensity in the Subarachnoid Space on FLAIR MRI23 - (pictorial essay of various conditions) - - - Acute subarachnoid haemorrhage, meningitis, leptomeningeal malignancy, leptomeningeal melanosis, moyamoya disease, elevated Blood Pool to CSF Ratio, IV contrast in context of altered blood-brain barrier or neovascularisation near subarachnoid space/ ventricles, artefacts (supplemental oxygen, CSF pulsation, motion artefact, magnetic susceptibility artefact) Abbreviations: BBB, blood brain barrier; CSF, cerebrospinal fluid; CNS, central nerve system; FLAIR, Fluid-attenuated inversion recovery; PFO Patent Foramen Ovale.    References:  1 Lee H, Kim E, Lee KM, Kim JH, Bae YJ, Choi BS et al. Clinical implications of sulcal enhancement on postcontrast fluid attenuated inversion recovery images in patients with acute stroke symptoms. Korean J Radiol 2015; 16(4): 906–913.  2  Kim EY, Kim SS, Na DG, Roh HG, Ryoo JW, Kim HK. Sulcal hyperintensity on fluid-attenuated inversion recovery imaging in acute ischemic stroke patients treated with intra-arterial thrombolysis: iodinated contrast media as its possible cause and the association with hemorrhagic transformation. J Comput Assist Tomogr 2005; 29(2): 264-9.  3 Noguchi K, Ogawa T, Inugami A, Toyoshima H, Okudera T, Uemura K. MR of acute subarachnoid hemorrhage: a preliminary report of fluid-attenuated inversion-recovery pulse sequences. AJNR Am J Neuroradiol 1994; 15(10): 1940-3.  4  Kidwell CS, Burgess R, Menon R, Warach S, Latour LL. Hyperacute injury marker (HARM) in primary hemorrhage: a distinct form of CNS barrier disruption. Neurology 2011; 77(19): 1725–1728.  5 Oshida S, Akamatsu Y, Matsumoto Y, Ishigame S, Ogasawara Y, Aso K et al. A case of chronic subdural hematoma demonstrating the epileptic focus at the area with sulcal hyperintensity on fluid-attenuated inversion recovery image. Radiol Case Rep. 2019;14(9):1109–1112.  6 Kamran S, Bener AB, Alper D, Bakshi R. Role of fluid-attenuated inversion recovery in the diagnosis of meningitis: comparison with contrast-enhanced magnetic resonance imaging. J Comput Assist Tomogr 2004; 28(1): 68-72.  7 Kuwahara S, Kawada M, Uga S. Cryptococcal meningoencephalitis presenting with an unusual magnetic resonance imaging appearance--case report.. Neurol Med Chir (Tokyo) 2001; 41(10): 517-521.  8 Boban J, Ardalı S, Thurnher MM. Leptomeningeal form of Immunoglobulin G4-related hypertrophic meningitis with perivascular spread: a case report and review of the literature. Neuroradiology 2018; 60(7): 769-773.  9 Kawagoe Y, Nakayama T, Matuzawa S, Fukushima K, Onishi J, Sato Y et al. Epithelial ovarian carcinoma associated with metastases to central nervous system: two case reports. Case Rep Obstet Gynecol 2018  10 Tsuchiya K, Katase S, Yoshino A, Hachiya J. FLAIR MR imaging for diagnosing intracranial meningeal carcinomatosis. American Journal of Roentgenology 2001; 176(6): 1585-1588.   11 Yazdani M, Stalcup ST, Chatterjee AR, Matheus MG. Sulcal FLAIR hyperintensity after CSF removal in two patients with intracranial hypertension. Eur J Radiol Open 2018; 6: 33–35.   12 Anzai Y, Ishikawa M, Shaw DW, Artru A, Yarnykh V, Maravilla KR. Paramagnetic effect of supplemental oxygen on csf hyperintensity on fluid-attenuated inversion recovery mr images. AJNR Am J Neuroradiol 2004; 25(2): 274-279.  13 Frigon C, Jardine DS, Weinberger E, Heckbert SR, Shaw DW.. Fraction of inspired oxygen in relation to cerebrospinal fluid hyperintensity on flair mr imaging of the brain in children and young adults undergoing anesthesia. AJR Am J Roentgenol 2002; 179(3): 791-796.  14 Goetz GF, Hecker H, Haeseler G, Becker H, Münte S. Hyperintense cerebrospinal fluid on flair images induced by ventilation with 100% oxygen. Clinical Neuroradiology 2007; 17(2): 108–115.  15  de Oliveira EP, Tsehmaister-Abitbul V, Kontolemos M, Glikstein R and Torres C. Reversible Sulcal FLAIR Hyperintensity on MRI in a Migraine Patient With Aura. Radiol Case Rep 2020; 15(3): 174–176  16 Gómez-Choco M, Capurro S, Obach V. Migraine With Aura Associated With Reversible Sulcal Hyperintensity in FLAIR. Neurology 2008; 70(24 Pt 2): 2416-8.  17 Kang KW, Kim JT, Chang J, Choi WH, Lim D, Bang DH et al. Transient Sulcal Hyperintensities on Fluid-Attenuated Inversion Recovery in Migraine With Aura: Transient Sulcal Hyperintensities in Migraine. Headache 2012; 52(9): 1430-3  18 Taoka T, Yuh WT, White ML, Quets JP, Maley JE, Ueda T. Sulcal hyperintensity on fluid-attenuated inversion recovery mr images in patients without apparent cerebrospinal fluid abnormality. AJR Am J Roentgenol 2001; 176(2): 519-24.  19 Hacein-Bey L, Mukundan G, Shahi K, Chan H, Tajlil AT. Hyperintense ipsilateral cortical sulci on FLAIR imaging in carotid stenosis: ivy sign equivalent from enlarged leptomeningeal collaterals. Clin Imaging 2014; 38(3): 314-7.  20 Bozzao A, Floris R, Fasoli F, Fantozzi LM, Colonnese C, Simonetti G. Cerebrospinal fluid changes after intravenous injection of gadolinium chelate: assessment by FLAIR MR imaging. Eur Radiol 2003; 13(3): 592-7.  21 Liu Z, Hu W, Sun Z, Wang X, Liu L, Shao X et al. MRI abnormalities predominate in the bottom part of the sulcus with type ii focal cortical dysplasia: a quantitative study. AJNR Am J Neuroradiol 2019; 40(1): 184-190.  22 van Veluw SJ, Wisse LE, Kuijf HJ, Spliet WG, Hendrikse J, Luijten PR at al. Hippocampal T2 hyperintensities on 7 Tesla MRI. Neuroimage Clin 2013; 3: 196–201.  23 Stuckey SL, Goh TD, Heffernan T, Rowan D. Hyperintensity in the subarachnoid space on FLAIR MRI. AJR Am J Roentgenol 2007; 189(4): 913-921.  24 Melhem ER, Jara H, Eustace S. 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The possible causes for sulcal hyperintensities on FLAIR images on brain MRI: the dataset derived from a systematic review

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