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Review

MRI detection of brain abnormality in sickle cell disease

Pages 473-491 | Received 27 Oct 2020, Accepted 18 Feb 2021, Published online: 07 Jun 2021

References

  • Kirkham FJ. Therapy insight: stroke risk and its management in patients with sickle cell disease. Nat Clin Pract Neurol. 2007;3:264–278.
  • DeBaun MR, Kirkham FJ. Central nervous system complications and management in sickle cell disease: a review. Blood. 2016;127:1–39.
  • DeBaun MR, Jordan LC, King AA, et al. American Society of hematology 2020 guidelines for sickle cell disease: prevention, diagnosis, and treatment of cerebrovascular disease in children and adults. Blood Adv. 2020;4:1554–1588.
  • Stotesbury H. Chapter 9 / Stroke and cognitive dysfunction. In: Gladwin MKGNE, editor. Sickle cell disease. 1st ed ed. New York: McGraw-Hill Education; 2021;159–192.
  • Moser FG, Miller ST, Bello JA, et al. The spectrum of brain MR abnormalities in sickle-cell disease: a report from the cooperative study of sickle cell disease. AJNR Am J Neuroradiol. 1996;17:965–972.
  • Vichinsky E, Neumayr L, Gold J. Neuropsychological dysfunction and neuroimaging abnormalities in neurologically intact adults with sickle cell anemia. JAMA. 2010;303:1823–1831.
  • Liem RI, Liu J, Gordon MO, et al. Reproducibility of detecting silent cerebral infarcts in pediatric sickle cell anemia. J Child Neurol. 2014;29:1685–1691.
  • Choudhury NA, DeBaun MR, Rodeghier M, et al. Silent cerebral infarct definitions and full-scale IQ loss in children with sickle cell anemia. Neurology. 2018;90:e239–e246.
  • Thangarajh M, Yang G, Fuchs D, et al. Magnetic resonance angiography-defined intracranial vasculopathy is associated with silent cerebral infarcts and glucose-6-phosphate dehydrogenase mutation in children with sickle cell anaemia. Br J Haematol [Internet]. [cited 2012 Jan 20];159:352–359.
  • Helton KJ, Adams RJ, Kesler KL, et al. Magnetic resonance imaging/angiography and transcranial Doppler velocities in sickle cell anemia: results from the SWiTCH trial. Blood. 2014;124:891–898.
  • Dlamini N, Saunders DE, Bynevelt M, et al. Nocturnal oxyhemoglobin desaturation and arteriopathy in a pediatric sickle cell disease cohort. Neurology. 2017;89:2406–2412.
  • Guilliams KP, Fields ME, Dowling MM. Advances in understanding ischemic stroke physiology and the impact of vasculopathy in children with sickle cell disease. Stroke 2019;50:266–273.
  • Jacob M, Saunders DE, Sangeda RZ, et al. Cerebral infarcts and vasculopathy in Tanzanian children with sickle cell anemia. Pediatr Neurol. 2020;107:64–70.
  • Kawadler JM, Kirkham FJ. Neurological complications and MRI. In: Sickle Cell Disease pain and common chronic complications, ed Baba Inusa. 2016. InTech. 127–152. https://www.intechopen.com/books/sickle-cell-disease-pain-and-common-chronic-complications/neurological-complications-and-mri
  • Jordan LC, DeBaun MR Cerebral hemodynamic assessment and neuroimaging across the lifespan in sickle cell disease [Internet]. J. Cereb. Blood Flow Metab. SAGE Publications Ltd; 2018;38:1438–1448.
  • Stotesbury H, Kawadler JM, Hales PW, et al. Vascular instability and neurological morbidity in sickle cell disease: an integrative framework. Front Neurol. 2019;10:871.
  • Earley CJ, Kittner SJ, Feeser BR, et al. Stroke in children and sickle-cell disease: Baltimore-Washington cooperative young stroke study. Neurology. 1998;51:169–176.
  • Ohene-Frempong K, Weiner SJ, Sleeper LA, et al. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood. 1998;91:288–294.
  • Kossorotoff M, Brousse V, Grevent D, et al. Cerebral haemorrhagic risk in children with sickle-cell disease. Dev Med Child Neurol. 2015;57:187–193.
  • Kirkham F, Angiobi E, Ganesan V. Preventing the recurrence of stroke in children. Expert Rev Neurother. 2021. In prep.
  • Ware RE, Davis BR, Schultz WH, et al. Hydroxycarbamide versus chronic transfusion for maintenance of transcranial doppler flow velocities in children with sickle cell anaemia-TCD with transfusions changing to hydroxyurea (TWiTCH): a multicentre, open-label, phase 3, non-inferiority trial. Lancet. 2016;387:661–670.
  • Kwiatkowski JL, Voeks JH, Kanter J, et al. Ischemic stroke in children and young adults with sickle cell disease in the post-STOP era. Am J Hematol. 2019;94:1335–1343.
  • Hulbert ML, McKinstry RC, Lacey JL, et al. Silent cerebral infarcts occur despite regular blood transfusion therapy after first strokes in children with sickle cell disease. Blood. 2011;117:772–779.
  • Jacob M, Stotesbury H, Kawadler JM, et al. White matter integrity in Tanzanian children with sickle cell anemia. Stroke. 2020;51:1166–1173.
  • Birkeland P, Gardner K, Kesse-Adu R, et al. Intracranial aneurysms in sickle-cell disease are associated with the hemoglobin SS genotype but not with moyamoya syndrome. Stroke. 2016;47:1710–1713.
  • Hamm J, Rathore N, Lee P, et al. Cranial epidural hematomas: a case series and literature review of this rare complication associated with sickle cell disease. Pediatr Blood Cancer. 2017;64:64.
  • Saha B, Saha A. spontaneous epidural hemorrhage in sickle cell disease, Are they all the same? A case report and comprehensive review of the literature. Case Rep Hematol. 2019:8974580.
  • Dowling MM, Noetzel MJ, Rodeghier MJ, et al. Headache and migraine in children with sickle cell disease are associated with lower hemoglobin and higher pain event rates but not silent cerebral infarction. J Pedatr. 2014;164:1175–1180.
  • Solh Z, Taccone MS, Marin S, et al. Neurological presentations in sickle cell patients are not always stroke: a review of posterior reversible encephalopathy syndrome in sickle cell disease. Pediatr Blood Cancer. 2016;63:983–989.
  • Vargas A, Testai FD. Posterior reversible encephalopathy syndrome in adult sickle-cell patients: case series and literature review. J Clin Neurosci. 2019;70:249–250.
  • Quinn CT, McKinstry RC, Dowling MM, et al. Acute silent cerebral ischemic events in children with sickle cell anemia. JAMA Neurol. 2013;70:58–65.
  • Van Der Land V, Mutsaerts HJMM, Engelen M, et al. Risk factor analysis of cerebral white matter hyperintensities in children with sickle cell disease. Br J Haematol. 2016;172:274–284.
  • Cancio MI, Helton KJ, Schreiber JE, et al. Silent cerebral infarcts in very young children with sickle cell anaemia are associated with a higher risk of stroke. Br J Haematol. 2015;171:120–129.
  • Kassim AA, Pruthi S, Day M, et al. Silent cerebral infarcts and cerebral aneurysms are prevalent in adults with sickle cell anemia. Blood. 2016;127:2038–2040.
  • Guilliams KP, Fields ME, Ragan DK, et al. Large-vessel vasculopathy in children with sickle cell disease: a magnetic resonance imaging study of infarct topography and focal atrophy. Pediatric Neurology. 2017;69:49–57.
  • Van Der Land V, Zwanenburg JJM, Fijnvandraat K, et al. Cerebral lesions on 7 tesla MRI in patients with sickle cell anemia. Cerebrovasc Dis. 2015;39:181–189.
  • Kassim AA, Pruthi S, Day M, et al. Silent cerebral infarcts and cerebral aneurysms are prevalent in adults with sickle cell disease. Blood. 2016;127:2038–2040.
  • Dowling MM, Quinn CT, Rogers ZR, et al. Acute silent cerebral infarction in children with sickle cell anemia. Pediatr Blood Cancer. 2010;54:461–464.
  • Kawadler JM, Clayden JD, Clark CA, et al. Intelligence quotient in paediatric sickle cell disease: a systematic review and meta-analysis. Dev Med Child Neurol. 2016;58:672–9.
  • K V P, Jordan LC, Debaun MR, et al. Cognitive function in sickle cell disease across domains, cerebral infarct status, and the lifespan: a meta-analysis. J Pediatr Psychol. 2019;44:1–11.
  • Russell MO, Goldberg HI, Hodson A, et al. Effect of transfusion therapy on arteriographic abnormalities and on recurrence of stroke in sickle cell disease. Blood. 1984;63:162–169.
  • Montanaro M, Colombatti R, Pugliese M, et al. Intellectual function evaluation of first generation immigrant children with sickle cell disease: the role of language and sociodemographic factors. Ital J Pediatr. 2013;39:36.
  • Nottage KA, Ware RE, Aygun B, et al. Hydroxycarbamide treatment and brain MRI/MRA findings in children with sickle cell anaemia. Br J Haematol. 2016;175:331–338.
  • Green NS, Munube D, Bangirana P, et al. Burden of neurological and neurocognitive impairment in pediatric sickle cell anemia in Uganda (BRAIN SAFE): a cross-sectional study. BMC Pediatr. 2019;19:381.
  • Kija EN, Saunders DE, Munubhi E, et al. Transcranial doppler and magnetic resonance in Tanzanian children with sickle cell disease. Stroke. 2019;50:1719–1726.
  • Husson B, Rodesch G, Lasjaunias P, et al. Magnetic resonance angiography in childhood arterial brain infarcts: a comparative study with contrast angiography. Stroke. 2002;33:1280–1285.
  • Kandeei AY, Zimmerman RA, Ohcnc-Frempong K, et al. Comparison of magnetic resonance angiography and conventional angiography in sickle cell disease: clinical significance and reliability. Diagnostic Neuroradiol. Springer-Verlag; 199638:409-16
  • Husson B, Lasjaunias P. Radiological approach to disorders of arterial brain vessels associated with childhood arterial stroke - A comparison between MRA and contrast angiography. Pediatr Radiol. 2004;34:10–15.
  • Kauv P, Gaudré N, Hodel J, et al. Characteristics of moyamoya syndrome in sickle-cell disease by magnetic resonance angiography: an adult-cohort study. Front Neurol. 2019;10:10.
  • Telfer PT, Evanson J, Butler P, et al. Cervical carotid artery disease in sickle cell anemia: clinical and radiological features. Blood. 2011;118:6192–6199.
  • Bernaudin F, Verlhac S, Arnaud C, et al. Chronic and acute anemia and extracranial internal carotid stenosis are risk factors for silent cerebral infarcts in sickle cell anemia. Blood. 2015;125:1653–1661.
  • Buch K, Arya R, Shah B, et al. Quantitative analysis of extracranial arterial tortuosity in patients with sickle cell disease. J Neuroimaging. 2017;27:421–427.
  • Steen RG, Langston JW, Ogg RJ, et al. Ectasia of the basilar artery in children with sickle cell disease: relationship to hematocrit and psychometric measures. J Stroke Cerebrovasc Dis. 1998;7:32–43.
  • Bishop S, Matheus MG, Abboud MR, et al. Effect of chronic transfusion therapy on progression of neurovascular pathology in pediatric patients with sickle cell anemia. Blood Cells Mol Dis. 2011;47:125–128.
  • Abboud MR, Cure J, Granger S, et al. Magnetic resonance angiography in children with sickle cell disease and abnormal transcranial Doppler ultrasonography findings enrolled in the STOP study. Blood. 2004;103:2822–2826.
  • Wang WC, Langston JW, Steen RG, et al. Abnormalities of the central nervous system in very young children with sickle cell anemia. J Pediatr. 1998;132:994–8.
  • Farrell AT, Panepinto J, Carroll CP, et al. End points for sickle cell disease clinical trials: patient-reported outcomes, pain, and the brain [Internet]. Blood Adv. 2019;3:3982–4001. Available from. 2019;3(23):. American Society of Hematology
  • Kaushal M, Byrnes C, Khademian Z, et al. Examination of reticulocytosis among chronically transfused children with sickle cell anemia. PLoS One. 2016;11:e0153244.
  • Choudhury NA, DeBaun MR, Ponisio MR, et al. Intracranial vasculopathy and infarct recurrence in children with sickle cell anaemia, silent cerebral infarcts and normal transcranial Doppler velocities [Internet]. Br J Haematol. 2018;183:324–326.
  • Roa JA, Zanaty M, Osorno-Cruz C, et al. Objective quantification of contrast enhancement of unruptured intracranial aneurysms: a high-resolution vessel wall imaging validation study. J Neurosurg. 2012;Feb 7:1–8.
  • Ahmed SU, Mocco J, Zhang X, et al. MRA versus DSA for the follow-up imaging of intracranial aneurysms treated using endovascular techniques: a meta-analysis. J Neurointerv Surg. 2019;11:1009–1014.
  • Zhu C, Wang X, Eisenmenger L, et al. Surveillance of unruptured intracranial saccular aneurysms using noncontrast 3d-black-blood mRI: comparison of 3D-TOF and contrast-enhanced MRA with 3D-DSA. AJNR Am J Neuroradiol. 2019;40:960–966.
  • Wrede KH, Matsushige T, Goericke SL, et al. Non-enhanced magnetic resonance imaging of unruptured intracranial aneurysms at 7 tesla: comparison with digital subtraction angiography. Eur Radiol. 2017;27:354–364.
  • Winchell AM, Taylor BA, Song R, et al. Evaluation of SWI in children with sickle cell disease. Am J Neuroradiol. 2014;39:1016–1021.
  • Novelli EM, Sarles C, Aizenstein J, et al. Brain venular pattern by 7T MRI correlates with memory and haemoglobin in sickle cell anaemia. Psychiatry Res – Neuroimaging. 2015;233:18–22.
  • Adler K, Reghunathan A, Hutchison LH, et al. Dural venous sinus diameters in children with sickle cell disease: correlation with history of stroke in a case-control study. South Med J. 2016;109:511–515.
  • Ciurea SO, Thulborn KR, Gowhari M. Dural venous sinus thrombosis in a patient with sickle cell disease: case report and literature review. Am J Hematol [Internet]. 2006;81:290–293.
  • Sidani CA, Ballourah W, El Dassouki M, et al. Venous sinus thrombosis leading to stroke in a patient with sickle cell disease on hydroxyurea and high hemoglobin levels: treatment with thrombolysis. Am J Hematol. 2008;83:818–820.
  • Wang MK, Shergill R, Jefkins M, et al. A sickle cell disease patient with dural venous sinus thrombosis: a case report and literature review. Hemoglobin. 2019;43:193–197.
  • Sébire G, Tabarki B, Saunders DE, et al. Cerebral venous sinus thrombosis in children: risk factors, presentation, diagnosis and outcome. Brain. 2005;128:477–489.
  • Choi S, Bush AM, Borzage MT, et al. Hemoglobin and mean platelet volume predicts diffuse T1-MRI white matter volume decrease in sickle cell disease patients. NeuroImage Clin. 2017;15:239–246.
  • Václavů L, Meynart BN, Mutsaerts HJMM, et al. Hemodynamic provocation with acetazolamide shows impaired cerebrovascular reserve in adults with sickle cell disease. Haematologica. 2019;104:690–699.
  • Baldeweg T, Hogan AM, Saunders DE, et al. Detecting white matter injury in sickle cell disease using voxel-based morphometry. Ann Neurol. 2006;59:662–672.
  • Schatz J, Buzan R. Decreased corpus callosum size in sickle cell disease: relationship with cerebral infarcts and cognitive functioning. J Int Neuropsychol Soc 2006;12:24–33.
  • Kawadler JM, Clayden JD, Kirkham FJ, et al. Subcortical and cerebellar volumetric deficits in paediatric sickle cell anaemia. Br J Haematol. 2013;163:373–376.
  • Kirk GR, Haynes MR, Palasis S, et al. Regionally specific cortical thinning in children with sickle cell disease. Cereb Cortex. 2009;19:1549–1556.
  • Kim JA, Leung J, Lerch JP, et al. Reduced cerebrovascular reserve is regionally associated with cortical thickness reductions in children with sickle cell disease. Brain Res. 2016;1642:263–269.
  • Manara R, Dalla Torre A, Lucchetta M, et al. Visual cortex changes in children with sickle cell disease and normal visual acuity: a multimodal magnetic resonance imaging study. Br J Haematol. 2021;192:151–157.
  • Coloigner J, Kim Y, Bush A, et al. Contrasting resting-state fMRI abnormalities from sickle and non-sickle anemia. PLoS One. 2017;12:12.
  • Choi S, O’Neil SH, Joshi AA, et al. Anemia predicts lower white matter volume and cognitive performance in sickle and non-sickle cell anemia syndrome. Am J Hematol. 2019;94:1055–1065.
  • Chen R, Arkuszewski M, Krejza J, et al. A prospective longitudinal brain morphometry study of children with sickle cell disease. Am J Neuroradiol. 2015;36:403–410.
  • Kawadler JM, Clark CA, McKinstry RC, et al. Brain atrophy in paediatric sickle cell anaemia: findings from the silent infarct transfusion (SIT) trial. Br J Haematol. 2017 Apr;177(1):151–153.
  • Darbari DS, Eigbire-Molen O, Ponisio MR, et al. Progressive loss of brain volume in children with sickle cell anemia and silent cerebral infarct: a report from the silent cerebral infarct transfusion trial. Am J Hematol. 2018;93:E406–E408.
  • Mackin RS, Insel P, Truran D, et al. Neuroimaging abnormalities in adults with sickle cell anemia: associations with cognition. Neurology [Internet]. 2014;82:835–841.
  • Cahill LS, Gazdzinski LM, Tsui AK, et al. Functional and anatomical evidence of cerebral tissue hypoxia in young sickle cell anemia mice. J Cereb Blood Flow Metab. 2017;37:994–1005.
  • Wang L, Almeida LEF, De Souza Batista CM, et al. Cognitive and behavior deficits in sickle cell mice are associated with profound neuropathologic changes in hippocampus and cerebellum. Neurobiol Dis. 2016;85:60–72.
  • Deoni SCL, Dean DC, Remer J, et al. Cortical maturation and myelination in healthy toddlers and young children. Neuroimage. 2015;115:147–161.
  • Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci. 2005;9:60–68.
  • Yeatman JD, Wandell BA, Mezer AA. Lifespan maturation and degeneration of human brain white matter. Nat Commun. 2014;5:4932.
  • Walhovd KB, Fjell AM, Reinvang I, et al. Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging. 2005;26:1261–1270. .
  • Somerville LH. Searching for signatures of brain maturity: what are we searching for? Neuron. 2016;92:1164–1167.
  • Chen R, Krejza J, Arkuszewski M, Zimmerman RA, Herskovits EH, Melhem ER Brain morphometric analysis predicts decline of intelligence quotient in children with sickle cell disease: A preliminary study. Adv Med Sci. 2017 Mar;62:151–157.
  • Kawadler JM, Kirkham FJ, Clayden JD, et al. White matter damage relates to oxygen saturation in children with sickle cell anemia without silent cerebral infarcts. Stroke. 2015;46:1793–1799.
  • Stotesbury H, Kirkham FJ, Kölbel M, et al. White matter integrity and processing speed in sickle cell anemia. Neurology. 2018;90:e2042–e2050.
  • Chai Y, Ji C, Coloigner J, et al. Tract‐specific analysis and neurocognitive functioning in sickle cell patients without history of overt stroke. Brain Behav. 2021;11(3):e01978.
  • Howard J, Slee AE, Skene S. et al. Overnight auto-adjusting continuous airway pressure+standard care compared with standard care alone in the prevention of morbidity in sickle cell disease phase II (POMS2b): study protocol for a randomised controlled trial. Trials. 2018;19:55.
  • Kapustin D, Leung J, Odame I, et al. Hydroxycarbamide treatment in children with sickle cell anaemia is associated with more intact white matter integrity: a quantitative MRI study. Br J Haematol. 2019;187:238–245.
  • Wasserthal J, Neher P, Maier-Hein KH. TractSeg – Fast and accurate white matter tract segmentation. Neuroimage. 2018;183:239–253.
  • Raffelt DA, Tournier JD, Smith RE, et al. Investigating white matter fibre density and morphology using fixel-based analysis. Neuroimage. 2017;144:58–73.
  • Veraart J, Poot DHJ, Van Hecke W, et al. More accurate estimation of diffusion tensor parameters using diffusion kurtosis imaging. Magn Reson Med. 2011;65:138–145.
  • Miao X, Choi S, Tamrazi B, et al. Increased brain iron deposition in patients with sickle cell disease: an MRI quantitative susceptibility mapping study [Internet]. Blood. 2018;132:1618–1621.
  • Kirkham FJ, Shmueli K. Brain iron in sickle cell disease? [Internet]. Blood. American Society of Hematology. 2018;132:1550–1552.
  • Zempsky WT, Stevens MC, Santanelli JP, et al. Altered functional connectivity in sickle cell disease exists at rest and during acute pain challenge. Clin J Pain. 2017;33:1060–1070.
  • Colombatti R, Lucchetta M, Montanaro M, et al. Cognition and the default mode network in children with sickle cell disease: a resting state functional MRI study. PLoS One. 2016;11:e0157090.
  • Darbari DS, Hampson JP, Ichesco E, et al. Frequency of hospitalizations for pain and association with altered brain network connectivity in sickle cell disease. J Pain. 2015;16:1077–1086.
  • Case M, Zhang H, Mundahl J, et al. NeuroImage: clinical characterization of functional brain activity and connectivity using EEG and fMRI in patients with sickle cell disease. NeuroImage Clin. 2017;14:1–17.
  • Coloigner J, Phlypo R, Coates TD, et al. Graph Lasso-based test for evaluating functional brain connectivity in sickle cell disease. Brain Connect. 2017;7:443–53.
  • Bhatt RR, Zeltzer LK, Coloigner J, et al. Patients with sickle-cell disease exhibit greater functional connectivity and centrality in the locus coeruleus compared to anemic controls. NeuroImage Clin. 2019;21:101686.
  • Sun B, Brown R, Burns T, et al. Differences in activation and deactivation in children with sickle cell disease compared with demographically matched controls. Pediatrics. 2017;38:1242–1247.
  • Karafin MS, Chen G, Wandersee NJ, et al. Chronic pain in adults with sickle cell disease is associated with alterations in functional connectivity of the brain. PLoS One. 2019;14:e0216994.
  • Kawadler JM, Slee A, Stotesbury H, et al. Index of pain experience in sickle cell anaemia (IPESCA): development from daily pain diaries and initial findings from use with children and adults with sickle cell anaemia. Br J Haematol. 2019;186:360–363.
  • Brandow AM, Farley RA, Panepinto JA. Neuropathic pain in patients with sickle cell disease. Pediatr Blood Cancer. 2014;61:512–517.
  • Zempsky WT, Wakefield EO, Santanelli JP, et al. Widespread pain among youth with sickle cell disease hospitalized with vasoocclusive pain. Clin J Pain. 2017;33:335–339.
  • Zou P, Helton KJ, Smeltzer M, et al. Hemodynamic responses to visual stimulation in children with sickle cell anemia. Brain Imaging Behav. 2012;5:295–306.
  • Prohovnik I, Pavlakis SG, Piomelli S, et al. Cerebral hyperemia, stroke, and transfusion in sickle cell disease. Neurology 1989;39:344–348. .
  • Helton KJ, Paydar A, Glass J, et al. Arterial spin-labeled perfusion combined with segmentation techniques to evaluate cerebral blood flow in white and gray matter of children with sickle cell anemia. Pediatr Blood Cancer. 2009;52:85–91.
  • Juttukonda MR, Lee CA, Patel NJ, et al. Differential cerebral hemometabolic responses to blood transfusions in adults and children with sickle cell anemia. J Magn Reson Imaging. 2019;49:466–477.
  • Jordan LC, Juttukonda MR, Kassim AA, et al. Haploidentical bone marrow transplantation improves cerebral hemodynamics in adults with sickle cell disease [Internet]. Am J Hematol. 2019;94:E155–E158.
  • Whitehead MT, Smitthimedhin A, Webb J, et al. Cerebral blood flow and marrow diffusion alterations in children with sickle cell anemia after bone marrow transplantation and transfusion. Am J Neuroradiol. 2018;39:2126–2131.
  • Strouse JJ, Cox CS, Melhem ER, et al. Inverse correlation between cerebral blood flow measured by continuous arterial spin-labeling (CASL) MRI and neurocognitive function in children with sickle cell anemia (SCA). Blood. 2006;108:379–381.
  • Kirkham FJ, Calamante F, Bynevelt M, et al. Perfusion magnetic resonance abnormalities in patients with sickle cell disease. Ann Neurol. 2001;49:477–485.
  • Hurlet-Jensen AM, Prohovnik I, Pavlakis SG, et al. Effects of total hemoglobin and hemoglobin s concentration on cerebral blood flow during transfusion therapy to prevent stroke in sickle cell disease. Stroke. 1994;25:1688–1692.
  • Behpour AM, Shah PS, Mikulis DJ, et al. Cerebral blood flow abnormalities in children with sickle cell disease: a systematic review. Pediatr Neurol. 2013;48:188–199..
  • Grueneich R, Ris MD, Ball W, et al. Relationship of structural magnetic resonance imaging, magnetic resonance perfusion, and other disease factors to neuropsychological outcome in sickle cell disease. J Pediatr Psychol. 2004;29:83–92.
  • Gevers S, Nederveen AJ, Fijnvandraat K, et al. Arterial spin labeling measurement of cerebral perfusion in children with sickle cell disease. J Magn Reson Imaging. 2012;35:779–787.
  • Oguz KK, Golay X, Pizzini FB, et al. Sickle cell disease: continuous arterial spin-labeling perfusion MR imaging in children. Radiology. 2003;227:567–574.
  • Václavů L, Petr J, Petersen ET, et al. Cerebral oxygen metabolism in adults with sickle cell disease. Am J Hematol. 2020;95:401–412.
  • Van Den Tweel XW, Nederveen AJ, Majoie CBLM, et al. Cerebral blood flow measurement in children with sickle cell disease using continuous arterial spin labeling at 3.0-Tesla MRI. Stroke. 2009;40:795–800.
  • Fields ME, Guilliams KP, Ragan D, et al. Elevations in MR measurements of whole brain and regional cerebral blood flow and oxygen extraction fraction suggest cerebral metabolic stress in children with sickle cell disease unaffected by overt stroke. Blood. 2015;126.
  • Fields ME, Guilliams KP, Ragan DK, et al. Regional oxygen extraction predicts border zone vulnerability to stroke in sickle cell disease. Neurology. 2018;90:e1134–e1144.
  • Chai Y, Bush AM, Coloigner J, et al. White matter has impaired resting oxygen delivery in sickle cell patients. Am J Hematol. 2019;94:467–474.
  • Arkuszewski M, Krejza J, Chen R, et al. Sickle cell disease: reference values and interhemispheric differences of nonimaging transcranial Doppler blood flow parameters. AJNR Am J Neuroradiol [Internet]. 2011;32:1444–1450.
  • Hales PW, Kawadler JM, Aylett SE, et al. Arterial spin labeling characterization of cerebral perfusion during normal maturation from late childhood into adulthood: normal ‘reference range’ values and their use in clinical studies. J Cereb Blood Flow & Metab. 2014;34:776–784.
  • Václavů L, Van Der Land V, Heijtel D, et al. In vivo T1 of blood measurements in children with sickle cell disease improve cerebral blood flow quantification from arterial spin-labeling MRI. Am J Neuroradiol. 2016;37:1727–32.
  • Juttukonda MR, Jordan LC, Gindville MC, et al. Cerebral hemodynamics and pseudo-continuous arterial spin labeling considerations in adults with sickle cell anemia. NMR Biomed. 2017;30:1–9.
  • Bush A, Chai Y, Choi SY, et al. Pseudo continuous arterial spin labeling quantification in anemic subjects with hyperemic cerebral blood flow. Magn Reson Imaging. 2018;47:137–146.
  • Kawadler JM, Hales PW, Barker S, et al. Cerebral perfusion characteristics show differences in younger versus older children with sickle cell anaemia: results from a multiple-inflow-time arterial spin labelling study. NMR Biomed. 2018;31:1–11.
  • Kosinski PD, Croal PL, Leung J, et al. The severity of anaemia depletes cerebrovascular dilatory reserve in children with sickle cell disease: a quantitative magnetic resonance imaging study. Br J Haematol. 2017;176:280–287.
  • Dowling MM, Kirkham FJ. Stroke in sickle cell anaemia is more than stenosis and thrombosis: the role of anaemia and hyperemia in ischaemia. Haematol. 2016;176:151–153.
  • Gupta A, Chazen JL, Hartman M, et al. Cerebrovascular reserve and stroke risk in patients with carotid stenosis or occlusion: a systematic review and meta-analysis. Strok. 2012;43:2884–2891.
  • Lu H, Xu F, Grgac K, et al. Calibration and validation of TRUST MRI for the estimation of cerebral blood oxygenation. Magn Reson Med. 2012;67:42–49.
  • Jordan LC, Gindville MC, Scott AO, et al. Non-invasive imaging of oxygen extraction fraction in adults with sickle cell anaemia. Brain [Internet]. 2016;139:738–750.
  • Bush A, Borzage M, Detterich J, et al. Empirical model of human blood transverse relaxation at 3 T improves MRI T2 oximetry. Magn Reson Med. 2017;77:2364–2371.
  • Watchmaker JM, Juttukonda MR, Davis LT, et al. Hemodynamic mechanisms underlying elevated oxygen extraction fraction (OEF) in moyamoya and sickle cell anemia patients. J Cereb Blood Flow Metab. 2018;38:1618–1630.
  • Bush AM, Coates TD, Wood JC. Diminished cerebral oxygen extraction and metabolic rate in sickle cell disease using T2 relaxation under spin tagging MRI. Magn Reson Med. 2017;80:294–303.
  • Li W, Xu X, Liu P, et al. Quantification of whole-brain oxygenation extraction fraction and cerebral metabolic rate of oxygen consumption in adults with sickle cell anemia using individual T2-based oxygenation calibrations. Magn Reson Med. 2020;83:1066–1080.
  • Guilliams KP, Fields ME, Ragan DK, et al. Red cell exchange transfusions lower cerebral blood flow and oxygen extraction fraction in pediatric sickle cell anemia. Blood. 2018;131:1012–1021.
  • Fields ME, Guilliams KP, Ragan D, et al. Hydroxyurea reduces cerebral metabolic stress in patients with sickle cell anemia [Internet]. 2019;133:2436–2444.
  • Croal PL, Leung J, Phillips CL, et al. Quantification of pathophysiological alterations in venous oxygen saturation: a comparison of global MR susceptometry techniques. Magn Reson Imaging. 2019;58:18–23.
  • Derdeyn CP, Videen TO, Grubb RL, et al. Comparison of PET oxygen extraction fraction methods for the prediction of stroke risk. J Nucl Med [Internet]. 2001;42:1195–1197.