Portable, bedside, low-field magnetic resonance imaging for evaluation of intracerebral hemorrhage

Mercy H Mazurek, Bradley A Cahn, Matthew M Yuen, Anjali M Prabhat, Isha R Chavva, Jill T Shah, Anna L Crawford, E Brian Welch, Jonathan Rothberg, Laura Sacolick, Michael Poole, Charles Wira, Charles C Matouk, Adrienne Ward, Nona Timario, Audrey Leasure, Rachel Beekman, Teng J Peng, Jens Witsch, Joseph P Antonios, Guido J Falcone, Kevin T Gobeske, Nils Petersen, Joseph Schindler, Lauren Sansing, Emily J Gilmore, David Y Hwang, Jennifer A Kim, Ajay Malhotra, Gordon Sze, Matthew S Rosen, W Taylor Kimberly, Kevin N Sheth, Mercy H Mazurek, Bradley A Cahn, Matthew M Yuen, Anjali M Prabhat, Isha R Chavva, Jill T Shah, Anna L Crawford, E Brian Welch, Jonathan Rothberg, Laura Sacolick, Michael Poole, Charles Wira, Charles C Matouk, Adrienne Ward, Nona Timario, Audrey Leasure, Rachel Beekman, Teng J Peng, Jens Witsch, Joseph P Antonios, Guido J Falcone, Kevin T Gobeske, Nils Petersen, Joseph Schindler, Lauren Sansing, Emily J Gilmore, David Y Hwang, Jennifer A Kim, Ajay Malhotra, Gordon Sze, Matthew S Rosen, W Taylor Kimberly, Kevin N Sheth

Abstract

Radiological examination of the brain is a critical determinant of stroke care pathways. Accessible neuroimaging is essential to detect the presence of intracerebral hemorrhage (ICH). Conventional magnetic resonance imaging (MRI) operates at high magnetic field strength (1.5-3 T), which requires an access-controlled environment, rendering MRI often inaccessible. We demonstrate the use of a low-field MRI (0.064 T) for ICH evaluation. Patients were imaged using conventional neuroimaging (non-contrast computerized tomography (CT) or 1.5/3 T MRI) and portable MRI (pMRI) at Yale New Haven Hospital from July 2018 to November 2020. Two board-certified neuroradiologists evaluated a total of 144 pMRI examinations (56 ICH, 48 acute ischemic stroke, 40 healthy controls) and one ICH imaging core lab researcher reviewed the cases of disagreement. Raters correctly detected ICH in 45 of 56 cases (80.4% sensitivity, 95%CI: [0.68-0.90]). Blood-negative cases were correctly identified in 85 of 88 cases (96.6% specificity, 95%CI: [0.90-0.99]). Manually segmented hematoma volumes and ABC/2 estimated volumes on pMRI correlate with conventional imaging volumes (ICC = 0.955, p = 1.69e-30 and ICC = 0.875, p = 1.66e-8, respectively). Hematoma volumes measured on pMRI correlate with NIH stroke scale (NIHSS) and clinical outcome (mRS) at discharge for manual and ABC/2 volumes. Low-field pMRI may be useful in bringing advanced MRI technology to resource-limited settings.

Conflict of interest statement

K.N.S. is the principal investigator. This study received support from the Collaborative Science Award from the American Heart Association (PIs: K.N.S., W.T.K., M.S.R.), National Institutes of Health Supplement Grant, and Hyperfine Research, Inc. research grant. W.T.K. receives grants from NIH and AHA; grants and personal fees from Biogen, Inc; grants and personal fees from NControl Therapeutics; has a patent pending that is licensed to NControl Therapeutics; holds equity in Woolsey Pharmaceuticals. M.S.R. is a co-founder of Hyperfine Research, Inc. J.R. is a co-founder of Hyperfine Research, Inc. E.B.W., L.S., and M.P. are research scientists and engineers at Hyperfine Research, Inc. All other authors declare no competing interests.

© 2021. The Author(s).

Figures

Fig. 1. Portable (0.064T) magnetic resonance imaging…
Fig. 1. Portable (0.064T) magnetic resonance imaging device dimensions.
a The portable MRI (pMRI) device has a height of 140 cm and a width of 86 cm. The critical 5 Gauss (0.5 mT) boundary around the scanner extends into a circle with a diameter of 158 cm. b The pMRI device is positioned at the head of the patient’s hospital bed. The scanner bridge (35 cm) adjoins the hospital bed with the pMRI device and the patient’s chest height and head and neck lengths are positioned within the vertical clearance between magnets (32 cm) and the head coil length (26 cm), respectively. c The patient’s head is positioned within the single channel transmit, 8-channel receiver head coil (26 × 20 cm) and the RF shield is closed for scan acquisition, which creates a horizontal clearance of 55 cm.
Fig. 2. Intracerebral hemorrhage at 0.064T versus…
Fig. 2. Intracerebral hemorrhage at 0.064T versus conventional imaging modalities (CT or 3T MRI).
The first and second columns are low-field FLAIR and T2W images, respectively. The third column is a gold-standard clinical examination for comparison (3T MRI: a3, b3, c3, and e3; CT: d3). a Left isointense fronto-parietal intracerebral hemorrhage (ICH) with hyperintense rim and bilateral frontal hematomas. b Bilateral isointense cerebellar ICH with hyperintense rim. c Left hypointense occipital lobe ICH with hyperintense rim. d Left homogenous, hyperintense ICH in corpus collosum. e Left hypointense temporal ICH with hyperintense rim.
Fig. 3. False negative intracerebral hemorrhage cases.
Fig. 3. False negative intracerebral hemorrhage cases.
The first and second columns are low-field FLAIR and T2W images, respectively. The third column is a gold-standard clinical examination for comparison. (3T MRI: b3, d3, and e3; CT: a3). a Right cerebellar pontine intracerebral hemorrhage (ICH). Missed by all raters. b Left temporal ICH. Missed by all raters. c Bilateral cerebellar ICH. Missed by 2/3 raters. d Left cerebellum ICH. Missed by all raters. e Left thalamus ICH. Missed by all raters.
Fig. 4. Hematoma volume measurements on portable…
Fig. 4. Hematoma volume measurements on portable MRI.
a1 Validation of manually segmented pMRI hematoma volumes against manual volumes on conventional (CT or 1.5/3T MRI) imaging (T2W (n = 37): r = 0.952, 95% CI: [0.907–0.975], p < 2.20e-16; FLAIR (n = 38): r = 0.899, 95% CI: [0.812–0.946], p = 1.90e-14). Bland-Altman plots for manual pMRI showed a bias of −1.70 cc [limits of agreement (LOA): −11.8–8.42] for (a2) T2W sequences (n = 37) and a bias of −1.22 cc [LOA: −20.8–18.4] for (a3) FLAIR (n = 38). b1 Validation of averaged ABC/2 estimated pMRI volumes against averaged estimated volumes on conventional (CT or 1.5/3T MRI) imaging (T2W (n = 40): r = 0.945, 95% CI: [0.892–0.972], p < 2.20e-16; FLAIR (n = 38): r = 0.835, 95% CI: [0.702–0.911], p = 7.53e-11). Bland–Altman plots for ABC/2 pMRI showed a bias of −3.74 cc [LOA: −20.2–12.7] for (b2) T2W (n = 40) and a bias of −7.89 [LOA: −38.0–22.2] for (b3) FLAIR (n = 38). c1 Manually segmented pMRI hematoma volumes against averaged estimated volumes using ABC/2 (T2W (n = 37): r = 0.977, 95% CI: [0.956–0.989], p < 2.20e-16; FLAIR (n = 38): r = 0.968, 95% CI: [0.936–0.984], p < 2.20e-16). Bland–Altman plots showed a bias of 1.962 [LOA: −5.76–9.68] for (c2) T2W (n = 37) and a bias of 1.79 [LOA: −4.46–8.04] for (c3) FLAIR (n = 38). Pearson correlations are reported for a1, b1, and c1 with confidence intervals. Line of identity shown in red (a1, b1). 95% confidence intervals are represented by bands (a1, b1, c1) and dashed gray lines (a2–3, b2–3, c2–3).
Fig. 5. Hematoma volume and cognitive scores…
Fig. 5. Hematoma volume and cognitive scores on portable MRI.
Manual pMRI hematoma volume versus (a1) cognitive status (NIHSS) at time of exam (pMRI T2W (n = 33): ρ = 0.750, 95% CI: [0.591–0.906], p = 4.95e-7; pMRI FLAIR (n = 34): ρ = 0.802, 95% CI: [0.669–0.930], p = 1.23e-8) and a2 functional status (mRS) at discharge (pMRI T2W (n = 36): ρ = 0.589, 95% CI: [0.372–0.804], p = 1.55e-4; pMRI FLAIR (n = 37): ρ = 0.641, 95% CI: [0.425–0.855], p = 1.89e-5). Averaged ABC/2 estimated pMRI hematoma volume versus (b1) cognitive status (NIHSS) at time of exam (pMRI T2W (n = 36): ρ = 0.805, 95% CI: [0.659–0.948], p = 3.18e-9; pMRI FLAIR (n = 34): ρ = 0.776, 95% CI: [0.617–0.930], p = 7.16e-8) and (b2) functional status (mRS) at discharge (pMRI T2W (n = 39): ρ = 0.747, 95% CI: [0.592–0.899], p = 4.85e-8; pMRI FLAIR (n = 37): ρ = 0.669, 95% CI: [0.483–0.853], p = 5.98e-6). Spearman correlations are reported for a1, a2, b1, and b2 with confidence intervals. Bands represent 95% confidence intervals.

References

    1. Kernan WN, et al. Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2014;45:2160–2236. doi: 10.1161/STR.0000000000000024.
    1. Saver JL. Time is brain—quantified. Stroke. 2006;37:263–266. doi: 10.1161/01.STR.0000196957.55928.ab.
    1. Campbell BC, Parsons MW. Imaging selection for acute stroke intervention. Int. J. Stroke. 2018;08:554–567. doi: 10.1177/1747493018765235.
    1. Morgan CD, et al. Physiologic imaging in acute stroke: patient selection. Interv. Neuroradiol. 2015;21:499–510. doi: 10.1177/1591019915587227.
    1. Powers WJ, et al. Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: A Guideline for Healthcare Professionals From the American Heart Association/American Stroke Association. Stroke. 2019;50:e344–e418. doi: 10.1161/STROKEAHA.118.022606.
    1. Macellari F, Paciaroni M, Agnelli G, Caso V. Neuroimaging in intracerebral hemorrhage. Stroke. 2014;45:903–908. doi: 10.1161/STROKEAHA.113.003701.
    1. Siddiqui FM, Bekker SV, Qureshi AI. Neuroimaging of hemorrhage and vascular defects. Neurotherapeutics. 2011;8:28–38. doi: 10.1007/s13311-010-0009-x.
    1. Christensen AF, Christensen H. Editorial: imaging in acute stroke-new options and state of the art. Front. Neurol. 2017;8:736. doi: 10.3389/fneur.2017.00736.
    1. Kidwell CS, et al. Comparison of MRI and CT for detection of acute intracerebral hemorrhage. JAMA. 2004;292:1823–1830. doi: 10.1001/jama.292.15.1823.
    1. Fiebach JB, et al. Stroke magnetic resonance imaging is accurate in hyperacute intracerebral hemorrhage: a multicenter study on the validity of stroke imaging. Stroke. 2004;35:502–506. doi: 10.1161/01.STR.0000114203.75678.88.
    1. Piliszek A, et al. Comprehensive imaging of stroke—Looking for the gold standard. Neurol. Neurochir. Pol. 2016;50:241–250. doi: 10.1016/j.pjnns.2016.04.009.
    1. Bevers MB, et al. Apparent diffusion coefficient signal intensity ratio predicts the effect of revascularization on ischemic cerebral edema. Cerebrovasc. Dis. 2018;45:93–100. doi: 10.1159/000487406.
    1. Kelly PJ, Hedley-Whyte ET, Primavera J, He J, Gonzalez RG. Diffusion MRI in ischemic stroke compared to pathologically verified infarction. Neurology. 2001;56:914–920. doi: 10.1212/WNL.56.7.914.
    1. Thomalla G, et al. A multicenter, randomized, double-blind, placebo-controlled trial to test efficacy and safety of magnetic resonance imaging-based thrombolysis in wake-up stroke (WAKE-UP) Int J. Stroke. 2014;9:829–836. doi: 10.1111/ijs.12011.
    1. Chalela JA, et al. Magnetic resonance imaging and computed tomography in emergency assessment of patients with suspected acute stroke: a prospective comparison. Lancet. 2007;369:293–298. doi: 10.1016/S0140-6736(07)60151-2.
    1. Shah S, et al. Screening with MRI for accurate and rapid stroke treatment: SMART. Neurology. 2015;84:2438–2444. doi: 10.1212/WNL.0000000000001678.
    1. Lansberg MG, Albers GW, Beaulieu C, Marks MP. Comparison of diffusion-weighted MRI and CT in acute stroke. Neurology. 2000;54:1557–1561. doi: 10.1212/WNL.54.8.1557.
    1. Fiebach JB, et al. CT and diffusion-weighted MR imaging in randomized order: diffusion-weighted imaging results in higher accuracy and lower interrater variability in the diagnosis of hyperacute ischemic stroke. Stroke. 2002;33:2206–2210. doi: 10.1161/01.STR.0000026864.20339.CB.
    1. Power SP, et al. Computed tomography and patient risk: Facts, perceptions and uncertainties. World J. Radiol. 2016;8:902–915. doi: 10.4329/wjr.v8.i12.902.
    1. Moser JB, et al. Radiation dose-reduction strategies in thoracic CT. Clin. Radiol. 2017;72:407–420. doi: 10.1016/j.crad.2016.11.021.
    1. Goldman AR, Maldijn PD. Reducing radiation dose in body CT: a practical approach to optimizing CT protocols. Am. J. Roentgenol. 2013;200:741–747. doi: 10.2214/AJR.12.10330.
    1. Cihngiroglu M, Ramsey RG, Dohrmann GJ. Brain injury: Analysis of imaging modalities. Neurol. Res. 2002;24:7–18. doi: 10.1179/016164102101199440.
    1. Algethamy HM, et al. Added value of MRI over CT of the brain in intensive care unit patients. Can. J. Neurol. Sci. 2015;42:324–332. doi: 10.1017/cjn.2015.52.
    1. Zimmerman RA, et al. Head injury: early results of comparing CT and high-field MR. Am. J. Roentgenol. 1986;147:1215–1222. doi: 10.2214/ajr.147.6.1215.
    1. Bhat S. S., et al. Low-field MRI of stroke: challenges and opportunities. J. Magn. Reson. Imaging. 10.1002/jmri.27324 (2020).
    1. An SJ, Kim TJ, Yoon BW. Epidemiology, risk factors, and clinical features of intracerebral hemorrhage: an update. J. Stroke. 2017;19:3–10. doi: 10.5853/jos.2016.00864.
    1. Sarracanie M, et al. Low-cost high-performance MRI. Sci. Rep. 2015;5:15177. doi: 10.1038/srep15177.
    1. Agrawal S, Hulme SL, Hayward R, Brierley J. A portable CT scanner in the pediatric intensive care unit decreases transfer-associated adverse events and staff disruption. Eur. J. Trauma Emerg. Surg. 2010;36:346–352. doi: 10.1007/s00068-009-9127-8.
    1. Peace K, et al. Portable head CT scan and its effect on intracranial pressure, cerebral perfusion pressure, and brain oxygen. J. Neurosurg. 2011;114:1479–1484. doi: 10.3171/2010.11.JNS091148.
    1. Peace K, et al. The use of a portable head CT scanner in the intensive care unit. J. Neurosci. Nurs. 2010;42:109–116. doi: 10.1097/JNN.0b013e3181ce5c5b.
    1. Moser E, et al. 7-T MR – from research to clinical applications? NMR Biomed. 2012;25:695–716. doi: 10.1002/nbm.1794.
    1. Hricak H, et al. Managing radiation use in medical imaging: a multifaceted challenge. Radiology. 2011;258:889–905. doi: 10.1148/radiol.10101157.
    1. Marques JP, Simonis FFJ, Webb AG, Low-field MRI, An MR. physics perspective. J. Magn. Reson. Imaging. 2019;49:1528–1542. doi: 10.1002/jmri.26637.
    1. Geethanath S, Vaughan JT. Accessible magnetic resonance imaging: a review. J. Magn. Reson. Imaging. 2019;49:e65–e77. doi: 10.1002/jmri.26638.
    1. Lovell MA, Mudaliar MY, Klineberg PL. Intrahospital transport of critically ill patients: complications and difficulties. Anaesth. Intensive Care. 2001;29:400–405. doi: 10.1177/0310057X0102900412.
    1. Rumboldt Z, Huda W, All JW. Review of portable CT with assessment of a dedicated head CT scanner. Am. J. Neuroradiol. 2009;30:1630–1636. doi: 10.3174/ajnr.A1603.
    1. Lother S, Schiff SJ, Neuberger T, Jakob PM, Fidler F. Design of a mobile, homogeneous, and efficient electromagnet with a large field of view for neonatal low-field MRI. MAGMA. 2016;29:691–698. doi: 10.1007/s10334-016-0525-8.
    1. Cooley C. Z., et al. A portable scanner for magnetic resonance imaging of the brain. Nat. Biomed. Eng. 10.1038/s41551-020-00641-5 (2020).
    1. Kraus R., et al. Ultra-low-field Nuclear Magnetic Resonance: A New MRI Regime (Oxford University Press, 2014). 10.1093/med/9780199796434.001.0001
    1. Campbell-Washburn AE, et al. Opportunities in interventional and diagnostic imaging by using high-performance low-field-strength MRI. Radiology. 2019;293:384–393. doi: 10.1148/radiol.2019190452.
    1. Klein H.-M. Clinical Low Field Strength Magnetic Resonance Imaging: A Practical Guide To Accessible MRI. p. 156 (Springer, 2016).
    1. Brott T, et al. Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke. 1997;28:1–5. doi: 10.1161/01.STR.28.1.1.
    1. Grysiewicz RA, Thomas K, Pandey DK. Epidemiology of ischemic and hemorrhagic stroke: incidence, prevalence, mortality, and risk factors. Neurol. Clin. 2008;26:871–895. doi: 10.1016/j.ncl.2008.07.003.
    1. Kothari RU, et al. The ABCs of measuring intracerebral hemorrhage volumes. Stroke. 1996;27:1304–1305. doi: 10.1161/01.STR.27.8.1304.
    1. Webb AJ, et al. Accuracy of the ABC/2 score for intracerebral hemorrhage: systematic review and analysis of MISTIE, CLEAR-IVH, and CLEAR III. Stroke. 2015;46:2470–2476. doi: 10.1161/STROKEAHA.114.007343.
    1. Broderick JP, et al. Volume of intracerebral hemorrhage: a powerful and easy-to-use predictor of 30-day mortality. Stroke. 1993;24:987–993. doi: 10.1161/01.STR.24.7.987.
    1. Gunnarsson T, et al. Mobile computerized tomography scanning in the neurosurgery intensive care unit: increase in patient safety and reduction of staff workload. J. Neurosurg. 2000;93:432–436. doi: 10.3171/jns.2000.93.3.0432.
    1. Waydhas C. Intrahospital transport of critically ill patients. Crit. Care. 1999;3:R83–R89. doi: 10.1186/cc362.
    1. Butler WE, et al. A mobile computed tomographic scanner with intraoperative and intensive care unit applications. Neurosurgery. 1998;42:1304–1310. doi: 10.1097/00006123-199806000-00064.
    1. Matson MB, et al. Evaluation of head examinations produced with a mobile CT unit. Br. J. Radiol. 1999;72:631–636. doi: 10.1259/bjr.72.859.10624318.
    1. McCunn M, et al. Physician utilization of a portable computed tomography scanner in the intensive care unit. Crit. Care Med. 2000;28:3808–3813. doi: 10.1097/00003246-200012000-00008.
    1. LaRovere KL, et al. Head computed tomography scanning during pediatric neurocritical care: diagnostic yield and the utility of portable studies. Neurocrit. Care. 2011;16:251–257. doi: 10.1007/s12028-011-9627-3.
    1. Sheth KN, et al. Assessment of brain injury using portable, low-field magnetic resonance imaging at the bedside of critically ill patients. JAMA Neurol. 2020;78:41–47. doi: 10.1001/jamaneurol.2020.3263.
    1. Luney MS, et al. Acute posterior cranial fossa hemorrhage–Is surgical decompression better than expectant medical management? Neurocrit. Care. 2016;25:365–370. doi: 10.1007/s12028-015-0217-7.
    1. Zhu B, Liu JZ, Cauley SF, Rosen BR, Rosen MS. Image reconstruction by domain-transform manifold learning. Nature. 2018;555:487–492. doi: 10.1038/nature25988.
    1. Sorensen AG, et al. Hyperacute stroke: evaluation with combined multisection diffusion-weighted and hemodynamically weighted echo-planar MR imaging. Radiology. 1996;199:391–401. doi: 10.1148/radiology.199.2.8668784.
    1. Schellinger PD, Jansen O, Fiebach JB, Hacke W, Sartor K. A standardized MRI stroke protocol: comparison with CT in hyperacute intracerebral hemorrhage. Stroke. 1999;30:765–768. doi: 10.1161/01.STR.30.4.765.
    1. U. S. Food and Drug Administration. Enforcement Policy For Imaging Systems During The Coronavirus Disease 2019 (COVID-19) Public Health Emergency: Guidance For Industry And Food And Drug Administration Staff. Published April 2020. Accessed 30 July 2020.
    1. Gwet KL. Computing inter-rater reliability and its variance in the presence of high agreement. Br. J. Math. Stat. Psychol. 2010;61:29–48. doi: 10.1348/000711006X126600.
    1. Wongpakaran N, et al. A comparison of Cohen’s Kappa and Gwet’s AC1 when calculating inter-rater reliability coefficients: a study conducted with personality disorder samples. BMC Med. Res. Methodol. 2013;13:1–7. doi: 10.1186/1471-2288-13-61.

Source: PubMed

3
Suscribir