Abstract
Purpose
Posterior reversible encephalopathy syndrome (PRES) is a disorder of cerebrovascular autoregulation that can result in brain edema, hemorrhage, and infarction. We sought to investigate whether certain imaging characteristics in PRES are associated with clinically significant patient outcomes.
Methods
We retrospectively reviewed all cases of PRES occurring between 2008 and 2014 at two major academic medical centers. Demographic, clinical, and radiographic data were collected. We analyzed imaging studies for vasogenic edema, hemorrhage, and diffusion restriction. We performed univariate analysis and stepwise logistic regression to assess the association between our radiologic findings of interest and clinical outcomes as defined by hospital discharge disposition and modified Rankin scale (mRS) at time of discharge.
Results
We identified 99 cases of PRES in 96 patients. The median age was 55 years (IQR 30–65) and 74% were women. In 99 cases, 60% of patients had active cancer, 19% had history of bone marrow or organ transplantation, 14% had autoimmune disease, and 8% were peripartum. Imaging at clinical presentation showed extensive vasogenic edema in 39%, hemorrhage in 36%, hemorrhage with mass effect in 7%, and restricted diffusion in 16%. In our final logistic regression models, the presence of extensive vasogenic edema, hemorrhage with mass effect, or diffusion restriction was associated with worse clinical outcome as defined by both discharge disposition (OR = 4.3; 95% CI: 1.4–36.3; p = 0.047) and mRS (OR = 3.6; 95% CI: 1.2–10.7; p = 0.019).
Conclusions
Extensive vasogenic edema, hemorrhage, and restricted diffusion on initial imaging in PRES are associated with worse clinical outcomes.
Similar content being viewed by others
References
Fugate JE, Rabinstein AA (2015) Posterior reversible encephalopathy syndrome: clinical and radiological manifestations, pathophysiology, and outstanding questions. Lancet Neurol 14:914–925. doi:10.1016/S1474-4422(15)00111-8
Hinchey J, Chaves C, Appignani B, Breen J, Pao L, Wang A, Pessin MS, Lamy C, Mas JL, Caplan LR (1996) A reversible posterior leukoencephalopathy syndrome. N Engl J Med 334:494–500. doi:10.1056/NEJM199602223340803
Liman TG, Bohner G, Heuschmann PU, Endres M, Siebert E (2012) The clinical and radiological spectrum of posterior reversible encephalopathy syndrome: the retrospective berlin PRES study. J Neurol 259:155–164. doi:10.1007/s00415-011-6152-4
Rabinstein AA, Mandrekar J, Merrell R, Kozak OS, Durosaro O, Fugate JE (2012) Blood pressure fluctuations in posterior reversible encephalopathy syndrome. J Stroke Cerebrovasc Dis 21:254–258. doi:10.1016/j.jstrokecerebrovasdis.2011.03.011
Li Y, Gor D, Walicki D, Jenny D, Jones D, Barbour P, Castaldo J (2012) Spectrum and potential pathogenesis of reversible posterior leukoencephalopathy syndrome. J Stroke Cerebrovasc Dis 21:873–882. doi:10.1016/j.jstrokecerebrovasdis.2011.05.010
Bartynski WS (2008) Posterior reversible encephalopathy syndrome, part 2: controversies surrounding pathophysiology of vasogenic edema. AJNR Am J Neuroradiol 29:1043–1049. doi:10.3174/ajnr.A0929
Fugate JE, Claassen DO, Cloft HJ, Kallmes DF, Kozak OS, Rabinstein AA (2010) Posterior reversible encephalopathy syndrome: associated clinical and radiologic findings. Mayo Clin Proc 85:427–432. doi:10.4065/mcp.2009.0590
Jung SM, Moon SJ, Kwok SK, Ju JH, Park KS, Park SH, Kim HY (2013) Posterior reversible encephalopathy syndrome in Korean patients with systemic lupus erythematosus: risk factors and clinical outcome. Lupus 22:885–891. doi:10.1177/0961203313496341
Hammerstrom AE, Howell J, Gulbis A, Rondon G, Champlin RE, Popat U (2013) Tacrolimus-associated posterior reversible encephalopathy syndrome in hematopoietic allogeneic stem cell transplantation. Am J Hematol 88:301–305. doi:10.1002/ajh.23402
Pruitt AA, Graus F, Rosenfeld MR (2013a) Neurological complications of solid organ transplantation. Neurohospitalist 3:152–166. doi:10.1177/1941874412466090
Pruitt AA, Graus F, Rosenfeld MR (2013b) Neurological complications of transplantation: part I: hematopoietic cell transplantation. Neurohospitalist 3:24–38. doi:10.1177/1941874412455338
Singer S, Grommes C, Reiner AS, Rosenblum MK, DeAngelis LM (2015) Posterior reversible encephalopathy syndrome in patients with cancer. Oncologist 20:806–811. doi:10.1634/theoncologist.2014-0149
Bartynski WS, Boardman JF, Zeigler ZR, Shadduck RK, Lister J (2006) Posterior reversible encephalopathy syndrome in infection, sepsis, and shock. AJNR Am J Neuroradiol 27:2179–2190
Brewer J, Owens MY, Wallace K, Reeves AA, Morris R, Khan M, LaMarca B, Martin JN (2013) Posterior reversible encephalopathy syndrome in 46 of 47 patients with eclampsia. Am J Obstet Gynecol 208:468.e461–468.e466. doi:10.1016/j.ajog.2013.02.015
Pande AR, Ando K, Ishikura R, Nagami Y, Takada Y, Wada A, Watanabe Y, Miki Y, Uchino A, Nakao N (2006) Clinicoradiological factors influencing the reversibility of posterior reversible encephalopathy syndrome: a multicenter study. Radiat Med 24:659–668. doi:10.1007/s11604-006-0086-2
Covarrubias DJ, Luetmer PH, Campeau NG (2002) Posterior reversible encephalopathy syndrome: prognostic utility of quantitative diffusion-weighted MR images. AJNR Am J Neuroradiol 23:1038–1048
Hefzy HM, Bartynski WS, Boardman JF, Lacomis D (2009) Hemorrhage in posterior reversible encephalopathy syndrome: imaging and clinical features. AJNR Am J Neuroradiol 30:1371–1379. doi:10.3174/ajnr.A1588
Aranas RM, Prabhakaran S, Lee VH (2009) Posterior reversible encephalopathy syndrome associated with hemorrhage. Neurocrit Care 10:306–312. doi:10.1007/s12028-009-9200-5
Sharma A, Whitesell RT, Moran KJ (2010) Imaging pattern of intracranial hemorrhage in the setting of posterior reversible encephalopathy syndrome. Neuroradiology 52:855–863. doi:10.1007/s00234-009-0632-6
Zeeman GG, Fleckenstein JL, Twickler DM, Cunningham FG (2004) Cerebral infarction in eclampsia. Am J Obstet Gynecol 190:714–720. doi:10.1016/j.ajog.2003.09.015
Gao B, Lerner A, Law M (2016) The clinical outcome of posterior reversible encephalopathy syndrome. AJNR Am J Neuroradiol 37:E55–E56. doi:10.3174/ajnr.A4853
McKinney AM, Sarikaya B, Gustafson C, Truwit CL (2012) Detection of microhemorrhage in posterior reversible encephalopathy syndrome using susceptibility-weighted imaging. AJNR Am J Neuroradiol 33:896–903. doi:10.3174/ajnr.A2886
Siebert E, Bohner G, Liebig T, Endres M, Liman T (2017) Factors associated with fatal outcome in posterior reversible encephalopathy syndrome: a retrospective analysis of the berlin PRES study. J Neurol 264:237–242. doi:10.1007/s00415-016-8328-4
Alhilali LM, Reynolds AR, Fakhran S (2014) A multi-disciplinary model of risk factors for fatal outcome in posterior reversible encephalopathy syndrome. J Neurol Sci 347:59–65. doi:10.1016/j.jns.2014.09.019
Legriel S, Schraub O, Azoulay E, Hantson P, Magalhaes E, Coquet I et al (2012) Determinants of recovery from severe posterior reversible encephalopathy syndrome. PLoS One 7:e44534. doi:10.1371/journal.pone.0044534
Junewar V, Verma R, Sankhwar PL, Garg RK, Singh MK, Malhotra HS et al (2014) Neuroimaging features and predictors of outcome in eclamptic encephalopathy: a prospective observational study. AJNR Am J Neuroradiol 35:1728–1734. doi:10.3174/ajnr.A3923
Akins PT, Axelrod Y, Silverthorn JW, Guppy K, Banerjee A, Hawk MW (2014) Management and outcomes of malignant posterior reversible encephalopathy syndrome. Clin Neurol Neurosurg 125:52–57. doi:10.1016/j.clineuro.2014.06.034
Merayo-Chalico J, Apodaca E, Barrera-Vargas A, Alcocer-Varela J, Colunga-Pedraza I, González-Patiño A et al (2016) Clinical outcomes and risk factors for posterior reversible encephalopathy syndrome in systemic lupus erythematosus: a multicentric case-control study. J Neurol Neurosurg Psychiatry 87:287–294. doi:10.1136/jnnp-2014-310145
Hinduja A, Habetz K, Raina S, Ramakrishnaiah R, Fitzgerald RT (2017) Predictors of poor outcome in patients with posterior reversible encephalopathy syndrome. Int J Neurosci 127:135–144 http://dx.doi.org/10.3109/00207454.2016.1152966
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP et al (2007) The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370:1453–1457. doi:10.1016/S0140-6736(07)61602-X
Navi BB, Singer S, Merkler AE, Cheng NT, Stone JB, Kamel H et al (2014) Cryptogenic subtype predicts reduced survival among cancer patients with ischemic stroke. Stroke 45:2292–2297. doi:10.1161/STROKEAHA.114.005784
Flint A, Kamel H, Navi B, Rao V, Faigeles B, Conell C et al (2012) Inpatient statin use predicts improved ischemic stroke discharge disposition. Neurology 78:1678–1683. doi:10.1212/WNL.0b013e3182575142
Qureshi AI, Chaudhry SA, Sapkota BL, Rodriguez GJ, Suri MFK (2012) Discharge destination as a surrogate for modified Rankin scale defined outcomes at 3-and 12-months poststroke among stroke survivors. Arch Phys Med Rehabil 93:1408–1413. doi:10.1016/j.apmr.2012.02.032
Van Swieten J, Koudstaal P, Visser M, Schouten H, Van Gijn J (1988) Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19:604–607
McKinney AM, Short J, Truwit CL, McKinney ZJ, Kozak OS, SantaCruz KS et al (2007) Posterior reversible encephalopathy syndrome: incidence of atypical regions of involvement and imaging findings. AJR Am J Roentgenol 189:904–912. doi:10.2214/AJR.07.2024
Bartynski WS, Boardman JF (2007) Distinct imaging patterns and lesion distribution in posterior reversible encephalopathy syndrome. AJNR Am J Neuroradiol 28:1320–1327. doi:10.3174/ajnr.A0549
Li R, Mitchell P, Dowling R, Yan B (2013) Is hypertension predictive of clinical recurrence in posterior reversible encephalopathy syndrome? J Clin Neurosci 20:248–252. doi:10.1016/j.jocn.2012.02.023
Karia S, Rykken J, McKinney Z, Zhang L, McKinney A (2016) Utility and significance of gadolinium-based contrast enhancement in posterior reversible encephalopathy syndrome. AJNR Am J Neuroradiol 37:415–422
Mueller-Mang C, Mang T, Pirker A, Klein K, Prchla C, Prayer D (2009) Posterior reversible encephalopathy syndrome: do predisposing risk factors make a difference in MRI appearance? Neuroradiology 51:373–383. doi:10.1007/s00234-009-0504-0
Acknowledgements
We are grateful to Monica Chen for administrative assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This study was funded by the NIH/National Center for Advancing Translational Sciences (KL2TR000458: AG) and the NIH/NINDS (K23NS091395) and the Florence Gould Endowment for Discovery in Stroke (BN).
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
For this type of study formal consent is not required. Waivers of informed consent were granted.
Electronic supplementary material
ESM 1
(DOCX 25 kb)
Rights and permissions
About this article
Cite this article
Schweitzer, A.D., Parikh, N.S., Askin, G. et al. Imaging characteristics associated with clinical outcomes in posterior reversible encephalopathy syndrome. Neuroradiology 59, 379–386 (2017). https://doi.org/10.1007/s00234-017-1815-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00234-017-1815-1