Comprehensive Update and Review of Clinical and Imaging Features of SMART Syndrome

References

1. 1.↵
   1. Turnquist C,
   2. Harris BT,
   3. Harris CC

   . Radiation-induced brain injury: current concepts and therapeutic strategies targeting neuroinflammation. Neurooncol Adv 2020;2:vdaa057 doi:10.1093/noajnl/vdaa057 pmid:32642709

   CrossRefPubMed
2. 2.↵
   1. Zheng Q,
   2. Yang L,
   3. Tan LM, et al

   . Stroke-like migraine attacks after radiation therapy syndrome. Chin Med J (Engl) 2015;128:2097–101 doi:10.4103/0366-6999.161393 pmid:26228225

   CrossRefPubMed
3. 3.↵
   1. Dominguez M,
   2. Malani R

   . Stroke-like migraine attacks after radiation therapy (SMART) syndrome: a comprehensive review. Curr Pain Headache Rep 2021;25:33 doi:10.1007/s11916-021-00946-3 pmid:33761013

   CrossRefPubMed
4. 4.↵
   1. Black DF,
   2. Morris JM,
   3. Lindell EP, et al

   . Stroke-like migraine attacks after radiation therapy (SMART) syndrome is not always completely reversible: a case series. AJNR Am J Neuroradiol 2013;34:2298–303 doi:10.3174/ajnr.A3602 pmid:23788601

   Abstract/FREE Full Text
5. 5.↵
   1. Ota Y,
   2. Leung D,
   3. Lin E, et al

   . Prognostic factors of stroke-like migraine attacks after radiation therapy (SMART) syndrome. AJNR Am J Neuroradiol 2022;43:396–401 doi:10.3174/ajnr.A7424 pmid:35177545

   Abstract/FREE Full Text
6. 6.↵
   1. Black DF,
   2. Bartleson JD,
   3. Bell ML, et al

   . SMART: stroke-like migraine attacks after radiation therapy. Cephalalgia 2006;26:1137–42 doi:10.1111/j.1468-2982.2006.01184.x pmid:16919065

   CrossRefPubMedWeb of Science
7. 7.↵
   1. Rigamonti A,
   2. Lauria G,
   3. Mantero V, et al

   . SMART (stroke-like migraine attack after radiation therapy) syndrome: a case report with review of the literature. Neurol Sci 2016;37:157–61 doi:10.1007/s10072-015-2396-6 pmid:26466588

   CrossRefPubMed
8. 8.↵
   1. Singh TD,
   2. Hajeb M,
   3. Rabinstein AA, et al

   . SMART syndrome: retrospective review of a rare delayed complication of radiation. Eur J Neurol 2021;28:1316–23 doi:10.1111/ene.14632 pmid:33159349

   CrossRefPubMed
9. 9.↵
   1. Rheims S,
   2. Ricard D,
   3. van den Bent M, et al

   . Peri-ictal pseudoprogression in patients with brain tumor. Neuro Oncol 2011;13:775–82 doi:10.1093/neuonc/nor082 pmid:21727213

   CrossRefPubMed
10. 10.↵
    1. Di Stefano AL,
    2. Berzero G,
    3. Vitali P, et al

    . Acute late-onset encephalopathy after radiotherapy: an unusual life-threatening complication. Neurology 2013;81:1014–17 doi:10.1212/WNL.0b013e3182a43b1f pmid:23935180

    CrossRefPubMed
11. 11.↵
    1. Kam WW,
    2. Banati RB

    . Effects of ionizing radiation on mitochondria. Free Radic Biol Med 2013;65:607–19 doi:10.1016/j.freeradbiomed.2013.07.024 pmid:23892359

    CrossRefPubMed
12. 12.↵
    1. Averbeck D,
    2. Rodriguez-Lafrasse C

    . Role of mitochondria in radiation responses: epigenetic, metabolic, and signaling impacts. Int J Mol Sci 2021;22:11047 doi:10.3390/ijms222011047 pmid:34681703

    CrossRefPubMed
13. 13.↵
    1. Iizuka T,
    2. Sakai F,
    3. Suzuki N, et al

    . Neuronal hyperexcitability in stroke-like episodes of MELAS syndrome. Neurology 2002;59:816–24 doi:10.1212/wnl.59.6.816 pmid:12297560

    Abstract/FREE Full Text
14. 14.↵
    1. Verma M,
    2. Lizama BN,
    3. Chu CT

    . Excitotoxicity, calcium and mitochondria: a triad in synaptic neurodegeneration. Transl Neurodegener 2022;11:3 doi:10.1186/s40035-021-00278-7 pmid:35078537

    CrossRefPubMed
15. 15.↵
    1. Ayata C,
    2. Lauritzen M

    . Spreading depression, spreading depolarizations, and the cerebral vasculature. Physiol Rev 2015;95:953–93 doi:10.1152/physrev.00027.2014 pmid:26133935

    CrossRefPubMed
16. 16.↵
    1. Auffenberg E,
    2. Hedrich UB,
    3. Barbieri R, et al

    . Hyperexcitable interneurons trigger cortical spreading depression in an Scn1a migraine model. J Clin Invest 2021;131:e142202 doi:10.1172/JCI142202 pmid:34546973

    CrossRefPubMed
17. 17.↵
    1. Vinogradova LV

    . Initiation of spreading depression by synaptic and network hyperactivity: insights into trigger mechanisms of migraine aura. Cephalalgia 2018;38:1177–87 doi:10.1177/0333102417724151 pmid:28750590

    CrossRefPubMed
18. 18.↵
    1. Dreier JP,
    2. Major S,
    3. Pannek HW, et al

    ; COSBID study group. Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain 2012;135:259–75 doi:10.1093/brain/awr303 pmid:22120143

    CrossRefPubMed
19. 19.↵
    1. Greene-Schloesser D,
    2. Robbins ME,
    3. Peiffer AM, et al

    . Radiation-induced brain injury: a review. Front Oncol 2012;2:73 doi:10.3389/fonc.2012.00073 pmid:22833841

    CrossRefPubMed
20. 20.↵
    1. Kessler AT,
    2. Bhatt AA

    . Brain tumour post-treatment imaging and treatment-related complications. Insights Imaging 2018;9:1057–75 doi:10.1007/s13244-018-0661-y pmid:30411280

    CrossRefPubMed
21. 21.↵
    1. Anderson RC,
    2. Patel V,
    3. Sheikh-Bahaei N, et al

    . Posterior reversible encephalopathy syndrome (PRES): pathophysiology and neuro-imaging. Front Neurol 2020;11:463 doi:10.3389/fneur.2020.00463 pmid:32612567

    CrossRefPubMed
22. 22.↵
    1. Di Stefano AL,
    2. Berzero G,
    3. Ducray F, et al

    . Stroke-like events after brain radiotherapy: a large series with long-term follow-up. Eur J Neurol 2019;26:639–50 doi:10.1111/ene.13870 pmid:30471162

    CrossRefPubMed
23. 23.↵
    1. Fan EP,
    2. Heiber G,
    3. Gerard EE, et al

    . Stroke-like migraine attacks after radiation therapy: a misnomer? Epilepsia 2018;59:259–68 doi:10.1111/epi.13963 pmid:29171011

    CrossRefPubMed
24. 24.↵
    1. Winter SF,
    2. Klein JP,
    3. Vaios EJ, et al

    . Clinical presentation and management of SMART syndrome. Neurology 2021 May 4. [Epub ahead of print] doi:10.1212/WNL.0000000000012150

    CrossRef
25. 25.↵
    1. Jia W,
    2. Saito R,
    3. Kanamori M, et al

    . SMART (stroke-like migraine attacks after radiation therapy) syndrome responded to steroid pulse therapy: report of a case and review of the literature. eNeurologicalSci 2018;12:1–4 doi:10.1016/j.ensci.2018.05.003 pmid:30003148

    CrossRefPubMed
26. 26.↵
    1. Wai K,
    2. Balabanski A,
    3. Chia N, et al

    . Reversible hemispheric hypoperfusion in two cases of SMART syndrome. J Clin Neurosci 2017;43:146–48 doi:10.1016/j.jocn.2017.05.013 pmid:28645744

    CrossRefPubMed
27. 27.↵
    1. Pai V,
    2. Sitoh YY,
    3. Purohit B

    . Gyriform restricted diffusion in adults: looking beyond thrombo-occlusions. Insights Imaging 2020;11:20 doi:10.1186/s13244-019-0829-0 pmid:32040645

    CrossRefPubMed
28. 28.↵
    1. Moritani T,
    2. Smoker WR,
    3. Sato Y, et al

    . Diffusion-weighted imaging of acute excitotoxic brain injury. AJNR Am J Neuroradiol 2005;26:216–28 pmid:15709116

    PubMedWeb of Science
29. 29.↵
    1. Greenberg SM,
    2. Vernooij MW,
    3. Cordonnier C

    ; et al; Microbleed Study Group. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009;8:165–74 doi:10.1016/S1474-4422(09)70013-4 pmid:19161908

    CrossRefPubMedWeb of Science
30. 30.↵
    1. Khanipour Roshan S,
    2. Salmela MB,
    3. McKinney AM

    . Susceptibility-weighted imaging in stroke-like migraine attacks after radiation therapy syndrome. Neuroradiology 2015;57:1103–09 doi:10.1007/s00234-015-1567-8 pmid:26242361

    CrossRefPubMed
31. 31.↵
    1. Goos JD,
    2. van der Flier WM,
    3. Knol DL, et al

    . Clinical relevance of improved microbleed detection by susceptibility-weighted magnetic resonance imaging. Stroke 2011;42:1894–900 doi:10.1161/STROKEAHA.110.599837 pmid:21566235

    Abstract/FREE Full Text
32. 32.↵
    1. Cheng AL,
    2. Batool S,
    3. McCreary CR, et al

    . Susceptibility-weighted imaging is more reliable than T2*-weighted gradient-recalled echo MRI for detecting microbleeds. Stroke 2013;44:2782–86 doi:10.1161/STROKEAHA.113.002267 pmid:23920014

    Abstract/FREE Full Text
33. 33.↵
    1. Hoeffner EG,
    2. Case I,
    3. Jain R, et al

    . Cerebral perfusion CT: technique and clinical applications. Radiology 2004;231:632–44 doi:10.1148/radiol.2313021488 pmid:15118110

    CrossRefPubMedWeb of Science
34. 34.↵
    1. Welker K,
    2. Boxerman J,
    3. Kalnin A, et al

    ; American Society of Functional Neuroradiology MR Perfusion Standards and Practice Subcommittee of the ASFNR Clinical Practice Committee. ASFNR recommendations for clinical performance of MR dynamic susceptibility contrast perfusion imaging of the brain. AJNR Am J Neuroradiol 2015;36:E41–51 doi:10.3174/ajnr.A4341 pmid:25907520

    Abstract/FREE Full Text
35. 35.↵
    1. Nar Senol P,
    2. Gocmen R,
    3. Karli Oguz K, et al

    . Perfusion imaging insights into SMART syndrome: a case report. Acta Neurol Belg 2015;115:807–10 doi:10.1007/s13760-015-0483-3 pmid:25972059

    CrossRefPubMed
36. 36.↵
    1. Teske N,
    2. Albert NL,
    3. Forbrig R, et al

    . Advanced imaging findings in stroke-like migraine attacks after radiation therapy (SMART) syndrome. Eur J Nucl Med Mol Imaging 2023;50:1264–65 doi:10.1007/s00259-022-06042-x pmid:36418589

    CrossRefPubMed
37. 37.↵
    1. Biju RD,
    2. Dower A,
    3. Moon BG, et al

    . SMART (stroke-like migraine attacks after radiation therapy) syndrome: a case study with imaging supporting the theory of vascular dysfunction. Am J Case Rep 2020;21:e921795 doi:10.12659/AJCR.921795 pmid:32221270

    CrossRefPubMed
38. 38.↵
    1. Gelfand JM,
    2. Wintermark M,
    3. Josephson SA

    . Cerebral perfusion-CT patterns following seizure. Eur J Neurol 2010;17:594–601 doi:10.1111/j.1468-1331.2009.02869.x pmid:19968701

    CrossRefPubMed
39. 39.↵
    1. Gomez-Cibeira E,
    2. Calleja-Castano P,
    3. Gonzalez de la Aleja J, et al

    . Brain magnetic resonance spectroscopy findings in the stroke-like migraine attacks after radiation therapy (SMART) syndrome. J Neuroimaging 2015;25:1056–58 doi:10.1111/jon.12227 pmid:25702932

    CrossRefPubMed
40. 40.↵
    1. Farid K,
    2. Meissner WG,
    3. Samier-Foubert A, et al

    . Normal cerebrovascular reactivity in stroke-like migraine attacks after radiation therapy syndrome. Clin Nucl Med 2010;35:583–85 doi:10.1097/RLU.0b013e3181e4db6f pmid:20631504

    CrossRefPubMed
41. 41.↵
    1. Pruitt A,
    2. Dalmau J,
    3. Detre J, et al

    . Episodic neurologic dysfunction with migraine and reversible imaging findings after radiation. Neurology 2006;67:676–78 doi:10.1212/01.wnl.0000228862.76269.62 pmid:16707725

    Abstract/FREE Full Text
42. 42.↵
    1. Bund C,
    2. Fahrer P,
    3. Gebus O, et al

    . Sequential FDG PET and MRI findings in a case of SMART syndrome. Seizure 2017;51:50–51 doi:10.1016/j.seizure.2017.07.012 pmid:28797914

    CrossRefPubMed
43. 43.↵
    1. Ponisio MR,
    2. Zempel JM,
    3. Day BK, et al

    . The role of SPECT and PET in epilepsy. AJR Am J Roentgenol 2021;216:759–68 doi:10.2214/AJR.20.23336 pmid:33474983

    CrossRefPubMed
44. 44.↵
    1. Jaraba S,
    2. Puig O,
    3. Miro J, et al

    . Refractory status epilepticus due to SMART syndrome. Epilepsy Behav 2015;49:189–92 doi:10.1016/j.yebeh.2015.05.033 pmid:26071996

    CrossRefPubMed
45. 45.↵
    1. von Oertzen TJ

    . PET and ictal SPECT can be helpful for localizing epileptic foci. Curr Opin Neurol 2018;31:184–91 doi:10.1097/WCO.0000000000000527 pmid:29303866

    CrossRefPubMed
46. 46.↵
    1. Hutterer M,
    2. Ebner Y,
    3. Riemenschneider MJ, et al

    . Epileptic activity increases cerebral amino acid transport assessed by 18F-fluoroethyl-l-tyrosine amino acid PET: a potential brain tumor mimic. J Nucl Med 2017;58:129–37 doi:10.2967/jnumed.116.176610 pmid:27469356

    Abstract/FREE Full Text
47. 47.↵
    1. Ota Y,
    2. Leung D,
    3. Moritani T, et al

    . Atypical imaging findings of presumed stroke-like migraine attacks after radiation therapy syndrome in the brainstem. Neuroradiology 2021;63:1377–81 doi:10.1007/s00234-021-02684-0 pmid:33694026

    CrossRefPubMed
48. 48.↵
    1. Shuper A,
    2. Packer RJ,
    3. Vezina LG, et al

    . “Complicated migraine-like episodes” in children following cranial irradiation and chemotherapy. Neurology 1995;45:1837–40 doi:10.1212/wnl.45.10.1837 pmid:7477978

    Abstract/FREE Full Text
49. 49.↵
    1. Maramattom BV,
    2. Panikar D

    . Brainstem SMART syndrome: Be-SMART. Neurol India 2022;70:1731–33 doi:10.4103/0028-3886.355087 pmid:36076710

    CrossRefPubMed
50. 50.↵
    1. Andersen BM,
    2. Miranda C,
    3. Hatzoglou V, et al

    . Leptomeningeal metastases in glioma: the Memorial Sloan Kettering Cancer Center experience. Neurology 2019;92:e2483–91 doi:10.1212/WNL.0000000000007529 pmid:31019097

    Abstract/FREE Full Text
51. 51.↵
    1. Chamberlain MC,
    2. Glantz M,
    3. Groves MD, et al

    . Diagnostic tools for neoplastic meningitis: detecting disease, identifying patient risk, and determining benefit of treatment. Semin Oncol 2009;36:S35–45 doi:10.1053/j.seminoncol.2009.05.005 pmid:19660682

    CrossRefPubMedWeb of Science
52. 52.↵
    1. Karonen JO,
    2. Partanen PL,
    3. Vanninen RL, et al

    . Evolution of MR contrast enhancement patterns during the first week after acute ischemic stroke. AJNR Am J Neuroradiol 2001;22:103–11 pmid:11158895

    Abstract/FREE Full Text
53. 53.↵
    1. Idiculla PS,
    2. Gurala D,
    3. Palanisamy M, et al

    . Cerebral venous thrombosis: a comprehensive review. Eur Neurol 2020;83:369–79 doi:10.1159/000509802 pmid:32877892

    CrossRefPubMed
54. 54.↵
    1. Fugate JE,
    2. Rabinstein AA

    . Posterior reversible encephalopathy syndrome: clinical and radiological manifestations, pathophysiology, and outstanding questions. Lancet Neurol 2015;14:914–25 doi:10.1016/S1474-4422(15)00111-8 pmid:26184985

    CrossRefPubMed
55. 55.↵
    1. Guerriero RM,
    2. Gaillard WD

    . Imaging modalities to diagnose and localize status epilepticus. Seizure 2019;68:46–51 doi:10.1016/j.seizure.2018.10.010 pmid:30385179

    CrossRefPubMed
56. 56.↵
    1. Pellerin A,
    2. Marois C,
    3. Mezouar N, et al

    . Neuronal injuries evidenced by transient cortical magnetic resonance enhancement in hemiplegic migraine: a case report. Cephalalgia 2019;39:323–25 doi:10.1177/0333102418794481 pmid:30092648

    CrossRefPubMed
57. 57.↵
    1. Bhatia KD,
    2. Krishnan P,
    3. Kortman H, et al

    . Acute cortical lesions in MELAS syndrome: anatomic distribution, symmetry, and evolution. AJNR Am J Neuroradiol 2020;41:167–73 doi:10.3174/ajnr.A6325 pmid:31806591

    Abstract/FREE Full Text
58. 58.↵
    1. Cheng W,
    2. Zhang Y,
    3. He L

    . MRI features of stroke-like episodes in mitochondrial encephalomyopathy with lactic acidosis and stroke-like episodes. Front Neurol 2022;13:843386 doi:10.3389/fneur.2022.843386 pmid:35222261

    CrossRefPubMed