Unpacking the CNS Manifestations of Epstein-Barr Virus: An Imaging Perspective

References

1. 1.↵
   2. Dunmire SK,
   3. Verghese PS,
   4. Balfour HH Jr.

   . Primary Epstein-Barr virus infection. J Clin Virol 2018;102:84–92 doi:10.1016/j.jcv.2018.03.001 pmid:29525635

   CrossRefPubMed
2. 2.↵
   2. Smatti MK,
   3. Al-Sadeq DW,
   4. Ali NH, et al

   . Epstein-Barr virus epidemiology, serology, and genetic variability of LMP-1 oncogene among healthy population: an update. Front Oncol 2018;8:211 doi:10.3389/fonc.2018.00211 pmid:29951372

   CrossRefPubMed
3. 3.↵
   2. Weinberg A,
   3. Li S,
   4. Palmer M, et al

   . Quantitative CSF PCR in Epstein-Barr virus infections of the central nervous system. Ann Neurol 2002;52:543–48 doi:10.1002/ana.10321 pmid:12402250

   CrossRefPubMed
4. 4.↵
   2. Cheng H,
   3. Chen D,
   4. Peng X, et al

   . Clinical characteristics of Epstein-Barr virus infection in the pediatric nervous system. BMC Infect Dis 2020;20:886 doi:10.1186/s12879-020-05623-1 pmid:33238935

   CrossRefPubMed
5. 5.↵
   2. Kim HJ,
   3. Ko YH,
   4. Kim JE, et al

   ; Hematopathology Study Group of the Korean Society of Pathologists. Epstein-Barr virus-associated lymphoproliferative disorders: review and update on 2016 WHO Classification. J Pathol Transl Med 2017;51:352–58 doi:10.4132/jptm.2017.03.15 pmid:28592786

   CrossRefPubMed
6. 6.↵
   2. Pons-Escoda A,
   3. Naval-Baudin P,
   4. Velasco R, et al

   . Imaging of lymphomas involving the CNS: an update-review of the full spectrum of disease with an emphasis on the World Health Organization Classifications of CNS Tumors 2021 and Hematolymphoid Tumors 2022. AJNR Am J Neuroradiol 2023;44:358–66 doi:10.3174/ajnr.A7795 pmid:36822829

   CrossRefPubMed
7. 7.↵
   2. Balaguer-Rosello A,
   3. Piñana JL,
   4. Bataller L, et al

   . Central nervous system involvement in Epstein-Barr virus-related post-transplant lymphoproliferative disorders after allogeneic hematopoietic stem cell transplantation. Transplant Cell Ther 2021;27:261.e1–261.e7 doi:10.1016/j.jtct.2020.12.019 pmid:33781531

   CrossRefPubMed
8. 8.↵
   2. Costa BK,
   3. Sato DK

   . Viral encephalitis: a practical review on diagnostic approach and treatment. J Pediatr (Rio J) 2020;96(Suppl 1):12–19 doi:10.1016/j.jped.2019.07.006 pmid:31513761

   CrossRefPubMed
9. 9.↵
   2. Abul-Kasim K,
   3. Palm L,
   4. Maly P, et al

   . The neuroanatomic localization of Epstein-Barr virus encephalitis may be a predictive factor for its clinical outcome: a case report and review of 100 cases in 28 reports. J Child Neurol 2009;24:720–26 doi:10.1177/0883073808327842 pmid:19151367

   CrossRefPubMed
10. 10.↵
    2. Fujimoto H,
    3. Asaoka K,
    4. Imaizumi T, et al

    . Epstein-Barr virus infections of the central nervous system. Intern Med 2003;42:33–40 doi:10.2169/internalmedicine.42.33 pmid:12583615

    CrossRefPubMed
11. 11.↵
    2. Doja A,
    3. Bitnun A,
    4. Ford Jones EL, et al

    . Pediatric Epstein-Barr virus-associated encephalitis: 10-year review. J Child Neurol 2006;21:384–91 doi:10.1177/08830738060210051101 pmid:16901443

    CrossRefPubMed
12. 12.↵
    2. Vyas S,
    3. Suthar R,
    4. Bhatia V, et al

    . Brain MRI in Epstein-Barr virus meningoencephalitis in children. Ann Indian Acad Neurol 2020;23:621–24 doi:10.4103/aian.AIAN_537_19 pmid:33623261

    CrossRefPubMed
13. 13.↵
    2. Thorley-Lawson DA

    . EBV persistence: introducing the virus. Curr Top Microbiol Immunol 2015;390:151–209 doi:10.1007/978-3-319-22822-8_8 pmid:26424647

    CrossRefPubMed
14. 14.↵
    2. Rodrigo-Armenteros P,
    3. Kapetanovic-García S,
    4. Antón-Méndez L, et al

    . Akinetic mutism and status epilepticus due to Epstein Barr virus encephalitis. Clin Neurol Neurosurg 2019;185:105492 doi:10.1016/j.clineuro.2019.105492 pmid:31470359

    CrossRefPubMed
15. 15.↵
    2. Selter RC,
    3. Brilot F,
    4. Grummel V, et al

    . Antibody responses to EBV and native MOG in pediatric inflammatory demyelinating CNS diseases. Neurology 2010;74:1711–15 doi:10.1212/WNL.0b013e3181e04096 pmid:20410464

    CrossRefPubMed
16. 16.↵
    2. Nakamura Y,
    3. Nakajima H,
    4. Tani H, et al

    . Anti-MOG antibody-positive ADEM following infectious mononucleosis due to a primary EBV infection: a case report. BMC Neurol 2017;17:76 doi:10.1186/s12883-017-0858-6 pmid:28420330

    CrossRefPubMed
17. 17.↵
    2. Zhang N,
    3. Zuo Y,
    4. Jiang L, et al

    . Epstein-Barr virus and neurological diseases. Front Mol Biosci 2022;8:816098 doi:10.3389/fmolb.2021.816098 pmid:35083281

    CrossRefPubMed
18. 18.↵
    2. Tsuruyama Y,
    3. Mori N,
    4. Yoshida S, et al

    . Epstein-Barr virus-related encephalitis in a young woman: a case report. J Infect Chemother 2020;26:741–44 doi:10.1016/j.jiac.2020.02.005 pmid:32147376

    CrossRefPubMed
19. 19.↵
    2. Tao Q,
    3. Young LS,
    4. Woodman CB, et al

    . Epstein-Barr virus (EBV) and its associated human cancers–genetics, epigenetics, pathobiology and novel therapeutics. Front Biosci 2006;11:2672–713 doi:10.2741/2000 pmid:16720343

    CrossRefPubMed
20. 20.↵
    2. Lanz TV,
    3. Brewer RC,
    4. Ho PP, et al

    . Clonally expanded B cells in multiple sclerosis bind EBV EBNA1 and GlialCAM. Nature 2022;603:321–27 doi:10.1038/s41586-022-04432-7 pmid:35073561

    CrossRefPubMed
21. 21.↵
    2. Sugita Y,
    3. Furuta T,
    4. Ohshima K, et al

    . The perivascular microenvironment in Epstein–Barr virus positive primary central nervous system lymphoma: the role of programmed cell death 1 and programmed cell death ligand 1. Neuropathology 2018;38:125–34 doi:10.1111/neup.12435 pmid:29067721

    CrossRefPubMed
22. 22.↵
    2. Pitjadi Tirelo M,
    3. Grayson W

    . Epstein-Barr virus-associated smooth muscle tumour: a case series with a significant proportion of tumours showing proclivity for cutaneous soft tissues. Dermatopathology (Basel) 2019;6:133–46 doi:10.1159/000497075 pmid:31700854

    CrossRefPubMed
23. 23.↵
    2. Ellul M,
    3. Solomon T

    . Acute encephalitis: diagnosis and management. Clin Med (Lond) 2018;18:155–59 doi:10.7861/clinmedicine.18-2-155 pmid:29626021

    CrossRefPubMed
24. 24.↵
    2. Hess RD

    . Routine Epstein-Barr virus diagnostics from the laboratory perspective: still challenging after 35 years. J Clin Microbiol 2004;42:3381–87 doi:10.1128/JCM.42.8.3381-3387.2004 pmid:15297472

    CrossRefPubMed
25. 25.↵
    2. Shian WJ,
    3. Chi CS

    . Epstein-Barr virus encephalitis and encephalomyelitis: MR findings. Pediatr Radiol 1996;26:690–93 doi:10.1007/BF01356839 pmid:8781116

    CrossRefPubMed
26. 26.↵
    2. Hung KL,
    3. Liao HT,
    4. Tsai ML

    . Epstein-Barr virus encephalitis in children. Acta Paediatr Taiwan 2000;41:140–46 pmid:10920547

    PubMed
27. 27.↵
    2. Lau JS,
    3. Low ZM,
    4. Abbott I, et al

    . Epstein-Barr virus encephalitis in solid organ transplantation. New Microbiol 2017;40:212–17 pmid:28513810

    PubMed
28. 28.↵
    2. Babik JM,
    3. Katrak S,
    4. Miller S, et al

    . Epstein-Barr virus encephalitis in a renal transplant recipient manifesting as hemorrhagic, ring-enhancing mass lesions. Transpl Infect Dis 2015;17:744–50 doi:10.1111/tid.12431 pmid:26252540

    CrossRefPubMed
29. 29.↵
    2. Khalil M,
    3. Enzinger C,
    4. Wallner-Blazek M, et al

    . Epstein-Barr virus encephalitis presenting with a tumor-like lesion in an immunosuppressed transplant recipient. J Neurovirol 2008;14:574–78 doi:10.1080/13550280802345715 pmid:18991070

    CrossRefPubMed
30. 30.↵
    2. Al-Shokri SD,
    3. Karumannil SA,
    4. Mohammed SS, et al

    . Post-Epstein-Barr virus acute cerebellitis in an adult. Am J Case Rep 2020;21:e918567 doi:10.12659/AJCR.918567 pmid:31905189

    CrossRefPubMed
31. 31.↵
    2. Ambrosio E,
    3. Khalighinejad F,
    4. Ionete C

    . Intravenous immunoglobulins in an adult case of post-EBV cerebellitis. BMJ Case Rep 2020;13:e231661 doi:10.1136/bcr-2019-231661 pmid:32075812

    CrossRefPubMed
32. 32.↵
    2. Hussain RS,
    3. Hussain NA

    . Ataxia and encephalitis in a young adult with EBV mononucleosis: a case report. Case Rep Neurol Med 2013;2013:516325 doi:10.1155/2013/516325 pmid:23781357

    CrossRefPubMed
33. 33.↵
    2. Liu WC,
    3. Chiu SK,
    4. Hsiang CW, et al

    . Acute unilateral cerebellitis, Epstein-Barr virus, and HIV. Lancet Infect Dis 2014;14:778 doi:10.1016/S1473-3099(14)70824-2 pmid:25056020

    CrossRefPubMed
34. 34.↵
    2. Van Lierde A,
    3. Righini A,
    4. Tremolati E

    . Acute cerebellitis with tonsillar herniation and hydrocephalus in Epstein-Barr virus infection. Eur J Pediatr 2004;163:689–91 doi:10.1007/s00431-004-1529-3 pmid:15309627

    CrossRefPubMed
35. 35.↵
    2. Grassin M,
    3. Rolland A,
    4. Leboucq N, et al

    . Bilateral facial nerve palsy associated with Epstein-Barr virus infection in a 3-year-old boy [in French]. Arch Pediatr 2017;24:564–67 doi:10.1016/j.arcped.2017.03.009 pmid:28416425

    CrossRefPubMed
36. 36.↵
    2. Steiner LA,
    3. Erbay A,
    4. Pache F, et al

    . Oculomotor nerve palsy as a presenting symptom of Epstein-Barr virus-associated infectious mononucleosis: case report and review of the literature. Case Rep Neurol 2021;13:756–62 doi:10.1159/000520437 pmid:35082645

    CrossRefPubMed
37. 37.↵
    2. Majid A,
    3. Galetta SL,
    4. Sweeney CJ, et al

    . Epstein–Barr virus myeloradiculitis and encephalomyeloradiculitis. Brain 2002;125:159–65 doi:10.1093/brain/awf010 pmid:11834601

    CrossRefPubMed
38. 38.↵
    2. Caldas C,
    3. Bernicker E,
    4. Nogare AD, et al

    . Case report: transverse myelitis associated with Epstein-Barr virus infection. Am J Med Sci 1994;307:45–48 doi:10.1097/00000441-199401000-00009 pmid:8291507

    CrossRefPubMed
39. 39.↵
    2. Mazur-Melewska K,
    3. Breńska I,
    4. Jończyk-Potoczna K, et al

    . Neurologic complications caused by Epstein-Barr virus in pediatric patients. J Child Neurol 2016;31:700–08 doi:10.1177/0883073815613563 pmid:26511720

    CrossRefPubMed
40. 40.↵
    2. Singhi P,
    3. Sharma JP,
    4. Gautam R, et al

    . Extensive longitudinal transverse myelitis associated with CSF Epstein-Barr virus infection: a case report. Child Neurol Open 2021;8:2329048X211049958 doi:10.1177/2329048X211049958 pmid:34692894

    CrossRefPubMed
41. 41.↵
    2. Ali D,
    3. Cardos B,
    4. Gorur Y, et al

    . A rare case of adult acute disseminated encephalomyelitis associated with primary Epstein-Barr virus infection. Eur J Case Rep Intern Med 2019;6:001094 doi:10.12890/2019_001094 pmid:31139588

    CrossRefPubMed
42. 42.↵
    2. Xiong CH,
    3. Yan Y,
    4. Liao Z, et al

    . Epidemiological characteristics of acute disseminated encephalomyelitis in Nanchang, China: a retrospective study. BMC Public Health 2014;14:111 doi:10.1186/1471-2458-14-111 pmid:24495742

    CrossRefPubMed
43. 43.↵
    2. Bathla G,
    3. Policeni B

    . Acute Disseminated Encephalomyelitis. In: Neuroradiology: Spectrum and Evolution of Disease. Elsevier; 2019:80–96
44. 44.↵
    2. Pohl D,
    3. Alper G,
    4. Van Haren K, et al

    . Acute disseminated encephalomyelitis. Neurology 2016;87(Suppl 2):S38–45 doi:10.1212/WNL.0000000000002825

    CrossRef
45. 45.↵
    2. Verhey LH,
    3. Branson HM,
    4. Shroff MM, et al

    ; Canadian Pediatric Demyelinating Disease Network. MRI parameters for prediction of multiple sclerosis diagnosis in children with acute CNS demyelination: a prospective national cohort study. Lancet Neurol 2011;10:1065–73 doi:10.1016/S1474-4422(11)70250-2 pmid:22067635

    CrossRefPubMed
46. 46.↵
    2. Kim S,
    3. Ahn SJ,
    4. Chu K

    . Epstein-Barr virus-associated acute disseminated encephalomyelitis successfully treated with rituximab: a case report. Encephalitis 2021;1:85–88 doi:10.47936/encephalitis.2021.00066

    CrossRefPubMed
47. 47.↵
    2. Crombie JL,
    3. LaCasce AS

    . Epstein Barr virus associated B-Cell lymphomas and iatrogenic lymphoproliferative disorders. Front Oncol 2019;9:109 doi:10.3389/fonc.2019.00109 pmid:30899698

    CrossRefPubMed
48. 48.↵
    2. Dunleavy K,
    3. Roschewski M,
    4. Wilson WH

    . Lymphomatoid granulomatosis and other Epstein-Barr virus associated lymphoproliferative processes. Curr Hematol Malig Rep 2012;7:208–15 doi:10.1007/s11899-012-0132-3 pmid:22814713

    CrossRefPubMed
49. 49.↵
    2. Melani C,
    3. Jaffe ES,
    4. Wilson WH

    . Pathobiology and treatment of lymphomatoid granulomatosis, a rare EBV-driven disorder. Blood 2020;135:1344–52 doi:10.1182/blood.2019000933 pmid:32107539

    CrossRefPubMed
50. 50.↵
    2. Xiang Y,
    3. Liu C,
    4. Xue Y, et al

    . Primary central nervous system lymphomatoid granulomatosis: systemic review. Front Neurol 2020;11:901 doi:10.3389/fneur.2020.00901 pmid:33041962

    CrossRefPubMed
51. 51.↵
    2. Patsalides AD,
    3. Atac G,
    4. Hedge U, et al

    . Lymphomatoid granulomatosis: abnormalities of the brain at MR imaging. Radiology 2005;237:265–73 doi:10.1148/radiol.2371041087 pmid:16100084

    CrossRefPubMed
52. 52.↵
    2. De Graaff HJ,
    3. Wattjes MP,
    4. Rozemuller-Kwakkel AJ, et al

    . Fatal B-cell lymphoma following chronic lymphocytic inflammation with pontine perivascular enhancement responsive to steroids. JAMA Neurol 2013;70:915–18 doi:10.1001/jamaneurol.2013.2016 pmid:23649857

    CrossRefPubMed
53. 53.↵
    2. Dang YL,
    3. Kok HK,
    4. McKelvie PA, et al

    . Chronic lymphocytic infiltration with pontine perivascular enhancement responsive to steroids (CLIPPERS) and its association with Epstein-Barr Virus (EBV)-related lymphomatoid granulomatosis: a case report. BMC Neurol 2021;21:80 doi:10.1186/s12883-021-02110-1 pmid:33602163

    CrossRefPubMed
54. 54.↵
    2. Soleja M,
    3. Jaso JM,
    4. Chen W, et al

    . Lymphomatoid granulomatosis of the central nervous system (CNS-LYG) posing a management challenge. Clin Case Rep 2021;9:e04808 doi:10.1002/ccr3.4808 pmid:34512987

    CrossRefPubMed
55. 55.↵
    2. Hajtovic S,
    3. Liu C,
    4. Diefenbach CM, et al

    . Epstein-Barr virus-positive primary central nervous system lymphoma in a 40-year-old immunocompetent patient. Cureus 2021;13:e12754 doi:10.7759/cureus.12754 pmid:33614348

    CrossRefPubMed
56. 56.↵
    2. Cree IA

    . The WHO Classification of Haematolymphoid Tumours. Leukemia 2022;36:1701–02 doi:10.1038/s41375-022-01625-x

    CrossRefPubMed
57. 57.↵
    2. Pons-Escoda A,
    3. García-Ruíz A,
    4. Naval-Baudin P, et al

    . Diffuse large B-cell Epstein-Barr virus-positive primary CNS lymphoma in non-AIDS patients: high diagnostic accuracy of DSC perfusion metrics. AJNR Am J Neuroradiol 2022;43:1567–74 doi:10.3174/ajnr.A7668 pmid:36202547

    CrossRefPubMed
58. 58.↵
    2. Bathla G,
    3. Hegde A

    . Lymphomatous involvement of the central nervous system. Clin Radiol 2016;71:602–09 doi:10.1016/j.crad.2016.02.006 pmid:27038652

    CrossRefPubMed
59. 59.↵
    2. Neska-Matuszewska M,
    3. Bladowska J,
    4. Sąsiadek M, et al

    . Differentiation of glioblastoma multiforme, metastases and primary central nervous system lymphomas using multiparametric perfusion and diffusion MR imaging of a tumor core and a peritumoral zone: searching for a practical approach. PLoS One 2018;13:e0191341 doi:10.1371/journal.pone.0191341 pmid:29342201

    CrossRefPubMed
60. 60.↵
    2. Talybov R,
    3. Beylerli O,
    4. Mochalov V, et al

    . Multiparametric MR imaging features of primary CNS lymphomas. Front Surg 2022;9:887249 doi:10.3389/fsurg.2022.887249 pmid:35510125

    CrossRefPubMed
61. 61.↵
    2. Lee HY,
    3. Kim HS,
    4. Park JW, et al

    . Atypical imaging features of Epstein-Barr virus–positive primary central nervous system lymphomas in patients without AIDS. AJNR Am J Neuroradiol 2013;34:1562–67 doi:10.3174/ajnr.A3429 pmid:23413244

    CrossRefPubMed
62. 62.↵
    2. Gandhi MK,
    3. Hoang T,
    4. Law SC, et al

    . EBV-associated primary CNS lymphoma occurring after immunosuppression is a distinct immunobiological entity. Blood 2021;137:1468–77 doi:10.1182/blood.2020008520 pmid:33202420

    CrossRefPubMed
63. 63.↵
    2. Mahale P,
    3. Shiels MS,
    4. Lynch CF, et al

    . Incidence and outcomes of primary central nervous system lymphoma in solid organ transplant recipients. Am J Transplant 2018;18:453–61 doi:10.1111/ajt.14465 pmid:28805292

    CrossRefPubMed
64. 64.↵
    2. Suh CH,
    3. Kim HS,
    4. Lee SS, et al

    . Atypical imaging features of primary central nervous system lymphoma that mimics glioblastoma: utility of intravoxel incoherent motion MR imaging. Radiology 2014;272:504–13 doi:10.1148/radiol.14131895 pmid:24697149

    CrossRefPubMed
65. 65.↵
    2. Sauter A,
    3. Faul C,
    4. Bitzer M, et al

    . Imaging findings in immunosuppressed patients with Epstein Barr virus-related B cell malignant lymphoma. AJR Am J Roentgenol 2010;194:W141–49 doi:10.2214/AJR.09.3264 pmid:20093565

    CrossRefPubMed
66. 66.↵
    2. Balaguer-Rosello A,
    3. Piñana JL,
    4. Bataller L, et al

    . Central nervous system involvement in Epstein–Barr virus-related post-transplant lymphoproliferative disorders after allogeneic hematopoietic stem cell transplantation. Transplant Cell Ther 2021;27:261.e1–261.e7 doi:10.1016/j.jtct.2020.12.019 pmid:33781531

    CrossRefPubMed
67. 67.↵
    2. Lee ES,
    3. Locker J,
    4. Nalesnik M, et al

    . The association of Epstein-Barr virus with smooth-muscle tumors occurring after organ transplantation. N Engl J Med 1995;332:19–25 doi:10.1056/NEJM199501053320104 pmid:7990861

    CrossRefPubMed
68. 68.↵
    2. Raheja A,
    3. Sowder A,
    4. Palmer C, et al

    . Epstein-Barr virus-associated smooth muscle tumor of the cavernous sinus: a delayed complication of allogenic peripheral blood stem cell transplantation: case report. J Neurosurg 2017;126:1479–83 doi:10.3171/2016.4.JNS16290 pmid:27341041

    CrossRefPubMed
69. 69.↵
    2. Paez-Nova M,
    3. Andaur K,
    4. García-Ballestas E, et al

    . Primary intracranial smooth muscle tumor associated with Epstein-Barr virus in immunosuppressed children: two cases report and review of literature. Childs Nerv Syst 2021;37:3923–32 doi:10.1007/s00381-021-05173-0 pmid:33884483

    CrossRefPubMed
70. 70.↵
    2. Willeke VM,
    3. Anderson MP,
    4. Mahadevan A, et al

    . Epstein Barr virus associated smooth muscle tumors in the central nervous system: a case report and systematic review of the literature. J Neurooncol 2020;147:247–60 doi:10.1007/s11060-020-03426-7 pmid:32140976

    CrossRefPubMed
71. 71.↵
    2. Lohan R,
    3. Bathla G,
    4. Gupta S, et al

    . Epstein-Barr virus (EBV)-related smooth muscle tumors of central nervous system–a report of two cases and review of literature. Clin Imaging 2013;37:564–68 doi:10.1016/j.clinimag.2012.09.019 pmid:23265981

    CrossRefPubMed
72. 72.↵
    2. Ehresman JS,
    3. Ahmed AK,
    4. Palsgrove DN, et al

    . Epstein-Barr virus-associated smooth muscle tumor involving the spine of an HIV-infected patient: case report and review of the literature. J Clin Neurosci 2018;52:145–50 doi:10.1016/j.jocn.2018.03.009 pmid:29605279

    CrossRefPubMed
73. 73.↵
    2. Purgina B,
    3. Rao UN,
    4. Miettinen M, et al

    . AIDS-related EBV-associated smooth muscle tumors: a review of 64 published cases. Patholog Res Int 2011;2011:561548 doi:10.4061/2011/561548 pmid:21437186

    CrossRefPubMed