Abstract
Neuromyelitis optica spectrum disorder (NMOSD) is a severe, inflammatory, immune-mediated astrocytopathy of the central nervous system, characterized by recurrent inflammatory events primarily involving optic nerves and the spinal cord. Recently, a triggering role of infectious events in the development of NMOSD has been suggested. Varicella zoster virus (VZV) is the agent most involved, although the linkage with anti-aquaporin-4 antibodies is so far unknown. A review of the literature on the association between NMOSD and VZV infection was carried out by searching PUBMED and EMBASE from 1975 to July 2020. A total of 13 articles concerning Herpes zoster preceding NMOSD were identified. All patients were female and the median age at NMOSD presentation was 28.5 (range 5–63) years. Four NMOSD cases occurred after chicken pox while the remaining ten after HZ. Full recovery occurred in 5/14 patients. From the review of the literature, we can infer that VZV seems to trigger LETM attacks and not the disease itself. The strict temporal relationship between VZV infection and NMOSD seems to exceed the pure chance and represents an unusual clinical scenario posing several diagnostic and management challenges.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- NMOSD:
-
Neuromyelitis optica spectrum disorder
- CNS:
-
Central nervous system
- AQP-4:
-
Anti-aquaporin-4
- MS:
-
Multiple sclerosis
- VZV:
-
Varicella-zoster virus
- CSF:
-
Cerebrospinal fluid
- LETM:
-
Longitudinally extensive transverse myelitis
References
Ahasan HA, Rafiqueuddin AK, Chowdhury MA, Azhar MA, Kabir F (1994) Neuromyelitis optica (Devic’s disease) following chicken pox. Trop Doct 24(2):75–76. https://doi.org/10.1177/004947559402400211
al-Deeb SM, Yaqub BA, Khoja WO (1993) Devic’s neuromyelitis optica and varicella. J Neurol 240(7):450–451
Bizzoco E, Lolli F, Repice AM, Hakiki B, Falcini M, Barilaro A, Taiuti R, Siracusa G, Amato MP, Biagioli T, Lori S, Moretti M, Vinattieri A, Nencini P, Massacesi L, Matà S (2009) Prevalence of neuromyelitis optica spectrum disorder and phenotype distribution. J Neurol 256(11):1891–1898. https://doi.org/10.1007/s00415-009-5171-x
Bruguier A, Ponsot G, Khouri-Dagher L, de Leersnyder H (1981) Neuromyelitis optica or Devic disease complicating chickenpox. Arch Fr Pediatr 38(10):763–764
Chusid MJ, Williamson SJ, Murphy JV, Ramey LS (1979) Neuromyelitis optica (Devic disease) following varicella infection. J Pediatr 95(5 Pt 1):737–738. https://doi.org/10.1016/s0022-3476(79)80723-4
Cohrs RJ, Koelle DM, Schuette MC, Mehta S, Pierson D, Gilden DH, Hill JM (2009) Asymptomatic alphaherpesvirus reactivation. In: Gluckman TR (ed). Herpesviridae: viral structure, life cycle and infections. Hauppauge, NY: Nova Publishers, chapter. 6: 133–168
Doutlík S, Sblová O, Kryl R, Novák M (1975). Neuromyelitis optica as a parainfectious complication of varicella. Cesk Neurol Neurochir 38(4):238–242. Czech
Feyissa AM, Singh P, Smith RG (2013) Neuromyelitis optica in patients with coexisting human immunodeficiency virus infections. Mult Scler 19:1363–1366. https://doi.org/10.1177/1352458513483891
Heerlein K, Jarius S, Jacobi C, Rohde S, Storch-Hagenlocher B, Wildemann B (2009) Aquaporin-4 antibody positive longitudinally extensive transverse myelitis following varicella zoster infection. J Neurol Sci 276:184–186. https://doi.org/10.1016/j.jns.2008.08.015
Insinga RP, Itzler RF, Pellissier JM, Saddier P, Nikas AA (2005) The incidence of herpes zoster in a United States administrative database. J Gen Intern Med. https://doi.org/10.1111/j.1525-1497.2005.0150.x
Jarius S, Eichhorn P, Franciotta D, Petereit HF, Akman-Demir G, Wick M, Wildemann B (2017) The MRZ reaction as a highly specific marker of multiple sclerosis: re-evaluation and structured review of the literature. J Neurol 264(3):453–466. https://doi.org/10.1007/s00415-016-8360-4
Jarius S, Paul F, Franciotta D, Waters P, Zipp F, Hohlfeld Vincent A, Wildemann (2008) Mechanisms of disease: aquaporin-4 antibodies in neuromyelitis optica. Nat Clin Pract Neurol 4:202–214. https://doi.org/10.1038/ncpneuro0764
Jonsson DI, Sveinsson O, Hakim R, Brundin L (2019). Epidemiology of NMOSD in Sweden from 1987 to 2013: a nationwide population-based study. Neurology 93(2):e181–e189. https://doi.org/10.1212/WNL.0000000000007746
Kitley J, Leite MI, Nakashima I, Waters P, McNeillis B, Brown R, Takai Y, Takahashi T, Misu T, Elsone L, Woodhall M, George J, Boggild M, Vincent A, Jacob A, Fujihara K, Palace J (2012) Prognostic factors and disease course in aquaporin-4 antibody-positive patients with neuromyelitis optica spectrum disorder from the United Kingdom and Japan. Brain 135:1834–1849. https://doi.org/10.1093/brain/aws109
Kleinschmidt-DeMasters BK, Gilden DH (2001) Varicella-zoster virus infections of the nervous system clinical and pathologic correlates. Arch Pathol Lab Med 125(6):770–780
Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, Nakashima I, Weinshenker BG (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364(9451):2106–2112. https://doi.org/10.1016/S0140-6736(04)17551-X
Machado C, Amorim J, Rocha J, Pereira J, Lourenço E, Pinho J (2015) Neuromyelitis optica spectrum disorder and varicella-zoster infection. J Neurol Sci 15;358(1–2):520–521. https://doi.org/10.1016/j.jns.2015.09.374
Masuda S, Mori M, Arai K, Uzawa A, Muto M, Uchida T, Masuda H, Kuwabara S (2015) Epstein-Barr virus persistence and reactivation in neuromyelitis optica. J Neurol Neurosurg Psychiatry 86:1137–1142
Mathew T, Thomas K, Shivde S, Venkatesh S, Rockey SM (2017) Post herpes zoster infection neuromyelitis optica spectrum disorder. Mult Scler Relat Disord 18:93–94. https://doi.org/10.1016/j.msard.2017.09.022
Matsumoto Y, Tsuchiya M, Norshalena S, Kaneko C, Kubo J, Yamamoto T, Takahashi T, Fujihara K (2018) Severe aquaporin 4-IgG-positive neuromyelitis optica with disseminated herpes zoster in a pregnant woman successfully treated with intravenous immunoglobulin. Mult Scler J Exp Transl Clin 9;4(1). https://doi.org/10.1177/2055217318758119
Merle H, Smadja D, Cordoba A (1998) Optic neuromyelitis and bilateral acute retinal necrosis due to varicella zoster in a patient with AIDS. J Fr Ophtalmol 21(5):381–386
Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 21(339):b2535. https://doi.org/10.1371/journal.pmed.1000097
Mori M, Hosoya M, Hiwasa T, Hayakawa S, Uzawa A, Kuwabara S (2011) Detection of mumps virus RNA in cerebrospinal fluid of patients with neuromyelitis optica. Neurol Sci 32:795–799. https://doi.org/10.1007/s10072-011-0564-x
Nagel MA, Cohrs RJ, Mahalingam R, Wellish MC, Forghani B, Schiller A, Safdieh JE, Kamenkovich E, Ostrow LW, Levy M, Greenberg B, Russman AN, Katzan I, Gardner CJ, Häusler M, Nau R, Saraya T, Wada H, Goto H, de Martino M, Ueno M, Brown WD, Terborg C, Gilden DH (2008) The varicella zoster virus vasculopathies: clinical, CSF, imaging, and virologic features. Neurology 70:853–860. https://doi.org/10.1212/01.wnl.0000304747.38502.e8
Nagel MA, Forghani B, Mahalingam R, Wellish MC, Cohrs RJ, Russman AN, Katzan I, Lin R, Gardner CJ, Gilden DH (2007) The value of detecting anti-VZV IgG antibody in CSF to diagnose VZV vasculopathy. Neurology 68:1069–1073. https://doi.org/10.1212/01.wnl.0000258549.13334.16
OskaWutzler P, Bonanni P, Burgess M, Gershon A, Sáfadi MA, Casabona G (2017) Varicella vaccination - the global experience. Expert Rev Vaccines 16(8):833–843. https://doi.org/10.1080/14760584.2017.1343669
Papp V, Iljicsov A, Rajda C, Magyari M, Koch-Henriksen N, Petersen T, Jakab G, Deme I, Nagy F, Imre P, Lohner Z, Kovács K, Birkás AJ, Köves Á, Rum G, Nagy Z, Kerényi L, Vécsei L, Bencsik K, Jobbágy Z, Diószeghy P, Horváth L, Galántai G, Kasza J, Molnár G, Simó M, Sátori M, Rózsa C, Ács P, Berki T, Lovas G, Komoly S, Illes Z (2020) A population-based epidemiological study of neuromyelitis optica spectrum disorder in Hungary. Eur J Neurol 27(2):308–317. https://doi.org/10.1111/ene.14079
Park JS, Hwang SJ, Shin JH, Kim DS (2013) A recurrent longitudinally extensive transverse myelitis with aquaporin-4(AQP4) antibody after herpes zoster. J Neurol Sci 334:69–71. https://doi.org/10.1016/j.jns.2013.07.2510
Reiber H, Lange P (1991) Quantification of virus-specific antibodies in cerebrospinal fluid and serum: sensitive and specific detection of antibody synthesis in brain. Clin Chem 37(7):1153–1160
Sellner J, Hemmer B, Mühlau M (2010) The clinical spectrum and immunobiology of parainfectious neuromyelitis optica (Devic) syndromes. J Autoimmun 34:371–379. https://doi.org/10.1016/j.jaut.2009.09.013
Sousa De, Da Silva AMP, De Moraes-Pinto MI, Succi RCM, Maria Teresa Terreri MD, Machado DM (2020) Clinical and laboratory characteristics of herpes zoster in patients with HIV/AIDS and those with juvenile systemic lupus erythematosus. Pediatr Infect Dis J 39(7):624–627. https://doi.org/10.1097/INF.0000000000002617
Suda M, Tsutsumiuchi M, Uesaka Y, Hayashi N (2017) A case of anti aquapolin-4 antibody positive myelitis with hyperhidrosis, following herpes zoster. Rinsho Shinkeigaku 31;57(1):26–28. https://doi.org/10.5692/clinicalneurol.cn-000820
Tan CT, Mao Z, Qiu W, Hu X, Wingerchuk DM, Weinshenker BG (2016) International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 86:491–2. https://doi.org/10.1212/WNL.0000000000002366
Tarlinton RE, Khaibullin T, Granatov E, Martynova E, Rizvanov A, Khaiboullina S (2019) The interaction between viral and environmental risk factors in the pathogenesis of multiple sclerosis. Int J Mol Sci 14;20(2). https://doi.org/10.3390/ijms20020303
Tenembaum S, Chitnis T, Nakashima I, Collongues N, McKeon A, Levy M, Rostasy K (2016) Neuromyelitis optica spectrum disorders in children and adolescents. Neurology 87(9 Suppl 2):S59–S665. https://doi.org/10.1212/WNL.0000000000002824
Turco EC, Curti E, Maffini V, Pisani F, Granella F (2020) Neuromyelitis optica spectrum disorder attack triggered by herpes zoster infection. Mult Scler Int 25(2020):6151258. https://doi.org/10.1155/2020/6151258
Wingerchuk DM, Hogancamp WF, O’Brien PC, Weinshenker BG (1999) The clinical course of neuromyelitis optica (Devic’s syndrome). Neurology 53:1107–1111. https://doi.org/10.1212/wnl.53.5.1107
Wang X, Zhang X, Yu Z, Zhang Q, Huang D, Yu S (2018) Long-term outcomes of varicella zoster virus infection-related myelitis in 10 immunocompetent patients. J Neuroimmunol 15(321):36–40. https://doi.org/10.1016/j.jneuroim.2018.05.005
Zhong X, Zhou Y, Lu T, Wang Z, Fang L, Peng L, Kermode AG, Qiu W (2017) Infections in neuromyelitis optica spectrum disorder. J Clin Neurosci 47:14–19. https://doi.org/10.1016/j.jocn.2017.10.005
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Turco, E.C., Curti, E., Pisani, F. et al. Herpes zoster preceding neuromyelitis optica spectrum disorder: casual or causal relationship? A systematic literature review. J. Neurovirol. 28, 201–207 (2022). https://doi.org/10.1007/s13365-022-01065-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13365-022-01065-4