Top

Published in:

Open Access 01-11-2024 | Meningoencephalitis | Brief Report

A meningoencephalitis outbreak associated with echovirus type 18 (E18) in south-western Hungary in mid-2023

Authors: Károly Takáts, Benigna Balázs, Ákos Boros, Dávid Sipos, Zoltán Péterfi, Márk Harmat, Dávid Varga, Zita Zengő-Bedő, Péter Pankovics, Dr. Gábor Reuter

Published in: Archives of Virology | Issue 11/2024

Abstract

Echovirus type 18 (E18) is a member of the genus Enterovirus of the family Picornaviridae. In this study, we investigated the characteristics of E18 infections in hospitalized adults with meningoencephalitis that occurred during an unusual epidemic in south-western Hungary in mid-2023. Five (6.1%) out of 82 cerebrospinal fluid specimens that were tested were positive for an enterovirus, four of which were E18 (OR372160 and PP861087-PP861090). Headache (100%), fever (75%), retrobulbar pain (50%), nausea (50%), joint/limb pain (50%), exanthema, photophobia, and vomiting were the most common symptoms. Sequence analysis showed that these viruses were related to unpublished emerging E18 strains from France (2022/2023) and China (2019/2020). Further study is necessary to monitor the circulation of epidemic/pandemic E18 variants over time.

Available only for authorised users

Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, Simmonds P, Skern T, Stanway G, Yamashita T.,(2017) ICTV virus taxonomy profile: Picornaviridae. J Gen Virol 98:2421–2422. https://doi.org/10.1099/jgv.0.000911CrossRefPubMedPubMedCentral

Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG, Smith DB (2018) Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res 46(D1):D708–D717. https://doi.org/10.1093/nar/gkx932CrossRefPubMed

Wells AI, Coyne CB (2019) Enteroviruses: A gut-wrenching game of entry, detection, and evasion. Viruses 11(5):460. https://doi.org/10.3390/v11050460CrossRefPubMedPubMedCentral

Wang C, Li J, Liu Y, Sun Q, Liu Z (2023) Pathogenesis of enterovirus infection in central nervous system. Biosaf Health 5(4):233–239CrossRef

Simmonds P, Gorbalenya AE, Harvala H, Hovi T, Knowles NJ, Lindberg AM, Oberste MS, Palmenberg AC, Reuter G, Skern T, Tapparel C, Wolthers KC, Woo PCY, Zell R (2020) Recommendations for the nomenclature of enteroviruses and rhinoviruses. Arch Virol 165(3):793–797. https://doi.org/10.1007/s00705-019-04520-6CrossRefPubMedPubMedCentral

Eichenwald HF (1958) Epidemic diarrhea in premature and older infants caused by echo virus type 18. J Am Med Assoc 166(13):1563. https://doi.org/10.1001/jama.1958.02990130023005CrossRefPubMed

Kennett ML, Ellis AW, Lewis FA, Gust ID (1972) An epidemic associated with echovirus type 18. J Hyg (Lond) 70(2):325–334. https://doi.org/10.1017/s0022172400022373CrossRefPubMed

Miyamura K, Yamashita K, Yamadera S, Kato N, Akatsuka M, Yamazaki S (1990) An epidemic of echovirus 18 in 1988 in Japan–high association with clinical manifestation of exanthem. Japan. Jpn J Med Sci Biol 43(2):51–58. https://doi.org/10.7883/yoken1952.43.51CrossRefPubMed

Sakae K (1992) The relationship of clinical manifestations and age distribution in enterovirus infections. Kansenshogaku Zasshi 66(12):1670–1681. https://doi.org/10.11150/kansenshogakuzasshi1970.66.1670CrossRefPubMed

10.

Yamashita K, Miyamura K, Yamadera S, Kato N, Akatsuka M, Inouye S, Yamazaki S (1992) Enteroviral aseptic meningitis in Japan, 1981–1991. Jpn J Med Sci Biol 45(3):151–161. https://doi.org/10.7883/yoken1952.45.151CrossRefPubMed

11.

Norder H, Bjerregaard L, Magnius L, Lina B, Aymard M, Chomel JJ (2003) Sequencing of ‘untypable’ enteroviruses reveals two new types, EV-77 and EV-78, within human enterovirus type B and substitutions in the BC loop of the VP1 protein for known types. J Gen Virol 84(4):827–836. https://doi.org/10.1099/vir.0.18647-0CrossRefPubMed

12.

Mirand A, Archimbaud C, Henquell C, Michel Y, Chambon M, Peigue-Lafeuille H, Bailly JL (2006) Prospective identification of HEV-B enteroviruses during the 2005 outbreak. J Med Virol 78(12):1624–1634. https://doi.org/10.1002/jmv.20747CrossRefPubMed

13.

Mirand A, Henquell C, Archimbaud C, Chambon M, Charbonne F, Peigue-Lafeuille H, Bailly JL (2008) Prospective identification of enteroviruses involved in meningitis in 2006 through direct genotyping in cerebrospinal fluid. J Clin Microbiol 46(1):87–96. https://doi.org/10.1128/JCM.01020-07CrossRefPubMed

14.

Volle R, Bailly JL, Mirand A, Pereira B, Marque-Juillet S, Chambon M, Regagnon C, Brebion A, Henquell C, Peigue-Lafeuille H, Archimbaud C (2014) Variations in cerebrospinal fluid viral loads among enterovirus genotypes in patients hospitalized with laboratory-confirmed meningitis due to enterovirus. J Infect Dis 210(4):576–584. https://doi.org/10.1093/infdis/jiu178CrossRefPubMed

15.

Tsai HP, Huang SW, Wu FL, Kuo PH, Wang SM, Liu CC, Su IJ, Wang JR (2011) An echovirus 18-associated outbreak of aseptic meningitis in Taiwan: Epidemiology and diagnostic and genetic aspects. J Med Microbiol 60(9):1360–1365. https://doi.org/10.1099/jmm.0.027698-0CrossRefPubMed

16.

Onishchenko GG, Novikova NA, Efimov EI, Kniagina ON, Petrov EI, Novikov DV, Golitsyna LN, Osipova TV, Okun’ IN, Kalashnikova NA, Lipshits DA, Gracheva EV, Epifanova NV, Klimova LL, Lukovnikova LB, Fomina SG, Ershov VI, Pogodina LV (2009) Aseptic meningitis season caused by enteroviruses in 2007: Molecular-epidemiological aspects. Zh Mikrobiol Epidemiol Immunobiol 2:24–30

17.

Krumbholz A, Egerer R, Braun H, Schmidtke M, Rimek D, Kroh C, Hennig B, Groth M, Sauerbrei A, Zell R (2016) Analysis of an echovirus 18 outbreak in Thuringia, Germany: Insights into the molecular epidemiology and evolution of several enterovirus species B members. Med Microbiol Immunol 205(5):471–483. https://doi.org/10.1007/s00430-016-0464-zCrossRefPubMed

18.

de Crom SCM, Rossen JWA, de Moor RA, Veldkamp EJM, van Furth AM, Obihara CC (2016) Prospective assessment of clinical symptoms associated with enterovirus and parechovirus genotypes in a multicenter study in Dutch children. J Clin Virol 77:15–20. https://doi.org/10.1016/j.jcv.2016.01.014CrossRefPubMed

19.

Othman I, Mirand A, Slama I, Mastouri M, Peigue-Lafeuille H, Aouni M, Bailly JL (2015) Enterovirus migration patterns between France and Tunisia. PLoS ONE 10:e0145674. https://doi.org/10.1371/journal.pone.0145674CrossRefPubMedPubMedCentral

20.

Cabrerizo M, Díaz-Cerio M, Muñoz‐Almagro C, Rabella N, Tarragó D, Romero MP, Pena MJ, Calvo C, Rey‐Cao S, Moreno‐Docón A, Martínez‐Rienda I, Otero A, Trallero G (2017) Molecular epidemiology of enterovirus and parechovirus infections according to patient age over a 4‐year period in Spain. J Med Virol 89(3):435–442. https://doi.org/10.1002/jmv.24658CrossRefPubMed

21.

Dumaidi K, Al-Jawabreh A, Samarah F, Zraiqi A, Yaseen D (2018) Genetic diversity of the enteroviruses detected from cerebrospinal fluid (CSF) samples of patients with suspected aseptic meningitis in northern West Bank, Palestine in 2017. PLoS ONE 13(12):e0202243. https://doi.org/10.1371/journal.pone.0202243CrossRefPubMedPubMedCentral

22.

Kim MJ, Lee JE, Kim KG, Park DW, Cho SJ, Kim TS, Kee HY, Kim SH, Park HJ, Seo MH, Chung JK, Seo JJ (2023) Long-term sentinel surveillance of enteroviruses in Gwangju, South Korea, 2011–2020. Sci Rep 13(1):2798. https://doi.org/10.1038/s41598-023-29461-8CrossRefPubMedPubMedCentral

23.

Yao X, Bian LL, Lu WW, Li JX, Mao QY, Wang YP, Gao F, Wu X, Ye Q, Xu M, Li XL, Zhu FC, Liang ZL (2015) Enterovirus spectrum from the active surveillance of hand foot and mouth disease patients under the clinical trial of inactivated Enterovirus A71 vaccine in Jiangsu, China, 2012–2013. J Med Virol 87(12):2009–2017. https://doi.org/10.1002/jmv.24275CrossRefPubMed

24.

Zhang H, Zhao Y, Liu H, Sun H, Huang X, Yang Z, Ma S (2017) Molecular characterization of two novel echovirus 18 recombinants associated with hand-foot-mouth disease. Sci Rep 7:8448. https://doi.org/10.1038/s41598-017-09038-yCrossRefPubMedPubMedCentral

25.

Chen X, Ji T, Guo J, Wang W, Xu W, Xie Z (2019) Molecular epidemiology of echovirus 18 circulating in mainland China from 2015 to 2016. Virol Sin 34(1):50–58. https://doi.org/10.1007/s12250-018-0080-8CrossRefPubMedPubMedCentral

26.

Sun Y, Miao Z, Yan J, Gong L, Chen Y, Chen Y, Mao H, Zhang Y (2019) Sero-molecular epidemiology of enterovirus-associated encephalitis in Zhejiang Province, China, from 2014 to 2017. Int J Infect Dis 79:58–64. https://doi.org/10.1016/j.ijid.2018.11.002CrossRefPubMed

27.

Chen L, Xu SJ, Yao XJ, Yang H, Zhang HL, Meng J, Zeng HR, Huang XH, Zhang RL, He YQ (2020) Molecular epidemiology of enteroviruses associated with severe hand, foot and mouth disease in Shenzhen, China, 2014–2018, Arch Virol. 165(10):2213–2227. https://doi.org/10.1007/s00705-020-04734-z

28.

Kang Y, Hua Y, Sun M, Qian J, Zhu P (2021) A potential new recombinant echovirus 18 strain detected in a 4-year-old child with encephalitis in China in 2019. Arch Virol 166(4):1231–1236. https://doi.org/10.1007/s00705-020-04907-wCrossRefPubMed

29.

Wang J, Meng M, Xu H, Wang T, Liu Y, Yan H, Liu P, Qin D, Yang Q (2021) Analysis of enterovirus genotypes in the cerebrospinal fluid of children associated with aseptic meningitis in Liaocheng, China, from 2018 to 2019. BMC Infect Dis 21:405. https://doi.org/10.1186/s12879-021-06112-9CrossRefPubMedPubMedCentral

30.

Yang X, Wu Y, Zhao H, Liu P, Liang L, Yin A (2024) Emergence and circulation of enterovirus B species in infants in southern China: A multicenter retrospective analysis. Virulence 15(1):2329569. https://doi.org/10.1080/21505594.2024.2329569CrossRefPubMedPubMedCentral

31.

Xi H, Tian Y, Shao H, Yin X, Ma L, Yang P, Li X (2023) An outbreak of nosocomial infection of neonatal aseptic meningitis caused by echovirus 18. Epidemiol Infect 151:e107. https://doi.org/10.1017/S0950268823000973CrossRefPubMedPubMedCentral

32.

Bubba L, Broberg EK, Jasir A, Simmonds P, Harvala H (2020) on behalf of the Enterovirus study collaborators. Circulation of non-polio enteroviruses in 24 EU and EEA countries between 2015 and 2017: a retrospective surveillance study. Lancet Infect Dis 20(3):350–361. https://doi.org/10.1016/S1473-3099(19)30566-3CrossRefPubMed

33.

Bujaki E, Farkas Á, Rigó Z, Takács M (2020) Distribution of enterovirus genotypes detected in clinical samples in Hungary, 2010–2018, Acta Microbiologica et Immunologica Hungarica. 67(4):201–208. https://doi.org/10.1556/030.2020.01200

34.

Boros A, Pankovics P, Knowles NJ, Reuter G (2012) Natural interspecies recombinant bovine/porcine enterovirus in sheep. J Gen Virol 93(9):1941–1951. https://doi.org/10.1099/vir.0.041335-0CrossRefPubMed

35.

Boros Á, Pankovics P, Reuter G (2011) Characterization of a novel porcine enterovirus in domestic pig in Hungary. Infect Genet Evol 11:1096–1102. https://doi.org/10.1016/j.meegid.2011.04.003CrossRefPubMed

36.

Nicholas KB, Nicolas HB (1997) Jr., GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the author.

37.

Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Mol Biol Evol 35(2):518–522. https://doi.org/10.1093/molbev/msx281CrossRefPubMed

38.

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37(5):1530–1534. https://doi.org/10.1093/molbev/msaa015CrossRefPubMedPubMedCentral

39.

Kalyaanamoorthy S, Minh BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285CrossRefPubMedPubMedCentral

40.

Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296. https://doi.org/10.1093/nar/gkab301CrossRefPubMedPubMedCentral

41.

Zhou J, Xie X, Fang L, Jin Y, Zeng H, Li J, Liu F, Li C, Li H, Liu Q, Zhang Y, Zheng H (2021) Genetic characteristics analysis of VP1 sequence of echovirus 18 that caused an acute gastroenteritis outbreak in Guangdong Province, China, Chin. J Virol 37(01):133–139. https://doi.org/10.13242/j.cnki.bingduxuebao.003843CrossRef

42.

Guo W, Xu D, Cong S, Du Z, Li L, Zhang M, Feng C, Bao G, Sun H, Yang Z, Ma S (2022) Co-infection and enterovirus B: post EV-A71 mass vaccination scenario in China. BMC Infect Dis 22(1):671. https://doi.org/10.1186/s12879-022-07661-3CrossRefPubMedPubMedCentral

43.

Dorsett M, Liang SY (2016) Diagnosis and treatment of central nervous system infections in the emergency department. Emerg Med Clin North Am 34(4):917–942. https://doi.org/10.1016/j.emc.2016.06.013CrossRefPubMedPubMedCentral

Title: A meningoencephalitis outbreak associated with echovirus type 18 (E18) in south-western Hungary in mid-2023
Authors: Károly Takáts
Benigna Balázs
Ákos Boros
Dávid Sipos
Zoltán Péterfi
Márk Harmat
Dávid Varga
Zita Zengő-Bedő
Péter Pankovics
Dr. Gábor Reuter
Publication date: 01-11-2024
Publisher: Springer Vienna
Keyword: Meningoencephalitis
Published in: Archives of Virology / Issue 11/2024
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-024-06166-5

Construction of a full-length infectious cDNA clone of zucchini tigre mosaic virus infecting snake gourd and genetic diversity analysis based on complete genome sequences of ZTMV isolates

Brief Report

Isolation and characterization of a subtype G2c variant of porcine epidemic diarrhea virus that adapts well to cell culture

Diarrhea
Original Article

Complete genome sequences of two novel Ralstonia jumbo phages isolated from leaf litter compost

Open Access
Annotated Sequence Record

Characterization and genomic analysis phage PmP19, a novel Proteus mirabilis phage with a broad host range

Brief Report

Molecular characterization and phylogenetic analysis of infectious laryngotracheitis virus isolates from commercial chicken flocks in Turkey

Croup
Original Article

Isolation and characterization of Yersinia phage fMtkYen3-01

Open Access
Yersinia
Brief Report

Keynote series | Spotlight on menopause

Menopause
Video Series

Menopause can have a significant impact on the body, with effects ranging beyond the endocrine and reproductive systems. Learn about the broader systemic effects of menopause, so you can help patients in your clinics through the transition.

Launching: Thursday 12th December 2024

Prof. Martha Hickey

Dr. Claudia Barth

Dr. Samar El Khoudary

Developed by: Springer Medicine

Keynote webinar | Spotlight on adolescent vaping

Live
Webinar | 29-01-2025 | 18:00 (CET)

Growing numbers of young people are using e-cigarettes, despite warnings of respiratory effects and addiction. How can doctors tackle the epidemic, and what health effects should you prepare to manage in your clinics?

Watch it live: Wednesday 29th January, 18:00-19:30 CET

Prof. Ann McNeill

Dr. Debbie Robson

Benji Horwell

Developed by: Springer Medicine

Join the webinar

Keynote webinar | Spotlight on modern management of frailty

Frailty in Geriatric Patients
On-demand webinar

Frailty has a significant impact on health and wellbeing, especially in older adults. Our experts explain the factors that contribute to the development of frailty and how you can manage the condition and reduce the risk of disability, dependency, and mortality in your patients.

Prof. Alfonso Cruz-Jentoft

Prof. Barbara C. van Munster

Prof. Mirko Petrovic

Developed by: Springer Medicine

Watch now

A quick guide to ECGs

Electrocardiography
Training Course

Improve your ECG interpretation skills with this comprehensive, rapid, interactive course. Expert advice provides detailed feedback as you work through 50 ECGs covering the most common cardiac presentations to ensure your practice stays up to date.

PD Dr. Carsten W. Israel

Developed by: Springer Medizin

Start the cases

At a glance: The STEP trials

Obesity
Clinical Trial Summary

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote series | Spotlight on menopause

Springer Medicine

Abstract

Please log in to get access to this content