Cited by 155Viral Infections and Immunology ResearchEvolution and Genetic DynamicsVirology and Viral Diseases

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Molecular Epidemiology and Genetic Diversity of Echovirus Type 30 (E30): Genotypes Correlate with Temporal Dynamics of E30 Isolation

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Oberste, M. Steven, Maher, Kaija, Kennett, Margery L., Campbell, Janice J., Carpenter, Michael S., Schnurr, David, Pallansch, Mark A.·1999·Journal of Clinical Microbiology

DOI 10.1128/jcm.37.12.3928-3933.1999PMC PMC85848

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Abstract

Echovirus type 30 (E30) (genus, Enterovirus; family, Picornaviridae) has caused large outbreaks of aseptic meningitis in many regions of the world in the last 40 years. U.S. enterovirus surveillance data for the period 1961 to 1998 indicated that the annual proportion of E30 isolations relative to total enterovirus isolations has fluctuated widely, from a low of 0% in 1966 to a high of 42% in 1998. Peaks of E30 isolations occurred in the years 1968 to 1969, 1981 to 1984, 1990 to 1993, and 1997 to 1998, coincident with large nationwide outbreaks of E30-associated aseptic meningitis. Analysis of the complete VP1 sequence (876 nucleotides) of 136 E30 strains isolated in geographically dispersed regions of the United States and nine other countries between 1956 and 1998 indicated that the currently circulating E30 strains are genetically distinct from those isolated 30 to 40 years ago. Phylogenetic reconstruction demonstrated the existence of at least four distinct genetic groups, three of which have not been isolated in North America since 1981. Two of the three groups disappeared during periods when E30 was isolated infrequently. All North American E30 strains isolated after 1988 were closely related to one another, and all post-1993 isolates were of the same lineage within this group. Surveillance data indicate that E30 causes large national outbreaks of 2- to 4-year durations, separated by periods of relative quiescence. Our results show that shifts in the overall genetic diversity of E30 and the predominant genetic type correlate temporally with the dynamics of E30 isolation. The sequence data also provide a basis for the application of molecular techniques for future epidemiologic investigations of E30 disease.

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Global phylodynamics of Echovirus 30 revealed differential behavior among viral lineages
Lema, C. L., Torres, C., van der Sanden, S., Cisterna, D. M., Freire, M. C., & Gomez, R. M. (2019) · Virology · doi:10.1016/j.virol.2019.02.012 · Cited by 37
Phylogenetic Patterns of Human Coxsackievirus B5 Arise from Population Dynamics between Two Genogroups and Reveal Evolutionary Factors of Molecular Adaptation and Transmission
Henquell, C., Mirand, A., Richter, J., Schuffenecker, I., Böttiger, B. E., Diedrich, S., Terletskaia‐Ladwig, E., Christodoulou, C., Peigue‐Lafeuille, H., & Bailly, J. (2013) · Journal of Virology · doi:10.1128/jvi.02075-13 · Cited by 42
Aseptic meningitis in Germany associated with echovirus type 13
Diedrich, S., & Schreier, E. (2001) · BMC Infectious Diseases · doi:10.1186/1471-2334-1-14 · Cited by 36
Analysis of enterovirus types in patients with symptoms of aseptic meningitis in 2014 in Shandong, China
Chen, P., Lin, X., Liu, G., Wang, S., Song, L., Tao, Z., & Xu, A. (2018) · Virology · doi:10.1016/j.virol.2018.01.022 · Cited by 34
Simultaneous type 1 diabetes onset in mother and son coincident with an enteroviral infection
Maria, H., Elshebani, A., Anders, Ö., Tuvemo, T., & Frisk, G. (2005) · Journal of Clinical Virology · doi:10.1016/j.jcv.2004.12.009 · Cited by 34
Phylogenetic analysis of Ljungan virus and A-2 plaque virus, new members of the Picornaviridae
Lindberg, A., & Johansson, S. (2002) · Virus Research · doi:10.1016/s0168-1702(02)00018-7 · Cited by 33
An Echovirus Type 33 Winter Outbreak in New Zealand
Huang, Q. S., Carr, J. M., Nix, W. A., Oberste, M. S., Kilpatrick, D. R., Pallansch, M. A., Croxson, M. C., Lindeman, J., Baker, M. G., & Grimwood, K. (2003) · Clinical Infectious Diseases · doi:10.1086/376915 · Cited by 33
“sequences (843 nucleotides) were amplified and sequenced [19].”
MethodSelf-citation
An echovirus 18-associated outbreak of aseptic meningitis in Taiwan: epidemiology and diagnostic and genetic aspects
Tsai, H., Huang, S.-W., Wu, F.-L., Kuo, P.-H., Wang, S.-M., Liu, C., Su, I., & Wang, J. (2011) · Journal of Medical Microbiology · doi:10.1099/jmm.0.027698-0 · Cited by 32
Genetic diversity of echovirus 30 involved in aseptic meningitis cases in Brazil (1998–2008)
dos Santos, G. P. L., da Costa, E. V., Tavares, F. N., da Costa, L. J., & da Silva, E. E. (2011) · Journal of Medical Virology · doi:10.1002/jmv.22235 · Cited by 30
“…and has often been associated with aseptic meningitis, responsible for many of the outbreaks and sporadic cases worldwide throughout history [Oberste et al., 1999; Trallero et al., 2000; Savolainen et al., 2001; Bailly et al., 2002; Dos Santos et al., 2006; Cabrerizo et al., 2008; Castro et…”
BackgroundMethodResultInfluential
Type-Specific Detection of Echovirus 30 Isolates Using Degenerate Reverse Transcriptase PCR Primers
Kilpatrick, D. R., Quay, J., Pallansch, M. A., & Oberste, M. S. (2001) · Journal of Clinical Microbiology · doi:10.1128/jcm.39.4.1299-1302.2001 · Cited by 28
“EV isolations reported to the Centers for Disease Control and Prevention by state and territorial public health laboratories ( 20 ).”
BackgroundMethodResultInfluentialSelf-citation
Early Entry Events in Echovirus 30 Infection
Vandesande, H., Laajala, M., Kantoluoto, T., Ruokolainen, V., Lindberg, A. M., & Marjomäki, V. (2020) · Journal of Virology · doi:10.1128/jvi.00592-20 · Cited by 26
Strain-dependent effects of clinical echovirus 30 outbreak isolates at the blood-CSF barrier
Dahm, T., Adams, O., Boettcher, S., Diedrich, S., Morozov, V., Hansman, G. S., Fallier‐Becker, P., Schädler, S., Burkhardt, C. J., Weiß, C., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1061-4 · Cited by 26
“and occurrence in meningitis outbreaks with E-30 [51].”
Distinct migratory pattern of naive and effector T cells through the blood–CSF barrier following Echovirus 30 infection
Wiatr, M., Stump-Guthier, C., Latorre, D., Uhlig, S., Weiß, C., Ilonen, J., Engelhardt, B., Ishikawa, H., Schwerk, C., Schroten, H., et al. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1626-x · Cited by 24
Molecular epidemiology of echoviruses 11 and 30 in Russia: Different properties of genotypes within an enterovirus serotype
Yarmolskaya, M. S., Shumilina, E. Y., Ivanova, O. E., Drexler, J. F., & Lukashev, A. N. (2015) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2014.12.033 · Cited by 24
Enteroviral Infection Outbreak in the Republic of Belarus: Principal Characteristics and Phylogenetic Analysis of Etiological Agents
Amvrosіeva, T. V., Paklonskaya, N. V., Biazruchka, A. A., Kazinetz, O. N., Bohush, Z. F., & Фисенко, Е. Г. (2006) · Central European Journal of Public Health · doi:10.21101/cejph.a3369 · Cited by 24
“Results of phylogenetic analysis showed that sequences of all Belarusian ECHO 30 isolates belong to the major genotype of ECHO 30 which has been circulating for last 15 years in countries of Europe and North America (22, 25): the maximum of genetic distances between them did not exceed 0.”
BackgroundInfluential
Enterovirus Surveillance (EVSurv) in Germany
Keeren, K., Böttcher, S., & Diedrich, S. (2021) · Microorganisms · doi:10.3390/microorganisms9102005 · Cited by 23
Molecular evolution and epidemiology of echovirus 6 in Finland
Smura, T., Kakkola, L., Blomqvist, S., Klemola, P., Parsons, A., Kallio‐Kokko, H., Savolainen‐Kopra, C., Kainov, D. E., & Roivainen, M. (2013) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2013.02.011 · Cited by 23
Phylogenetic analysis of Echovirus 30 isolated during the 2005 outbreak in France reveals existence of multiple lineages and suggests frequent recombination events
Lévêque, N., Jacques, J., Renois, F., Antona, D., Abély, M., Chomel, J. J., & Andréoletti, L. (2010) · Journal of Clinical Virology · doi:10.1016/j.jcv.2010.03.011 · Cited by 23
Genetic and phenotypic diversity of echovirus 30 strains and pathogenesis of type 1 diabetes
Paananen, A., Savolainen‐Kopra, C., Kaijalainen, S., Vaarala, O., Hovi, T., & Roivainen, M. (2007) · Journal of Medical Virology · doi:10.1002/jmv.20922 · Cited by 23
“The last genotype spread all over the world and caused outbreaks of aseptic meningitis, especially in children, from the mid 1990s onward [Oberste et al., 1999; Savolainen et al., 2001; Palacios et al., 2002].”
Background
Molecular epidemiology of echovirus 30 in Fujian, China between 2001 and 2011
Yang, X., Yan, Y., Weng, Y., He, A., Zhang, H., Chen, W., & Zhou, Y. (2013) · Journal of Medical Virology · doi:10.1002/jmv.23503 · Cited by 22
“The sequence of the gene encoding the complete VP1 capsid protein was generated for each isolate as two overlapping fragments with PCR primers (008, 013, 012, and 011) [Oberste et al., 1999b].”
BackgroundMethodInfluential
Echovirus 30 meningitis epidemic followed by an outbreak-specific RT-qPCR
Österback, R., Kalliokoski, T., Lähdesmäki, T., Peltola, V. T., Ruuskanen, O., & Waris, M. E. (2015) · Journal of Clinical Virology · doi:10.1016/j.jcv.2015.05.012 · Cited by 22
“Previously, genetic diversity of E-30 has been studied and the virus variants are phylogenetically divided into several genogroups [2–5].”
Background
Molecular characterization of enteroviruses detected in Gyeong-Ju and Po-Hang provinces of Korea in 2003
Jeong, E., Lee, J., Kim, M.-S., Bae, G., Jung, C., Lee, K., Choi, S.-M., Kim, D. K., Lee, D., Kim, W.-D., et al. (2010) · Archives of Virology · doi:10.1007/s00705-010-0755-4 · Cited by 22
“[16] classified EV30 into five genotypes (1, 2, 3, 4, and 5) and two subgroups (4a and 4b).”
Method
FDJS03 Isolates Causing an Outbreak of Aseptic Meningitis in China That Evolved from a Distinct Echovirus 30 Lineage Imported from Countries of the Commonwealth of Independent States
Zhao, Y. N., Perlin, D. S., Park, S., Jiang, R. J., Chen, L., Chen, Y., Gardiner, R., & Jiang, Q. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.01049-06 · Cited by 22
“Viral RNA was extracted from 200 lo f tissue culture supernatant and then reversely transcribed ( 15 ).”
BackgroundMethodResultInfluential
Genetic variability within the VP1 coding region of echovirus type 30 isolates
Künkel, U., & Schreier, E. (2000) · Archives of Virology · doi:10.1007/s007050070102 · Cited by 21
“[11] by analysing VP1 sequences of ECV30 strains isolated in the United States and other countries.”
Background
Molecular sub-grouping of enterovirus reference and wild type strains into distinct genetic clusters using a simple RFLP assay
Siafakas, N., Markoulatos, P., Vlachos, C., Stanway, G., Tzanakaki, G., & Kourea-Kremastinou, J. (2003) · Molecular and Cellular Probes · doi:10.1016/s0890-8508(03)00029-x · Cited by 20
Pathological Characteristics of Echovirus 30 Infection in a Mouse Model
Li, J., Zhang, G., Sun, Q., Zhang, K., Lu, H., Xiao, J., Han, Z., Zhao, H., Xu, W., Zhang, Y., et al. (2022) · Journal of Virology · doi:10.1128/jvi.00129-22 · Cited by 19
Molecular characterization of echovirus 30-associated outbreak of aseptic meningitis in Korea in 2008.
Choi, Y. J., Park, K. S., Baek, K. A., Jung, E. H., Nam, H. S., Kim, Y. B., & Park, J. (2010) · PubMed · Cited by 19
A decade of enterovirus genetic diversity in Belgium
Wollants, E., Beller, L., Beuselinck, K., Bloemen, M., Lagrou, K., Reynders, M., & Ranst, M. A. V. (2019) · Journal of Clinical Virology · doi:10.1016/j.jcv.2019.104205 · Cited by 19
Description of a widespread outbreak of aseptic meningitis due to echovirus 30 in Rio de Janeiro state, Brazil
Pinto, V. L., Rebelo, M. C., da Costa, E. V., da Silva, E. E., & Bóia, M. N. (2009) · The Brazilian Journal of Infectious Diseases · doi:10.1590/s1413-86702009000500011 · Cited by 19
“Molecular epidemiology studies performed during outbreaks evidenced five different genotypes of echovirus 30, which is the proposed explanation for this epidemiological behavior [17,18].”
Background
Molecular epidemiology and dual serotype specificity detection of echovirus 11 strains in Finland
Savolainen‐Kopra, C., Al‐Hello, H., Paananen, A., Blomqvist, S., Klemola, P., Sobotová, Z., & Roivainen, M. (2008) · Virus Research · doi:10.1016/j.virusres.2008.10.003 · Cited by 18
“…African strains of -11 have been shown to cluster chronologically (Bouslama et al., 007), a characteristic similar to another HEV-B virus, echovirus 30 Oberste et al., 1999; Palacios et al., 2002; Savolainen et al., 2001). his feature can also be seen among the Finnish E-11 strains of enogroup D.”
Background
Phylogenetic analysis of complete VP1 sequences of echoviruses 11 and 6: high genetic diversity and circulation of genotypes with a wide geographical and temporal range
Farès, W., Rezig, D., Seghier, M., Yahia, A. B., Touzi, H., & Triki, H. (2011) · Journal of Medical Microbiology · doi:10.1099/jmm.0.028795-0 · Cited by 17
Phylogenetic and serological characterization of echovirus 11 and echovirus 19 strains causing uveitis
Lukashev, A. N., Lashkevich, V. A., Koroleva, G. A., & Karganova, G. G. (2002) · Archives of Virology · doi:10.1007/s705-002-8307-2 · Cited by 16
“These findings practically exclude the possibility that the echoviruses were occasional isolates and were not associated with the disease, because occasional isolates of enteroviruses from different locations are usually much more divergent [ 28 ].”
Result
Mosaic genome structure of echovirus type 30 that circulated in Taiwan in 2001
Chen, G., Huang, J.-H., Lo, Y.-L., Tsao, K.-C., & Chang, S. (2007) · Archives of Virology · doi:10.1007/s00705-007-1018-x · Cited by 15
“Pairwise comparison was employed in the molecular typing method [12, 13] using the program Needle in the EMBOSS package [22].”
MethodInfluential
Use of the 5′ untranslated region and VP1 region to examine the molecular diversity in enterovirus B species
Zhou, F., Wang, Q., Sintchenko, V., Gilbert, G. L., O'Sullivan, M. V. N., Iredell, J. R., & Dwyer, D. E. (2014) · Journal of Medical Microbiology · doi:10.1099/jmm.0.074682-0 · Cited by 14
“Several studies have shown different clustering of E30 variants based on VP1 sequences (Oberste et al., 1999a; Lukashev et al., 2008; Palacios et al., 2002).”
Background
Analysis of enterovirus genotypes in the cerebrospinal fluid of children associated with aseptic meningitis in Liaocheng, China, from 2018 to 2019
Wang, J., Meng, M., Xu, H., Wang, T., Liu, Y., Yan, H., Liu, P., Qin, D., & Yang, Q. (2021) · BMC Infectious Diseases · doi:10.1186/s12879-021-06112-9 · Cited by 14
An approach for differentiating echovirus 30 and Japanese encephalitis virus infections in acute meningitis/encephalitis: a retrospective study of 103 cases in Vietnam
Takamatsu, Y., Uchida, L., Nga, P. T., Okamoto, K., Nabeshima, T., Thao, D. T. T., Hai, D. T., Tuyết, N. T., Duc, H. M., Luat, L. X., et al. (2013) · Virology Journal · doi:10.1186/1743-422x-10-280 · Cited by 14
“To amplify the complete VP1 gene of E30, RNA templates were subjected to reverse transcription and polymerase chain reaction (RT-PCR) using the forward primer 5′GCRTGCAATGAYTTCTCWGT-3′ and the reverse primer 5′-GCICCIGAYTGITGICCRAA-3′ [24].”
Method
Echovirus 30 associated with cases of aseptic meningitis in state of Pará, Northern Brazil
de Castro, C. M. O., Oliveira, D. D. S., Macêdo, O., Lima, M. J. L., Santana, M. B., Wanzeller, A. L. M., da Silveira, E., & Gomes, M. D. L. C. (2009) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762009000300008 · Cited by 13
“Using the classification system described by Oberste et al. (1999), it was noted that all the strains detected in PA, together with the ones from Australia (1996-1997), probably constituted a new subgroup (4c), independent of subgroup 4b (Fig. 3), with a divergence of 10.6%. Such distinctive molecular characteristics…”
BackgroundMethodResultInfluential
Enteroviruses and Parechoviruses
Pallansch, M. A., & Oberste, M. S. (2009) · Wiley eBooks · doi:10.1128/9781555815974.ch18 · Cited by 13
Self-citation
Temporal phylogeny and molecular characterization of echovirus 30 associated with aseptic meningitis outbreaks in China
Tian, X., Han, Z., He, Y., Sun, Q., Wang, W., Xu, W., Li, H., & Zhang, Y. (2021) · Virology Journal · doi:10.1186/s12985-021-01590-4 · Cited by 11
Antiviral Activity of Itraconazole against Echovirus 30 InfectionIn Vitro
Lee, J.-S., Choi, H., Song, J.-H., Ko, H., Yoon, K., & Seong, J.-M. (2017) · Osong Public Health and Research Perspectives · doi:10.24171/j.phrp.2017.8.5.05 · Cited by 12
Molecular diagnosis of echovirus 30 as the etiological agent in an outbreak of aseptic meningitis in Panama: May – June 2008
Martínez, A. A., Castillo, J., Sanchez, M. C., Zaldívar, Y. L., Mendoza, Y., Tribaldos, M., Acosta, P., Smith, R. E., & Pascale, J. M. (2012) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.2615 · Cited by 12
“In the past 40 years, echoviruses have been an important recurring cause of large outbreaks of aseptic meningitis throughout the world [6,9,16], alone or in combination with other enteroviruses [3].”
Background
Rapid Construction of Adeno-Associated Virus Vectors Expressing Multiple Short Hairpin RNAs with High Antiviral Activity Against Echovirus 30
Rothe, D., Wajant, G., Grunert, H., Zeichhardt, H., Fechner, H., & Kurreck, J. (2010) · Oligonucleotides · doi:10.1089/oli.2010.0236 · Cited by 13
“Echovirus 30 (EV-30), which is one of the most frequently isolated viruses from aseptic meningitis outbreaks worldwide (Oberste et al., 1999; CDC, 2006), is a member of the genus Enterovirus in the family Picornaviridae.”
Epidemiology of viral encephalitis
Khetsuriani, N., & Anderson, L. J. (2008) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541728.022 · Cited by 11
Molecular epidemiology of coxsackievirus type B1
Abdelkhalek, I., Seghier, M., Yahia, A. B., Touzi, H., Meddeb, Z., Triki, H., & Rezig, D. (2015) · Archives of Virology · doi:10.1007/s00705-015-2561-5 · Cited by 10
“In the literature, different genotypes and clusters for echoviruses 3, 6, 11 and 30, coxsackievirus type B4 and B5 have been described [23–29].”
Background
Molecular analysis of enterovirus in Cameroon by partial 5′UTR-VP4 gene sequencing reveals a high genetic diversity and frequency of infections
Ayukekbong, J. A., Fobisong, C., Lindh, M., Nkuo-Akenji, T., Bergström, T. B., & Norder, H. (2014) · Journal of Medical Virology · doi:10.1002/jmv.23926 · Cited by 10
“C 2014 WILEY PERIODICALS, INC. et al., 1998; Oberste et al., 1999].”
Update on molecular characterization of coxsackievirus B5 strains
Rezig, D., Farès, W., Seghier, M., Yahia, A. B., Touzi, H., & Triki, H. (2011) · Journal of Medical Virology · doi:10.1002/jmv.22084 · Cited by 10
“The recent development of molecular techniques provided more sensitive and accessible methods facilitating studies on their molecular epidemiology [Oberste et al., 1999a; Oberste et al., 2003a].”
BackgroundMethod

Authors: Oberste, M. S., Maher, K., Kennett, M. L., Campbell, J. J., Carpenter, M. S., Schnurr, D., & Pallansch, M. A.
Affiliations: Centers for Disease Control and Prevention (US)
Victorian Infectious Diseases Reference Laboratory (AU)
National Centre for Enteroviruses, Halifax, Nova Scotia, Canada3 and
California Health and Human Services Agency (US)
ORCID: Oberste, M. Steven
Pallansch, Mark A.
Venue: Journal of Clinical Microbiology
Publisher: American Society for Microbiology
Published: 1999-12
Volume: 37
Issue: 12
Pages: 3928-3933
ISSN: 0095-1137 (ISSN-L)
1098-660X
DOI: 10.1128/jcm.37.12.3928-3933.1999
PMC: PMC85848
OpenAlex: W1787418790
Cited by: 154
References: 27
Citations by year: 2026: 1 · 2025: 2 · 2024: 3 · 2023: 3 · 2022: 3 · 2021: 14 · 2020: 4 · 2019: 4 · 2018: 3 · 2017: 4 · 2016: 5 · 2015: 4 · 2014: 6 · 2013: 6 · 2012: 6
FWCI: 2.91
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Clinical Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Infectious Diseases › Viral Infections and Immunology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
Keywords: aseptic meningitis, genetic diversity, phylogenetic analysis, enterovirus surveillance, outbreak epidemiology, molecular epidemiology, North America
MeSH terms: Canada, Echovirus Infections, Genotype, Humans, Meningitis, Aseptic, Molecular Sequence Data, Phylogeny, United States, Genetic Variation, Viral Proteins, Sequence Analysis, DNA, Reverse Transcriptase Polymerase Chain Reaction, Enterovirus B, Human

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Molecular Epidemiology and Genetic Diversity of Echovirus Type 30 (E30): Genotypes Correlate with Temporal Dynamics of E30 Isolation

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