Identification and Phylogenetic Characterization of Human Enteroviruses Isolated from Cases of Aseptic Meningitis in Brazil, 2013–2017
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Study Background
2.3. Virus Isolation and Molecular Typing
2.4. Phylogenetic Analysis
3. Results
3.1. Epidemiological Analysis
3.2. Enterovirus Identification
3.3. Phylogenetic Analysis
4. Discussion
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Tapparel, C.; Siegrist, F.; Petty, T.J.; Kaiser, L. Picornavirus and enterovirus diversity with associated human diseases. Infect. Genet. Evol. 2013, 14, 282–293. [Google Scholar] [CrossRef] [PubMed]
- Sousa, I.P., Jr.; Maximo, A.C.B.; Figueiredo, M.A.A.; Maia, Z.; da Silva, E.E. Echovirus 30 detection in an outbreak of acute myalgia and rhabdomyolysis, Brazil 2016–2017. Clin. Microbiol. Infect. 2019, 25, 252.e5–252.e8. [Google Scholar] [CrossRef] [PubMed]
- Lee, B.E.; Davies, H.D. Aseptic Meningitis. Curr. Opin. Infect. Dis. 2007, 20, 272–277. [Google Scholar] [CrossRef] [PubMed]
- Dos Santos, G.P.; da Costa, E.V.; Tavares, F.N.; da Costa, L.J.; da Silva, E.E. Genetic diversity of Echovirus 30 involved in aseptic meningitis cases in Brazil (1998–2008). J. Med. Virol. 2011, 83, 2164–2171. [Google Scholar] [CrossRef] [PubMed]
- Kmetzsch, C.I.; Balkie, E.M.; Monteiro, A.; Costa, E.V.; dos Santos, G.P.; da Silva, E.E. Echovirus 13 aseptic meningitis, Brazil. Emerg. Infect. Dis. 2006, 12, 1289–1290. [Google Scholar] [CrossRef] [PubMed]
- Sousa, I.P., Jr.; Burlandy, F.M.; Oliveira, S.S.; Nunes, A.M.; Sousa, C.; da Silva, E.M.; Souza, J.G.A.; de Paula, V.A.; Oliveira, I.C.M.; Tavares, F.N.; et al. Acute flaccid paralysis laboratorial surveillance in a polio-free country: Brazil, 2005–2014. Hum. Vaccines Immunother. 2017, 13, 717–723. [Google Scholar] [CrossRef] [PubMed]
- Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA 7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef]
- Guindon, S.; Gascuel, O. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst. Biol. 2003, 52, 696–704. [Google Scholar] [CrossRef]
- Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef]
- Lefort, V.; Longueville, J.E.; Gascuel, O. SMS: Smart Model Selection in PhyML. Mol. Biol. Evol. 2017, 34, 2422–2424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anisimova, M.; Gascuel, O. Approximate Likelihood-Ratio Test for Branches: A Fast, Accurate, and Powerful Alternative. Syst. Biol. 2006, 55, 539–552. [Google Scholar] [CrossRef] [PubMed]
- Drummond, A.J.; Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7, 214. [Google Scholar] [CrossRef] [PubMed]
- Suchard, M.A.; Rambaut, A. Many-Core Algorithms for Statistical Phylogenetics. Bioinformatics 2009, 25, 1370–1376. [Google Scholar] [CrossRef] [PubMed]
- Drummond, A.J.; Nicholls, G.K.; Rodrigo, A.G.; Solomon, W. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 2002, 161, 1307–1320. [Google Scholar]
- Minin, V.N.; Bloomquist, E.W.; Suchard, M.A. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol. Biol. Evol. 2008, 25, 1459–1471. [Google Scholar] [CrossRef] [PubMed]
- Rambaut, A.; Drummond, A.J.; Xie, D.; Baele, G.; Suchard, M.A. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018, 67, 901–904. [Google Scholar] [CrossRef]
- Hasbun, R.; Rosenthal, N.; Balada-Llasat, J.M.; Chung, J.; Duff, S.; Bozzette, S.; Zimmer, L.; Ginocchio, C.C. Epidemiology of Meningitis and Encephalitis in the United States, 2011–2014. Clin. Infect. Dis. 2017, 65, 359–363. [Google Scholar] [CrossRef]
- Kim, H.J.; Kang, B.; Hwang, S.; Hong, J.; Kim, K.; Cheon, D.S. Epidemics of viral meningitis caused by echovirus 6 and 30 in Korea in 2008. Virol. J. 2012, 9, 38. [Google Scholar] [CrossRef]
- Chen, P.; Linb, X.; Liub, G.; Wangb, S.; Songb, L.; Tao, Z.; Xua, A. Analysis of enterovirus types in patients with symptoms of aseptic meningitis in 2014 in Shandong, China. Virology 2018, 516, 196–201. [Google Scholar] [CrossRef]
- Zhu, Y.; Zhou, X.; Liu, J.; Xia, L.; Pan, Y.; Chen, J.; Luo, N.; Yin, J.; Ma, S. Molecular identification of human enteroviruses associated with aseptic meningitis in Yunnan province, Southwest China. SpringerPlus 2016, 5, 1515. [Google Scholar] [CrossRef]
- Liu, N.; Jia, L.; Yin, J.; Wu, Z.; Wang, Z.; Li, P.; Hao, R.; Wang, L.; Wang, Y.; Qiu, S.; et al. An outbreak of aseptic meningitis caused by a distinct lineage of coxsackievirus B5 in China. Int. J. Infect. Dis. 2014, 23, 101–104. [Google Scholar] [CrossRef] [Green Version]
- Chen, X.; Li, J.; Guo, J.; Xu, W.; Sun, S.; Xie, Z. An outbreak of echovirus 18 encephalitis/meningitis in children in Hebei Province, China, 2015. Emerg. Microbes Infect. 2017, 6, e54. [Google Scholar] [CrossRef]
- Strikas, R.A.; Anderson, L.J.; Parker, R.A. Temporal and geographic patterns of isolates of nonpolio enterovirus in the United States, 1970–1983. J. Infect. Dis. 1986, 153, 346–351. [Google Scholar] [CrossRef]
- Papadakis, G.; Chibo, D.; Druce, J.; Catton, M.; Birch, C. Detection and genotyping of enteroviruses in cerebrospinal fluid in patients in Victoria, Australia, 2007–2013. J. Med. Virol. 2014, 86, 1609–1613. [Google Scholar] [CrossRef]
- Smuts, H.; Cronje, S.; Thomas, J.; Brink, D.; Korsman, S.; Hardie, D. Molecular characterization of an outbreak of enterovirus-associated meningitis in Mossel Bay, South Africa, December 2015–January 2016. BMC Infect. Dis. 2018, 18, 709. [Google Scholar] [CrossRef]
- Dos Santos, G.P.L.; Skraba, I.; Oliveira, D.; Lima, A.A.F.; de Melo, M.M.M.; Kmetzsch, C.I.; Costa, E.V.; da Silva, E.E. Enterovirus Meningitis in Brazil, 1998–2003. J. Med. Virol. 2006, 78, 98–104. [Google Scholar] [CrossRef]
- Pinto Junior, V.L.; Rebelo, M.C.; Costa, E.V.; Silva, E.E.; Bóia, M.N. Description of a widespread outbreak of aseptic meningitis due to echovirus 30 in Rio de Janeiro state, Brazil. Braz. J. Infect. Dis. 2009, 13, 367–370. [Google Scholar] [CrossRef] [Green Version]
- Luchs, A.; Russo, D.H.; Cilli, A.; Costa, F.F.; Morillo, S.G.; Machado, B.C.; Pellini, A.C.; Carmona, R.C.C.; Timenetsky, M.C. Echovirus 6 associated to aseptic meningitis outbreak, in São Joaquim da Barra, São Paulo, Brazil. Braz. J. Microbiol. 2008, 39, 28–31. [Google Scholar] [CrossRef]
- Bailly, J.-L.; Mirand, A.; Henquell, C.; Archimbaud, C.; Chambon, M.; Regagnon, C.; Charbonne, F.; Peigue-Lafeuille, H. Repeated genomic transfers from echovirus 30 to echovirus 6 lineages indicate co-divergence between co-circulating populations of the two human enterovirus serotypes. Infect. Genet. Evol. 2011, 11, 276–289. [Google Scholar] [CrossRef]
- Chonmaitree, T.; Ford, C.; Sanders, C.; Lucia, H.L. Comparison of cell cultures for rapid isolation of enteroviruses. J. Clin. Microbiol. 1988, 26, 2576–2580. [Google Scholar] [Green Version]
- Singh, S.; Chow, V.T.; Phoon, M.C.; Chan, K.P.; Poh, C.L. Direct Detection of Enterovirus 71 (EV71) in Clinical Specimens from a Hand, Foot, and Mouth Disease Outbreak in Singapore by Reverse Transcription-PCR with Universal Enterovirus and EV71-Specific Primers. J. Clin. Microbiol. 2002, 40, 2823–2827. [Google Scholar] [CrossRef] [Green Version]
- Sousa, I.P., Jr.; Burlandy, F.M.; Costa, E.V.; Tavares, F.N.; da Silva, E.E. Enteroviruses associated with hand, foot, and mouth disease in Brazil. J. Infect. 2018, 77, 448–454. [Google Scholar] [CrossRef]
Variable | Year (All Patients/EV-Positive) | ||||
---|---|---|---|---|---|
Year | 2013 | 2014 | 2015 | 2016 | 2017 |
Year | |||||
≤15 year | 287/21 | 318/73 | 530/84 | 247/39 | 459/70 |
Region | |||||
South | 358/14 (3.9) * | 365/67 (18.3) | 464/56 (12) | 399/38 (9.5) | 588/61 (10.4) |
Southeast | 3/0 (0) | 13/6 (46.1) | 3/0 (0) | 5/0 (0) | 24/2 (8.3) |
Northeast | 45/7 (15.5) | 79/8 (10.1) | 229/30 (13.1) | 5/3 (60) | 50/11 (22) |
Midwest | 2/0 (0) | 8/0 (0) | 11/0 (0) | 7/0 (0) | 1/0 (0) |
Sex | |||||
Male | 230/12 (5.2) | 275/47 (17) | 420/59 (14) | 247/23 (9.3) | 380/40 (10.5) |
Female | 178/9 (5) | 190/34 (17.9) | 287/27 (9.4) | 169/18 (10.6) | 283/34 (12) |
Total | 408/21 | 465/81 | 707/86 | 416/41 | 663/74 |
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Ramalho, E.; Sousa, I., Jr.; Burlandy, F.; Costa, E.; Dias, A.; Serrano, R.; Oliveira, M.; Lopes, R.; Debur, M.; Burger, M.; et al. Identification and Phylogenetic Characterization of Human Enteroviruses Isolated from Cases of Aseptic Meningitis in Brazil, 2013–2017. Viruses 2019, 11, 690. https://doi.org/10.3390/v11080690
Ramalho E, Sousa I Jr., Burlandy F, Costa E, Dias A, Serrano R, Oliveira M, Lopes R, Debur M, Burger M, et al. Identification and Phylogenetic Characterization of Human Enteroviruses Isolated from Cases of Aseptic Meningitis in Brazil, 2013–2017. Viruses. 2019; 11(8):690. https://doi.org/10.3390/v11080690
Chicago/Turabian StyleRamalho, Emanuelle, Ivanildo Sousa, Jr., Fernanda Burlandy, Eliane Costa, Amanda Dias, Roseane Serrano, Maria Oliveira, Renato Lopes, Maria Debur, Marion Burger, and et al. 2019. "Identification and Phylogenetic Characterization of Human Enteroviruses Isolated from Cases of Aseptic Meningitis in Brazil, 2013–2017" Viruses 11, no. 8: 690. https://doi.org/10.3390/v11080690