Genomic constellations of RVA detected in Brazil from 1986 to 2016: a temporal and geographical distribution and occurrence of reassortments
Main Article Content
Abstract
Introduction: Species A rotavirus (RVA) infections are a major cause of severe gastroenteritis in children of <5 years worldwide. In Brazil, before vaccination, RVA was associated with 3.5 million episodes of acute diarrheal disease per year. Due to the segmented nature of their genomes, rotaviruses can exchange genes during co-infections, and generate new virus strains and new reinfections. Objective: To evaluate the genomic diversity of RVA isolated in Brazil in 30 years, between 1986 to 2016, to investigate possible changes in the frequency of genotype constellations before and after the implementation of the vaccine. Methods: In total, 4,474 nucleotide sequences were obtained from the Virus Variation Database. Genomic constellation was compared, and the proportion of rotavirus genotypes was analyzed by time and geographic region. Results: Our results showed that major known genotypes were circulating in the country during the period under analysis, with a prevalence of the G1P[8] Wa-like genotype, decreasing only in the period immediately after the introduction of the vaccine. Regarding the geographical distribution, most of our constellations, 62 (39.2%), and 50 (31.6%) were concentrated in the North and Northeast regions. Our analysis also showed the circulation of multiple strains during the periods when the DS-1-like and AU-1-like genotypes were co-circulating with the Wa-like genotype. Conclusion: Therefore, it is likely that inter-genogroup reassortments are still occurring in Brazil and so it is important to establish an efficient surveillance system to follow the emergence of novel reassorted strains that might not be targeted by the vaccine.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY) that allows others to share and adapt the work with an acknowledgement of the work's authorship and initial publication in this journal.
Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.References
Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF, Ahmed T, et al. Rotavirus vaccination and the global burden of rotavirus diarrhea Among Children Younger Than 5 years. JAMA Pediatr. 2018;172(10):958-65. https://doi.org/10.1001/jamapediatrics.2018.1960
World Health Organization. Rotavirus vaccines WHO position paper: January 2013 – Recommendations. Vaccine. 2013;31(52):6170-1. https://doi.org/10.1016/j.vaccine.2013.05.037
Kotloff KL. The Burden and Etiology of Diarrheal Illness in Developing Countries. Pediatr Clin North Am. 2017;64(4):799-14. https://doi.org/10.1016/j.pcl.2017.03.006
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the global enteric multicenter study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209-22. https://doi.org/10.1016/S0140-6736(13)60844-2
Lanata CF, Fischer-Walker CL, Olascoaga AC, Torres CX, Aryee MJ, Black RE, et al. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One. 2013;8(9):e72788. https://doi.org/10.1371/journal.pone.0072788
Sartori AMC, Valentim J, Soárez PC, Novaes HMD. Rotavirus morbidity and mortality in children in Brazil. Rev Pan Am Salud Publica. 2008;23(2):92-100. https://doi.org/10.1590/s1020-49892008000200004
Linhares AC, Justino MCA. Rotavirus vaccination in Brazil: effectiveness and health impact seven years post-introduction. Expert Rev Vaccines. 2014;13(1):43-7. https://doi.org/10.1586/14760584.2014.861746
Tate JE, Burton AH, Boschi-Pinto C, Parashar UD; World Health Organization–Coordinated Global Rotavirus Surveillance Network. Global, regional, and National Estimates of rotavirus mortality in children <5 years of age, 2000-2013. Clin Infect Dis. 2016;62(Suppl 2):S96-105. https://doi.org/10.1093/cid/civ1013
De Jesus MCS, Santos VS, Storti-Melo LM, Souza CDF, Barreto IDC, Paes MVC, et al. Impact of a twelve-year rotavirus vaccine program on acute diarrhea mortality and hospitalization in Brazil: 2006-2018. Expert Rev Vaccines. 2020;19(6):585-93. https://doi.org/10.1080/14760584.2020.1775081
Silva MFM, Rose TL, Gomez MM, Carvalho-Costa FA, Fialho AM, Assis RMS, et al. G1P[8] species A rotavirus over 27 years – Pre- and post-vaccination eras – in Brazil: Full genomic constellation analysis and no evidence for selection pressure by Rotarix vaccine. Infect Genet Evol. 2015;30:206-18. https://doi.org/10.1016/j.meegid.2014.12.030
Estes MK, Greenberg HB. Rotaviruses In: Knipe DM, Howley PM. Fields Virology. Philadelphia: Williams and Wilkins, 2013; p. 1347.
Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K, Estes MK, et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol. 2008;153(8):1621-9. https://doi.org/10.1007/s00705-008-0155-1
Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, et al. Full Genome-Based Classification of Rotaviruses Reveals a Common Origin between Human Wa-Like and Porcine Rotavirus Strains and Human DS-1-Like and Bovine Rotavirus Strains. J Virol. 2008;82(7):3204-19. https://doi.org/10.1128/JVI.02257-07
Matthijnssens J, Ranst MV. Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol. 2012;2(4):426-33. https://doi.org/10.1016/j.coviro.2012.04.007
Benati FJ, Maranhao AG, Lima RS, Silva RC, Santos N. Multiple-gene characterization of rotavirus strains: evidence of genetic linkage among the VP7-, VP4-, VP6-, and NSP4-encoding genes. J Med Virol. 2010;82(10):1797-802. https://doi.org/10.1002/jmv.21816
Tate JE, Patel MM, Steele AD, Gentsch JR, Payne DC, Cortese MM, et al. Global impact of rotavirus vaccines. Expert Rev Vaccines. 2010;9(4):395-07. https://doi.org/10.1586/erv.10.17
Rose TL, Silva MFM, Gomez MM, Resque HR, Ichihara MYT, Volotão EMV, et al. Evidence of vaccine-related reassortment of rotavirus, Brazil, 2008–2010. Emerg Infect Dis. 2013;19(11):1843-6. https://doi.org/10.3201/eid1911.121407
Zhang M, Zeng CKY, Morris AP, Estes MK. A Functional NSP4 Enterotoxin Peptide Secreted from Rotavirus-Infected Cells. J Virol. 2000;74(24):11663-70. https://doi.org/10.1128/jvi.74.24.11663-11670.2000
Gomez MM, Resque HR, Volotao ED, Rose TL, Silva MFM, Heylen E, et al. Distinct evolutionary origins of G12P[8] and G12P[9] group A rotavirus strains circulating in Brazil. Infect Genet Evol. 2014;28:385-8. https://doi.org/10.1016/j.meegid.2014.04.007
Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7. https://doi.org/10.1093/nar/gkh340
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731-9. https://doi.org/10.1093/molbev/msr121
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754-5. https://doi.org/10.1093/bioinformatics/17.8.754
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572-4. https://doi.org/10.1093/bioinformatics/btg180
Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25(7):1253-6. https://doi.org/10.1093/molbev/msn083
Santos VS, Nóbrega FA, Soares MWS, Moreira RD, Cuevas LE, Gurgel RQ. Rotavirus Genotypes Circulating in Brazil Before and After the National Rotavirus Vaccine Program: a review. Pediatr Infect Dis J. 2018;37(3):e63-5. https://doi.org/10.1097/INF.0000000000001770
Gutierrez MB, Fialho AM, Maranhão AG, Malta FC, Andrade JSR, Assis RMS, et al. Rotavirus A in Brazil: Molecular Epidemiology and Surveillance during 2018-2019. Pathogens. 2020;9(7):515. https://doi.org/10.3390/pathogens9070515
Pankov RC, Gondim RNDG, Prata MMG, Medeiros PHQS, Veras HN, Santos AKS, et al. Rotavirus A Infections in Community Childhood Diarrhea in the Brazilian Semiarid Region During Postvaccination Era. J Pediatr Gastroenterol Nutr. 2019;69(4):e91-8. https://doi.org/10.1097/MPG.0000000000002416
Guerra SFS, Fecury PCMS, Bezerra DAM, Lobo PS, Penha ET, Sousa Junior EC, et al. Emergence of G12P[6] rotavirus strains among hospitalised children with acute gastroenteritis in Belém, Northern Brazil, following introduction of a rotavirus vaccine. Arch Virol. 2019;164(8):2107-17. https://doi.org/10.1007/s00705-019-04295-w
Kirkwood CD, Cannan D, Bogdanovic-Sakran N, Bishop RF, Barnes GL; National Rotavirus Surveillance Group. Australian Rotavirus Surveillance Program: annual report, 2006-07. Commun Dis Intell. 2007;31(4):375-9.
Esteban LE, Rota RP, Gentsch JR, Jiang B, Esona M, Glass RI, et al. Molecular epidemiology of group A rotavirus in Buenos Aires, Argentina 2004–2007: Reemergence of G2P[4] and emergence of G9P[8] strains. J Med Virol. 2010;82(6):1083-93. https://doi.org/10.1002/jmv.21745
Parra GI. Seasonal shifts of group A rotavirus strains as a possible mechanism of persistence in the human population. J Med Virol. 2009;81(3):568-71. https://doi.org/10.1002/jmv.21423
Theamboonlers A, Maiklang O, Thongmee T, Chieochansin T, Vuthitanachot V, Poovorawan Y. Complete genotype constellation of human rotavirus group A circulating in Thailand, 2008-2011. Infect Genet Evol. 2014;21:295-302. https://doi.org/10.1016/j.meegid.2013.11.020
Arora R, Chitambar SD. Full genomic analysis of Indian G1P[8] rotavirus strains. Infect Genet Evol. 2011;11(2):504-11. https://doi.org/10.1016/j.meegid.2011.01.005
Fujii Y, Nakagomi T, Nishimura N, Noguchi A, Miura S, Ito H, et al. Spread and predominance in Japan of novel G1P[8] double-reassortant rotavirus strains possessing a DS-1-like genotype constellation typical of G2P[4] strains. Infect Genet Evol. 2014;28:426-33. https://doi.org/10.1016/j.meegid.2014.08.001
Agbemabiese CA, Nakagomi T, Doan YH, Do LP, Damanka S, Armah GE, et al. Genomic constellation and evolution of Ghanaian G2P[4] rotavirus strains from a global perspective. Infect Genet Evol. 2016;45:122-31. https://doi.org/10.1016/j.meegid.2016.08.024
Sadiq A, Bostan N, Bokhari H, Yinda KC, Matthijnssens J. Whole Genome Analysis of Selected Human Group A Rotavirus Strains Revealed Evolution of DS-1-Like Single- and Double-Gene Reassortant Rotavirus Strains in Pakistan During 2015-2016. Front Microbiol. 2019;10:2641. https://doi.org/10.3389/fmicb.2019.02641
Luchs A, Costa AC, Cilli A, Komninakis SCV, Carmona RCC, Boen L, et al. Spread of the emerging equine-like G3P[8] DS-1-like genetic backbone rotavirus strain in Brazil and identification of potential genetic variants. J Gen Virol. 2019;100(1):7-25. https://doi.org/10.1099/jgv.0.001171
Mascarenhas JD, Linhares AC, Gabbay YB, Leite JPG. Detection and characterization of rotavirus G and P types from children participating in a rotavirus vaccine trial in Belem, Brazil. Mem Inst Oswaldo Cruz. 2002;97(1):113-7. https://doi.org/10.1590/S0074-02762002000100020
Tsugawa T, Kaitlin RL, Hiroyuki T. Human G3P[9] rotavirus strains possessing an identical genotype constellation to AU-1 isolated at high prevalence in Brazil, 1997-1999. J Gen Virol. 2015;96)Pt 3):590-600. https://doi.org/10.1099/vir.0.071373-0
Brasil Instituto Brasileiro de Geografia e Estatística (IBGE). Censo Brasileiro de 2010. Rio de Janeiro: IBGE, 2012.