1887
Surveillance Open Access
Like 0

Abstract

Introduction

Group A rotaviruses (RVA) are the leading cause of acute gastroenteritis (AGE) in young children, causing ca 250,000 deaths worldwide, mainly in low-income countries. Two proteins, VP7 (glycoprotein, G genotype) and VP4 (protease-sensitive protein, P genotype), are the basis for the binary RVA nomenclature. Although 36 G types and 51 P types are presently known, most RVA infections in humans worldwide are related to five G/P combinations: G1P[8], G2P[4], G3P[8], G4P[8], G9P[8].

Aim

This study aimed to characterise the RVA strains circulating in Italy in the pre-vaccination era, to define the trends of circulation of genotypes in the Italian paediatric population.

Methods

Between September 2014 and August 2017, after routine screening in hospital by commercial antigen detection kit, 2,202 rotavirus-positive samples were collected in Italy from children hospitalised with AGE; the viruses were genotyped following standard European protocols.

Results

This 3-year study revealed an overall predominance of the G12P[8] genotype (544 of 2,202 cases; 24.70%), followed by G9P[8] (535/2,202; 24.30%), G1P[8] (459/2,202; 20.84%) and G4P[8] (371/2,202; 16.85%). G2P[4] and G3P[8] genotypes were detected at low rates (3.32% and 3.09%, respectively). Mixed infections accounted for 6.49% of cases (143/2,202), uncommon RVA strains for 0.41% of cases (9/2,202).

Conclusions

The emergence of G12P[8] rotavirus in Italy, as in other countries, marks this genotype as the sixth most common human genotype. Continuous surveillance of RVA strains and monitoring of circulating genotypes are important for a better understanding of rotavirus evolution and genotype distribution, particularly regarding strains that may emerge from reassortment events.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.15.1800418
2019-04-11
2024-11-05
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.15.1800418
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/15/eurosurv-24-15-2.html?itemId=/content/10.2807/1560-7917.ES.2019.24.15.1800418&mimeType=html&fmt=ahah

References

  1. 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  PMID: 27059362 
  2. Estes MK, Cohen J. Rotavirus gene structure and function. Microbiol Rev. 1989;53(4):410-49. PMID: 2556635 
  3. Desselberger U. Rotaviruses. Virus Res. 2014;190:75-96.  https://doi.org/10.1016/j.virusres.2014.06.016  PMID: 25016036 
  4. Mihalov-Kovács E, Gellért Á, Marton S, Farkas SL, Fehér E, Oldal M, et al. Candidate new rotavirus species in sheltered dogs, Hungary. Emerg Infect Dis. 2015;21(4):660-3.  https://doi.org/10.3201/eid2104.141370  PMID: 25811414 
  5. Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, et al. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol. 1992;30(6):1365-73. PMID: 1320625 
  6. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, et al. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol. 1990;28(2):276-82. PMID: 2155916 
  7. Rotavirus classification working group; List of accepted genotypes Leuven. Laboratory of Viral Metagenomics. [Accessed: 2 Apr 2019]. Available from: https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/newgenotypes
  8. Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J, Diedrich S, et al. Rotavirus genotypes co-circulating in Europe between 2006 and 2009 as determined by EuroRotaNet, a pan-European collaborative strain surveillance network. Epidemiol Infect. 2011;139(6):895-909.  https://doi.org/10.1017/S0950268810001810  PMID: 20707941 
  9. Matthijnssens J, Van Ranst M. 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  PMID: 22683209 
  10. Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol. 2005;15(1):29-56.  https://doi.org/10.1002/rmv.448  PMID: 15484186 
  11. Anderson EJ, Weber SG. Rotavirus infection in adults. Lancet Infect Dis. 2004;4(2):91-9.  https://doi.org/10.1016/S1473-3099(04)00928-4  PMID: 14871633 
  12. Ramig RF. Genetics of the rotaviruses. Annu Rev Microbiol. 1997;51(1):225-55.  https://doi.org/10.1146/annurev.micro.51.1.225  PMID: 9343350 
  13. Linhares AC, Velázquez FR, Pérez-Schael I, Sáez-Llorens X, Abate H, Espinoza F, et al. Efficacy and safety of an oral live attenuated human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in Latin American infants: a randomised, double-blind, placebo-controlled phase III study. Lancet. 2008;371(9619):1181-9.  https://doi.org/10.1016/S0140-6736(08)60524-3  PMID: 18395579 
  14. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, et al. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med. 2006;354(1):11-22.  https://doi.org/10.1056/NEJMoa052434  PMID: 16394298 
  15. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, et al. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med. 2006;354(1):23-33.  https://doi.org/10.1056/NEJMoa052664  PMID: 16394299 
  16. Sánchez-Uribe E, Esparza-Aguilar M, Parashar UD, Richardson V. Sustained reduction of childhood diarrhea-related mortality and hospitalizations in Mexico after rotavirus vaccine universalization. Clin Infect Dis. 2016;62(Suppl 2):S133-9.  https://doi.org/10.1093/cid/civ1205  PMID: 27059347 
  17. Ruggeri FM, Delogu R, Petouchoff T, Tcheremenskaia O, De Petris S, Fiore L, et al. Molecular characterization of rotavirus strains from children with diarrhea in Italy, 2007-2009. J Med Virol. 2011;83(9):1657-68.  https://doi.org/10.1002/jmv.22163  PMID: 21739459 
  18. Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K, Ramachandran M, et al. Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis. 2005;192(s1) Suppl 1;S146-59.  https://doi.org/10.1086/431499  PMID: 16088798 
  19. Mita V, Arigliani M, Zaratti L, Arigliani R, Franco E. Italian physicians’ opinions on rotavirus vaccine implementation. Pathogens. 2017;6(4):E56.  https://doi.org/10.3390/pathogens6040056  PMID: 29099756 
  20. Costantino C, Restivo V, Tramuto F, Casuccio A, Vitale F. Universal rotavirus vaccination program in Sicily: Reduction in health burden and cost despite low vaccination coverage. Hum Vaccin Immunother. 2018;14(9):2297-302.  https://doi.org/10.1080/21645515.2018.1471306  PMID: 29757707 
  21. Kobayashi N, Lintag IC, Urasawa T, Taniguchi K, Saniel MC, Urasawa S. Unusual human rotavirus strains having subgroup I specificity and "long" RNA electropherotype. Arch Virol. 1989;109(1-2):11-23.  https://doi.org/10.1007/BF01310514  PMID: 2558627 
  22. De Grazia S, Dóró R, Bonura F, Marton S, Cascio A, Martella V, et al. Complete genome analysis of contemporary G12P[8] rotaviruses reveals heterogeneity within Wa-like genomic constellation. Infect Genet Evol. 2016;44:85-93.  https://doi.org/10.1016/j.meegid.2016.06.039  PMID: 27353490 
  23. Ide T, Komoto S, Higo-Moriguchi K, Htun KW, Myint YY, Myat TW, et al. Whole genomic analysis of human G12P[6] and G12P[8] rotavirus strains that have emerged in Myanmar. PLoS One. 2015;10(5):e0124965.  https://doi.org/10.1371/journal.pone.0124965  PMID: 25938434 
  24. Nakagomi T, Do LP, Agbemabiese CA, Kaneko M, Gauchan P, Doan YH, et al. Whole-genome characterisation of G12P[6] rotavirus strains possessing two distinct genotype constellations co-circulating in Blantyre, Malawi, 2008. Arch Virol. 2017;162(1):213-26.  https://doi.org/10.1007/s00705-016-3103-5  PMID: 27718073 
  25. Cilla G, Montes M, Gomariz M, Alkorta M, Iturzaeta A, Perez-Yarza EG, et al. Rotavirus genotypes in children in the Basque Country (North of Spain): rapid and intense emergence of the G12[P8] genotype. Epidemiol Infect. 2013;141(4):868-74.  https://doi.org/10.1017/S0950268812001306  PMID: 22873952 
  26. González-Ochoa G, J G, Calleja-García PM, Rosas-Rodríguez JA, Virgen-Ortíz A, Tamez-Guerra P. Detection of emerging rotavirus G12P[8] in Sonora, México. Acta Virol. 2016;60(2):136-42.  https://doi.org/10.4149/av_2016_02_136  PMID: 27265462 
  27. Wylie KM, Weinstock GM, Storch GA. Emergence of rotavirus G12P[8] in St. Louis during the 2012-2013 rotavirus season. J Pediatric Infect Dis Soc. 2015;4(4):e84-9.  https://doi.org/10.1093/jpids/piu090  PMID: 26513823 
  28. da Silva MF, Fumian TM, de Assis RM, Fialho AM, Carvalho-Costa FA, da Silva Ribeiro de Andrade J, et al. VP7 and VP8* genetic characterization of group A rotavirus genotype G12P[8]: Emergence and spreading in the Eastern Brazilian coast in 2014. J Med Virol. 2017;89(1):64-70.  https://doi.org/10.1002/jmv.24605  PMID: 27322509 
  29. Delogu R, Ianiro G, Camilloni B, Fiore L, Ruggeri FM. Unexpected spreading of G12P[8] rotavirus strains among young children in a small area of central Italy. J Med Virol. 2015;87(8):1292-302.  https://doi.org/10.1002/jmv.24180  PMID: 25758365 
  30. Giammanco GM, Bonura F, DI Bernardo F, Cascio A, Ferrera G, Dones P, et al. Introduction and prolonged circulation of G12 rotaviruses in Sicily. Epidemiol Infect. 2016;144(9):1943-50.  https://doi.org/10.1017/S0950268815003258  PMID: 26743189 
  31. EuroRotaNet. Rotavirus detection and typing methods. UK: EuroRotaNet; 2009. Available from: http://www.eurorota.net/docs.php
  32. Iturriza-Gómara M, Kang G, Gray J. Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J Clin Virol. 2004;31(4):259-65.  https://doi.org/10.1016/j.jcv.2004.04.009  PMID: 15494266 
  33. Italian National Institute for Statistics. Indicatori demografici. [Demographical indicators.] Rome: Instituto nazionale di Statistica. [Accessed 2 Apr 2019]. Italian. Available from: https://www.istat.it/it/archivio/indicatori+demografici
  34. Bányai K, László B, Duque J, Steele AD, Nelson EA, Gentsch JR, et al. Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine. 2012;30(Suppl 1):A122-30.  https://doi.org/10.1016/j.vaccine.2011.09.111  PMID: 22520121 
  35. Wang P, Goggins WB, Chan EYY. A time-series study of the association of rainfall, relative humidity and ambient temperature with hospitalizations for rotavirus and norovirus infection among children in Hong Kong. Sci Total Environ. 2018;643:414-22.  https://doi.org/10.1016/j.scitotenv.2018.06.189  PMID: 29940452 
  36. Barril PA, Fumian TM, Prez VE, Gil PI, Martínez LC, Giordano MO, et al. Rotavirus seasonality in urban sewage from Argentina: effect of meteorological variables on the viral load and the genetic diversity. Environ Res. 2015;138:409-15.  https://doi.org/10.1016/j.envres.2015.03.004  PMID: 25777068 
  37. Viboud C, Pakdaman K, Boëlle PY, Wilson ML, Myers MF, Valleron AJ, et al. Association of influenza epidemics with global climate variability. Eur J Epidemiol. 2004;19(11):1055-9.  https://doi.org/10.1007/s10654-004-2450-9  PMID: 15648600 
  38. Wu X, Lu Y, Zhou S, Chen L, Xu B. Impact of climate change on human infectious diseases: Empirical evidence and human adaptation. Environ Int. 2016;86:14-23.  https://doi.org/10.1016/j.envint.2015.09.007  PMID: 26479830 
  39. Italian Ministry of Defence. Meteo aeronautica. [Aeronautic meteorology]. Rome: Ministera della Difesa. [Accessed: 2 Apr 2019]. Italian. Available from: www.meteoam.it/
  40. EuroRotaNet. Annual report 2015. Liverpool: University of Liverpool; 2016. Available from: https://docplayer.net/53024487-Eurorotanet-annual-report-2015.html
  41. Italian Ministry of Health. Vaccinazioni dell'età pediatrica. Anno 2017 (coorte 2013). [Vaccinations at paediatric age. Year 2007 (2003 cohort)]. Rome: Ministero della Salute; 2018. Available from: http://www.salute.gov.it/imgs/C_17_tavole_20_allegati_iitemAllegati_2_fileAllegati_itemFile_6_file.pdf
  42. Bishop RF, Barnes GL, Cipriani E, Lund JS. Clinical immunity after neonatal rotavirus infection. A prospective longitudinal study in young children. N Engl J Med. 1983;309(2):72-6.  https://doi.org/10.1056/NEJM198307143090203  PMID: 6304516 
  43. Angel J, Franco MA, Greenberg HB. Rotavirus immune responses and correlates of protection. Curr Opin Virol. 2012;2(4):419-25.  https://doi.org/10.1016/j.coviro.2012.05.003  PMID: 22677178 
  44. Leshem E, Lopman B, Glass R, Gentsch J, Bányai K, Parashar U, et al. Distribution of rotavirus strains and strain-specific effectiveness of the rotavirus vaccine after its introduction: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(9):847-56.  https://doi.org/10.1016/S1473-3099(14)70832-1  PMID: 25082561 
  45. Payne DC, Boom JA, Staat MA, Edwards KM, Szilagyi PG, Klein EJ, et al. Effectiveness of pentavalent and monovalent rotavirus vaccines in concurrent use among US children <5 years of age, 2009-2011. Clin Infect Dis. 2013;57(1):13-20.  https://doi.org/10.1093/cid/cit164  PMID: 23487388 
  46. Steele AD, Neuzil KM, Cunliffe NA, Madhi SA, Bos P, Ngwira B, et al. Human rotavirus vaccine Rotarix™ provides protection against diverse circulating rotavirus strains in African infants: a randomized controlled trial. BMC Infect Dis. 2012;12(1):213.  https://doi.org/10.1186/1471-2334-12-213  PMID: 22974466 
  47. Ogden KM, Tan Y, Akopov A, Stewart LS, McHenry R, Fonnesbeck CJ, et al. Multiple introductions and antigenic mismatch with vaccines may contribute to increased predominance of G12P[8] rotaviruses in the United States. J Virol. 2018;93(1):e01476-18.  https://doi.org/10.1128/JVI.01476-18  PMID: 30333170 
/content/10.2807/1560-7917.ES.2019.24.15.1800418
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error