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Genetic diversity in the G protein gene of group A human respiratory syncytial viruses circulating in Riyadh, Saudi Arabia

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Abstract

Human respiratory syncytial virus (HRSV) is a frequent cause of hospitalization and mortality in children worldwide. The molecular epidemiology and circulation pattern of HRSV in Saudi Arabia is mostly uncharted. In the current study, the genetic variability and phylogenetic relationships of HRSV type A strains circulating in Riyadh Province were explored. Nasopharyngeal aspirates were collected from hospitalized children with acute respiratory symptoms during the winter-spring seasons of 2007/08 and 2008/09. Among 175 samples analyzed, 39 (22.3 %) were positive for HRSV by one-step RT-PCR (59 % type A and 41 % type B). Propagation of positive samples in HEp-2 cells permitted the recovery of the first Saudi HRSV isolates. Genetic variability among Saudi HRSV-A strains was evaluated by sequence analysis of the complete attachment (G) protein gene. The nucleotide sequence was compared to representatives of the previously identified HRSV-A genotypes. Sequence and phylogenetic analysis showed that the strains examined in this study were very closely related at both the nucleotide and amino acid level, and all of them are clustered in the GA2 genotype (and mostly belonged to the NA-1 subtype). A total of 23 mutation sites, 14 of which resulted in an amino acid change, were recorded only in Saudi strains. This is the first report on genetic diversity of HRSV-A strains in Saudi Arabia. Further analysis of strains on a geographical and temporal basis is needed to fully understand HRSV-A circulation patterns in Saudi Arabia.

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References

  1. Collins PL, Crowe JE (2007) Respiratory syncytial virus and metapneumovirus. In: Knipe DM, Howley PM, Griffin DE, Martin MA, Lamb RA, Roizman B, Straus SE (eds) Fields virology, 5th edn. Lippincott Williams and Wilkins, Philadelphia, pp 1601–1646

    Google Scholar 

  2. Glezen WP, Taber LH, Frank AL, Juliuss AK (1986) Risk of primary infection and reinfection with respiratory syncytial virus. Am J Dis Child 140:543–546

    CAS  PubMed  Google Scholar 

  3. Falsey AR, Walsh EE (2000) Respiratory syncytial virus infection in adults. Clin Microbiol Rev 13:371–384

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. King AM, Adams MJ, Carstens EB, Lefkowitz EJ (2012) Virus taxonomy and nomenclature of viruses. Ninth report of the International Committee on taxonomy of viruses. Elsevier-Academic Press, Amsterdam

    Google Scholar 

  5. Anderson LJ, Hierholzer JC, Tsou C, Hendry RM, Fernie BF, Stone Y, McIntosh K (1985) Antigenic characterization of respiratory syncytial virus strains with monoclonal antibodies. J Infect Dis 151:626–633

    Article  CAS  PubMed  Google Scholar 

  6. Sullender W (2000) Respiratory syncytial virus genetic and antigenic diversity. Clin Microbiol Rev 13:1–15

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Carballal G, Videla C, Sequeira MD, Mistchenko A, Requeijo PV, Arbiza J (2000) Respiratory syncytial virus: changes in prevalence of subgroups A and B among Argentinian children, 1990-1996. J Med Virol 61:275–279

    Article  CAS  PubMed  Google Scholar 

  8. Zhang Y, Xu W, Shen K, Xie Z, Sun L, Lu Q, Liu C, Liang G, Beeler JA, Anderson LJ (2007) Genetic variability of group A and B human respiratory syncytial viruses isolated from 3 provinces in China. Arch Virol 152:1425–1434

    Article  CAS  PubMed  Google Scholar 

  9. Peret TC, Hall CB, Hammond GW, Piedra PA, Storch GA, Sullender WM, Tsou C, Anderson LJ (2000) Circulation patterns of group A and B human respiratory syncytial virus genotypes in 5 communities in North America. J Infect Dis 181:1891–1896

    Article  CAS  PubMed  Google Scholar 

  10. Venter M, Madhi SA, Tiemessen CT, Schoub BD (2001) Genetic diversity and molecular epidemiology of respiratory syncytial virus over four consecutive seasons in South Africa: identification of new subgroup A and B genotypes. J Gen Virol 82:2117–2424

    CAS  PubMed  Google Scholar 

  11. Baek YH, Choi EH, Song MS, Pascua PN, Kwon HI, Park SJ, Lee JH, Woo SI, Ahn BH, Han HS, Hahn YS, Shin KS, Jang HL, Kim SY, Choi YK (2012) Prevalence and genetic characterization of respiratory syncytial virus (RSV) in hospitalized children in Korea. Arch Virol 157:1039–1050

    Article  CAS  PubMed  Google Scholar 

  12. Eshaghi A, Duvvuri VR, Lai R, Nadarajah JT, Li A, Patel SN, Low DE, Gubbay JB (2012) Genetic variability of human respiratory syncytial virus A strains circulating in Ontario: a novel genotype with a 72 nucleotide G gene duplication. PLoS One 7:e32807

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Shobugawa Y, Saito R, Sano Y, Zaraket H, Suzuki Y, Kumaki A, Dapat I, Oguma T, Yamaguchi M, Suzuki H (2009) Emerging genotypes of human respiratory syncytial virus subgroup A among patients in Japan. J Clin Microbiol 47:2475–2482

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Choi EH, Lee HJ (2000) Genetic diversity and molecular epidemiology of the G protein of subgroups A and B of respiratory syncytial viruses isolated over 9 consecutive epidemics in Korea. J Infect Dis 181:1547–1556

    Article  CAS  PubMed  Google Scholar 

  15. Levine S, Klaiber-Franco R, Paradiso PR (1987) Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol 68:2521–2524

    Article  CAS  PubMed  Google Scholar 

  16. Johnson PR, Spriggs MK, Olmsted RA, Collins PL (1987) The G glycoprotein of human respiratory syncytial viruses of subgroups A and B: extensive sequence divergence between antigenically related proteins. Proc Natl Acad Sci USA 84:5625–5629

    Article  CAS  PubMed  Google Scholar 

  17. Kuroiwa Y, Nagai K, Okita L, Yui I, Kase T, Nakayama T, Tsutsumi H (2005) A phylogenetic study of human respiratory syncytial viruses group A and B strains isolated in two cities in Japan from 1980-2002. J Med Virol 76:241–247

    Article  CAS  PubMed  Google Scholar 

  18. al-Hajjar S, Akhter J, Al-Jumaah S, Qadri H (1998) Respiratory viruses in children attending a major referral centre in Saudi Arabia. Ann Trop Paediatr 18:87–92

    CAS  PubMed  Google Scholar 

  19. Al-Majhdi FN, Al-Jarallah A, Elaeed M, Latif A, Gissmann L, Amer HM (2009) Prevalence of respiratory syncytial virus infection in Riyadh during the winter season 2007-2008 and different risk factors impact. Inter J Virol 5:154–163

    Article  CAS  Google Scholar 

  20. Al-Shehri MA, Sadeq A, Quli K (2005) Bronchiolitis in Abha, Southwest Saudi Arabia: viral etiology and predictors for hospital admission. West Afr J Med 24:299–304

    PubMed  Google Scholar 

  21. Bakir TM, Halawani M, Ramia S (1998) Viral aetiology and epidemiology of acute respiratory infections in hospitalized Saudi children. J Trop Pediatr 44:100–103

    Article  CAS  PubMed  Google Scholar 

  22. Meqdam M, Subaih SH (2006) Rapid detection and clinical features of infants and young children with acute lower respiratory tract infection due to respiratory syncytial virus. FEMS Immunol Med Microbiol 47:129–133

    Article  CAS  PubMed  Google Scholar 

  23. Shier MK, Badr MA (2005) Respiratory syncytial virus infection in patients visiting King Khaled university hospital. Minoufia Med J 18:11–18

    Google Scholar 

  24. Cane P, Pringle C (1991) Respiratory syncytial virus heterogeneity during an epidemic: analysis by limited nucleotide sequencing (SH gene) and restriction mapping (N gene). J Gen Virol 72:349–357

    Article  CAS  PubMed  Google Scholar 

  25. Yamada A, Lam L-Y, Tam JS (2004) Typing and subtyping of influenza viruses and respiratory syncytial viruses by multiplex RT-PCR. Int Congr Ser 1263:381–385

    Article  CAS  Google Scholar 

  26. Hughes JH, Daniel RM, Vincent V (1988) Detection of respiratory syncytial virus in clinical specimens by viral culture, direct and indirect immunofluorescence, and enzyme immunoassay. J Clin Microbiol 26:588–591

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Rossiter PB, Jessett DM, Taylor WP (1985) Microneutralisation systems for use with different strains of peste des petits ruminants virus and rinderpest virus. Trop Anim Health Prod 17:75–81

    Article  CAS  PubMed  Google Scholar 

  28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  29. Cane P, Pringle C (1995) Evolution of subgroup A respiratory syncytial virus: evidence for progressive accumulation of amino acid changes in the attachment protein. J Virol 69:2918–2925

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Peret TC, Hall CB, Schnabel KC, Golub JA, Anderson LJ (1998) Circulation patterns of genetically distinct group A and B strains of human respiratory syncytial virus in a community. J Gen Virol 79:2221–2229

    CAS  PubMed  Google Scholar 

  31. Faghihloo E, Salimi V, Rezaeil F, Naseril M, Mamishi S, Mahmoodi M, Mokhtari-Azad T (2011) Genetic diversity in the G protein gene of human respiratory syncytial virus among Iranian children with acute respiratory symptoms. Iran J Pediatr 21:58–64

    PubMed Central  PubMed  Google Scholar 

  32. Meqdam MM, Nasrallah GK (2000) Enhanced detection of respiratory syncytial virus by shell vial in children hospitalised with respiratory illnesses in northern Jordan. J Med Virol 62:518–523

    Article  CAS  PubMed  Google Scholar 

  33. Fattouh AM, Mansi YA, El-Anany MG, El-Kholy AA, El-Karaksy HM (2011) Acute lower respiratory tract infection due to respiratory syncytial virus in a group of Egyptian children under 5 years of age. Ital J Pediatr 37:14

    Article  PubMed Central  PubMed  Google Scholar 

  34. Rajala MS, Sullender WM, Prasad AK, Dar L, Broor S (2003) Genetic variability among Group A and B respiratory syncytial virus isolates from a large referral hospital in New Delhi, India. J Clin Microbiol 41:2311–2316

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Hall CB, Walsh EE, Schnabel KC, Long CE, McConnochie KM, Hildreth SW, Anderson LJ (1990) Occurrence of groups A and B of respiratory syncytial virus over 15 years: associated epidemiologic and clinical characteristics in hospitalized and ambulatory children. J Infect Dis 162:1283–1290

    Article  CAS  PubMed  Google Scholar 

  36. Forcic D, Ivancic-Jelecki J, Mlinaric-Galinovic G, Vojnovic G, Babic-Erceg A, Tabain I (2012) A study of the genetic variability of human respiratory syncytial virus in Croatia, 2006-2008. J Med Virol 84:1985–1992

    Article  CAS  PubMed  Google Scholar 

  37. Nakamura M, Itokazu K, Taira K, Kawaki T, Kudaka J, Nidaira M, Okano S, Koja Y, Tamanaha K, Kimura H, Noda M (2009) Genotypic and phylogenetic analysis of the G gene of respiratory syncytial virus isolates in Okinawa, Japan, 2008. Jpn J Infect Dis 62:326–327

    PubMed  Google Scholar 

  38. Ostlund MR, Lindell AT, Stenler S, Riedel HM, Wirgart BZ, Grillner L (2008) Molecular epidemiology and genetic variability of respiratory syncytial virus (RSV) in Stockholm, 2002-2003. J Med Virol 80:159–167

    Article  PubMed  Google Scholar 

  39. Rebuffo-Scheer C, Bose M, He J, Khaja S, Ulatowski M, Beck ET, Fan J, Kumar S, Nelson MI, Henrickson KJ (2011) Whole genome sequencing and evolutionary analysis of human respiratory syncytial virus A and B from Milwaukee, WI 1998-2010. PLoS One 6:e25468

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Viegas M, Mistchenko AS (2005) Molecular epidemiology of human respiratory syncytial virus subgroup A over a six-year period (1999-2004) in Argentina. J Med Virol 77:302–310

    Article  CAS  PubMed  Google Scholar 

  41. Plotnicky-Gilquin H, Goetsch L, Huss T, Champion T, Beck A, Haeuw JF, Nguyen TN, Bonnefoy JY, Corvaia N, Power UF (1999) Identification of multiple protective epitopes (protectopes) in the central conserved domain of a prototype human respiratory syncytial virus G protein. J Virol 73:5637–5645

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Rueda P, Delgado T, Portela A, Melero JA, Garcia-Barreno B (1991) Premature stop codons in the G glycoprotein of human respiratory syncytial viruses resistant to neutralization by monoclonal antibodies. J Virol 65:3374–3378

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Melero JA, Garcia-Barreno B, Martinez I, Pringle CR, Cane PA (1997) Antigenic structure, evolution and immunobiology of human respiratory syncytial virus attachment (G) protein. J Gen Virol 78:2411–2418

    CAS  PubMed  Google Scholar 

  44. Palomo CP, Cane A, Melero JA (2000) Evaluation of the antibody specificities of human convalescent-phase sera against the attachment (G) protein of human respiratory syncytial virus: influence of strain variation and carbohydrate side chains. J Med Virol 60:468–474

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

This study was partially supported by the research grant (RGP-VPP-136), for the Deanship of Scientific Research, King Saud University.

Conflicts of interest

The authors declare that they have no conflicts of interest.

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Authors and Affiliations

  1. Department of Botany and Microbiology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Fahad N. Almajhdi, Mohamed A. Farrag & Haitham M. Amer

  2. Center of Excellence in Biotechnology Research, College of Science, King Saud University, Riyadh, 11451, Saudi Arabia

    Fahad N. Almajhdi

  3. Department of Virology, Faculty of Veterinary Medicine, Cairo University, Giza, 12211, Egypt

    Haitham M. Amer

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  1. Fahad N. Almajhdi
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  2. Mohamed A. Farrag
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Correspondence to Fahad N. Almajhdi.

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Almajhdi, F.N., Farrag, M.A. & Amer, H.M. Genetic diversity in the G protein gene of group A human respiratory syncytial viruses circulating in Riyadh, Saudi Arabia. Arch Virol 159, 73–81 (2014). https://doi.org/10.1007/s00705-013-1792-6

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  • DOI: https://doi.org/10.1007/s00705-013-1792-6

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