Diversity of rotavirus strains circulating in children under 5 years of age admitted to hospital for acute gastroenteritis in morocco, june 2006 to may 2009

Journal of Medical Virology

Volumn 85, Issue 2, 2013, Pages 354-362

  Benhafid, Mohammed ^a,b   Elomari, Nezha ^a   Elqazoui, Maria ^a   Meryem, Azzouzi Idrissi ^a   Rguig, Ahmed ^c   Filali Maltouf, Abdelkarim ^b   Elaouad, Rajae ^a  

^a INSTITUT NATIONAL D HYGIÈNE   (Morocco)

^b FACULTÉ DES SCIENCES   (Morocco)

^c Ministry of Health Morocco   (Morocco)

Author keywords

Genotype; Morocco; Rotavirus; Surveillance; Vaccination

Indexed keywords

ROTAVIRUS VACCINE;

ACUTE GASTROENTERITIS; ARTICLE; CHILD; DIARRHEA; DRUG SURVEILLANCE PROGRAM; ENZYME IMMUNOASSAY; FECES ANALYSIS; GENOTYPE; HUMAN; INFANT; MAJOR CLINICAL STUDY; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS; ROTAVIRUS INFECTION; VACCINATION; VIRUS DETECTION; VIRUS STRAIN;

CHILD, PRESCHOOL; DIARRHEA; ENZYME-LINKED IMMUNOSORBENT ASSAY; FECES; FEMALE; GASTROENTERITIS; GENETIC VARIATION; GENOTYPE; HOSPITALS; HUMANS; INFANT; INFANT, NEWBORN; MALE; MOLECULAR EPIDEMIOLOGY; MOROCCO; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; ROTAVIRUS; SEQUENCE ANALYSIS, DNA;

ROTAVIRUS;

EID: 84871075831     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23445     Document Type: Article

References (51)

1. Abugalia M, Cuevas L, Kirby A, Dove W, Nakagomi O, Nakagomi T, Kara M, Gweder R, Smeo M, Cunliffe N. 2011. Clinical features and molecular epidemiology of rotavirus and norovirus infections in Libyan children. J Med Virol 83:1849-1856.
2. Akran V, Peenze I, Akoua-Koffi C, Kette H, de Beer MC, Dosso M, Steele AD. 2010. Molecular characterization and genotyping of human rotavirus strains in Abidjan, Cote d'Ivoire. J Infect Dis 202:220-224. and norovirus infections in Libyan children. J Med Virol 83: 1849-1856.
3. Armah GE, Steele AD, Esona MD, Akran VA, Nimzing L, Pennap G. 2010. Diversity of rotavirus strains circulating in West Africa from 1996 to 2000. J Infect Dis 202:64-71.
4. Bányai K, László B, Duque J, Steele AD, Nelson EA, Gentsch JR, Parashar UD. 2012. 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 30:122-130.
5. Benhafid M, Youbi M, Klena JD, Gentsch JR, Teleb N, Widdowson MA, Elaouad R. 2009. Epidemiology of rotavirus gastroenteritis among children <5 years of age in Morocco during 1 year of sentinel hospital surveillance, June 2006-May 2007. J Infect Dis 200:70-75.
6. Chakravarti A, Chauhan MS, Sharma A, Verma V. 2010. Distribution of human rotavirus G and P genotypes in a hospital setting from Northern India. Southeast Asian J Trop Med Public Health 41:1145-1152.
7. Chouikha A, Fodha I, Noomen S, Bouzid L, Mastouri M, Peenze I, De Beer M, Dewar J, Geyer A, Sfar T, Gueddiche N, Messaadi F, Trabelsi A, Boujaafar N, Steele AD. 2007. Group A rotavirus strains circulating in the eastern center of Tunisia during a ten-year period (1995-2004). J Med Virol 79:1002-1008.
8. Correia JB, Patel MM, Nakagomi O, Montenegro FM, Germano EM, Correia NB, Cuevas LE, Parashar UD, Cunliffe NA, Nakagomi T. 2010. Effectiveness of monovalent rotavirus vaccine (Rotarix) against severe diarrhea caused by serotypically unrelated G2P[4] strains in Brazil. J Infect Dis 201:363-369.
9. Das BK, Gentsch JR, Cicirello HG, Woods PA, Gupta A, Ramachandran M, Kumar R, De Grazia S, Ramirez S, Giammanco GM, Colomba C, Martella V, Lo Biundo C, Mazzola R, Arista S. 1994. Characteization of rotavirusstrains from newborns in New Delhi, India. J Clin Microbiol 32:1820-1822.
10. Dennehy PH, Bertrand HR, Silas PE, Damaso S, Friedland LR, Abu-Elyazeed R. 2008. Coadministration of RIX4414 oral human rotavirus vaccine does not impact the immune response to antigens contained in routine infant vaccines in the United States. Pediatrics 122:e1062-e1066.
11. Desai R, Parashar UD, Lopman B, Helena de Oliveira L, Clark AD, Sanderson CF, Tate JE, Matus CR, Andrus JK, Patel MM. 2012. Potential intussusception risk versus health benefits from rotavirus vaccination in latin america. Clin Infect Dis 54:1397-1405.
12. Esteban LE, Rota RP, Gentsch JR, Jiang B, Esona M, Glass RI, Glikmann G, Castello AA. 2010. 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 82:1083-1093.
13. Estes MK. 1996. Advances in molecular biology: Impact on rotavirus vaccine development. J Infect Dis 174Suppl 1:37-46.
14. Estes MK, Cohen J. 1989. Rotavirus gene structure and function. Microbiol Rev 53:410-449.
15. Ferreira MS, Xavier Mda P, Tinga AC, Rose TL, Fumian TM, Fialho AM, de Assis RM, Costa FA, de Oliveira SA, Leite JP, Miagostovich MP. 2012. Assessment of gastroenteric viruses frequency in a children's day care center in Rio De Janeiro, Brazil: A Fifteen Year Study (1994-2008). PLoS ONE 7:e33754.
16. Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK. 1992. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30:1365-1373.
17. Gentsch JR, Woods PA, Ramachandran M, Das BK, Leite JP, Alfieri A, Kumar R, Bhan MK, Glass RI. 1996. Review of G and P typing results from a global collection of rotavirus strains: Implications for vaccine development. J Infect Dis 174:30-36.
18. Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K, Ramachandran M, Jain V, Cunliffe NA, Nakagomi O, Kirkwood CD, Fischer TK, Parashar UD, Bresee JS, Jiang B, Glass RI. 2005. Serotype diversity and reassortment between human and animal rotavirus strains: Implications for rotavirus vaccine programs. J Infect Dis 192:146-159.
19. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY. 1990. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28:276-282.
20. Gurgel RQ, Cuevas LE, Vieira SC, Barros VC, Fontes PB, Salustino EF, Nakagomi O, Nakagomi T, Dove W, Cunliffe N, Hart CA. 2007. Predominance of rotavirus P[4]G2 in a vaccinated population, Brazil. Emerg Infect Dis 13:1571-1573.
21. Hassine-Zaafrane M, Sdiri-Loulizi K, Ben Salem I, Kaplon J, Ayouni S, Ambert-Balay K, Sakly N, Pothier P, Aouni M. 2011. The molecular epidemiology of circulating rotaviruses: Three-year surveillance in the region of Monastir, Tunisia. BMC Infect Dis 11:266.
22. Iturriza-Gómara M, Isherwood B, Desselberger U, Gray J. 2001. Reassortment in vivo: Driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J Virol 75:3696-3705.
23. Iturriza-Gómara M, Dallman T, Bányai K, Böttiger B, Buesa J, Diedrich S, Fiore L, Johansen K, Koopmans M, Korsun N, Koukou D, Kroneman A, László B, Lappalainen M, Maunula L, Marques AM, Matthijnssens J, Midgley S, Mladenova Z, Nawaz S, Poljsak-Prijatelj M, Pothier P, Ruggeri FM, Sanchez-Fauquier A, Steyer A, Sidaraviciute-Ivaskeviciene I, Syriopoulou V, Tran AN, Usonis V, VAN Ranst M, DE Rougemont A, Gray J. 2010. Rotavirus genotypes co-circulating in Europe between 2006 and 2009 as determined by EuroRotaNet, a pan-European collaborative strain surveillance network. Epidemiol Infect 139:895-909.
24. Justino MC, Linhares AC, Lanzieri TM, Miranda Y, Mascarenhas JD, Abreu E, Guerra SF, Oliveira AS, da Silva VB, Sanchez N, Meyer N, Shafi F, Ortega-Barria E, Soriano-Gabarró M, Colindres RE. 2011. Effectiveness of the monovalent G1P[8] human rotavirus vaccine against hospitalization for severe G2P[4] rotavirus gastroenteritis in Belém, Brazil. Pediatr Infect Dis J 30:396-401.
25. Khamrin P, Peerakome S, Tonusin S, Malasao R, Okitsu S, Mizuguchi M, Ushijima H, Maneekarn N. 2007. Changing pattern of rotavirus G genotype distribution in Chiang Mai, Thailand from 2002 to 2004: Decline of G9 and reemergence of G1 and G2. J Med Virol 79:1775-1782.
26. Kirkwood CD, Boniface K, Barnes GL, Bishop RF. 2011. Distribution of rotavirus genotypes after introduction of rotavirus vaccines, Rotarix® and RotaTeq®, into the National Immunization Program of Australia. Pediatr Infect Dis J 30:48-53.
27. Madhi SA, Cunliffe NA, Steele D, Witte D, Kirsten M, Louw C, Ngwira B, Victor JC, Gillard PH, Cheuvart BB, Han HH, Neuzil KM. 2010. Effect of human rotavirus vaccine on severe diarrhea in African infants. N Engl J Med 362:289-298.
28. Martella V, Ciarlet M, Bányai K, Lorusso E, Cavalli A, Corrente M, Elia G, Arista S, Camero M, Desario C, Decaro N, Lavazza A, Buonavoglia C. 2006. Identification of a novel VP4 genotype carried by a serotype G5 porcine rotavirus strain. Virology 346:301-311.
29. Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K, Rahman M, Zeller M, Beutels P, Van Damme P, Van Ranst M. 2009. Rotavirus disease and vaccination: Impact on genotype diversity. Future Microbiol 4:1303-1316.
30. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K, Brister JR, Buesa J, Esona MD, Estes MK, Gentsch JR, Iturriza-Gómara M, Johne R, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Parreño V, Rahman M, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Patton JT, Desselberger U, Van Ranst M. 2011. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397-1413.
31. Page NA, Steele AD. 2004. Antigenic and genetic characterization of serotype G2 human rotavirus strains from South Africa from 1984 to 1998. J Med Virol 72:320-327.
32. Patel MM, de Oliveira LH, Bispo AM, Gentsch J, Parashar UD. 2008. Rotavirus P[4]G2 in a vaccinated population, Brazil. Emerg Infect Dis 14:863-865.
33. Patel MM, Steele D, Gentsch JR, Wecker J, Glass RI, Parashar UD. 2011. Real-world impact of rotavirus vaccination. Pediatr Infect Dis J 30:1-5.
34. Rahman M, Matthijnssens J, Nahar S, Podder G, Sack DA, Azim T, Van Ranst M. 2005. Characterization of a novel P[25], G11 human group a rotavirus. J Clin Microbiol 43:3208-3212.
35. Rahman M, Sultana R, Ahmed G, Nahar S, Hassan ZM, Saiada F, Podder G, Faruque AS, Siddique AK, Sack DA, Matthijnssens J, Van Ranst M, Azim T. 2007. Prevalence of G2P[4] and G12P[6] rotavirus, Bangladesh. Emerg Infect Dis 13:18-24.
36. Rahouma A, Klena JD, Krema Z, Abobker AA, Treesh K, Franka E, Abusnena O, Shaheen HI, El Mohammady, H, Abudher A, Ghenghesh KS. 2011. Enteric pathogens associated with childhood diarrhea in Tripoli-Libya. Am J Trop Med Hyg 84:886-891.
37. Ramachandran M, Das BK, Vij A, Kumar R, Bhambal SS, Kesari N, Rawat H, Bahl L, Thakur S, Woods PA, Glass RI, Bhan MK, Gentsch JR. 1996. Unusual diversity of human rotavirus G and P genotypes in India. J Clin Microbiol 34:436-439.
38. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, Cervantes Y, Linhares AC, López P, Macías-Parra M, Ortega-Barría E, Richardson V, Rivera-Medina DM, Rivera L, Salinas B, Pavía-Ruz N, Salmerón J, Rüttimann R, Tinoco JC, Rubio P, Nuñez E, Guerrero ML, Yarzábal JP, Damaso S, Tornieporth N, Sáez-Llorens X, Vergara RF, Vesikari T, Bouckenooghe A, Clemens R, De Vos B, O'Ryan M, Human Rotavirus Vaccine Study Group. 2006. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 354:11-22.
39. Santos N, Hoshino Y. 2005. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15:29-56.
40. Shui IM, Baggs J, Patel M, Parashar UD, Rett M, Belongia EA, Hambidge SJ, Glanz JM, Klein NP, Weintraub E. 2012. Risk of intussusception following administration of a pentavalent rotavirus vaccine in US infants. JAMA 307:598-604.
41. Soares-Weiser K, Maclehose H, Bergman H, Ben-Aharon I, Nagpal S, Goldberg E, Pitan F, Cunliffe N. 2012. Vaccines for preventing rotavirus diarrhoea: Vaccines in use. Cochrane Database Syst Rev 2:CD008521.
42. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD, WHO-coordinated Global Rotavirus Surveillance Network. 2012. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: A systematic review and meta-analysis. Lancet Infect Dis 12:136-141.
43. Todd S, Page NA, Duncan Steele A, Peenze I, Cunliffe NA. 2010. Rotavirus strain types circulating in Africa: Review of studies published during 1997-2006. J Infect Dis 202:34-42.
44. Trabelsi A, Fodha I, Chouikha A, Ben Hadj, Fredj M, Mastouri M, Abdelaziz AB, Sfar T, Essoussi AS, Jaoua S, Steele AD. 2010. Rotavirus strain diversity in the centre coast of Tunisia from 2000 through 2003. J Infect Dis 202:252-257.
45. Vesikari T, Itzler R, Matson DO, Santosham M, Christie CD, Coia M, Cook JR, Koch G, Heaton P. 2007. Efficacy of a pentavalent rotavirus vaccine in reducing rotavirus-associated health care utilization across three regions (11 countries). Int J Infect Dis 11:29-35.
46. Vesikari T, Karvonen A, Prymula R, Schuster V, Tejedor JC, Cohen R, Meurice F, Han HH, Damaso S, Bouckenooghe A. 2007. Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: Randomised, double-blind controlled study. Lancet 370:1757-1763.
47. Vizzi E, Piñeros O, González GG, Zambrano JL, Ludert JE, Liprandi F. 2011. Genotyping of human rotaviruses circulating among children with diarrhea in Valencia, Venezuela. J Med Virol 83:2225-2232.
48. Wierzba TF, Abdel-Messih IA, Abu-Elyazeed R, Putnam SD, Kamal KA, Rozmajzl P, Ahmed SF, Fatah A, Zabedy K, Shaheen HI, Sanders J, Frenck R. 2006. Clinic-based surveillance for bacterial- and rotavirus-associated diarrhea in Egyptian children. Am J Trop Med Hyg 74:148-153.
49. Yen C, Tate JE, Patel MM, Cortese MM, Lopman B, Fleming J, Lewis K, Jiang B, Gentsch J, Steele D, Parashar UD. 2011. Rotavirus vaccines: Update on global impact and future priorities. Hum Vaccin 7:1282-1290.
50. Zaman K, Dang DA, Victor JC, Shin S, Yunus M, Dallas MJ, Podder G, Vu DT, Le TP, Luby SP, Le HT, Coia ML, Lewis K, Rivers SB, Sack DA, Schödel F, Steele AD, Neuzil KM, Ciarlet M. 2010. Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: A randomised, double-blind, placebo-controlled trial. Lancet 376:615-623.
51. Zickafoose JS, Benneyworth BD, Riebschleger MP, Espinosa CM, Davis MM. 2012. Hospitalizations for intussusception before and after the reintroduction of rotavirus vaccine in the United States. Arch Pediatr Adolesc Med 166:350-355.