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PLOS ONE  2013 

Epidemiology and Genetic Diversity of Rotavirus Strains in Children with Acute Gastroenteritis in Lahore, Pakistan

DOI: 10.1371/journal.pone.0067998

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Abstract:

Pakistan harbors high disease burden of gastro-enteric infections with majority of these caused by rotavirus. Unfortunately, lack of proper surveillance programs and laboratory facilities have resulted in scarcity of available data on rotavirus associated disease burden and epidemiological information in the country. We investigated 1306 stool samples collected over two years (2008–2009) from hospitalized children under 5 years of age for the presence of rotavirus strains and its genotypic diversity in Lahore. The prevalence rate during 2008 and 2009 was found to be 34% (n = 447 out of 1306). No significant difference was found between different age groups positive for rotavirus (p>0.05). A subset of EIA positive samples was further screened for rotavirus RNA through RT-PCR and 44 (49.43%) samples, out of total 89 EIA positive samples, were found positive. G and P type prevalence was found as follows: G1P [4] = 3(6.81%); G1P [6] = 9(20.45%); G1P [8] = 1(2.27%); G2P [4] = 21(47.72%); G2P [8] = 1(2.27%); G9P [4] = 1(2.27%); G9P [6] = 1(2.27%) and G9P [8] = 7(15.90%). Phylogenetic analysis revealed that the VP7 and VP4 sequences clustered closely with the previously detected strains in the country as well as Belgian rotaviruses. Antigenic characterization was performed by analyzing major epitopes in the immunodominant VP7 and VP4 gene segments. Although the neutralization conferring motifs were found variable between the Pakistani strains and the two recommended vaccines strains (Rotarix? and RotaTeq?), we validate the use of rotavirus vaccine in Pakistan based on the proven and recognized vaccine efficacy across the globe. Our findings constitute the first report on rotavirus’ genotype diversity, their phylogenetic relatedness and epidemiology during the pre-vaccination era in Lahore, Pakistan and support the immediate introduction of rotavirus vaccine in the routine immunization program of the country.

References

[1]  Hoshino Y, Kapikian AZ (2000) Rotavirus serotypes: classification and importance in epidemiology, immunity, and vaccine development. J Health Popul Nutr 18: 5–14.
[2]  Rotavirus vaccines. Wkly Epidemiol Rec 82: 285–295.
[3]  Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI (2003) Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9: 565–572.
[4]  Glass RI, Bresee JS, Turcios R, Fischer TK, Parashar UD, et al. (2005) Rotavirus vaccines: targeting the developing world. J Infect Dis 192 Suppl 1S160–166.
[5]  Rotavirus surveillance–worldwide, 2001–2008. MMWR Morb Mortal Wkly Rep 57: 1255–1257.
[6]  Phan TG, Khamrin P, Quang TD, Dey SK, Takanashi S, et al. (2007) Detection and genetic characterization of group A rotavirus strains circulating among children with acute gastroenteritis in Japan. J Virol 81: 4645–4653.
[7]  Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Banyai K, et al. (2008) Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153: 1621–1629.
[8]  Gentsch JR, Laird AR, Bielfelt B, Griffin DD, Banyai K, et al. (2005) Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis 192 Suppl 1S146–159.
[9]  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.
[10]  Martella V, Banyai K, Matthijnssens J, Buonavoglia C, Ciarlet M (2010) Zoonotic aspects of rotaviruses. Vet Microbiol 140: 246–255.
[11]  Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Banyai K, et al. (2009) Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 4: 1303–1316.
[12]  Koopmans M, Brown D (1999) Seasonality and diversity of Group A rotaviruses in Europe. Acta Paediatr Suppl 88: 14–19.
[13]  Alam MM, Malik SA, Shaukat S, Naeem A, Sharif S, et al. (2009) Genetic characterization of rotavirus subtypes in Pakistan-first report of G12 genotype from Pakistan under WHO-Eastern Mediterranean region. Virus Res 144: 280–284.
[14]  Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, et al. (1990) Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28: 276–282.
[15]  Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, et al. (1992) Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30: 1365–1373.
[16]  Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, et al. (2009) Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science 324: 1444–1447.
[17]  Monnier N, Higo-Moriguchi K, Sun ZY, Prasad BV, Taniguchi K, et al. (2006) High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. J Virol 80: 1513–1523.
[18]  Lopman BA, Reacher MH, Van Duijnhoven Y, Hanon FX, Brown D, et al. (2003) Viral gastroenteritis outbreaks in Europe, 1995–2000. Emerg Infect Dis 9: 90–96.
[19]  McIver CJ, Hansman G, White P, Doultree JC, Catton M, et al. (2001) Diagnosis of enteric pathogens in children with gastroenteritis. Pathology 33: 353–358.
[20]  Simpson R, Aliyu S, Iturriza-Gomara M, Desselberger U, Gray J (2003) Infantile viral gastroenteritis: on the way to closing the diagnostic gap. J Med Virol 70: 258–262.
[21]  Dennehy PH (2005) Acute diarrheal disease in children: epidemiology, prevention, and treatment. Infect Dis Clin North Am 19: 585–602.
[22]  Logan C, O’Leary JJ, O’Sullivan N (2006) Real-time reverse transcription-PCR for detection of rotavirus and adenovirus as causative agents of acute viral gastroenteritis in children. J Clin Microbiol 44: 3189–3195.
[23]  Iturriza-Gomara M, Green J, Brown DW, Ramsay M, Desselberger U, et al. (2000) Molecular epidemiology of human group A rotavirus infections in the United Kingdom between 1995 and 1998. J Clin Microbiol 38: 4394–4401.
[24]  Kawai K, O’Brien MA, Goveia MG, Mast TC, El Khoury AC (2012) Burden of rotavirus gastroenteritis and distribution of rotavirus strains in Asia: a systematic review. Vaccine 30: 1244–1254.
[25]  Ansari SA, Springthorpe VS, Sattar SA (1991) Survival and vehicular spread of human rotaviruses: possible relation to seasonality of outbreaks. Rev Infect Dis 13: 448–461.
[26]  Bishop RF (1996) Natural history of human rotavirus infection. Arch Virol Suppl 12: 119–128.
[27]  Stoll BJ, Glass RI, Huq MI, Khan MU, Holt JE, et al. (1982) Surveillance of patients attending a diarrhoeal disease hospital in Bangladesh. Br Med J (Clin Res Ed) 285: 1185–1188.
[28]  Bresee J, Fang ZY, Wang B, Nelson EA, Tam J, et al. (2004) First report from the Asian Rotavirus Surveillance Network. Emerg Infect Dis 10: 988–995.
[29]  Dutta SR, Khalfan SA, Baig BH, Philipose L, Fulayfil R (1990) Epidemiology of rotavirus diarrhoea in children under five years in Bahrain. Int J Epidemiol 19: 722–727.
[30]  Hieber JP, Shelton S, Nelson JD, Leon J, Mohs E (1978) Comparison of human rotavirus disease in tropical and temperate settings. Am J Dis Child 132: 853–858.
[31]  Glass RI, Kilgore PE, Holman RC, Jin S, Smith JC, et al. (1996) The epidemiology of rotavirus diarrhea in the United States: surveillance and estimates of disease burden. J Infect Dis 174 Suppl 1S5–11.
[32]  Konno T, Suzuki H, Katsushima N, Imai A, Tazawa F, et al. (1983) Influence of temperature and relative humidity on human rotavirus infection in Japan. J Infect Dis 147: 125–128.
[33]  Nakagomi T, Nakagomi O, Takahashi Y, Enoki M, Suzuki T, et al. (2005) Incidence and burden of rotavirus gastroenteritis in Japan, as estimated from a prospective sentinel hospital study. J Infect Dis 192 Suppl 1S106–110.
[34]  Bishop RF, Masendycz PJ, Bugg HC, Carlin JB, Barnes GL (2001) Epidemiological patterns of rotaviruses causing severe gastroenteritis in young children throughout Australia from 1993 to 1996. J Clin Microbiol 39: 1085–1091.
[35]  Cook SM, Glass RI, LeBaron CW, Ho MS (1990) Global seasonality of rotavirus infections. Bull World Health Organ 68: 171–177.
[36]  Qazi R, Sultana S, Sundar S, Warraich H, un-Nisa T, et al. (2009) Population-based surveillance for severe rotavirus gastroenteritis in children in Karachi, Pakistan. Vaccine 27 Suppl 5F25–30.
[37]  Wen L, Ushijima H, Kakizawa J, Fang ZY, Nishio O, et al. (1995) Genetic variation in VP7 gene of human rotavirus serotype 2 (G2 type) isolated in Japan, China, and Pakistan. Microbiol Immunol 39: 911–915.
[38]  Nishio O, Matsui K, Oka T, Ushijima H, Mubina A, et al. (2000) Rotavirus infection among infants with diarrhea in Pakistan. Pediatr Int 42: 425–427.
[39]  Bhan MK, Lew JF, Sazawal S, Das BK, Gentsch JR, et al. (1993) Protection conferred by neonatal rotavirus infection against subsequent rotavirus diarrhea. J Infect Dis 168: 282–287.
[40]  Clark HF, Lawley DA, Schaffer A, Patacsil JM, Marcello AE, et al. (2004) Assessment of the epidemic potential of a new strain of rotavirus associated with the novel G9 serotype which caused an outbreak in the United States for the first time in the 1995–1996 season. J Clin Microbiol 42: 1434–1438.
[41]  Miles MG, Lewis KD, Kang G, Parashar UD, Steele AD (2012) A systematic review of rotavirus strain diversity in India, Bangladesh, and Pakistan. Vaccine 30 Suppl 1A131–139.
[42]  Rahman M, Matthijnssens J, Nahar S, Podder G, Sack DA, et al. (2005) Characterization of a novel P[25],G11 human group a rotavirus. J Clin Microbiol 43: 3208–3212.
[43]  Das S, Varghese V, Chaudhury S, Barman P, Mahapatra S, et al. (2003) Emergence of novel human group A rotavirus G12 strains in India. J Clin Microbiol 41: 2760–2762.
[44]  Rotavirus vaccines. WHO position paper - January 2013. Wkly Epidemiol Rec 88: 49–64.
[45]  McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L, et al. (2009) Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog 5: e1000634.
[46]  Zeller M, Rahman M, Heylen E, De Coster S, De Vos S, et al. (2010) Rotavirus incidence and genotype distribution before and after national rotavirus vaccine introduction in Belgium. Vaccine 28: 7507–7513.
[47]  Zeller M, Patton JT, Heylen E, De Coster S, Ciarlet M, et al. (2012) Genetic analyses reveal differences in the VP7 and VP4 antigenic epitopes between human rotaviruses circulating in Belgium and rotaviruses in Rotarix and RotaTeq. J Clin Microbiol 50: 966–976.
[48]  Kirkwood CD, Boniface K, Barnes GL, Bishop RF (2011) Distribution of rotavirus genotypes after introduction of rotavirus vaccines, Rotarix(R) and RotaTeq(R), into the National Immunization Program of Australia. Pediatr Infect Dis J 30: S48–53.
[49]  Boom JA, Tate JE, Sahni LC, Rench MA, Hull JJ, et al. (2010) Effectiveness of pentavalent rotavirus vaccine in a large urban population in the United States. Pediatrics 125: e199–207.
[50]  Hull JJ, Teel EN, Kerin TK, Freeman MM, Esona MD, et al. (2011) United States rotavirus strain surveillance from 2005 to 2008: genotype prevalence before and after vaccine introduction. Pediatr Infect Dis J 30: S42–47.
[51]  Iturriza-Gomara M, Cubitt D, Steele D, Green J, Brown D, et al. (2000) Characterisation of rotavirus G9 strains isolated in the UK between 1995 and 1998. J Med Virol 61: 510–517.
[52]  Oka T, Nakagomi T, Nakagomi O (2000) Apparent re-emergence of serotype G9 in 1995 among rotaviruses recovered from Japanese children hospitalized with acute gastroenteritis. Microbiol Immunol 44: 957–961.
[53]  Laird AR, Gentsch JR, Nakagomi T, Nakagomi O, Glass RI (2003) Characterization of serotype G9 rotavirus strains isolated in the United States and India from 1993 to 2001. J Clin Microbiol 41: 3100–3111.
[54]  Coulson BS, Kirkwood C (1991) Relation of VP7 amino acid sequence to monoclonal antibody neutralization of rotavirus and rotavirus monotype. J Virol 65: 5968–5974.
[55]  Gomara MI, Cubitt D, Desselberger U, Gray J (2001) Amino acid substitution within the VP7 protein of G2 rotavirus strains associated with failure to serotype. J Clin Microbiol 39: 3796–3798.
[56]  Jin Q, Ward RL, Knowlton DR, Gabbay YB, Linhares AC, et al. (1996) Divergence of VP7 genes of G1 rotaviruses isolated from infants vaccinated with reassortant rhesus rotaviruses. Arch Virol 141: 2057–2076.
[57]  Soares-Weiser K, Maclehose H, Ben-Aharon I, Goldberg E, Pitan F, et al.. (2010) Vaccines for preventing rotavirus diarrhoea: vaccines in use. Cochrane Database Syst Rev: CD008521.
[58]  Patel MM, Clark AD, Sanderson CF, Tate J, Parashar UD (2012) Removing the age restrictions for rotavirus vaccination: a benefit-risk modeling analysis. PLoS Med 9: e1001330.
[59]  Giaquinto C, Dominiak-Felden G, Van Damme P, Myint TT, Maldonado YA, et al. (2011) Summary of effectiveness and impact of rotavirus vaccination with the oral pentavalent rotavirus vaccine: a systematic review of the experience in industrialized countries. Hum Vaccin 7: 734–748.
[60]  Richardson V, Hernandez-Pichardo J, Quintanar-Solares M, Esparza-Aguilar M, Johnson B, et al. (2010) Effect of rotavirus vaccination on death from childhood diarrhea in Mexico. N Engl J Med 362: 299–305.
[61]  do Carmo GM, Yen C, Cortes J, Siqueira AA, de Oliveira WK, et al. (2011) Decline in diarrhea mortality and admissions after routine childhood rotavirus immunization in Brazil: a time-series analysis. PLoS Med 8: e1001024.
[62]  Linhares AC, Velazquez FR, Perez-Schael I, Saez-Llorens X, Abate H, et al. (2008) 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 371: 1181–1189.
[63]  Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, Abate H, Breuer T, et al. (2006) Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 354: 11–22.
[64]  Vesikari T, Karvonen A, Puustinen L, Zeng SQ, Szakal ED, et al. (2004) Efficacy of RIX4414 live attenuated human rotavirus vaccine in Finnish infants. Pediatr Infect Dis J 23: 937–943.
[65]  Block SL, Vesikari T, Goveia MG, Rivers SB, Adeyi BA, et al. (2007) Efficacy, immunogenicity, and safety of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine at the end of shelf life. Pediatrics 119: 11–18.
[66]  Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, et al. (2006) Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 354: 23–33.
[67]  Meeting of the immunization Strategic Advisory Group of Experts, April 2009–conclusions and recommendations. Wkly Epidemiol Rec 84: 220–236.

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