Skip to main content
NCBI home page
Wiley - PMC COVID-19 Collection logoLink to Wiley - PMC COVID-19 Collection
. 2010 Jan 19;82(3):519–527. doi: 10.1002/jmv.21708

Characterization of group A rotavirus infections in adolescents and adults from Pune, India: 1993–1996 and 2004–2007†

Vaishali S Tatte 1, Jon R Gentsch 2, Shobha D Chitambar 1,✉
PMCID: PMC7167167  PMID: 20087938

Abstract

A total of 1,591 fecal specimens were collected in 1993–1996 and 2004–2007 from adolescents and adults with acute gastroenteritis in Pune, India for detection and characterization of rotavirus. At the two time points, group A rotavirus was detected in 8.6% and 16.2% of the adolescents and 5.2% and 17.2% of the adults, respectively. Reverse transcription‐PCR with consensus primers followed by multiplex genotyping PCR detected common strains G1P[8], G2P[4], G3P[8], and G4P[8] in a total of 53.1% of the samples from 1993 to 1996, while the only prevalent strain identified in 2004–2007 was G2P[4] (23.5% of total). Uncommon rotavirus strains (G1P[4], G2P[8] G9P[6]/P[4]) increased from 7.8% (1993–1996) to 41.2% (2004–2007), while the prevalence of mixed rotavirus infections was high (39%/35%) at both time points. Mixed infections detected by multiplex PCR were confirmed by sequencing two or more individual genotype‐specific PCR products of the VP7 and VP4 genes from the same sample. Phylogenetic analysis of the sequences showed circulation of a heterogeneous rotavirus strain population comprising genotypes G1 (lineages I and IIb), G2 (lineages I and IIb), G4 (lineage Ia), P[4] (lineages P[4]‐5 and P[4]‐1), P[8] (lineages P[8]‐II and P[8]‐III), and P[6] (M37‐like lineage). The VP6 gene sequences of the nontypeable strains were most homologous to animal strains. This study documents the molecular epidemiology of rotavirus strains in adolescents and adults in India, and suggests that it may be important to monitor these strains over time for the potential impact on rotavirus vaccines under development for use in the Indian population. J. Med. Virol. 82:519–527, 2010. © 2010 Wiley‐Liss, Inc.

Keywords: epidemiology, adult diarrhea, G and P types, rotavirus

†

The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention

REFERENCES

  1. Anderson EJ, Weber SG. 2004. Rotavirus infection in adults. Lancet Infect Dis 4: 91–99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ansaldi F, Pastorino B, Valle L, Durando P, Sticchi L, Tucci P, Biasci P, Lai P, Gasparini R, Icardi G. 2007. Molecular characterization of a new variant of rotavirus P[8]G9 predominant in a sentinal‐based survey in central Italy. J Clin Microbiol 45: 1011–1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Araujo IT, Assis RM, Fialho AM, Mascarenhas JD, Heinemann MB, Leite JP. 2007. Brazilian P[8]G1,P[8]G5, P[8]G9, and P[4]G2 rotavirus stains: Nucleotide sequence and phylogenetic analysis. J Med Virol 79: 995–1001. [DOI] [PubMed] [Google Scholar]
  4. Arista S, Giammanco GM, De., Grazia S, Ramirez S, Biundo CL, Colomba C, Cascio A, Martella V. 2006. Heterogeneity and temporal dynamics of evolution of G1 human rotaviruses in a settled population. J Virol 80: 10724–10733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Banyai K, Martella V, Jakab F, Melegh B, Szucs G. 2004. Sequencing and phylogenetic analysis of human genotype P[6] rotavirus strains detected in Hungary provides evidence for genetic heterogeneity within the P[6] VP4 gene. J Clin Microbiol 42: 4338–4343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bok K, Matson DO, Gomez JA. 2002. Genetic variation of capsid protein VP7 in genotype G4 human rotavirus strains: Simultaneous emergence and spread of different lineages in Argentina. J Clin Microbiol 40: 2016–2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carraro E, Perosa AHS, Siqueira I, Pasternak J, Martino MDV. 2008. Rotavirus infections in children and adult patients attending in a tertiary hospital of Sao Paulo, Brazil. Brazil J Infect Dis 12: 44–46. [DOI] [PubMed] [Google Scholar]
  8. Chitambar SD, Tatte V, Dhongde R, Kalrao V. 2008. High frequency of rotavirus viremia in children with acute gastroenteritis: Discordance of strains detected in stool and sera. J Med Virol 80: 2169–2176. [DOI] [PubMed] [Google Scholar]
  9. Chouikha A, Fodha I, Noomen S, Bouzid L, Mastouri M, Peeze I, Beer MD, 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. [DOI] [PubMed] [Google Scholar]
  10. Cook SM, Glass RI, Lebaron CW, Ho MS. 1990. Global seasonality of rotavirus infections. Bull WHO 68: 171–177. [PMC free article] [PubMed] [Google Scholar]
  11. Crouch CF, Acres SD. 1984. Prevalence of rotavirus and coronavirus antigens in the feces of normal cows. Can J Comp Med 48: 340–342. [PMC free article] [PubMed] [Google Scholar]
  12. Cunliffe NA, Gondwe JS, Graham SM, Thindwa BD, Dove W, Broadhead RL, Molyneux ME, Hart CA. 2001. Rotavirus strain diversity in Blantyre, Malawi, from 1997–1999. J Clin Microbiol 39: 836–843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Das S, Sen A, Uma G, Varghese V, Chaudhuri S, Bhattacharya SK, Mitra U, Kobayashi N, Naik TN. 2002. Genomic diversity of group A rotavirus strains infecting humans in eastern India. J Clin Microbiol 40: 146–149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. del Refugio Gonzalez‐Losa M, Polanco‐Marin GG, Manzano‐Cabrera L, Puerto‐Solis M. 2001. Acute gastroenteritis associated with rotavirus in adults. Arch Med Res 32: 164–167. [DOI] [PubMed] [Google Scholar]
  15. Espinola EE, Amarilla A, Arbiza J, Parra GI. 2008. Sequence and phylogenetic analysis of the VP4 gene of human rotaviruses in Paraguay. Arch Virol 153: 1067–1073. [DOI] [PubMed] [Google Scholar]
  16. Estes MK, Kapikian AZ. 2007. Rotaviruses In: Knipe DM, Howley PM, Griffin DE, Martin MA, Lamb RA, Roizman B, Straus SE, editors. Fields virology. 5th edition Philadelphia, PA: Lippincott‐Raven Publishers; pp. 1917–1974. [Google Scholar]
  17. Faruque AS, Malek MA, Khan AI, Hug S, Salam MA, Sack DA. 2004. Diarrhea in elderly people: Aetiology, and clinical characteristics. Scand J Infect Dis 36: 204–208. [DOI] [PubMed] [Google Scholar]
  18. Fischer TK, Eugen‐Olsen J, Pedersen AG, Molbak K, Bottiger B, Rostgaard K, Nielsen NM. 2005. Characterization of rotavirus strains in a Danish population: High frequency of mixed infections and diversity within the VP4 gene of P[8] strains. J Clin Microbiol 43: 1099–1104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Freeman MM, Kerin T, Jennifer H, Caustland KM, Gentsch J. 2008. Enhancement of detection and quantification of rotavirus in stool using a modified real time RT‐PCR assay. J Med Virol 80: 1489–1496. [DOI] [PubMed] [Google Scholar]
  20. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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: S146–S159. [DOI] [PubMed] [Google Scholar]
  22. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hrdy DB. 1987. Epidemiology of rotaviral infection in adults. Rev Infect Dis 9: 461–469. [DOI] [PubMed] [Google Scholar]
  24. Iturriza‐Gomara M, Green J, Brown DW, Ramsay M, Desselberger U, Gray JJ. 2000a. Molecular epidemiology of human group A rotavirus infections in the United Kingdom between 1995 and 1998. J Clin Microbiol 38: 4394–4401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Iturriza‐Gomara M, Green J, David WG, Desselberger U, Gray JJ. 2000b. Diversity within the VP4 gene of rotavirus P[8] strains: Implications for the reverse transcription‐PCR genotyping. J Clin Microbiol 38: 898–901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Iturriza‐Gomara M, Wong C, Blome S, Desselberger U, Gray J. 2002. Molecular characterization of VP6 genes of human rotavirus isolates: Correlation of genogroups with subgroups and evidence of independent segregation. J Virol 76: 6596–6601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jain V, Das BK, Bhan MK, Glass RI, Gentsch JR, Indian Strain Surveillance Collaborating Laboratories . 2001. Great diversity of group A rotavirus strains and high prevalence of mixed rotavirus infections in India. J Clin Microbiol 39: 3524–3529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kang G, Kelkar SD, Chitambar SD, Ray P, Naik T. 2005. Epidemiological profile of rotavirus infection in India: Challenges for the 21st century. J Infect Dis 192: S120–S126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kelkar SD, Ayachit VL. 2000. Circulation of group A rotavirus subgroups and serotypes in Pune, India, 1990–1997. J Health Popul Nutr 18: 163–170. [PubMed] [Google Scholar]
  30. Kelkar SD, Bhide VS, Ranshing SS, Bedekar SS. 2004. Rapid ELISA for the diagnosis of rotavirus. Ind J Med Res 119: 60–65. [PubMed] [Google Scholar]
  31. Kerin TK, Kane EM, Glass RI, Gentsch JR. 2007. Characterization of VP6 genes from rotavirus strains collected in the United States from 1996–2002. Virus Genes 35: 489–495. [DOI] [PubMed] [Google Scholar]
  32. Kudo S, Zhou Y, Cao XR, Yamanashi S, Nakata S, Ushijima H. 2001. Molecular characterization in the VP7, VP4 and NSP4 genes of human rotavirus serotype 4 (G4) isolated in Japan and Kenya. Microbiol Immunol 45: 167–171. [DOI] [PubMed] [Google Scholar]
  33. Kumar S, Tamura K, Nei M. 2004. MEGA 3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150–163. [DOI] [PubMed] [Google Scholar]
  34. Maldonado YA, Yolken RH. 1990. Rotavirus. Baillieres Clin Gastroenterol 4: 609–625. [DOI] [PubMed] [Google Scholar]
  35. Mascarenhas J, D'Arc. P, Linarhes AC, Bayma APG, Lima JC, Sousa MS, Araujo IT, Heinemann MB, Gusmao RHP, Gabbay YB, Leite JPG. 2006. Molecular analysis of VP4, VP7 and NSP4 genes of P[6]G2 rotavirus genotype strains recovered from neonates admitted to hospital in Belem, Brazil. J Med Virol 78: 281–289. [DOI] [PubMed] [Google Scholar]
  36. Page NA, Steele AD. 2004. Antigenic and genetic characterization of serotype G2 human rotavirus strains from the African continent. J Clin Microbiol 42: 595–600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Parashar UD, Gibson CJ, Bresse JS, Glass RI. 2006. Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12: 304–306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pietruchinski E, Benati F, Lauretti F, Kisielius J, Ueda M, Volotao EM, Soares CC, Hoshino Y, Linhares RE, Nozawa C, Santos N. 2006. Rotavirus diarrhea in children and adults in a southern city of Brazil in 2003: Distribution of G–P types and finding of a rare G12 strain. J Med Virol 78: 1241–1249. [DOI] [PubMed] [Google Scholar]
  39. 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: 436–444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ramani S, Kang G. 2007. Burden of disease and molecular epidemiology of group A rotavirus infections in India. Ind J Med Res 125: 612–632. [PMC free article] [PubMed] [Google Scholar]
  41. Ray PG, Kelkar SD. 2004. Measurement of antirotavirus IgM/IgA/IgG responses in the serum samples of Indian children following rotavirus diarrhea and their mothers. J Med Virol 72: 416–423. [DOI] [PubMed] [Google Scholar]
  42. Rubliar‐Abreu E, Hedlund KO, Svensson L, Mittelholzer C. 2005. Serotype G9 rotavirus infections in adults in Sweden. J Clin Microbiol 43: 1374–1376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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. [DOI] [PubMed] [Google Scholar]
  44. Sharma S, Ray P, Gentsh JR, Glass RI, Kalra V, Bhan MK. 2008. Emergence of [12G] rotavirus strains in Dehli, 2000–2007. J Clin Microbiol 46: 1343–1348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Solberg OD, Hasing ME, Trueba G, Eisenberg JNS. 2009. Characterization of novel VP7, VP4, and VP6 genotypes of a previously untypeable group A rotavirus. Virology 385: 58–67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The Clustal X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Timenetsky MC, Gouvea V, Santos N, Alge ME, Kisiellius JJ, Carmona RC. 1996. Outbreak of severe gastroenteritis in adults and children associated with type G2 rotavirus. J Diarrhoeal Dis Res 14: 71–74. [PubMed] [Google Scholar]
  48. Unicomb LE, Podder G, Gentsch JR, Woods PA, Hazan KZ, Faruque AS, Albert MJ, Glass RI. 1999. Evidence of high‐frequency genomic reassortment of group A rotavirus strains in Bangladesh: Emergence of type G9 in 1995. J Clin Microbiol 37: 1885–1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wang YH, Kobayashi N, Zhou DJ, Yang ZQ, Zhou X, Peng JS, Zhu ZR, Zhao DF, Liu MQ, Gong J. 2007. Molecular epidemiologic analysis of group A rotaviruses in adults and children with Wuhan city, China, 2000–2006. Arch Virol 152: 669–685. [DOI] [PubMed] [Google Scholar]
  50. Wilde J, Eiden J, Yolken R. 1990. Removal of inhibitory substances from human fecal specimens for detection of group A rotaviruses by reverse transcriptase and polymerase chain reaction. J Clin Microbiol 28: 1300–1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Xin KQ, Morikawa S, Fang ZY, Mukoyama A, Okuda K, Ushijima H. 1993. Genetic variation in VP7 gene of human rotavirus serotype I (G1 type) isolated in Japan and China. Virology 197: 813–816. [DOI] [PubMed] [Google Scholar]
  52. Zade JK, Chhabra P, Chitambar SD. 2009. Characterization of VP7 and VP4 genes of rotavirus strains: 1990–1994 and 2000–2002. Epidemiol Infect 137: 938–942. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Medical Virology are provided here courtesy of Wiley

RESOURCES