Enteric Viruses

  • C. Anthony Hart
  • Nigel A. Cunliffe


Viruses interact with the gastro-intestinal tract in a number of ways. Some viruses such as hepatitis A virus and the enteroviruses use the intestine as a portal of entry and rarely, if ever, produce diarrhoeal disease. Others cause diarrhoeal disease only when the immune system is compromised, for example, HIV and cytomegalovirus (HHV-5). Human papillomaviruses and Kaposi’s sarcoma associated herpesvirus (HHV-8) can affect the gastro-intestinal tract causing local tumours. On stool electron microscopy, bacteriophages can be seen (Fig. 1) which can be mistaken for other viruses. Bacteriophages are viruses that infect bacteria and are involved only indirectly in human disease, for example, acting as vectors for toxin genes (e.g. shiga toxins 1 and 2 in Escherichia coli 0157). However, here we will concentrate on the virology and laboratory diagnosis of the enteric viruses that are primary pathogens causing diarrhoeal disease (Table 1). The relative importance of viruses and the various enteric viruses depends upon the patient’s age and their state of immunity. Undoubtedly, viruses are the most important causes of diarrhoeal disease in infants and young children whether HIV-infected or not [1].


Enteric Virus Bovine Diarrhoea Virus Diarrhoeal Disease Rabbit Haemorrhagic Disease Virus Norwalk Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Hart CA, Cunliffe NA (1999) Viral gastroenteritis. Curr Opin Infect Dis 12:447–457PubMedCrossRefGoogle Scholar
  2. 2.
    Bishop RF, Davidson GP, Holmes IH, Ruck BJ (1973) Virus particles from children with viral gastroenteritis. Lancet 1:1281–1283CrossRefGoogle Scholar
  3. 3.
    Burns NW, Sidat-Pajouh M, Krishnaney AA, Greenberg HB (1996) Protective effect of rotavirus VP6-spe-cific IgA monoclonal antibodies that lack neutralizing activity. Science 272:104–107PubMedCrossRefGoogle Scholar
  4. 4.
    Riepenhaff-Talty SM, Morse K, Wang CH, et al(1997) Epidemiology of group C rotavirus infection in western New York women of child-bearing age. J Clin Microbiol 35:486–488Google Scholar
  5. 5.
    Cunliffe NA, Dove W, Jiang B, et al(2001) Detection of group C rotavirus in children with acute gastroenteritis in Blantyre, Malawi. Pediatr Infect Dis J 20:1088–1190PubMedCrossRefGoogle Scholar
  6. 6.
    Krishnan T, Sen A, Sinha J, et al(1999) Emergence of adult diarrhoea rotavirus in Calcutta, India. Lancet 353:380–381PubMedCrossRefGoogle Scholar
  7. 7.
    Cunliffe NA, Bresee JS, Gentsch JR, et al(2002) The expanding diversity of rotaviruses. Lancet 359:640–642PubMedCrossRefGoogle Scholar
  8. 8.
    Gentsch JR, Woods PA, Ramachandran M, et al (1996) Review of G and P typing results from a global collection rotavirus strains: implications for vaccine development. J Infect Dis 174:S30–S36PubMedCrossRefGoogle Scholar
  9. 9.
    Gouvea V, de Castro L, Timenetsky M, et al(1994) Rotavirus serotype G5 associated with diarrhea in Brazilian children. J Clin Microbiol 32:1408–1409PubMedGoogle Scholar
  10. 10.
    Cunliffe NA, Gondwe JS, Graham SM, et al(2001) Rotavirus strain diversity in Blantyre Malawi from 1997 to 1999; J Clin Microbiol 39:836–843PubMedCrossRefGoogle Scholar
  11. 11.
    Abah MA, Rohwedder A, Olaleye OD, Werchau H (1997) Nigerican rotavirus G8 could not be typed by PCR due to nucleotide mutation at the 3’ end of the primer binding site. Arch Virol 142:1881–1887CrossRefGoogle Scholar
  12. 12.
    Ramachandran M, Kirkwood CD, Unicomb L, et al (2000) Molecular characterization of serotype G9 rotavirus strains from a global collection. Virology 278:436–444PubMedCrossRefGoogle Scholar
  13. 13.
    Cunliffe NA, Dove W, Bunn JEG, et al(2001) Expanding global distribution of rotavirus serotype G9: detection in Libya, Kenya and Cuba. Emerg Infect Dis 7:890–892PubMedGoogle Scholar
  14. 14.
    Lynch M, Bresee JS, Gentsch JR, Glass RI (2000) Rotavirus vaccines. Curr Opin Infect Dis 13:495–502PubMedCrossRefGoogle Scholar
  15. 15.
    Cunliffe NA, Kilgore PE, Bresee JS, et al(1998) Epidemiology of rotavirus diarrhoea in Africa: a review to assess the need for rotavirus immunization. Bull WHO 76:525–537PubMedGoogle Scholar
  16. 16.
    Batt RM, Embaye H, van de Waal S, et al(1995) Application of organ culture of small intestine to the investigation of enterocyte damage by equine rotavirus. J Pediatr Gastroenterol Nutr 20:326–332PubMedCrossRefGoogle Scholar
  17. 17.
    Jourdan N, Brunet JP, Sapia C, et al(1998) Rotavirus infection reduces sucrase-isomaltase expression in human intestinal epithelial cells by perturbing protein targetting and organisation of microvillar cytoskeleton. J Virol 72:7228–7236PubMedGoogle Scholar
  18. 18.
    Perez JF, Chemello MC, Kiprandi F, et al(1998) Oncosis in MA 104 cells is induced by rotavirus infection through an increase in intracellular Ca2+ concentrations. Virology 252:17–27PubMedCrossRefGoogle Scholar
  19. 19.
    Lundgren O, Svensson L (2001) Pathogenesis of rotavirus diarrhea. Microbes Infect 3:1145–1166PubMedCrossRefGoogle Scholar
  20. 20.
    Ball JM, Jian P, Zeng CQ-Y et al (1996) Age dependent diarrhea induced by a rotaviral non-structural protein. Science 272:101–104PubMedCrossRefGoogle Scholar
  21. 21.
    Franco MA, Greenberg HB (1995) Role of B-cells and cytotoxic T-lymphocytes in clearance of and immunity to rotavirus in mice. J Virol 69:7800–7806PubMedGoogle Scholar
  22. 22.
    Velazquez FR, Matson DO, Calva JJ, et al(1996) Rotavirus infection in infants as protection against subsequent infection. New Engl J Med 335:1022–1028PubMedCrossRefGoogle Scholar
  23. 23.
    Yuan L, Ward LA, Rosen BI, et al(1996) Systemic and intestinal antibody secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J Virol 70:3075–3081PubMedGoogle Scholar
  24. 24.
    Ibrahim OS, Sunderland D, Hart CA (1990) Comparison of four methods for detection of rotavirus in faeces. Trop Doct 20:30–32PubMedGoogle Scholar
  25. 25.
    Hammarstrom L (1999) Passive immunity against rotavirus in infants. Acta paediatr 88 [Suppl]:127–132CrossRefGoogle Scholar
  26. 26.
    Sarker SA, Casswall TH, Juneja LR, et al(2001) Randomized, placebo-controlled, clinical trial of hyperimmunized chicken egg yolk immunoglobulin in children with rotavirus diarrhea. J Pediatr Gastroenterol Nutr 32:19–25PubMedCrossRefGoogle Scholar
  27. 27.
    Szajewska H, Mrukowicz JZ (2001) Probiotics in the treatment of prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J Pediatr Gastroenterol Nutr 33:S17–S25PubMedCrossRefGoogle Scholar
  28. 28.
    Murphy TV, Garguillo PM, Massoudi MS, et al(2001) Intussusception among infants given oral rotavirus vaccine. New Engl J Med 334:564–572CrossRefGoogle Scholar
  29. 29.
    Cunliffe NA, Bresee JS, Hart CA (2002) Rotavirus vaccines: development, current issues and future prospects. J Infect, (in press)Google Scholar
  30. 30.
    Cunliffe NA, Gondwe JS, Kirkwood CD, et al(2001) Effect of concomitant HIV infection on presentation and outcome of rotavirus gastroenteritis in Malawian children. Lancet 358:550–555PubMedCrossRefGoogle Scholar
  31. 31.
    De Jong JC, Wermenbol AG, Verweij-Uijterwaal MW, et al (1999) Adenovirus from human immunodeficiency virus-infected individuals including two strains that represent new candidate serotypes Ad50 and Ad51 of species B1 and D respectively. J Clin Microbiol 37:3940–3945PubMedGoogle Scholar
  32. 32.
    Lord A, Bailey AS, Klapper PE, et al(2000) Impaired humoral responses to subgenus D adenovirus infections in HIV-positive patients. J Med Virol 62:405–409PubMedCrossRefGoogle Scholar
  33. 33.
    Unicomb LE, Jareckikhan K, Hall A, Podder G (1996) Previous enteric adenovirus infection does not protect against subsequent symptomatic infection: longitudinal follow-up of 8 infants. Microbiol Immunol 40:161–168PubMedGoogle Scholar
  34. 34.
    Moore PL, Steele AD, Alexander JJ (2000) Relevance of commercial diagnostic tests to detection of enteric adenovirus infections in South Africa. J Clin Microbiol 38:1661–1663PubMedGoogle Scholar
  35. 35.
    Abad FX, Villena C, Guix S, et al(2001) Potential role of fomites in vehicular transmission of human astroviruses. Appl Env Microbiol 67:3904–3907CrossRefGoogle Scholar
  36. 36.
    Herrmann JE, Taylor BN, Echeverria P, Blacklow NR (1991) Astroviruses as a cause of gastroenteritis in children. New Engl J Med 324:1757–1760PubMedCrossRefGoogle Scholar
  37. 37.
    Maldonaldo Y, Cantwell M, Old M, et al(1998) Population-based prevalence of symptomatic and asymptomatic astrovirus infection in rural Mayan infants. J Infect Dis 178:334–339CrossRefGoogle Scholar
  38. 38.
    Cunliffe NA, Dove W, Gondwe JS, et al(2002) Detection and characterization of human astroviruses in children with acute gastroenteritis in Blantyre, Malawi. J Med Virol 67:563–566PubMedCrossRefGoogle Scholar
  39. 39.
    Guix S, Caballero S, Villena C, et al(2002) Molecular epidemiology of astrovirus infection in Barcelona, Spain. J Clin Microbiol 40:133–139PubMedCrossRefGoogle Scholar
  40. 40.
    Walter JE, Mitchell DK (2000) Role of astroviruses in childhood diarrhea. Curr Opin Pediatr 12:275–279PubMedCrossRefGoogle Scholar
  41. 41.
    Koopmans MPG, Bijen MHL, Monroe SS, Vinje J (1998) Age-stratified seroprevalence of neutralizing antibodies to astrovirus types 1 to 7 in humans in the Netherlands. Clin Diagn Lab Immunol 5:33–37PubMedGoogle Scholar
  42. 42.
    Unicomb LE, Banu NN, Azim T, et al(1998) Astrovirus in association with acute, persistent and nosocomial diarrhea in Bangladesh. Pediatr Infect Dis J 17:611–614PubMedCrossRefGoogle Scholar
  43. 43.
    Grohmann GS, Glass RI, Pereira WG, et al(1993) Enteric viruses and diarrhea in HIV-infected patients. New Engl J Med 329:14–20PubMedCrossRefGoogle Scholar
  44. 44.
    Gonzalez GG, Pinjol FH, Liprandi F, et al(1993) prevalence of enteric viruses in human immunodeficiency virus seropositive patients in Venezuela. J Med Virol 55:288–292CrossRefGoogle Scholar
  45. 45.
    Liste MB, Natera I, Suarez JA, et al(2000) Enteric virus infections and diarrhea in healthy and human immunodeficiency virus-infected children. J Clin Microbiol 38:2873–2877PubMedGoogle Scholar
  46. 46.
    Cox GJ, Matsui SM, Lo RS, et al(1994) Etiology and outcome of diarrhea after marrow transplantation: a prospective study. Gastroenterol 107:1398–1407Google Scholar
  47. 47.
    Clarke IN, Lambden PR (1997) The molecular biology of caliciviruses. J Gen Virol 78:291–301PubMedGoogle Scholar
  48. 48.
    Atmar RL, Estes MK (2001) Diagnosis of noncultivable gastroenteritis viruses, the human caliciviruses. Clin Microbiol Rev 14:15–37PubMedCrossRefGoogle Scholar
  49. 49.
    Green KY, Ando T, Balayan MS, et al (2000) Taxonomy of the caliciviruses. J Infect Dis 181[Suppl 2]:S322–S330PubMedCrossRefGoogle Scholar
  50. 50.
    Noel JS, Fankhauser RL, Ando T, et al(1999) Identification of a distinct common strain of “Norwalk-like virus” having a global distribution. J Infect Dis 179:1334–1344PubMedCrossRefGoogle Scholar
  51. 51.
    Glass RI, Noel J, Ando T, et al (2000) The epidemiology of enteric caliciviruses from humans: a reassessment using new diagnostics. J Infect Dis 181[Suppl 2]:S254–S261PubMedCrossRefGoogle Scholar
  52. 52.
    Nakata S, Honma S, Numata K, et al(1998) Prevalence of human calicivirus infections in Kenya as determined by enzyme immunoassays for three genogroups of virus. J Clin Microbiol 36:3160–3163PubMedGoogle Scholar
  53. 53.
    Honma S, Nakata S, Numata K, et al(1998) Epidemiological study of prevalence of genogroup II human calicivirus (Mexico virus) infections in Japan and Southeast Asia as determined by enzyme-linked immunosorbent assay. J Clin Microbiol 36:2481–2484PubMedGoogle Scholar
  54. 54.
    Pang X-L, Honma S, Jakata S, Vesikari T (2000) Human caliciviruses in acute gastroenteritis of young children in the community. J Infect Dis 181[Suppl 2]:S288–S294PubMedCrossRefGoogle Scholar
  55. 55.
    Gaulin C, Frigon M, Poirier D, Fournier C (1999) Transmission of calicivirus by a foodhandler in the presymptomatic phase of illness. Epidemiol Infect 123:475–478PubMedCrossRefGoogle Scholar
  56. 56.
    Becker KM, Southwick KL, et al(2000) Transmission of Norwalk virus during a football game. New Engl J Med 343:1223–1227PubMedCrossRefGoogle Scholar
  57. 57.
    Okhuysen PC, Jiang X, Ye L, et al(1995) Viral shedding and fecal IgA response after Norwalk virus infection. J Infect Dis 171:566–569PubMedCrossRefGoogle Scholar
  58. 58.
    Matsui SM, Greenberg HB (2000) Immunity to calicivirus infection. J Infect Dis 181[Suppl 2]:S331–S335PubMedCrossRefGoogle Scholar
  59. 59.
    Gonin P, Couillard M, d’Halewyn M-A (2000) Genetic diversity and molecular epidemiology of Norwalk-like viruses. J Infect Dis 181[Suppl 2]:S691–S697CrossRefGoogle Scholar
  60. 60.
    Zang XM, Herbst W, Kousoulas KG, Storz J (1994) Biological and genetic characterization of a haemag-glutinating Coronavirus isolated from a diarrhoeic child. J Med Virol 44:152–161CrossRefGoogle Scholar
  61. 61.
    Duckmanton L, Luan B, Devenish J, et al(1997) Characterization of torovirus from human fecal specimens. Virology 239:158–168PubMedCrossRefGoogle Scholar
  62. 62.
    Jamieson FB, Wang EEL, Bain C, et al(1998) Human torovirus: a new nosocomial gastrointestinal pathogen. J Infect Dis 178:1263–1269PubMedCrossRefGoogle Scholar
  63. 63.
    Waters V, Ford-Jones EL, Petric M, et al(2000) Etiology of community-acquired pediatric viral diarrhea. A prospective longitudinal study in hospitals, emergency departments, pediatric practices and child care centers during the winter rotavirus outbreak 1997 to 1998. Pediatr Infect Dis J 19:843–848PubMedCrossRefGoogle Scholar
  64. 64.
    Yolken R, Dubovi E, Leister F, et al(1989) Infantile gastroenteritis associated with excretion of pestvirus antigens. Lancet 1:517–520PubMedCrossRefGoogle Scholar
  65. 65.
    Giangaspero M, Vacira M, Morgan D, et al(1993) Anti-bovine diarrhoea virus antibodies in adult Zambian patients infected with human immunodeficiency virus. Int J STD AIDS 4:300–302PubMedGoogle Scholar
  66. 66.
    Chandra R (1997) Picobirnavirus, a novel group of undescribed viruses of mammals and birds: a mini review. Acta Virol 41:59–62PubMedGoogle Scholar
  67. 67.
    Giordano MO, Martinez LC, Rinaldi D, et al(1998) Detection of picobirnavirus in HIV-infected patients with diarrhea in Argentina. J Acquir Immun Defic Syndr Hum Retrovirol 18:380–383CrossRefGoogle Scholar
  68. 68.
    Giordano MO, Martinez LC, Rinaldi D, et al(1999) Diarrhea and enteric emerging viruses in HIV-infected patients. AIDS Res Hum Retroviruses 15:1427–1432PubMedCrossRefGoogle Scholar
  69. 69.
    Rosen BI, Fang ZY, Glass RI, et al(2000) Cloning of human picobirnavirus genomic segments and development of an RT-PCR detection assay. Virology 277:316–329PubMedCrossRefGoogle Scholar
  70. 70.
    O’Neill HJ, McCaughey C, Wyatt DE, et al(2001) Gastroenteritis outbreaks associated with Norwalk-like viruses and their investigation by nested RT-PCR. BMC Microbiol
  71. 71.
    Berke T, Golding B, Jiang X, et al (1997) Phylogenetic analysis of caliciviruses. J Med Virol 52:419–424PubMedCrossRefGoogle Scholar
  72. 72.
    Jiang X, Huang PW, Zhong WM, et al(1999) Design and evaluation of a primer pair that detects both Norwalk-and Sapporo-like caliciviruses by RT-PCR. J Virol Methods 83:145–154PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 2003

Authors and Affiliations

  • C. Anthony Hart
  • Nigel A. Cunliffe

There are no affiliations available

Personalised recommendations