Chapter 28 : Viral Pathogens of the Intestine

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Viral Pathogens of the Intestine, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817848/9781555812614_Chap28-1.gif /docserver/preview/fulltext/10.1128/9781555817848/9781555812614_Chap28-2.gif


Rotaviruses and caliciviruses are currently recognized as the etiologic agents of greatest medical and epidemiologic importance for humans, and this chapter summarizes current information on the epidemiology and consequences of infection with these viruses. Much of the chapter focuses on information about the pathophysiology of rotavirus-induced disease because this disease is the best understood at present. Pathologic changes induced by rotavirus infections are almost exclusively limited to enterocytes in the small intestine. In pigs and lambs, the most pronounced lesions are seen in the distal intestine (jejunum, ileum), while the proximal intestine (duodenum, jejunum) is infected in calves, with changes being seen throughout the length of the small intestine. In mice, the most pronounced changes are in the proximal to middle small intestine, and lesions in rabbits are seen throughout the small intestine. A number of studies have shown that rotavirus infection can lead to malabsorption due to destruction of enterocytes. This mechanism is based on the observation that histopathologic changes are seen in the intestines of rotavirus-infected animals and loss of enterocytes is associated with depressed levels of mucosal disaccharidases. The site of primary replication is assumed to be in the upper small intestine, because biopsies of the jejunum of volunteers who developed illness following oral administration of the Norwalk or Hawaii virus exhibit histopathologic lesions.

Citation: Estes M, Atmar R. 2003. Viral Pathogens of the Intestine, p 525-545. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch28
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Schematic of the small intestinal epithelium and sites of virus infection. The left panel shows the locations of cells infected by specific GI viruses. The right panel shows the release of the viral enterotoxin from infected cells that can affect neighboring uninfected epithelial cells, and outlines the effects of rotavirus infection of mature enterocytes.

Citation: Estes M, Atmar R. 2003. Viral Pathogens of the Intestine, p 525-545. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch28
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Norwalk virus genome organization. The top line illustrates this nonenveloped virus's singlestranded RNA genome of ∼7.7 kb. The lower boxes depict the three predicted ORFs encoded in the genome. ORF1 produces the nonstructural proteins, ORF2 is the major capsid protein, and ORF3 is a basic protein present as a few copies in virus particles. Expression of the 3′end of the genome using recombinant baculoviruses results in the self-assembly of VLPs.

Citation: Estes M, Atmar R. 2003. Viral Pathogens of the Intestine, p 525-545. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch28
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Agus, S. G.,, R. Dolin,, R. G. Wyatt,, A. J. Tousimis,, and R. S. Northrup. 1973. Acute infectious nonbacterial gastroenteritis: intestinal histopathology. Histologic and enzymatic alterations during illness produced by the Norwalk agent in man. Ann. Intern. Med. 79: 18 25.
2. Atmar, R. L.,, and M. K. Estes. 2001. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 14: 15 37.
3. Ball, J. M.,, P. Tian,, C. Q. Zeng,, A. P. Morris,, and M. K. Estes. 1996. Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 272: 101 104.
4. Blutt, S. E.,, K. L. Warfield,, D. E. Lewis,, and M. E. Conner, 2002. Early response to rotavirus infection involves massive B cell activation. J. Immunol. 168: 5716 5721.
5. Brunet, J. P.,, J. Cotte-Laffitte,, C. Linxe,, A. M. Quero,, M. Geniteau-Legendre,, and A. Servin. 2000. Rotavirus infection induces an increase in intracellular calcium concentration in human intestinal epithelial cells: role in microvillar actin alteration. J. Virol. 74: 2323 2332.
6. Chadwick, D.,, and J. A. Goode. 2001. Novartis Foundation Symposium 238: Gastroenteritis Viruses. John Wiley & Sons, Ltd., West Sussex, United Kingdom.
7. Ciarlet, M.,, M. E. Conner,, M. J. Finegold,, and M. K. Estes. 2002. Group A rotavirus infection and age-dependent diarrheal disease in rats: a new animal model to study the pathophysiology of rotavirus infection. J. Virol. 76: 41 57.
8. Ciarlet, M.,, S. E. Crawford,, C. Barone,, A. Bertolotti-Ciarlet,, M. K. Estes,, and M. E. Conner. 1998. Subunit rotavirus vaccine administered parenterally to rabbits induces protective immunity. J. Virol. 72: 9233 9246.
9. Ciarlet, M.,, S. E. Crawford,, and M. K. Estes. 2001. Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acid-independent rotavirus strains. J. Virol. 75: 11834 11850.
10. Ciarlet, M.,, and M. K. Estes. 2001. Rotavirus and calicivirus infections of the gastrointestinal tract. Curr. Opin. Gastroenterol. 17: 10 16.
11. Conner, M. E.,, and R. F. Ramig,. 1997. Viral enteric diseases, p. 713 743. In N. Nathanson,, R. Ahmed,, F. Gonzalez-Scarano,, D. E. Griffin,, K. V. Holmes,, F. A. Murphy,, and H. L. Robinson (ed.), Viral Pathogenesis. Lippincott-Raven Publishers, Philadelphia, Pa.
12. Coste, A.,, J. C. Sirard,, K. Johansen,, J. Cohen,, and J. P. Kraehenbuhl. 2000. Nasal immunization of mice with virus-like particles protects offspring against rotavirus diarrhea. J. Virol. 74: 8966 8971.
13. Crawford, S. E.,, M. K. Estes,, M. Ciarlet,, C. Barone,, C. M. O’Neal,, J. Cohen,, and M. E. Conner. 1999. Heterotypic protection and induction of a broad heterotypic neutralization response by rotavirus-like particles. J. Virol. 73: 4813 4822.
15. Crawford, S. E.,, A. K. Mukherjee,, M. K. Estes,, J. A. Lawton,, A. L. Shaw,, R. F. Ramig,, and B. V. Prasad. 2001. Trypsin cleavage stabilizes the rotavirus VP4 spike. J. Virol. 75: 6052 6061.
15. Cuadras, M. A.,, D. A. Feigelstock,, S. An,, and H. B. Greenberg. 2002. Gene expression pattern in Caco-2 cells following rotavirus infection. J. Virol. 76: 4467 4482.
16. Cunliffe, N. A.,, J. S. Gondwe,, C. D. Kirkwood,, S. M. Graham,, N. M. Nhlane,, B. D. Thindwa,, W. Dove,, R. L. Broadhead,, M. E. Molyneaux,, and C. A. Hart. 2001. Effect of concomitant HIV infection on presentation and outcome of rotavirus gastroenteritis in Malawian children. Lancet 358: 550 555.
17. Dastjerdi, A. M.,, J. Green,, C. I. Gallimore,, D. W. Brown,, and J. C. Bridger. 1999. The bovine Newbury agent-2 is genetically more closely related to human SRSVs than to animal caliciviruses. Virology 254: 1 5.
18. Desselberger, U.,, and J. J. Gray. 2002. Perspectives in Medical Virology: Viral Gastroenteritis. Elsevier Science, Amsterdam, The Netherlands.
19. Dong, Y.,, C. Q. Zeng,, J. M. Ball,, M. K. Estes,, and A. P. Morris. 1997. The rotavirus enterotoxin NSP4 mobilizes intracellular calcium in human intestinal cells by stimulating phospholipase C-mediated inositol 1,4,5-trisphosphate production. Proc. Natl. Acad. Sci. USA 94: 3960 3965.
20. Dormitzer, P. R.,, H. B. Greenberg,, and S. C. Harrison. 2001. Proteolysis of monomeric recombinant rotavirus VP4 yields an oligomeric VP5 core. J. Virol. 75: 7739 7750.
21. Dormitzer, P. R.,, Z. Y. Sun,, G. Wagner,, and S. C. Harrison. 2002. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 21: 885 897.
22. Estes, M. K.,, J. M. Ball,, R. A. Guerrero,, A. R. Opekun,, M. A. Gilger,, S. S. Pacheco,, and D. Y. Graham. 2000. Norwalk virus vaccines: challenges and progress. J. Infect. Dis. 181: S367 S373.
23. Estes, M. K.,, and A. P. Morris. 1999. A viral enterotoxin. A new mechanism of virus-induced pathogenesis. Adv. Exp. Med. Biol. 473: 73 82.
24. Fankhauser, R. L.,, J. S. Noel,, S. S. Monroe,, T. Ando,, and R. I. Glass. 1998. Molecular epidemiology of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States. J. Infect. Dis. 178: 1571 1578.
25. Franco, M. A.,, and H. B. Greenberg. 1997. Immunity to rotavirus in T cell deficient mice. Virology 238: 169 179.
26. Glass, R. I.,, P. E. Kilgore,, R. C. Holman,, S. Jin,, J. C. Smith,, P. A. Woods,, M. J. Clarke,, M. S. Ho,, and J. R. Gentsch. 1996. The epidemiology of rotavirus diarrhea in the United States: surveillance and estimates of disease burden. J. Infect. Dis. 174(Suppl. 1): S5 S11.
26a.Graff, J. W.,, D. N. Mitzel,, C. M. Weisend,, M. L. Flenniken,, and M. E. Hardy. 2002. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J. Virol. 76: 9545 9550.
27. Graham, D. Y.,, X. Jiang,, H. Tanaka,, A. R. Opekun,, H. P. Madore,, and M. K. Estes. 1994. Norwalk virus infection of volunteers: new insights based on improved assays. J. Infect. Dis. 170: 34 43.
28. Green, K. Y.,, G. Belliot,, J. L. Taylor,, J. Valdesuso,, J. F. Lew,, A. Kapikian,, and F. Y. Lin. 2002. A predominant role for Norwalk-like viruses as agents of epidemic gastroenteritis in Maryland nursing homes for the elderly. J. Infect. Dis. 185: 133 146.
29. Green, K. Y.,, R. M. Chanock,, and A. Z. Kapikian,. 2001. Human caliciviruses, p. 841 874. In D. M. Knipe, and P. M. Howley (ed.), Fields Virology. Lippincott Williams & Wilkins, Philadelphia, Pa.
30. Greenberg, H. B.,, H. F. Clark,, and P. A. Offit. 1994. Rotavirus pathology and pathophysiology. Curr. Top. Microbiol. Immunol. 185: 255 283.
31. Guarino, A.,, R. Berni Canani,, and S. Russo. 1994. Oral immunoglobulins for treatment of acute rotaviral gastroenteritis. Pediatrics 93: 12 16.
32. Guo, M.,, K. O. Chang,, M. E. Hardy,, Q. Zhang,, A. V. Parwani,, and L. J. Saif. 1999. Molecular characterization of a porcine calicivirus genetically related to Sapporo-like human viruses. J. Virol. 73: 9625 9631.
33. Guo, M.,, J. Hayes,, K. O. Cho,, A. V. Parwani,, L. M. Lucas,, and L. J. Saif. 2001. Comparative pathogenesis of tissue culture-adapted and wild-type Cowden porcine enteric calicivirus (PEC) in gnotobiotic pigs and induction of diarrhea by intravenous inoculaton of wild-type PEC. J. Virol. 75: 9239 9251.
34. Halaihel, N.,, V. Lievin,, J. M. Ball,, M. K. Estes,, F. Alvarado,, and M. Vasseur. 2000. Direct inhibitory effect of rotavirus NSP4 (114-135) peptide on the Na_-D-glucose symporter of rabbit intestinal brush border membrane. J. Virol. 74: 9464 9470.
35. Horie, Y.,, O. Nakagomi,, Y. Koshimura,, T. Nakagomi,, Y. Suzuki,, T. Oka,, S. Sasaki,, Y. Matsuda,, and S. Watanabe. 1999. Diarrhea induction by rotavirus NSP4 in the homologous mouse model system. Virology 262: 398 407.
36. Hughes, R. C. 1999. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473: 172 185.
37. Hutson, A. M.,, R. L. Atmar,, D. Y. Graham,, and M. K. Estes. 2002. Norwalk virus infection and disease is associated with ABO histo-blood group type. J. Infect. Dis. 185: 1335 1337.
37a.Hutson, A. M.,, R. L. Atmar,, D. M. Marcus,, and M. K. Estes. 2003. Norwalk virus-like particle hemagglutination by binding to H histoblood group antigens. J. Virol. 77: 405 415.
38. Jiang, B.,, C. Barone,, V. Barniak,, C. M. O’Neal,, A. Ottaiano,, H. P. Madore,, M. K. Estes,, and M. E. Conner. 1999. Heterotypic protection against rotavirus infection in mice vaccinated with virus-like particles. Vaccine 17: 1005 1013.
39.Jiang, X, D. Y. Graham, K. Wang, and M. K. Estes. 1990. Norwalk virus genome: cloning and characterization. Science 250: 15801583.
40. Jiang, X.,, M. Wang,, D. Y. Graham,, and M. K. Estes. 1992. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 66: 6527 6532.
41. Jourdan, N.,, J. P. Brunet,, C. Sapin,, A. Blais,, J. Cotte-Laffitte,, F. Forestier,, A. M. Quero,, G. Trugnan,, and A. L. Servin. 1998. Rotavirus infection reduces sucrase-isomaltase expression in human intestinal epithelial cells by perturbing protein targeting and organization of microvillar cytoskeleton. J. Virol. 72: 7228 7236.
42. Jourdan, N.,, M. Maurice,, D. Delautier,, A. M. Quero,, A. L. Servin,, and G. Trugnan. 1997. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 71: 8268 8278.
43. LaMonica, R.,, S. S. Kocer,, J. Nazarova,, W. Dowling,, E. Geimonen,, R. D. Shaw,, and E. R. Mackow. 2001. VP4 differentially regulates TRAF2 signaling, disengaging JNK activation while directing NF-kappa B to effect rotavirus specific cellular receptors. J. Biol. Chem. 276: 19889 19896.
44. Liu, B. L.,, P. R. Lambden,, H. Gunther,, P. Otto,, M. Elschner,, and I. N. Clarke. 1999. Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J. Virol. 73: 818 825.
45. Lundgren, O.,, A. T. Peregrin,, K. Persson,, S. Kordasti,, I. Uhnoo,, and L. Svensson. 2000. Role of the enteric nervous system in the fluid and electrolyte secretion of rotavirus diarrhea. Science 287: 491 495.
46. Madore, H. P.,, D. Zarley,, B. Hu,, S. Parsons,, B. Jiang,, B. Corsaro,, S. E. Crawford,, M. E. Conner,, and M. K. Estes. 1999. Biochemical and immunologic comparison of viruslike particles for a rotavirus subunit vaccine. Vaccine 17: 2461 2471.
47. Meeroff, J. C.,, D. S. Schreiber,, J. S. Trier,, and N. R. Blacklow. 1980. Abnormal gastric motor function in viral gastroenteritis. Ann. Intern. Med. 92: 370 373.
48. Mori, Y.,, M. A. Borgan,, N. Ito,, M. Sugiyama,, and N. Minamoto. 2002. Diarrheainducing activity of avian rotavirus NSP4 glycoproteins, which differ greatly from mammalian rotavirus NSP4 glycoproteins in deduced amino acid sequence, in suckling mice. J. Virol. 76: 5829 5834.
49. Morris, A. P.,, and M. K. Estes. 2001. M icrobes and microbial toxins: paradigms for microbial-mucosal interactions. VIII. Pathological consequences of rotavirus infection and its enterotoxin. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G303 G310.
50. Morris, A. P.,, J. K. Scott,, J. M. Ball,, C. Q. Zeng,, W. K. O’Neal,, and M. K. Estes. 1999. NSP4 elicits age-dependent diarrhea and Ca(2+) mediated I(-) influx into intestinal crypts of CF mice. Am. J. Physiol. 277: G431 G444.
51. Murphy, T. V.,, P. M. Gargiullo,, M. S. Massoudi,, D. B. Nelson,, A. O. Jumaan,, C. A. Okoro,, L. R. Zanardi,, S. Setia,, E. Fair,, C. W. LeBaron,, M. Wharton,, and J. R. Livingood. 2001. Intussusception among infants given an oral rotavirus vaccine. N. Engl. J. Med. 344: 564 572.
52. Noel, J. S.,, R. L. Fankhauser,, T. Ando,, S. S. Monroe,, and R. I. Glass. 1999. Identification of a distinct common strain of ‘‘Norwalk-like viruses’’ having a global distribution. J. Infect. Dis. 179: 1334 1344.
53. O’Neal, C. M.,, J. D. Clements,, M. K. Estes,, and M. E. Conner. 1998. Rotavirus 2/6 viruslike particles administered intranasally with cholera toxin, Escherichia coli heat-labile toxin (LT), and LT-R192G induce protection from rotavirus challenge. J. Virol. 72: 3390 3393.
54. O’Neal, C. M.,, S. E. Crawford,, M. K. Estes,, and M. E. Conner. 1997. Rotavirus virusparticles administered mucosally induce protective immunity. J. Virol. 71: 8707 8717.
55. Obert, G.,, I. Peiffer,, and A. L. Servin. 2000. Rotavirus-induced structural and functional alterations in tight junctions of polarized intestinal Caco-2 cell monolayers J. Virol. 74: 4645 4651.
56. Okhuysen, P. C.,, X. Jiang,, L. Ye,, P. C. Johnson,, and M. K. Estes. 1995. Viral shedding and fecal IgA response after Norwalk virus infection. J. Infect. Dis. 171: 566 569.
57. Osborne, M. P.,, S. J. Haddon,, A. J. Spencer,, J. Collins,, W. G. Starkey,, T. S. Wallis,, G. J. Clarke,, K. J. Worton,, D. C. Candy,, and J. Stephen. 1988. An electron microscopic investigation of time-related changes in the intestine of neonatal mice infected with murine rotavirus. J. Pediatr. Gastroenterol. Nutr. 7: 236 248.
58. Pacyna, J.,, K. Siwek,, S. J. Terry,, E. S. Roberton,, R. B. Johnson,, and G. P. Davidson. 2001. Survival of rotavirus antibody activity derived from bovine colostrum after passage through the human gastrointestinal tract. J. Pediatr. Gastroenterol. Nutr. 32: 162 167.
59. Pang, X. L.,, S. Q. Zeng,, S. Honma,, S. Nakata,, and T. Vesikari. 2001. Effect of rotavirus vaccine on Sapporo virus gastroenteritis in Finnish infants. Pediatr. Infec. Dis. J. 20: 295 300.
60. Parashar, U. D.,, and S. S. Monroe. 2001. "Norwalk-like viruses" as a cause of foodborne disease outbreaks. Rev. Med. Virol. 11: 243 252.
61. Parrino, T. A.,, D. S. Schreiber,, J. S. Trier,, A. Z. Kapikian,, and N. R. Blacklow. 1977. Clinical immunity in acute gastroenteritis caused by Norwalk agent. N. Engl. J. Med. 297: 86 89.
62. Parwani, A. V.,, W. T. Flynn,, K. L. Gadfield,, and L. J. Saif. 1991. Serial propagation of porcine enteric calicivirus in a continuous cell line. Effect of medium supplementation with intestinal contents or enzymes. Arch. Virol. 120: 115 122.
63. Ponka, A.,, L. Maunula,, C. H. Von Bonsdorf,, and O. Lyytikainen. 1999. An outbreak of calicivirus associated with consumption of frozen raspberries. Epidemiol. Infect. 123: 469 474.
64. Prasad, B. V.,, M. E. Hardy,, T. Dokland,, J. Bella,, M. G. Rossmann,, and M. K. Estes. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286: 287 290.
65. Raza, S.,, S. M. Graham,, S. J. Allen,, S. Sultana,, L. Cuevas,, C. A. Hart,, M. Kaila,, E. Isolauri,, and M. A. H. Saxelin. 1995. Lactobacillus GG in acute diarrhea. Indian J. Pediatr. 32: 1140 1142.
66. Rennels, M. B. 2000. The rotavirus vaccine story: a clinical investigator’s view. Pediatrics 106: 123 125.
67. Rockx, B.,, M. de Wit,, H. Vennema,, J. Vinje,, E. de Bruin,, Y. van Duynhoven,, and M. Koopmans. 2002. Natural history of human calicivirus infection: a prospective cohort study. Clin. Infect. Dis. 35: 246 253.
68. Ruiz, M. C.,, J. Cohen,, and F. Michelangeli. 2000. Role of Ca2_ in the replication and pathogenesis of rotavirus and other viral infections. Cell Calcium 28: 137 149.
69. Ruveon-Clouet, N.,, D. Blanchard,, G. Andre-Fontaine,, and J. P. Ganiere. 1995. Partial characterization of the human erythrocyte receptor for rabbit haemorrhagic disease virus. Res. Virol. 146: 33 41.
70. Salazar-Lindo, E.,, J. Santisteban-Ponce,, E. Chea-Woo,, and M. Gutierrez. 2000. Racecadotril in the treatment of acute watery diarrhea in children. N. Engl. J. Med. 343: 463 467.
71. Sapin, C.,, O. Colard,, O. Delmas,, C. Tessier,, M. Breton,, V. Enouf,, S. Chwetzoff,, J. Ouanich,, J. Cohen,, C. Wolf,, and G. Trugnan. 2002. Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J. Virol. 76: 4591 4602.
72. Sugieda, M.,, H. Nagaoka,, Y. Kakishima,, T. Ohshita,, S. Nakamuira,, and S. Nakajama. 1998. Detection of Norwalk-like virus genes in the caecum contents of pigs. Arch. Virol. 143: 1215 1221.
73. Tafazoli, F.,, C. Q.-Y. Zeng,, M. K. Estes,, K. E. Magnusson,, and L. Svensson. 2001. The NSP4 enterotoxin of rotavirus induces paracellular leakage in polarized epithelial cells. J. Virol. 75: 1540 1546.
74. Tamura, M.,, K. Natori,, M. Kobayashi,, T. Miyamura,, and N. Takeda. 2000. Interaction of recombinant Norwalk virus particles with the 105-kilodalton cellular binding protein, a candidate receptor molecule for virus attachment. J. Virol. 74: 11589 11597.
75. Vinje, J.,, S. A. Altena,, and M. P. Koopmans. 1997. The incidence and genetic variability of small round-structured viruses in outbreaks of gastroenteritis in The Netherlands. J. Infect. Dis. 176: 1374 1378.
76. White, L.,, J. M. Ball,, M. E. Hardy,, T. N. Tanaka,, N. Kitamoto,, and M. K. Estes. 1996. Attachment and entry of recombinant Norwalk virus capsids to cultured human and animal cell lines. J. Virol. 70: 6589 6597.
77.World Health Organization. 1999. Rotavirus vaccines. Wkly. Epidemiol. Rec. 74: 3338.
78. Xu, A.,, A. R. Bellamy,, and J. A. Taylor. 2000. Immobilization of the early secretory pathway by a virus glycoprotein that binds to microtubules. EMBO J. 19: 6465 6474.
79. Youngman, K. R.,, M. A. Franco,, N. Kuklin,, L. S. Rott,, E. C. Butcher,, and H. B. Greenberg. 2002. Correlation of tissue distribution, developmental phenotype, and intestinal homing receptor expression of antigen-specific B cells during the murine anti-rotavirus immune response. J. Immunol. 68: 2173 2181.
80. Yu, J.,, and W. H. Langridge. 2001. A plantbased multicomponent vaccine protects mice from enteric diseases. Nat. Biotechnol. 19: 548 552.
81. Yuan, L.,, A. Geyer,, D. C. Hodgins,, Z. Fan,, Y. Qian,, K. O. Chang,, S. E. Crawford,, V. Parreno,, L. A. Ward,, M. K. Estes,, M. E. Conner,, and L. J. Saif. 2000. Intranasal administration of 2/6-rotavirus-like particles with mutant Escherichia coli heat-labile toxin (LT-R192G) induces antibody-secreting cell responses but not protective immunity in gnotobiotic pigs. J. Virol. 74: 8843 8853.
82. Zarate, S.,, R. Espinosa,, P. Romero,, E. Mendez,, C. F. Arias,, and S. Lopez. 2000. The VP5 domain of VP4 can mediate attachment of rotaviruses to cells. J. Virol. 74: 593 599.
83. Zhang, M.,, C. Q.-Y. Zeng,, A. P. Morris,, and M. K. Estes. 2000. A functional NSP4 enterotoxin peptide secreted from rotavirus-infected cells. J. Virol. 74: 11663 11670.
84. Zijlstra, R. T.,, S. M. Donovan,, J. Odle,, H. B. Gelberg,, B. W. Petschow,, and H. R. Gaskins. 1997. Protein-energy malnutrition delays small-intestinal recovery in neonatal pigs infected with rotavirus. J. Nutr. 127: 1118 1127.


Generic image for table

Viral gastroenteritis in humans

Citation: Estes M, Atmar R. 2003. Viral Pathogens of the Intestine, p 525-545. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch28

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error