Skip to main content
PMC home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 1998 Mar 11;16(5):507–516. doi: 10.1016/S0264-410X(97)80004-7

Passive immunity to bovine rotavirus in newborn calves fed colostrum supplements from cows immunized with recombinant SA11 rotavirus core-like particle (CLP) or virus-like particle (VLP) vaccines

FM Fernandez ∗,†, ME Conner ‡,§, DC Hodgins ∗, AV Parwani ∗, PR Nielsen ∗, SE Crawford ‡, MK Estes ‡, LJ Saif ∗,
PMCID: PMC7131086  PMID: 9491505

Abstract

Heterotypic passive immunity to IND (P[5]G6) bovine rotavirus (BRV) was evaluated. Three groups of calves (n = 5 per group) were fed 1% pooled colostrum supplements (birth to 7 days of age) from BRV seropositive cows vaccinated with recombinant SA11(P[2]G3) rotavirus-like particles (VLPs), recombinant SA11 rotavirus core-like particles (CLPs), or inactivated SA11 rotavirus (SA11). Control calves (n = 5 per group) received either pooled colostrum from unvaccinated (BRV field exposure seropositive) control cows, or no colostrum. IgG1 antibody titers to IND BRV for the pooled colostrum were: 1048576 (VLP); 1048576 (CLP); 262144 (SA11); and 16384 (control colostrum). Elevated titers of BRV neutralizing (VN) antibodies were present in VLP colostrum (98 000), and SA11 colostrum (25 000), but not in CLP colostrum (1400), compared to colostrum from nonvaccinates (2081). Calves were orally inoculated with virulent IND BRV at 2 days of age and challenged at post-inoculation day (PID) 21. Calves were monitored daily for diarrhea and faecal BRV shedding through PID 10 and post-challenge day (PCD) 10. After colostrum feeding, the IgG1 antibody titers were highest in serum and faeces of calves fed VLP and CLP colostrum, but VN and IgA antibodies were highest in calves fed VLP colostrum. After BRV inoculation, calves fed colostrum from vaccinated cows had significantly fewer days of BRV-associated diarrhea and BRV shedding than control calves. All calves fed VLP colostrum were protected from diarrhea after BRV inoculation; two calves shed BRV. In the CLP colostrum group, one calf developed BRV-associated diarrhea and all calves shed virus. In the SA11 colostrum group, three calves developed BRV-associated diarrhea and four calves shed virus. BRV-associated diarrhea and shedding occurred in 9 of 10 control calves. Active IgM antibody responses occurred in faeces and/or serum of most calves after BRV inoculation. However, the highest active antibody responses (IgM and IgG1 in serum, and IgM, IgG1 or IgA in faeces) after BRV inoculation were in calves fed control or no colostrum, in association with clinical diarrhea in most of these calves. After challenge at PID 21, BRV-associated diarrhea and shedding were of short duration or absent, in all groups. These results demonstrate the efficacy of colostrum from VLP vaccinated cows to provide heterologous, passive protection against BRV diarrhea and shedding in calves. In comparison, calves fed CLP or SA11 colostrum were only partially protected against BRV diarrhea or shedding.

Keywords: recombinant rotavirus subunit vaccines, core-like particles, virus-like particles, passive immunity in calves, bovine rotavirus

References

  • 1.Bridger J.C., Woode G.N. Neonatal calf diarrhoea: identification of reovirus-like (rotavirus) agent in faeces by immunofluorescence and immune electron microscopy. Br. Vet. J. 1975;131:528–535. [PubMed] [Google Scholar]
  • 2.McNulty M.S. Rotaviruses. J. Gen. Virol. 1978;40:2–18. doi: 10.1099/0022-1317-40-1-1. [DOI] [PubMed] [Google Scholar]
  • 3.Snodgrass D.R., Fahey K.L., Wells P.W., Campbell I., Whitelaw A. Passive immunity in calf rotavirus infections. Maternal vaccination increases and prolongs immunoglobulin G1 antibody secretion in milk. Infect. Immun. 1980;28:344–349. doi: 10.1128/iai.28.2.344-349.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Saif L.J., Redman D.R., Smith K.L., Theil K.W. Passive immunity to bovine rotavirus in newborn calves fed colostrum supplements from immunized or non-immunized cows. Infect. Immun. 1983;41:1118–1131. doi: 10.1128/iai.41.3.1118-1131.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Saif L.J., Smith K.L. Proceedings of the 4th International Symposium on Neonatal Diarrhea. Vet. Infect. Dis. Organ; Saskatchewan, Canada: 1984. Keynote address: A review of rotavirus immunization of cows and passive protection in calves; pp. 394–423. [Google Scholar]
  • 6.Snodgrass D.R., Wells P.W. Passive immunity in rotaviral infections. JAVMA. 1978;173:565–568. [PubMed] [Google Scholar]
  • 7.Saif L.J. Passive immunity to coronavirus and rotavirus infections in swine and cattle: enhancement by maternal vaccination. In: Tzipori S., editor. Proceedings Infectious Diarrhea in the Young. Elsevier; Amsterdam: 1985. pp. 456–467. [Google Scholar]
  • 8.Saif L.J., Jackwood D.J. Enteric virus vaccines: theoretical considerations, current status, and future approaches. In: Saif L.J., Theil K.W., editors. Viral Diarrhea of Man and Animals. CRC Press; Boca Raton, FL: 1990. pp. 313–329. [Google Scholar]
  • 9.DeLeeuw P.W., Ellens D.J., Talmon F.P., Zimmer G.N., Kommerij R. Rotavirus infections in calves: efficacy of oral vaccination in endemically infected herds. Res. Vet. Sci. 1980;29:142–147. doi: 10.1016/S0034-5288(18)32654-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Labbe M., Charpilienne A., Crawford S.E., Estes M.K., Cohen J. Expression of rotavirus VP2 produces empty core-like particles. J. Virol. 1991;65:2946–2952. doi: 10.1128/jvi.65.6.2946-2952.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Crawford S.E., Labbe M., Cohen J., Burroughs M., Zhou Y.J., Estes M. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J. Virol. 1994;68:5945–5952. doi: 10.1128/jvi.68.9.5945-5952.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Conner M.E., Crawford S.E., Barone C., Estes M.K. Rotavirus or virus-like particles administered parenterally induce active immunity. Vaccines 94 Proceedings of Modern Approaches to New Vaccines Including Prevention of AIDS; Cold Spring Harbor 1993; Cold Spring Harbor, NY: Cold Spring Harbor Press; 1994. pp. 351–355. [Google Scholar]
  • 13.Saif L.J., Todhunter D., Smith K.L., Gadfield K., Parwani A., Estes M.K., Crowford S.E., Conner M.E. Antibody responses in cows inoculated with recombinant rotavirus-like particles (VLP) as a subunit vaccine [abstract W4–7]. Proceedings and abstracts of the 13th Annual Meeting of the American Society for Virology; Madison, Wisconsin; 1994. p. 113. [Google Scholar]
  • 14.Fernandez F.M., Conner M.E., Parwani A.V. Isotype-specific antibody responses to rotavirus and virus proteins in cows inoculated with subunit vaccines comprised of recombinant SA11 rotavirus core-like particles (CLP) or virus-like particles (VLP) Vaccine. 1996;14:1303–1312. doi: 10.1016/S0264-410X(96)00065-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Saif L.J., Bohl E.H., Kohler E.M., Hughes J.H. Immune electron microscopy of TGE and rotavirus in swine. Am. J. Vet. Res. 1977;38:13–20. [PubMed] [Google Scholar]
  • 16.Lucchelli A., Lance S.E., Bartlett P.B., Miller G.Y., Saif L.J. Prevalence of bovine group A rotavirus shedding among dairy calves in Ohio. Am. J. Vet. Res. 1992;53:169–174. [PubMed] [Google Scholar]
  • 17.Saif L.J., Smith K.L., Landmeier B.J., Bohl E.H., Theil K.W. Immune response of pregnant cows to bovine rotavirus immunization. Am. J. Vet. Res. 1984;45:49–58. [PubMed] [Google Scholar]
  • 18.Castrucci G., Frigeri F., Ferrari M., Aldrovandi V., Tassini F., Gatti R. The protection of newborn calves against experimental rotavirus infection by feeding mammary secretions from vaccinated cows. Microbiologica. 1988;11:379–385. [PubMed] [Google Scholar]
  • 19.Tsunemitsu H., Shimizu M., Hirai T. Protection against bovine rotaviruses in newborn calves by continuous feeding of immune colostrum. J. Vet. Sci. 1989;2:300–308. doi: 10.1292/jvms1939.51.300. [DOI] [PubMed] [Google Scholar]
  • 20.Conner M.E., Crawford S.E., Barone C. Rotavirus subunit vaccines. Arch. Virol. 1996;S12:199–206. doi: 10.1007/978-3-7091-6553-9_21. [DOI] [PubMed] [Google Scholar]
  • 21.Estes M.K., Crawford S.E., Penaranda M.E. Synthesis and immunogenicity of the rotavirus major capsid antigen using a baculovirus expression system. J. Virol. 1987;61:1488–1494. doi: 10.1128/jvi.61.5.1488-1494.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Redmond M.J., Ijaz M.K., Parker M.D. Assembly of recombinant rotavirus proteins into virus-like particles and assessment of vaccine potential. Vaccine. 1993;11:273–281. doi: 10.1016/0264-410x(93)90029-w. [DOI] [PubMed] [Google Scholar]
  • 23.Ijaz M.K., Attah-poku S.K., Redmond M.J., Parker M.D., Sabara M.I., Babiuk L.A. Heterotypic passive protection induced by synthetic peptides corresponding to VP7 and VP4 of bovine rotavirus. J. Virol. 1991;65:3106–3113. doi: 10.1128/jvi.65.6.3106-3113.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Sheridan J.F., Smith C.C., Manak M.M., Aurelian L.J. Prevention of rotavirus-induced diarrhea in neonatal mice to dams immunized with empty capsids of simian rotavirus SA11. Infect. Dis. 1984;149:434–438. doi: 10.1093/infdis/149.3.434. [DOI] [PubMed] [Google Scholar]
  • 25.Brussow H., Bruttin A., Marc-Martin S. Polypeptide composition of rotavirus empty capsids and their possible use as a subunit vaccine. J. Virol. 1990;64:3635–3642. doi: 10.1128/jvi.64.8.3635-3642.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Besser T.E., Gay C.C., McGuire T.C., Evermann J.F. Passive immunity to bovine rotavirus infection associated with transfer of serum antibody into the intestinal lumen. J. Virol. 1988;62:2238–2242. doi: 10.1128/jvi.62.7.2238-2242.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Feng N., Burns J.W., Bracy L., Greenberg H.B. Comparison of monoclonal and systemic humoral immune responses and subsequent protection in mice orally inoculated with a homologous or a heterologous rotavirus. J. Virol. 1994;68:7766–7773. doi: 10.1128/jvi.68.12.7766-7773.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Yuan L., Ward L.A., To T.L., Saif L.J. Systemic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J. Virol. 1996;70:3075–3083. doi: 10.1128/jvi.70.5.3075-3083.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Saif L.J., Ward L.A., Rosen B.I., To T.L. The gnotobiotic piglet as a model for studies of disease pathogenesis and immunity to human rotaviruses. Arch. Virol. 1996;S12:153–161. doi: 10.1007/978-3-7091-6553-9_17. [DOI] [PubMed] [Google Scholar]
  • 30.Burns J.W., Siadat-Pajouh M., Krishnaney A.A., Greenberg H.B. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science. 1996;272:104–107. doi: 10.1126/science.272.5258.104. [DOI] [PubMed] [Google Scholar]
  • 31.Hammer D.K., Kickhofen B., Malchow H. Preferential adsorption of a single bovine IgG type by isolated epithelial cells of the mammary gland. In: Peeters H., editor. 16th Colloquium on Protides of the Biological Fluids. Pergamon Press; London: 1969. p. 663. [Google Scholar]
  • 32.Husband A.J., Brandon M.R., Lascelles A.K. Absorption and endogenous production of immunoglobulins in calves. Aust. J. Exp. Biol. Med. Sci. 1972;50:491–498. doi: 10.1038/icb.1972.41. [DOI] [PubMed] [Google Scholar]
  • 33.Saif L.J. Development of nasal, faecal and serum isotype-specific antibodies in calves challenged with bovine corona-virus or rotavirus. Vet. Immunol. Immunopath. 1987;17:425–437. doi: 10.1016/0165-2427(87)90159-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Vaccine are provided here courtesy of Elsevier

RESOURCES