Effects of dietary vitamin A content on antibody responses of feedlot calves inoculated intramuscularly with an inactivated bovine coronavirus vaccine

Junbae Jee Food Animal Health Research Program, Department of Veterinary Preventive Medicine, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Junbae Jee in
Current site
Google Scholar
PubMed
Close
 PhD
,
Armando E. Hoet Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210.

Search for other papers by Armando E. Hoet in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Marli P. Azevedo Food Animal Health Research Program, Department of Veterinary Preventive Medicine, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Marli P. Azevedo in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Anastasia N. Vlasova Food Animal Health Research Program, Department of Veterinary Preventive Medicine, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Anastasia N. Vlasova in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Steve C. Loerch Department of Animal Sciences, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Steve C. Loerch in
Current site
Google Scholar
PubMed
Close
 PhD
,
Carrie L. Pickworth Department of Animal Sciences, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Carrie L. Pickworth in
Current site
Google Scholar
PubMed
Close
 PhD
,
Juliette Hanson Food Animal Health Research Program, Department of Veterinary Preventive Medicine, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Juliette Hanson in
Current site
Google Scholar
PubMed
Close
 DVM
, and
Linda J. Saif Food Animal Health Research Program, Department of Veterinary Preventive Medicine, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Search for other papers by Linda J. Saif in
Current site
Google Scholar
PubMed
Close
 PhD

Abstract

Objective—To investigate effects of low dietary vitamin A content on antibody responses in feedlot calves inoculated with an inactivated bovine coronavirus (BCoV) vaccine.

Animals—40 feedlot calves.

Procedures—Calves were fed diets containing high (3,300 U/kg) or low (1,100 U/kg) amounts of vitamin A beginning on the day of arrival at a feedlot (day 0) and continuing daily until the end of the study (day 140). Serum retinol concentrations were evaluated in blood samples obtained throughout the study. Calves were inoculated IM with an inactivated BCoV vaccine on days 112 and 126. Blood samples obtained on days 112 and 140 were used for assessment of BCoV-specific serum IgG1, IgG2, IgM, and IgA titers via an ELISA.

Results—The low vitamin A diet reduced serum retinol concentrations between days 112 and 140. After the BCoV inoculation and booster injections, predominantly serum IgG1 antibodies were induced in calves fed the high vitamin A diet; however, IgG1 titers were compromised at day 140 in calves fed the low vitamin A diet. Other isotype antibodies specific for BCoV were not affected by the low vitamin A diet.

Conclusions and Clinical Relevance—Dietary vitamin A restriction increases marbling in feedlot cattle; however, its effect on antibody responses to vaccines is unknown. A low vitamin A diet compromised the serum IgG1 responses against inactivated BCoV vaccine, which suggested suppressed T-helper 2-associated antibody (IgG1) responses. Thus, low vitamin A diets may compromise the effectiveness of viral vaccines and render calves more susceptible to infectious disease.

Abstract

Objective—To investigate effects of low dietary vitamin A content on antibody responses in feedlot calves inoculated with an inactivated bovine coronavirus (BCoV) vaccine.

Animals—40 feedlot calves.

Procedures—Calves were fed diets containing high (3,300 U/kg) or low (1,100 U/kg) amounts of vitamin A beginning on the day of arrival at a feedlot (day 0) and continuing daily until the end of the study (day 140). Serum retinol concentrations were evaluated in blood samples obtained throughout the study. Calves were inoculated IM with an inactivated BCoV vaccine on days 112 and 126. Blood samples obtained on days 112 and 140 were used for assessment of BCoV-specific serum IgG1, IgG2, IgM, and IgA titers via an ELISA.

Results—The low vitamin A diet reduced serum retinol concentrations between days 112 and 140. After the BCoV inoculation and booster injections, predominantly serum IgG1 antibodies were induced in calves fed the high vitamin A diet; however, IgG1 titers were compromised at day 140 in calves fed the low vitamin A diet. Other isotype antibodies specific for BCoV were not affected by the low vitamin A diet.

Conclusions and Clinical Relevance—Dietary vitamin A restriction increases marbling in feedlot cattle; however, its effect on antibody responses to vaccines is unknown. A low vitamin A diet compromised the serum IgG1 responses against inactivated BCoV vaccine, which suggested suppressed T-helper 2-associated antibody (IgG1) responses. Thus, low vitamin A diets may compromise the effectiveness of viral vaccines and render calves more susceptible to infectious disease.

Contributor Notes

Dr. Azevedo's present address is National Center for Toxicological Research, US FDA, Jefferson, AR 72079.

Supported in part by an Ohio Agricultural Research and Development Center Interdisciplinary Research Grant.

Presented in part as an abstract at the Conference of Research Workers in Animal Diseases Meeting, Chicago, December 2008.

The authors thank Peggy Lewis for technical assistance.

Address correspondence to Dr. Saif (saif.2@osu.edu).
  • 1. Villamor E, Fawzi WW. Effects of vitamin a supplementation on immune responses and correlation with clinical outcomes. Clin Microbiol Rev 2005; 18:446464.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Wang JL, Swartz-Basile DA, Rubin DC, et al. Retinoic acid stimulates early cellular proliferation in the adapting remnant rat small intestine after partial resection. J Nutr 1997; 127:12971303.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Baltes S, Nau H, Lampen A. All-trans retinoic acid enhances differentiation and influences permeability of intestinal Caco-2 cells under serum-free conditions. Dev Growth Differ 2004; 46:503514.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Swartz-Basile DA, Wang L, Tang Y, et al. Vitamin A deficiency inhibits intestinal adaptation by modulating apoptosis, proliferation, and enterocyte migration. Am J Physiol Gastrointest Liver Physiol 2003; 285:G424G432.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Bloem MW, Wedel M, Egger RJ, et al. Mild vitamin A deficiency and risk of respiratory tract diseases and diarrhea in preschool and school children in northeastern Thailand. Am J Epidemiol 1990; 131:332339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Sommer A, Katz J, Tarwotjo I. Increased risk of respiratory disease and diarrhea in children with preexisting mild vitamin A deficiency. Am J Clin Nutr 1984; 40:10901095.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Barclay AJ, Foster A, Sommer A. Vitamin A supplements and mortality related to measles: a randomised clinical trial. Br Med J (Clin Res Ed) 1987; 294:294296.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Coutsoudis A, Broughton M, Coovadia HM. Vitamin A supplementation reduces measles morbidity in young African children: a randomized, placebo-controlled, double-blind trial. Am J Clin Nutr 1991; 54:890895.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Hossain S, Biswas R, Kabir I, et al. Single dose vitamin A treatment in acute shigellosis in Bangladesh children: randomised double blind controlled trial. BMJ 1998; 316:422426.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Neuman MI, Willett WC, Curhan GC. Vitamin and micronutrient intake and the risk of community-acquired pneumonia in US women. Am J Med 2007; 120:330336.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Rahman MM, Mahalanabis D, Alvarez JO, et al. Acute respiratory infections prevent improvement of vitamin A status in young infants supplemented with vitamin A. J Nutr 1996; 126:628633.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Shankar AH, Genton B, Semba RD, et al. Effect of vitamin A supplementation on morbidity due to Plasmodium falciparum in young children in Papua New Guinea: a randomised trial. Lancet 1999; 354:203209.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Nussenblatt V, Semba RD. Micronutrient malnutrition and the pathogenesis of malarial anemia. Acta Trop 2002; 82:321337.

  • 14. Semba RD, Tang AM. Micronutrients and the pathogenesis of human immunodeficiency virus infection. Br J Nutr 1999; 81:181189.

  • 15. Coutsoudis A, Bobat RA, Coovadia HM, et al. The effects of vitamin A supplementation on the morbidity of children born to HIV-infected women. Am J Public Health 1995; 85:10761081.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Semba RD, Muhilal, Ward BJ, et al. Abnormal T-cell subset proportions in vitamin-A-deficient children. Lancet 1993; 341:58.

  • 17. Jiang Y, Obuseh F, Ellis W, et al. Association of vitamin A deficiency with decrease in TNF-alpha expressing CD3-CD56+ NK cells in Ghanaians. Nutr Res 2007; 27:400407.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Rosales FJ, Topping JD, Smith JE, et al. Relation of serum retinol to acute phase proteins and malarial morbidity in Papua New Guinea children. Am J Clin Nutr 2000; 71:15821588.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Jason J, Archibald LK, Nwanyanwu OC, et al. Vitamin A levels and immunity in humans. Clin Diagn Lab Immunol 2002; 9:616621.

  • 20. Gorocica-Buenfil MA, Fluharty FL, Loerch SC. Effect of vitamin A restriction on carcass characteristics and immune status of beef steers. J Anim Sci 2008; 86:16091616.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Siebert BD, Kruk ZA, Davis J, et al. Effect of low vitamin A status on fat deposition and fatty acid desaturation in beef cattle. Lipids 2006; 41:365370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Adachi K, Kawano H, Tsuno K, et al. Relationship between serum biochemical values and marbling scores in Japanese Black steers. J Vet Med Sci 1999; 61:961964.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Hidiroglou M, Markham F. Effect of oral supplements of vitamin A on the plasma retinol levels in calves and their immunological unresponsiveness. Reprod Nutr Dev 1996; 36:467472.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Nonnecke BJ, Horst RL, Waters WR, et al. Modulation of fat-soluble vitamin concentrations and blood mononuclear leukocyte populations in milk replacer-fed calves by dietary vitamin A and beta-carotene. J Dairy Sci 1999; 82:26322641.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Schottstedt T, Muri C, Morel C, et al. Effects of feeding vitamin A and lactoferrin on epithelium of lymphoid tissues of intestine of neonatal calves. J Dairy Sci 2005; 88:10501061.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Higuchi H, Nagahata H. Effects of vitamins A and E on superoxide production and intracellular signaling of neutrophils in Holstein calves. Can J Vet Res 2000; 64:6975.

    • Search Google Scholar
    • Export Citation
  • 27. Rajaraman V, Nonnecke BJ, Franklin ST, et al. Effect of vitamins A and E on nitric oxide production by blood mononuclear leukocytes from neonatal calves fed milk replacer. J Dairy Sci 1998; 81:32783285.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Ross AC. Vitamin A supplementation as therapy—are the benefits disease specific? Am J Clin Nutr 1998; 68:89.

  • 29. McNulty MS, Bryson DG, Allan GM, et al. Coronavirus infection of the bovine respiratory tract. Vet Microbiol 1984; 9:425434.

  • 30. Lin XQ, Oe KL, Storz J, et al. Antibody responses to respiratory coronavirus infections of cattle during shipping fever pathogenesis. Arch Virol 2000; 145:23352349.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Storz J, Purdy CW, Lin X, et al. Isolation of respiratory bovine coronavirus, other cytocidal viruses, and Pasteurella spp from cattle involved in two natural outbreaks of shipping fever. J Am Vet Med Assoc 2000; 216:15991604.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Saif LJ. Bovine respiratory coronavirus. Vet Clin North Am Food Anim Pract 2010; 26:349364.

  • 33. Hasoksuz M, Hoet AE, Loerch SC, et al. Detection of respiratory and enteric shedding of bovine coronaviruses in cattle in an Ohio feedlot. J Vet Diagn Invest 2002; 14:308313.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Heckert RA, Saif LJ, Hoblet KH, et al. A longitudinal study of bovine coronavirus enteric and respiratory infections in dairy calves in two herds in Ohio. Vet Microbiol 1990; 22:187201.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Storz J, Lin X, Purdy CW, et al. Coronavirus and Pasteurella infections in bovine shipping fever pneumonia and Evans' criteria for causation. J Clin Microbiol 2000; 38:32913298.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Thomas CJ, Hoet AE, Sreevatsan S, et al. Transmission of bovine coronavirus and serologic responses in feedlot calves under field conditions. Am J Vet Res 2006; 67:14121420.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Smith DR, Fedorka-Cray PJ, Mohan R, et al. Epidemiologic herd-level assessment of causative agents and risk factors for winter dysentery in dairy cattle. Am J Vet Res 1998; 59:9941001.

    • Search Google Scholar
    • Export Citation
  • 38. Smith DR, Fedorka-Cray PJ, Mohan R, et al. Evaluation of cow-level risk factors for the development of winter dysentery in dairy cattle. Am J Vet Res 1998; 59:986993.

    • Search Google Scholar
    • Export Citation
  • 39. Saif LJ, Brock KV, Redman DR, et al. Winter dysentery in dairy herds: electron microscopic and serological evidence for an association with coronavirus infection. Vet Rec 1991; 128:447449.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Saif LJ, Redman DR, Brock KV, et al. Winter dysentery in adult dairy cattle: detection of coronavirus in the faeces. Vet Rec 1988; 123:300301.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41. Natsuaki S, Goto K, Nakamura K, et al. Fatal winter dysentery with severe anemia in an adult cow. J Vet Med Sci 2007; 69:957960.

  • 42. White ME, Schukken YH, Tanksley B. Space-time clustering of, and risk factors for, farmer-diagnosed winter dysentery in dairy cattle. Can Vet J 1989; 30:948951.

    • Search Google Scholar
    • Export Citation
  • 43. Jactel B, Espinasse J, Viso M, et al. An epidemiological study of winter dysentery in fifteen herds in France. Vet Res Commun 1990; 14:367379.

  • 44. Cho KO, Hoet AE, Loerch SC, et al. Evaluation of concurrent shedding of bovine coronavirus via the respiratory tract and enteric route in feedlot cattle. Am J Vet Res 2001; 62:14361441.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45. Heckert RA, Saif LJ, Myers GW, et al. Epidemiologic factors and isotype-specific antibody responses in serum and mucosal secretions of dairy calves with bovine coronavirus respiratory tract and enteric tract infections. Am J Vet Res 1991; 52:845851.

    • Search Google Scholar
    • Export Citation
  • 46. Pickworth CL, Loerch SC, Fluharty FL. Effects of timing and duration of dietary vitamin A reduction on carcass quality of finishing beef cattle. J Anim Sci 2012; 90:26772691.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47. National Research Council. Nutrient requirements of beef cattle. 7th ed. Washington, DC: National Academies Press, 1996;7576.

  • 48. Gorocica-Buenfil MA, Fluharty FL, Reynolds CK, et al. Effect of dietary vitamin A restriction on marbling and conjugated linoleic acid content in Holstein steers. J Anim Sci 2007; 85:22432255.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49. Hasoksuz M, Vlasova A, Saif LJ. Detection of group 2a coronaviruses with emphasis on bovine and wild ruminant strains. Virus isolation and detection of antibody, antigen, and nucleic acid. Methods Mol Biol 2008; 454:4359.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 50. Frey A, Di Canzio J, Zurakowski D. A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods 1998; 221:3541.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51. Saif LJ, Redman DR, Moorhead PD, et al. Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tracts. Am J Vet Res 1986; 47:14261432.

    • Search Google Scholar
    • Export Citation
  • 52. Saif LJ, Smith KL. Enteric viral infections of calves and passive immunity. J Dairy Sci 1985; 68:206228.

  • 53. Swanson KS, Merchen NR, Erdman JW Jr, et al. Influence of dietary vitamin A content on serum and liver vitamin A concentrations and health in preruminant Holstein calves fed milk replacer. J Dairy Sci 2000; 83:20272036.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 54. Stephensen CB. Vitamin A, infection, and immune function. Annu Rev Nutr 2001; 21:167192.

  • 55. Herdt TH, Stowe HD. Fat-soluble vitamin nutrition for dairy cattle. Vet Clin North Am Food Anim Pract 1991; 7:391415.

  • 56. National Research Council. Nutrient requirements of dairy cattle. 6th ed. Washington, DC: National Academies Press, 1988;4244.

  • 57. Lin X, O'Reilly KL, Burrell ML, et al. Infectivity-neutralizing and hemagglutinin-inhibiting antibody responses to respiratory coronavirus infections of cattle in pathogenesis of shipping fever pneumonia. Clin Diagn Lab Immunol 2001; 8:357362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 58. El-Kanawati ZR, Tsunemitsu H, Smith DR, et al. Infection and cross-protection studies of winter dysentery and calf diarrhea bovine coronavirus strains in colostrum-deprived and gnotobiotic calves. Am J Vet Res 1996; 57:4853.

    • Search Google Scholar
    • Export Citation
  • 59. Saif LJ. Development of nasal, fecal and serum isotype-specific antibodies in calves challenged with bovine coronavirus or rotavirus. Vet Immunol Immunopathol 1987; 17:425439.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 60. Ballow M, Wang W, Xiang S. Modulation of B-cell immunoglobulin synthesis by retinoic acid. Clin Immunol Immunopathol 1996; 80:S73S81.

  • 61. Quadro L, Gamble MV, Vogel S, et al. Retinol and retinol-binding protein: gut integrity and circulating immunoglobulins. J Infect Dis 2000;182(suppl 1):S97S102.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 62. Pasatiempo AM, Kinoshita M, Taylor CE, et al. Antibody production in vitamin A-depleted rats is impaired after immunization with bacterial polysaccharide or protein antigens. FASEB J 1990; 4:25182527.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 63. Antón IM, Sune C, Meloen RH, et al. A transmissible gastroenteritis coronavirus nucleoprotein epitope elicits T helper cells that collaborate in the in vitro antibody synthesis to the three major structural viral proteins. Virology 1995; 212:746751.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 64. Antón IM, Gonzalez S, Bullido MJ, et al. Cooperation between transmissible gastroenteritis coronavirus (TGEV) structural proteins in the in vitro induction of virus-specific antibodies. Virus Res 1996; 46:111124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 65. Cantorna MT, Nashold FE, Hayes CE. Vitamin A deficiency results in a priming environment conducive for Th1 cell development. Eur J Immunol 1995; 25:16731679.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 66. Carman JA, Hayes CE. Abnormal regulation of IFN-gamma secretion in vitamin A deficiency. J Immunol 1991; 147:12471252.

  • 67. Carman JA, Pond L, Nashold F, et al. Immunity to Trichinella spiralis infection in vitamin A-deficient mice. J Exp Med 1992; 175:111120.

  • 68. Ma Y, Chen Q, Ross AC. Retinoic acid and polyriboinosin ic:polyribocytidylic acid stimulate robust anti-tetanus antibody production while differentially regulating type 1/type 2 cytokines and lymphocyte populations. J Immunol 2005; 174:79617969.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 69. Welsh MD, Cunningham RT, Corbett DM, et al. Influence of pathological progression on the balance between cellular and humoral immune responses in bovine tuberculosis. Immunology 2005; 114:101111.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 70. Faldyna M, Oborilova E, Krejci J, et al. A correlation of in vitro tests for the immune response detection: a bovine trichophytosis model. Vaccine 2007; 25:79487954.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 71. Koets AP, Rutten VP, de Boer M, et al. Differential changes in heat shock protein-, lipoarabinomannan-, and purified protein derivative-specific immunoglobulin G1 and G2 isotype responses during bovine Mycobacterium avium subsp. paratuberculosis infection. Infect Immun 2001; 69:14921498.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 72. Brown WC, Davis WC, Dobbelaere DA, et al. CD4+ T-cell clones obtained from cattle chronically infected with Fasciola hepatica and specific for adult worm antigen express both unrestricted and Th2 cytokine profiles. Infect Immun 1994; 62:818827.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 73. Clery D, Torgerson P, Mulcahy G. Immune responses of chronically infected adult cattle to Fasciola hepatica. Vet Parasitol 1996; 62:7182.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 74. Estes DM, Brown WC. Type 1 and type 2 responses in regulation of Ig isotype expression in cattle. Vet Immunol Immunopathol 2002; 90:110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 75. Brown WC, McElwain TF, Palmer GH, et al. Bovine CD4(+)T-lymphocyte clones specific for rhoptry-associated protein 1 of Babesia bigemina stimulate enhanced immunoglobulin G1 (IgG1) and IgG2 synthesis. Infect Immun 1999; 67:155164.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 76. Brown WC, Rice-Ficht AC, Estes DM. Bovine type 1 and type 2 responses. Vet Immunol Immunopathol 1998; 63:4555.

  • 77. Koopmans M, Cremers H, Woode G, et al. Breda virus (Toroviridae) infection and systemic antibody response in sentinel calves. Am J Vet Res 1990; 51:14431448.

    • Search Google Scholar
    • Export Citation
  • 78. Han MG, Cheetham S, Azevedo M, et al. Immune responses to bovine norovirus-like particles with various adjuvants and analysis of protection in gnotobiotic calves. Vaccine 2006; 24:317326.

    • Crossref
    • Search Google Scholar
    • Export Citation

Advertisement