Modulation by colostrum-acquired maternal antibodies of systemic and mucosal antibody responses to rotavirus in calves experimentally challenged with bovine rotavirus

Abstract

The effect of colostral maternal antibodies (Abs), acquired via colostrum, on passive protection and development of systemic and mucosal immune responses against rotavirus was evaluated in neonatal calves. Colostrum-deprived (CD) calves, or calves receiving one dose of pooled control colostrum (CC) or immune colostrum (IC), containing an IgG1 titer to bovine rotavirus (BRV) of 1:16,384 or 1:262,144, respectively, were orally inoculated with 105.5 FFU of IND (P[5]G6) BRV at 2 days of age. Calves were monitored daily for diarrhea, virus shedding and anti-BRV Abs in feces by ELISA. Anti-rotavirus Ab titers in serum were evaluated weekly by isotype-specific ELISA and virus neutralization (VN). At 21 days post-inoculation (dpi), all animals were euthanized and the number of anti-BRV antibody secreting cells (ASC) in intestinal and systemic lymphoid tissues were evaluated by ELISPOT. After colostrum intake, IC calves had significantly higher IgG1 serum titers (GMT=28,526) than CC (GMT=1195) or CD calves (GMT<4). After BRV inoculation, all animals became infected with a mean duration of virus shedding between 6 and 10 days. However, IC calves had significantly fewer days of diarrhea (0.8 days) compared to CD and CC calves (11 and 7 days, respectively). In both groups receiving colostrum there was a delay in the onset of diarrhea and virus shedding associated with IgG1 in feces. In serum and feces, CD and CC calves had peak anti-BRV IgM titers at 7 dpi, but IgA and IgG1 responses were significantly lower in CC calves. Antibody titers detected in serum and feces were associated with circulation of ASC of the same isotype in blood. The IC calves had only an IgM response in feces. At 21 dpi, anti-BRV ASC responses were observed in all analyzed tissues of the three groups, except bone marrow. The intestine was the main site of ASC response against BRV and highest IgA ASC numbers. There was an inverse relationship between passive IgG1 titers and magnitude of ASC responses, with fewer IgG1 ASC in CC calves and significantly lower ASC numbers of all isotypes in IC calves. Thus, passive anti-BRV IgG1 negatively affects active immune responses in a dose-dependent manner. In ileal Peyer's patches, IgM ASC predominated in calves receiving colostrum; IgG1 ASC predominated in CD calves. The presence in IC calves of IgG1 in feces in the absence of an IgG1 ASC response is consistent with the transfer of serum IgG1 back into the gut contributing to the protection of the intestinal mucosa.

High Titers of Circulating Maternal Antibodies Suppress Effector and Memory B-Cell Responses Induced by an Attenuated Rotavirus Priming and Rotavirus-Like Particle-Immunostimulating Complex Boosting Vaccine Regimen

“…Thus, the effect of different levels of MatAbs on different antibody isotypes varies. Similarly, calves fed with colostrum before inoculation with bovine rotavirus showed an inverse relationship between the IgG1 titers in colostrum and the ASC responses (18). These studies, demonstrating the effects of different titers of MatAbs (circulating or local) on infection with virulent rotaviruses, established the basis for our current study to develop rotavirus vaccine regimens that can overcome the suppressive effects of MatAbs.…”

Llama-Derived Single-Chain Antibody Fragments Directed to Rotavirus VP6 Protein Possess Broad Neutralizing Activity In Vitro and Confer Protection against Diarrhea in Mice

“…The tissue culture-adapted BRV C486 (Sb1, P[1]G6) was used for mouse challenge. Fecal samples from newborn colostrum-deprived calves experimentally infected with BRV IND, taken at preinoculation and at the peak of virus shedding, were also included (42).…”

“…The antibody response was monitored by ELISA and VN assay (see below). To evaluate the effector B-cell response, an ELISPOT assay determining the number of RV-specific antibody-secreting cells (ASC) in the peripheral blood of the inoculated llama was adapted from previous ELISPOT assays conducted in pigs and calves (42,58 , and 1.25 ϫ 10 5 cells/well). After centrifugation at 500 ϫ g for 5 min, plates were incubated for 12 to 14 h at 37°C in 5% CO 2 .…”

Multispecies Multistrain Probiotic Effects on Calves Development and Health

“…This is particularly important in cattle because calves are born hypogammaglobulinemic and depend solely on transfer from colostrum for antibodymediated immunoprotection [4,5]. Limited or complete failure of transfer of immunoglobulin can result in an increased incidence of morbidity, which can contribute to a failure to thrive as evidenced by suboptimal or diminished growth [6,7].…”