Modulation by colostrum-acquired maternal antibodies of systemic and mucosal antibody responses to rotavirus in calves experimentally challenged with bovine rotavirus.
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.
Parreño
V
V
Instituto de Virologia, CICV y A, INTA, Castelar, Bs. As., Argentina. vparreno@cicv.inta.gov.ar
Béjar
C
C
Vagnozzi
A
A
Barrandeguy
M
M
Costantini
V
V
Craig
M I
MI
Yuan
L
L
Hodgins
D
D
Saif
L
L
Fernández
F
F
D000818:Animals; D000831:Animals, Newborn; D000914:Antibodies, Viral / Q000097:blood; D002417:Cattle; D002418:Cattle Diseases / Q000276:immunology* / Q000821:virology*; D003126:Colostrum / Q000276:immunology*; D003967:Diarrhea / Q000276:immunology / Q000662:veterinary / Q000821:virology; D004797:Enzyme-Linked Immunosorbent Assay / Q000662:veterinary; D005243:Feces / Q000821:virology; D005767:Gastrointestinal Diseases / Q000276:immunology / Q000662:veterinary* / Q000821:virology; D007112:Immunity, Maternally-Acquired / Q000276:immunology*; D007074:Immunoglobulin G / Q000276:immunology; D007413:Intestinal Mucosa / Q000276:immunology / Q000821:virology; D008297:Male; D009500:Neutralization Tests / Q000662:veterinary; D011897:Random Allocation; D012401:Rotavirus / Q000276:immunology*; D012400:Rotavirus Infections / Q000276:immunology / Q000662:veterinary* / Q000821:virology; D017201:Virus Shedding / Q000276:immunology
D000914:Antibodies, Viral; D007074:Immunoglobulin G