Effect of ovalbumin aerosol exposure on colonization of the porcine upper airway by Pasteurella multocida and effect of colonization on subsequent immune function

Abstract

Seventy-three piglets were weaned at 1 week of age, randomly assigned to 10 groups (A to J), accommodated in stainless steel exposure chambers, and exposed continuously to a controlled environment containing aerosolized ovalbumin. The concentrations of ovalbumin dust were as follows (milligrams per cubic meter): A and F, 16.6; B and G, 8.4; C and H, 4.2; D and I, 2.1; E and J, 0. At weekly intervals, the pigs were bled via venipuncture and anesthetized for nasal lavage and tonsilar biopsies performed for subsequent bacteriologic analysis. At 2 weeks of age, the pigs in groups A to E were challenged with toxigenic Pasteurella multocida (10(8) CFU pig(-1)), and at 6 weeks of age, the pigs were euthanatized. At postmortem, the extent of turbinate atrophy was assessed on the snout sections by using a morphometric index. Exposure to aerial ovalbumin resulted in a dose-dependent increase in serum antiovalbumin immunoglobulin G (IgG; P < 0.001) and serum antiovalbumin IgA (P < 0.001). Exposure also caused a significant increase in the numbers of P. multocida organisms isolated from the upper respiratory tract (P < 0.001) and a corresponding increase in turbinate atrophy, as judged by the morphometric index (P < 0.001). Concurrent challenge with P. multocida and ovalbumin resulted in a significant decrease in both the IgG and IgA responses to ovalbumin (P < 0.001). These results show that ovalbumin exposure increases pig susceptibility to P. multocida colonization and that toxigenic P. multocida modifies the serum IgG and IgA responses to ovalbumin in the pig. Both of these effects may enhance the virulence of this respiratory pathogen and so influence the pathogenesis of atrophic rhinitis in pigs.

FIG. 1

Relationship between the cumulative total number of P. multocida organisms isolated from the tonsil (□; linear regression, y = 0.027x + 1.232 [R² = 0.968]) and nasal cavity (◊; quadratic regression, y = 0.010x² − 1.229x + 37.055 [R² = 0.921]) over the course of the experiment plotted in relation to the MI at the end of the experiment.

FIG. 2

Cumulative total number of P. multocida organisms isolated from the tonsil (□; linear regression, y = 0.024x + 0.393 [R² = 0.645]) and the nasal cavity (◊; quadratic regression, y = 0.010x² − 0.065x + 0.605 [R² = 0.963]) over the course of the experiment plotted in relation to the mean ovalbumin dust concentration in the air.

FIG. 3

Mean IgG responses of pigs to exposure to inhaled ovalbumin dust from 1 to 6 weeks of age, with (open bars, groups A to E) and without (closed bars, groups F to J) challenge with P. multocida. Mean concentrations of ovalbumin in air are shown above the respective exposure groups. Mean IgG responses to ovalbumin exposure were calculated by subtracting the EU value at week 0 from the EU value at week 6. Error bars denote the SD (when not shown, the SD is less than 3).

FIG. 4

Mean IgA responses of pigs to exposure to inhaled ovalbumin dust from 1 to 6 weeks of age, with (open bars, groups A to E) and without (closed bars, groups F to J) challenge with P. multocida. Mean concentrations of ovalbumin in air are shown above the respective exposure groups. Mean IgA responses to ovalbumin exposure were calculated by subtracting the EU value at week 0 from the EU value at week 6. Error bars denote the SD (when not shown, the SD is less than 3).