Bifidobacterium animalis subspecies lactis modulates the local immune response and glucose uptake in the small intestine of juvenile pigs infected with the parasitic nematode Ascaris suum

Authors: Solano-Aguilar, Gloria; SHEA-DONOHUE, TEREZ - University Of Maryland; MADDEN, KATHLEEN - University Of Maryland; QUINONES, ALEJANDRO - University Of California; Beshah, Ethiopia; Lakshman, Sukla; XIE, YUE - Non ARS Employee; Dawson, Harry; Urban, Joseph

Submitted to: Gut Microbes
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/15/2018
Publication Date: 7/19/2018
Citation: Solano Aguilar, G., Shea-Donohue, T., Madden, K., Quinones, A., Beshah, E., Lakshman, S., Xie, Y., Dawson, H.D., Urban Jr, J.F. 2018. Bifidobacterium animalis subspecies lactis modulates the local immune response and glucose uptake in the small intestine of juvenile pigs infected with the parasitic nematode Ascaris suum. Gut Microbes. 19:1-15. https://doi.org/10.1080/19490976.2018.1460014.
DOI: https://doi.org/10.1080/19490976.2018.1460014

Interpretive Summary: The assertion of the health promoting effects of probiotic bacteria in the diet benefits from careful measurement of the probiotic bacteria in the intestine and related changes in host immune and gut function. Bifidobacterium lactis (Bb12) or a placebo containing vehicle was fed to pregnant sows during the last trimester of pregnancy and to their offspring from birth until the end of the study. Weaned piglets were inoculated with infective eggs of a parasitic worm called Ascaris suum. This worm is prevalent in pigs and humans mostly from underdeveloped areas of the world but occasionally found also in the U.S. Sections of intestinal tissue were mounted in specialized chambers to determine changes in permeability and the absorption of nutrients such as glucose. Other tissue were collected to measure changes in gene expression related to specific worm protective responses and levels of inflammation. Blood samples were also collected to detect antibody responses to the worm. The probiotic Bb12 was detected in the highest concentrations in the intestine and proximal colon of pigs fed the probiotic but not placebo fed pigs, and its abundance was not affected by the worm infection. Feeding Bb12 significantly reduced the prototypical secretory response and change in glucose absorption induced by the worm but did not alter the immune protective response to the infection. There were also some protective genes that were expressed at higher levels in the worm-infected pigs fed the probiotic. These results suggest that a human-derived probiotic species can affect local immune responses in pigs and improve intestinal function during a worm infection, and could also reduce some of the negative effects of the inflammatory response to the worm. This information will help scientists and clinicians that study the health benefits of feeding probiotics to humans and animals.

Technical Abstract: The probiotic bacteria Bifidobacterium animalis subspecies lactis (Bb12) or a placebo containing vehicle without Bb12 was administered orally to pregnant sows during the last trimester of pregnancy, and to their offspring from birth through the termination of the study three months later. Weaned-pigs were inoculated with infective Ascaris suum (A. suum) eggs and sections of jejunal mucosa were mounted in Ussing chambers to determine changes in permeability and glucose absorption. Tissue samples from jejunum, liver, mesenteric lymph nodes, and proximal colon were also collected for analysis of host gene expression. Intestinal abundance of Bb12, measured by real-time PCR, was not affected by parasite infection, but influenced the intestinal responses in the small intestine. Treatment with Bb12 did not change mucosal resistance in the jejunum, but significantly attenuated the prototypical parasite-induced secretory response to histamine and reduced absorption of glucose. Parasite antigen specific IgA and IgG2 responses in the serum and IgG1 and IgG2 antibodies in the ileal fluid were significantly increased in A. suum-infected pigs treated with Bb12 compared to infected pigs given the placebo. Ascaris suum-induced eosinophilia in the small intestinal mucosa was inhibited by Bb12 treatment without affecting the normal expulsion of A. suum 4th stage larvae (L4) or the morphometry of the intestine. Expression of genes associated with Th1/Th2, Tregs, mast cells, and physiological function in the intestine were modulated in A. suum infected-pigs treated with Bb12. These results suggested that Bb12, a human-derived probiotic species, can modulate local immune responses and improve intestinal function during a nematode infection that induces a strong allergenic type-2 response in the pig without compromising the normal expulsion of parasite.