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Title: Stage of gestation at porcine epidemic diarrhea virus infection of pregnant swine impacts maternal immunity and lactogenic immune protection of neonatal suckling piglets

Author
item LANGEL, STEPHANIE - THE OHIO STATE UNIVERSITY
item PAIM, FRANCINE - THE OHIO STATE UNIVERSITY
item ALHAMO, MOYASAR - THE OHIO STATE UNIVERSITY
item BUCKLEY, ALEXANDRA - ORISE FELLOW
item VAN GEELEN, ALBERT - ORISE FELLOW
item LAGER, KELLY
item VLASOVA, ANASTASIA N - THE OHIO STATE UNIVERSITY
item SAIF, LINDA - THE OHIO STATE UNIVERSITY

Submitted to: Frontiers in Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2019
Publication Date: 4/24/2019
Citation: Langel, S.N., Paim, F.C., Alhamo, M.A., Buckley, A., van Geelen, A., Lager, K.M., Vlasova, A.N., Saif, L.J. 2019. Stage of gestation at porcine epidemic diarrhea virus infection of pregnant swine impacts maternal immunity and lactogenic immune protection of neonatal suckling piglets. Frontiers in Immunology. 10:727. https://doi.org/10.3389/fimmu.2019.00727.
DOI: https://doi.org/10.3389/fimmu.2019.00727

Interpretive Summary: Infectious diseases in swine can cause dramatic economic loss for pork producers. Their control is based on preventing the pig from becoming infected, and if infected, reduction in clinical disease. The use of vaccines may prevent infection and reduce disease in swine, and when available for specific diseases, vaccination is a common practice. One swine disease, porcine epidemic diarrhea, causes severe diarrhea in piglets and the only prevention strategy is to vaccinate the sow prior to farrowing which will allow time to mount a protective immune response that is passed to her baby pigs through colostrum, the "first milk" that piglets ingest right after birth. This paper describes a study that tested the best time to vaccinate the sow prior to farrowing so that a good protective immune response would occur, and then be passed to her baby piglets. Results indicated that vaccinating the sow during the second trimester of gestation was better than vaccinating during the first or third trimesters. This information may be useful in developing better strategies to control and prevent porcine epidemic diarrhea in young pigs.

Technical Abstract: During pregnancy, the maternal immune response changes dramatically over the course of gestation. This has implications for generation of lactogenic immunity and subsequent protection in suckling neonates against enteric viral infections. For example, porcine epidemic diarrhea virus (PEDV) is an alphacoronavirus that causes acute diarrhea in neonatal piglets. Due to the high virulence of PEDV and the naïve, immature immune system of neonatal suckling piglets, passive lactogenic immunity to PEDV induced during pregnancy, via the gut-mammary gland (MG)-secretory IgA (sIgA) axis, is critical for piglet protection. However, the anti-PEDV immune response during pregnancy and stage of gestation required to optimally stimulate the gut-MG-sIgA axis is undefined. We hypothesize that there is a gestational window in which non-lethal PEDV infection of pregnant gilts influences maximum lymphocyte mucosal trafficking to the MG, resulting in optimal passive lactogenic protection in suckling piglets. To understand how the stages of gestation affect maternal immune responses to PEDV, three groups of gilts were orally infected with PEDV in the first, second or third trimester. Control (mock) gilts were inoculated with medium in the third trimester. To determine if lactogenic immunity correlated with protection, all piglets were PEDV-challenged at 3-5 days postpartum. Pregnant second trimester gilts had significantly higher levels of circulating PEDV IgA and IgG antibodies (Abs) and antibody secreting cells (ASCs) and PEDV virus neutralizing (VN) Abs post PEDV infection. Coinciding with the significantly higher PEDV Ab responses in second trimester gilts, the survival rate of their PEDV-challenged piglets was 100%, compared with 87.2%, 55.9% and 5.7% for first, third and mock litters, respectively. Additionally, piglet survival correlated with PEDV IgA Abs and ASCs and VN Abs in milk and PEDV IgA and IgG Abs in piglet serum. Our findings have implications for gestational timing of oral attenuated PEDV maternal vaccines, whereby PEDV intestinal infection in the second trimester optimally stimulated the gut-MG-sIgA axis resulting in 100% lactogenic immune protection in suckling piglets.