Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (20): 4145-4160.doi: 10.3864/j.issn.0578-1752.2024.20.018

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles    

Effects of Aflatoxin B1 on Influenza Virus Replication, Organ Damages and Intestinal Microbiota Disorder of Swine

ZHAO WenShuo(), ZHANG JinLong, YAO ZhaoRan, SONG YuQi, LÜ Shun, LIU YingXue, YUAN CongCong, SUN YuHang*()   

  1. College of Animal Science and Medicine, Shenyang Agricultural University, Shenyang 110866
  • Received:2024-04-17 Accepted:2024-08-25 Online:2024-10-16 Published:2024-10-24
  • Contact: SUN YuHang

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Abstract:

【Background】 Aflatoxin B1 (AFB1) is a secondary metabolite produced by Aspergillus parasiticus, which is widely found in contaminated food and feed all over the world and is considered one of the major risk factors affecting human and animal health. The swine influenza virus (SIV) is currently one of the most widespread viruses in the world, and its replication is susceptible to environmental and nutritional factors. However, the relationship between AFB1 contamination in feed and SIV infection is not clear.【Objective】The objective of this study was to investigate the effects of AFB1 exposure on SIV replication, organs damage and intestinal microbiota, so as to lay a foundation for the study on the mechanism of mycotoxin poisoning, and also provide a reference for exploring the reasons for the increase in susceptibility to other infectious diseases. 【Method】 In this study, thirty-two male piglets were randomly divided into 4 groups (8 piglets in each group), the low-pathogenic SIV virus dilution was inoculated on the first and fourth day of the trial, and established a piglet model of SIV infection (the natural host of SIV). AFB1 was freshly diluted daily and and given 0, 10, 20 and 40 μg·kg-1 (feed) AFB1 to piglets for 21 days. The piglets were weighed before feeding at 7, 14 and 21 days, respectively, and used a variety of technologies to assess the effects of dietary AFB1 exposure on the weight gain, SIV replication, organs index, autopsy changes, and pathological characteristics, On this basis, the expression of nucleoprotein (NP) of SIV in the lungs were further analyzed by Western blotting and the changes of intestinal microbiota were detected by 16S rRNA, thereby elucidate the effect of AFB1 exposure on SIV infection, organ damage, and intestinal microbiota. 【Result】The results showed that piglets exposed to 40 μg·kg-1AFB1 had significantly lower weight gain (P<0.01), the expression of NP and lung index of SIV were significantly higher (P<0.01), and the spleen index was significantly lower than those exposed to 0 μg·kg-1AFB1 (P<0.01); The results of autopsy showed severe spleen, liver and lung damage in piglets exposed to 40 μg·kg-1 AFB1; HE-stained also showed similar results, compared with the SIV control group, 40 μg·kg-1 AFB1 treatment group showed congestion in the spleen, the red and white pulp were not clear; the liver tissue was hemorrhage, inflammatory cells were infiltrated; the small alveoli of the lungs fused into large alveoli with irregular morphology, the alveolar interstitium was thickened, and the inflammatory cell infiltration was increased; in addition, the intestinal villi were irregularly shaped, the connective tissue was loose, and there was lymphocytic infiltration. The results from 16S rRNA sequencing showed that the exposure to 40 μg·kg-1 AFB1 significantly increased the relative abundance of Actinomycetota and Clostridium in the intestinal tract of piglets, and decreased the abundance of Lactobacillus and Bacteroidetes. 【Conclusion】Taken together, our results suggest that AFB1 exposure can reduce the body weight gain, promote SIV replication, aggravated the damage of lung tissue and other organs, and cause intestinal microbiota disorders, which provided a theoretical reference for the study of the toxic mechanism of AFB1.

Key words: aflatoxin B1, swine influenza virus, virus replication, organs damage, 16S rRNA, intestinal microbiota

Fig. 1

Effect of AFB1 exposure on body weight gain in SIV-infected piglets SIV: SIV control group; SIV+AFB1（10）: SIV+10 µg·kg-1 AFB1; SIV+AFB1（20）: SIV+20 µg·kg-1 AFB1; SIV+AFB1（40）: SIV+40 µg·kg-1 AFB1; *，P<0.05 was considered significant; **, P<0.01 was considered strongly significant"

Fig. 2

AFB1 exposure promotes SIV replication and aggravates lung damage a: viral NP protein expression levels; b: lung index; c: HE-stained images of the lungs. Representative images from piglets in each group were obtained at 100×（100 µm） and 400×（25 µm）magnification. SIV: SIV control group; SIV+AFB1（10）: SIV+10 µg·kg-1 AFB1; SIV+AFB1（20）: SIV+20 µg·kg-1 AFB1; SIV+AFB1（40）: SIV+40 µg·kg-1 AFB1; *，P<0.05 was considered significant; **, P<0.01 was considered strongly significant. The green circles represent the confluent large alveoli, the normal alveolar contour is completely lost, the yellow arrows represent inflammatory cell infiltration, and the black arrows represent the thickened alveolar interstitial"

Fig. 3

Effects of AFB1 on immune and digestive organs in SIV-infected piglets a：spleen index；b：liver index；c、d and e：HE-stained images of the spleens、livers and Intestines, Representative images from piglets in each group were obtained at 100×（100 µm） and 400×（25 µm）magnification. SIV: SIV control group; SIV+AFB1（10）: SIV+10 µg·kg-1 AFB1; SIV+AFB1（20）: SIV+20 µg·kg-1 AFB1; SIV+AFB1（40）: SIV+40 µg·kg-1 AFB1; *, P<0.05 was considered significant; **, P<0.01 was considered strongly significant. The white arrows represent the spleen and blood, and the yellow circles represent the unclear boundaries between the red and white pulp; the black arrows represent hepatic hemorrhage, and the yellow arrows represent inflammatory cell infiltration; the red arrows represent lymphocyte infiltration, and the green arrows represent loose connective tissue"

Fig. 4

Analysis of the number of OTU in intestinal content A: SIV control group; B: SIV+AFB1（40 µg·kg-1 AFB1）"

Fig. 5

Effect of AFB1 exposure on intestinal microbial composition of SIV-infected piglets a: The phylum-level composition of intestine microbiome; b: The genus-level composition of microbiome; c: The genus-level composition of microbiome. A: SIV control group; B: SIV+AFB1（40 µg·kg-1 AFB1）"

Fig. 6

Screening of differential microbiota between groups Heat map of differential microflora composition of plylum（a）、genus（b） and species（c）; Random forest analysis plots of plylum（d）、genus（e） and species（f）. A: SIV control group，B: SIV+AFB1 group; From top to bottom, the importance of species to the model decreases; These highly important species can be considered to be markers of intergroup differences"

Fig. 7

Effect of AFB1 exposure on gut microbial metabolic pathway a: KEGG metabolic pathway statistical chart; b: differential pathway diagram; c: KO_pathway chart。A: SIV control group, B: SIV+AFB1（40 μg/kg）; P<0.001 was considered strongly significant; P = 1, not significant"

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