Restored intestinal integrity, nutrients transporters, energy metabolism, antioxidative capacity and decreased harmful microbiota were associated with IUGR piglet's catch-up growth before weanling

Chang Cui; Caichi Wu; Jun Wang; Ziwei Ma; Xiaoyu Zheng; Pengwei Zhu; Nuan Wang; Yuhua Zhu; Wutai Guan; Fang Chen

doi:10.1186/s40104-022-00770-8

Restored intestinal integrity, nutrients transporters, energy metabolism, antioxidative capacity and decreased harmful microbiota were associated with IUGR piglet's catch-up growth before weanling

J Anim Sci Biotechnol. 2022 Oct 14;13(1):129. doi: 10.1186/s40104-022-00770-8.

Authors

Chang Cui¹, Caichi Wu¹, Jun Wang¹, Ziwei Ma¹, Xiaoyu Zheng¹, Pengwei Zhu¹, Nuan Wang¹, Yuhua Zhu^{2

3

4}, Wutai Guan^{5

6

7}, Fang Chen^{8

9

10}

Affiliations

¹ Guangdong Provincial Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou, 510642, China.
² Shenzhen Kingsino Technology CO., LTD, Shenzhen, 518107, China.
³ Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan, 430070, China.
⁴ Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518116, China.
⁵ Guangdong Provincial Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou, 510642, China. wtguan@scau.edu.cn.
⁶ College of Animal Science and National Engineering Research Center for Breeding Swine Industry, South China Agricultural University, Guangzhou, 510642, China. wtguan@scau.edu.cn.
⁷ Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, 510642, China. wtguan@scau.edu.cn.
⁸ Guangdong Provincial Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou, 510642, China. chenfang1111@scau.edu.cn.
⁹ College of Animal Science and National Engineering Research Center for Breeding Swine Industry, South China Agricultural University, Guangzhou, 510642, China. chenfang1111@scau.edu.cn.
¹⁰ Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, 510642, China. chenfang1111@scau.edu.cn.

Abstract

Background: Intrauterine growth restriction (IUGR) is a major inducer of higher morbidity and mortality in the pig industry and catch-up growth (CUG) before weanling could significantly restore this negative influence. But there was limited knowledge about the underlying mechanism of CUG occurrence.

Methods: Eighty litters of newborn piglets were divided into normal birth weight (NBW) and IUGR groups according to birth weight. At 26 d, those piglets with IUGR but over average body weight of eighty litters of weaned piglets were considered as CUG, and the piglets with IUGR still below average body weight were considered as NCUG. This study was conducted to systemically compare the intestinal difference among NBW, CUG and NCUG weaned piglets considering the crucial role of the intestine for piglet growth.

Results: The results indicated that the mRNA expression of nutrients (amino acids, glucose, and fatty acids) transporters, and mitochondrial electron transport chain (ETC) I were upregulated in CUG piglets' gut with improved morphology compared with those NCUG, as well as the ratio of P-AMPK/AMPK protein expression which is the indicator of energy metabolism. Meanwhile, CUG piglet's gut showed higher antioxidative capacity with increased SOD and GSH-Px activity, decreased MDA levels, as well as higher mRNA expressions of Nrf2, Keap1, SOD, and GSH-Px. Furthermore, inflammatory parameters including TNF-α, IL-1β, IL-6, and IL-12 factors, and the activation of MAPK and NF-κB signaling pathways were significantly elevated in the NCUG intestine, while the protein expression of ZO-1, Occludin and Claudin-1 was reduced. The alpha diversity of fecal microbiota was higher in CUG piglets in contrast with NCUG piglets, and the increased beneficial bacteria and decreased pathogenic bacteria was also observed in CUG piglets.

Conclusions: CUG piglet's intestine showed comprehensive restoration including higher nutrients transport, energy metabolism, antioxidant capacity, and intestinal physical barrier, while lower oxidative stress, inflammatory response, and pathogenic microbiota.

Keywords: Antioxidative capacity; Catch-up growth; Gut; Intrauterine growth retardation; Piglets.

Abstract

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