Skip to main content Accessibility help

Effects of early protein restriction on the growth performance and gut development of pigs fed diets with or without antibiotic

  • X. Zhao (a1), H. Y. Fu (a1), S. N. Qiu (a1), T. Teng (a1), G. D. Bai (a1), D. X. Ju (a1), Y. C. Sun (a1) and B. M. Shi (a1)...


In the livestock husbandry compensatory growth may be explored as a means to improve nutrient utilization, to reduce gut health problems due to excess protein intake, to simplify feeding strategies and thus to improve production efficiencies. This study investigated the effects of early protein restriction (EPR) and early antibiotic intervention (EAI) on growth performance, intestinal morphology, colonic bacteria, metabolites and mucosal gene expressions during the restriction phase and re-alimentation phase. A total of 64 piglets (10.04 ± 0.73 kg) were randomly divided into four treatment groups according to a 2 × 2 factorial arrangement with two levels of proteins (14% v. 20%) and two levels of antibiotics (0 v. 50 mg/kg kitasamycin and 20 mg/kg colistin sulphate). After a 30-day restriction phase with four kinds of diets, all groups were fed the same diets for another 74 days. The results showed that EPR decreased BW, average daily gain (ADG), average daily feed intake in the restriction phase (P < 0.01) and increased ADG on days 66 to 104 of the late re-alimentation phase. Early protein restriction could decrease the villus height in the jejunum (P < 0.05), while shifting to the same diets restored the villus height. Meanwhile, during the re-alimentation phase, pigs in the protein restriction groups had increased concentrations of total short chain fatty acids (P < 0.05), and modified the abundances of Firmicutes and Bacteroidetes in the colon. Furthermore, the lower microbial diversity caused by EPR was improved, and gene expression analysis indicated a better barrier function in the colon. During the whole trial, EAI had no interaction with EPR and played a dispensable role in compensatory growth. Collectively, the retardation of growth caused by EPR can be compensated for in the later stages of pig raising, and accompanied by altered intestinal morphology, microbial composition.


Corresponding author


Hide All
Allen, HK, Looft, T, Bayles, DO, Humphrey, S, Levine, UY, Alt, D and Stanton, TB 2011. Antibiotics in feed induce prophages in swine fecal microbiomes. MBio 2, e00260-11.
Chaosap, C, Parr, T and Wiseman, J 2011. Effect of compensatory growth on performance, carcass composition and plasma IGF-1 in grower finisher pigs. Animal 5, 749756.
Chen, JC, Xu, QQ, Li, YX, Tang, ZR, Sun, WZ, Zhang, XX, Sun, JJ and Sun, ZH 2019. Comparative effects of dietary supplementations with sodium butyrate, medium-chain fatty acids, and n-3 polyunsaturated fatty acids in late pregnancy and lactation on the reproductive performance of sows and growth performance of suckling piglets. Journal of Animal Science 97, 42564267.
Chiba, LI 2000. Feeding systems for pigs. In Feeding systems and feed evaluation models (ed. Theodorou, MK and France, J), pp. 181209. CABI Publishing, Wallingford, UK.
Choi, JY, Kim, JS, Ingale, SL, Kim, KH, Shinde, PL, Kwon, IK and Chae, BJ 2011. Effect of potential multimicrobe probiotic product processed by high drying temperature and antibiotic on performance of weanling pigs. Journal of Animal Science 89, 17951804.
Claus, SP, Ellero, SL, Berger, B, Krause, L, Bruttin, A, Molina, J, Paris, A, Want, EJ, de Waziers, I, Cloarec, O, Richards, SE, Wang, Y, Dumas, ME, Ross, A, Rezzi, S, Kochhar, S, Van Bladeren, P, Lindon, JC, Holmes, E and Nicholson, JK 2011. Colonization-induced host-gut microbial metabolic interaction. MBio 2, e00271-10.
Davila, AM, Blachier, F, Gotteland, M, Andriamihaja, M, Benetti, PH, Sanz, Y and Tome, D 2013. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacological Research 68, 95107.
Fan, YK, Croom, J, Christensen, VL, Black, BL, Bird, AR, Daniel, LR, McBride, BW and Eisen, EJ 1997. Jejunal glucose uptake and oxygen consumption in Turkey poults selected for rapid growth. Poultry Science 76, 17381745.
Gao, PK, Li, Y, Tan, LJ, Guo, FF and Ma, T 2019. Composition of bacterial and archaeal communities in an alkali-surfactant-polyacrylamide-flooded oil reservoir and the responses of microcosms to nutrients. Frontiers in Microbiology 10, 2197.
Gill, M, Smith, P and Wilkinson, JM 2010. Mitigating climate change: the role of domestic livestock. Animal 4, 323333.
Greenhill, C 2015. Gut microbiota: Firmicutes and Bacteroidetes involved in insulin resistance by mediating levels of glucagon-like peptide 1. Nature Reviews Endocrinology 11, 254
Hamer, HM, De Preter, V, Windey, K and Verbeke, K 2012. Functional analysis of colonic bacterial metabolism: relevant to health? American Journal of Physiology-Gastrointestinal and Liver Physiology 302, G1G9.
Hooper, LV, Dan, RL and Macpherson, AJ 2012. Interactions between the microbiota and the immune system. Science 336, 12681273.
Ishida, A, Kyoya, T, Nakashima, K and Katsumata, M 2012. Nitrogen balance during compensatory growth when changing the levels of dietary lysine from deficiency to sufficiency in growing pigs. Animal Science Journal 83, 743749.
Istasse, L 2000. Mechanisms of reduced and compensatory growth. Domestic Animal Endocrinology 19, 121132.
Johnson, EC, Doser, TA, Cepurna, WO, Dyck, JA, Jia, LJ, Guo, Y, Lambert, WS and Morrison, JC 2011. Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma. Investigative Ophthalmology & Visual Science 52, 504518.
Konstantinov, SR, Favier, CF, Zhu, WY, Williams, BA, Kluss, J, Souffrant, WB, de Vos, WM, Akkermans, ADL and Smidt, H 2004. Microbial diversity studies of the porcine gastrointestinal ecosystem during weaning transition. Animal Research 53, 317324.
Lebret, B, Heyer, A, Gondret, F and Louveau, I 2007. The response of various muscle types to a restriction-re-alimentation feeding strategy in growing pigs. Animal 1, 849857.
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.
Ma, X, Fan, PX, Li, LS, Qiao, SY, Zhang, GL and Li, DF 2012. Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. Journal of Animal Science 90, 266268.
Martínez-Ramírez, HR and Lange, CFM DE 2008. Compensatory growth in pigs. Recent Advances in Animal Nutrition 1, 331352.
Meng, QW, Sun, SS, Luo, Z, Shi, BM, Shan, AS and Cheng, BJ 2019. Maternal dietary resveratrol alleviates weaning-associated diarrhea and intestinal inflammation in pig offspring by changing intestinal gene expression and microbiota. Food & Function 10, 56265643.
Ministry of Agriculture of the People’s Republic of China (MOA ) 2004. Feeding standard of swine, NY/T65. China Agriculture Press, Beijing, China.
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th revised edition. National Academy Press, Washington, DC, USA.
Nicholson, JK, Holmes, E, Kinross, J, Burcelin, R, Gibson, G, Jia, W and Pettersson, S 2012. Host-gut microbiota metabolic interactions. Science 336, 12621267.
Nyachoti, CM, Omogbenigun, FO, Rademacher, M and Blank, G 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. Journal of Animal Science 84, 125.
Peng, L, He, Z, Chen, W, Holzman, IR and Lin, J 2007. Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatric Research 61, 3741.
Rasmussen, HS, Holtug, K and Mortensen, PB 1988. Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scandinavian Journal of Gastroenterology 23, 178182.
Ríoscovián, D, Ruasmadiedo, P, Margolles, A, Gueimonde, M, Cg, RG and Salazar, N 2016. Intestinal short chain fatty acids and their link with diet and human health. Frontiers in Microbiology 7, 185.
Samuel, BS, Shaito, A, Motoike, T, Rey, FE, Backhed, F, Manchester, JK, Hammer, RE, Williams, SC, Crowley, J, Yanagisawa, M and Gordon, JI 2008. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proceedings of the National Academy of Sciences of the United States of America 105, 1676716772.
Sen, S, Ingale, SL, Kim, YW, Kim, JS, Kim, KH, Lohakare, JD, Kim, EK, Kim, HS, Ryu, MH and Kwon, IK 2012. Effect of supplementation of Bacillus subtilis LS 1-2 to broiler diets on growth performance, nutrient retention, caecal microbiology and small intestinal morphology. Research in Veterinary Science 93, 264.
Tossou, MCB, Liu, H, Bai, M, Shuai, C, Cai, Y, Veeramuthu, D, Liu, H, Adebowale, TO, Abdullah, ADN and Long, L 2016. Effect of high dietary tryptophan on intestinal morphology and tight junction protein of weaned pig. BioMed Research International 6, 16.
Weis, RN, Birkett, SH, Morel, PCH and de Lange, CFM 2004. Effects of energy intake and body weight on physical and chemical body composition in growing entire male pigs. Journal of Animal Science 82, 109121.
Yang, Y, Mu, C, Zhang, J and Zhu, W 2014. Determination of biogenic amines in digesta by high performance liquid chromatography with precolumn dansylation. Analytical Letters 47, 12901298.
Ye, G, Qiu, Y, He, X, Zhao, L, Shi, F, Lv, C, Jing, B and Li, Y 2015. Effect of two macrocephala flavored powder supplementation on intestinal morphology and intestinal microbiota in weaning pigs. International Journal of Clinical and Experimental Medicine 8, 15041514.
Yoon, JH, Ingale, SL, Kim, JS, Kim, KH, Lee, SH, Park, YK, Kwon, IK and Chae, BJ 2012. Effects of dietary supplementation of antimicrobial peptide-A3 on growth performance, nutrient digestibility, intestinal and fecal microflora and intestinal morphology in weanling pigs. Animal Feed Science and Technology 177, 98107.
Zhang, C, Yu, M, Yang, Y, Mu, C, Su, Y and Zhu, W 2016. Differential effect of early antibiotic intervention on bacterial fermentation patterns and mucosal gene expression in the colon of pigs under diets with different protein levels. Applied Microbiology & Biotechnology 101, 113.


Type Description Title
Supplementary materials

Zhao et al. supplementary material
Zhao et al. supplementary material

 Word (200 KB)
200 KB

Effects of early protein restriction on the growth performance and gut development of pigs fed diets with or without antibiotic

  • X. Zhao (a1), H. Y. Fu (a1), S. N. Qiu (a1), T. Teng (a1), G. D. Bai (a1), D. X. Ju (a1), Y. C. Sun (a1) and B. M. Shi (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed