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Published in: European Journal of Nutrition 4/2017

01-06-2017 | Original Contribution

Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period

Authors: Liang Hu, Xie Peng, Hong Chen, Chuan Yan, Yan Liu, Qin Xu, Zhengfeng Fang, Yan Lin, Shengyu Xu, Bin Feng, Jian Li, De Wu, Lianqiang Che

Published in: European Journal of Nutrition | Issue 4/2017

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Abstract

Objectives

The aim of this study was to investigate the effects of intrauterine growth retardation (IUGR) and Bacillus subtilis PB6 supplementation in formula milk (FORM) on growth performance, intestinal development and immune function of neonates using a porcine model.

Methods

Fourteen pairs of normal birth weight and IUGR piglets (7 days old) were randomly assigned to receive FORM or FORM supplemented with B. subtilis PB6 (FORM-BsPB6) for a period of 21 days. Blood samples, intestinal tissues and digesta were collected at necropsy and analysed for morphology, digestive enzyme activities, immune cell abundance, expression of genes associated with innate immunity and barrier function and microbial populations.

Results

Regardless of diet, IUGR significantly decreased average daily dry matter intake and average daily weight gain (P < 0.05). Moreover, IUGR significantly decreased plasma concentrations of immunoglobulin A, interleukin 1β, count and percentage of blood lymphocytes (P < 0.05). Meanwhile, IUGR markedly decreased villous height and maltase activity, as well as mRNA abundance of Toll-like receptor 9 and Toll-interacting protein in the ileum (P < 0.05). Regardless of body weight, FORM-BsPB6 markedly decreased the feed conversion ratio (P < 0.05), due to better intestinal development, as indicated by increased villous height (P < 0.05), activities of maltase and sucrase in the intestine (P < 0.10). Moreover, both mRNA and protein abundances of zonula occludens-1 and claudin-1 in the ileum as well as the copy number of Bacillus in colonic digesta were increased (P < 0.05) in piglets fed FORM-BsPB6 relative to FORM.

Conclusion

The results of this study indicate that IUGR delayed growth, intestinal development and immune function of piglets, while FORM-BsPB6 improved digestive capability and intestinal barrier function.
Literature
1.
go back to reference Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84(9):2316–2337. doi:10.2527/jas.2006-156 CrossRef Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84(9):2316–2337. doi:10.​2527/​jas.​2006-156 CrossRef
2.
go back to reference Pallotto EK, Kilbride HW (2006) Perinatal outcome and later implications of intrauterine growth restriction. Clin Obstet Gynecol 49(2):257–269CrossRef Pallotto EK, Kilbride HW (2006) Perinatal outcome and later implications of intrauterine growth restriction. Clin Obstet Gynecol 49(2):257–269CrossRef
3.
go back to reference Wang J, Chen L, Li D, Yin Y, Wang X, Li P, Dangott LJ, Hu W, Wu G (2008) Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J Nutr 138(1):60–66 Wang J, Chen L, Li D, Yin Y, Wang X, Li P, Dangott LJ, Hu W, Wu G (2008) Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J Nutr 138(1):60–66
4.
go back to reference Wang T, Huo YJ, Shi F, Xu RJ, Hutz RJ (2005) Effects of intrauterine growth retardation on development of the gastrointestinal tract in neonatal pigs. Biol Neonate 88(1):66–72. doi:10.1159/000084645 CrossRef Wang T, Huo YJ, Shi F, Xu RJ, Hutz RJ (2005) Effects of intrauterine growth retardation on development of the gastrointestinal tract in neonatal pigs. Biol Neonate 88(1):66–72. doi:10.​1159/​000084645 CrossRef
5.
6.
go back to reference Han F, Hu L, Xuan Y, Ding X, Luo Y, Bai S, He S, Zhang K, Che L (2013) Effects of high nutrient intake on the growth performance, intestinal morphology and immune function of neonatal intra-uterine growth-retarded pigs. Br J Nutr 110(10):1819–1827. doi:10.1017/S0007114513001232 CrossRef Han F, Hu L, Xuan Y, Ding X, Luo Y, Bai S, He S, Zhang K, Che L (2013) Effects of high nutrient intake on the growth performance, intestinal morphology and immune function of neonatal intra-uterine growth-retarded pigs. Br J Nutr 110(10):1819–1827. doi:10.​1017/​S000711451300123​2 CrossRef
7.
go back to reference Hu L, Liu Y, Yan C, Peng X, Xu Q, Xuan Y, Han F, Tian G, Fang Z, Lin Y, Xu S, Zhang K, Chen D, Wu D, Che L (2015) Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction. Br J Nutr 114(1):53–62. doi:10.1017/S0007114515001579 CrossRef Hu L, Liu Y, Yan C, Peng X, Xu Q, Xuan Y, Han F, Tian G, Fang Z, Lin Y, Xu S, Zhang K, Chen D, Wu D, Che L (2015) Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction. Br J Nutr 114(1):53–62. doi:10.​1017/​S000711451500157​9 CrossRef
8.
9.
go back to reference Wang M, Radlowski EC, Monaco MH, Fahey GC Jr, Gaskins HR, Donovan SM (2013) Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. J Nutr 143(6):795–803. doi:10.3945/jn.112.173096 CrossRef Wang M, Radlowski EC, Monaco MH, Fahey GC Jr, Gaskins HR, Donovan SM (2013) Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. J Nutr 143(6):795–803. doi:10.​3945/​jn.​112.​173096 CrossRef
10.
go back to reference Fanca-Berthon P, Hoebler C, Mouzet E, David A, Michel C (2010) Intrauterine growth restriction not only modifies the cecocolonic microbiota in neonatal rats but also affects its activity in young adult rats. J Pediatr Gastroenterol Nutr 51(4):402–413. doi:10.1097/MPG.0b013e3181d75d52 CrossRef Fanca-Berthon P, Hoebler C, Mouzet E, David A, Michel C (2010) Intrauterine growth restriction not only modifies the cecocolonic microbiota in neonatal rats but also affects its activity in young adult rats. J Pediatr Gastroenterol Nutr 51(4):402–413. doi:10.​1097/​MPG.​0b013e3181d75d52​ CrossRef
11.
go back to reference D’Inca R, Kloareg M, Gras-Le Guen C, Le Huerou-Luron I (2010) Intrauterine growth restriction modifies the developmental pattern of intestinal structure, transcriptomic profile, and bacterial colonization in neonatal pigs. J Nutr 140(5):925–931. doi:10.3945/jn.109.116822 CrossRef D’Inca R, Kloareg M, Gras-Le Guen C, Le Huerou-Luron I (2010) Intrauterine growth restriction modifies the developmental pattern of intestinal structure, transcriptomic profile, and bacterial colonization in neonatal pigs. J Nutr 140(5):925–931. doi:10.​3945/​jn.​109.​116822 CrossRef
12.
go back to reference Lin H-C, Su B-H, Chen A-C, Lin T-W, Tsai C-H, Yeh T-F, Oh W (2005) Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 115(1):1–4CrossRef Lin H-C, Su B-H, Chen A-C, Lin T-W, Tsai C-H, Yeh T-F, Oh W (2005) Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 115(1):1–4CrossRef
13.
go back to reference Alexopoulos C, Georgoulakis IE, Tzivara A, Kyriakis CS, Govaris A, Kyriakis SC (2004) Field evaluation of the effect of a probiotic-containing Bacillus licheniformis and Bacillus subtilis spores on the health status, performance, and carcass quality of grower and finisher pigs. J Vet Med A Physiol Pathol Clin Med 51(6):306–312. doi:10.1111/j.1439-0442.2004.00637.x CrossRef Alexopoulos C, Georgoulakis IE, Tzivara A, Kyriakis CS, Govaris A, Kyriakis SC (2004) Field evaluation of the effect of a probiotic-containing Bacillus licheniformis and Bacillus subtilis spores on the health status, performance, and carcass quality of grower and finisher pigs. J Vet Med A Physiol Pathol Clin Med 51(6):306–312. doi:10.​1111/​j.​1439-0442.​2004.​00637.​x CrossRef
14.
go back to reference Braga TD, da Silva GA, de Lira PI, de Carvalho Lima M (2011) Efficacy of Bifidobacterium breve and Lactobacillus casei oral supplementation on necrotizing enterocolitis in very-low-birth-weight preterm infants: a double-blind, randomized, controlled trial. Am J Clin Nutr 93(1):81–86. doi:10.3945/ajcn.2010.29799 CrossRef Braga TD, da Silva GA, de Lira PI, de Carvalho Lima M (2011) Efficacy of Bifidobacterium breve and Lactobacillus casei oral supplementation on necrotizing enterocolitis in very-low-birth-weight preterm infants: a double-blind, randomized, controlled trial. Am J Clin Nutr 93(1):81–86. doi:10.​3945/​ajcn.​2010.​29799 CrossRef
15.
go back to reference Han GQ, Xiang ZT, Yu B, Chen DW, Qi HW, Mao XB, Chen H, Mao Q, Huang ZQ (2012) Effects of different starch sources on Bacillus spp. in intestinal tract and expression of intestinal development related genes of weanling piglets. Mol Biol Rep 39(2):1869–1876. doi:10.1007/s11033-011-0932-x CrossRef Han GQ, Xiang ZT, Yu B, Chen DW, Qi HW, Mao XB, Chen H, Mao Q, Huang ZQ (2012) Effects of different starch sources on Bacillus spp. in intestinal tract and expression of intestinal development related genes of weanling piglets. Mol Biol Rep 39(2):1869–1876. doi:10.​1007/​s11033-011-0932-x CrossRef
17.
go back to reference Hu Y, Dun Y, Li S, Zhao S, Peng N, Liang Y (2014) Effects of Bacillus subtilis KN-42 on growth performance, diarrhea and faecal bacterial flora of weaned piglets. Asian Australas J Anim Sci 27(8):1131CrossRef Hu Y, Dun Y, Li S, Zhao S, Peng N, Liang Y (2014) Effects of Bacillus subtilis KN-42 on growth performance, diarrhea and faecal bacterial flora of weaned piglets. Asian Australas J Anim Sci 27(8):1131CrossRef
19.
go back to reference Rolfe RD (2000) The role of probiotic cultures in the control of gastrointestinal health. J Nutr 130(2S Suppl):396S–402S Rolfe RD (2000) The role of probiotic cultures in the control of gastrointestinal health. J Nutr 130(2S Suppl):396S–402S
20.
go back to reference Sangild PT (2006) Gut responses to enteral nutrition in preterm infants and animals. Exp Biol Med 231(11):1695–1711CrossRef Sangild PT (2006) Gut responses to enteral nutrition in preterm infants and animals. Exp Biol Med 231(11):1695–1711CrossRef
21.
go back to reference Che L, Thymann T, Bering SB, LEH-L I, D’Inca R, Zhang K, Sangild PT (2010) IUGR does not predispose to necrotizing enterocolitis or compromise postnatal intestinal adaptation in preterm pigs. Pediatr Res 67(1):54–59. doi:10.1203/PDR.0b013e3181c1b15e CrossRef Che L, Thymann T, Bering SB, LEH-L I, D’Inca R, Zhang K, Sangild PT (2010) IUGR does not predispose to necrotizing enterocolitis or compromise postnatal intestinal adaptation in preterm pigs. Pediatr Res 67(1):54–59. doi:10.​1203/​PDR.​0b013e3181c1b15e​ CrossRef
22.
go back to reference Zhang Y, Chen DW, Yu B, He J, Yu J, Mao XB, Wang JX, Luo JQ, Huang ZQ, Cheng GX, Zheng P (2015) Spray-dried chicken plasma improves intestinal digestive function and regulates intestinal selected microflora in weaning piglets. J Anim Sci 93(6):2967–2976. doi:10.2527/jas.2014-8820 CrossRef Zhang Y, Chen DW, Yu B, He J, Yu J, Mao XB, Wang JX, Luo JQ, Huang ZQ, Cheng GX, Zheng P (2015) Spray-dried chicken plasma improves intestinal digestive function and regulates intestinal selected microflora in weaning piglets. J Anim Sci 93(6):2967–2976. doi:10.​2527/​jas.​2014-8820 CrossRef
23.
go back to reference Chen Y, Chen D, Tian G, He J, Mao X, Mao Q, Yu B (2012) Dietary arginine supplementation alleviates immune challenge induced by Salmonella enterica serovar Choleraesuis bacterin potentially through the Toll-like receptor 4-myeloid differentiation factor 88 signalling pathway in weaned piglets. Br J Nutr 108(6):1069–1076. doi:10.1017/S0007114511006350 CrossRef Chen Y, Chen D, Tian G, He J, Mao X, Mao Q, Yu B (2012) Dietary arginine supplementation alleviates immune challenge induced by Salmonella enterica serovar Choleraesuis bacterin potentially through the Toll-like receptor 4-myeloid differentiation factor 88 signalling pathway in weaned piglets. Br J Nutr 108(6):1069–1076. doi:10.​1017/​S000711451100635​0 CrossRef
24.
25.
go back to reference Zhang B, Guo Y (2009) Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets. Br J Nutr 102(5):687–693. doi:10.1017/S0007114509289033 CrossRef Zhang B, Guo Y (2009) Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets. Br J Nutr 102(5):687–693. doi:10.​1017/​S000711450928903​3 CrossRef
26.
go back to reference Garite TJ, Clark R, Thorp JA (2004) Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol 191(2):481–487CrossRef Garite TJ, Clark R, Thorp JA (2004) Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol 191(2):481–487CrossRef
27.
go back to reference Mandruzzato G, Antsaklis A, Botet F, Chervenak FA, Figueras F, Grunebaum A, Puerto B, Skupski D, Stanojevic M, WAPM (2008) Intrauterine restriction (IUGR). J Perinat Med 36(4):277–281. doi:10.1515/JPM.2008.050 CrossRef Mandruzzato G, Antsaklis A, Botet F, Chervenak FA, Figueras F, Grunebaum A, Puerto B, Skupski D, Stanojevic M, WAPM (2008) Intrauterine restriction (IUGR). J Perinat Med 36(4):277–281. doi:10.​1515/​JPM.​2008.​050 CrossRef
28.
go back to reference Musa H, Wu S, Zhu C, Seri H, Zhu G (2009) The potential benefits of probiotics in animal production and health. J Anim Vet Adv 8(2):313–321 Musa H, Wu S, Zhu C, Seri H, Zhu G (2009) The potential benefits of probiotics in animal production and health. J Anim Vet Adv 8(2):313–321
29.
go back to reference Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 84(Suppl):E113–E123CrossRef Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 84(Suppl):E113–E123CrossRef
30.
go back to reference Morise A, Seve B, Mace K, Magliola C, Le Huerou-Luron I, Louveau I (2011) Growth, body composition and hormonal status of growing pigs exhibiting a normal or small weight at birth and exposed to a neonatal diet enriched in proteins. Br J Nutr 105(10):1471–1479. doi:10.1017/S0007114510005386 CrossRef Morise A, Seve B, Mace K, Magliola C, Le Huerou-Luron I, Louveau I (2011) Growth, body composition and hormonal status of growing pigs exhibiting a normal or small weight at birth and exposed to a neonatal diet enriched in proteins. Br J Nutr 105(10):1471–1479. doi:10.​1017/​S000711451000538​6 CrossRef
31.
go back to reference Alvarenga AL, Chiarini-Garcia H, Cardeal PC, Moreira LP, Foxcroft GR, Fontes DO, Almeida FR (2013) Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits. Reprod Fertil Dev 25(2):387–395. doi:10.1071/RD12021 CrossRef Alvarenga AL, Chiarini-Garcia H, Cardeal PC, Moreira LP, Foxcroft GR, Fontes DO, Almeida FR (2013) Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits. Reprod Fertil Dev 25(2):387–395. doi:10.​1071/​RD12021 CrossRef
32.
go back to reference Chen Y, Min B, Cho J, Kwon O, Son K, Kim H, Kim I (2006) Effects of dietary Bacillus-based probiotic on growth performance, nutrients digestibility, blood characteristics and fecal noxious gas content in finishing pigs. Asian Australas J Anim Sci 19(4):587CrossRef Chen Y, Min B, Cho J, Kwon O, Son K, Kim H, Kim I (2006) Effects of dietary Bacillus-based probiotic on growth performance, nutrients digestibility, blood characteristics and fecal noxious gas content in finishing pigs. Asian Australas J Anim Sci 19(4):587CrossRef
33.
go back to reference Lee SH, Ingale SL, Kim JS, Kim KH, Lokhande A, Kim EK, Kwon IK, Kim YH, Chae BJ (2014) Effects of dietary supplementation with Bacillus subtilis LS 1–2 fermentation biomass on growth performance, nutrient digestibility, cecal microbiota and intestinal morphology of weanling pig. Anim Feed Sci Technol 188:102–110. doi:10.1016/j.anifeedsci.2013.12.001 CrossRef Lee SH, Ingale SL, Kim JS, Kim KH, Lokhande A, Kim EK, Kwon IK, Kim YH, Chae BJ (2014) Effects of dietary supplementation with Bacillus subtilis LS 1–2 fermentation biomass on growth performance, nutrient digestibility, cecal microbiota and intestinal morphology of weanling pig. Anim Feed Sci Technol 188:102–110. doi:10.​1016/​j.​anifeedsci.​2013.​12.​001 CrossRef
34.
35.
go back to reference Amdi C, Krogh U, Flummer C, Oksbjerg N, Hansen CF, Theil PK (2013) Intrauterine growth restricted piglets defined by their head shape ingest insufficient amounts of colostrum. J Anim Sci 91(12):5605–5613. doi:10.2527/jas.2013-6824 CrossRef Amdi C, Krogh U, Flummer C, Oksbjerg N, Hansen CF, Theil PK (2013) Intrauterine growth restricted piglets defined by their head shape ingest insufficient amounts of colostrum. J Anim Sci 91(12):5605–5613. doi:10.​2527/​jas.​2013-6824 CrossRef
36.
go back to reference Hales J, Moustsen VA, Nielsen MB, Hansen CF (2013) Individual physical characteristics of neonatal piglets affect preweaning survival of piglets born in a noncrated system. J Anim Sci 91(10):4991–5003. doi:10.2527/jas.2012-5740 CrossRef Hales J, Moustsen VA, Nielsen MB, Hansen CF (2013) Individual physical characteristics of neonatal piglets affect preweaning survival of piglets born in a noncrated system. J Anim Sci 91(10):4991–5003. doi:10.​2527/​jas.​2012-5740 CrossRef
38.
go back to reference Dong L, Zhong X, He J, Zhang L, Bai K, Xu W, Wang T, Huang X (2015) Supplementation of tributyrin improves the growth and intestinal digestive and barrier functions in intrauterine growth-restricted piglets. Clin Nutr. doi:10.1016/j.clnu.2015.03.002 Dong L, Zhong X, He J, Zhang L, Bai K, Xu W, Wang T, Huang X (2015) Supplementation of tributyrin improves the growth and intestinal digestive and barrier functions in intrauterine growth-restricted piglets. Clin Nutr. doi:10.​1016/​j.​clnu.​2015.​03.​002
39.
go back to reference Xu RJ, Mellor DJ, Birtles MJ, Reynolds GW, Simpson HV (1994) Impact of intrauterine growth retardation on the gastrointestinal tract and the pancreas in newborn pigs. J Pediatr Gastroenterol Nutr 18(2):231–240CrossRef Xu RJ, Mellor DJ, Birtles MJ, Reynolds GW, Simpson HV (1994) Impact of intrauterine growth retardation on the gastrointestinal tract and the pancreas in newborn pigs. J Pediatr Gastroenterol Nutr 18(2):231–240CrossRef
40.
go back to reference Montagne L, Pluske J, Hampson D (2003) A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim Feed Sci Technol 108(1):95–117CrossRef Montagne L, Pluske J, Hampson D (2003) A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim Feed Sci Technol 108(1):95–117CrossRef
41.
go back to reference Kelly D, Coutts AG (2000) Early nutrition and the development of immune function in the neonate. Proc Nutr Soc 59(2):177–185CrossRef Kelly D, Coutts AG (2000) Early nutrition and the development of immune function in the neonate. Proc Nutr Soc 59(2):177–185CrossRef
42.
go back to reference Amu S, Hahn-Zoric M, Malik A, Ashraf R, Zaman S, Kjellmer I, Hagberg H, Padyukov L, Hanson LÅ (2006) Cytokines in the placenta of Pakistani newborns with and without intrauterine growth retardation. Pediatr Res 59(2):254–258CrossRef Amu S, Hahn-Zoric M, Malik A, Ashraf R, Zaman S, Kjellmer I, Hagberg H, Padyukov L, Hanson LÅ (2006) Cytokines in the placenta of Pakistani newborns with and without intrauterine growth retardation. Pediatr Res 59(2):254–258CrossRef
43.
go back to reference Briana DD, Liosi S, Gourgiotis D, Boutsikou M, Marmarinos A, Baka S, Hassiakos D, Malamitsi-Puchner A (2012) Fetal concentrations of the growth factors TGF-alpha and TGF-beta1 in relation to normal and restricted fetal growth at term. Cytokine 60(1):157–161. doi:10.1016/j.cyto.2012.06.005 CrossRef Briana DD, Liosi S, Gourgiotis D, Boutsikou M, Marmarinos A, Baka S, Hassiakos D, Malamitsi-Puchner A (2012) Fetal concentrations of the growth factors TGF-alpha and TGF-beta1 in relation to normal and restricted fetal growth at term. Cytokine 60(1):157–161. doi:10.​1016/​j.​cyto.​2012.​06.​005 CrossRef
44.
go back to reference Contreras YM, Yu X, Hale MA, Callaway CW, Bareyan D, McKnight RA, Joss-Moore LA, Enioutina EY, Lane RH (2011) Intrauterine growth restriction alters T-lymphocyte cell number and dual specificity phosphatase 1 levels in the thymus of newborn and juvenile rats. Pediatr Res 70(2):123–129. doi:10.1203/PDR.0b013e31821f6e75 CrossRef Contreras YM, Yu X, Hale MA, Callaway CW, Bareyan D, McKnight RA, Joss-Moore LA, Enioutina EY, Lane RH (2011) Intrauterine growth restriction alters T-lymphocyte cell number and dual specificity phosphatase 1 levels in the thymus of newborn and juvenile rats. Pediatr Res 70(2):123–129. doi:10.​1203/​PDR.​0b013e31821f6e75​ CrossRef
46.
go back to reference Wang S-P, Yang L, Tang X-S, Cai L-C, Liu G, Kong X-F, Blachier F, Yin Y-L (2011) Dietary supplementation with high-dose Bacillus subtilis or Lactobacillus reuteri modulates cellular and humoral immunities and improves performance in weaned piglets. J Food Agric Environ 9(2):181–187 Wang S-P, Yang L, Tang X-S, Cai L-C, Liu G, Kong X-F, Blachier F, Yin Y-L (2011) Dietary supplementation with high-dose Bacillus subtilis or Lactobacillus reuteri modulates cellular and humoral immunities and improves performance in weaned piglets. J Food Agric Environ 9(2):181–187
47.
go back to reference Suarez-Souto MA, Lara-Padilla E, Reyna-Garfias H, Viloria M, Lopez-Sanchez P, Rivera-Aguilar V, Miliar-Garcia A, Kormanovski A, Dominguez-Lopez ML, Campos-Rodriguez R (2012) Caloric restriction modifies both innate and adaptive immunity in the mouse small intestine. J Physiol Biochem 68(2):163–173. doi:10.1007/s13105-011-0128-9 CrossRef Suarez-Souto MA, Lara-Padilla E, Reyna-Garfias H, Viloria M, Lopez-Sanchez P, Rivera-Aguilar V, Miliar-Garcia A, Kormanovski A, Dominguez-Lopez ML, Campos-Rodriguez R (2012) Caloric restriction modifies both innate and adaptive immunity in the mouse small intestine. J Physiol Biochem 68(2):163–173. doi:10.​1007/​s13105-011-0128-9 CrossRef
52.
go back to reference Blasig IE, Bellmann C, Cording J, Del Vecchio G, Zwanziger D, Huber O, Haseloff RF (2011) Occludin protein family: oxidative stress and reducing conditions. Antioxid Redox Signal 15(5):1195–1219. doi:10.1089/ars.2010.3542 CrossRef Blasig IE, Bellmann C, Cording J, Del Vecchio G, Zwanziger D, Huber O, Haseloff RF (2011) Occludin protein family: oxidative stress and reducing conditions. Antioxid Redox Signal 15(5):1195–1219. doi:10.​1089/​ars.​2010.​3542 CrossRef
Metadata
Title
Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period
Authors
Liang Hu
Xie Peng
Hong Chen
Chuan Yan
Yan Liu
Qin Xu
Zhengfeng Fang
Yan Lin
Shengyu Xu
Bin Feng
Jian Li
De Wu
Lianqiang Che
Publication date
01-06-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 4/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1223-z

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