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Microbial insight into dietary protein source affects intestinal function of pigs with intrauterine growth retardation

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Abstract

Purpose

Dietary protein, as important macronutrient, is vital for intestinal function and health status. We aimed to determine the effects of dietary protein source on growth performance and intestinal function of neonates with intrauterine growth retardation (IUGR) in a pig model.

Methods

Eighteen pairs of IUGR and normal birth weight (NBW) weaned pigs were allotted to be fed starter diet containing soybean protein concentrate (SPC) or spray-dried porcine plasma (SDPP) for 2 weeks. Growth performance, antioxidant variables, intestinal morphology and absorption capability, microbiota composition and short-chain fatty acids (SCFA) were assessed.

Results

IUGR led to poor growth performance, absorption capability and changes on antioxidant variables, while SDPP diet improved the growth performance, diarrhea index, intestinal morphology and antioxidant variables of IUGR or NBW pigs relative to that fed SPC diet. Importantly, SDPP diet improved bacterial diversity and increased the abundance of phylum Firmicutes, but decreased the phylum Proteobacteria in colonic digesta, associating with higher genera Lactobacillus and lower genera EscherichiaShigella, linking to the increased concentration of SCFA.

Conclusions

Our findings indicate that IUGR impairs the growth rate, intestinal function and oxidative status of weaned pigs, which could be partly improved by SDPP diet either for IUGR or NBW pigs, associating with the better antioxidant capability, composition of microbiotas and their metabolites.

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References

  1. 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. https://doi.org/10.2527/jas.2006-156

    Article  CAS  PubMed  Google Scholar 

  2. McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85(2):571–633. https://doi.org/10.1152/physrev.00053.2003

    Article  CAS  PubMed  Google Scholar 

  3. Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B Biol Sci 363(1497):1635–1645. https://doi.org/10.1098/rstb.2007.0011

    Article  PubMed  Google Scholar 

  4. 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. https://doi.org/10.1017/S0007114515001579

    Article  CAS  PubMed  Google Scholar 

  5. Zhong X, Wang T, Zhang X, Li W (2010) Heat shock protein 70 is upregulated in the intestine of intrauterine growth retardation piglets. Cell Stress Chaperones 15(3):335–342. https://doi.org/10.1007/s12192-009-0148-3

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  PubMed  Google Scholar 

  7. 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 Neonatol 88(1):66–72. https://doi.org/10.1159/000084645

    Article  Google Scholar 

  8. Longo S, Bollani L, Decembrino L, Di Comite A, Angelini M, Stronati M (2013) Short-term and long-term sequelae in intrauterine growth retardation (IUGR). J Matern Fetal Neonatal Med 26(3):222–225. https://doi.org/10.3109/14767058.2012.715006

    Article  CAS  PubMed  Google Scholar 

  9. Michiels J, De Vos M, Missotten J, Ovyn A, De Smet S, Van Ginneken C (2013) Maturation of digestive function is retarded and plasma antioxidant capacity lowered in fully weaned low birth weight piglets. Br J Nutr 109(1):65–75. https://doi.org/10.1017/S0007114512000670

    Article  CAS  PubMed  Google Scholar 

  10. Biri A, Bozkurt N, Turp A, Kavutcu M, Himmetoglu O, Durak I (2007) Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Investig 64(4):187–192. https://doi.org/10.1159/000106488

    Article  CAS  Google Scholar 

  11. Halkjaer J, Olsen A, Bjerregaard LJ, Deharveng G, Tjonneland A, Welch AA, Crowe FL, Wirfalt E, Hellstrom V, Niravong M, Touvier M, Linseisen J, Steffen A, Ocke MC, Peeters PH, Chirlaque MD, Larranaga N, Ferrari P, Contiero P, Frasca G, Engeset D, Lund E, Misirli G, Kosti M, Riboli E, Slimani N, Bingham S (2009) Intake of total, animal and plant proteins, and their food sources in 10 countries in the European Prospective Investigation into cancer and nutrition. Eur J Clin Nutr 63(Suppl 4):S16–S36. https://doi.org/10.1038/ejcn.2009.73

    Article  CAS  PubMed  Google Scholar 

  12. Boudry G, Rome V, Perrier C, Jamin A, Savary G, Le Huerou-Luron I (2014) A high-protein formula increases colonic peptide transporter 1 activity during neonatal life in low-birth-weight piglets and disturbs barrier function later in life. Br J Nutr 112(7):1073–1080. https://doi.org/10.1017/S0007114514001901

    Article  CAS  PubMed  Google Scholar 

  13. McAllan L, Skuse P, Cotter PD, O’Connor P, Cryan JF, Ross RP, Fitzgerald G, Roche HM, Nilaweera KN (2014) Protein quality and the protein to carbohydrate ratio within a high fat diet influences energy balance and the gut microbiota in C57BL/6J mice. PLoS One 9(2):e88904. https://doi.org/10.1371/journal.pone.0088904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Liu X, Blouin JM, Santacruz A, Lan A, Andriamihaja M, Wilkanowicz S, Benetti PH, Tome D, Sanz Y, Blachier F, Davila AM (2014) High-protein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: the increased luminal bulk connection. Am J Physiol Gastrointest Liver Physiol 307(4):G459–G470. https://doi.org/10.1152/ajpgi.00400.2013

    Article  CAS  PubMed  Google Scholar 

  15. 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. https://doi.org/10.1097/MPG.0b013e3181d75d52

    Article  PubMed  Google Scholar 

  16. 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. https://doi.org/10.3945/jn.109.116822

    Article  CAS  PubMed  Google Scholar 

  17. Hu L, Peng X, Chen H, Yan C, Liu Y, Xu Q, Fang Z, Lin Y, Xu S, Feng B, Li J, Wu D, Che L (2017) Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period. Eur J Nutr 56(4):1753–1765. https://doi.org/10.1007/s00394-016-1223-z

    Article  CAS  PubMed  Google Scholar 

  18. Che L, Hu L, Liu Y, Yan C, Peng X, Xu Q, Wang R, Cheng Y, Chen H, Fang Z, Lin Y, Xu S, Feng B, Chen D, Wu D (2016) Dietary nucleotides supplementation improves the intestinal development and immune function of neonates with intra-uterine growth restriction in a pig model. PLoS One 11(6):e0157314. https://doi.org/10.1371/journal.pone.0157314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lin Y, Bolca S, Vandevijvere S, De Vriese S, Mouratidou T, De Neve M, Polet A, Van Oyen H, Van Camp J, De Backer G, De Henauw S, Huybrechts I (2011) Plant and animal protein intake and its association with overweight and obesity among the Belgian population. Br J Nutr 105(7):1106–1116. https://doi.org/10.1017/S0007114510004642

    Article  CAS  PubMed  Google Scholar 

  20. Richter CK, Skulas-Ray AC, Champagne CM, Kris-Etherton PM (2015) Plant protein and animal proteins: do they differentially affect cardiovascular disease risk? Adv Nutr 6(6):712–728. https://doi.org/10.3945/an.115.009654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhu Y, Lin X, Zhao F, Shi X, Li H, Li Y, Zhu W, Xu X, Li C, Zhou G (2015) Meat, dairy and plant proteins alter bacterial composition of rat gut bacteria. Sci Rep 5:15220. https://doi.org/10.1038/srep15220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sangild PT (2006) Gut responses to enteral nutrition in preterm infants and animals. Exp Biol Med (Maywood) 231(11):1695–1711

    Article  CAS  Google Scholar 

  23. Ferenc K, Pietrzak P, Godlewski MM, Piwowarski J, Kilianczyk R, Guilloteau P, Zabielski R (2014) Intrauterine growth retarded piglet as a model for humans—studies on the perinatal development of the gut structure and function. Reprod Biol 14(1):51–60

    Article  PubMed  Google Scholar 

  24. Su W, Zhang H, Ying Z, Li Y, Zhou L, Wang F, Zhang L, Wang T (2017) Effects of dietary l-methionine supplementation on intestinal integrity and oxidative status in intrauterine growth-retarded weanling piglets. Eur J Nutr. https://doi.org/10.1007/s00394-017-1539-3

    Article  PubMed  Google Scholar 

  25. Peace RM, Campbell J, Polo J, Crenshaw J, Russell L, Moeser A (2011) Spray-dried porcine plasma influences intestinal barrier function, inflammation, and diarrhea in weaned pigs. J Nutr 141(7):1312–1317. https://doi.org/10.3945/jn.110.136796

    Article  CAS  PubMed  Google Scholar 

  26. Che L, Zhan L, Fang Z, Lin Y, Yan T, Wu D (2012) Effects of dietary protein sources on growth performance and immune response of weanling pigs. Livest Sci 148(1–2):1–9. https://doi.org/10.1016/j.livsci.2012.04.019

    Article  Google Scholar 

  27. 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. https://doi.org/10.1017/S0007114513001232

    Article  CAS  PubMed  Google Scholar 

  28. Che L, Thymann T, Bering SB, I LEH-L, 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. https://doi.org/10.1203/PDR.0b013e3181c1b15e

    Article  PubMed  Google Scholar 

  29. Owusu-Asiedu A, Baidoot SK, Nyachoti CM, Marquardt RR (2002) Response of early-weaned pigs to spray-dried porcine or animal plasma-based diets supplemented with egg-yolk antibodies against enterotoxigenic Escherichia coli. J Anim Sci 80(11):2895–2903

    Article  CAS  PubMed  Google Scholar 

  30. Kelly D, O’Brien JJ, McCracken KJ (1990) Effect of creep feeding on the incidence, duration and severity of post-weaning diarrhoea in pigs. Res Vet Sci 49(2):223–228

    Article  CAS  PubMed  Google Scholar 

  31. Mansoori B, Nodeh H, Modirsanei M, Rahbari S, Aparnak P (2009) d-Xylose absorption test: a tool for the assessment of the effect of anticoccidials on the intestinal absorptive capacity of broilers during experimental coccidiosis. Anim Feed Sci Technol 148(2–4):301–308. https://doi.org/10.1016/j.anifeedsci.2008.04.009

    Article  CAS  Google Scholar 

  32. Zhou P, Zhao Y, Zhang P, Li Y, Gui T, Wang J, Jin C, Che L, Li J, Lin Y, Xu S, Feng B, Fang Z, Wu D (2017) Microbial mechanistic insight into the role of inulin in improving maternal health in a pregnant sow model. Front Microbiol 8:2242. https://doi.org/10.3389/fmicb.2017.02242

    Article  PubMed  PubMed Central  Google Scholar 

  33. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. https://doi.org/10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. McDonald D, Clemente JC, Kuczynski J, Rideout JR, Stombaugh J, Wendel D, Wilke A, Huse S, Hufnagle J, Meyer F, Knight R, Caporaso JG (2012) The biological observation matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome. Gigascience 1(1):7. https://doi.org/10.1186/2047-217X-1-7

    Article  PubMed  PubMed Central  Google Scholar 

  35. Rosero DS, Odle J, Moeser AJ, Boyd RD, van Heugten E (2015) Peroxidised dietary lipids impair intestinal function and morphology of the small intestine villi of nursery pigs in a dose-dependent manner. Br J Nutr 114(12):1985–1992. https://doi.org/10.1017/S000711451500392X

    Article  CAS  PubMed  Google Scholar 

  36. Cicalese L, Corsello T, Stevenson HL, Damiano G, Tuveri M, Zorzi D, Montalbano M, Shirafkan A, Rastellini C (2015) Evidence of absorptive function in vivo in a neo-formed bio-artificial intestinal segment using a rodent model. J Gastrointest Surg. https://doi.org/10.1007/s11605-015-2974-1

    Article  Google Scholar 

  37. Chen J, Kang B, Jiang Q, Han M, Zhao Y, Long L, Fu C, Yao K (2018) Alpha-ketoglutarate in low-protein diets for growing pigs: effects on cecal microbial communities and parameters of microbial metabolism. Front Microbiol 9:1057. https://doi.org/10.3389/fmicb.2018.01057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Greenwood PL, Hunt AS, Bell AW (2004) Effects of birth weight and postnatal nutrition on neonatal sheep: IV. Organ growth. J Anim Sci 82(2):422–428

    Article  CAS  PubMed  Google Scholar 

  39. Beaulieu AD, Aalhus JL, Williams NH, Patience JF (2010) Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, carcass quality, muscle composition, and eating quality of pork. J Anim Sci 88(8):2767–2778. https://doi.org/10.2527/jas.2009-2222

    Article  CAS  PubMed  Google Scholar 

  40. Pierce JL, Cromwell GL, Lindemann MD, Russell LE, Weaver EM (2005) Effects of spray-dried animal plasma and immunoglobulins on performance of early weaned pigs. J Anim Sci 83(12):2876–2885. https://doi.org/10.2527/2005.83122876x

    Article  CAS  PubMed  Google Scholar 

  41. Caine WR, Sauer WC, Tamminga S, Verstegen MW, Schulze H (1997) Apparent ileal digestibilities of amino acids in newly weaned pigs fed diets with protease-treated soybean meal. J Anim Sci 75(11):2962–2969

    Article  CAS  PubMed  Google Scholar 

  42. Perez-Bosque A, Miro L, Polo J, Russell L, Campbell J, Weaver E, Crenshaw J, Moreto M (2010) Dietary plasma protein supplements prevent the release of mucosal proinflammatory mediators in intestinal inflammation in rats. J Nutr 140(1):25–30. https://doi.org/10.3945/jn.109.112466

    Article  CAS  PubMed  Google Scholar 

  43. Hedegaard CJ, Strube ML, Hansen MB, Lindved BK, Lihme A, Boye M, Heegaard PM (2016) Natural Pig plasma immunoglobulins have anti-bacterial effects: potential for use as feed supplement for treatment of intestinal infections in pigs. PLoS One 11(1):e0147373. https://doi.org/10.1371/journal.pone.0147373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Jiang R, Chang X, Stoll B, Fan MZ, Arthington J, Weaver E, Campbell J, Burrin DG (2000) Dietary plasma protein reduces small intestinal growth and lamina propria cell density in early weaned pigs. J Nutr 130(1):21–26. https://doi.org/10.1093/jn/130.1.21

    Article  CAS  PubMed  Google Scholar 

  45. Pluske JR, Kim J-C, Hansen CF, Mullan BP, Payne HG, Hampson DJ, Callesen J, Wilson RH (2007) Piglet growth before and after weaning in relation to a qualitative estimate of solid (creep) feed intake during lactation: a pilot study*. Arch Anim Nutr 61(6):469–480. https://doi.org/10.1080/17450390701664249

    Article  PubMed  Google Scholar 

  46. 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. https://doi.org/10.1016/j.clnu.2015.03.002

    Article  PubMed  Google Scholar 

  47. Che L, Xuan Y, Hu L, Liu Y, Xu Q, Fang Z, Lin Y, Xu S, Wu D, Zhang K, Chen D (2015) Effect of postnatal nutrition restriction on the oxidative status of neonates with intrauterine growth restriction in a pig model. Neonatology 107(2):93–99. https://doi.org/10.1159/000368179

    Article  CAS  PubMed  Google Scholar 

  48. Hu L, Peng X, Qin L, Wang R, Fang Z, Lin Y, Xu S, Feng B, Wu D, Che L (2018) Dietary nucleotides supplementation during the suckling period improves the antioxidative ability of neonates with intrauterine growth retardation when using a pig model. RSC Adv 8(29):16152–16160. https://doi.org/10.1039/c8ra00701b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yara S, Lavoie JC, Levy E (2015) Oxidative stress and DNA methylation regulation in the metabolic syndrome. Epigenomics 7(2):283–300. https://doi.org/10.2217/epi.14.84

    Article  CAS  PubMed  Google Scholar 

  50. Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18(10):872–879

    Article  CAS  PubMed  Google Scholar 

  51. El-Sheikh NM, Khalil FA (2011) L-arginine and l-glutamine as immunonutrients and modulating agents for oxidative stress and toxicity induced by sodium nitrite in rats. Food Chem Toxicol 49(4):758–762. https://doi.org/10.1016/j.fct.2010.11.039

    Article  CAS  PubMed  Google Scholar 

  52. Li H, Wan H, Mercier Y, Zhang X, Wu C, Wu X, Tang L, Che L, Lin Y, Xu S, Tian G, Wu D, Fang Z (2014) Changes in plasma amino acid profiles, growth performance and intestinal antioxidant capacity of piglets following increased consumption of methionine as its hydroxy analogue. Br J Nutr 112(6):855–867. https://doi.org/10.1017/S000711451400172X

    Article  CAS  PubMed  Google Scholar 

  53. Wang W, Degroote J, Van Ginneken C, Van Poucke M, Vergauwen H, Dam TM, Vanrompay D, Peelman LJ, De Smet S, Michiels J (2016) Intrauterine growth restriction in neonatal piglets affects small intestinal mucosal permeability and mRNA expression of redox-sensitive genes. FASEB J 30(2):863–873. https://doi.org/10.1096/fj.15-274779

    Article  CAS  PubMed  Google Scholar 

  54. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60. https://doi.org/10.1016/j.phrs.2012.10.020

    Article  CAS  PubMed  Google Scholar 

  55. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55(2):205–211. https://doi.org/10.1136/gut.2005.073817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Li P, Niu Q, Wei Q, Zhang Y, Ma X, Kim SW, Lin M, Huang R (2017) Microbial shifts in the porcine distal gut in response to diets supplemented with Enterococcus faecalis as alternatives to antibiotics. Sci Rep 7:41395. https://doi.org/10.1038/srep41395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S, Tu ZJ, Isaacson RE (2012) Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc Natl Acad Sci USA 109(38):15485–15490. https://doi.org/10.1073/pnas.1205147109

    Article  PubMed  PubMed Central  Google Scholar 

  58. Xie Z, Hu L, Li Y, Geng S, Cheng S, Fu X, Zhao S, Han X (2017) Changes of gut microbiota structure and morphology in weaned piglets treated with fresh fermented soybean meal. World J Microbiol Biotechnol 33(12):213. https://doi.org/10.1007/s11274-017-2374-7

    Article  CAS  PubMed  Google Scholar 

  59. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023. https://doi.org/10.1038/4441022a

    Article  CAS  PubMed  Google Scholar 

  60. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL (2012) IBD—what role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 9(4):219–230. https://doi.org/10.1038/nrgastro.2012.14

    Article  CAS  PubMed  Google Scholar 

  61. Chen L, Xu Y, Chen X, Fang C, Zhao L, Chen F (2017) The maturing development of gut microbiota in commercial piglets during the weaning transition. Front Microbiol 8:1688. https://doi.org/10.3389/fmicb.2017.01688

    Article  PubMed  PubMed Central  Google Scholar 

  62. Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, Arora T, Hallen A, Martens E, Bjorck I, Backhed F (2015) Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab 22(6):971–982. https://doi.org/10.1016/j.cmet.2015.10.001

    Article  CAS  PubMed  Google Scholar 

  63. Molbak L, Thomsen LE, Jensen TK, Bach Knudsen KE, Boye M (2007) Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. J Appl Microbiol 103(5):1853–1867. https://doi.org/10.1111/j.1365-2672.2007.03430.x

    Article  CAS  PubMed  Google Scholar 

  64. Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L (2014) The role of short-chain fatty acids in health and disease. Adv Immunol 121:91–119. https://doi.org/10.1016/B978-0-12-800100-4.00003-9

    Article  CAS  PubMed  Google Scholar 

  65. Correa-Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MA (2016) Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunol 5(4):e73. https://doi.org/10.1038/cti.2016.17

    Article  CAS  Google Scholar 

  66. Kim CH, Park J, Kim M (2014) Gut microbiota-derived short-chain Fatty acids, T cells, and inflammation. Immune Netw 14(6):277–288. https://doi.org/10.4110/in.2014.14.6.277

    Article  PubMed  PubMed Central  Google Scholar 

  67. Castillo M, Martin-Orue SM, Nofrarias M, Manzanilla EG, Gasa J (2007) Changes in caecal microbiota and mucosal morphology of weaned pigs. Vet Microbiol 124(3–4):239–247. https://doi.org/10.1016/j.vetmic.2007.04.026

    Article  CAS  PubMed  Google Scholar 

  68. Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, Mao Y, Zhang X, Pang X, Wei C, Zhao G, Chen Y, Zhao L (2010) Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4(2):232–241. https://doi.org/10.1038/ismej.2009.112

    Article  CAS  PubMed  Google Scholar 

  69. Xu J, Xu C, Chen X, Cai X, Yang S, Sheng Y, Wang T (2014) Regulation of an antioxidant blend on intestinal redox status and major microbiota in early weaned piglets. Nutrition 30(5):584–589. https://doi.org/10.1016/j.nut.2013.10.018

    Article  CAS  PubMed  Google Scholar 

  70. Masanta WO, Heimesaat MM, Bereswill S, Tareen AM, Lugert R, Gross U, Zautner AE (2013) Modification of intestinal microbiota and its consequences for innate immune response in the pathogenesis of campylobacteriosis. Clin Dev Immunol 2013:526860. https://doi.org/10.1155/2013/526860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Schierack P, Walk N, Reiter K, Weyrauch KD, Wieler LH (2007) Composition of intestinal Enterobacteriaceae populations of healthy domestic pigs. Microbiology 153(Pt 11):3830–3837. https://doi.org/10.1099/mic.0.2007/010173-0

    Article  CAS  PubMed  Google Scholar 

  72. Windey K, De Preter V, Verbeke K (2012) Relevance of protein fermentation to gut health. Mol Nutr Food Res 56(1):184–196. https://doi.org/10.1002/mnfr.201100542

    Article  CAS  PubMed  Google Scholar 

  73. Yang H, Huang X, Fang S, He M, Zhao Y, Wu Z, Yang M, Zhang Z, Chen C, Huang L (2017) Unraveling the fecal microbiota and metagenomic functional capacity associated with feed efficiency in pigs. Front Microbiol 8:1555. https://doi.org/10.3389/fmicb.2017.01555

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31101727); the International Cooperation in Science and Technology Project of Sichuan Province (2014HH0034); and the Natural Science Foundation of Sichuan Province (12ZA110).

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The authors’ responsibilities were as follows: LQC, LH, DW and ZFF: designed the research; LH, QZ, XP, YL, JYT and YHL: conducted the research; YL, SYX, BF and JL: analyzed the data; LH: wrote the manuscript; LQC: had primary responsibility for the final contents; and all authors: read and approved the final manuscript.

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Correspondence to Lianqiang Che.

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The use of animals for this research was approved by the Institutional Animal Care and Use Committee of Sichuan Agricultural University.

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Che, L., Hu, L., Zhou, Q. et al. Microbial insight into dietary protein source affects intestinal function of pigs with intrauterine growth retardation. Eur J Nutr 59, 327–344 (2020). https://doi.org/10.1007/s00394-019-01910-z

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