Top

Published in:

01-02-2020 | Diarrhea | Original Contribution

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

Authors: Lianqiang Che, Liang Hu, Qiang Zhou, Xie Peng, Yang Liu, Yuheng Luo, Zhengfeng Fang, Yan Lin, Shengyu Xu, Bin Feng, Jian Li, Jiayong Tang, De Wu

Published in: European Journal of Nutrition | Issue 1/2020

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 Escherichia–Shigella, 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.

Available only for authorised users

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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):60–66CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

22.

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

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):51–60CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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):2895–2903CrossRefPubMed

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):223–228CrossRefPubMed

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 CrossRef

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMedPubMedCentral

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):422–428CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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):2962–2969CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

50.

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

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

Title: Microbial insight into dietary protein source affects intestinal function of pigs with intrauterine growth retardation
Authors: Lianqiang Che
Liang Hu
Qiang Zhou
Xie Peng
Yang Liu
Yuheng Luo
Zhengfeng Fang
Yan Lin
Shengyu Xu
Bin Feng
Jian Li
Jiayong Tang
De Wu
Publication date: 01-02-2020
Publisher: Springer Berlin Heidelberg
Keywords: Diarrhea
Respiratory Microbiota
Diarrhea
Published in: European Journal of Nutrition / Issue 1/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-019-01910-z

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

Illustration of figure on mountain summit/© Orapun / Stock.adobe.com, STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2020

Evaluation of the efficacy of Lactobacillus plantarum HEAL9 and Lactobacillus paracasei 8700:2 on aspects of common cold infections in children attending day care: a randomised, double-blind, placebo-controlled clinical study

Chronic consumption of the dietary polyphenol chrysin attenuates metabolic disease in fructose-fed rats

Prudent dietary pattern influences homocysteine level more than folate, vitamin B12, and docosahexaenoic acid: a structural equation model approach

Magnesium and health outcomes: an umbrella review of systematic reviews and meta-analyses of observational and intervention studies

Relationship between sensory liking for fat, sweet or salt and cardiometabolic diseases: mediating effects of diet and weight status

An inverse association between the Mediterranean diet and bladder cancer risk: a pooled analysis of 13 cohort studies

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage