barrier function; citrus pulp; gut morphology; inflammation; intestinal health; inulin; metabolites; microbiota; Food Science; Endocrinology, Diabetes and Metabolism; Nutrition and Dietetics
Abstract :
[en] We investigated the use of citrus pulp (CP) as a novel prebiotic capable of exerting microbiota and immunomodulating capacities to alleviate weaning stress. Inulin (IN), a well-known prebiotic, was used for comparison. Hundred and 28 male weaned piglets of 21 days old were assigned to 32 pens of 4 piglets each. Piglets were assigned to one of the four treatments, i.e., control, IN supplemented at 0.2% (IN0.2%), and CP supplemented either at 0.2% (CP0.2%) or at 2% (CP2%). On d10-11 and d31-32 post-weaning, one pig per pen was euthanized for intestinal sampling to evaluate the growth performance, chyme characteristics, small intestinal morphology, colonic inflammatory response and barrier integrity, metabolite profiles [gas chromatography-mass spectrometry (GC-MS), and liquid chromatography-mass spectrometry (LC-MS)], and microbial populations. The IN treatment and the two CP treatments induced higher small intestinal villus height to crypt depth ratios in comparison with the control diet at both sampling times. All treatments decreased acidic goblet cell absolute counts in the crypts in comparison to the control diet of the duodenum on d10-11 and d31-32. The gene expression of β-defensin 2 was downregulated in colonic tissues following the IN and CP2% inclusion on d31-32. On d31-32, piglets fed with IN and CP0.2% showed lower mRNA levels of occludin and claudin-3, respectively. Not surprisingly, flavonoids were observed in the colon in the CP treatments. Increased colonic acetate proportions on d10-11, at the expense of branched-chain fatty acid (BCFA) levels, were observed following the CP2% supplementation compared to the control diet, inferring a reduction of proteolytic fermentation in the hindgut. The beneficial microbial community Faecalibacterium spp. was promoted in the colon of piglets fed with CP2% on d10-11 (p = 0.04; false discovery rate (FDR) non-significant) and on d31-32 (p = 0.03; FDR non-significant) in comparison with the control diet. Additionally, on d31-32, CP2% increased the relative abundance of Megasphaera spp. compared to control values (p = 0.03; FDR non-significant). In conclusion, CP2% promoted the growth of beneficial bacterial communities in both post-weaning time points, modulating colonic fermentation patterns in the colon. The effects of CP supplementation were similar to those of IN and showed the potential as a beneficial feed supplement to alleviate weaning stress.
Disciplines :
Agriculture & agronomy
Author, co-author :
Uerlings, Julie ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition ; Research Foundation for Industry and Agriculture, National Scientific Research Foundation (FRIA-FNRS), Brussels, Belgium
Arevalo Sureda, Ester ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition
Kroeske, Kikianne ; Université de Liège - ULiège > TERRA Research Centre ; Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Melle, Belgium
Tanghe, Sofie; Royal Agrifirm Group, Apeldoorn, Netherlands
De Vos, Maartje; Royal Agrifirm Group, Apeldoorn, Netherlands
Bruggeman, Geert; Royal Agrifirm Group, Apeldoorn, Netherlands
Wavreille, José ; Université de Liège - ULiège > Département GxABT
Bindelle, Jérôme ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition
Purcaro, Giorgia ; Université de Liège - ULiège > TERRA Research Centre > Chimie des agro-biosystèmes
Everaert, Nadia ; Université de Liège - ULiège > Département GxABT ; Animal and Human Health Engineering, Department of Biosystems, Katholieke Universiteit Leuven, Heverlee, Belgium
Language :
English
Title :
Impact of Citrus Pulp or Inulin on Intestinal Microbiota and Metabolites, Barrier, and Immune Function of Weaned Piglets.
ID33848511), and the Fonds de la Recherche Scientifique-FNRS (Grant No. 31248729).This work was supported by the Research Foundation for Industry and Agriculture, FRIA-FNRS, Belgium (Grant No.
Everaert N Van Cruchten S Weström B Bailey M Van Ginneken C Thymann T et al. review on early gut maturation and colonization in pigs, including biological and dietary factors affecting gut homeostasis. Anim Feed Sci Technol. (2017) 233:89–103. 10.1016/j.anifeedsci.2017.06.011
Campbell JM Crenshaw JD Polo J. The biological stress of early weaned piglets. J Anim Sci Biotechnol. (2013) 4:19. 10.1186/2049-1891-4-19
Dong GZ Pluske JR. The low feed intake in newly-weaned pigs: problems and possible solutions. Asian-Australasian J Anim Sci. (2007) 20:440–52. 10.5713/ajas.2007.440
Weström BR Arévalo Sureda E Pierzynowska K Pierzynowski SG Pérez-Cano FJ. The immature gut barrier and its importance in establishing immunity in newborn mammals. Front Immunol. (2020) 11:153. 10.3389/fimmu.2020.01153
Lallès JP Bosi P Smidt H Stokes CR. Weaning - A challenge to gut physiologists. Livest Sci. (2007) 108:82–93. 10.1016/j.livsci.2007.01.091
Moeser AJ Pohl CS Rajput M. Weaning stress and gastrointestinal barrier development: implications for lifelong gut health in pigs. Anim Nutr. (2017) 3:313–21. 10.1016/j.aninu.2017.06.003
Pié S Lallès JP Blazy F Laffitte J Sève B Oswald IP. Weaning is associated with an upregulation of expression of inflamatory cytokines in the intestine of piglets. J Nutr. (2004) 134:641–7. 10.1093/jn/134.3.641
Pluske JR Hampson DJ Williams IH. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest Prod Sci. (1997) 51:215–36. 10.1016/S0301-6226(97)00057-2
Boudry G Péron V Le Huërou-Luron I Lallès JP Sève B. Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J. Nutri. (2004) 13:2256–62. 10.1093/jn/134.9.2256
Moeser AJ Klok C. Vander, Ryan KA, Wooten JG, Little D, Cook VL, Blikslager AT. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am J Physiol - Gastrointest Liver Physiol. (2007) 292:G173–81. 10.1152/ajpgi.00197.2006
Hu CH Xiao K Luan ZS Song J. Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs. J Anim Sci. (2013) 91:1094–101. 10.2527/jas.2012-5796
Stokes CR Bailey M Haverson K Harris C Jones P Inman C Pié S Oswald IP Williams BA Akkermans ADL et al. Postnatal development of intestinal immune system in piglets: Implications for the process of weaning. Anim Res. (2004) 53:325–34. 10.1051/animres:2004020
Bailey M Haverson K Inman C Harris C Jones P Corfield G et al. The development of the mucosal immune system pre- and post-weaning: balancing regulatory and effector function. Proc Nutr Soc. (2005) 64:451–7. 10.1079/PNS2005452
Konstantinov SR Awati AA Williams BA Miller BG Jones P Stokes CR et al. Post-natal development of the porcine microbiota composition and activities. Environ Microbiol. (2006) 8:1191–9. 10.1111/j.1462-2920.2006.01009.x
Heo JM Opapeju FO Pluske JR Kim JC Hampson DJ Nyachoti CM. Gastrointestinal health and function in weaned pigs: A review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr. (2013) 97:207–37. 10.1111/j.1439-0396.2012.01284.x
Flis M Sobotka W Antoszkiewicz Z. Fiber substrates in the nutrition of weaned piglets—a review. Ann Anim Sci. (2017) 17:627–43. 10.1515/aoas-2016-0077
Molist F van Oostrum M Pérez JF Mateos GG Nyachoti CM van der Aar PJ. Relevance of functional properties of dietary fibre in diets for weanling pigs. Anim Feed Sci Technol. (2014) 189:1–10. 10.1016/j.anifeedsci.2013.12.013
Rist VTS Weiss E Eklund M Mosenthin R. Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review. Animal. (2013) 7:1067–78. 10.1017/S1751731113000062
Gibson GR Probert HM Loo J. Van, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. (2004) 17:259–75. 10.1079/NRR200479
Roberfroid M. Prebiotics: the concept revisited. J Nutri. (2003) 137:830–837. 10.1093/jn/137.3.830S
Bampidis VA Robinson PH. Citrus by-products as ruminant feeds: a review. Anim Feed Sci Technol. (2006) 128:175–217. 10.1016/j.anifeedsci.2005.12.002
Wadhwa M Bakshi SPM. Utilization of fruit and vegetable wastes as livestock feed and as substrates for generation of other value-added products. (2013). Available online at: http://www.fao.org.webtranslate-widget.systransoft.com/docrep/018/i3273e/i3273e.pdf
Olano-Martin E Gibson GR Rastall RA. Comparison of the in vitro bifidogenic properties of pectins and pectic-oligosaccharides. J Appl Microbiol. (2002) 93:505–11. 10.1046/j.1365-2672.2002.01719.x
Tian L Bruggeman G van den Berg M Borewicz K Scheurink AJW Bruininx E et al. Effects of pectin on fermentation characteristics, carbohydrate utilization, and microbial community composition in the gastrointestinal tract of weaning pigs. Mol Nutr Food Res. (2017) 61:186. 10.1002/mnfr.201600186
Almeida V V Nuñez AJC Schinckel AP Alvarenga PVA Castelini FR Silva-Guillen Y V et al. Interactive effect of dietary protein and dried citrus pulp levels on growth performance, small intestinal morphology, and hindgut fermentation of weanling pigs. J Anim Sci. (2017) 95:257–69. 10.2527/jas.2016.0498
Weber TE Ziemer CJ Kerr BJ. Effects of adding fibrous feedstuffs to the diet of young pigs on growth performance, intestinal cytokines, and circulating acute-phase proteins. J Anim Sci. (2008) 86:871–81. 10.2527/jas.2007-0330
Brambillasca S Zunino P Cajarville C. Addition of inulin, alfalfa and citrus pulp in diets for piglets: Influence on nutritional and faecal parameters, intestinal organs, and colonic fermentation and bacterial populations. Livest Sci. (2015) 178:243–50. 10.1016/j.livsci.2015.06.003
Van Waes C Baert J Carlier L Van Bockstaele E. A rapid determination of the total sugar content and the average inulin chain length in roots of chicory (Cichorium intybus L). J Sci Food Agric. (1998) 76:107–110. 10.1002/(SICI)1097-0010(199801)76:1<107::AID-JSFA911>3.0.CO;2-6
Samanta AK Jayapal N Senani S Kolte AP Sridhar M. Prebiotic inulin: Useful dietary adjuncts to manipulate the livestock gut microflora. Brazilian J Microbiol. (2013) 44:1–14. 10.1590/S1517-83822013005000023
Kozłowska I Marć-Pieńkowska J Bednarczyk M. 2. Beneficial aspects of inulin supplementation as a fructooligosaccharide prebiotic in monogastric animal nutrition. a review. Ann Anim Sci. (2016) 16:315–31. 10.1515/aoas-2015-0090
Christoforidou Z Mora Ortiz M Poveda C Abbas M Walton G Bailey M et al. Sexual dimorphism in immune development and in response to nutritional intervention in neonatal piglets. Front Immunol. (2019) 10:2705. 10.3389/fimmu.2019.02705
Zhao W Yuan M Li P Yan H Zhang H Liu J. Short-chain fructo-oligosaccharides enhances intestinal barrier function by attenuating mucosa inflammation and altering colonic microbiota composition of weaning piglets. Ital J Anim Sci. (2019) 18:976–86. 10.1080/1828051X.2019.1612286
Chang M Zhao Y Qin G Zhang X. Fructo-oligosaccharide alleviates soybean-induced anaphylaxis in piglets by modulating gut microbes. Front Microbiol. (2018) 9:769. 10.3389/fmicb.2018.02769
Metzler-Zebeli BU Trevisi P Prates JAM Tanghe S Bosi P Canibe N et al. Assessing the effect of dietary inulin supplementation on gastrointestinal fermentation, digestibility and growth in pigs: a meta-analysis. Anim Feed Sci Technol. (2017) 233:120–32. 10.1016/j.anifeedsci.2017.05.010
Uerlings J Schroyen M Bautil AA Courtin C Richel A Sureda EAEA et al. In vitro prebiotic potential of agricultural by-products on intestinal fermentation, gut barrier and inflammatory status of piglets. Br J Nutr. (2020) 123:293–307. 10.1017/S0007114519002873
Bach Knudsen KE Lærke HN Ingerslev AK Hedemann MS Nielsen TS Theil PK et al. Carbohydrates in pig nutrition—recent advances. J Anim Sci. (2016) 94:1–11. 10.2527/jas.2015-9785
Andersen CL Jensen JL Ørntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. (2004) 64:5245–50. 10.1158/0008-5472.CAN-04-0496
Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. (2001) 29:E45. 10.1093/nar/29.9.e45
Leblois J Massart S Li B Wavreille J Bindelle J Everaert N. Modulation of piglets' microbiota: Differential effects by a high wheat bran maternal diet during gestation and lactation. Sci Rep. (2017) 7:2. 10.1038/s41598-017-07228-2
Eberts TJ Sample RHB Glick MR Ellis GH. A simplified, colorimetric micromethod for xylose in serum or urine, with phloroglucinol. Clin Chem. (1979) 25:1440–3. 10.1093/clinchem/25.8.1440
Scheubert K Hufsky F Petras D Wang M Nothias LF Dührkop K et al. Significance estimation for large scale metabolomics annotations by spectral matching. Nat Commun. (2017) 8:1494. 10.1038/s41467-017-01318-5
Uerlings J Bindelle J Schroyen M Richel A Bruggeman G Willems E et al. Fermentation capacities of fructan- and pectin-rich by-products and purified fractions via an in vitro piglet faecal model. J Sci Food Agric. (2019) 99:5720–33. 10.1002/jsfa.9837
Li B Schroyen M Leblois J Wavreille J Soyeurt H Bindelle J et al. Effects of inulin supplementation to piglets in the suckling period on growth performance, postileal microbial and immunological traits in the suckling period and three weeks after weaning. Arch Anim Nutr. (2018) 72:425–42. 10.1080/1745039X.2018.1508975
Corfield AP. Mucins: A biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta Gen Subj. (2015) 1850:236–52. 10.1016/j.bbagen.2014.05.003
Hedemann MS Eskildsen M Lærke HN Pedersen C Lindberg JE Laurinen P et al. Intestinal morphology and enzymatic activity in newly weaned pigs fed contrasting fiber concentrations and fiber properties. J Anim Sci. (2006) 84:1375–86. 10.2527/2006.8461375x
Swiech E Tuśnio A Taciak M Boryczka M Buraczewska L. The effects of pectin and rye on amino acid ileal digestibility, threonine metabolism, nitrogen retention, and morphology of the small intestine in young pigs. J Anim Feed Sci. (2012) 21:89–106. 10.22358/jafs/66055/2012
Uerlings J Schroyen M Willems E Tanghe S Bruggeman G Bindelle J et al. Differential effects of inulin or its fermentation metabolites on gut barrier and immune function of porcine intestinal epithelial cells. J Funct Foods. (2020) 67:103855. 10.1016/j.jff.2020.103855
Branner GR Böhmer BM Erhardt W Henke J Roth-Maier DA. Investigation on the precaecal and faecal digestibility of lactulose and inulin and their influence on nutrient digestibility and microbial characteristics. Arch Anim Nutr. (2004) 58:353–66. 10.1080/00039420400005075
Chen K Chen H Faas MM de Haan BJ Li J Xiao P Zhang H et al. Specific inulin-type fructan fibers protect against autoimmune diabetes by modulating gut immunity, barrier function, and microbiota homeostasis. Mol Nutr Food Res. (2017) 61:1601006. 10.1002/mnfr.201601006
Moset V Piquer O Cervera C Fernández CJ Hernández P Cerisuelo A. Ensiled citrus pulp as a by-product feedstuff for finishing pigs: Nutritional value and effects on intestinal microflora and carcass quality. Spanish J Agric Res. (2015) 13:e0607. 10.5424/sjar/2015133-6717
Pascoal LAF Thomaz MC Watanabe PH Ruiz U. dos S, Amorim AB, Daniel E, da Silva SZ. Purified cellulose, soybean hulls and citrus pulp as a source of fiber for weaned piglets. Sci Agric. (2015) 72:400–10. 10.1590/0103-9016-2014-0210
Zacharias B Kerler A Drochner W. The influence of 5% and 10% dietary apple pectin on parameters of fermentation in faeces and caecal digesta of weaning pigs. Arch Anim Nutr. (2004) 58:149–56. 10.1080/00039420410001667502
Harapu CD Miron A Cuciureanu M Cuciureanu R. [Flavonoids–bioactive compounds in fruits juice]. Rev medico-chirurgicalǎ a Soc Medici şi Nat din Iaşi. (2010) 114:1209–14.
Moran AW Al-Rammahi MA Arora DK Batchelor DJ Coulter EA Daly K et al. Expression of Na+/glucose co-transporter 1 (SGLT1) is enhanced by supplementation of the diet of weaning piglets with artificial sweeteners. Br J Nutr. (2010) 104:637–46. 10.1017/S0007114510000917
Daly K Darby AC Hall N Nau A Bravo D Shirazi-Beechey SP. Dietary supplementation with lactose or artificial sweetener enhances swine gut Lactobacillus population abundance. Br J Nutr. (2014) 111:S30–5. 10.1017/S0007114513002274
Bang SJ Kim G Lim MY Song EJ Jung DH Kum JS et al. Do, Park CS, Seo DH. The influence of in vitro pectin fermentation on the human fecal microbiome. AMB Express. (2018) 8:98. 10.1186/s13568-018-0629-9
Biddle A Stewart L Blanchard J Leschine S. Untangling the genetic basis of fibrolytic specialization by lachnospiraceae and ruminococcaceae in diverse gut communities. Diversity. (2013) 5:627–40. 10.3390/d5030627
Lopez-Siles M Khan TM Duncan SH Harmsen HJM Garcia-Gil LJ Flint HJ. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol. (2012) 78:420–8. 10.1128/AEM.06858-11
Chung WSF Meijerink M Zeuner B Holck J Louis P Meyer AS et al. Prebiotic potential of pectin and pectic oligosaccharides to promote anti-inflammatory commensal bacteria in the human colon. FEMS Microbiol Ecol. (2017) 93:127. 10.1093/femsec/fix127
Furumoto H Nanthirudjanar T Kume T Izumi Y Park SB Kitamura N et al. 10-Oxo-trans-11-octadecenoic acid generated from linoleic acid by a gut lactic acid bacterium Lactobacillus plantarum is cytoprotective against oxidative stress. Toxicol Appl Pharmacol. (2016) 296:1–9. 10.1016/j.taap.2016.02.012
Geng S Cheng S Li Y Wen Z Ma X Jiang X et al. Faecal Microbiota Transplantation Reduces Susceptibility to Epithelial Injury and Modulates Tryptophan Metabolism of the Microbial Community in a Piglet Model. J Crohn's Colitis. (2018) 12:1359–74. 10.1093/ecco-jcc/jjy103
De Juan A Segura E. Modulation of Immune Responses by Nutritional Ligands of Aryl Hydrocarbon Receptor. Front Immunol. (2021) 12:645168. 10.3389/fimmu.2021.645168
Ma N He T Johnston LJ Ma X. Host–microbiome interactions: the aryl hydrocarbon receptor as a critical node in tryptophan metabolites to brain signaling. Gut Microbes. (2020) 11:1203–19. 10.1080/19490976.2020.1758008
Ye Y Wu J Quan J Ding R Yang M Wang X et al. Lipids and organic acids in three gut locations affect feed efficiency of commercial pigs as revealed by LC–MS-based metabolomics. Sci Rep. (2021) 11:8. 10.1038/s41598-021-87322-8
