Skip to main content Accessibility help
×
Home
Hostname: page-component-55597f9d44-mzfmx Total loading time: 0.309 Render date: 2022-08-16T10:26:20.382Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

Dietary supplementation of fructo-oligosaccharides alleviates enterotoxigenic E. coli-induced disruption of intestinal epithelium in a weaned piglet model

Published online by Cambridge University Press:  12 November 2021

Yuheng Luo
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Lei Liu
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Daiwen Chen
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Bing Yu
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Ping Zheng
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Xiangbing Mao
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Zhiqing Huang
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Jie Yu
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Junqiu Luo
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Hui Yan
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
Jun He*
Affiliation:
Key Laboratory for Animal Disease-Resistance Nutrition of Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Sichuan Province, Chengdu, 611130, People’s Republic of China
*
*Corresponding author: Dr J. He, fax +86 28 86290922, email hejun8067@163.com

Abstract

Diarrhoea caused by pathogens such as enterotoxigenic E. coli (ETEC) is a serious threat to the health of young animals and human infants. Here, we investigated the protective effect of fructo-oligosaccharides (FOS) on the intestinal epithelium with ETEC challenge in a weaned piglet model. Twenty-four weaned piglets were randomly divided into three groups: (1) non-ETEC-challenged control (CON); (2) ETEC-challenged control (ECON); and (3) ETEC challenge + 2·5 g/kg FOS (EFOS). On day 19, the CON pigs were orally infused with sterile culture, while the ECON and EFOS pigs were orally infused with active ETEC (2·5 × 109 colony-forming units). On day 21, pigs were slaughtered to collect venous blood and small intestine. Result showed that the pre-treatment of FOS improved the antioxidant capacity and the integrity of intestinal barrier in the ETEC-challenged pigs without affecting their growth performance. Specifically, compared with ECON pigs, the level of GSH peroxidase and catalase in the plasma and intestinal mucosa of EFOS pigs was increased (P < 0·05), and the intestinal barrier marked by zonula occluden-1 and plasmatic diamine oxidase was also improved in EFOS pigs. A lower level (P < 0·05) of inflammatory cytokines in the intestinal mucosa of EFOS pigs might be involved in the inhibition of TLR4/MYD88/NF-κB pathway. The apoptosis of jejunal cells in EFOS pigs was also lower than that in ECON pigs (P < 0·05). Our findings provide convincing evidence of possible prebiotic and protective effect of FOS on the maintenance of intestinal epithelial function under the attack of pathogens.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work

References

Nagy, B & Fekete, PZ (2005) Enterotoxigenic Escherichia coli in veterinary medicine. Int J Med Microbiol 295, 443454.CrossRefGoogle ScholarPubMed
Rhouma, M, Fairbrother, JM, Beaudry, F, et al. (2017) Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Vet Scand 59, 31.CrossRefGoogle ScholarPubMed
Bhandari, SK, Xu, B, Nyachoti, CM, et al. (2008) Evaluation of alternatives to antibiotics using an Escherichia coli K88+ model of piglet diarrhea: effects on gut microbial ecology1. J Anim Sci 86, 836847.CrossRefGoogle Scholar
Burkey, TE, Skjolaas, K & Minton, J (2009) Board-invited review: porcine mucosal immunity of the gastrointestinal tract. J Anim Sci 87, 14931501.CrossRefGoogle ScholarPubMed
Owusu-Asiedu, A, Nyachoti, C & Marquardt, R (2003) Response of early-weaned pigs to an enterotoxigenic Escherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody, zinc oxide, fumaric acid, or antibiotic. J Anim Sci 81, 17901798.CrossRefGoogle ScholarPubMed
Kiarie, E, Bhandari, S, Scott, M, et al. (2011) Growth performance and gastrointestinal microbial ecology responses of piglets receiving Saccharomyces cerevisiae fermentation products after an oral challenge with Escherichia coli (K88). J Anim Sci 89, 10621078.CrossRefGoogle Scholar
Thacker, PA (2003) Alternatives to antibiotics as growth promoters for use in swine production: a review. J Anim Sci Biotechnol 4, 35.CrossRefGoogle Scholar
Bornet, F, Brouns, F, Tashiro, Y, et al. (2002) Nutritional aspects of short-chain fructooligosaccharides: natural occurrence, chemistry, physiology and health implications. Dig Liver Dis 34, S111S120.CrossRefGoogle ScholarPubMed
Nishizawa-Yokoi, A, Yabuta, Y & Shigeoka, S (2008) The contribution of carbohydrates including raffinose family oligosaccharides and sugar alcohols to protection of plant cells from oxidative damage. Plant Signaling Behav 3, 10161018.CrossRefGoogle ScholarPubMed
Le Bourgot, C, Ferret-Bernard, S, Blat, S, et al. (2016) Short-chain fructooligosaccharide supplementation during gestation and lactation or after weaning differentially impacts pig growth and IgA response to influenza vaccination. J Funct Foods 24, 307315.CrossRefGoogle Scholar
Sabater-Molina, M, Larqué, E, Torrella, F, et al. (2009) Dietary fructooligosaccharides and potential benefits on health. J Physiol Biochem 65, 315328.CrossRefGoogle ScholarPubMed
Schokker, D, Fledderus, J, Jansen, R, et al. (2018) Supplementation of fructooligosaccharides to suckling piglets affects intestinal microbiota colonization and immune development. J Anim Sci 96, 21392153.CrossRefGoogle ScholarPubMed
Gao, F, Jiang, Y, Zhou, G, et al. (2001) Effect of fructooligosaccharides (FOS) on growth, metabolism and immune in weaning piglets. China Anim Husb Vet Med 33, 8–9.Google Scholar
Oswald, IP (2006) Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet Res 37, 359368.CrossRefGoogle ScholarPubMed
Pié, S, Lallès, JP, Blazy, F, et al. (2004) Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr 134, 641647.CrossRefGoogle ScholarPubMed
Nyachoti, C, Kiarie, E, Bhandari, S, et al. (2012) Weaned pig responses to Escherichia coli K88 oral challenge when receiving a lysozyme supplement. J Anim Sci 90, 252260.CrossRefGoogle ScholarPubMed
Bosi, P, Casini, L, Finamore, A, et al. (2004) Spray- dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. J Anim Sci 82, 17641772.CrossRefGoogle ScholarPubMed
Csernus, B & Czeglédi, L (2020) Physiological, antimicrobial, intestine morphological, and immunological effects of fructooligosaccharides in pigs. Arch Anim Breed 63, 325335.CrossRefGoogle ScholarPubMed
Kraemer, JG, Ramette, A, Aebi, S, et al. (2018) Influence of pig farming on the human nasal microbiota: key role of airborne microbial communities. Appl Environ Microbiol 84, e02470e02417.CrossRefGoogle ScholarPubMed
Liu, L, Chen, D, Yu, B, et al. (2020) Fructooligosaccharides improve growth performance and intestinal epithelium function in weaned pigs exposed to enterotoxigenic Escherichia coli . Food Funct 11, 95999612.CrossRefGoogle ScholarPubMed
National Research Council (2012) Nutrient Requirements of Swine, 11th ed. Washington, DC: National Academies Press.Google Scholar
Xiao, D, Wang, Y, Liu, G, et al. (2014) Effects of chitosan on intestinal inflammation in weaned pigs challenged by enterotoxigenic Escherichia coli . PLOS ONE 9, e104192.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248254.CrossRefGoogle ScholarPubMed
Liu, L, Wu, C, Chen, D, et al. (2020) Selenium-enriched yeast alleviates oxidative stress-induced intestinal mucosa disruption in weaned pigs. Oxid Med Cell Longevity 2020, 111.Google ScholarPubMed
Wan, J, Zhang, J, Chen, D, et al. (2018) Alginate oligosaccharide enhances intestinal integrity of weaned pigs through altering intestinal inflammatory responses and antioxidant status. RSC Adv 8, 1348213492.CrossRefGoogle ScholarPubMed
Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.CrossRefGoogle Scholar
Bolzán, AD, Bianchi, MS & Bianchi, NO (1997) Superoxide dismutase, catalase and glutathione peroxidase activities in human blood: influence of sex, age and cigarette smoking. Clin Biochem 30, 449454.CrossRefGoogle ScholarPubMed
Lightfoot, TJ, Skibola, CF, Smith, AG, et al. (2006) Polymorphisms in the oxidative stress genes, superoxide dismutase, glutathione peroxidase and catalase and risk of non-Hodgkin’s lymphoma. Haematologica 91, 12221227.Google ScholarPubMed
Yang, C, Ferket, P, Hong, Q, et al. (2012) Effect of chito-oligosaccharide on growth performance, intestinal barrier function, intestinal morphology and cecal microflora in weaned pigs. J Anim Sci 90, 26712676.CrossRefGoogle ScholarPubMed
Kim, Y-M, Pae, H-O, Park, JE, et al. (2011) Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signaling 14, 137167.CrossRefGoogle ScholarPubMed
Luo, Q, Kumar, P, Vickers, TJ, et al. (2013) Enterotoxigenic Escherichia coli secretes a highly conserved mucin-degrading metalloprotease to effectively engage intestinal epithelial cells. Infect Immun 82, 509521.CrossRefGoogle ScholarPubMed
Gao, Y, Han, F, Huang, X, et al. (2013) Changes in gut microbial populations, intestinal morphology, expression of tight junction proteins, and cytokine production between two pig breeds after challenge with Escherichia coli K88: a comparative study. J Anim Sci 91, 56145625.CrossRefGoogle ScholarPubMed
Tang, Y, Tan, B, Xiong, X, et al. (2015) Methionine deficiency reduces autophagy and accelerates death in intestinal epithelial cells infected with enterotoxigenic Escherichia coli . Amino Acids 47, 21992204.CrossRefGoogle ScholarPubMed
Dokladny, K, Zuhl, MN & Moseley, PL (2016) Intestinal epithelial barrier function and tight junction proteins with heat and exercise. J Appl Physiol 120, 692701.CrossRefGoogle ScholarPubMed
Fanning, AS, Jameson, BJ, Jesaitis, LA, et al. (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273, 2974529753.CrossRefGoogle ScholarPubMed
Maria Paola, A-C & Autuori, F (2018) Localization of Diamine Oxidase in Animal Tissues. Structure and Functions of Amine Oxidases. Boca Raton, FL: CRC Press.Google Scholar
Thompson, JS, Vaughan, W, Forst, C, et al. (1987) The effect of the route of nutrient delivery on gut structure and diamine oxidase levels. J Parenter Enteral Nutr 11, 2832.CrossRefGoogle ScholarPubMed
Vereecke, L, Beyaert, R & van Loo, G (2011) Enterocyte death and intestinal barrier maintenance in homeostasis and disease. Trends Mol Med 17, 584593.CrossRefGoogle ScholarPubMed
Fujimoto, K, Iwakiri, R, Wu, B, et al. (2002) Homeostasis in the small intestinal mucosa balanced between cell proliferation and apoptosis is regulated partly by the central nervous system. J Gastroenterol 37, 139144.CrossRefGoogle ScholarPubMed
Bernstein, H, Holubec, H, Warneke, JA, et al. (2002) Patchy field defects of apoptosis resistance and dedifferentiation in flat mucosa of colon resections from colon cancer patients. Ann Surg Oncol 9, 505517.CrossRefGoogle ScholarPubMed
Souza, HS, Tortori, CJ, Castelo-Branco, MT, et al. (2005) Apoptosis in the intestinal mucosa of patients with inflammatory bowel disease: evidence of altered expression of FasL and perforin cytotoxic pathways. Int J Colorectal Dis 20, 277286.CrossRefGoogle ScholarPubMed
Ren, W, Yin, J, Chen, S, et al. (2016) Proteome analysis for the global proteins in the jejunum tissues of enterotoxigenic Escherichia coli-infected piglets. Sci Rep 6, 19.Google ScholarPubMed
Xia, Y, Bin, P, Liu, S, et al. (2018) Enterotoxigenic Escherichia coli infection promotes apoptosis in piglets. Microb Pathog 125, 290294.CrossRefGoogle ScholarPubMed
Neuzil, J, Wang, X-F, Dong, L-F, et al. (2006) Molecular mechanism of ‘mitocan’-induced apoptosis in cancer cells epitomizes the multiple roles of reactive oxygen species and Bcl-2 family proteins. FEBS Lett 580, 51255129.CrossRefGoogle ScholarPubMed
Yuan, Z, Liu, S, Yao, J, et al. (2016) Expression of Bcl-2 genes in channel catfish after bacterial infection and hypoxia stress. Dev Comp Immunol 65, 7990.CrossRefGoogle ScholarPubMed
Budihardjo, I, Oliver, H, Lutter, M, et al. (1999) Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15, 269290.CrossRefGoogle ScholarPubMed
Riedl, SJ & Shi, Y (2004) Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5, 897907.CrossRefGoogle ScholarPubMed
Sabroe, I, Parker, LC, Dower, SK, et al. (2008) The role of TLR activation in inflammation. J Pathol 214, 126135.CrossRefGoogle ScholarPubMed
Pomorska-Mo, M & Markowska-Daniel, I (2011) Porcine cathelicidins and defensins. Med Weter 67, 2024.Google Scholar
Le Bourgot, C, Ferret-Bernard, S, Apper, E, et al. (2019) Perinatal short-chain fructooligosaccharides program intestinal microbiota and improve enteroinsular axis function and inflammatory status in high-fat diet-fed adult pigs. FASEB J 33, 301313.CrossRefGoogle ScholarPubMed
Le Bourgot, C, Le Normand, L, Formal, M, et al. (2017) Maternal short-chain fructo-oligosaccharide supplementation increases intestinal cytokine secretion, goblet cell number, butyrate concentration and Lawsonia intracellularis humoral vaccine response in weaned pigs. Br J Nutr 117, 8392.CrossRefGoogle ScholarPubMed
Scholtens, PA, Alliet, P, Raes, M, et al. (2008) Fecal secretory immunoglobulin A is increased in healthy infants who receive a formula with short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides. J Nutr 138, 11411147.CrossRefGoogle ScholarPubMed
Che, T, Song, M, Liu, Y, et al. (2012) Mannan oligosaccharide increases serum concentrations of antibodies and inflammatory mediators in weanling pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J Anim Sci 90, 27842793.CrossRefGoogle ScholarPubMed
Supplementary material: File

Luo et al. supplementary material

Tables S1-S2

Download Luo et al. supplementary material(File)
File 19 KB

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Dietary supplementation of fructo-oligosaccharides alleviates enterotoxigenic E. coli-induced disruption of intestinal epithelium in a weaned piglet model
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Dietary supplementation of fructo-oligosaccharides alleviates enterotoxigenic E. coli-induced disruption of intestinal epithelium in a weaned piglet model
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Dietary supplementation of fructo-oligosaccharides alleviates enterotoxigenic E. coli-induced disruption of intestinal epithelium in a weaned piglet model
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *