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Early intervention with faecal microbiota transplantation: an effective means to improve growth performance and the intestinal development of suckling piglets

  • C. S. Cheng (a1), H. K. Wei (a1) (a2), P. Wang (a1), H. C. Yu (a1), X. M. Zhang (a1), S. W. Jiang (a3) (a4) (a2) and J. Peng (a1) (a2)...
Abstract

Recent studies indicate that early postnatal period is a critical window for gut microbiota manipulation to optimise the immunity and body growth. This study investigated the effects of maternal faecal microbiota orally administered to neonatal piglets after birth on growth performance, selected microbial populations, intestinal permeability and the development of intestinal mucosal immune system. In total, 12 litters of crossbred newborn piglets were selected in this study. Litter size was standardised to 10 piglets. On day 1, 10 piglets in each litter were randomly allotted to the faecal microbiota transplantation (FMT) and control groups. Piglets in the FMT group were orally administrated with 2ml faecal suspension of their nursing sow per day from the age of 1 to 3 days; piglets in the control group were treated with the same dose of a placebo (0.1M potassium phosphate buffer containing 10% glycerol (vol/vol)) inoculant. The experiment lasted 21 days. On days 7, 14 and 21, plasma and faecal samples were collected for the analysis of growth-related hormones and cytokines in plasma and lipocalin-2, secretory immunoglobulin A (sIgA), selected microbiota and short-chain fatty acids (SCFAs) in faeces. Faecal microbiota transplantation increased the average daily gain of piglets during week 3 and the whole experiment period. Compared with the control group, the FMT group had increased concentrations of plasma growth hormone and IGF-1 on days 14 and 21. Faecal microbiota transplantation also reduced the incidence of diarrhoea during weeks 1 and 3 and plasma concentrations of zonulin, endotoxin and diamine oxidase activities in piglets on days 7 and 14. The populations of Lactobacillus spp. and Faecalibacterium prausnitzii and the concentrations of faecal and plasma acetate, butyrate and total SCFAs in FMT group were higher than those in the control group on day 21. Moreover, the FMT piglets have higher concentrations of plasma transforming growth factor-β and immunoglobulin G, and faecal sIgA than the control piglets on day 21. These findings indicate that early intervention with maternal faecal microbiota improves growth performance, decreases intestinal permeability, stimulates sIgA secretion, and modulates gut microbiota composition and metabolism in suckling piglets.

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Andersen, AD, Cilieborg, MS, Lauridsen, C, Mørkbak, AL and Sangild, PT 2017. Supplementation with Lactobacillus paracasei or Pediococcus pentosaceus does not prevent diarrhoea in neonatal pigs infected with Escherichia coli F18. British Journal of Nutrition 118, 109120.
Bafeta, A, Yavchitz, A, Riveros, C, Batista, R and Ravaud, P 2017. Methods and reporting studies assessing faecal microbiota transplantation: a systematic review. Annals of Internal Medicine 167, 3439.
Blanton, LV, Charbonneau, MR, Salih, T, Barratt, MJ, Venkatesh, S, Ilkaveya, O, Subramanian, S, Manary, MJ, Trehan, I, Jorgensen, JM, Fan, YM, Henrissat, B, Leyn, SA, Rodionov, DA, Osterman, AL, Maleta, K, Newgard, CB, Ashorn, P, Dewey, KG and Brown, WR 2014. Faecal microbiota transplantation in treating Clostridium difficile infection. Journal of Digestive Diseases 15, 405408.
Butler, AA and Roith, DL 2001. Control of growth by the somatropic axis: growth hormone and the insulin-like growth factors have related and independent roles. Annual Review of Physiology 63, 141164.
Cani, PD, Bibiloni, R, Knauf, C, Waget, A, Neyrinck, AM, Delzenne, NM and Burcelin, R 2008. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57, 14701481.
Chassaing, B, Srinivasan, G, Delgado, MA, Young, AN, Gewirtz, AT and Vijaykumar, M 2012. Faecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. Plos One 7, e44328.
Corrêa-oliveira, R, Fachi, JL, Vieira, A, Sato, FT and Vinolo, MAR 2016. Regulation of immune cell function by short-chain fatty acids. Clinical & Translational Immunology 5, e73.
Dror, T, Dickstein, Y, Dubourg, G and Paul, M 2017. Microbiota manipulation for weight change. Microbial Pathogenesis 106, 146161.
Fonseca, JE, Santos, MJ, Canhão, H and Choy, E 2009. Interleukin-6 as a key player in systemic inflammation and joint destruction. Autoimmunity Reviews 8, 538542.
Fukuda, S, Toh, H, Hase, K, Oshima, K, Nakanishi, Y, Yoshimura, K, Tobe, T, Clarke, JM, Topping, DL, Suzuki, T, Taylor, TD, Itoh, K, Kikuchi, J, Morita, H, Hattori, M and Ohno, H 2011. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543547.
Gall, ML, Gallois, M, Sève, B, Louveau, I, Holst, JJ, Oswald, IP, Lallès, JP and Guilloteau, P 2009. Comparative effect of orally administered sodium butyrate before or after weaning on growth and several indices of gastrointestinal biology of piglets. British Journal of Nutrition 102, 12851296.
Gensollen, T, Iyer, SS, Kasper, DL and Blumberg, RS 2016. How colonization by microbiota in early life shapes the immune system. Science 352, 539544.
Guilloteau, P, Martin, L, Eeckhaut, V, Ducatelle, R, Zabielski, R and Immerseel, FV 2010. From the gut to the peripheral tissues: the multiple effects of butyrate. Nutrition Research Reviews 23, 366384.
Hamilton, MJ, Weingarden, AR, Sadowsky, MJ and Khoruts, A 2012. Standardised frozen preparation for transplantation of faecal microbiota for recurrent Clostridium difficile infection. American Journal of Gastroenterology 107, 761767.
Hou, C, Zeng, X, Yang, F, Liu, H and Qiao, S 2016. Study and use of the probiotic Lactobacillus reuteri in pigs: a review. Journal of Animal Science and Biotechnology 6, 14.
Jost, T, Lacroix, C, Braegger, C and Chassard, C 2015. Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutrition Reviews 73, 426437.
Kelly, CJ, Zheng, L, Campbell, EL, Saeedi, B, Scholz, CC, Bayless, AJ, Wilson, KE, Glover, LE, Kominsky, DJ, Magnuson, A, Weir, TL, Ehrentraut, SF, Pickel, C, Kuhn, KA, Lanis, JM, Nguyen, V, Taylor, CT and Colgan, SP 2015. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host & Microbe 17, 662671.
Lu, H, Su, S and Ajuwon, KM 2012. Butyrate supplementation to gestating sows and piglets induces muscle and adipose tissue oxidative genes and improves growth performance. Journal of Animal Science 90 (suppl. 4), 430432.
Luk, GD, Bayless, TM and Baylin, SB 1983. Plasma postheparin diamine oxidase. Sensitive provocative test for quantitating length of acute intestinal mucosal injury in the rat. Journal of Clinical Investigation 71, 13081315.
Marquardt, RR, Jin, L, Kim, JW, Fang, L, Frohlich, AA and Baidoo, SK 1999. Passive protective effect of egg-yolk antibodies against enterotoxigenic Escherichia coli K88+ infection in neonatal and early-weaned piglets. FEMS Immunology and Medical Microbiology 23, 283288.
Mathias, A, Pais, B, Favre, L, Benyacoub, J and Corthésy, B 2014. Role of secretory IgA in the mucosal sensing of commensal bacteria. Gut Microbes 5, 688695.
Miquel, S, Martín, R, Rossi, O, Bermúdez-Humarán, LG, Chatel, JM, Sokol, H, Thomas, M, Wells, JM and Langella, P 2013. Faecalibacterium prausnitzii and human intestinal health. Current Opinion in Microbiology 16, 255261.
National Research Council 2012. Nutrient requirements of swine, 11th revised edition. National Academy Press, Washington, DC, USA.
Nguyen, QN, Himes, JE, Martinez, DR and Permar, SR 2016. The impact of the gut microbiota on humoral immunity to pathogens and vaccination in early infancy. Plos Pathogens 12, e1005997.
Niu, Q, Li, P, Hao, S, Zhang, Y, Kim, SW, Li, H, Ma, X, Gao, S, He, L and Wu, W 2015. Dynamic distribution of the gut microbiota and the relationship with apparent crude fibre digestibility and growth stages in pigs. Scientific Reports 5, 9938.
Pang, X, Hua, X, Qian, Y, Ding, D, Che, C, Li, C, Wei, J, Bucheli, P and Zhao, L 2007. Inter-species transplantation of gut microbiota from human to pigs. ISME Journal 1, 156162.
Ramayo-Caldas, Y, Mach, N, Lepage, P, Levenez, F, Denis, C, Lemonnier, G, Leplat, JJ, Billon, Y, Berri, M, Dore, J, Rogel-Gaillard, C and Estelle, J 2016. Phylogenetic network analysis applied to pig gut microbiota identifies an ecosystem structure linked with growth traits. ISME Journal 10, 29732977.
Rauch, M and Lynch, SV 2010. Probiotic manipulation of the gastrointestinal microbiota. Gut Microbes 1, 335338.
Schwarzer, M, Makki, K, Storelli, G, Machuca-Gayet, I, Srutkova, D, Hermanova, P, Martino, ME, Balmand, S, Hudcovic, T, Heddi, A, Rieusset, J, Kozakova, H, Vidal, H and Leulier, F 2016. Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351, 854857.
Tan, J, Mckenzie, C, Potamitis, M, Thorburn, AN, Mackay, CR and Macia, L 2014. The role of short-chain fatty acids in health and disease. Advances in Immunology 121, 91119.
Torow, N and Hornef, MW 2017. The neonatal window of opportunity: setting the stage for life-long host-microbial interaction and immune homeostasis. Journal of Immunology 198, 557563.
Tripathi, A, Lammers, KM, Goldblum, S, Shea-Donohue, T, Netzel-Arnett, S, Buzza, MS, Antalis, TM, Vogel, SN, Zhao, AP, Yang, SQ, Arrietta, MC, Meddings, JB and Fasano, A 2009. Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proceedings of the National Academy of Sciences of the United States of America 106, 1679916804.
Walia, R, Garg, S, Song, Y, Girotra, M, Cuffari, C, Fricke, WF and Dutta, SK 2014. Efficacy of faecal microbiota transplantation in 2 children with recurrent Clostridium difficile infection and its impact on their growth and gut microbiome. Journal of Pediatric Gastroenterology and Nutrition 59, 565570.
Wei, HK, Xue, HX, Zhou, ZX and Peng, J 2017. A carvacrol-thymol blend decreased intestinal oxidative stress and influenced selected microbes without changing the messenger RNA levels of tight junction proteins in jejunal mucosa of weaning piglets. Animal 11, 193201.
Wu, W, Sun, M, Chen, F, Yao, S, Liu, Z and Cong, Y 2016. 1081 – microbiota metabolite short chain fatty acid acetate promotes intestinal IgA response to microbiota which is mediated by GPR43. Mucosal Immunology 10, 946956.
Yang, F, Hou, C, Zeng, X and Qiao, S 2015. The use of lactic acid bacteria as a probiotic in swine diets. Pathogens 4, 3445.
Yang, J, Qian, K, Wang, C and Wu, Y 2017. Roles of probiotic lactobacilli inclusion in helping piglets establish healthy intestinal inter-environment for pathogen defense. Probiotics and Antimicrobial Proteins 10, 243250.
Yang, L, Pang, Y and Moses, HL 2010. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends in Immunology 31, 220227.
Yu, LC, Wang, JT, Wei, SC and Ni, YH 2012. Host-microbial interactions and regulation of intestinal epithelial barrier function: from physiology to pathology. World Journal of Gastrointestinal Pathophysiology 3, 2743.
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