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Early feed restriction of lambs modifies ileal epimural microbiota and affects immunity parameters during the fattening period

  • J. Frutos (a1), S. Andrés (a1), D. R. Yáñez-Ruiz (a2), J. Benavides (a1), S. López (a1), A. Santos (a1), M. Martínez-Valladares (a1), F. Rozada (a1) and F. J. Giráldez (a1)...


Bacteria firmly attached to the gastrointestinal epithelium during the pre-weaning phase may show a significant impact on nutrient processing, immunity parameters, health and feed efficiency of lambs during post-weaning phases. Thus, the aim of this study was to describe the differences in the ileal epimural microbiota (e.g. total bacteria, Prevotella spp., Bifidobacterium spp. and Lactobacillus spp.) of fattening lambs promoted by early feed restriction during the suckling phase trying to elucidate some of the underlying mechanisms behind changes in feed efficiency during the fattening period. A total of 24 Merino lambs (average BW 4.81±0.256 kg) were used, 12 of them (ad libitum, ADL) kept permanently in individual pens with their mothers, whereas the other 12 lambs were separated from their dams for 9 h each day to be exposed to milk restriction (RES). After weaning (BW=15 kg) all the animals were penned individually, offered the same complete pelleted diet (35 g/kg BW per day) and slaughtered at a BW of 27 kg. During the fattening period, reduced gain : feed ratio (0.320 v. 0.261, P<0.001) was observed for the RES group. Moreover, increments of Prevotella spp. were detected in the ileal epimural microbiota of RES lambs (P<0.05). There were also higher numbers of infiltrated lymphocytes (T and B cells) in the ileal lamina propria (P<0.05), a higher M-cell labelling intensity in ileal Peyer’s patches domes (P<0.05) and a trend towards a thickening of the submucosa layer when compared with the ADL group (P=0.057). Some other immunological parameters, such as an increased immunoglobulin A (IgA) production (pg IgA/µg total protein) and increments in CD45+ cells were also observed in the ileum of RES group (P<0.05), whereas transforming growth factor β and toll-like receptor gene expression was reduced (P<0.05). In conclusion, early feed restriction during the suckling phase promoted changes in ileal epimural microbiota and several immunity parameters that could be related to differences in feed efficiency traits during the fattening period of Merino lambs.


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Present address: Instituto de Ganadería de Montaña, CSIC-Universidad de León, Finca Marzanas s/n, 24346 Grulleros, León, Spain.



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Abecia, L, Jiménez, E, Martínez-Fernández, G, Martín-García, AI, Ramos-Morales, E, Pinloche, E, Denman, SE, Newbold, CJ and Yáñez-Ruiz, DR 2017. Natural and artificial feeding management before weaning promote different rumen microbial colonization but not differences in gene expression levels at the rumen epithelium of newborn goats. PLoS One 12, e0182235.
Ahmed, AM, Sebastiano, SR, Sweeney, T, Hanrahan, JP, Glynn, A, Keane, OM, Mukhopadhya, A, Thornton, K and Good, B 2015. Breed differences in humoral and cellular responses of lambs to experimental infection with the gastrointestinal nematode Teladorsagia circumcincta . Veterinary Research 46, 8.
Andrés, S, Bodas, R, Tejido, ML, Giráldez, FJ, Valdés, C and López, S 2016. Effects of the inclusion of flaxseed and quercetin in the diet of fattening lambs on ruminal microbiota, in vitro fermentation and biohydrogenation of fatty acids. Journal of Agricultural Science 154, 542552.
Animal Task Force 2013. Research & innovation for a sustainable livestock sector in Europe. Retrieved on 12 March 2018 from
Arranz-Solís, D, Benavides, J, Regidor-Cerrillo, J, Horcajo, P, Castaño, P, Ferreras, MC, Jiménez-Pelayo, L, Collantes-Fernández, E, Ferre, I, Hemphill, A, Pérez, V and Ortega-Mora, LM 2016. Systemic and local immune responses in sheep after Neospora caninum experimental infection at early, mid and late gestation. Veterinary Research 47, 2.
Cerutti, A and Rescigno, M 2008. The biology of intestinal IgA responses. Immunity 28, 740750.
Charavaryamath, C, Fries, P, Gomis, S, Bell, C, Doig, K, Guan, LL, Potter, A, Napper, S and Griebel, PJ 2011. Mucosal changes in a long-term bovine intestinal segment model following removal of ingesta and microflora. Gut Microbes 2, 134144.
Corpa, JM, Juste, RA, Marín, JFG, Reyes, LE, González, J and Pérez, V 2001. Distribution of lymphocyte subsets in the small intestine lymphoid tissue of 1-month-old lambs. Anatomia Histologia Embryologia-Journal of Veterinary Medicine Series C 30, 121127.
Delroisse, JM, Boulvin, AL, Parmentier, I, Dauphin, RD, Vandenbol, M and Portetelle, D 2008. Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiological Research 163, 663670.
Gebert, A, Rothkotter, HJ and Pabst, R 1994. Cytokeratin-18 is an M-cell marker in porcine Peyer’s patches. Cell and Tissue Research 276, 213221.
Greenwood, PL and Cafe, LM 2007. Prenatal and pre-weaning growth and nutrition of cattle: long-term consequences for beef production. Animal 1, 12831296.
Letterio, JJ and Roberts, AB 1998. Regulation of immune responses by TGF-beta. Annual Review of Immunology 16, 137161.
Ley, RE 2016. Gut microbiota in 2015: Prevotella in the gut: choose carefully. Nature Reviews Gastroenterology & Hepatology 13, 6970.
Lim, SM, Jeong, JJ, Jang, SE, Han, MJ and Kim, DH 2016. A mixture of the probiotic strains Bifidobacterium longum CH57 and Lactobacillus brevis CH23 ameliorates colitis in mice by inhibiting macrophage activation and restoring the Th17/Treg balance. Journal of Functional Foods 27, 295309.
Lukens, JR, Gurung, P, Vogel, P, Johnson, GR, Carter, RA, McGoldrick, DJ, Bandi, SR, Calabrese, CR, Vande Walle, L, Lamkanfi, M and Kanneganti, TD 2014. Dietary modulation of the microbiome affects autoinflammatory disease. Nature 516, 246249.
Malmuthuge, N, Li, M, Fries, P, Griebel, PJ and Guan, LL 2012. Regional and age dependent changes in gene expression of Toll-like receptors and key antimicrobial defence molecules throughout the gastrointestinal tract of dairy calves. Veterinary Immunology and Immunopathology 146, 1826.
Mao, S, Zhang, M, Liu, J and Zhu, W 2015. Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Scientific Reports 5, 16116.
Martínez-Pérez, JM, Robles-Pérez, D, Rojo-Vázquez, FA and Martínez-Valladares, M 2014. Immunological features of LPS from Ochrobactrum intermedium on sheep experimentally infected with Fasciola hepatica . Research in Veterinary Science 97, 329332.
McCann, JC, Wiley, LM, Forbes, TD, Rouquette, FM Jr and Tedeschi, LO 2014. Relationship between the rumen microbiome and residual feed Intake-efficiency of Brahman bulls stocked on bermudagrass pastures. PLoS One 9, e91864.
Myer, PR, Smith, TPL, Wells, JE, Kuehn, LA and Freetly, HC 2015a. Rumen microbiome from steers differing in feed efficiency. PLoS One 10, e0129174.
Myer, PR, Wells, JE, Smith, TPL, Kuehn, LA and Freetly, HC 2015b. Cecum microbial communities from steers differing in feed efficiency. Journal of Animal Science 93, 53275340.
Myer, PR, Wells, JE, Smith, TPL, Kuehn, LA and Freetly, HC 2015c. Microbial community profiles of the colon from steers differing in feed efficiency. Springerplus 4, 454.
Myer, PR, Wells, JE, Smith, TPL, Kuehn, LA and Freetly, HC 2016. Microbial community profiles of the jejunum from steers differing in feed efficiency. Journal of Animal Science 94, 327338.
Petri, RM, Schwaiger, T, Penner, GB, Beauchemin, KA, Forster, RJ, McKinnon, JJ and McAllister, TA 2013. Changes in the rumen epimural bacterial diversity of beef cattle as affected by diet and induced ruminal acidosis. Applied and Environmental Microbiology 79, 37443755.
Prims, S, Pintens, N, Vergauwen, H, Van Cruchten, S, Van Ginneken, C and Casteleyn, C 2017. Effect of artificial rearing of piglets on the volume densities of M cells in the tonsils of the soft palate and ileal Peyer’s patches. Veterinary Immunology and Immunopathology 184, 17.
Rauw, WM 2012. Immune response from a resource allocation perspective. Frontiers in Genetics 3, 267.
Santos, A, Giráldez, FJ, Trevisi, E, Lucini, L, Frutos, J and Andrés, S 2018a. Liver transcriptomic and plasma metabolomic profiles of fattening lambs are modified by feed restriction during the suckling period. Journal of Animal Science,, Published online by Oxford University Press 19 February 2018.
Santos, A, Valdés, C, Giráldez, FJ, López, S, France, J, Frutos, J, Fernández, M and Andrés, S 2018b. Feed efficiency and the liver proteome of fattening lambs are modified by feed restriction during the suckling period. Animal,, Published online by Cambridge University Press 24 January 2018.
Taschuk, R and Griebel, PJ 2012. Commensal microbiome effects on mucosal immune system development in the ruminant gastrointestinal tract. Animal Health Research Reviews 13, 129141.
Vargas, JE, Andrés, S, Snelling, TJ, López-Ferreras, L, Yáñez-Ruiz, DR, García-Estrada, C and López, S 2017. Effect of sunflower and marine oils on ruminal microbiota, in vitro fermentation and digesta fatty acid profile. Frontiers in Microbiology 8, 1124.
Varghese, F, Bukhari, AB, Malhotra, R and De, A 2014. IHC Profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PLoS One 9, e96801.
Verdonk, JMAJ, Spreeuwenberg, MAM, Bakker, GCM and Verstegen, MWA 2001. Nutrient intake level affects histology and permeability of the small intestine in newly weaned piglets. In Digestive Physiology of Pigs (ed. JE Lindberg and B Ogle), pp. 332334. CABI Publishing, Wallingford, UK.
Villena, J, Aso, H and Kitazawa, H 2014. Regulation of toll-like receptors-mediated inflammation by immunobiotics in bovine intestinal epitheliocytes: role of signalling pathways and negative regulators. Frontiers in Immunology 5, 421.
Yáñez-Ruiz, DR, Abecia, L and Newbold, CJ 2015. Manipulating rumen microbiome and fermentation through interventions during early life: a review. Frontiers in Microbiology 6, 1133.
Zhang, GL and Ghosh, S 2002. Negative regulation of toll-like receptor-mediated signalling by Tollip. Journal of Biological Chemistry 277, 70597065.



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