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Impact of feed restriction on health, digestion and faecal microbiota of growing pigs housed in good or poor hygiene conditions

Published online by Cambridge University Press:  25 June 2014

N. Le Floc’h*
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
C. Knudsen
Affiliation:
INRA, UMR1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, F-31320 Castanet-Tolosan, France INPT ENSAT, UMR1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, Université de Toulouse, F-31320 Castanet-Tolosan, France ENVT, UMR 1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, F-31000 Toulouse, France
T. Gidenne
Affiliation:
INRA, UMR1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, F-31320 Castanet-Tolosan, France INPT ENSAT, UMR1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, Université de Toulouse, F-31320 Castanet-Tolosan, France ENVT, UMR 1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, F-31000 Toulouse, France
L. Montagne
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France Université européenne de Bretagne, F-35000 Rennes, France
E. Merlot
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
O. Zemb
Affiliation:
INRA, UMR1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, F-31320 Castanet-Tolosan, France INPT ENSAT, UMR1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, Université de Toulouse, F-31320 Castanet-Tolosan, France ENVT, UMR 1289 Tissus Animaux Nutrition Digestion Ecosystème et Métabolisme, F-31000 Toulouse, France
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Abstract

Feed restriction could be a relevant strategy to preserve gut health, reduce systemic inflammatory response and finally limit antibiotic use. This study assessed the effect of feed restriction on growing pigs submitted to a moderate inflammatory challenge induced by the degradation of the environmental hygiene that is known to alter growth rate. The experiment was run on 80 pigs selected at 7 weeks of age according to a 2×2 factorial design: two feeding levels, ad libitum (AL) and feed restricted (FR) at 60% of AL, and two conditions of environmental hygiene, clean and dirty. Pigs were housed individually throughout the experiment. From 61 to 68 days of age (day 0 to 7), pigs were housed in a post weaning unit and feed restriction was applied to half of the pigs from day 0 to day 29. At 68 days of age (day 7 of the experiment), pigs were transferred in a growing unit where half of FR and half of AL pigs were housed in a dirty environment (poor hygiene) and the other half in a clean environment (good hygiene) until day 42. Growth performance was recorded weekly. Blood and faeces samples were collected to measure indicators of inflammation, nutrient digestibility and microbiota composition. Faecal consistency was monitored daily to detect diarrhoeas. Feed restriction decreased daily weight gain (−35% to −50%, P<0.001), increased the feed conversion ratio (+15%, P<0.001) and CP digestibility (+3%, P<0.05) and reduced the occurrence of diarrhoeas irrespective of hygiene conditions. Poor hygiene conditions decreased growth performance (−20%, P<0.05) and total tract digestibility of all nutrients (P<0.001). Haptoglobin (+50%) concentrations and lymphocyte (+10%) and granulocyte (+40%) numbers were higher in poor hygiene conditions (P<0.05), confirming that the model was effective to induce a systemic inflammatory response. Both feed restriction and hygiene modified the profile of the faecal microbiota. In this study, feed restriction did not reduce the systemic inflammatory response caused by poor hygiene conditions despite the limitation of the occurrence of digestive disorders. However, our study opens discussions regarding the impact of hygiene and feed restriction on gut microbial communities and digestive health.

Type
Research Article
Copyright
© The Animal Consortium 2014 

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References

Booth, PJ, Craigon, J and Foxcroft, GR 1994. Nutritional manipulation of growth and metabolic and reproductive status in prepubertal gilts. Journal of Animal Science 72, 24152424.CrossRefGoogle ScholarPubMed
Cole, JR, Chai, B, Farris, RJ, Wang, Q, Kulam-Syed-Mohideen, AS, McGarrell, DM, Bandela, AM, Cardenas, E, Garrity, GM and Tiedje, JM 2007. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Research 35, 169172.Google Scholar
Combes, S, Michelland, RJ, Monteils, V, Cauquil, L, Soulie, V, Ngoc Uyen, T, Gidenne, T and Fortun-Lamothe, L 2011. Postnatal development of the rabbit caecal microbiota composition and activity. FEMS Microbiology Ecology 77, 680689.Google Scholar
De Leeuw, JA and Ekkel, ED 2004. Effects of feeding level and the presence of a foraging substrate on the behaviour and stress physiological response of individually housed gilts. Applied Animal Behaviour Science 86, 1525.Google Scholar
Dowd, SE, Callaway, TR, Wolcott, RD, Sun, Y, McKeehan, T, Hagevoort, RG and Edrington, TS 2008. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology 8, 125.CrossRefGoogle ScholarPubMed
Eckersall, PD, Saini, PK and McComb, C 1996. The acute phase response of acid soluble glycoprotein, α1-acid glycoprotein, ceruloplasmin, haptoglobin and C-reactive protein, in the pig. Veterinary Immunology Immunopathology 51, 377385.Google Scholar
Eeckhaut, V, Machiels, K, Perrier, C, Romero, C, Maes, S, Flahou, B, Steppe, M, Haesebrouck, F, Sas, B, Ducatelle, R, Vermeire, S and Van Immerseel, F 2013. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 62, 17451752.CrossRefGoogle ScholarPubMed
Gidenne, T, Combes, S and Fortun-Lamothe, L 2012. Feed intake limitation strategies for the growing rabbit: effect on feeding behaviour, welfare, performance, digestive physiology and health: a review. Animal 6, 14071419.CrossRefGoogle ScholarPubMed
Harding, JC, Baarsch, MJ and Murtaugh, MP 1997. Association of tumour necrosis factor and acute phase reactant changes with post arrival disease in swine. Journal of Veterinary Medicine 44, 405413.Google Scholar
Hayashi, A, Sato, T, Kamada, N, Mikami, Y, Matsuoka, K, Hisamatsu, T, Hibi, T, Roers, A, Yagita, H, Ohteki, T, Yoshimura, A and Kanai, T 2013. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host and Microbe 13, 711722.CrossRefGoogle ScholarPubMed
Jombart, T, Devillard, S and Balloux, F 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11, 94.Google Scholar
Karunasena, E, Kurkure, PC, Lackey, RD, McMahon, KW, Kiernan, EP, Graham, S, Alabady, MS, Campos, DL, Tatum, OL and Brashears, MM 2013. Effects of the probiotic Lactobacillus animalis in murine Mycobacterium avium subspecies paratuberculosis infection. BMC Microbiology 13, 14712180.Google Scholar
Kil, DY and Stein, HH 2010. Management and feeding strategies to ameliorate the impact of removing antibiotic growth promoters from diets fed to weanling pigs. Canadian Journal of Animal Science 90, 447460.CrossRefGoogle Scholar
Klasing, KC and Johnstone, BJ 1991. Monokines in growth and development. Poultry Science 70, 17811789.Google Scholar
Le Floc’h, N, Jondreville, C, Matte, JJ and Sève, B 2006. Importance of sanitary environment for growth performance and plasma nutrient homeostasis during the post-weaning period in piglets. Archives of Animal Nutrition 60, 2334.Google Scholar
Le Floc’h, N, Lebellego, L, Matte, JJ, Melchior, D and Sève, B 2009. The effect of sanitary status degradation and dietary tryptophan content on growth rate and tryptophan metabolism in weaning pigs. Journal of Animal Science 87, 16861694.Google Scholar
Leser, TD, Amenuvor, JZ, Jensen, TK, Lindecrona, RH, Boye, M and Moller, K 2002. Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Applied and Environmental Microbiology 68, 673690.Google Scholar
Lipperheide, C, Rabe, M, Knura, S and Petersen, B 2000. Effects of farm hygiene on blood chemical variables in fattening pigs. Tierärztliche Umschau 55, 3036.Google Scholar
Lkhagvadorj, S, Qu, L, Cai, W, Couture, OP, Barb, CR, Hausman, GJ, Nettleton, D, Anderson, LL, Dekkers, JC and Tuggle, CK 2010. Gene expression profiling of the short-term adaptive response to acute caloric restriction in liver and adipose tissues of pigs differing in feed efficiency. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 298, R494R507.Google Scholar
Lovatto, PA, Sauvant, D, Noblet, J, Dubois, S and van Milgen, J 2006. Effects of feed restriction and subsequent refeeding on energy utilization in growing pigs. Journal of Animal Science 84, 33293336.Google Scholar
MacDonald, L, Radler, M, Paolini, AG and Kent, S 2011. Calorie restriction attenuates LPS-induced sickness behavior and shifts hypothalamic signaling pathways to an anti-inflammatory bias. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 301, R172R184.Google Scholar
Matsuzaki, J, Kuwamura, M, Yamaji, R, Inui, H and Nakano, Y 2001. Inflammatory responses to lipopolysaccharide are suppressed in 40% energy-restricted mice. Journal of Nutrition 131, 21392144.CrossRefGoogle ScholarPubMed
Merlot, E, Mounier, AM and Prunier, A 2011. Endocrine response of gilts to various common stressors: a comparison of indicators and methods of analysis. Physiology and Behavior 102, 259265.Google Scholar
Messori, S, Trevisi, P, Simongiovanni, A, Priori, D and Bosi, P 2013. Effect of susceptibility to enterotoxigenic Escherichia coli F4 and of dietary tryptophan on gut microbiota diversity observed in healthy young pigs. Veterinary Microbiology 162, 173179.Google Scholar
Montagne, L, Le Floc’h, N, Arturo-Schaan, M, Foret, R, Urdaci, MC and Le Gall, M 2012. Comparative effects of level of dietary fiber and sanitary conditions on the growth and health of weanling pigs. Journal of Animal Science 90, 25562569.Google Scholar
Moshage, H 1997. Cytokines and the hepatic acute phase response. Journal of Pathology 181, 257266.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, CD, Musk, CC and Kelly, D 2009. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7, 17417007.Google Scholar
Odink, J, Smeets, JF, Visser, IJ, Sandman, H and Snijders, JM 1990. Hematological and clinicochemical profiles of healthy swine and swine with inflammatory processes. Journal of Animal Science 68, 163170.Google Scholar
Pastorelli, H, Le Floc'h, N, Merlot, E, Meunier-Salaun, MC, van Milgen, J and Montagne, L 2012. Sanitary housing conditions modify the performance and behavioural response of weaned pigs to feed- and housing-related stressors. Animal 6, 18111820.Google Scholar
Plata-Salaman, CR 1995. Cytokines and feeding suppression: an integrative view from neurologic to molecular levels. Nutrition 11, 674677.Google Scholar
Rantzer, D, Svendsen, J and Westrom, B 1996. Effects of a strategic feed restriction on pig performance and health during the post-weaning period. Acta Agriculturae Scandinavica Section A – Animal Science 46, 219226.Google Scholar
Scaria, J, Janvilisri, T, Fubini, S, Gleed, RD, McDonough, SP and Chang, YF 2011. Clostridium difficile transcriptome analysis using pig ligated loop model reveals modulation of pathways not modulated in vitro. Journal of Infectious Diseases 203, 16131620.Google Scholar
Schloss, PD, Westcott, SL, Ryabin, T, Hall, JR, Hartmann, M, Hollister, EB, Lesniewski, RA, Oakley, BB, Parks, DH, Robinson, CJ, Sahl, JW, Stres, B, Thallinger, GG, Van Horn, DJ and Weber, CF 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 75377541.Google Scholar
Scrimshaw, NS and SanGiovanni, JP 1997. Synergism of nutrition, infection, and immunity: an overview. American Journal of Clinical Nutrition 66, 464S477S.CrossRefGoogle ScholarPubMed
Splichalova, A, Trebichavsky, I, Rada, V, Vlkova, E, Sonnenborn, U and Splichal, I 2011. Interference of Bifidobacterium choerinum or Escherichia coli Nissle 1917 with Salmonella Typhimurium in gnotobiotic piglets correlates with cytokine patterns in blood and intestine. Clinical and Experimental Immunology 163, 242249.Google Scholar
Sun, YJ, Cai, YP, Huse, SM, Knight, R, Farmerie, WG, Wang, XY and Mai, V 2011. A large-scale benchmark study of existing algorithms for taxonomy-independent microbial community analysis. Briefings in Bioinformatics 13, 107121.Google Scholar
Thompson, CL and Holmes, AJ 2009. A window of environmental dependence is evident in multiple phylogenetically distinct subgroups in the faecal community of piglets. FEMS Microbiology Letters 290, 9197.Google Scholar
Whang, KY, Kim, SW, Donovan, SM, McKeith, FK and Easter, RA 2003. Effects of protein deprivation on subsequent growth performance, gain of body components, and protein requirements in growing pigs. Journal of Animal Science 81, 705716.Google Scholar
Wilfart, A, Montagne, L, Simmins, PH, van Milgen, J and Noblet, J 2007. Sites of nutrient digestion in growing pigs: effect of dietary fiber. Journal of Animal Science 85, 976983.Google Scholar