Skip to main content
×
×
Home

Health relevance of intestinal protein fermentation in young pigs

  • R. Pieper (a1), C. Villodre Tudela (a1) (a2), M. Taciak (a3), J. Bindelle (a4), J. F. Pérez (a2) and J. Zentek (a1)...
Abstract

The physiological role of the gastrointestinal microbiota has become an important subject of nutrition research in pigs in the past years, and the importance of intestinal microbial activity in the etiology of disease is doubtless. This review summarizes the recent knowledge related to the microbial ecology of protein fermentation and the appearance of protein-derived metabolites along the pig intestine. The amount of fermentable protein depends on factors such as dietary protein concentration, protein digestibility due to secondary or tertiary structure, the interaction with dietary compounds or anti-nutritional factors, and the secretion of endogenous proteins into the gut lumen. High protein diets increase the luminal concentrations and epithelial exposure to putatively toxic metabolites and increase the risk for post-weaning diarrhea, but the mechanisms are not yet clarified. Although the use of fermentable carbohydrates to reduce harmful protein-derived metabolites in pigs is well-established, recent studies suggest that the inclusion of fermentable carbohydrates into diets with low protein digestibility or high dietary protein level may not ameliorate all negative effects with regard to epithelial response. Based on the current knowledge, the use of diets with low levels of high-quality protein may help to reduce the risk for intestinal disease in young pigs.

Copyright
Corresponding author
*Corresponding author. E-mail: robert.pieper@fu-berlin.de
References
Hide All
Ahrens, R, Gäbel, G, Garz, B and Aschenbach, JR (2003). Histamine-induced chloride secretion is mediated via H2-receptors in the pig proximal colon. Inflammation Research 52: 7985.
Aschenbach, JR, Honscha, KU, von Vietinghoff, V and Gäbel, G (2009). Bioelimination of histamine in epithelia of the porcine proximal colon of pigs. Inflammation Research 58: 269276.
Aumiller, T, Mosenthin, R and Weiss, E (2014). Potential of cereal grains and grain legumes in modulating pig's intestinal microbiota-A review. Livestock Science 172: 1632.
Awati, A, Williams, BA, Bosch, MW, Gerrits, WJJ and Verstegen, MWA (2006). Effect of inclusion of fermentable carbohydrates in the diet on fermentation end-product profile in feces of weanling piglets. Journal of Animal Science 84: 21332140.
Ball, RO and Aherne, FX (1987). Influence of dietary nutrient density, level of feed intake and weaning age on young pigs. II. Apparent nutrient digestibility and incidence and severity of diarrhea. Canadian Journal of Animal Science 67: 11051115.
Bikker, P, Dirkzwager, A, Fledderus, J, Trevisi, P, le Huerou-Luron, I, Lalles, JP and Awati, A (2006). The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. Journal of Animal Science 84: 33373345.
Bindelle, J, Buldgen, A, Michaux, D, Wavreille, J, Destain, JP and Leterme, P (2007). Influence of purified dietary fibre on bacterial protein synthesis in the large intestine of pigs, as measured by the gas production technique. Livestock Science 109: 232235.
Bindelle, J, Buldgen, A, Delacollette, M, Wavreille, J, Agneessens, R, Destain, JP and Leterme, P (2009). Influence of source and concentrations of dietary fiber on in vivo nitrogen excretion pathways in pigs as reflected by in vitro fermentation and nitrogen incorporation by fecal bacteria. Journal of Animal Science 87: 583593.
Blachier, F, Mariotti, F, Huneau, JF and Tomé, D (2007). Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33: 547562.
Blachier, F, Davila, AM, Mimoun, S, Benetti, PH, Atanasiu, C, Andriamihaja, M, Benamouzig, R, Bouillaud, F and Tomé, D (2010). Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids 39: 335347.
Blaut, M and Clavel, T (2007). Metabolic diversity of the intestinal microbiota: implication for health and disease. Journal of Nutrition 137: 751755.
Borthakur, A, Priyamvada, S, Kumar, A, Natarajan, AA, Gill, RK, Alrefai, WA and Dudeja, PK (2012). A novel nutrient sensing mechanism underlies substrate-induced regulation of monocarboxylate transporter-1. American Journal of Gastrointestinal and Liver Physiology 303: 11261133.
Burger-van Paassen, N, Vincent, A, Puiman, P, Van Der Sluis, M, Bouma, J, Boehm, G, van Goudoever, JB, van Seuningen, I and Renes, I (2009). The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochemical Journal 420: 211219.
Carbonaro, M, Vecchini, P and Carnovale, E (1993). Protein solubility of raw and cooked beans (Phaseolus vulgaris): role of the basic residues. Journal of Agricultural and Food Chemistry 41: 11691175.
Carbonaro, M, Cappelloni, M, Nicoli, S, Lucarini, M and Carnovale, E (1997). Solubility-digestibility relationship of legume proteins. Journal of Agricultural and Food Chemistry 45: 33873394.
Carbonaro, M, Maselli, P and Nucara, A (2012). Relationship between digestibility and secondary structure of raw and thermally treated legume proteins: a Fourier transform infrared (FT-IR) spectroscopic study. Amino Acids 43: 911921.
Carbonero, F, Benefiel, AC, Alizadeh-Ghamsari, AH and Gaskins, HR (2012). Microbial pathways in colonic sulphur metabolism and links with health and disease. Frontiers in Physiology 3: 448.
Choct, M and Annison, G (1992). Anti-nutritive effect of wheat pentosans in broiler chickens: roles of viscosity and gut microflora. British Poultry Science 33: 821834.
Cosgrove, DJ (1966). The chemistry and biochemistry of inositol polyphosphates. Reviews of Pure and Applied Chemistry 16: 209224.
Dai, ZL, Wu, G and Zhu, WY (2011). Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Frontiers in Bioscience 16: 17681786.
Davila, AM, Blachier, F, Gotteland, M, Andriamihaja, M, Benetti, PH, Sanz, Y and Tomé, D (2013). Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacological Research 68: 95107.
De Lange, CFM, Sauer, WC, Mosenthin, R and Souffrant, WB (1989). The effect of feeding different protein-free diets on the recovery and amino acid composition of endogenous protein collected from the distal ileum and feces in pigs. Journal of Animal Science 67: 746754.
DiLorenzo, M, Bass, J and Krantis, A (1995). An intraluminal model of necrotizing enterocolitis in the developing neonatal piglet. Journal of Pediatric Surgery 30: 11381142.
Engemann, A, Focke, C and Humpf, HU (2013). Intestinal formation of N-nitroso compounds in the pig cecum model. Journal of Agricultural and Food Chemistry 61: 9981005.
Erickson, RH and Kim, YS (1990). Digestion and absorption of dietary protein. Annual Reviews of Medicine 41: 133139.
Fairbrother, JM, Nadeau, E and Gyles, CL (2005). Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Animal Health Research Reviews 6: 1739.
Fontaine, J, Zimmer, U, Moughan, PJ and Rutherfurd, SM (2007). Effect of heat damage in an autoclave on the reactive lysine contents of soy products and corn distillers dried grains with solubles. Use of the results to check on lysine damage in common qualities of these ingredients. Journal of Agricultural and Food Chemistry 55: 1073710743.
Ganapathy, V (2012). Protein digestion and absorption. In: Johnson, LR, Gishan, FK, Kaunitz, Merchant, JL, Said, HM, and Wood, JD (eds) Physiology of the Gastrointestinal Tract, 5th edn, Elsevier Academic Press, San Diego, pp. 15951623.
Gehring, CK, Bedford, MR, Cowieson, AJ and Dozier, WA (2012). Effects of corn source on the relationship between in vitro assays and ileal nutrient digestibility. Poultry Science 91: 19081914.
Geypens, B, Claus, D, Evenepoel, P, Hiele, M, Maes, B, Peeters, M, Rutgeerts, P and Ghoos, Y (1997). Influence of dietary protein supplements on the formation of bacterial metabolites in the colon. Gut 41: 7076.
González-Vega, JC, Kim, BG, Htoo, JK, Lemme, A and Stein, HH (2011). Amino acid digestibility in heated soybean meal fed to growing pigs. Journal of Animal Science 89: 36173625.
Govers, MJAP, Gannon, NJ, Dunshea, FR, Gibson, PR and Muir, JG (1999). Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs. Gut 45: 840847.
Hamer, HM, Jonkers, D, Venema, K, Vanhoutvin, S, Troost, FJ and Brummer, RJ (2008). Review article: the role of butyrate on colonic function. Alimentary Pharmacology and Therapeutics 27: 104119.
Heo, JM, Kim, JC, Hansen, CF, Mullan, BP, Hampson, DJ and Pluske, JR (2008). Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhea and performance after weaning. Archives of Animal Nutrition 62: 343358.
Heo, JM, Kim, JC, Hansen, CF, Mullan, BP, Hampson, DJ and Pluske, JR (2009). Feeding a diet with decreased protein content reduces indices of protein fermentation and the incidence of postweaning diarrhea in weaned pigs challenged with an enterotoxigenic strain of Escherichia coli . Journal of Animal Science 87: 28332843.
Heo, JM, Opapeju, FO, Pluske, JR, Kim, JC, Hampson, DJ and Nyachoti, CM (2012). Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. Journal of Animal Physiology and Animal Nutrition 97, 207237.
Heo, JM, Kim, JC, Yoo, J and Pluske, JR (2015). A between-experiment analysis of relationships linking dietary protein intake and post-weaning diarrhea in weanling piglets under conditions of experimental infection with an enterotoxigenic strain of Escherichia coli . Animal Science Journal 86: 286293.
Hermes, RG, Molist, F, Ywazaki, M, Nofrarias, M, Gomez De Segura, A, Gasa, J and Perez, JF (2009). Effect of dietary level of protein and fiber on the productive performance and health status of piglets. Journal of Animal Science 87: 35693577.
Hughes, R, Magee, EAM and Bingham, S (2000). Protein degradation in the large intestine: relevance to colorectal cancer. Current Issues in Intestinal Microbiology 1: 5158.
Hughes, R, Kurth, MJ, McGilligan, V, McGlynn, H and Rowland, I (2008). Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro . Nutrition and Cancer 60: 259266.
Isaacson, R and Kim, HB (2012). The intestinal microbiome of the pig. Animal Health Research Reviews 13: 100109.
Jha, R and Berrocoso, JFD (2016). Dietary fiber and protein fermentation in the intestine of swine and their interactive effects on gut health and on the environment: A review. Animal Feed Science and Technology 212: 1826.
Jensen, MT, Cox, RP and Jensen, BB (1995). Microbial production of skatole in the hindgut of pigs given different diets and its relation to skatole deposition in backfat. Animal Science 61: 293304.
Jha, R and Berrocoso, JFD (2016). Dietary fiber and protein fermentation in the intestine of swine and their interactive effects on gut health and on the environment: a review. Animal Feed Science and Technology 212: 1826.
Kambashi, B, Boudry, C, Picron, P and Bindelle, J (2014). Forage plants as an alternative feed resource for sustainable pig production in the tropics: a review. Animal 8: 12981311.
Kikugawa, K and Kato, T (1988). Formation of a mutagenic diazoquinone by interaction of phenol with nitrite. Food and Chemical Toxicology 26: 209214.
Kim, HB, Borewicz, K, White, BA, Singer, RS, Sreevatsan, S, Tu, ZJ and Isaacson, RE (2011a) Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Veterinary Microbiology 153: 124133.
Kim, JC, Heo, JM, Mullan, BP and Pluske, JR (2011b) Efficacy of a reduced protein diet on clinical expression of post-weaning diarrhoea and life-time performance after experimental challenge with an enterotoxigenic strain of Escherichia coli . Animal Feed Science and Technology 170: 222230.
Kim, MH, Kang, SG, Park, JH, Yanagisawa, M and Kim, CH (2013). Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 145: 396406.
Knuckles, BE, Kuzmicky, DD, Gumbmann, MR and Betschart, AA (1989). Effect of myoinositol phosphate esters on in vitro and in vivo digestion of protein. Journal of Food Science 54: 13481350.
Kröger, S, Pieper, R, Schwelberger, HG, Wang, J, Villodre Tudela, C, Aschenbach, JR, Van Kessel, AG and Zentek, J (2013). Diets high in heat-treated soybean meal reduce the histamine-induced epithelial response in the colon of weaned piglets and increase epithelial catabolism of histamine. PLoS ONE 8: e80612.
Kröger, S, Pieper, R, Aschenbach, JR, Martin, L, Liu, P, Rieger, J, Schwelberger, HG, Neumann, K and Zentek, J (2015). Effects of high levels of dietary zinc oxide on ex vivo epithelial histamine response and investigations on histamine receptor action in the proximal colon of weaned piglets. Journal of Animal Science 93: 52655272.
Kuley, E, Balıkcı, E, Özoğul, I, Gökdogan, S and Özoğul, F (2012). Stimulation of cadaverine production by food borne pathogens in the presence of Lactobacillus, Lactococcus, and Streptococcus spp. Journal of Food Science 77: 650658.
Leschelle, X, Robert, V, Delpal, S, Mouille, B, Mayeur, C, Martel, P and Blachier, F (2002). Isolation of pig colonic crypts for cytotoxic assay of luminal compounds: effects of hydrogen sulfide, ammonia, and deoxycholic acid. Cell Biology and Toxicology 18: 193203.
Lewis, MC, Inman, CF, Patel, D, Schmidt, B, Mulder, I, Miller, B, Gill, BP, Pluske, J, Kelly, D, Stokes, CR and Bailey, M (2012). Direct experimental evidence that early-life farm environment influences regulation of immune responses. Pediatric Allergy and Immunology 23: 265269.
Lin, J (2004). Too much short chain fatty acids cause neonatal necrotizing enterocolitis. Medical Hypotheses 62: 291293.
Liu, Y, Ipharraguerre, IR and Pettigrew, JE (2013). Digestive physiology of the pig symposium: potential applications of knowledge of gut chemosensing in pig production. Journal of Animal Science 91: 19821990.
Looft, T, Allen, HA, Cantarel, BL, Levine, UY, Bayles, DO, Alt, DP, Henrissat, B and Stanton, TB (2014). Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME Journal 8: 15661576.
Mann, E, Schmitz-Esser, S, Zebeli, Q, Wagner, M, Ritzmann, M and Metzler-Zebeli, BU (2014). Mucosa-associated bacterial microbiome of the gastrointestinal tract of weaned pigs and dynamics linked to dietary calcium-phosphorus. PLoS ONE 9: e86950.
Merrifield, CA, Lewis, M, Berger, B, Cloarec, O, Heinzmann, SS, Charton, F, Krause, L, Levin, NS, Duncker, S, Mercenier, A, Holmes, E, Bailey, M and Nicholson, JK (2015). Neonatal environment exert a sustained influence on the development of the intestinal microbiota and metabolic phenotype. ISME Journal 10, 145157.
Moughan, PJ, Ravindran, V and Sorbara, JOB (2014). Dietary protein and amino acids – Consideration of the undigestible fraction. Poultry Science 93: 111.
Mulder, IE, Schmidt, B, Lewis, M, Delday, M, Stokes, CR, Bailey, M, Aminov, RI, Gill, BP, Pluske, JR, Mayer, CD and Kelly, D (2011). Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity. PLoS ONE 6: e28279.
Nyachoti, CM, Omogbenigun, FO, Rademacher, M and Blank, G (2006). Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low- protein amino acid-supplemented diets. Journal of Animal Science 84: 125134.
Opapeju, FO, Krause, DO, Payne, RL, Rademacher, M and Nyachoti, CM (2009). Effect of dietary protein level on growth performance, indicators of enteric health, and gastrointestinal microbial ecology of weaned pigs induced with postweaning colibacillosis. Journal of Animal Science 87: 26352643.
Pieper, R, Kröger, S, Richter, JF, Wang, J, Martin, L, Bindelle, J, Htoo, JK, von Smolinski, D, Vahjen, W, Zentek, J and Van Kessel, AG (2012). Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. Journal of Nutrition 142: 661667.
Pieper, R, Boudry, C, Bindelle, J, Vahjen, W and Zentek, J (2014). Interaction between dietary protein content and the source of carbohydrates along the gastrointestinal tract of weaned piglets. Archives of Animal Nutrition 68: 263280.
Pieper, R, Vahjen, W and Zentek, J (2015). Dietary fibre and crude protein: impact on gastrointestinal microbial fermentation characteristics and host response. Animal Production Science 55: 13671375.
Pietrzak, T, Schad, A, Zentek, J and Mosenthin, R (2002). Biogene amine in der Tierernährung: Entstehung, Stoffwechsel und physiologische Aspekte. Übersichten zur Tierernährung 31: 3764.
Plöger, S, Stumpff, F, Penner, GB, Schulzke, JD, Gäbel, G, Martens, H, Shen, Z, Günzel, D and Aschenbach, JR (2012). Microbial butyrate and its role for barrier function in the gastrointestinal tract. Annals of the New York Academy of Sciences 1258: 5259.
Prohaszka, L and Baron, F (1980). The predisposing role of high dietary protein supplies in enteropathogenic Escherichia coli infections in weaned pigs. Zentralblatt Veterinarmedizin 27: 222232.
Rajendran, S and Prakash, V (1993). Kinetics and thermodynamics of the mechanism of interaction of sodium phytate with alpha-globulin. Biochemistry 32: 34743478.
Richter, JF, Pieper, R, Zakrzewski, SS, Günzel, D, Schulzke, JD and Van Kessel, AG (2014). Diets high in fermentable protein and fibre alter tight junction protein composition with minor effects on barrier function in piglet colon. British Journal of Nutrition 111: 10401049.
Rist, VTS, Weiss, E, Eklund, M and Mosenthin, R (2013). Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review. Animal 7: 10671078.
Rojas, OJ and Stein, HH (2013). Concentration of digestible, metabolizable, and net energy and digestibility of energy and nutrients in fermented soybean meal, conventional soybean meal, and fish meal fed to weanling pigs. Journal of Animal Science 91: 43974405.
Seiler, N and Raul, F (2007). Polyamines and the intestinal tract. Critical Reviews in Clinical Laboratory Sciences 44: 365411.
Selle, PH, Cowieson, AJ, Cowieson, NP and Ravindran, V (2012). Protein–phytate interactions in pig and poultry nutrition: a reappraisal. Nutrition Research Reviews 25: 117.
Slezak, K, Hanske, L, Loh, G and Blaut, M (2013). Increased bacterial putrescine has no impact on gut morphology and physiology in gnotobiotic adolescent mice. Beneficial Microbes 4: 253266.
Smith, EA and Macfarlane, GT (1998). Enumeration of amino acid fermenting bacteria in the human large intestine: effects of pH and starch on peptide metabolism and dissimilation of amino acids. FEMS Microbiology Ecology 25: 355368.
Souffrant, WB (2001). Effect of dietary fibre on ileal digestibility and endogenous nitrogen losses in the pig. Animal Feed Science and Technology 90: 93102.
Stein, HH, Fuller, MF, Moughan, PJ, Sève, B, Mosenthin, R, Jansman, AJM and De Lange, CFM (2007). Definition of apparent, true, and standardized ileal digestibility of amino acids in pigs. Livestock Science 109: 282285.
Stokes, CR, Miller, BG and Bourne, FJ (1987). Animal models of food sensitivity. Food Allergy and Intolerance 2: 286300.
Stumpff, F, Lodemann, U, Van Kessel, AG, Pieper, R, Klingspor, S, Wolf, K, Martens, H, Zentek, J and Aschenbach, JR (2013). Effects of dietary fibre and protein on urea transport across the cecal mucosa of piglets. Journal of Comparative Physiology B 183: 10531063.
Torres, AG (2009). The cad locus of Enterobacteriaceae: more than just lysine decarboxylation. Anaerobe 15: 16.
Ulven, T (2012). Short-chain free fatty acid receptors FFA2/GPR43 and FFA3/GPR41 as new potential therapeutic targets. Frontiers in Endocrinology 3: 111.
Villodre Tudela, C, Boudry, C, Stumpff, F, Aschenback, JR, Vahjen, W, Zentek, J and Pieper, R (2015). Down-regulation of monocarboxylate transporter 1 (MCT1) gene expression in the colon of piglets is linked to bacterial protein fermentation and pro-inflammatory cytokine-mediated signalling. British Journal of Nutrition 113: 610617.
Villodre Tudela, C, Tedin, K, Zentek, J and Pieper, R (2016). Influence of bacterial metabolites on barrier function and pro-inflammatory signalling in epithelial cells in vitro . Proceedings of the Society of Nutrition Physiology 25: 23.
Vinolo, MAR, Rodrigues, HG, Nachbar, RT and Curi, R (2011). Regulation of inflammation by short chain fatty acids. Nutrients 3: 858876.
Wallace, JL, Ferraz, JG and Muscara, MN (2012). Hydrogen sulfide: an endogenous mediator of resolution of inflammation and injury. Antioxidants and Redox Signaling 17: 5867.
Wellock, IJ, Fortomaris, PD, Houdijk, JGM and Kyriazakis, I (2006). The effect of dietary protein supply on the performance and risk of post-weaning enteric disorders in newly weaned pigs. Animal Science 82: 327335.
Wellock, IJ, Fortomaris, PD, Houdijk, JGM and Kyriazakis, I (2008). Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: health. Animal 2: 834842.
Wikoff, WR, Anfora, AT, Liu, J, Schultz, PG, Lesley, SA, Peters, EC and Siuzdak, G (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences 106: 36983703.
Willing, B and Van Kessel, AG (2010). Host pathways for recognition: establishing gastrointestinal microbiota as relevant in animal health and nutrition. Livestock Science 133: 8291.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Animal Health Research Reviews
  • ISSN: 1466-2523
  • EISSN: 1475-2654
  • URL: /core/journals/animal-health-research-reviews
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 36
Total number of PDF views: 196 *
Loading metrics...

Abstract views

Total abstract views: 1448 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 24th May 2018. This data will be updated every 24 hours.