Pigs experimentally infected with an enterotoxigenic strain of Escherichia coli have improved feed efficiency and indicators of inflammation with dietary supplementation of tryptophan and methionine in the immediate post-weaning period
M. M. Capozzalo A G , J. C. Kim A , J. K. Htoo B , C. F. M. de Lange C , B. P. Mullan D , C. F. Hansen E , J. W. Resink F and J. R. Pluske A H
+ Author Affiliations
- Author Affiliations
A School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia.
B Evonik Industries AG, Hanau, Germany.
C Department of Animal Biosciences, University of Guelph, Guelph, Ontario, Canada.
D Department of Agriculture and Food Western Australia, South Perth, WA 6151, Australia.
E Department of Large Animal Sciences, University of Copenhagen, Copenhagen, Denmark.
F Nutreco R & D, Boxmeer, The Netherlands.
G Present address: Selko B.V., Jellinghausstraat 24, 5048AZ Tilburg, The Netherlands.
H Corresponding author. Email: J.Pluske@murdoch.edu.au
Animal Production Science 57(5) 935-947 https://doi.org/10.1071/AN15289
Submitted: 7 June 2015 Accepted: 22 February 2016 Published: 21 June 2016
Abstract
This experiment tested the hypothesis that pigs challenged with an enterotoxigenic strain of E. coli (ETEC) will improve performance by dietary supplementation of sulfur amino acids (SAA) and tryptophan (Trp) above the current recommended levels in the immediate post-weaning period. Male pigs (n = 96) weighing 6.2 ± 0.78 kg (mean ± s.d.) and weaned at 21 days were stratified into one of four treatments based on weaning weight (n = 24). Four diets were formulated [11.2 MJ NE/kg; 20.1% crude protein, 1.25% standardised ileal digestible (SID) lysine (Lys)] according to a 2 × 2 factorial arrangement of treatments with two levels of SID SAA : Lys ratio (0.52 vs 0.60) and two levels of SID Trp : Lys ratio (0.16 vs 0.24). Diets did not contain any antimicrobial compounds. Pigs were individually housed and were fed diets for 14 days after weaning. Pigs were infected with ETEC (3.44 × 108 CFU/mL, serotype O149 : K91 : K88) on Days 5, 6, and 7 after weaning. Pigs were bled on Days 5, 8 and 14 and subsequently analysed for plasma levels of acute-phase proteins, urea, cytokines (Days 5 and 8 only) and amino acids (Days 5 and 8 only). Increasing Trp (P = 0.036) and SAA (P = 0.028) improved feed conversion ratio, and combined supplementation of SAA and Trp further improved FCR than individual supplementation of either SAA or Trp (P = 0.092). Dietary treatments had no impact on the incidence of post-weaning diarrhoea (P > 0.05). Increasing SAA increased shedding of ETEC on Days 12 and 14 after weaning (P < 0.019). Increasing dietary Trp reduced the intensity of inflammation (as measured by APP Index = [(C-reactive protein × PigMAP)/apolipoprotein A1]) immediately after infection with ETEC (P < 0.05), while increasing dietary SAA reduced the APP index on 24 h and 7 days after ETEC infection (P < 0.05). Increasing dietary SAA reduced plasma levels of interferon-gamma regardless of dietary Trp or day of sampling (P = 0.043). Increasing dietary SAA decreased plasma urea (PU) levels on Days 5, 8 and 14 (P < 0.05). These data indicate that Trp supplementation reduced the intensity of inflammation and SAA supplementation decreased the pro-inflammatory interferon-gamma response and improved protein utilisation, as measured by PU, whereas supplementation with both Trp and SAA improved feed conversion ratio.
Additional keywords: E. coli, methionine, tryptophan, weaner pigs.
References
Boisen S (2003) Ideal dietary amino acid profiles for pigs. In ‘Amino acids in animal nutrition’. (Ed. JPF D’Mello) pp. 157–168. (CABI Publishing: Edinburgh)Burrin DG, Stoll B (2003) Intestinal nutrient requirements in weanling pigs. In ‘Weaning the pig: concepts and consequences’. (Eds JR Pluske, J Le Dividich, MWA Verstegen) pp. 301–335. (Wageningen Academic Publishers: Wageningen, The Netherlands)
Capozzalo MM, Kim JC, Htoo JK, de Lange CFM, Mullan BP, Resink JW, Hansen CF, Stumbles PA, Hampson DJ, Ferguson N, Pluske JR (2013) Pigs kept under commercial conditions respond to a higher dietary tryptophan: lysine ratio immediately after weaning. In ‘Manipulating pig production XIV: proceedings of the fourteenth biennial conference of the Australasian Pig Science Association (APSA)’. (Eds JR Pluske JM Pluske) p. 91. (Australasian Pig Science Association: Melbourne)
Capozzalo MM, Kim JC, Htoo JK, de Lange CFM, Mullan BP, Hansen CF, Resink J-W, Stumbles PA, Hampson DJ, Pluske JR (2014) Optimum sulfur amino acid to lysine ratio for weaner pigs infected with enterotoxigenic E. coli. Journal of Animal Science 92, 091
Capozzalo MM, Kim JC, Htoo JK, de Lange CFM, Mullan BP, Hansen CF, Resink J-W, Stumbles PA, Hampson DJ, Pluske JR (2015) Effect of increasing the dietary tryptophan to lysine ratio on plasma levels of tryptophan, kynurenine and urea and on production traits in weaner pigs experimentally infected with an enterotoxigenic strain of Escherichia coli. Archives of Animal Nutrition 69, 17–29.
| Effect of increasing the dietary tryptophan to lysine ratio on plasma levels of tryptophan, kynurenine and urea and on production traits in weaner pigs experimentally infected with an enterotoxigenic strain of Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVCksbg%3D&md5=8ffbc618294c680c951a309a5148b571CAS | 25562691PubMed |
Carpintero R, Pineiro M, Andres M, Iturralde M, Alava MA, Heegaard PMH, Jobert JL, Madec F, Lampreave F (2005) The concentration of apolipoprotein AI decreases during experimentally induced acute-phase processes in pigs. Infection and Immunity 73, 3184–3187.
| The concentration of apolipoprotein AI decreases during experimentally induced acute-phase processes in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvV2itrY%3D&md5=7b63d657d2dccd92ee63e4e9c3d84a3fCAS | 15845530PubMed |
Casini L, Bosi P, Gremokolini C, Trevisi P, Mazzoni M, Bonilauri P (2011) Oral challenge with E. coli K88 as a tool to assess growth and health performance in feeding trials of-weaned pigs. Italian Journal of Animal Science 2, 358–360.
de Ridder K, Levesque CL, Htoo JK, de Lange CFM (2012) Immune system stimulation reduces the efficiency of tryptophan utilization for body protein deposition in growing pigs. Journal of Animal Science 90, 3485–3491.
| Immune system stimulation reduces the efficiency of tryptophan utilization for body protein deposition in growing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKrs7bO&md5=63eeb74be475a9ecd92714c5dc3b273cCAS | 22851250PubMed |
Du Clos TW, Mold C (2004) C-reactive protein. Immunologic Research 30, 261–277.
| C-reactive protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFahu77J&md5=49d362350f196410f2c63c1fc281a8a8CAS | 15531769PubMed |
Fekkes D (1996) State-of-the-art of high-performance liquid chromatographic analysis of amino acids in physiological samples. Journal of Chromatography. B, Biomedical Sciences and Applications 682, 3–22.
| State-of-the-art of high-performance liquid chromatographic analysis of amino acids in physiological samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjvF2qur4%3D&md5=96065038202c9b54365bbb42f97bade5CAS |
Gallois M, Rothkötter HJ, Bailey M, Stokes CR, Oswald IP (2009) Natural alternatives to in-feed antibiotics in pig production: can immunomodulators play a role? Animal 3, 1644–1661.
| Natural alternatives to in-feed antibiotics in pig production: can immunomodulators play a role?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sjt77J&md5=3fc4e2d168c9f7a5518ff66424fe9470CAS | 22443549PubMed |
Gratzfeld-Huesgen A (1998) Sensitive and reliable amino acid analysis in protein hydrolysates using the HP 1100 Series HPLC. Technical Note by Agilent Technologies Publication No. 5968–5658E. Available at https://www.agilent.com/cs/library/technicaloverviews/Public/59685658.pdf [Verified 2 June 2016]
Heegaard PM, Stockmarr A, Piñeiro M, Carpintero R, Lampreave F, Campbell FM, Eckersall PD, Toussaint MJ, Gruys E, Sorensen NS (2011) Optimal combinations of acute phase proteins for detecting infectious disease in pigs. Veterinary Research 42, 50–62.
| Optimal combinations of acute phase proteins for detecting infectious disease in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkslWrs7c%3D&md5=dbb0897117515d7a5a49f6e1ef6cfeefCAS | 21414190PubMed |
Heo J-M, Kim J-C, Hansen CF, Mullan BP, Hampson DJ, Pluske JR (2008) Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhoea and performance after weaning. Archives of Animal Nutrition 62, 343–358.
| Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhoea and performance after weaning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOrurvJ&md5=31c21b3589527802ed21decc735325b9CAS | 18942582PubMed |
Heo JM, Kim JC, Hansen CF, Mullan BP, Hampson DJ, 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, 2833–2843.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFSqu7bN&md5=959f3ff4e2f49347eb8ec3caf25f2810CAS | 19502498PubMed |
Hopwood DE, Hampson DJ (2003) Interactions between the intestinal microflora, diet and diarrhoea, and their influences on piglet health in the immediate post-weaning period. In ‘Weaning the pig: concepts and consequences’. (Eds JR Pluske, J Le Dividich, MWA Verstegen) pp. 199–217. (Wageningen Academic Publishers: Wageningen, The Netherlands)
Jose DG, Good RA (1973) Quantitative effects of nutritional essential amino acid deficiency upon immune responses to tumors in mice. The Journal of Experimental Medicine 137, 1–9.
| Quantitative effects of nutritional essential amino acid deficiency upon immune responses to tumors in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXhtV2lsrs%3D&md5=301ed2357563b8986938da3a3e56ab24CAS | 4688318PubMed |
Kim JC, Heo JM, Mullan BP, Pluske JR (2011a) 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, 222–230.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOrurfM&md5=2f895d38a4c400943e6903550cec32d1CAS |
Kim JC, Mullan BP, Frey B, Capozzalo MM, Payne HG, Mansfield JM, Langridge MD, Pluske JR (2011b) Chronic immune system activation increases the growing pig’s requirement for sulfur amino acids. In ‘Manipulating pig production XIII: proceedings of the thirteenth biennial conference of the Australasian Pig Science Association (APSA)’. (Ed. R van Barneveld) pp. 48. (Australasian Pig Science Association: Adelaide)
Kim JC, Mullan BP, Frey B, Payne HG, Pluske JR (2012) Whole body protein deposition and plasma amino acid profiles in growing and/or finishing pigs fed increasing levels of sulphur amino acids with and without Escherichia coli lipopolysaccharide challenge. Journal of Animal Science 90, 362–365.
| Whole body protein deposition and plasma amino acid profiles in growing and/or finishing pigs fed increasing levels of sulphur amino acids with and without Escherichia coli lipopolysaccharide challenge.Crossref | GoogleScholarGoogle Scholar | 23365380PubMed |
Laich A, Neurauter G, Widner B, Fuchs D (2002) More rapid method for simultaneous measurement of tryptophan and kynurenine by HPLC. Clinical Chemistry 48, 579–581.
Lampreave F, González-Ramón N, Martínez-Ayensa S, Hernández MA, Lorenzo HK, García‐Gil A, Piñeiro A (1994) Characterization of the acute phase serum protein response in pigs. Electrophoresis 15, 672–676.
| Characterization of the acute phase serum protein response in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksFGit7g%3D&md5=d91cdfe4bd4fed7b9357bb1e9e938f91CAS | 7523107PubMed |
Le Floc’h N, Sève B (2007) Biological roles of tryptophan and its metabolism: potential implications for pig feeding. Livestock Science 112, 23–32.
| Biological roles of tryptophan and its metabolism: potential implications for pig feeding.Crossref | GoogleScholarGoogle Scholar |
Le Floc’h N, Melchior D, Obled C (2004a) Modifications of protein and amino acid metabolism during inflammation and immune system activation. Livestock Production Science 87, 37–45.
| Modifications of protein and amino acid metabolism during inflammation and immune system activation.Crossref | GoogleScholarGoogle Scholar |
Le Floc’h N, Melchior D, Sève B (2004b) The importance of dietary tryptophan for preserving growth and controlling inflammatory response of weaned pigs submitted to immune stress. In ‘Animal production in Europe: the way forward in a changing world, proceedings of the International Society for Animal Hygiene’. (Eds F Madec, G Clément) pp. 239–240. (ZOOPOLE: Ploufragan, France)
Le Floc’h N, Jondreville C, Matte JJ, 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, 23–34.
| Importance of sanitary environment for growth performance and plasma nutrient homeostasis during the post-weaning period in piglets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFyqtg%3D%3D&md5=af3042a9ab1d7f6aadb4adc2406b40e3CAS |
Le Floc’h N, LeBellego L, Matte JJ, Melchior D, 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, 1686–1694.
| The effect of sanitary status degradation and dietary tryptophan content on growth rate and tryptophan metabolism in weaning pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlt1OntrY%3D&md5=54a710c02081655aff1c7b5988104a4cCAS | 19151146PubMed |
Li P, Yin Y-l, Li D, Kim SW, Wu G (2007) Amino acids and immune function. British Journal of Nutrition 98, 237–252.
| Amino acids and immune function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFentrg%3D&md5=17b21a4cd46b99f3cd670ef0c943bbfbCAS | 17403271PubMed |
Litvak N, Rakhshandeh A, Htoo JK, de Lange CFM (2013) Immune system stimulation increases the optimal dietary methionine to methionine plus cysteine ratio in growing pigs. Journal of Animal Science 91, 4188–4196.
| Immune system stimulation increases the optimal dietary methionine to methionine plus cysteine ratio in growing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVOlsbrP&md5=66c4ab21c176d635b95b94962055e5dfCAS | 23825332PubMed |
Madec F, Bridoux N, Bounaix S, Cariolet R, Duval-Iflah Y, Hampson DJ, Jestin A (2000) Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field. Veterinary Microbiology 72, 295–310.
| Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ptl2rtQ%3D%3D&md5=3674c4e9ad6d22cd41ffc51d9c955c01CAS | 10727839PubMed |
Makimura S, Suzuki N (1982) Quantitative determination of bovine serum haptoglobin and its elevation in some inflammatory diseases. Japanese Journal of Veterinary Science 44, 15–21.
| Quantitative determination of bovine serum haptoglobin and its elevation in some inflammatory diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XitFelsbY%3D&md5=fdeedb8c583d4723862631ac7762709aCAS | 7098236PubMed |
Malmezat T, Breuille D, Pouyet C, Buffiere C, Denis P, Mirand PP, Obled C (2000) Methionine transsulfuration is increased during spesis in rats. American Journal of Physiology: Endocrinology and Metabolism 279, E1391–E1397.
Melchior D, Sève B, Le Floc’h N (2004) Chronic lung inflammation affects plasma amino acid concentrations in pigs. Journal of Animal Science 82, 1091–1099.
Moffett JR, Namboodiri MA (2003) Tryptophan and the immune response. Immunology and Cell Biology 81, 247–265.
| Tryptophan and the immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFSmtLw%3D&md5=35e4613ad6671e87135bbf0eb015a4fcCAS | 12848846PubMed |
Moore KW, de Waal Malefyt R, Coffman RL, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annual Review of Immunology 19, 683–765.
| Interleukin-10 and the interleukin-10 receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivFKgu70%3D&md5=5197048c198ffa6ebe6e58d4272e0774CAS | 11244051PubMed |
National Research Council (2012) ‘Nutrient requirements of swine.’ pp. 210–212. (National Academies Press: Washington, DC)
Owen KQ, Goodband RD, Nelssen JL, Tokach MD, Dritz SS (1995) The effect of dietary methionine and its relationship to lysine on growth performance of the segregated early-weaned pig. Journal of Animal Science 73, 3666–3672.
Piñeiro C, Piñeiro M, Morales J, Andrés M, Lorenzo E, del Pozo M, Alava MA, Lampreave F (2009) Pig-MAP and haptoglobin concentration reference values in swine from commercial farms. Veterinary Journal (London, England) 179, 78–84.
| Pig-MAP and haptoglobin concentration reference values in swine from commercial farms.Crossref | GoogleScholarGoogle Scholar |
Pluske JR, Hampson DJ, Williams IH (1997) Factors influencing the structure and function of the small intestine in the weaned pig: A review. Livestock Production Science 51, 215–236.
| Factors influencing the structure and function of the small intestine in the weaned pig: A review.Crossref | GoogleScholarGoogle Scholar |
Pluske JR, Pethick DW, Hopwood DE, Hampson DJ (2002) Nutritional influences on some major enteric bacterial diseases of pigs. Nutrition Research Reviews 15, 333–371.
| Nutritional influences on some major enteric bacterial diseases of pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1KlsL8%3D&md5=f120ee9a75c1e4908fb774297eb07386CAS | 19087411PubMed |
Rakhshandeh A, Rademacher M, de Lange CFM (2007) Effect of immune system stimulation and dietary methionine plus cysteine intake on protein deposition and digestibility in growing pigs. In ‘Energy and protein metabolism and nutrition: European Association for Animal Production Publication No. 124’. (Eds I Ortigues-Marty, N Miraux W Brand-Williams) pp. 171–172. (Wageningen Academic Publishers: Wageningen, The Netherlands)
Reeds PJ, Jahoor F (2001) The amino acid requirements of disease. Clinical Nutrition (Edinburgh, Lothian) 20, 15–22.
| The amino acid requirements of disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVyrtb4%3D&md5=3da00e511f3fec231ae67d2fb11de5cfCAS |
Sauvant D, Perez J-M, Tran G (2004) ‘Tables of composition and nutritional value of feed materials: pigs, poultry, cattle, sheep, goats, rabbits, horses and fish.’ (Wageningen Academic Publishers: Wageningen, The Netherlands)
Shen YB, Voilqué G, Kim JD, Odle J, Kim SW (2012) Effects of increasing tryptophan intake on growth and physiological changes in nursery pigs. Journal of Animal Science 90, 2264–2275.
| Effects of increasing tryptophan intake on growth and physiological changes in nursery pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFehsbvJ&md5=b4b31ca8cb793f8fd4ea16dabf8c23f0CAS | 22287672PubMed |
Simongiovanni A, Corrent E, Le Floc’h N, van Milgen J (2010) Estimation of the tryptophan requirement in piglets by meta-analysis. Journées de la Recherche Porcine en France 42, 107–112.
Skinner JG (2001) International standardization of acute phase proteins. Veterinary Clinical Pathology 30, 2–7.
| International standardization of acute phase proteins.Crossref | GoogleScholarGoogle Scholar | 12024323PubMed |
Trevisi P, Melchior D, Mazzoni M, Casini L, De Filippi S, Minieri L, Lalatta-Costerbosa G, Bosi P (2009) A tryptophan-enriched diet improves feed intake and growth performance of susceptible weanling pigs orally challenged with Escherichia coli K88. Journal of Animal Science 87, 148–156.
| A tryptophan-enriched diet improves feed intake and growth performance of susceptible weanling pigs orally challenged with Escherichia coli K88.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFOmtQ%3D%3D&md5=ab5300cada2a480fea7fbab8782a24beCAS | 18791156PubMed |
Zhang G, Ross CR, Dritz SS, Nietfeld JC, Blecha F (1997) Salmonella infection increases porcine antibacterial peptide concentrations in serum. Clinical and Diagnostic Laboratory Immunology 4, 774–777.
