Effect of dietary protein supply originating from soybean meal orcasein on the intestinal microbiota of piglets

Anaerobe

Volumn 25, Issue , 2014, Pages 72-79

  Rist, Vanessa T S ^a   Weiss, Eva ^a   Sauer, Nadja ^a   Mosenthin, Rainer ^a   Eklund, Meike ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Intestinal microbiota; Piglet; Protein level; Protein source

Indexed keywords

CASEIN; PROTEIN INTAKE;

ANIMAL EXPERIMENT; ARTICLE; BACTEROIDES; BIFIDOBACTERIUM; CLOSTRIDIUM; DIETARY FIBER; ENTEROBACTERIACEAE; FECES ANALYSIS; FERMENTATION; GASTROINTESTINAL SYMPTOM; GENE DOSAGE; INTESTINE FLORA; LACTOBACILLUS; NONHUMAN; PIGLET; PORPHYROMONAS; PREVOTELLA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTAKE; REAL TIME POLYMERASE CHAIN REACTION; SOYBEAN; ANIMAL; ANIMAL FOOD; BACTERIA; BACTERIAL LOAD; BIOTA; CLASSIFICATION; DIET; FECES; GENETICS; ILEUM; METABOLISM; MICROBIOLOGY; NEWBORN; PROCEDURES; SWINE;

ANIMAL FEED; ANIMALS; ANIMALS, NEWBORN; BACTERIA; BACTERIAL LOAD; BIOTA; CASEINS; DIET; DIETARY PROTEINS; FECES; ILEUM; REAL-TIME POLYMERASE CHAIN REACTION; SOYBEANS; SWINE;

EID: 84891354359     PISSN: 10759964     EISSN: 10958274     Source Type: Journal    
DOI: 10.1016/j.anaerobe.2013.10.003     Document Type: Article

References (67)

1. Aherne F., Hogberg M.G., Kornegay E.T., Shurson G.C., Brocksmith M., Brocksmith S., et al. Pork industry handbook 1992, National Pork Producers Council, Des Moines, IA. 111th ed.
2. Wellock I.J., Fortomaris P.D., Houdijk J.G.M., Kyriazakis I. Effects of dietary protein supply, weaning age and experimental entertoxigenic Escherichia coli infection on newly weaned pigs: health. Animal 2008, 2:834-842.
3. Klose V., Bayer K., Bruckbeck R., Schatzmayr G., Loibner A.P. Invitro antagonistic activities of animal intestinal strains against swine-associated pathogens. Vet Microbiol 2010, 144:515-521.
4. Sørensen M.T., Vestergaard E.M., Jensen S.K., Lauridsen C., Højsgaard S. Performance and diarrhoea in piglets following weaning at seven weeks of age: challenge with E.coli O 149 and effect of dietary factors. Livest Sci 2009, 123:314-321.
5. Mosenthin R., Hambrecht E., Sauer W.C. Utilisation of different fibres in piglet feeds. Recent advances in animal nutrition 1999, 227-256. Nottingham University Press, Nottingham, UK. P.C. Garnsworthy, J. Wiseman (Eds.).
6. Mul A.J., Perry F.G. The role of fructo-oligosaccharides in animal nutrition. Recent advances in animal nutrition 1994, 57-79. Nottingham University Press, Nottingham, UK. P.C. Garnsworthy, D.J.A. Cole (Eds.).
7. Bauer E., Williams B.A., Smidt H., Mosenthin R., Verstegen M.W.A. Influence of dietary components on development of the microbiota in single-stomached species. Nutr Res Rev 2006, 19:63-78.
8. Heo J.M., Opapeju F.O., Pluske J.R., Kim J.C., Hampson D.J., Nyachoti C.M. Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. JAnim Physiol Anim Nutr 2013, 97:207-237.
9. Mackie R.I., Stroot P.G., Varel V.H. Biochemical identification and biological origin of key odor components in livestock waste. JAnim Sci 1998, 76:1331-1342.
10. Bertschinger H.U., Eggenberger E., Jucker H., Pfirter H.P. Evaluation of low nutrient, high fibre diets for the prevention of porcine Escherichia coli enterotoxaemia. Vet Microbiol 1979, 3:281-290.
11. Hampson D.J. Postweaning Escherichia coli diarrhoea in pigs. Escherichia coli in domestic animals and humans 1994, 171-191. CAB Int., Wallingford, UK. C.L. Gyles (Ed.).
12. Libao-Mercado A.J.O., Zhu C.L., Cant J.P., Lapierre H., Thibault J.N., Sève B., et al. Dietary and endogenous amino acids are the main contributors to microbial protein in the upper gut of normally nourished pigs. JNutr 2009, 139:1088-1094.
13. Wellock I.J., Fortomaris P.D., Houdijk J.G.M., Kyriazakis I. The effect of dietary protein supply on the performance and risk of post-weaning enteric disorders in newly weaned pigs. Anim Sci 2006, 82:327-335.
14. Hillman K., Spencer R.J., Murdoch T.A., Stewart C.S. The effect of mixtures of Lactobacillus spp. on the survival of enterotoxigenic Escherichia coli in invitro continuous culture of porcine intestinal bacteria. Lett Appl Microbiol 1995, 20:130-133.
15. Pluske J.R., Pethick D.W., Hopwood D.E., Hampson D.J. Nutritional influences on some major enteric bacterial diseases of pigs. Nutr Res Rev 2002, 15:333-371.
16. Manzanilla E.G., Pérez J.F., Martín M., Blandón J.C., Baucells F., Kamel C., et al. Dietary protein modifies effect of plant extracts in the intestinal ecosystem of the pig at weaning. JAnim Sci 2009, 87:2029-2037.
17. Nørgaard J.V., Fernández J.A., Jørgensen H. Ileal digestibility of sunflower meal, pea, rapeseed cake, and lupine in pigs. JAnim Sci 2012, 90:203-205.
18. Robinson I.M., Allison M.J., Bucklin J.A. Characterization of the cecal bacteria of normal pigs. Appl Environ Microbiol 1981, 41:950-955.
19. Claesson M.J., Cusack S., O'Sullivan O., Greene-Diniz R., de Weerd H., Flannery E., et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. PNAS 2010, 108:4586-4591.
20. Gibson G.R., Roberfroid M.B. Dietary modulation of the human colonic microbiota: introducing the concept of probiotics. JNutr 1995, 125:1401-1412.
21. Lorz A., Metzger E. Tierschutzgesetz: Tierschutzgesetz mit allgemeiner Verwaltungsvorschrift, Rechtsverordnung und europaeischen Uebereinkommen 1999, Kommentar, Beck, Munich, Germany. 5th ed.
22. Li S., Sauer W.C., Fan M.Z. The effect of dietary crude protein level on amino acid digestibility in early-weaned pigs. JAnim Physiol Anim Nutr 1993, 70:26-37.
23. National Research Council (NRC) Nutrient requirements of swine, tenth rev 1998, Nat. Acad. Press, Washington, D.C.
24. Naumann C., Basler R. Die chemische Untersuchung von Futtermitteln 1997, VDLUFA-Methodenbuch Band III, VDLUFA-Verlag, Germany, Darmstadt.
25. Lee C., Kim J., Shin S.G., Hwang S. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. JBiotechnol 2006, 123:273-280.
26. Metzler-Zebeli B.U., Ratriyanto A., Jezierny D., Sauer N., Eklund M., Mosenthin R. Effects of betaine, organic acids and inulin as single feed additives or in combination on bacterial populations in the gastrointestinal tract of weaned pigs. Arch Anim Nutr 2009, 63:427-441.
27. Rist V.T.S., Bauer E., Eklund M., Sauer N., Mosenthin R. Effect of feeding level on the composition of the intestinal microbiota in weaned piglets. JAnim Sci 2012, 90:19-21.
28. Pieper R., Kröger S., Richter J.F., Wang J., Martin L., Bindelle J., et al. Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. JNutr 2012, 142:661-667.
29. Hermes R.G., Molist F., Ywazaki M., Nofrarías M., Gomez de Segura A., Gasa J., et al. Effect of dietary level of protein and fiber on the productive performance and health status of piglets. JAnim Sci 2009, 87:3569-3577.
30. Castillo M., Skene G., Roca M., Anguita M., Badiola I., Duncan S.H., et al. Application of 16S rRNA gene-targetted fluorescence in situ hybridization and restriction fragment length polymorphism to study porcine microbiota along the gastrointestinal tract in response to different sources of dietary fibre. FEMS Microbiol Ecol 2007, 59:138-146.
31. Sauer N., Eklund M., Gänzle M.G., Field C.J., Zijlstra R.T., Mosenthin R. The effects of pure nucleotides on performance, humoral immunity, gut structure and numbers of intestinal bacteria of newly weaned pigs. JAnim Sci 2012, 90:3126-3134.
32. Awati A., Konstantinov S.R., Williams B.A., Akkermans A.D.L., Bosch M.W., Smidt H., et al. Effect of substrate adaptation on the microbial fermentation and microbial composition of faecal microbiota of weaning piglets studied invitro. JSci Food Agric 2005, 85:1765-1772.
33. Choct M., Dersjant-Li Y., McLeish J., Peisker M. Soy oligosaccharides and soluble non-starch polysaccharides: a review of digestion, nutritive and anti-nutritive effects in pigs and poultry, Asian-Aust. JAnim Sci 2010, 23:1386-1398.
34. Metzler B.U., Bauer E., Mosenthin R. Microflora management in the gastrointestinal tract of piglets, Asian-Austr. JAnim Sci 2005, 18:1353-1362.
35. Houdijk J.G.M., Bosch M.W., Verstegen M.W.A., Berenpas H.J. Effects of dietary oligosaccharides on the growth performance and faecal characteristics of young growing pigs. Anim Feed Sci Technol 1998, 71:35-48.
36. Mosenthin R., Sauer W.C., Henkel H., Ahrens F., de Lange C.F.M. Tracer studies of urea kinetics in growing pigs: II. The effect of starch infusion at the distal ileum on urea recycling and bacterial nitrogen excretion. JAnim Sci 1992, 70:3467-3472.
37. Cervantes-Pahm S.K., Stein H.H. Ileal digestibility of amino acids in conventional, fermented, and enzyme-treated soybean meal and in soy protein isolate, fish meal, and casein fed to weanling pigs. JAnim Sci 2010, 88:2674-2683.
38. Heo J.M., Kim J.C., Hansen C.F., Mullan B.P., Hampson D.J., Pluske J.R. Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhoea and performance after weaning. Arch Anim Nutr 2008, 62:343-358.
39. Bikker P., Dirkzwager A., Fledderus J., Trevisi P., le Huërou-Luron I., Lallès J.P., et al. Dietary protein and fermentable carbohydrates contents influence growth performance and intestinal characteristics in newly weaned pigs. Livest Sci 2007, 108:194-197.
40. Jeaurond E.A., Rademacher M., Pluske J.R., Zhu C.H., de Lange C.F.M. Impact of feeding fermentable proteins and carbohydrates on growth performance, gut health and gastrointestinal function of newly weaned pigs. Can J Anim Sci 2008, 88:271-281.
41. Nyachoti C.M., Omogbenigun F.O., Rademacher M., Blank G. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. JAnim Sci 2006, 84:125-134.
42. Anugwa F.O.I., Varel V.H., Dickson J.S., Pond W.G., Krook L.P. Effects of dietary fiber and protein concentration on growth, feed efficiency, visceral organ weights and large intestine microbial populations of swine. JNutr 1989, 119:879-886.
43. Konstantinov S.R., Zhu W.Y., Williams B.A., Tamminga S., de Vos W.M., Akkermans A.D.L. Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gel electrophoresis analysis of 16S ribosomal DNA. FEMS Micobiol Ecol 2003, 43:225-235.
44. Lynch B., Callan J.J., O'Doherty J.V. The interaction between dietary crude protein and fermentable carbohydrate source on piglet post weaning performance, diet digestibility and selected faecal microbial populations and volatile fatty acid concentration. Livest Sci 2009, 124:93-100.
45. Atasoglu C., Valdes C., Walker N.D., Newbold C.J., Wallace R.J. De novo synthesis of amino acids by the ruminal bacteria Prevotella bryantii B14, Selenomonas ruminantium HD4, and Streptococcus bovis ES1. Appl Environ Microbiol 1998, 64:2836-2843.
46. Atasoglu C., Valdes C., Newbold C.J., Wallace R.J. Influence of peptides and amino acids on fermentation rate and de novo synthesis of amino acids by mixed microorganisms from the sheep rumen. Brit J Nutr 1999, 81:307-314.
47. Canibe N., Jensen B.B. Fermented and nonfermented liquid feed to growing pigs: effect on aspects of gastrointestinal ecology and growth performance. JAnim Sci 2003, 81:2019-2031.
48. Rolfe R. Colonization resistance. Gastrointestinal microbes and host interactions 1997, Vol 2:501-536. Chapman and Hall, New York. R.I. Mackie, B.A. White, R.E. Isaacson (Eds.).
49. Bikker P., Dirkzwager A., Fledderus J., Trevisi P., le Huërou-Luron I., Lallès J.P., et al. The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. JAnim Sci 2006, 84:3337-3345.
50. Lan Y., Williams B.A., Tamminga S., Boer H., Akkermans A., Erdi G., et al. Invitro fermentation kinetics of some non-digestible carbohydrates by the caecal microbial community of broilers. Anim Food Sci Technol 2005, 123-124:687-702.
51. Smiricky-Tjardes M.R., Grieshop C.M., Flickinger E.A., Bauer L.L., Fahey G.C. Dietary galactooligosaccharides affect ileal and total-tract nutrient digestibility, ileal and fecal bacterial concentrations, and ileal fermentative characteristics of growing pigs. JAnim Sci 2003, 81:2535-2545.
52. Bach Knudsen K.E. Carbohydrate and lignin contents of plant materials used in animal feeding. Anim Feed Sci Technol 1997, 67:319-338.
53. Loh G., Eberhard M., Brunner R.M., Hennig U., Kuhla S., Kleessen B., et al. Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. JNutr 2006, 136:1198-1202.
54. Mikkelsen L.L., Jensen B.B. Effect of fructo-oligosaccharides and transgalacto-oligosaccharides on microbial populations and microbial activity in the gastrointestinal tract of piglets post-weaning. Anim Feed Sci Technol 2004, 117:107-119.
55. Mølbak L., Thomsen L.E., Jensen T.K., Bach Knudsen K.E., Boye M. Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. JAppl Microbiol 2007, 103:1853-1867.
56. Smiricky-Tjardes M.R., Flickinger E.A., Grieshop C.M., Bauer L.L., Murphy M.R., Fahey G.C. Invitro fermentation characteristics of selected oligosaccharides by swine fecal microflora. JAnim Sci 2003, 81:2505-2514.
57. Eklund M., Mosenthin R., Piepho H.P., Rademacher M. Effect of dietary crude protein level on basal ileal endogenous losses and standardized ileal digestibilities of crude protein and amino acids in newly weaned pigs. JAnim Physiol Anim Nutr 2008, 92:578-590.
58. Eklund M., Mosenthin R., Piepho H.P., Rademacher M. Estimates of dietary threshold levels for crude protein and amino acids to obtain plateau values of apparent ileal crude protein and amino acid digestibilities in newly weaned pigs. Arch Anim Nutr 2010, 64:357-372.
59. Li D.F., Nelssen J.L., Reddy P.G., Blecha F., Klemm R., Goodband R.D. Interrelationship between hypersensitivity to soybean proteins and growth performance in early-weaned pigs. JAnim Sci 1991, 69:4062-4069.
60. Heo J.M., Kim J.C., Hansen C.F., Mullan B.P., Hampson D.J., Pluske J.R. Feeding a diet with a decreased protein content reduces both nitrogen content in the gastrointestinal tract and post-weaning diarrhoea, but does not affect apparent nitrogen digestibility in weaner pigs challenged with an enterotoxigenic strain of Escherichia coli. Anim Feed Sci Tech 2010, 160:148-159.
61. Lee D.H., Zo Y.G., Kim S.J. Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand-conformation polymorphism. Appl Environ Microbiol 1996, 62:3112-3120.
62. Walter J., Hertel C., Tannock G.W., Lis C.M., Munro K., Hammes W.P. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 2001, 67:2578-2585.
63. Heilig H.G.H.J., Zoetendal E.G., Vaughan E.E., Marteau P., Akkermans A.D.L., de Vos V.M. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 2002, 68:114-123.
64. Bartosch S., Fite A., Macfarlane G.T., McMurdo M.E.T. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 2004, 70:3575-3581.
65. Rinttilä T., Kassinen A., Malinen E., Krogius L., Palva A. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. JAppl Microbiol 2004, 97:1166-1177.
66. Matsuki T., Watanabe K., Fujimoto J., Takada T., Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 2004, 70:7220-7228.
67. Matsuki T., Watanabe K., Fujimoto J., Miyamoto Y., Takada T., Matsumoto K., et al. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 2002, 68:5445-5451.