Effect of alginate and inulin on intestinal microbial ecology of weanling pigs reared under different husbandry conditions

FEMS Microbiology Ecology

Volumn 72, Issue 1, 2010, Pages 132-142

  Janczyk, Pawel ^a   Pieper, Robert ^a   Smidt, Hauke ^b   Souffrant, Wolfgang B ^a  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Alginate; Husbandry; Intestinal microbiota; Inulin; Prebiotics; Weanling pig

Indexed keywords

ALGINIC ACID; GLUCURONIC ACID; HEXURONIC ACID; INULIN; PREBIOTIC AGENT;

AGEISM; ALGINATE; ARTIFICIAL DIET; BACTERIUM; DIGESTIVE SYSTEM; ECOPHYSIOLOGY; ELECTROKINESIS; EXPERIMENTAL STUDY; GENETIC ANALYSIS; METABOLITE; MICROBIAL ECOLOGY; MULTIVARIATE ANALYSIS; PIG; RNA; YEAST;

ANIMAL; ANIMAL FOOD; ANIMAL HUSBANDRY; ARTICLE; BACTERIAL COUNT; BACTERIUM; CECUM; CHEMISTRY; COLON; COMPARATIVE STUDY; ENTEROCOCCACEAE; GENETICS; GROWTH, DEVELOPMENT AND AGING; ILEUM; INTESTINE; ISOLATION AND PURIFICATION; LACTOBACILLUS; MICROBIOLOGY; PH; RNA GENE; SWINE; WEANING; YEAST;

ALGINATES; ANIMAL FEED; ANIMAL HUSBANDRY; ANIMALS; BACTERIA; CECUM; COLON; COLONY COUNT, MICROBIAL; ENTEROCOCCACEAE; GENES, RRNA; GLUCURONIC ACID; HEXURONIC ACIDS; HYDROGEN-ION CONCENTRATION; ILEUM; INTESTINES; INULIN; LACTOBACILLUS; PREBIOTICS; SWINE; WEANING; YEASTS;

ENTEROCOCCUS; LACTOBACILLUS; SUIDAE;

EID: 77949284424     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2009.00826.x     Document Type: Article

References (50)

1. Bailey M, Haverson K, Inman C, Harris C, Jones P, Corfield G, Miller B Stokes C (2005) The influence of environment on development of the mucosal immune system. Vet Immunol Immunop 108 : 189 198.
2. Brownlee IA, Allen A, Pearson JP, Dettmar PW, Havler ME, Atherton MR Onsøyen E (2005) Alginate as source of dietary fiber. Crit Rev Food Sci 45 : 497 510.
3. Canibe N, Steien SH, Overland M Jensen BB (2001) Effect of K-diformate in starter diets on acidity, microbiota, and the amount of organic acids in the digestive tract of piglets, and on gastric alterations. J Anim Sci 79 : 2123 2133.
4. Eberhard M, Hennig U, Kuhla S, Brunner RM, Kleesen B Metges CC (2007) Effect of inulin supplementation on selected gastric, duodenal, and caecal microbiota and short chain fatty acid pattern in growing piglets. Arch Anim Nutr 61 : 235 246.
5. Franklin MA, Mathews AG, Vickers JR Clift RA (2002) Characterization of microbial populations and volatile fatty acid concentrations in the jejunum, ileum and caecum of pigs weaned at 17 vs 24 days of age. J Anim Sci 80 : 2904 2910.
6. Fuentes S, Egert M, Jiménez-Valera M, Ramos-Cormenzana A, Ruiz-Bravo A, Smidt H Monteoliva-Sanchez M (2008) Administration of Lactobacillus casei and Lactobacillus plantarum affects the diversity of murine intestinal lactobacilli, but not the overall bacterial community structure. Res Microbiol 159 : 237 243.
7. Haacker K, Block HJ Weissbach F (1983) On the colorimetric determination of lactic-acid in silages with para-hydroxy diphenyl. Arch Anim Nutr 33 : 505 512.
8. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54 : 427 431.
9. Hoebler C, Guillon F, Darcy-Vrillon B, Vaugelade P, Lahaye M, Worthington E, Duée P-H Barry J-L (2000) Supplementation of pig diet with algal fibre changes the chemical and physicochemical characteristics of digesta. J Sci Food Agr 80 : 1357 1364.
10. Howard MD, Gordon DT, Pace LW, Garleb KA Kerley MS (1995) Effects of dietary supplementation with fructooligosaccharides on colonic microbiota populations and epithelial cell proliferation in neonatal pigs. J Pediatr Gastr Nutr 21 : 297 303.
11. Janczyk P, Pieper R, Smidt H Souffrant WB (2007a) Changes in the diversity of pig ileal lactobacilli around weaning determined by means of 16S rRNA-gene amplification and denaturing gradient gel electrophoresis. FEMS Microbiol Ecol 61 : 132 140.
12. Janczyk P, Pieper R, Smidt H, Souffrant WB, Bimczok D, Rothkötter H-J Smidt H (2007b) Parenteral long-acting amoxicillin reduces intestinal bacterial community diversity in piglets even 5 weeks after the administration. ISME J 1 : 180 183.
13. Janczyk P, Trevisi P, Souffrant WB Bosi P (2008) Effect of thymol on microbial diversity in the porcine jejunum. Int J Food Microbiol 126 : 258 261.
14. Klasing KC Johnstone BJ (1991) Monokines in growth and development. Poultry Sci 70 : 1781 1789.
15. Kluess J (2004) Evaluation of ileal digesta in weaning piglets fed different diets. Ph.D. thesis, Free University of Berlin, Berlin. Available at
16. Knura-Deszczka S (2000) Evaluation of haptoglobin as a parameter of assessment of health status of fattening pigs. Dissertation, School of Veterinary Medicine Hannover, Hannover, Germany. Available at
17. Konstantinov SR, Zhu WY, Williams BA, Tamminga S, de Vos WM Akkermans ADL (2003) Effect of fermentable carbohydrates on piglet faecal communities as revealed by DGGE analysis of 16S ribosomal RNA. FEMS Microbiol Ecol 43 : 225 235.
18. Konstantinov SR, Awati A, Smidt H, Williams BA, Akkermans ADL de Vos WM (2004) Specific response of a novel and abundant Lactobacillus amylovorus-like phylotype to dietary prebiotics in the guts of weaning piglets. Appl Environ Microb 70 : 3821 3830.
19. Lallès JP, Bosi P, Janczyk P, Koopmans SJ Torrallardona D (2009) Impact of bioactive substances on the gastrointestinal tract and performance of weaned piglets, a review. Animal 3 : 1625 1643.
20. Le Floc'h N, Jondreville C, Matte JJ Seve B (2006) Importance of sanitary environment for growth performance and plasma nutrient homeostasis during the post-weaning period in piglets. Arch Anim Nutr 60 : 23 34.
21. Lepš J šmilauer P (2003) Multivariate Analysis of Ecological Data Using CANOCO. Cambridge University Press, Cambridge.
22. Loh G, Eberhard M, Brunner RM, Hennig U, Kuhla S, Kleesen B Metges CC (2006) Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. J Nutr 136 : 1198 1202.
23. Magurran AE (2004) Measuring Biological Diversity. Blackwell Science Ltd, Oxford.
24. McCann KS (2000) The diversity-stability debate. Nature 405 : 228 233.
25. McCracken BA, Spurlock ME, Roos MA, Zuckermann FA Gaskins HR (1999) Weaning anorexia may contribute to local inflammation in the piglet small intestine. J Nutr 129 : 613 619.
26. Mikkelsen LL, Bendixen C, Jakobsen M Jensen BB (2003) Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl Environ Microb 69 : 654 658.
27. Mountzouris KC, Balaskas C, Fava F, Tuohy KM, Gibson GR Fegeros K (2006) Profiling of composition and metabolic activities of the colonic microflora of growing pigs fed diets supplemented with prebiotic oligosaccharides. Anaerobe 12 : 178 185.
28. Nabuurs M (1991) Etiologic and pathogenic studies on postweaning diarrhoea. PhD Thesis, University of Utrecht, Utrecht, The Netherlands.
29. Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178 : 5636 5643.
30. Petersen HH, Ersbøll AK, Jensen CS Nielsen JP (2002) Serum-haptoglobin concentration in Danish slaughter pigs of different health status. Prev Vet Med 54 : 325 335.
31. Petersen HH, Nielsen JP Heegaard PMH (2004) Application of acute phase protein measurements in veterinary clinical chemistry. Vet Res 35 : 163 187.
32. Pié S, Lalles JP, Blazy F, Laffitte J, Seve B Oswald IP (2004) Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr 134 : 641 647.
33. Pieper R, Janczyk P, Schumann R Souffrant WB (2006) The intestinal microflora of piglets around weaning - with emphasis on lactobacilli. Arch Zootec 9 : 28 40.
34. Pieper R, Janczyk P, Zeyner A, Smidt H, Guiard V Souffrant WB (2008) Ecophysiology of the developing total bacterial and Lactobacillus communities in the terminal small intestine of weaning piglets. Microb Ecol 56 : 474 483.
35. Pieper R, Janczyk P, Urubschurov V, Korn U, Pieper B Souffrant WB (2009) Effect of a single oral administration of Lactobacillus plantarum DSMZ 8862/8866 before and at the time point of weaning on intestinal microbial communities in piglets. Int J Food Microbiol 130 : 227 232.
36. Pierce KM, Sweeney T, Brophy PO, Callan JJ, McCarthy P O'Doherty JV (2005) Dietary manipulation post weaning to improve piglet performance and gastro-intestinal health. Anim Sci 81 : 347 356.
37. Pierce KM, Sweeney T, Brophy PO, Callan JJ, Fitzpatrick E, McCarthy P O'Doherty JV (2006) The effect of lactose and inulin on intestinal morphology, selected microbial populations and volatile fatty acid concentrations in the gastro-intestinal tract of the weanling pig. Anim Sci 82 : 311 318.
38. Pluske JR, Hampson DJ Williams IH (1997) Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest Prod Sci 51 : 215 236.
39. Pluske JR, Durmic Z, Payne HG, Mansfield J, Mullan BP, Hampson DJ Vercoe PE (2007) Microbial diversity in the large intestine of pigs born and reared in different environments. Livest Sci 108 : 113 116.
40. Simpson EH (1949) Measurement of diversity. Nature 163 : 688.
41. Simpson JM, McCracken VJ, White BA, Gaskins HR Mackie RI (1999) Application of denaturant gradient gel electrophoresis for the analysis of the porcine gastrointestinal microbiota. J Microbiol Meth 36 : 167 179.
42. Sokal RR Rohlf FJ (1995) Biometry. The principles and Practice of Statistics in Biological Research. W.H. Freeman and Co., New York.
43. Spreeuwenberg MAM, Verdonk JMAJ, Gaskins HR Verstegen MWA (2001) Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. J Nutr 131 : 1520 1527.
44. Tako E, Glahn RP, Welch RM, Lei X, Yasuda K Miller DD (2007) Dietary inulin affects the expression of intestinal eneterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. Brit J Nutr 99 : 472 480.
45. ter Braak CJF (1987) The analysis of vegetation-environment relationships by canonical correspondance analysis. Vegetation 69 : 69 77.
46. ter Braak CJF šmilauer P (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca, NY.
47. Tzeneva VA, Salles JF, Naumova N, de Vos WM, Kuikman PJ, Dolfing J Smidt H (2009) Effect of soil sample preservation, compared to the effect of other environmental variables, on bacterial and eukaryotic diversity. Res Microbiol 160 : 89 98.
48. Urubschurov V, Janczyk P, Pieper R Souffrant WB (2008) Biological diversity of yeasts in the gastrointestinal tract of weaned piglets kept under different farm conditions. FEMS Yeast Res 8 : 1349 1356.
49. Verdonk JMAJ, Shim SB, van Leeuwen P Verstegen MWA (2005) Application of inulin-type fructans in animal feed and pet food. Brit J Nutr 93 (suppl 1) : 125 138.
50. Wang Y, Han F, Hu B, Li J Yu W (2006) In vivo prebiotic properties of alginate oligosaccharides prepared through enzymatic hydrolysis of alginate. Nutr Res 26 : 597 603.