Assessment of the probiotic potential of a dairy product fermented by propionibacterium freudenreichii in piglets

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 32, 2012, Pages 7917-7927

  Cousin, Fabien J ^a,b,c   Foligné, Benoît ^d   Deutsch, Stéphanie Marie ^a,b   Massart, Sébastien ^e   Parayre, Sandrine ^a,b   Loir, Yves Le ^a,b   Boudry, Gaëlle ^f   Jan, Gwénaël ^a,b  

^a UMR1253   (France)

^b AGROCAMPUS OUEST   (France)

^c CNIEL/Syndifrais   (France)

^d UNIV LILLE   (France)

^e DNAVision SA   (Belgium)

^f CEMAGREF   (France)

Author keywords

dairy propionibacteria; immunomodulation; intestinal barrier; pig; probiotic

Indexed keywords

IMMUNOMODULATION; INTESTINAL BARRIER; PIG; PROBIOTICS; PROPIONIBACTERIA;

RNA; STRAIN;

DAIRY PRODUCTS;

INTERLEUKIN 8; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ARTICLE; COLON; EATING; FEMALE; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; IMMUNOMODULATION; INTESTINE MUCOSA; MALE; MICROBIOLOGY; MILK; PHYSIOLOGY; PROPIONIBACTERIUM; SECRETION (PROCESS); SPECIES DIFFERENCE; SWINE;

ANIMALS; COLON; EATING; FEMALE; FERMENTATION; IMMUNOMODULATION; INTERLEUKIN-8; INTESTINAL MUCOSA; MALE; MILK; PROBIOTICS; PROPIONIBACTERIUM; SPECIES SPECIFICITY; SUS SCROFA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84865127914     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf302245m     Document Type: Article

References (65)

1. Cousin, F. J.; Mater, D.; Foligné, B.; Jan, G. Dairy propionibacteria as human probiotics: A review of recent evidence Dairy Sci. Technol. 2011, 91 (1) 1-26
2. Bouglé, D.; Roland, N.; Lebeurrier, F.; Arhan, P. Effect of propionibacteria supplementation on fecal bifidobacteria and segmental colonic transit time in healthy human subjects Scand. J. Gastroenterol. 1999, 34 (2) 144-148 (Pubitemid 29138863)
3. Foligné, B.; Deutsch, S. M.; Breton, J.; Cousin, F. J.; Dewulf, J.; Samson, M.; Pot, B.; Jan, G. Promising immunomodulatory effects of selected strains of dairy propionibacteria as evidenced in vitro and in vivo Appl. Environ. Microbiol. 2010, 76 (24) 8259-8264
4. Deutsch, S. M.; Parayre, S.; Bouchoux, A.; Guyomarch, F.; Dewulf, J.; Dols-Lafargue, M.; Baglinière, F.; Cousin, F. J.; Falentin, H.; Jan, G.; Foligné, B. Contribution of surface beta-glucan polysaccharide to physicochemical and immunomodulatory properties of Propionibacterium freudenreichii Appl. Environ. Microbiol. 2012, 78 (6) 1765-1775
5. Hervé, C.; Fondrevez, M.; Cheron, A.; Barloy-Hubler, F.; Jan, G. Transcarboxylase mRNA: A marker which evidences P. freudenreichii survival and metabolic activity during its transit in the human gut Int. J. Food Microbiol. 2007, 113 (3) 303-314 (Pubitemid 46151695)
6. Lan, A.; Bruneau, A.; Philippe, C.; Rochet, V.; Rouault, A.; Hervé, C.; Roland, N.; Rabot, S.; Jan, G. Survival and metabolic activity of selected strains of Propionibacterium freudenreichii in the gastrointestinal tract of human microbiota-associated rats Br. J. Nutr. 2007, 97 (4) 714-724 (Pubitemid 46470680)
7. Hosseini, E.; Grootaert, C.; Verstraete, W.; Van de Wiele, T. Propionate as a health-promoting microbial metabolite in the human gut Nutr. Rev. 2011, 69 (5) 245-258
8. Wong, J. M.; de, S. R.; Kendall, C. W.; Emam, A.; Jenkins, D. J. Colonic health: Fermentation and short chain fatty acids J. Clin. Gastroenterol. 2006, 40 (3) 235-243 (Pubitemid 44309560)
9. Lan, A.; Bruneau, A.; Bensaada, M.; Philippe, C.; Bellaud, P.; Rabot, S.; Jan, G. Increased induction of apoptosis by Propionibacterium freudenreichii TL133 in colonic mucosal crypts of human microbiota-associated rats treated with 1,2-dimethylhydrazine Br. J. Nutr. 2008, 100, 1251-1259
10. Foo, N. P.; Ou, Y. H.; Chiu, H. H.; Chan, H. Y.; Liao, C. C.; Yu, C. K.; Wang, Y. J. Probiotics prevent the development of 1,2-dimethylhydrazine (DMH)-induced colonic tumorigenesis through suppressed colonic mucosa cellular proliferation and increased stimulation of macrophages J. Agric. Food Chem. 2011, 59 (24) 13337-13345
11. Tedelind, S.; Westberg, F.; Kjerrulf, M.; Vidal, A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: A study with relevance to inflammatory bowel disease World J. Gastroenterol. 2007, 13 (20) 2826-2832 (Pubitemid 47007897)
12. Kaneko, T.; Mori, H.; Iwata, M.; Meguro, S. Growth stimulator for bifidobacteria produced by Propionibacterium freudenreichii and several intestinal bacteria J. Dairy Sci. 1994, 77 (2) 393-404
13. Okada, Y.; Tsuzuki, Y.; Miyazaki, J.; Matsuzaki, K.; Hokari, R.; Komoto, S.; Kato, S.; Kawaguchi, A.; Nagao, S.; Itoh, K.; Watanabe, T.; Miura, S. Propionibacterium freudenreichii component 1.4-dihydroxy-2-naphthoic acid (DHNA) attenuates dextran sodium sulphate induced colitis by modulation of bacterial flora and lymphocyte homing Gut 2006, 55 (5) 681-688
14. Okada, Y.; Hokari, R.; Kato, S.; Mataki, N.; Okudaira, K.; Takebayashi, K.; Matsunaga, H.; Tsuzuki, Y.; Komoto, S.; Watanabe, C.; Kawaguchi, A.; Nagao, S.; Itoh, K.; Miura, S. 1.4-dihydroxy-2-naphthoic acid (DHNA) shows anti-inflammatory effect on NSAID-induced colitis in IL-10-knockout mice through suppression of inflammatory cell infiltration and increased number of genus Bifidobacterium Gastroenterology 2006, 130 (4) A313
15. Xu, S.; Boylston, T. D.; Glatz, B. A. Conjugated linoleic acid content and organoleptic attributes of fermented milk products produced with probiotic bacteria J. Agric. Food Chem. 2005, 53 (23) 9064-9072 (Pubitemid 41735672)
16. Uchida, M.; Mogami, O. Milk whey culture with Propionibacterium freudenreichii ET-3 is effective on the colitis induced by 2,4,6-trinitrobenzene sulfonic acid in rats J. Pharmacol. Sci. 2005, 99 (4) 329-334 (Pubitemid 41813424)
17. Kekkonen, R. A.; Lummela, N.; Karjalainen, H.; Latvala, S.; Tynkkynen, S.; Jarvenpaa, S.; Kautiainen, H.; Julkunen, I.; Vapaatalo, H.; Korpela, R. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults World J. Gastroenterol. 2008, 14 (13) 2029-2036 (Pubitemid 351795822)
18. Foligné, B.; Nutten, S.; Grangette, C.; Dennin, V.; Goudercourt, D.; Poiret, S.; Dewulf, J.; Brassart, D.; Mercenier, A.; Pot, B. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria World J. Gastroenterol. 2007, 13 (2) 236-243 (Pubitemid 46231326)
19. Sanders, M. E.; Marco, M. L. Food formats for effective delivery of probiotics Annu. Rev. Food Sci. Technol. 2010, 1, 65-85
20. Koskenniemi, K.; Koponen, J.; Kankainen, M.; Savijoki, K.; Tynkkynen, S.; de Vos, W. M.; Kalkkinen, N.; Varmanen, P. Proteome analysis of Lactobacillus rhamnosus GG using 2-D DIGE and mass spectrometry shows differential protein production in laboratory and industrial-type growth media J. Proteome Res. 2009, 8 (11) 4993-5007
21. Cousin, F. J.; Louesdon, S.; Maillard, M. B.; Parayre, S.; Falentin, H.; Deutsch, S. M.; Boudry, G.; Jan, G. The first dairy product exclusively fermented by Propionibacterium freudenreichii: A new vector to study probiotic potentialities in vivo Food Microbiol. 2012, 32, 135-146
22. Cross, M. L.; Gill, H. S. Immunomodulatory properties of milk Br. J. Nutr. 2000, 84 (Suppl. 1) S81-S89
23. Malik, A. C.; Reinbold, G. W.; Vedamuthu, E. R. An evaluation of the taxonomy of Propionibacterium Can. J. Microbiol. 1968, 14 (11) 1185-1191
24. Michalski, M. C.; Leconte, N.; Briard-Bion, V.; Fauquant, J.; Maubois, J. L.; Goudedranche, H. Microfiltration of raw whole milk to select fractions with different fat globule size distributions: Process optimization and analysis J. Dairy Sci. 2006, 89 (10) 3778-3790 (Pubitemid 44505349)
25. Thierry, A.; Salvat-Brunaud, D.; Madec, M. N.; Michel, F.; Maubois, J. L. Swiss cheese ripening: Dynamics of bacterial populations and evolution of the aqueous phase composition for three industrial cheeses Lait 1998, 78 (5) 521-542
26. Chatelais, L.; Jamin, A.; Gras-Le, G. C.; Lalles, J. P.; Le Huerou-Luron, I.; Boudry, G. The level of protein in milk formula modifies ileal sensitivity to LPS later in life in a piglet model PLoS ONE 2011, 6 (5) e19594
27. Thierry, A.; Maillard, M. B.; Yvon, M. Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL 34 and ITGP23 Appl. Environ. Microbiol. 2002, 68 (2) 608-615 (Pubitemid 34113048)
28. De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J. B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa Proc. Natl. Acad. Sci. U.S.A 2010, 107 (33) 14691-14696
29. Deutsch, S. M.; Le Bivic, P.; Hervé, C.; Madec, M. N.; Lapointe, G.; Jan, G.; Le Loir, Y.; Falentin, H. Correlation of the capsular phenotype in Propionibacterium freudenreichii with the level of expression of gtf, a unique polysaccharide synthase-encoding gene Appl. Environ. Microbiol. 2010, 76 (9) 2740-2746
30. Dalmasso, M.; Nicolas, P.; Falentin, H.; Valence, F.; Tanskanen, J.; Jatila, H.; Salusjarvi, T.; Thierry, A. Multilocus sequence typing of Propionibacterium freudenreichii Int. J. Food Microbiol. 2011, 145 (1) 113-120
31. Anastasiou, R.; Leverrier, P.; Krestas, I.; Rouault, A.; Kalantzopoulos, G.; Boyaval, P.; Tsakalidou, E.; Jan, G. Changes in protein synthesis during thermal adaptation of Propionibacterium freudenreichii subsp. shermanii Int. J. Food Microbiol. 2006, 108 (3) 301-314
32. Hugenschmidt, S.; Schwenninger, S. M.; Gnehm, N.; Lacroix, C. Screening of a natural biodiversity of lactic and propionic acid bacteria for folate and vitamin B12 production in supplemented whey permeate Int. Dairy J. 2010, 20 (12) 852-857
33. Medrano, M.; Racedo, S. M.; Rolny, I. S.; Abraham, A. G.; Perez, P. F. Oral administration of kefiran induces changes in the balance of immune cells in a murine model J. Agric. Food Chem. 2011, 59 (10) 5299-5304
34. Peng, S.; Lin, J. Y.; Lin, M. Y. Antiallergic effect of milk fermented with lactic acid bacteria in a murine animal model J. Agric. Food Chem. 2007, 55 (13) 5092-5096 (Pubitemid 47056061)
35. Plumed-Ferrer, C.; Koistinen, K. M.; Tolonen, T. L.; Lehesranta, S. J.; Karenlampi, S. O.; Makimattila, E.; Joutsjoki, V.; Virtanen, V.; von Wright, A. Comparative study of sugar fermentation and protein expression patterns of two Lactobacillus plantarum strains grown in three different media Appl. Environ. Microbiol. 2008, 74 (17) 5349-5358
36. Yuan, J.; Zhu, L.; Liu, X.; Li, T.; Zhang, Y.; Ying, T.; Wang, B.; Wang, J.; Dong, H.; Feng, E.; Li, Q.; Wang, J.; Wang, H.; Wei, K.; Zhang, X.; Huang, C.; Huang, P.; Huang, L.; Zeng, M.; Wang, H. A proteome reference map and proteomic analysis of Bifidobacterium longum NCC2705 Mol. Cell. Proteomics 2006, 5 (6) 1105-1118 (Pubitemid 43985934)
37. Masuda, S.; Yamaguchi, H.; Kurokawa, T.; Shirakami, T.; Tsuji, R. F.; Nishimura, I. Immunomodulatory effect of halophilic lactic acid bacterium Tetragenococcus halophilus Th221 from soy sauce moromi grown in high-salt medium Int. J. Food Microbiol. 2008, 121 (3) 245-252
38. Sashihara, T.; Sueki, N.; Furuichi, K.; Ikegami, S. Effect of growth conditions of Lactobacillus gasseri OLL2809 on the immunostimulatory activity for production of interleukin-12 (p70) by murine splenocytes Int. J. Food Microbiol. 2007, 120 (3) 274-281 (Pubitemid 350137510)
39. Alexopoulos, C.; Georgoulakis, I. E.; Tzivara, A.; Kritas, S. K.; Siochu, A.; Kyriakis, S. C. Field evaluation of the efficacy of a probiotic containing Bacillus licheniformis and Bacillus subtilis spores, on the health status and performance of sows and their litters J. Anim. Physiol. Anim. Nutr. 2004, 88 (11-12) 381-392 (Pubitemid 40068274)
40. Taras, D.; Vahjen, W.; Macha, M.; Simon, O. Performance, diarrhea incidence, and occurrence of Escherichia coli virulence genes during long-term administration of a probiotic Enterococcus faecium strain to sows and piglets J. Anim. Sci. 2006, 84 (3) 608-617 (Pubitemid 44405674)
41. Zeyner, A.; Boldt, E. Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets J. Anim. Physiol. Anim. Nutr. 2006, 90 (1-2) 25-31
42. Bohmer, B. M.; Kramer, W.; Roth-Maier, D. A. Dietary probiotic supplementation and resulting effects on performance, health status, and microbial characteristics of primiparous sows J. Anim. Physiol. Anim. Nutr. 2006, 90 (7-8) 309-315 (Pubitemid 44392313)
43. Guo, X.; Li, D.; Lu, W.; Piao, X.; Chen, X. Screening of Bacillus strains as potential probiotics and subsequent confirmation of the in vivo effectiveness of Bacillus subtilis MA139 in pigs Antonie van Leeuwenhoek 2006, 90 (2) 139-146 (Pubitemid 44263953)
44. Ross, G. R.; Gusils, C.; Oliszewski, R.; de Holgado, S. C.; Gonzalez, S. N. Effects of probiotic administration in swine J. Biosci. Bioeng. 2010, 109 (6) 545-549
45. Konstantinov, S. R.; Smidt, H.; Akkermans, A. D.; Casini, L.; Trevisi, P.; Mazzoni, M.; De Filippi, S.; Bosi, P.; de Vos, W. M. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets FEMS Microbiol. Ecol. 2008, 66 (3) 599-607
46. Mantere-Alhonen, S. Propionibacteria used as probiotics-A review Lait 1995, 75 (4/5) 447-452
47. Vondruskova, H.; Slamova, R.; Trckova, M.; Zraly, Z.; Pavlik, I. Alternatives to antibiotic growth promoters in prevention of diarrhoea in weaned piglets: A review Vet. Med. 2010, 55 (5) 199-224
48. Ross, G. R.; Van Nieuwenhove, C. P.; Gonzalez, S. N. Fatty acid profile of pig meat after probiotic administration J. Agric. Food Chem. 2012, 60 (23) 5974-5978
49. Sougioultzis, S.; Simeonidis, S.; Bhaskar, K. R.; Chen, X. H.; Anton, P. M.; Keates, S.; Pothoulakis, C.; Kelly, C. P. Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-kappa B-mediated IL-8 gene expression Biochem. Biophys. Res. Commun. 2006, 343 (1) 69-76
50. Riedel, C. U.; Foata, F.; Philippe, D.; Adolfsson, O.; Eikmanns, B. J.; Blum, S. Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappa B activation World J. Gastroenterol. 2006, 12 (23) 3729-3735 (Pubitemid 43950950)
51. Grimoud, J.; Durand, H.; de Souza, S.; Monsan, P.; Ouarne, F.; Theodorou, V.; Rogues, C. In vitro screening of probiotics and synbiotics according to anti-inflammatory and anti-proliferative effects Int. J. Food Microbiol. 2010, 144 (1) 42-50
52. Watanabe, T.; Nishio, H.; Tanigawa, T.; Yamagami, H.; Okazaki, H.; Watanabe, K.; Tominaga, K.; Fujiwara, Y.; Oshitani, N.; Asahara, T.; Nomoto, K.; Higuchi, K.; Takeuchi, K.; Arakawa, T. Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: involvement of lactic acid Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297 (3) G506-G513
53. Paolillo, R.; Carratelli, C. R.; Sorrentino, S.; Mazzola, N.; Rizzo, A. Immunomodulatory effects of Lactobacillus plantarum on human colon cancer cells Int. Immunopharmacol. 2009, 9 (11) 1265-1271
54. Liu, Y. Y.; Fatheree, N. Y.; Mangalat, N.; Rhoads, J. M. Human-derived probiotic Lactobacillus reuteri strains differentially reduce intestinal inflammation Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299 (5) G1087-G1096
55. Tsai, Y. T.; Cheng, P. C.; Pan, T. M. Immunomodulating activity of Lactobacillus paracasei subsp. paracasei NTU 101 in enterohemorrhagic Escherichia coli O157H7-infected mice J. Agric. Food Chem. 2010, 58 (21) 11265-11272
56. Vahjen, W.; Pieper, R.; Zentek, J. Bar-coded pyrosequencing of 16S rRNA gene amplicons reveals changes in ileal porcine bacterial communities due to high dietary zinc intake Appl. Environ. Microbiol. 2010, 76 (19) 6689-6691
57. Dowd, S. E.; Sun, Y.; Wolcott, R. D.; Domingo, A.; Carroll, J. A. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella -infected pigs Foodborne Pathog. Dis. 2008, 5 (4) 459-472
58. Mitsuyama, K.; Masuda, J.; Yamasaki, H.; Kuwaki, K.; Kitazaki, S.; Koga, H.; Uchida, M.; Sata, M. Treatment of ulcerative colitis with milk whey culture with Propionibacterium freudenreichii J. Intest. Microbiol. 2007, 21 (2) 143-147
59. Sarkar, S.; Misra, A. K. Effect of feeding propiono-acido-bifido (PAB) milk on the nutritional status and excretory pattern in rats and infants Milchwissenschaft-Milk Sci. Int. 1998, 53 (12) 666-668 (Pubitemid 128376629)
60. Perez Chaia, A.; Zarate, G.; Oliver, G. The probiotic properties of propionibacteria Lait 1999, 79 (1) 175-185 (Pubitemid 129511861)
61. Mair, C.; Plitzner, C.; Pfaffl, M. W.; Schedle, K.; Meyer, H. H. D.; Windisch, W. Inulin and probiotics in newly weaned piglets: effects on intestinal morphology, mRNA expression levels of inflammatory marker genes and haematology Arch. Anim. Nutr. 2010, 64 (4) 304-321
62. Muftoglu, M. A.; Civak, T.; Cetin, S.; Civak, L.; Gungor, O.; Saglam, A. Effects of probiotics on experimental short-bowel syndrome Am. J. Surg. 2011, 202 (4) 461-468
63. Ohland, C. L.; MacNaughton, W. K. Probiotic bacteria and intestinal epithelial barrier function Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298 (6) G807-G819
64. Zareie, M.; Johnson-Henry, K.; Jury, J.; Yang, P. C.; Ngan, B. Y.; Mckay, D. M.; Soderholm, J. D.; Perdue, M. H.; Sherman, P. M. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress Gut 2006, 55 (11) 1553-1560 (Pubitemid 44629200)
65. Karczewski, J.; Troost, F. J.; Konings, I.; Dekker, J.; Kleerebezem, M.; Brummer, R. J. M.; Wells, J. M. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298 (6) G851-G859