An in vitro approach to study effects of prebiotics and probiotics on the faecal microbiota and selected immune parameters relevant to the elderly

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Liu, Yue ^a   Gibson, Glenn R ^a   Walton, Gemma E ^a  

^a UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSE OLIGOSACCHARIDE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; INULIN; PREBIOTIC AGENT; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR;

AGED; AGING; ARTICLE; BACILLUS COAGULANS; BACTERIAL STRAIN; BIFIDOBACTERIUM BIFIDUM; CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FECES ANALYSIS; FECES MICROFLORA; FERMENTATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOLOGICAL PARAMETERS; IN VITRO STUDY; INTESTINE FLORA; LACTOBACILLUS ACIDOPHILUS; PERIPHERAL BLOOD MONONUCLEAR CELL; BACTEROIDES THETAIOTAOMICRON; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; FECES; FLUORESCENCE IN SITU HYBRIDIZATION; METABOLISM; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; MONONUCLEAR CELL; PHYSIOLOGY; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM;

AGED; BACILLUS COAGULANS; BACTEROIDES THETAIOTAOMICRON; BIFIDOBACTERIUM BIFIDUM; CELL SURVIVAL; CELLS, CULTURED; FECES; FERMENTATION; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERLEUKIN-10; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOCYTES, MONONUCLEAR; MICROBIOTA; MIDDLE AGED; PREBIOTICS; PROBIOTICS; SALMONELLA TYPHIMURIUM;

EID: 84990955020     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0162604     Document Type: Article

References (72)

1. WHO. Facts about ageing 2014 [Accessed 30 January 2015]. Available: http://www.who.int/ageing/about/facts/en/.
2. Kleessen B, Sykura B, Zunft HJ, Blaut M. Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Clin Nutr. 1997; 65(5):1397-402. PMID: 9129468
3. Yagamata A. Histopathological studies of the colon in relation to age. Jap J Gastroenterol. 1965; 62:229-34.
4. Brocklehurst JC. Bowel management in the neurologically disabled. The problems of old age. Proc R Soc Med. 1972; 65(1):66-9. PMID: 5015482
5. Woodmansey EJ. Intestinal bacteria and ageing. J Appl Microbiol. 2007; 102(5):1178-86. PMID: 17448153
6. Doty RL, Shaman P, Applebaum SL, Giberson R, Siksorski L, Rosenberg L. Smell identification ability: changes with age. Science. 1984; 226(4681):1441-3. PMID: 6505700
7. Newton JP, Yemm R, Abel RW, Menhinick S. Changes in human jaw muscles with age and dental state. Gerodontology. 1993; 10(1):16-22. PMID: 8300113
8. Castell DO. Eating and swallowing disorders in the elderly. Pract Gastroenterol. 1988; 12:32-43.
9. Schiffrin EJ, Morley JE, Donnet-Hughes A, Guigoz Y. The inflammatory status of the elderly: the intestinal contribution. Mutat Res. 2010; 690(1-2):50-6. doi: 10.1016/j.mrfmmm.2009.07.011 PMID: 19666034
10. Goodwin JS. Decreased immunity and increased morbidity in the elderly. Nutr Rev. 1995; 53(4 Pt 2): S41-4; discussion S4-6. PMID: 7644153
11. Bruunsgaard H, Pedersen AN, Schroll M, Skinhoj P, Pedersen BK. Decreased natural killer cell activity is associated with atherosclerosis in elderly humans. Exp Gerontol. 2001; 37(1):127-36. PMID: 11738153
12. Butcher SK, Chahal H, Nayak L, Sinclair A, Henriquez NV, Sapey E, et al. Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans. J Leukocyte Biol. 2001; 70(6):881-6. PMID: 11739550
13. Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr. 2008; 88(5):1438-46. PMID: 18996881
14. Agrawal A, Agrawal S, Tay J, Gupta S. Biology of dendritic cells in aging. J Clin Immunol. 2008; 28 (1):14-20. PMID: 17828583
15. Min H, Montecino-Rodriguez E, Dorshkind K. Effects of aging on the common lymphoid progenitor to pro-B cell transition. J Immunol. 2006; 176(2):1007-12. PMID: 16393987
16. Bartosch S, Woodmansey EJ, Paterson JC, McMurdo ME, Macfarlane GT. Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis, and oligofructose in elderly persons, determined by real-time polymerase chain reaction and counting of viable bacteria. Clin Infect Dis. 2005; 40(1):28-37. PMID: 15614689
17. McCartney AL, Wenzhi W, Tannock GW. Molecular analysis of the composition of the bifidobacterial and lactobacillus microflora of humans. Appl Environ Microbiol. 1996; 62(12):4608-13. PMID: 8953730
18. Hopkins MJ, Sharp R, Macfarlane GT. Variation in human intestinal microbiota with age. Dig Liver Dis. 2002; 34 Suppl 2:S12-8. PMID: 12408433
19. Hopkins MJ, Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J Med Microbiol. 2002; 51(5):448-54. PMID: 11990498
20. Woodmansey EJ, McMurdo ME, Macfarlane GT, Macfarlane S. Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-Antibiotic-treated elderly subjects. Appl Environ Microbiol. 2004; 70(10):6113-22. PMID: 15466557
21. Gavini F, Cayuela C, Antoine J-M, Lecoq C, Lefebvre B, Membré J-M, et al. Differences in the distribution of bifidobacterial and enterobacterial species in human faecal microbiota of three (children, adults, elderly) age groups. Microb Ecol Health Dis. 2001; 13:40-5.
22. Hopkins MJ, Sharp R, Macfarlane GT. Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. Gut. 2001; 48(2):198-205. PMID: 11156640
23. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006; 72(2):1027-33. PMID: 16461645
24. Claesson MJ, 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. Proc Natl Acad Sci U S A. 2011; 108 Suppl 1:4586-91. doi: 10.1073/pnas.1000097107 PMID: 20571116
25. Mitsuoka T. Intestinal flora and aging. Nutr Rev. 1992; 50(12):438-46. PMID: 1488186
26. Makivuokko H, Tiihonen K, Tynkkynen S, Paulin L, Rautonen N. The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr. 2010; 103(2):227-34. doi: 10.1017/S0007114509991553 PMID: 19703328
27. Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, Dore J, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009; 9:123. doi: 10.1186/1471-2180-9-123 PMID: 19508720
28. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012; 488(7410):178-84. doi: 10.1038/nature11319 PMID: 22797518
29. Peterson CT, Sharma V, Elmen L, Peterson SN. Immune homeostasis, dysbiosis and therapeutic modulation of the gut microbiota. Clin Exp Immunol. 2014; 179(3):363-77.
30. Tonna I, Welsby PD. Pathogenesis and treatment of Clostridium difficile infection. Postgrad Med J. 2005; 81(956):367-9. PMID: 15937201
31. Walton GE, van den Heuvel EG, Kosters MH, Rastall RA, Tuohy KM, Gibson GR. A randomised crossover study investigating the effects of galacto-oligosaccharides on the faecal microbiota in men and women over 50 years of age. Br J Nutr. 2012; 107(10):1466-75. doi: 10.1017/S0007114511004697 PMID: 21910949
32. Ouwehand AC, Bergsma N, Parhiala R, Lahtinen S, Gueimonde M, Finne-Soveri H, et al. Bifidobacterium microbiota and parameters of immune function in elderly subjects. FEMS Immunol Med Microbiol. 2008; 53(1):18-25. doi: 10.1111/j.1574-695X.2008.00392.x PMID: 18336547
33. Honda H, Hoyles L, Gibson GR, Farmer S, Keller D, McCartney AL. Impact of GanedenBC30 (Bacillus coagulans GBI-30, 6086) on population dynamics of the human gut microbiota in a continuous culture fermentation system. Int J Probiotics Prebiotics. 2011; 6(1):65-72.
34. Guigoz Y, Rochat F, Perruisseau-Carrier G, Rochat I, Schiffrin EJ. Effects of oligosaccharide on the faecal flora and non-specific immune system in elderly people. Nutr Res. 2002; 22(1-2):13-25.
35. Arunachalam K, Gill HS, Chandra RK. Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur J Clin Nutr. 2000; 54(3):263-7. PMID: 10713750
36. Jensen GS, Benson KF, Carter SG, Endres JR. GanedenBC30 cell wall and metabolites: anti-inflammatory and immune modulating effects in vitro. BMC Immunol. 2010; 11:15. doi: 10.1186/1471-2172-11-15 PMID: 20331905
37. Gibson GR, Scott KP, Rastall RA, Tuohy KM, Hotchkiss A, Dubert-Ferrandon A, et al. Dietary prebiotics: current status and new definition. IFIS Functional Foods Bulletin. 2010; 7:1-19.
38. FAO/WHO. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. 2001 [Accessed 14th December 2011]. Available from: ftp://ftp.fao.org/docrep/fao/009/a0512e/a0512e00.pdf.
39. FAO/WHO. Guidelines for the evaluation of probiotics in food 2002 [Accessed 14th December 2011]. Available from: ftp://ftp.fao.org/es/esn/food/wgreport2.pdf.
40. Langkamp-Henken B, Bender BS, Gardner EM, Herrlinger-Garcia KA, Kelley MJ, Murasko DM, et al. Nutritional formula enhanced immune function and reduced days of symptoms of upper respiratory tract infection in seniors. J Am Geriatr Soc. 2004; 52(1):3-12. PMID: 14687308
41. Langkamp-Henken B, Wood SM, Herlinger-Garcia KA, Thomas DJ, Stechmiller JK, Bender BS, et al. Nutritional formula improved immune profiles of seniors living in nursing homes. J Am Geriatr Soc. 2006; 54(12):1861-70. PMID: 17198491
42. Ouwehand AC, Tiihonen K, Saarinen M, Putaala H, Rautonen N. Influence of a combination of Lactobacillus acidophilus NCFM and lactitol on healthy elderly: intestinal and immune parameters. Br J Nutr. 2009; 101(3):367-75. doi: 10.1017/S0007114508003097 PMID: 18634707
43. Honda H, Gibson GR, Farmer S, Keller D, McCartney AL. Use of a continuous culture fermentation system to investigate the effect of GanedenBC30 (Bacillus coagulans GBI-30, 6086) supplementation on pathogen survival in the human gut microbiota. Anaerobe. 2011; 17(1):36-42. doi: 10.1016/j.anaerobe. 2010.12.006 PMID: 21195203
44. Harmsen HJ, Wildeboer-Veloo AC, Grijpstra J, Knol J, Degener JE, Welling GW. Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol. 2000; 66(10):4523-7. PMID: 11010909
45. Harmsen HJ, Elfferich P, Schut F, Welling GW. A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microb Ecol Health Dis. 1999; 11 (1):3-12.
46. Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, et al. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol. 1995; 61(8):3069-75. PMID: 7487040
47. Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol. 1998; 64(9):3336-45. PMID: 9726880
48. Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment. Microbiology. 1996; 142 (Pt 5):1097-106. PMID: 8704951
49. Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M. The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol. 1999; 22(3):434-44. PMID: 10553296
50. Daims H, Stoecker K, Wagner M. Fluorescence in situ hybridization for the detection of prokaryotes. In: Osborn AM, Smith CJ, editors. Molecular microbial ecology. Abingdon, UK: Garland Science; 2005. p. 213-39.
51. Richardson AJ, Calder AG, Stewart CS, Smith A. Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol. 1989; 9(1):5-8.
52. Vulevic J, Juric A, Tzortzis G, Gibson GR. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults. The Journal of Nutrition. 2013; 143(3):324-31. doi: 10.3945/jn.112.166132 PMID: 23303873
53. Silk DB, Davis A, Vulevic J, Tzortzis G, Gibson GR. Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment Pharmacol Ther. 2009; 29(5):508-18. doi: 10.1111/j.1365-2036.2008.03911.x PMID: 19053980
54. Tzortzis G, Goulas AK, Gee JM, Gibson GR. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J Nutr. 2005; 135(7):1726-31. PMID: 15987856
55. Vulevic J, Juric A, Walton GE, Claus SP, Tzortzis G, Toward RE, et al. Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. The British journal of nutrition. 2015; 114(4):586-95. doi: 10.1017/S0007114515001889 PMID: 26218845
56. Wang X, Gibson GR. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. The Journal of applied bacteriology. 1993; 75(4):373-80. PMID: 8226394
57. Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, Louis P. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr. 2009; 101(4):541-50. doi: 10.1017/S0007114508019880 PMID: 18590586
58. Costabile A, Kolida S, Klinder A, Gietl E, Bauerlein M, Frohberg C, et al. A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr. 2010; 104(7):1007-17. doi: 10.1017/S0007114510001571 PMID: 20591206
59. Ogué-Bon E, Khoo C, McCartney AL, Gibson GR, Rastall RA. In vitro effects of synbiotic fermentation on the canine faecal microbiota. FEMS Microbiol Ecol. 2010; 73(3):587-600. doi: 10.1111/j.1574-6941. 2010.00915.x PMID: 20579101
60. Björklund M, Ouwehand AC, Forssten SD, Nikkilä J, Tiihonen K, Rautonen N, et al. Gut microbiota of healthy elderly NSAID users is selectively modified with the administration of Lactobacillus acidophilus NCFM and lactitol. Age (Dordrecht, Netherlands). 2012; 34(4):987-99.
61. Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 2007; 102(5):1197-208. PMID: 17448155
62. Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. Journal of proteome research. 2012; 11(12):5573-85. doi: 10. 1021/pr300637d PMID: 23116228
63. Dong H, Rowland I, Yaqoob P. Comparative effects of six probiotic strains on immune function in vitro. Br J Nutr. 2012; 108(3):459-70. doi: 10.1017/S0007114511005824 PMID: 22054064
64. Capitan-Canadas F, Ortega-Gonzalez M, Guadix E, Zarzuelo A, Suarez MD, de Medina FS, et al. Prebiotic oligosaccharides directly modulate proinflammatory cytokine production in monocytes via activation of TLR4. Mol Nutr Food Res. 2014; 58(5):1098-110. doi: 10.1002/mnfr.201300497 PMID: 24549946
65. Imaoka A, Shima T, Kato K, Mizuno S, Uehara T, Matsumoto S, et al. Anti-inflammatory activity of probiotic Bifidobacterium: enhancement of IL-10 production in peripheral blood mononuclear cells from ulcerative colitis patients and inhibition of IL-8 secretion in HT-29 cells. World J Gastroenterol. 2008; 14 (16):2511-6. PMID: 18442197
66. Vendrig JC, Coffeng LE, Fink-Gremmels J. In vitro evaluation of defined oligosaccharide fractions in an equine model of inflammation. BMC veterinary research. 2013; 9:147. doi: 10.1186/1746-6148-9-147 PMID: 23875544
67. Liu T, Li J, Liu Y, Xiao N, Suo H, Xie K, et al. Short-chain fatty acids suppress lipopolysaccharideinduced production of nitric oxide and proinflammatory cytokines through inhibition of NF-kappaB pathway in RAW264.7 cells. Inflammation. 2012; 35(5):1676-84. doi: 10.1007/s10753-012-9484-z PMID: 22669487
68. Vinolo MA, Rodrigues HG, Hatanaka E, Sato FT, Sampaio SC, Curi R. Suppressive effect of shortchain fatty acids on production of proinflammatory mediators by neutrophils. J Nutr Biochem. 2011; 22 (9):849-55. doi: 10.1016/j.jnutbio.2010.07.009 PMID: 21167700
69. Segain JP, Raingeard de la Bletiere D, Bourreille A, Leray V, Gervois N, Rosales C, et al. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut. 2000; 47(3):397-403. PMID: 10940278
70. Usami M, Kishimoto K, Ohata A, Miyoshi M, Aoyama M, Fueda Y, et al. Butyrate and trichostatin A attenuate nuclear factor kappaB activation and tumor necrosis factor alpha secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells. Nutrition Research. 2008; 28 (5):321-8. doi: 10.1016/j.nutres.2008.02.012 PMID: 19083427
71. Saemann MD, Bohmig GA, Osterreicher CH, Burtscher H, Parolini O, Diakos C, et al. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000; 14(15):2380-2. PMID: 11024006
72. Cavaglieri CR, Nishiyama A, Fernandes LC, Curi R, Miles EA, Calder PC. Differential effects of shortchain fatty acids on proliferation and production of pro-And anti-inflammatory cytokines by cultured lymphocytes. Life Sci. 2003; 73(13):1683-90. PMID: 12875900