Associations of probiotic fermented milk (PFM) and yogurt consumption with bifidobacterium and lactobacillus components of the gut microbiota in healthy adults

Nutrients

Volumn 11, Issue 3, 2019, Pages

  Redondo Useros, Noemí ^a   Gheorghe, Alina ^a   Díaz Prieto, Ligia E ^a   Villavisencio, Brenda ^a   Marcos, Ascensión ^a   Nova, Esther ^a  

^a INSTITUTE OF FOOD SCIENCE   (Spain)

Author keywords

Bifidobacteria; Gut microbiota; Healthy adults; Probiotic fermented milk; Yogurt

Indexed keywords

PROBIOTIC AGENT; YOGHURT; RNA 16S;

ADULT; ANTHROPOMETRY; ARTICLE; BACTERIUM IDENTIFICATION; BACTEROIDES; BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM LONGUM; BODY MASS; CONTROLLED STUDY; FECES MICROFLORA; FEMALE; FERMENTED DAIRY PRODUCT; FIRMICUTES; FOOD FREQUENCY QUESTIONNAIRE; HUMAN; INTESTINE FLORA; INTRA-ABDOMINAL FAT; LACTOBACILLUS; MAJOR CLINICAL STUDY; MALE; NONHUMAN; QUESTIONNAIRE; STREPTOCOCCUS THERMOPHILUS; WAIST CIRCUMFERENCE; ANIMAL; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MILK; REFERENCE VALUE;

ADULT; ANIMALS; BIFIDOBACTERIUM; FEMALE; FERMENTATION; GASTROINTESTINAL MICROBIOME; HUMANS; LACTOBACILLUS; MALE; MILK; PROBIOTICS; REFERENCE VALUES; RNA, RIBOSOMAL, 16S; STREPTOCOCCUS THERMOPHILUS; YOGURT;

EID: 85063268649     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu11030651     Document Type: Article

References (64)

1. Qin, J.; Li, R.; Raes, J.; Arumugam, M.; Burgdorf, K.S.; Manichanh, C.; Nielsen, T.; Pons, N.; Levenez, F.; Yamada, T.; et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464, 59–65. [CrossRef]
2. Lozupone, C.A.; Stombaugh, J.I.; Gordon, J.I.; Jansson, J.K.; Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489, 220–230. [CrossRef]
3. Tap, J.; Mondot, S.; Levenez, F.; Pelletier, E.; Caron, C.; Furet, J.P.; Ugarte, E.; Muñoz-Tamayo, R.; Paslier, D.L.; Nalin, R.; et al. Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 2009, 11, 2574–2584. [CrossRef]
4. Reuter, G. The Lactobacillus and Bifidobacterium microflora of the human intestine: Composition and succession. Curr. Issues Intest. Microbiol. 2001, 2, 43–53.
5. Kok, C.R.; Hutkins, R. Yogurt and other fermented foods as sources of health-promoting bacteria. Nutr. Rev. 2018, 76, 4–15. [CrossRef]
6. Derrien, M.; van Hylckama Vlieg, J.E. Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol. 2015, 23, 354–366. [CrossRef]
7. McNulty, N.P.; Yatsunenko, T.; Hsiao, A.; Faith, J.J.; Muegge, B.D.; Goodman, A.L.; Henrissat, B.; Oozeer, R.; Cools-Portier, S.; Gobert, G.; et al. The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci. Transl. Med. 2011, 3, 106ra106. [CrossRef]
8. Bezkorovainy, A. Probiotics: Determinants of survival and growth in the gut. Am. J. Clin. Nutr. 2001, 73, 399S–405S. [CrossRef]
9. Uyeno, Y.; Sekiguchi, Y.; Kamagata, Y. Impact of consumption of probiotic lactobacilli-containing yogurt on microbial composition in human feces. Int. J. Food Microbiol. 2008, 122, 16–22. [CrossRef]
10. Del Campo, R.; Bravo, D.; Cantón, R.; Ruiz-Garbajosa, P.; García-Albiach, R.; Montesi-Libois, A.; Yuste, F.J.; Abraira, V.; Baquero, F. Scarce Evidence of Yogurt Lactic Acid Bacteria in Human Feces after Daily Yogurt Consumption by Healthy Volunteers. Appl. Environ. Microb. 2005, 71, 547–549. [CrossRef]
11. García-Albiach, R.; Pozuelo de Felipe, M.; Angulo, S.; Morosini, M.I.; Bravo, D.; Baquero, F.; del Campo, R. Molecular analysis of yogurt containing Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus in human intestinal microbiota. Am. J. Clin. Nutr. 2008, 87, 91–96. [CrossRef]
12. Elli, M.; Callegari, M.L.; Ferrari, S.; Bessi, E.; Cattivelli, D.; Soldi, S.; Morelli, L.; Goupil Feuillerat, N.; Antoine, J.M. Survival of yogurt bacteria in the human gut. Appl. Environ. Microbiol. 2006, 72, 5113–5117. [CrossRef]
13. Mater, D.D.; Bretigny, L.; Firmesse, O.; Flores, M.J.; Mogenet, A.; Bresson, J.L.; Corthier, G. Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus survive gastrointestinal transit of healthy volunteers consuming yogurt. FEMS Microbiol. Lett. 2005, 250, 185–187. [CrossRef]
14. Morelli, L. Yogurt, living cultures, and gut health. Am. J. Clin. Nutr. 2014, 99, 1248S–1250S. [CrossRef]
15. Lisko, D.J.; Johnston, G.P.; Johnston, C.G. Effects of Dietary Yogurt on the Healthy Human Gastrointestinal (GI) Microbiome. Microorganisms 2017, 5, 6. [CrossRef]
16. Redondo, N.; García-González, N.; Diaz-Prieto, L.E.; Olmedilla-Alonso, B.; Martín-Diana, A.B.; Asensio-Vegas, C.; Nova, E. Effects of ewe’s milk yogurt (whole and semi-skimmed) and cow’s milk yogurt on inflammation markers and gut microbiota of subjects with borderline-high plasma cholesterol levels: A crossover study. Eur. J. Nutr. 2018. [CrossRef]
17. Farhana Fazilaha, N.; Ariffac, A.; Khayatbc, M.E.; Rios-Solis, L.; Hali, D. Influence of probiotics, prebiotics, synbiotics and bioactive phytochemicals on the formulation of functional yogurt. J. Funct. Foods 2018, 48, 387–399. [CrossRef]
18. Filteau, M.; Matamoros, S.; Savard, P.; Roy, D. Molecular monitoring of fecal microbiota in healthy adults following probiotic yogurt intake. Pharma Nutr. 2013, 1, 123–129. [CrossRef]
19. Kim, S.W.; Suda, W.; Kim, S.; Oshima, K.; Fukuda, S.; Ohno, H.; Morita, H.; Hattori, M. Robustness of gut microbiota of healthy adults in response to probiotic intervention revealed by high-throughput pyrosequencing. DNA Res. 2013, 20, 241–253. [CrossRef]
20. Burton, K.J.; Rosikiewicz, M.; Pimentel, G.; Bütikofer, U.; von Ah, U.; Voirol, M.J.; Croxatto, A.; Aeby, S.; Drai, J.; McTernan, P.G.; et al. Probiotic yogurt and acidified milk similarly reduce postprandial inflammation and both alter the gut microbiota of healthy, young men. Br. J. Nutr. 2017, 117, 1312–1322. [CrossRef]
21. Tanaka, Y.; Takami, K.; Nishijima, T.; Aoki, R.; Mawatari, T.; Ikeda, T. Short-and long-term dynamics in the intestinal microbiota following ingestion of Bifidobacterium animalis subsp. lactis GCL2505. BMFH 2015, 34, 77–85. [CrossRef]
22. Matsumoto, K.; Takada, T.; Shimizu, K.; Moriyama, K.; Kawakami, K.; Hirano, K.; Kajimoto, O.; Nomoto, K. Effects of a probiotic fermented milk beverage containing Lactobacillus casei strain Shirota on defecation frequency, intestinal microbiota, and the intestinal environment of healthy individuals with soft stools. J. Biosci. Bioeng. 2010, 110, 547–552. [CrossRef]
23. Savard, P.; Lamarche, B.; Paradis, M.E.; Thiboutot, H.; Laurin, É.; Roy, D. Impact of Bifidobacterium animalis subsp. lactis BB-12 and Lactobacillus acidophilus LA-5-containing yoghurt, on fecal bacterial counts of healthy adults. Int. J. Food Microbiol. 2011, 149, 50–57. [CrossRef]
24. Zhang, J.; Wang, L.; Guo, Z.; Sun, Z.; Gesudu, Q.; Kwok, L.; Menghebilige; Zhang, H. 454 pyrosequencing reveals changes in the faecal microbiota of adults consuming Lactobacillus casei Zhang. FEMS Microbiol. Ecol. 2014, 88, 612–622. [CrossRef]
25. Fooks, L.J.; Gibson, G.R. Probiotics as modulators of the gut flora. Br. J. Nutr. 2002, 88, S39–S49. [CrossRef]
26. Eales, J.; Gibson, P.; Whorwell, P.; Kellow, J.; Yellowlees, A.; Perry, R.H.; Edwards, M.; King, S.; Wood, H.; Glanville, J. Systematic review and meta-analysis: The effects of fermented milk with Bifidobacterium lactis CNCM I-2494 and lactic acid bacteria on gastrointestinal discomfort in the general adult population. Ther. Adv. Gastroenterol. 2017, 10, 74–88. [CrossRef]
27. Delcenserie, V.; Martel, D.; Lamoureux, M.; Amiot, J.; Boutin, Y.; Roy, D. Immunomodulatory effects of probiotics in the intestinal tract. Curr. Issues Mol. Biol. 2008, 10, 37–54.
28. Lemon, K.P.; Armitage, G.C.; Relman, D.A.; Fischbach, M.A. Microbiota-targeted therapies: An ecological perspective. Sci. Transl. Med. 2002, 4, 137rv5. [CrossRef]
29. David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563. [CrossRef]
30. World Health Organization (WHO). Global Strategy on Diet, Physical Activity and Health, 57th World Health Assembly (WHA); WHO: Geneva, Switzerland, 2004.
31. Vulevic, J.; Juric, A.; Tzortzis, G.; Gibson, G.R. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults. J. Nutr. 2013, 143, 324–331. [CrossRef]
32. Revicki, D.A.; Wood, M.; Wiklund, I.; Crawley, J. Reliability and validity of the Gastrointestinal Symptom Rating Scale in patients with gastroesophageal reflux disease. Qual. Life Res. 1998, 7, 75–83. [CrossRef]
33. Martin-Moreno, J.M.; Boyle, P.; Gorgojo, L.; Maisonneuve, P.; Fernandez-Rodriguez, J.C.; Salvini, S.; Willett, W.C. Development and validation of a food frequency questionnaire in Spain. Int. J. Epidemiol. 1993, 22, 512–519. [CrossRef]
34. Dore, J.; Ehrlich, S.D.; Levenez, F.; Pelletier, E.; Alberti, A.; Bertrand, L.; Bork, P.; Costea, P.I.; Sunagawa, S.; Guarner, F.; et al. IHMS_SOP 06 V1: Standard operating procedure for faecal samples DNA extraction, Protocol, Q. International Human Microbiome Standards. 2015. Available online: http://www.microbiome-standards.org (accessed on 13 May 2016).
35. Illumina. Available online: https://support.illumina.com/help/BaseSpace:App_16S_Metagenomics_help/16S_Metagenomics_App_Help.htm#Vault/Informatics/Sequencing_Analysis/Apps/swSEQ_mAPP_16S_ Read_Classification.htm%3FToc (accessed on 20 December 2018).
36. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Meth. 1995, 57, 289–300. [CrossRef]
37. Khalesi, S.; Bellissimo, N.; Vandelanotte, C.; Williams, S.; Stanley, D.; Irwin, C. A review of probiotic supplementation in healthy adults: Helpful or hype? Eur. J. Clin. Nutr. 2019, 73, 24–37. [CrossRef]
38. Ouwehand, A.C. A review of dose-responses of probiotics in human studies. Benef. Microbes 2017, 8, 143–151. [CrossRef]
39. Larsen, C.N.; Nielsen, S.; Kaestel, P.; Brockmann, E.; Bennedsen, M.; Christensen, H.R.; Eskesen, D.C.; Jacobsen, B.L.; Michaelsen, K.F. Dose-response study of probiotic bacteria Bifidobacterium animalis subsp. lactis BB-12 and Lactobacillus paracasei subsp paracasei CRL-341 in healthy young adults. Eur. J. Clin. Nutr. 2006, 60, 1284–1293. [CrossRef]
40. Kristensen, N.B.; Bryrup, T.; Allin, K.H.; Nielsen, T.; Hansen, T.H.; Pedersen, O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: A systematic review of randomized controlled trials. Genome Med. 2016, 8, 52. [CrossRef]
41. Turroni, F.; Foroni, E.; Pizzetti, P.; Giubellini, V.; Ribbera, A.; Merusi, P.; Cagnasso, P.; Bizzarri, B.; de’Angelis, G.L.; Shanahan, F.; et al. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl. Environ. Microbiol. 2009, 75, 1534–1545. [CrossRef]
42. Ventura, M.; Turroni, F.; van Sinderen, D. Bifidobacteria: General Overview on Ecology, Taxonomy, and Genomics. In Lactic Acid Bacteria. Microbiological and Functional Aspects, 4th ed.; Lahtinen, S., Ouwehand, A.C., Salminen, S., Von wright, A., Eds.; CRC Press: New York, NY, USA, 2012; p. 149.
43. Moens, F.; Verce, M.; De Vuyst, L. Lactate-and acetate-based cross-feeding interactions between selected strains of lactobacilli, bifidobacteria and colon bacteria in the presence of inulin-type fructans. Int. J. Food Microbiol. 2017, 241, 225–236. [CrossRef]
44. Mack, D.R.; Michail, S.; Wei, S.; McDougall, L.; Hollingsworth, M.A. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am. J. Physiol. 1999, 276, G941–G950.
45. Turroni, F.; Bottacini, F.; Foroni, E.; Mulder, I.; Kim, J.H.; Zomer, A.; Sánchez, B.; Bidossi, A.; Ferrarini, A.; Giubellini, V.; et al. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc. Natl. Acad. Sci. USA 2010, 107, 19514–19519. [CrossRef]
46. Marteau, P.; Cuillerier, E.; Meance, S.; Gerhardt, M.F.; Myara, A.; Bouvier, M.; Bouley, C.; Tondu, F.; Bommelaer, G.; Grimaud, J.C. Bifidobacterium animalis strain DN-173 010 shortens the colonic transit time in healthy women: A double-blind, randomized, controlled study. Aliment. Pharmacol. Ther. 2002, 16, 587–593. [CrossRef]
47. Meng, H.; Ba, Z.; Lee, Y.; Peng, J.; Lin, J.; Fleming, J.A.; Furumoto, E.J.; Roberts, R.F.; Kris-Etherton, P.M.; Rogers, C.J. Consumption of Bifidobacterium animalis subsp. lactis BB-12 in yogurt reduced expression of TLR-2 on peripheral blood-derived monocytes and pro-inflammatory cytokine secretion in young adults. Eur. J. Nutr. 2017, 56, 649–661. [CrossRef]
48. Lugli, G.A.; Milani, C.; Turroni, F.; Duranti, S.; Ferrario, C.; Viappiani, A.; Mancabelli, L.; Mangifesta, M.; Taminiau, B.; Delcenserie, V.; et al. Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics. Appl. Environ. Microbiol. 2014, 80, 6383–6394. [CrossRef]
49. Schirmer, M.; Ijaz, U.Z.; D’Amore, R.; Hall, N.; Sloan, W.T.; Quince, C. Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Res. 2015, 43, e37. [CrossRef]
50. Rizkalla, S.W.; Luo, J.; Kabir, M.; Chevalier, A.; Pacher, N.; Slama, G. Chronic consumption of fresh but not heated yogurt improves breath hydrogen status and short-chain fatty acid profiles: A controlled study in healthy men with or without lactose maldigestion. Am. J. Clin. Nutr. 2000, 72, 1474–1479. [CrossRef]
51. Guarner, F.; Perdigon, G.; Corthier, G.; Salminen, S.; Koletzko, B.; Morelli, L. Should yoghurt cultures be considered probiotic? Br. J. Nutr. 2005, 93, 783–786. [CrossRef]
52. Plaza-Díaz, J.; Fernández-Caballero, J.Á.; Chueca, N.; García, F.; Gómez-Llorente, C.; Sáez-Lara, M.J.; Fontana, L.; Gil, Á. Pyrosequencing analysis reveals changes in intestinal microbiota of healthy adults who received a daily dose of immunomodulatory probiotic strains. Nutrients 2015, 7, 3999–4015. [CrossRef]
53. Stolaki, M.; De Vos, W.M.; Kleerebezem, M.; Zoetendal, E.G. Lactic Acid Bacteria in the gut. In Lactic Acid Bacteria. Microbiological and Functional Aspects, 4th ed.; Lahtinen, S., Ouwehand, A.C., Salminen, S., Von wright, A., Eds.; CRC Press: New York, NY, USA, 2012; pp. 385–390.
54. Lahti, L.; Salonen, A.; Kekkonen, R.A.; Salojärvi, J.; Jalanka-Tuovinen, J.; Palva, A.; Orešič, M.; de Vos, W.M. Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data. PeerJ 2013, 1, e32. [CrossRef]
55. Ferrario, C.; Taverniti, V.; Milani, C.; Fiore, W.; Laureati, M.; De Noni, I.; Stuknyte, M.; Chouaia, B.; Riso, P.; Guglielmetti, S. Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillus paracasei DG varies among healthy adults. J. Nutr. 2014, 144, 1787–1796. [CrossRef]
56. Koeth, R.A.; Wang, Z.; Levison, B.S.; Buffa, J.A.; Org, E.; Sheehy, B.T.; Britt, E.B.; Fu, X.; Wu, Y.; Li, L.; et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 2013, 19, 576–585. [CrossRef]
57. Fan, Y.; Ya, E.Z.; Ji-Dong, W.; Yu-Fan, L.; Ying, Z.; Ya-Lun, S.; Meng-Yu, M.; Rui-Ling, Z. Comparison of Microbial Diversity and Composition in Jejunum and Colon of the Alcohol-dependent Rats. J. Microbiol. Biotechnol. 2018, 28, 1883–1895. [CrossRef]
58. Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506–514. [CrossRef]
59. Claesson, M.J.; O’Sullivan, O.; Wang, Q.; Nikkilä, J.; Marchesi, J.R.; Smidt, H.; de Vos, W.M.; Ross, R.P.; O’Toole, P.W. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE 2009, 4, e6669. [CrossRef]
60. Pokusaeva, K.; Fitzgerald, G.F.; van Sinderen, D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 2011, 6, 285–306. [CrossRef]
61. Haro, C.; Rangel-Zúñiga, O.A.; Alcalá-Díaz, J.F.; Gómez-Delgado, F.; Pérez-Martínez, P.; Delgado-Lista, J.; Quintana-Navarro, G.M.; Landa, B.B.; Navas-Cortés, J.A.; Tena-Sempere, M.; et al. Intestinal microbiota is influenced by gender and body mass index. PLoS ONE 2016, 11, e0154090. [CrossRef]
62. Fransen, F.; van Beek, A.A.; Borghuis, T.; Meijer, B.; Hugenholtz, F.; van der Gaast-de Jongh, C.; Savelkoul, H.F.; de Jonge, M.I.; Faas, M.M.; Boekschoten, M.V.; et al. The impact of gut microbiota on gender-specific differences in immunity. Front. Immunol. 2017, 8, 754. [CrossRef]
63. Wahlström, A.; Sayin, S.I.; Marschall, H.U.; Bäckhed, F. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 2016, 24, 41–50. [CrossRef]
64. Hyland, N.P.; Cryan, J.F. Microbe-host interactions: Influence of the gut microbiota on the enteric nervous system. Dev. Biol. 2016, 417, 182–187. [CrossRef]