Specific signatures of the gut microbiota and increased levels of butyrate in children treated with fermented cow's milk containing heat-killed Lactobacillus paracasei CBA L74

Applied and Environmental Microbiology

Volumn 83, Issue 19, 2017, Pages

  Canani, Roberto Berni ^a   De Filippis, Francesca ^a   Nocerino, Rita ^a   Laiola, Manolo ^a   Paparo, Lorella ^a   Calignano, Antonio ^a   De Caro, Carmen ^a   Coretti, Lorena ^a   Chiariotti, Lorenzo ^a   Gilbert, Jack A ^b   Ercolini, Danilo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b University of Chicago   (United States)

Author keywords

Fecal butyrate; Gut microbiota; Immune system

Indexed keywords

BACILLI; DAIRY PRODUCTS; DIETARY SUPPLEMENTS; FERMENTED MILK; FREQUENCY MODULATION; GENES; RNA;

ALPHA AND BETA DIVERSITIES; BUTYRATE CONCENTRATIONS; DIETARY SUPPLEMENTATION; FECAL BUTYRATE; GASTROINTESTINAL TRACT; GUT MICROBIOTA; PROBIOTIC LACTOBACILLI; RANDOMIZED CONTROLLED TRIAL;

IMMUNE SYSTEM;

BACTERIUM; BIOMARKER; BUTYLTIN; CONCENTRATION (COMPOSITION); DIGESTIVE SYSTEM; FERMENTATION; GENETIC ANALYSIS; IMMUNE SYSTEM; INFECTIOUS DISEASE; MILK; RELATIVE ABUNDANCE; RNA;

FAECALIBACTERIUM; LACTOBACILLUS; LACTOBACILLUS PARACASEI; ROSEBURIA;

BUTYRIC ACID; PROBIOTIC AGENT;

ANALYSIS; ANIMAL; BACTERIUM; BOVINE; CHEMISTRY; CLASSIFICATION; CONTROLLED STUDY; FEMALE; FERMENTATION; FERMENTED MILK PRODUCT; GASTROINTESTINAL TRACT; GENETICS; HUMAN; INFANT; INTESTINE FLORA; ISOLATION AND PURIFICATION; LACTOBACILLUS PARACASEI; MALE; METABOLISM; MICROBIOLOGY; PRESCHOOL CHILD; RANDOMIZED CONTROLLED TRIAL;

ANIMALS; BACTERIA; BUTYRIC ACID; CATTLE; CHILD, PRESCHOOL; CULTURED MILK PRODUCTS; FEMALE; FERMENTATION; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; INFANT; LACTOBACILLUS PARACASEI; MALE; PROBIOTICS;

EID: 85029561977     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01206-17     Document Type: Article

References (48)

1. Maldonado J, Cañabate F, Sempere L, Vela F, Sánchez AR, Narbona E, López-Huertas E, Geerlings A, Valero AD, Olivares M, Lara-Villoslada F. 2012. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J Pediatr Gastroenterol Nutr 54:55-61. https://doi.org/10.1097/ MPG.0b013e3182333f18
2. Prodeus A, Niborski V, Schrezenmeir J, Gorelov A, Shcherbina A, Rumyantsev A. 2016. Fermented milk consumption and common infections in children attending day-care centers: a randomized trial. J Pediatr Gastroenterol Nutr 63:534-543. https://doi.org/10.1097/ MPG.0000000000001248
3. Merenstein D, Murphy M, Fokar A, Hernandez RK, Park H, Nsouli H, Sanders ME, Davis BA, Niborski V, Tondu F, Shara NM. 2010. Use of a fermented dairy probiotic drink containing Lactobacillus casei (DN-114 001) to decrease the rate of illness in kids: the DRINK study. A patientoriented, double-blind, cluster-randomized, placebo-controlled, clinical trial. Eur J Clin Nutr 64:669-677
4. Campeotto F, Suau A, Kapel N, Magne F, Viallon V, Ferraris L, Waligora-Dupriet AJ, Soulaines P, Leroux B, Kalach N, Dupont C, Butel MJ. 2011. A fermented formula in pre-term infants: clinical tolerance, gut microbiota, downregulation of faecal calprotectin and upregulation of faecal secretory IgA. Br J Nutr 105:1843-1851. https:// doi.org/10.1017/S0007114510005702
5. Nagata S, Asahara T, Ohta T, Yamada T, Kondo S, Bian L, Wang C, Yamashiro Y, Nomoto K. 2011. Effect of the continuous intake of probiotic-fermented milk containing Lactobacillus casei strain Shirota on fever in a mass outbreak of norovirus gastroenteritis and the faecal microflora in a health service facility for the aged. Br J Nutr 106:549-556. https://doi.org/10.1017/S000711451100064X
6. Thibault H, Aubert-Jacquin C, Goulet O. 2004. Effects of long-term consumption of a fermented infant formula (with Bifidobacterium breve c50 and Streptococcus thermophilus 065) on acute diarrhea in healthy infants. J Pediatr Gastroenterol Nutr 39:147-152. https://doi.org/10.1097/00005176-200408000-00004
7. Mullié C, Yazourh A, Thibault H, Odou MF, Singer E, Kalach N, Kremp O, Romond MB. 2004. Increased poliovirus-specific intestinal antibody response coincides with promotion of Bifidobacterium longum-infantis and Bifidobacterium breve in infants: a randomized, double-blind, placebocontrolled trial. Pediatr Res 56:791-795. https://doi.org/10.1203/01.PDR.0000141955.47550.A0
8. Agostoni C, Goulet O, Kolacek S, Koletzko B, Moreno L, Puntis J, Rigo J, Shamir R, Szajewska H, Turck D, ESPGHAN Committee on Nutrition. 2007. Fermented infant formulae without live bacteria. J Pediatr Gastroenterol Nutr 44:392-397. https://doi.org/10.1097/01.mpg.0000258887.93866.69
9. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, Gänzle M, Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R. 2017. Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol 44: 94-102. https://doi.org/10.1016/j.copbio.2016.11.010
10. Tamang JP, Watanabe K, Holzapfel WH. 2016. Review: Diversity of microorganisms in global fermented foods and beverages. Front Microbiol 7:377. https://doi.org/10.3389/fmicb.2016.00377
11. Unno T, Hisada T, Takahashi S. 2015. Hesperetin modifies the composition of fecal microbiota and increases cecal levels of short-chain fatty acids in rats. J Agric Food Chem 63:7952-7957. https://doi.org/10.1021/ acs.jafc.5b02649
12. Derrien M, van Hylckama Vlieg JE. 2015. Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol 23:354-366. https://doi.org/10.1016/j.tim.2015.03.002
13. Corrêa-Oliveira R, Fachi JL, Vieira A, Takeo Sato F, Vinolo MAR. 2016. Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunol 5:e73. https://doi.org/10.1038/cti.2016.17
14. Vieira AT, Rocha VM, Tavares L, Garcia CC, Teixeira MM, Oliveira SC, Cassali GD, Gamba C, Martins FS, Nicoli JR. 2015. Control of Klebsiella pneumoniae pulmonary infection and immunomodulation by oral treatment with the commensal probiotic Bifidobacterium longum 5(1A). Microbes Infect 18:180-189. https://doi.org/10.1016/j.micinf.2015.10.008
15. Vieira AT, Fukumori C, Ferreira CM. 2016. New insights into therapeutic strategies for gut microbiota modulation in inflammatory diseases. Clin Transl Immunol 5:e87. https://doi.org/10.1038/cti.2016.38
16. Asama T, Kimura Y, Kono T, Tatefuji T, Hashimoto K, Benno Y. 2016. Effects of heat-killed Lactobacillus kunkeei YB38 on human intestinal environment and bowel movement: a pilot study. Benef Microbes 7:337-344. https://doi.org/10.3920/BM2015.0132
17. Nocerino R, Paparo L, Terrin G, Pezzella V, Amoroso A, Cosenza L, Cecere G, De Marco G, Micillo M, Albano F, Nugnes R, Ferri P, Ciccarelli G, Giaccio G, Spadaro R, Maddalena Y, Berni Canani F, Berni Canani R. 2015. Cow's milk and rice fermented with Lactobacillus paracasei CBA L74 prevent infectious diseases in children: a randomized controlled trial. Clin Nutr 36:118-125. https://doi.org/10.1016/j.clnu.2015.12.004
18. Gensollen T, Iyer SS, Kasper DL, Blumberg RS. 2016. How colonization by microbiota in early life shapes the immune system. Science 352: 539-544. https://doi.org/10.1126/science.aad9378
19. Corsello G, Carta M, Marinello R, Picca M, De Marco G, Micillo M, Ferrara D, Vigneri P, Cecere G, Ferri P, Roggero P, Bedogni G, Mosca F, Paparo L, Nocerino R, Berni Canani R. 2017. Preventive effect of cow's milk fermented with L. paracasei CBA L74 on common infectious diseases in children: a multicenter randomized controlled trial. Nutrients 9:669. https://doi.org/10.3390/nu9070669
20. Konikoff T, Gophna U. 2016. Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol 24:523-524. https://doi.org/10.1016/j.tim.2016.02.015
21. Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, de los Reyes-Gavilán CG, Salazar N. 2016. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 7:185. https://doi.org/10.3389/fmicb.2016.00185
22. Rossi O, van Berkel LA, Chain F, Tanweer Khan M, Taverne N, Sokol H, Duncan SH, Flint HJ, Harmsen HJ, Langella P, Samsom JN, Wells JM. 2016. Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci Rep 6:18507. https://doi.org/10.1038/srep18507
23. De Filippis F, Pellegrini N, Laghi L, Gobbetti M, Ercolini D. 2016. Unusual subgenus associations of faecal Prevotella and Bacteroides with specific dietary patterns. Microbiome 4:57. https://doi.org/10.1186/s40168-016-0202-1
24. Ley RE. 2016. Gut microbiota in 2015: Prevotella in the gut: choose carefully. Nat Rev Gastroenterol Hepatol 13:69-70. https://doi.org/10.1038/nrgastro.2016.4
25. Duncan SH, Louis P, Flint HJ. 2004. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70:5810-5817. https://doi.org/10.1128/ AEM.70.10.5810-5817.2004
26. Berni Canani R, Di Costanzo M, Leone L, Pedata M, Meli R, Calignano A. 2011. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 17:1519-1528. https://doi.org/10.3748/wjg.v17.i12.1519
27. Keku TO, Dulal S, Deveaux A, Jovov B, Han X. 2015. The gastrointestinal microbiota and colorectal cancer. Am J Physiol Gastrointest Liver Physiol 308:G351-G363. https://doi.org/10.1152/ajpgi.00360.2012
28. Macfarlane GT, Macfarlane S. 2012. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 95:50-60. https://doi.org/10.5740/ jaoacint.SGE_Macfarlane
29. Honda K. 2015. TFH-IgA responses keep microbiota in check. Cell Host Microbe 17:144-146. https://doi.org/10.1016/j.chom.2015.01.009
30. Jenke AC, Postberg J, Mariel B, Hensel K, Foell D, Däbritz J, Wirth S. 2013. S100A12 and hBD2 correlate with the composition of the fecal microflora in ELBW infants and expansion of Escherichia coli is associated with NEC. Biomed Res Int 2013:150372. https://doi.org/10.1155/2013/150372
31. Paparo L, Aitoro R, Nocerino R, Maddalena Y, Pezzella V, Amoroso A, Di Scala C, Siciliano E, Buono B, Berni Canani R. 2015. Direct effects of fermented cow's milk with Lactobacillus paracasei CBA L74 on human enterocytes. 48th Annu Meet Eur Soc Paediatr Gastroenterol Hepatol Nutr, Amsterdam, Netherlands, 6 to 9 May 2015
32. Kolida S, Meyer D, Gibson GR. 2007. A double-blind placebo-controlled study to establish the bifidogenic dose of inulin in healthy humans. Eur J Clin Nutr 61:1189-1195. https://doi.org/10.1038/sj.ejcn.1602636
33. Abrams SA, Griffin IJ, Hawthorne KM, Liang L, Gunn SK, Darlington G, Ellis KJ. 2005. A combination of prebiotic short-and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr 82:471-476
34. Costabile A, Kolida S, Klinder A, Gietl E, Bäuerlein M, Frohberg C, Landschütze V, Gibson GR. 2010. A double-blind, placebo-controlled, crossover 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 104:1007-1017. https://doi.org/10.1017/S0007114510001571
35. Nickerson KP, Chanin R, McDonald C. 2015. Deregulation of intestinal antimicrobial defense by the dietary additive, maltodextrin. Gut Microbes 6:78-83. https://doi.org/10.1080/19490976.2015.1005477
36. Kredier RB, Earnest CP, Lundberg J, Rasmussen C, Greenwood M, Cowan P, Almada AL. 2007. Effects of ingesting protein with various forms of carbohydrate following resistance-exercise on substrate availability and markers of anabolism, catabolism, and immunity. J Int Soc Sports Nutr 4:18. https://doi.org/10.1186/1550-2783-4-18
37. Berni Canani R, Sangwan N, Stefka AT, Nocerino R, Paparo L, Aitoro R, Calignano A, Khan AA, Gilbert JA, Nagler CR. 2016. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J 10:742-750. https://doi.org/10.1038/ismej.2015.151
38. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. https://doi.org/10.1093/nar/gks808
39. Magoc T, Salzberg SL. 2011. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957-2963. https://doi.org/10.1093/bioinformatics/btr507
40. Schmieder R, Edwards R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863-864. https://doi.org/10.1093/bioinformatics/btr026
41. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Peña A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. https://doi.org/10.1038/nmeth.f.303
42. McDonald D, Price MN, Goodrich J, Nawrocki EP, De Santis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610-618. https://doi.org/10.1038/ismej.2011.139
43. De Filippis F, Vannini L, La Storia A, Laghi L, Piombino P, Stellato G, Serrazanetti DI, Gozzi G, Turroni S, Ferrocino I, Lazzi C, Di Cagno R, Gobbetti M, Ercolini D. 2014. The same microbiota and a potentially discriminant metabolome in the saliva of omnivore, ovo-lactovegetarian and vegan individuals. PLoS One 9:e112373. https://doi.org/ 10.1371/journal.pone.0112373
44. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31: 814-821. https://doi.org/10.1038/nbt.2676
45. De Filippis F, Pellegrini N, Vannini L, Jeffery IB, La Storia A, Laghi L, Serrazanetti DI, Di Cagno R, Ferrocino I, Lazzi C, Turroni S, Cocolin L, Brigidi P, Neviani E, Gobbetti M, O'Toole PW, Ercolini D. 2016. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut 65:1812-1821. https://doi.org/10.1136/gutjnl-2015-309957
46. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
47. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289-300
48. Eren AM, Maignien L, Sul WJ, Murphy LG, Grim SL, Morrison HG, Sogin ML. 2013. Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol Evol 4:1111-1119. https:// doi.org/10.1111/2041-210X.12114