3,521
Views
4
CrossRef citations to date
0
Altmetric
Research Paper

Effect of synbiotic supplementation on immune parameters and gut microbiota in healthy adults: a double-blind randomized controlled trial

, , , , , , , , , , , , & show all
Article: 2247025 | Received 03 Mar 2023, Accepted 08 Aug 2023, Published online: 23 Aug 2023

References

  • Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30(6):492–16. doi:10.1038/s41422-020-0332-7.
  • Libertucci J, Young VB. The role of the microbiota in infectious diseases. Nat Microbiol. 2019;4(1):35–45. doi:10.1038/s41564-018-0278-4.
  • Swanson KS, Gibson GR, Hutkins R, Reimer RA, Reid G, Verbeke K, Scott KP, Holscher HD, Azad MB, Delzenne NM, et al. The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol. 2020;17(11):687–701. doi:10.1038/s41575-020-0344-2.
  • Fernandes R, Do Rosario VA, Mocellin MC, Kuntz MGF, Trindade E. Effects of inulin-type fructans, galacto-oligosaccharides and related synbiotics on inflammatory markers in adult patients with overweight or obesity: a systematic review. Clin Nutr. 2017;36(5):1197–1206. doi:10.1016/j.clnu.2016.10.003.
  • Kazemi A, Soltani S, Ghorabi S, Keshtkar A, Daneshzad E, Nasri F, Mazloomi SM. Effect of probiotic and synbiotic supplementation on inflammatory markers in health and disease status: A systematic review and meta-analysis of clinical trials. Clin Nutr. 2020;39(3):789–819. doi:10.1016/j.clnu.2019.04.004.
  • Zheng HJ, Guo J, Jia Q, Huang YS, Huang WJ, Zhang W, Zhang F, Liu WJ, Wang Y. The effect of probiotic and synbiotic supplementation on biomarkers of inflammation and oxidative stress in diabetic patients: a systematic review and meta-analysis of randomized controlled trials. Pharmacol Res. 2019;142:303–313. doi:10.1016/j.phrs.2019.02.016.
  • Zheng HJ, Guo J, Wang Q, Wang L, Wang Y, Zhang F, Huang WJ, Zhang W, Liu WJ, Wang Y. Probiotics, prebiotics, and synbiotics for the improvement of metabolic profiles in patients with chronic kidney disease: A systematic review and meta-analysis of randomized controlled trials. Crit Rev Food Sci Nutr. 2021;61(4):577–598. doi:10.1080/10408398.2020.1740645.
  • McLoughlin RF, Berthon BS, Jensen ME, Baines KJ, Wood LG. Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis. Am J Clin Nutr. 2017;106(3):930–945. doi:10.3945/ajcn.117.156265.
  • O’Connor LE, Gahche JJ, Herrick KA, Davis CD, Potischman N, Vargas AJ. Nonfood prebiotic, probiotic, and synbiotic use has increased in US adults and children from 1999 to 2018. Gastroenterology. 2021;161(2):476–486.e473. doi:10.1053/j.gastro.2021.04.037.
  • Costea PI, Hildebrand F, Arumugam M, Backhed F, Blaser MJ, Bushman FD, de Vos WM, Ehrlich SD, Fraser CM, Hattori M, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol. 2018;3(1):8–16. doi:10.1038/s41564-017-0072-8.
  • Hjorth MF, Christensen L, Larsen TM, Roager HM, Krych L, Kot W, Nielsen DS, Ritz C, Astrup A. Pretreatment Prevotella-to-Bacteroides ratio and salivary amylase gene copy number as prognostic markers for dietary weight loss. Am J Clin Nutr. 2020;111(5):1079–1086. doi:10.1093/ajcn/nqaa007.
  • Hjorth MF, Roager HM, Larsen TM, Poulsen SK, Licht TR, Bahl MI, Zohar Y, Astrup A. Erratum: Pre-treatment microbial Prevotella-to-Bacteroides ratio, determines body fat loss success during a 6-month randomized controlled diet intervention. Int J Obes (Lond). 2018;42(2):284. doi:10.1038/ijo.2018.1.
  • Braat H, van den Brande J, van Tol E, Hommes D, Peppelenbosch M, van Deventer S. Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. Am J Clin Nutr. 2004;80(6):1618–1625. doi:10.1093/ajcn/80.6.1618.
  • Gill HS, Rutherfurd KJ, Prasad J, Gopal PK. Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr. 2000;83(2):167–176. doi:10.1017/s0007114500000210.
  • Chiang BL, Sheih YH, Wang LH, Liao CK, Gill HS. Enhancing immunity by dietary consumption of a probiotic lactic acid bacterium (Bifidobacterium lactis HN019): optimization and definition of cellular immune responses. Eur J Clin Nutr. 2000;54(11):849–855. doi:10.1038/sj.ejcn.1601093.
  • Miller LE, Lehtoranta L, Lehtinen MJ. The effect of Bifidobacterium animalis ssp. lactis HN019 on cellular immune function in healthy elderly subjects: systematic review and meta-analysis. Nutrients. 2017;9(3). doi:10.3390/nu9030191.
  • Drescher LS, Thiele S, Mensink GB. A New index to measure healthy food diversity better reflects a healthy diet than traditional measures ,2. J Nutr. 2007;137(3):647–651. doi:10.1093/jn/137.3.647.
  • Macfarlane S, Cleary S, Bahrami B, Reynolds N, Macfarlane GT. Synbiotic consumption changes the metabolism and composition of the gut microbiota in older people and modifies inflammatory processes: a randomised, double-blind, placebo-controlled crossover study. Aliment Pharmacol Ther. 2013;38(7):804–816. doi:10.1111/apt.12453.
  • Gomes AC, de Sousa RG, Botelho PB, Gomes TL, Prada PO, Mota JF. The additional effects of a probiotic mix on abdominal adiposity and antioxidant status: A double-blind, randomized trial. Obesity (Silver Spring). 2017;25(1):30–38. doi:10.1002/oby.21671.
  • Quero CD, Manonelles P, Fernandez M, Abellan-Aynes O, Lopez-Plaza D, Andreu-Caravaca L, Hinchado MD, Galvez I, Ortega E. Differential Health effects on inflammatory, immunological and stress parameters in professional soccer players and sedentary individuals after consuming a synbiotic. A triple-blinded, randomized, placebo-controlled pilot study. Nutrients. 2021;13(4). doi:10.3390/nu13041321.
  • Costabile A, Bergillos-Meca T, Rasinkangas P, Korpela K, de Vos WM, Gibson GR. Effects of soluble corn fiber alone or in synbiotic combination with Lactobacillus rhamnosus GG and the pilus-deficient derivative GG-PB12 on fecal microbiota, metabolism, and markers of immune function: a randomized, double-blind, placebo-controlled, Crossover study in healthy elderly (Saimes study). Front Immunol. 2017;8:1443. doi:10.3389/fimmu.2017.01443.
  • Khabbazi A, Ahangari Maleki M, Soltani-Zangbar MS, Yousefi M, Malek Mahdavi A. Effects of synbiotic supplementation on regulatory T cells’ response in patients with axial spondyloarthritis: a randomized double-masked placebo-controlled trial. Food Funct. 2022;13(24):12733–12741. doi:10.1039/d2fo01377k.
  • Widhani A, Djauzi S, Suyatna FD, Dewi BE. Changes in gut microbiota and systemic inflammation after synbiotic supplementation in patients with systemic lupus erythematosus: a randomized, double-blind, placebo-controlled trial. Cells. 2022;11(21). doi:10.3390/cells11213419.
  • Cheng J, Laitila A, Ouwehand AC. Bifidobacterium animalis subsp. lactis HN019 effects on gut Health: a review. Front Nutr. 2021;8:790561. doi:10.3389/fnut.2021.790561.
  • Sheih YH, Chiang BL, Wang LH, Liao CK, Gill HS. Systemic immunity-enhancing effects in healthy subjects following dietary consumption of the lactic acid bacterium Lactobacillus rhamnosus HN001. J Am Coll Nutr. 2001;20(2 Suppl):149–156. doi:10.1080/07315724.2001.10719027.
  • Gutzeit C, Magri G, Cerutti A. Intestinal IgA production and its role in host-microbe interaction. Immunol Rev. 2014;260(1):76–85. doi:10.1111/imr.12189.
  • Beghin L, Tims S, Roelofs M, Rouge C, Oozeer R, Rakza T, Chirico G, Roeselers G, Knol J, Roze JC, et al. Fermented infant formula (with Bifidobacterium breve C50 and Streptococcus thermophilus O65) with prebiotic oligosaccharides is safe and modulates the gut microbiota towards a microbiota closer to that of breastfed infants. Clin Nutr. 2021;40(3):778–787. doi:10.1016/j.clnu.2020.07.024.
  • Nocerino R, Paparo L, Terrin G, Pezzella V, Amoroso A, Cosenza L, Cecere G, De Marco G, Micillo M, Albano F, et al. Cow’s milk and rice fermented with Lactobacillus paracasei CBA L74 prevent infectious diseases in children: A randomized controlled trial. Clin Nutr. 2017;36(1):118–125. doi:10.1016/j.clnu.2015.12.004.
  • Childs CE, Roytio H, Alhoniemi E, Fekete AA, Forssten SD, Hudjec N, Lim YN, Steger CJ, Yaqoob P, Tuohy KM, et al. Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study. Br J Nutr. 2014;111(11):1945–1956. doi:10.1017/S0007114513004261.
  • 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):367–375. doi:10.1017/s0007114508003097.
  • Murphy R, Morgan XC, Wang XY, Wickens K, Purdie G, Fitzharris P, Otal A, Lawley B, Stanley T, Barthow C, et al. Eczema-protective probiotic alters infant gut microbiome functional capacity but not composition: sub-sample analysis from a RCT. Benef Microbes. 2019;10(1):5–17. doi:10.3920/BM2017.0191.
  • Ahmed M, Prasad J, Gill H, Stevenson L, Gopal P. Impact of consumption of different levels of Bifidobacterium lactis HN019 on the intestinal microflora of elderly human subjects. J Nutr Health Aging. 2007;11:26–31.
  • Andrade RC, Figueredo CS, de Carvalho Alves J, Roselino MN. Evidence and updates on non-dairy synbiotic beverage development. Recent Pat Biotechnol. 2022;16(3):214–225. doi:10.2174/1872208316666220303095807.
  • Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano GAD, Gasbarrini A, Mele MC. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019;7(1). doi:10.3390/microorganisms7010014.
  • Qin P, Zou Y, Dai Y, Luo G, Zhang X, Xiao L. Characterization a novel butyric acid-producing bacterium Collinsella aerofaciens subsp. Shenzhenensis subsp. Nov. Microorganisms. 2019;7(3). doi:10.3390/microorganisms7030078.
  • Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Sci. 2018;359(6371):104–108. doi:10.1126/science.aao3290.
  • Gao X, Du L, Randell E, Zhang H, Li K, Li D. Effect of different phosphatidylcholines on high fat diet-induced insulin resistance in mice. Food Funct. 2021;12(4):1516–1528. doi:10.1039/d0fo02632h.
  • Ezeji JC, Sarikonda DK, Hopperton A, Erkkila HL, Cohen DE, Martinez SP, Cominelli F, Kuwahara T, Dichosa AEK, Good CE, et al. Parabacteroides distasonis: intriguing aerotolerant gut anaerobe with emerging antimicrobial resistance and pathogenic and probiotic roles in human health. Gut Microbes. 2021;13(1):1922241. doi:10.1080/19490976.2021.1922241.
  • Anstee QM, Day CP. S-adenosylmethionine (SAMe) therapy in liver disease: a review of current evidence and clinical utility. J Hepatol. 2012;57(5):1097–1109. doi:10.1016/j.jhep.2012.04.041.
  • Sharma A, Gerbarg P, Bottiglieri T, Massoumi L, Carpenter LL, Lavretsky H, Muskin PR, Brown RP, Mischoulon D, Work Group of the American Psychiatric Association Council on R. S-Adenosylmethionine (SAMe) for neuropsychiatric disorders: A clinician-oriented review of research. J Clin Psychiatry. 2017;78(6):e656–e667. doi:10.4088/JCP.16r11113.
  • Parada Venegas D, De la Fuente MK, Landskron G, Gonzalez MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. Short Chain Fatty Acids (SCFAs)-mediated gut Epithelial and immune regulation and its Relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277. doi:10.3389/fimmu.2019.00277.
  • Yao Y, Cai X, Fei W, Ye Y, Zhao M, Zheng C. The role of short-chain fatty acids in immunity, inflammation and metabolism. Crit Rev Food Sci Nutr. 2022;62(1):1–12. doi:10.1080/10408398.2020.1854675.
  • Wilkinson NM, Chen HC, Lechner MG, Su MA. Sex differences in immunity. Annu Rev Immunol. 2022;40:75–94. doi:10.1146/annurev-immunol-101320-125133.
  • Dominianni C, Sinha R, Goedert JJ, Pei Z, Yang L, Hayes RB, Ahn J, Wilson BA. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One. 2015;10(4):e0124599. doi:10.1371/journal.pone.0124599.
  • Choi Y, Choi SI, Kim N, Nam RH, Jang JY, Na HY, Shin CM, Lee DH, Min H, Kim YR, et al. Effect of Clostridium butyricum on high-fat diet-induced intestinal inflammation and production of short-chain fatty acids. Dig Dis Sci. 2023;68(6):2427–2440. doi:10.1007/s10620-023-07835-2.
  • Vemuri R, Sylvia KE, Klein SL, Forster SC, Plebanski M, Eri R, Flanagan KL. The microgenderome revealed: sex differences in bidirectional interactions between the microbiota, hormones, immunity and disease susceptibility. Semin Immunopathol. 2019;41(2):265–275. doi:10.1007/s00281-018-0716-7.
  • Derosa G, Guasti L, D’Angelo A, Martinotti C, Valentino MC, Di Matteo S, Bruno GM, Maresca AM, Gaudio GV, Maffioli P. Probiotic Therapy with VSL#3((R)) in patients with NAFLD: A randomized clinical trial. Front Nutr. 2022;9:846873. doi:10.3389/fnut.2022.846873.
  • Hou Q, Zhao F, Liu W, Lv R, Khine WWT, Han J, Sun Z, Lee YK, Zhang H. Probiotic-directed modulation of gut microbiota is basal microbiome dependent. Gut Microbes. 2020;12(1):1736974. doi:10.1080/19490976.2020.1736974.
  • Sandberg J, Kovatcheva-Datchary P, Bjorck I, Backhed F, Nilsson A. Abundance of gut Prevotella at baseline and metabolic response to barley prebiotics. Eur J Nutr. 2019;58(6):2365–2376. doi:10.1007/s00394-018-1788-9.
  • Santoro A, Guidarelli G, Ostan R, Giampieri E, Fabbri C, Bertarelli C, Nicoletti C, Kadi F, de Groot L, Feskens E, et al. Gender-specific association of body composition with inflammatory and adipose-related markers in healthy elderly Europeans from the NU-AGE study. Eur Radiol. 2019;29(9):4968–4979. doi:10.1007/s00330-018-5973-2.
  • Song EJ, Han K, Lim TJ, Lim S, Chung MJ, Nam MH, Kim H, Nam YD. Effect of probiotics on obesity-related markers per enterotype: a double-blind, placebo-controlled, randomized clinical trial. EPMA J. 2020;11(1):31–51. doi:10.1007/s13167-020-00198-y.
  • Hjorth MF, Blaedel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P, Roager HM, Kristiansen K, Larsen LH, Astrup A. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes (Lond). 2019;43(1):149–157. doi:10.1038/s41366-018-0093-2.
  • Christensen L, Roager HM, Astrup A, Hjorth MF. Microbial enterotypes in personalized nutrition and obesity management. Am J Clin Nutr. 2018;108(4):645–651. doi:10.1093/ajcn/nqy175.
  • Gu Y, Wang X, Li J, Zhang Y, Zhong H, Liu R, Zhang D, Feng Q, Xie X, Hong J, et al. Analyses of gut microbiota and plasma bile acids enable stratification of patients for antidiabetic treatment. Nat Commun. 2017;8(1):1785. doi:10.1038/s41467-017-01682-2.
  • Li X, Yin J, Zhu Y, Wang X, Hu X, Bao W, Huang Y, Chen L, Chen S, Yang W, et al. Effects of whole Milk supplementation on gut microbiota and cardiometabolic biomarkers in subjects with and without Lactose Malabsorption. Nutrients. 2018;10(10). doi:10.3390/nu10101403.
  • Kuczynski J, Stombaugh J, Walters WA, Gonzalez A, Caporaso JG, Knight R. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Microbiol. 2012;27(1): Chapter 1:Unit 1E 5. doi:10.1002/9780471729259.mc01e05s27.
  • Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–2461. doi:10.1093/bioinformatics/btq461.
  • Edgar RC. UNOISE2: Improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. 2016. doi:10.1101/081257.
  • Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. Picrust2 for prediction of metagenome functions. Nat Biotechnol. 2020;38(6):685–688. doi:10.1038/s41587-020-0548-6.
  • Roager HM, Licht TR, Poulsen SK, Larsen TM, Bahl MI. Microbial enterotypes, inferred by the prevotella-to-bacteroides ratio, remained stable during a 6-month randomized controlled diet intervention with the new Nordic diet. Appl Environ Microbiol. 2014;80(3):1142–1149. doi:10.1128/AEM.03549-13.