The fermented soy beverage Q-CAN® plus induces beneficial changes in the oral and intestinal microbiome

Evangelos Dioletis, Ricardo S Paiva, Eleanna Kaffe, Eric R Secor, Theresa R Weiss, Maxine R Fields, Xinshou Ouyang, Ather Ali, Evangelos Dioletis, Ricardo S Paiva, Eleanna Kaffe, Eric R Secor, Theresa R Weiss, Maxine R Fields, Xinshou Ouyang, Ather Ali

Abstract

Background: Soy products are associated with many beneficial health consequences, but their effects on the human intestinal microbiome are poorly characterized.

Objectives: To identify the changes in the oral and fecal microbiome in lean and obese participants due to consumption of Q-CAN®, and to assess the expected consequences of these changes based on the published literature.

Methods: Prospective study of lean (10) and obese (9) participants consuming Q-CAN® twice daily for 4 weeks with 8 weeks follow-up. Microbial DNA was extracted from saliva and stool samples, amplified against the V4 region of the 16S ribosomal RNA gene and data analyzed using QIIME 1.9.1 bioinformatics. Four hundred forty-four samples were collected in total, 424 of which were productive and yielded good quality data.

Results: STOOL. In the lean population Bifidobacteria and Blautia show a significant increase while taking Q-CAN®, and there was a trend for this in the obese population. ORAL. There were relatively fewer major changes in the oral microbiome with an increase in the family Veillonellaceae in the lean population while on Q-CAN®.

Conclusion: Q-CAN® consumption induced a number of significant changes in the fecal and oral microbiome. Most notably an increase in the stool microbiome of Bifidobacteria and Blautia, both of which are associated with positive health benefits, and in the saliva an increase in Veillonellaceae.

Trial registration: This trial was registered with Clinicaltrials.gov on January 14th 2016. ClinicalTrials.gov Identifier: NCT02656056.

Keywords: Commensals; Gut microbiome; Obesity; Oral microbiome; Soy.

Conflict of interest statement

There are no competing interests.

Figures

Fig. 1
Fig. 1
a Depiction of the time-frame of Q-CAN® consumption or withdrawal. b-d Shannon Diversity Index of intestinal or oral microbiome is not altered upon Q-CAN® consumption or withdrawal in lean or obese people. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 9 participants), Lean (n = 10 participants). The data are presented as Tukey box plots showing the median values
Fig. 2
Fig. 2
Intestinal microbiome analysis at the level of Phylum. a-f Bacteria at Phylum level in both lean and obese shows that only Actinobacteria and Fusobacteria are altered upon Q-CAN® consumption. e The ratio of Firmicutes/Bacteroidetes has a trend for increase in obese compared to lean ones. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 9 participants), Lean (n = 10 participants). The data are presented as median with SEM, *p < 0.05
Fig. 3
Fig. 3
Intestinal microbiome analysis at the level of Family. A-D) Bacteria at Family level in both lean and obese shows that only Bifidobacteriaea, S24–7 and EtOH8 are altered upon Q-CAN® consumption. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 9 participants), Lean (n = 10 participants). The data are presented as median with SEM, *p < 0.05
Fig. 4
Fig. 4
Intestinal microbiome analysis at the level of genus. a-f Bacteria distribution at genus level in both lean and obese participants. The levels of Blautia, Bifidobacterium and Staphylococcus genera are altered upon Q-CAN® consumption in lean and the levels of Sutterela and Lactobacillus in obese. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 9 participants), Lean (n = 10 participants). The data are presented as median with SEM, *p < 0.05
Fig. 5
Fig. 5
Intestinal microbiome analysis at the level of species. a-b Relative abundance of bacterial species is visualized by heat map. Each column represents a subject and each colored row a bacterial taxon. The intensity of the red color represents the highest abundance taxa and the intensity of the blue color the lowest abundance taxa in lean and obese people. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 9 participants), Lean (n = 10 participants)
Fig. 6
Fig. 6
Oral microbiome analysis at the level of Family and Genus. a, b Bacteria at Family level in both lean and obese shows increase of Veillonelleae in lean and Tissierallacea in obese upon Q-CAN® consumption. c-f Bacteria distribution at genus level in both lean and obese participants. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 10 participants), Lean (n = 10 participants). The data are presented as median with SEM, *p < 0.05
Fig. 7
Fig. 7
Oral microbiome analysis at the level of Species. a-b Relative abundance of bacterial species is visualized by heat map. Each column represents a subject and each colored row a bacterial taxon. The intensity of the red color represents the highest abundance taxa and the intensity of the blue color the lowest abundance taxa in lean and obese people. The results are the average of 3 visits in pre Q-CAN® group, 4 visits in on Q-CAN® group and 4 visits in post Q-CAN® group for each participant. Obese (n = 10 participants), Lean (n = 10 participants)

References

    1. Messina M. Soy and health update: evaluation of the clinical and epidemiologic literature. Nutrients. 2016;8(12):754. doi: 10.3390/nu8120754.
    1. Kwon DY, et al. Long-term consumption of fermented soybean-derived Chungkookjang attenuates hepatic insulin resistance in 90% pancreatectomized diabetic rats. Horm Metab Res. 2007;39(10):752–757. doi: 10.1055/s-2007-990287.
    1. Kwon DY, et al. Antidiabetic effects of fermented soybean products on type 2 diabetes. Nutr Res. 2010;30(1):1–13. doi: 10.1016/j.nutres.2009.11.004.
    1. Nozue M, et al. Fermented soy product intake is inversely associated with the development of high blood pressure: the Japan public health center-based prospective study. J Nutr. 2017;147(9):1749–1756.
    1. Lee Y, et al. PPARgamma2 C1431T polymorphism interacts with the antiobesogenic effects of Kochujang, a Korean fermented, soybean-based red pepper paste, in overweight/obese subjects: a 12-week, double-blind randomized clinical trial. J Med Food. 2017;20(6):610–617. doi: 10.1089/jmf.2016.3911.
    1. Lourenco JM, et al. The successional changes in the gut microbiome of pasture-raised chickens fed soy-containing and soy-free diets. Front Sustain Food Syst. 2019;3:1–8. doi: 10.3389/fsufs.2019.00001.
    1. Boue S, et al. A novel gastrointestinal microbiome modulator from soy pods reduces absorption of dietary fat in mice. Obesity (Silver Spring) 2016;24(1):87–95. doi: 10.1002/oby.21197.
    1. Cheng IC, et al. Effect of fermented soy milk on the intestinal bacterial ecosystem. World J Gastroenterol. 2005;11(8):1225–1227. doi: 10.3748/wjg.v11.i8.1225.
    1. Fernandez-Raudales D, et al. Consumption of different soymilk formulations differentially affects the gut microbiomes of overweight and obese men. Gut Microbes. 2012;3(6):490–500. doi: 10.4161/gmic.21578.
    1. Inoguchi S, et al. Effects of non-fermented and fermented soybean milk intake on faecal microbiota and faecal metabolites in humans. Int J Food Sci Nutr. 2012;63(4):402–410. doi: 10.3109/09637486.2011.630992.
    1. Piacentini G, et al. Molecular characterization of intestinal microbiota in infants fed with soymilk. J Pediatr Gastroenterol Nutr. 2010;51(1):71–76. doi: 10.1097/MPG.0b013e3181dc8b02.
    1. Vazquez L, et al. Effect of soy isoflavones on growth of representative bacterial species from the human gut. Nutrients. 2017;9(7):727. doi: 10.3390/nu9070727.
    1. Miele L, et al. Impact of gut microbiota on obesity, diabetes, and cardiovascular disease risk. Curr Cardiol Rep. 2015;17(12):120. doi: 10.1007/s11886-015-0671-z.
    1. Kolodziejczyk AA, et al. The role of the microbiome in NAFLD and NASH. EMBO Mol Med. 2018;11(2):e9302.
    1. Ambalam P, et al. Probiotics, prebiotics and colorectal cancer prevention. Best Pract Res Clin Gastroenterol. 2016;30(1):119–131. doi: 10.1016/j.bpg.2016.02.009.
    1. Yu LX, Schwabe RF. The gut microbiome and liver cancer: mechanisms and clinical translation. Nat Rev Gastroenterol Hepatol. 2017;14(9):527–539. doi: 10.1038/nrgastro.2017.72.
    1. Hruby A, Hu FB. The epidemiology of obesity: a big picture. Pharmacoeconomics. 2015;33(7):673–689. doi: 10.1007/s40273-014-0243-x.
    1. Loman BR, et al. Chemotherapy-induced neuroinflammation is associated with disrupted colonic and bacterial homeostasis in female mice. Sci Rep. 2019;9(1):16490. doi: 10.1038/s41598-019-52893-0.
    1. Binda C, et al. Actinobacteria: a relevant minority for the maintenance of gut homeostasis. Dig Liver Dis. 2018;50(5):421–428. doi: 10.1016/j.dld.2018.02.012.
    1. Hardy H, et al. Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients. 2013;5(6):1869–1912. doi: 10.3390/nu5061869.
    1. Fukuda S, et al. Acetate-producing bifidobacteria protect the host from enteropathogenic infection via carbohydrate transporters. Gut Microbes. 2012;3(5):449–454. doi: 10.4161/gmic.21214.
    1. Scott KP, et al. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. FEMS Microbiol Ecol. 2014;87(1):30–40. doi: 10.1111/1574-6941.12186.
    1. Davila AM, et al. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacol Res. 2013;68(1):95–107. doi: 10.1016/j.phrs.2012.11.005.
    1. Backhed F, Crawford PA. Coordinated regulation of the metabolome and lipidome at the host-microbial interface. Biochim Biophys Acta. 2010;1801(3):240–245. doi: 10.1016/j.bbalip.2009.09.009.
    1. Younes H, et al. Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. Br J Nutr. 2001;86(4):479–485. doi: 10.1079/BJN2001430.
    1. Sun M, et al. Regulatory immune cells in regulation of intestinal inflammatory response to microbiota. Mucosal Immunol. 2015;8(5):969–978. doi: 10.1038/mi.2015.49.
    1. McCarville JL, Caminero A, Verdu EF. Novel perspectives on therapeutic modulation of the gut microbiota. Ther Adv Gastroenterol. 2016;9(4):580–593. doi: 10.1177/1756283X16637819.
    1. Duca FA, Sakar Y, Covasa M. The modulatory role of high fat feeding on gastrointestinal signals in obesity. J Nutr Biochem. 2013;24(10):1663–1677. doi: 10.1016/j.jnutbio.2013.05.005.
    1. Scarpellini E, Tack J. Obesity and metabolic syndrome: an inflammatory condition. Dig Dis. 2012;30(2):148–153. doi: 10.1159/000336664.
    1. Cano PG, et al. Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet-fed mice. Obesity (Silver Spring) 2013;21(11):2310–2321. doi: 10.1002/oby.20330.
    1. Gionchetti P, et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology. 2003;124(5):1202–1209. doi: 10.1016/S0016-5085(03)00171-9.
    1. Abu-Shanab A, Quigley EM. The role of the gut microbiota in nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol. 2010;7(12):691–701. doi: 10.1038/nrgastro.2010.172.
    1. Selinger CP, et al. Probiotic VSL#3 prevents antibiotic-associated diarrhoea in a double-blind, randomized, placebo-controlled clinical trial. J Hosp Infect. 2013;84(2):159–165. doi: 10.1016/j.jhin.2013.02.019.
    1. Pinto-Sanchez MI, et al. Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology. 2017;153(2):448–459. doi: 10.1053/j.gastro.2017.05.003.
    1. Castellarin M, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22(2):299–306. doi: 10.1101/gr.126516.111.
    1. Sears CL. The who, where and how of fusobacteria and colon cancer. Elife. 2018;7:e28434. doi: 10.7554/eLife.28434.
    1. Ormerod KL, et al. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals. Microbiome. 2016;4(1):36. doi: 10.1186/s40168-016-0181-2.
    1. Ozato N, et al. Blautia genus associated with visceral fat accumulation in adults 20-76 years of age. NPJ Biofilms Microbiomes. 2019;5:28. doi: 10.1038/s41522-019-0101-x.
    1. Jenq RR, et al. Intestinal Blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant. 2015;21(8):1373–1383. doi: 10.1016/j.bbmt.2015.04.016.
    1. Martinez I, et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 2013;7(2):269–280. doi: 10.1038/ismej.2012.104.
    1. Goodman B, et al. Treating cancer using a blautia strain. US Patent Office. 2019;2019 0240268(1):1–45.
    1. Counotte GH, et al. Role of Megasphaera elsdenii in the fermentation of dl-[2-C] lactate in the rumen of dairy cattle. Appl Environ Microbiol. 1981;42(4):649–655. doi: 10.1128/AEM.42.4.649-655.1981.
    1. Stanton TB, Humphrey SB. Persistence of antibiotic resistance: evaluation of a probiotic approach using antibiotic-sensitive MEGASPHAERA elsdenii strains to prevent colonization of swine by antibiotic-resistant strains. Appl Environ Microbiol. 2011;77(20):7158–7166. doi: 10.1128/AEM.00647-11.
    1. Virgili E, et al. Soy intake and breast cancer. J Health Med Inf. 2018;9(316):1–3.
    1. Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe. 2011;10(4):324–335. doi: 10.1016/j.chom.2011.10.003.
    1. Le Chatelier E, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–546. doi: 10.1038/nature12506.
    1. Peters BA, et al. A taxonomic signature of obesity in a large study of American adults. Sci Rep. 2018;8(1):9749. doi: 10.1038/s41598-018-28126-1.
    1. Kim EK, et al. Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients. Nutr Res. 2011;31(6):436–443. doi: 10.1016/j.nutres.2011.05.011.
    1. Kim MS, et al. Long-term fermented soybean paste improves metabolic parameters associated with non-alcoholic fatty liver disease and insulin resistance in high-fat diet-induced obese mice. Biochem Biophys Res Commun. 2018;495(2):1744–1751. doi: 10.1016/j.bbrc.2017.12.003.
    1. Mohd Yusof H, et al. Hepatoprotective effect of fermented soybean (nutrient enriched soybean tempeh) against alcohol-induced liver damage in mice. Evid Based Complement Alternat Med. 2013;2013:274274. doi: 10.1155/2013/274274.
    1. Song JL, et al. Anti-colitic effects of kanjangs (fermented soy sauce and sesame sauce) in dextran sulfate sodium-induced colitis in mice. J Med Food. 2014;17(9):1027–1035. doi: 10.1089/jmf.2013.3119.
    1. Takagi A, Kano M, Kaga C. Possibility of breast cancer prevention: use of soy isoflavones and fermented soy beverage produced using probiotics. Int J Mol Sci. 2015;16(5):10907–10920. doi: 10.3390/ijms160510907.
    1. Jayachandran M, Xu B. An insight into the health benefits of fermented soy products. Food Chem. 2019;271:362–371. doi: 10.1016/j.foodchem.2018.07.158.

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