L. plantarum, L. fermentum, and B. breve Beads Modified the Intestinal Microbiota and Alleviated the Inflammatory Response in High-Fat Diet–Fed Mice


This paper aims to study the effects of compound microbe-based beads on changes in the intestinal microbiota and alleviation of high-fat (HF) diet–induced inflammatory responses. Forty-eight mice were fed base chow or a high-fat diet for 4 weeks and then randomly separated into six groups: normal diet (group A), high-fat diet (group B), high-fat positive control (fed with high-fat chow plus Tetrahydrolipstatin, group C), high-fat chow plus B. breve beads (group D), high-fat chow plus L. plantarum-L. fermentum beads (group E), and high-fat chow plus L. plantarum-L. fermentum-B. breve beads (group F). The body weights were measured. The serum cytokine and lipid levels were determined by ELISA, and high-throughput sequence analysis of the fecal microbiota was conducted. Beads with cell encapsulation rates higher than 99% decreased the body weight from 50.97 ± 3.44 g in group B to 42.64 ± 2.63 g in group F at the end of the experiment (p = 0.00019). The total cholesterol content in group F was 80.14 ± 9.37 mmol/L, which was significantly lower than that in group A (96.13 ± 24.07 mmol/L) (p = 0.02765), group B (102.52 ± 12.20 mmol/L) (p = 0.00196), and group C (98.99 ± 11.32 mmol/L) (p = 0.00804). In addition, the serum IL-6 level showed no significant difference between group F and the base chow control group. The microbial cell-loaded bead intervention led to increased abundances of Bifidobacterium and Lactobacillus in mouse feces. Oral administration of three strain-based beads led to alleviation of inflammatory reactions in high-fat diet–fed mice.

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  1. 1.

    Korneychuk N (2014) Composition of the intestinal flora and predisposition to obesity. Med Sci M/s 30:41

    Google Scholar 

  2. 2.

    Yazigi A, Gaborit B, Nogueira JP, Butiler ME, Andreelli F (2008) Role of intestinal flora in insulin resistance and obesity. Presse Med 37:1427–1430

    Article  Google Scholar 

  3. 3.

    Schoefer L (2015) Intestinal bacteria promotes obesity - new findings on the influence of the intestinal flora on the body-mass-index. Forsch Komplementmed 106:421–421

    Google Scholar 

  4. 4.

    Moran CP, Shanahan F (2014) Gut microbiota and obesity: role in aetiology and potential therapeutic target. Best Pract Res Clin Gastroenterol 28:585–597

    CAS  Article  Google Scholar 

  5. 5.

    Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102:11070–11075. https://doi.org/10.1073/pnas.0504978102

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 106:2365–2370

    CAS  Article  Google Scholar 

  7. 7.

    de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE (2010) Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 299:G440–G448

    Article  Google Scholar 

  8. 8.

    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) 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 11:506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  9. 9.

    Chiou YS, Lee PS, Pan MH (2018) Food bioactives and their effects on obesity-accelerated inflammatory bowel disease. J Agric Food Chem 66:773–779. https://doi.org/10.1021/acs.jafc.7b05854

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Kondo S, Xiao JZ, Sugahara H, Satoh T, Yaeshima T, Iwatsuki K, Odamaki T, Kamei A, Takahashi S, Abe AK (2010) Antiobesity effects of Bifidobacterium breve strain B-3 supplementation in a mouse model with high-fat diet-induced obesity. Biosci Biotechnol Biochem 74:1656–1661. https://doi.org/10.1271/bbb.100267

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Moya-Perez A, Neef A, Sanz Y (2015) Bifidobacterium pseudocatenulatum CECT 7765 reduces obesity-associated inflammation by restoring the lymphocyte-macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS One 10:e0126976. https://doi.org/10.1371/journal.pone.0126976

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Kong LC, Tap J, Aronwisnewsky J, Pelloux V, Basdevant A, Bouillot JL, Zucker JD, Doré J, Clément K (2013) Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr 98:16–24

    CAS  Article  Google Scholar 

  13. 13.

    Wang Y, Xie J, Li Y, Dong S, Liu H, Chen J, Wang Y, Zhao S, Zhang Y, Zhang H (2016) Probiotic Lactobacillus casei Zhang reduces pro-inflammatory cytokine production and hepatic inflammation in a rat model of acute liver failure. Eur J Nutr 55:821–831. https://doi.org/10.1007/s00394-015-0904-3

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Ahlroos T, Tynkkynen S (2009) Quantitative strain-specific detection of Lactobacillus rhamnosus GG in human faecal samples by real-time PCR. J Appl Microbiol 106:506–514. https://doi.org/10.1111/j.1365-2672.2008.04018.x

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Kim DH, Kim H, Jeong D, Kang IB, Chon JW, Kim HS, Song KY, Seo KH (2017) Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: targeted and untargeted community analysis with correlation of biomarkers. J Nutr Biochem 44:35–43. https://doi.org/10.1016/j.jnutbio.2017.02.014

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Li XL, Song Y, Ma XY, Zhang YY, Liu XY, Cheng L, Han DQ, Shi Y, Sun Q, Yang CH, Pan B, Sun QS (2018) Lactobacillus plantarum and Lactobacillus fermentum alone or in combination regulate intestinal flora composition and systemic immunity to alleviate obesity syndrome in high-fat diet rat. Int J Food Sci Technol 53(1):137–146. https://doi.org/10.1111/ijfs.13567

    CAS  Article  Google Scholar 

  17. 17.

    Li MY, Jin YX, Wang YW, Meng L, Zhang N, Sun Y, Hao JF, Fu Q, Sun QS (2019) Preparation of Bifidobacterium breve encapsulated in low methoxyl pectin beads and its effects on yogurt quality. J Dairy Sci 102(6):4832–4843. https://doi.org/10.3168/jds.2018-15597

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Sandoval-Castilla O, Lobato-Calleros C, García-Galindo HS, Alvarez-Ramírez J, Vernon-Carter EJ (2010) Textural properties of alginate–pectin beads and survivability of entrapped Lb. casei in simulated gastrointestinal conditions and in yoghurt. Food Res Int 43:111–117. https://doi.org/10.1016/j.foodres.2009.09.010

    CAS  Article  Google Scholar 

  19. 19.

    Oehme A, Valotis A, Krammer G, Zimmermann I, Schreier P (2011) Preparation and characterization of shellac-coated anthocyanin pectin beads as dietary colonic delivery system. Mol Nutr Food Res 55(Suppl 1):S75–S85. https://doi.org/10.1002/mnfr.201000467

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Sandolo C, Pechine S, Le Monnier A, Hoys S, Janoir C, Coviello T, Alhaique F, Collignon A, Fattal E, Tsapis N (2011) Encapsulation of Cwp84 into pectin beads for oral vaccination against Clostridium difficile. Eur J Pharm Biopharm 79:566–573. https://doi.org/10.1016/j.ejpb.2011.05.011

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Nguyen AT, Winckler P, Loison P, Wache Y, Chambin O (2014) Physico-chemical state influences in vitro release profile of curcumin from pectin beads. Colloids Surf B: Biointerfaces 121:290–298. https://doi.org/10.1016/j.colsurfb.2014.05.023

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Ghibaudo F, Gerbino E, Hugo AA, Simoes MG, Alves P, Costa BFO, Campo Dall' Orto V, Gomez-Zavaglia A, Simoes PN (2018) Development and characterization of iron-pectin beads as a novel system for iron delivery to intestinal cells. Colloids Surf B: Biointerfaces 170:538–543. https://doi.org/10.1016/j.colsurfb.2018.06.052

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Shamekhi F, Shuhaimi M, Ariff A, Manap YA (2013) Cell viability of microencapsulated Bifidobacterium animalis subsp. lactis under freeze-drying, storage and gastrointestinal tract simulation conditions. Folia Microbiol 58:91–101. https://doi.org/10.1007/s12223-012-0183-9

    CAS  Article  Google Scholar 

  24. 24.

    Zhao JL, Zhao YY, Zhu WJ (2017) A high-fat, high-protein diet attenuates the negative impact of casein-induced chronic inflammation on testicular steroidogenesis and sperm parameters in adult mice. Gen Comp Endocrinol 252:48–59. https://doi.org/10.1016/j.ygcen.2017.07.013

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Mashmoul M, Azlan A, Yusof BNM, Khaza'ai H, Mohtarrudin N, Boroushaki MT (2014) Effects of saffron extract and crocin on anthropometrical, nutritional and lipid profile parameters of rats fed a high fat diet. J Funct Foods 8:180–187. https://doi.org/10.1016/j.jff.2014.03.017

    CAS  Article  Google Scholar 

  26. 26.

    Almeida MA, Nadal JM, Grassiolli S, Paludo KS, Zawadzki SF, Cruz L, Paula JP, Farago PV (2014) Enhanced gastric tolerability and improved anti-obesity effect of capsaicinoids-loaded PCL microparticles. Mater Sci Eng C Mater Biol Appl 40:345–356. https://doi.org/10.1016/j.msec.2014.03.049

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Zhang X, Zhang M, Ho C-T, Guo X, Wu Z, Weng P, Yan M, Cao J (2018) Metagenomics analysis of gut microbiota modulatory effect of green tea polyphenols by high fat diet-induced obesity mice model. J Funct Foods 46:268–277. https://doi.org/10.1016/j.jff.2018.05.003

    CAS  Article  Google Scholar 

  28. 28.

    Jiménez-Pranteda ML, Pérez-Davó A, Monteoliva-Sánchez M, Ramos-Cormenzana A, Aguilera M (2015) Food omics validation: towards understanding key features for gut microbiota, probiotics and human health. Food Analyt Method 8:272–289

    Article  Google Scholar 

  29. 29.

    Li C, Ding Q, Nie SP, Zhang YS, Xiong T, Xie MY (2014) Carrot juice fermented with Lactobacillus plantarum NCU116 ameliorates type 2 diabetes in rats. J Agric Food Chem 62(49):11884–11891. https://doi.org/10.1021/jf503681r

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Wu CC, Weng WL, Lai WL, Tsai HP, Liu WH, Lee MH, Tsai YC (2015) Effect of Lactobacillus plantarum strain K21 on high-fat diet-fed obese mice. Evid Based Complement Alternat Med 2015:391767. https://doi.org/10.1155/2015/391767

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Zhang W, Liao J, Li H, Dong H, Bai H, Yang A, Hammock BD, Yang GY (2013) Reduction of inflammatory bowel disease-induced tumor development in IL-10 knockout mice with soluble epoxide hydrolase gene deficiency. Mol Carcinog 52:726–738

    CAS  Article  Google Scholar 

  32. 32.

    Zhou Y, Wang H, Liang L, Zhao WC, Chen Y, Deng HZ (2010) Total alkaloids of Sophora alopecuroides increases the expression of CD4+ CD25+ Tregs and IL-10 in rats with experimental colitis. Am J Chin Med 38:265–277

    CAS  Article  Google Scholar 

  33. 33.

    Bouaziz JD, Le Buanec H, Saussine A, Bensussan A, Bagot M (2012) IL-10 producing regulatory b cells in mice and humans: state of the art. Curr Mol Med 12:519–527

    CAS  Article  Google Scholar 

  34. 34.

    Wang L, Lin Q, Yang T, Liang Y, Nie Y, Luo Y, Shen J, Fu X, Tang Y, Luo F (2017) Oryzanol modifies high fat diet-induced obesity, liver gene expression profile, and inflammation response in mice. J Agric Food Chem 65:8374–8385. https://doi.org/10.1021/acs.jafc.7b03230

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Wunderlich CM, Ackermann PJ, Ostermann AL, Adams-Quack P, Vogt MC, Tran ML, Nikolajev A, Waisman A, Garbers C, Theurich S, Mauer J, Hovelmeyer N, Wunderlich FT (2018) Obesity exacerbates colitis-associated cancer via IL-6-regulated macrophage polarisation and CCL-20/CCR-6-mediated lymphocyte recruitment. Nat Commun 9:1646. https://doi.org/10.1038/s41467-018-03773-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Lim SM, Jeong JJ, Woo KH, Han MJ, Kim DH (2016) Lactobacillus sakei OK67 ameliorates high-fat diet-induced blood glucose intolerance and obesity in mice by inhibiting gut microbiota lipopolysaccharide production and inducing colon tight junction protein expression. Nutr Res 36:337–348. https://doi.org/10.1016/j.nutres.2015.12.001

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Tanida M, Shen J, Maeda K, Horii Y, Yamano T, Fukushima Y, Nagai K (2008) High-fat diet-induced obesity is attenuated by probiotic strain Lactobacillus paracasei ST11 (NCC2461) in rats. Obes Res Clin Pract 2:I-ii. https://doi.org/10.1016/j.orcp.2008.04.003

    Article  PubMed  Google Scholar 

  38. 38.

    Million M, Maraninchi M, Henry M, Armougom F, Richet H, Carrieri P, Valero R, Raccah D, Vialettes B, Raoult D (2012) Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes 36:817–825. https://doi.org/10.1038/ijo.2011.153

    CAS  Article  Google Scholar 

  39. 39.

    Zhang Y, Tang K, Deng Y, Chen R, Liang S, Xie H, He Y, Chen Y, Yang Q (2018) Effects of shenling baizhu powder herbal formula on intestinal microbiota in high-fat diet-induced NAFLD rats. Biomed Pharmacother 102:1025–1036. https://doi.org/10.1016/j.biopha.2018.03.158

    Article  PubMed  Google Scholar 

  40. 40.

    Yuan H, Shi F, Meng L, Wang W (2018) Effect of sea buckthorn protein on the intestinal microbial community in streptozotocin-induced diabetic mice. Int J Biol Macromol 107:1168–1174. https://doi.org/10.1016/j.ijbiomac.2017.09.090

    CAS  Article  PubMed  Google Scholar 

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This work was supported by the Heilongjiang Province Natural Science Foundation of China (C2016049) and Harbin City Technology Bureau Youth Talented Person Project (RC2017QN020010).

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Correspondence to Xiuliang Li.

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Sun, Q., Liu, X., Zhang, Y. et al. L. plantarum, L. fermentum, and B. breve Beads Modified the Intestinal Microbiota and Alleviated the Inflammatory Response in High-Fat Diet–Fed Mice. Probiotics & Antimicro. Prot. 12, 535–544 (2020). https://doi.org/10.1007/s12602-019-09564-3

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  • Bifidobacterium breve
  • Lactobacillus plantarum
  • Lactobacillus fermentum
  • High-fat diet
  • Inflammatory response
  • Intestinal microbiota