Skip to main content

Blueberry and cranberry anthocyanin extracts reduce bodyweight and modulate gut microbiota in C57BL/6 J mice fed with a high-fat diet

European Journal of Nutrition volume 60, pages 2735–2746 (2021)Cite this article

Abstract

Purpose

Blueberry and cranberry are rich in anthocyanins. The present study was to investigate the effects of anthocyanin extracts from blueberry and cranberry on body weight and gut microbiota.

Methods

C57BL/6 J Mice were divided into six groups (n = 9 each) fed one of six diets namely low-fat diet (LFD), high-fat diet (HFD), HFD with the addition of 1% blueberry extract (BL), 2% blueberry extract (BH), 1% cranberry extract (CL), and 2% cranberry extract (CH), respectively.

Results

Feeding BL and BH diets significantly decreased body weight gain by 20–23%, total adipose tissue weight by 18–20%, and total liver lipids by 16–18% compared with feeding HFD. Feeding CH diet but not CL diet reduced the body weight by 27%, accompanied by a significant reduction of total plasma cholesterol by 25% and tumor necrosis factor alpha (TNF-α) by 38%. The metagenomic analysis showed that the supplementation of blueberry and cranberry anthocyanin extracts reduced plasma lipopolysaccharide concentration, accompanied by a reduction in the relative abundance of Rikenella and Rikenellaceae. Dietary supplementation of berry anthocyanin extracts promoted the growth of Lachnoclostridium, Roseburia, and Clostridium_innocuum_group in genus level, leading to a greater production of fecal short-chain fatty acids (SCFA).

Conclusions

It was concluded that both berry anthocyanins could manage the body weight and favorably modulate the gut microbiota at least in mice.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. World Health Organization (2018) Obesity and overweight. https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight

  2. Pi-Sunyer FX (2002) The obesity epidemic: pathophysiology and consequences of obesity. Obes Res 10(S12):97S-104S

    PubMed  Google Scholar 

  3. Mulders R, de Git K, Schele E, Dickson S, Sanz Y, Adan R (2018) Microbiota in obesity: interactions with enteroendocrine, immune and central nervous systems. Obes Rev 19(4):435–451

    CAS  PubMed  Google Scholar 

  4. THMP Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214

    Google Scholar 

  5. Guinane CM, Cotter PD (2013) Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Ther Adv Gastroenterol 6:295–308

    Google Scholar 

  6. Klimesova K, Kverka M, Zakostelska Z, Hudcovic T, Hrncir T, Stepankova R, Rossmann P, Ridl J, Kostovcik M, Mrazek J, Kopecny J, Kobayashi KS, Tlaskalova-Hogenova H (2013) Altered gut microbiota promotes colitis-associated cancer in IL-1 receptor–associated kinase M–deficient mice. Inflamm Bowel DIS 19(6):1266–1277

    PubMed  Google Scholar 

  7. Patterson E, Ryan PM, Cryan JF, Dinan TG, Ross RP, Fitzgerald GF, Stanton C (2016) Gut microbiota, obesity and diabetes. Postgrad Med J 92(1087):286–300

    CAS  PubMed  Google Scholar 

  8. Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503

    CAS  PubMed  Google Scholar 

  9. Shang Q, Song G, Zhang M, Shi J, Xu C, Hao J, Li G, Yu G (2017) Dietary fucoidan improves metabolic syndrome in association with increased Akkermansia population in the gut microbiota of high-fat diet-fed mice. J Funct Foods 28:138–146

    CAS  Google Scholar 

  10. Liu J, He Z, Ma N, Chen Z-Y (2019) Beneficial effects of dietary polyphenols on high-fat diet-induced obesity linking with modulation of gut microbiota. J Agric Food Chem 68(1):33–47

    PubMed  Google Scholar 

  11. Blaut M, Clavel T (2007) Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr 137(3):751S-755S

    CAS  PubMed  Google Scholar 

  12. Peron G, Hidalgo-Liberona N, González-Domínguez R, Garcia-Aloy M, Guglielmetti S, Bernardi S, Kirkup B, Kroon A, Cherubini A, Riso P, Andrés-Lacueva C (2019) Exploring the molecular pathways behind the effects of nutrients and dietary polyphenols on gut microbiota and intestinal permeability: a perspective on the potential of metabolomics and future clinical applications. J Agri Food Chem 68(7):1780–1789

    Google Scholar 

  13. Hithamani G, Srinivasan K (2014) Effect of domestic processing on the polyphenol content and bioaccessibility in finger millet (Eleusine coracana) and pearl millet (Pennisetum glaucum). Food Chem 164:55–62

    CAS  PubMed  Google Scholar 

  14. Jamar G, Estadella D, Pisani LP (2017) Contribution of anthocyanin-rich foods in obesity control through gut microbiota interactions. BioFactors 43(4):507–516

    CAS  PubMed  Google Scholar 

  15. Tian L, Tan Y, Chen G, Wang G, Sun J, Ou S, Chen W, Bai W (2018) Metabolism of anthocyanins and consequent effects on the gut microbiota. Crit Rev Food Sci Nutr 59(6):982–991

    PubMed  Google Scholar 

  16. Guglielmetti S, Fracassetti D, Taverniti V, Del Bo C, Vendrame S, Klimis-Zacas D, Arioli S, Riso P, Porrini M (2013) Differential modulation of human intestinal bifidobacterium populations after consumption of a wild blueberry (Vaccinium angustifolium) drink. J Agric Food Chem 61(34):8134–8140

    PubMed  Google Scholar 

  17. Jiao X, Wang Y, Lin Y, Lang Y, Li E, Zhang X, Zhang Q, Feng Y, Meng X, Li B (2019) Blueberry polyphenols extract as a potential prebiotic with anti-obesity effects on C57BL/6 J mice by modulating the gut microbiota. J Nutr Biochem 64:88–100

    CAS  PubMed  Google Scholar 

  18. Anhê FF, Roy D, Pilon G, Dudonné S, Matamoros S, Varin TV, Garofalo C, Moine Q, Desjardins Y, Levy E (2015) A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 64(6):872–883

    PubMed  Google Scholar 

  19. Rodríguez-Morató J, Matthan NR, Liu J, de la Torre R, Chen C-YO (2018) Cranberries attenuate animal-based diet-induced changes in microbiota composition and functionality: a randomized crossover controlled feeding trial. J Nutr Biochem 62:76–86

    PubMed  Google Scholar 

  20. He WS, Cui D, Li L, Rui J, Tong LT (2020) Plasma triacylglycerol-reducing activity of ergosterol linolenate is associated with inhibition of intestinal lipid absorption. J Funct Foods 64:103686

    CAS  Google Scholar 

  21. Zhao Y, He Z, Hao W, Zhu H, Liang N, Liu J, Zhang C, Ma KY, He WS, Yang Y (2020) Vinegars but not acetic acid are effective in reducing plasma cholesterol in hamsters fed a high-cholesterol diet. Food Funct 11(3):2163–2172

    CAS  PubMed  Google Scholar 

  22. Liu J, Hao W, He Z, Kwek E, Zhao Y, Zhu H, Liang N, Ma KY, Lei L, He WS (2019) Beneficial effects of tea water extracts on the body weight and gut microbiota in C57BL/6J mice fed with a high-fat diet. Food Funct 10(5):2847–2860

    CAS  PubMed  Google Scholar 

  23. Zhao Y, Liu J, Hao W, Zhu H, Liang N, He Z, Ma KY, Chen ZY (2017) Structure-specific effects of short-chain fatty acids on plasma cholesterol concentration in male Syrian hamsters. J Agric Food Chem 65(50):10984–10992

    CAS  PubMed  Google Scholar 

  24. Hao W, Kwek E, He Z, Zhu H, Liu J, Zhao Y, Ma KY, He WS, Chen ZY (2020) Ursolic acid alleviates hypercholesterolemia and modulates gut microbiota in Hamsters. Food Func 1:9–23

    Google Scholar 

  25. Wang J, Wang P, Li D, Hu X, Chen F (2020) Beneficial effects of ginger on prevention of obesity through modulation of gut microbiota in mice. Eur J Nutr 59(2):699–718

    CAS  PubMed  Google Scholar 

  26. Wu T, Jiang Z, Yin J, Long H, Zheng X (2016) Anti-obesity effects of artificial planting blueberry (Vaccinium ashei) anthocyanin in high-fat diet-treated mice. Int J Food Sci Nutr 67(3):257–264

    CAS  PubMed  Google Scholar 

  27. Ghattamaneni NK, Sharma A, Panchal SK, Brown L (2019) Pelargonidin 3-glucoside-enriched strawberry attenuates symptoms of DSS-induced inflammatory bowel disease and diet-induced metabolic syndrome in rats. Eur J Nutr 1:14

    Google Scholar 

  28. Kim AY, Jeong YJ, Park YB, Lee MK, Jeon SM, McGregor RA, Choi MS (2012) Dose dependent effects of lycopene enriched tomato-wine on liver and adipose tissue in high-fat diet fed rats. Food Chem 130(1):42–48

    CAS  Google Scholar 

  29. Rojo LE, Ribnicky D, Logendra S, Poulev A, Rojas-Silva P, Kuhn P, Dorn R, Grace MH, Lila MA, Raskin I (2012) In vitro and in vivo anti-diabetic effects of anthocyanins from Maqui Berry (Aristotelia chilensis). Food Chem 131(2):387–396

    CAS  PubMed  Google Scholar 

  30. Prior RL, Wu X, Gu L, Hager T, Hager A, Wilkes S, Howard L (2009) Purified berry anthocyanins but not whole berries normalize lipid parameters in mice fed an obesogenic high fat diet. Mol Nutr Food Res 53(11):1406–1418

    CAS  PubMed  Google Scholar 

  31. Kowalska K, Olejnik A (2016) Beneficial effects of cranberry in the prevention of obesity and related complications: Metabolic syndrome and diabetes–a review. J Funct foods 20:171–181

    CAS  Google Scholar 

  32. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22(3):659–661

    CAS  PubMed  Google Scholar 

  33. Hassellund SS, Flaa A, Sandvik L, Kjeldsen SE, Rostrup M (2012) Effects of anthocyanins on blood pressure and stress reactivity: a double-blind randomized placebo-controlled crossover study. J Hum Hypertens 26(6):396–404

    CAS  PubMed  Google Scholar 

  34. You Y, Han X, Guo J, Guo Y, Yin M, Liu G, Huang W, Zhan J (2018) Cyanidin-3-glucoside attenuates high-fat and high-fructose diet-induced obesity by promoting the thermogenic capacity of brown adipose tissue. J Funct Foods 41:62–71

    CAS  Google Scholar 

  35. Chang CJ, Lin CS, Lu CC, Martel J, Ko YF, Ojcius DM, Tseng SF, Wu TR, Chen YM, Young JD, Lai HC (2017) Corrigendum: Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun 8:16130

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Wu S, Yano S, Chen J, Hisanaga A, Sakao K, He X, He J, Hou D-X (2017) Polyphenols from Lonicera caerulea L. berry inhibit LPS-induced inflammation through dual modulation of inflammatory and antioxidant mediators. J Agric Food Chem 65(25):5133–5141

    CAS  PubMed  Google Scholar 

  37. Lin HV, Frassetto A, Kowalik EJ Jr, Nawrocki AR, Lu MM, Kosinski JR, Hubert JA, Szeto D, Yao X, Forrest G, Marsh DJ (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE 7(4):e35240

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SE, MacDougall K, Preston T, Tedford C, Finlayson G, Blundell JE, Bell JD, Thomas EL, Mt-lsa S, Ashby D, Gibson GR, Kolida S, Dhillo WS, Bloom SR, Morley W, Clegg S, Frost G (2015) Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut 64(11):1744–1754

    CAS  PubMed  Google Scholar 

  39. den Besten G, Bleeker A, Gerding A, van Eunen K, Havinga R, van Dijk TH, Oosterveer MH, Jonker JW, Groen AK, Reijngoud DJ, Bakker BM (2015) Short-chain fatty acids protect against high-fat diet-induced obesity via a PPARγ-dependent switch from lipogenesis to fat oxidation. Diabetes 64(7):2398–2408

    Google Scholar 

  40. Anhê FF, Nachbar RT, Varin TV, Vilela V, Dudonné S, Pilon G, Fournier M, Lecours M-A, Desjardins Y, Roy D (2017) A polyphenol-rich cranberry extract reverses insulin resistance and hepatic steatosis independently of body weight loss. Mol Metab 6(12):1563–1573

    PubMed  PubMed Central  Google Scholar 

  41. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102(31):11070–11075

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3(4):213–223

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Lee S, Keirsey KI, Kirkland R, Grunewald ZI, Fischer JG, de La Serre CB (2018) Blueberry supplementation influences the gut microbiota, inflammation, and insulin resistance in high-fat-diet-fed rats. J Nutr 148(2):209–219

    PubMed  PubMed Central  Google Scholar 

  44. Abdulamir AS, Hafidh RR, Bakar FA (2011) The association of Streptococcus bovis/gallolyticus with colorectal tumors: the nature and the underlying mechanisms of its etiological role. J Exp Clin Cancer Res 30(1):1–13

    Google Scholar 

  45. Qiao Y, Sun J, Xie Z, Shi Y, Le G (2014) Propensity to high-fat diet-induced obesity in mice is associated with the indigenous opportunistic bacteria on the interior of Peyer’s patches. J Clin Biochem Nutr 55(2):120–128

    CAS  PubMed  PubMed Central  Google Scholar 

  46. He WS, Li L, Rui J, Li J, Sun Y, Cui D, Xu B (2020) Tomato seed oil attenuates hyperlipidemia and modulates gut microbiota in C57BL/6J mice. Food Funct 23:6–12

    Google Scholar 

  47. Liu H-X, Rocha CS, Dandekar S, Wan Y-JY (2016) Functional analysis of the relationship between intestinal microbiota and the expression of hepatic genes and pathways during the course of liver regeneration. J hepatol 64(3):641–650

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Daniel H, Gholami AM, Berry D, Desmarchelier C, Hahne H, Loh G, Mondot S, Lepage P, Rothballer M, Walker A (2014) High-fat diet alters gut microbiota physiology in mice. ISME J 8(2):295–308

    CAS  PubMed  Google Scholar 

  49. Langille MG, Meehan CJ, Koenig JE, Dhanani AS, Rose RA, Howlett SE, Beiko RG (2014) Microbial shifts in the aging mouse gut. Microbiome 2(1):50

    PubMed  PubMed Central  Google Scholar 

  50. Khan I, Huang G, Li X-a, Liao W, Leong WK, Xia W, Bian X, Wu J, Hsiao WW (2019) Mushroom polysaccharides and jiaogulan saponins exert cancer preventive effects by shaping the gut microbiota and microenvironment in ApcMin/+ mice. Pharmacol Res 148:104448

    CAS  PubMed  Google Scholar 

  51. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, Flint HJ (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66(4):1654–1661

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Duncan SH, Barcenilla A, Stewart CS, Pryde SE, Flint HJ (2002) Acetate utilization and butyryl coenzyme A (CoA): acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Appl Environ Microbiol 68(10):5186–5190

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Louis P, Duncan SH, McCrae SI, Millar J, Jackson MS, Flint HJ (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186(7):2099–2106

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125(6):1401–1412

    CAS  PubMed  Google Scholar 

  55. Collins B, Hoffman J, Martinez K, Grace M, Lila MA, Cockrell C, Nadimpalli A, Chang E, Chuang CC, Zhong W, Mackert J, Shen W, Cooney P, Hopkins R, Mackert J (2016) A polyphenol-rich fraction obtained from table grapes decreases adiposity, insulin resistance and markers of inflammation and impacts gut microbiota in high-fat-fed mice. J Nutr Biochem 31:150–165

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This project was supported by a GRF grant of Hong Kong University Grants Committee (Project title:14105820).

Author information

Affiliations

  1. College of Food Science and Engineering, Nanjing University of Finance and Economics, Nanjing, China

    Jianhui Liu & Ning Ma

  2. School of Life Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong, NT, China

    Jianhui Liu, Wangjun Hao, Zouyan He, Erika Kwek, Hanyue Zhu, Ka Ying Ma & Zhen-Yu Chen

Authors
  1. Jianhui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wangjun Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zouyan He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erika Kwek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hanyue Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ning Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ka Ying Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhen-Yu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhen-Yu Chen.

Ethics declarations

Conflict of interest

The authors confirm that they have no conflicts of interest with respect to the work described in this manuscript.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Hao, W., He, Z. et al. Blueberry and cranberry anthocyanin extracts reduce bodyweight and modulate gut microbiota in C57BL/6 J mice fed with a high-fat diet. Eur J Nutr 60, 2735–2746 (2021). https://doi.org/10.1007/s00394-020-02446-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-020-02446-3

Keywords

  • Blueberry
  • Cranberry
  • Anthocyanin
  • Microbiota
  • Lipopolysaccharide
  • SCFA