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Artificial sweeteners induce glucose intolerance by altering the gut microbiota

Author

Listed:
  • Jotham Suez

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Tal Korem

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • David Zeevi

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Gili Zilberman-Schapira

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Christoph A. Thaiss

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Ori Maza

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • David Israeli

    (Day Care Unit and the Laboratory of Imaging and Brain Stimulation, Kfar Shaul hospital, Jerusalem Center for Mental Health, Jerusalem 91060, Israel)

  • Niv Zmora

    (Tel Aviv Sourasky Medical Center, Tel Aviv 64239, Israel
    Research Center for Digestive Tract and Liver Diseases, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 69978, Israel
    Digestive Center, Tel Aviv Sourasky Medical Center, Tel Aviv 64239, Israel)

  • Shlomit Gilad

    (The Nancy and Stephen Grand Israel National Center for Personalized Medicine (INCPM), Weizmann Institute of Science, Rehovot 76100, Israel)

  • Adina Weinberger

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Yael Kuperman

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Alon Harmelin

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Ilana Kolodkin-Gal

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Hagit Shapiro

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Zamir Halpern

    (Research Center for Digestive Tract and Liver Diseases, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 69978, Israel
    Digestive Center, Tel Aviv Sourasky Medical Center, Tel Aviv 64239, Israel)

  • Eran Segal

    (Weizmann Institute of Science, Rehovot 76100, Israel)

  • Eran Elinav

    (Weizmann Institute of Science, Rehovot 76100, Israel)

Abstract

Non-caloric artificial sweeteners (NAS) are among the most widely used food additives worldwide, regularly consumed by lean and obese individuals alike. NAS consumption is considered safe and beneficial owing to their low caloric content, yet supporting scientific data remain sparse and controversial. Here we demonstrate that consumption of commonly used NAS formulations drives the development of glucose intolerance through induction of compositional and functional alterations to the intestinal microbiota. These NAS-mediated deleterious metabolic effects are abrogated by antibiotic treatment, and are fully transferrable to germ-free mice upon faecal transplantation of microbiota configurations from NAS-consuming mice, or of microbiota anaerobically incubated in the presence of NAS. We identify NAS-altered microbial metabolic pathways that are linked to host susceptibility to metabolic disease, and demonstrate similar NAS-induced dysbiosis and glucose intolerance in healthy human subjects. Collectively, our results link NAS consumption, dysbiosis and metabolic abnormalities, thereby calling for a reassessment of massive NAS usage.

Suggested Citation

  • Jotham Suez & Tal Korem & David Zeevi & Gili Zilberman-Schapira & Christoph A. Thaiss & Ori Maza & David Israeli & Niv Zmora & Shlomit Gilad & Adina Weinberger & Yael Kuperman & Alon Harmelin & Ilana , 2014. "Artificial sweeteners induce glucose intolerance by altering the gut microbiota," Nature, Nature, vol. 514(7521), pages 181-186, October.
    • Handle: RePEc:nat:nature:v:514:y:2014:i:7521:d:10.1038_nature13793
    DOI: 10.1038/nature13793
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    Cited by:

    1. Louzada, Maria Laura da Costa & Levy, Renata Bertazzi & Martins, Ana Paula Bortoletto & Claro, Rafael Moreira & Steele, Euridice Martinez & Verly Jr., Eliseu & Cafiero, Carlo & Monteiro, Carlos August, 2017. "Validating the usage of household food acquisition surveys to assess the consumption of ultra-processed foods: Evidence from Brazil," Food Policy, Elsevier, vol. 72(C), pages 112-120.
    2. Marijana Savin & Aleksandra Vrkatić & Danijela Dedić & Tomislav Vlaški & Ivana Vorgučin & Jelena Bjelanović & Marija Jevtic, 2022. "Additives in Children’s Nutrition—A Review of Current Events," IJERPH, MDPI, vol. 19(20), pages 1-18, October.
    3. Qiao-Ping Wang & Duncan Browman & Herbert Herzog & G Gregory Neely, 2018. "Non-nutritive sweeteners possess a bacteriostatic effect and alter gut microbiota in mice," PLOS ONE, Public Library of Science, vol. 13(7), pages 1-13, July.
    4. Rajita Menon & Vivek Ramanan & Kirill S Korolev, 2018. "Interactions between species introduce spurious associations in microbiome studies," PLOS Computational Biology, Public Library of Science, vol. 14(1), pages 1-20, January.
    5. Yoona Kim & Jennifer B. Keogh & Peter M. Clifton, 2020. "Consumption of a Beverage Containing Aspartame and Acesulfame K for Two Weeks Does Not Adversely Influence Glucose Metabolism in Adult Males and Females: A Randomized Crossover Study," IJERPH, MDPI, vol. 17(23), pages 1-9, December.
    6. Lidy M Pelsser & Klaas Frankena & Jan Toorman & Rob Rodrigues Pereira, 2017. "Diet and ADHD, Reviewing the Evidence: A Systematic Review of Meta-Analyses of Double-Blind Placebo-Controlled Trials Evaluating the Efficacy of Diet Interventions on the Behavior of Children with ADH," PLOS ONE, Public Library of Science, vol. 12(1), pages 1-25, January.
    7. Yun Han Kwon & Suhrid Banskota & Huaqing Wang & Laura Rossi & Jensine A. Grondin & Saad A. Syed & Yeganeh Yousefi & Jonathan D. Schertzer & Katherine M. Morrison & Michael G. Wade & Alison C. Holloway, 2022. "Chronic exposure to synthetic food colorant Allura Red AC promotes susceptibility to experimental colitis via intestinal serotonin in mice," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Alexandria Turner & Martin Veysey & Simon Keely & Christopher J. Scarlett & Mark Lucock & Emma L. Beckett, 2020. "Intense Sweeteners, Taste Receptors and the Gut Microbiome: A Metabolic Health Perspective," IJERPH, MDPI, vol. 17(11), pages 1-18, June.
    9. Emanuele Rinninella & Marco Cintoni & Pauline Raoul & Antonio Gasbarrini & Maria Cristina Mele, 2020. "Food Additives, Gut Microbiota, and Irritable Bowel Syndrome: A Hidden Track," IJERPH, MDPI, vol. 17(23), pages 1-15, November.

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