Effect of fructose on the intestinal microbiota: a systematic review of randomized clinical trials

Effect of fructose on the intestinal microbiota

Autores

  • Letícia Lourenço da Silva Instituto Federal do Sudeste de Minas Gerais, Campus Barbacena https://orcid.org/0009-0001-8812-167X
  • Rayane Rodrigues Lopes Instituto Federal do Sudeste de Minas Gerais, Campus Barbacena https://orcid.org/0009-0002-9822-4514
  • Mariana Julião Guilarducci Faculdade de Saúde Pública, Universidade de São Paulo https://orcid.org/0000-0002-7217-5470
  • Olívia Gonçalves Leão Coelho Departamento de Nutrição e Saúde, Universidade Federal de Viçosa
  • Flávia Galvão Cândido Departamento de Nutrição e Saúde, Universidade Federal de Viçosa
  • Nathalia Sernizon Guimarães Faculdade Ciências Médicas de Minas Gerais https://orcid.org/0000-0002-0487-0500
  • Júnia Maria Geraldo Gomes Instituto Federal do Sudeste de Minas Gerais, Campus Barbacena https://orcid.org/0000-0002-9554-4419

DOI:

https://doi.org/10.34019/1982-8047.2024.v50.42991

Palavras-chave:

Frutose, Microbiota Gastrointestinal, Interações entre Hospedeiro e Microrganismos, Inflamação

Resumo

Introduction: Preclinical data suggest that at least part of the harmful effects of excessive fructose consumption are due to alterations in the intestinal microbiota, which may be associated with a number of metabolic diseases, such as diabetes mellitus, obesity, inflammatory bowel disease, metabolic syndrome, and non-alcoholic fatty liver disease. Objective: The aim of this systematic review is to evaluate the effects of fructose consumption on the human intestinal microbiota. Material and Methods: A systematic search was carried out in electronic databases: Medline, Embase, and Cochrane Library without restriction to a year of publication and language. Inclusion criteria were primary articles that evaluated the effect of fructose consumption on the human intestinal microbiota. Results: Five randomized clinical trials were included. It was observed that the composition of the human intestinal microbiota seems to be altered differently in response to fructose consumption at distinct sources and concentrations. Overall, fructose administration increased bacterial profile associated with inflammation, hepatic steatosis, butyrate production, and inhibition of microbial aerobic respiration in the ileum (Proteobacteria, Actinobacteria, Anaerostipes, and Faecalibacterium). The administration of fructose showed a negative correlation for Firmicutes and a positive correlation for Parabacteroides in relation to total cholesterol and LDL-c. However, studies had great methodological heterogeneity and presented high risk of bias. Conclusion: Fructose administration affects the composition of human intestinal microbiota. More studies are needed to reach definitive conclusions.

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Referências

Febbraio MA, Karin M. Sweet death: fructose as a metabolic toxin that targets the gut-liver axis. Cell Metab. 2021; 33(12):2316-28. doi: 10.1016/j.cmet.2021.09.004

Beisner J, Gonzalez-Granda A, Basrai M, Damms-Machado A, Bischoff SC. Fructose-induced intestinal microbiota shift following two types of short-term high-fructose dietary phases. Nutrients. 2020; 12(11):3444. doi: 10.3390/nu12113444

Stricker S, Rudloff S, Geier A, Steveling A, Roeb E, Zimmer KP. Fructose consumption-free sugars and their health effects. Dtsch Arztebl Int. 2021; 118(5):71-78. doi: 10.3238/arztebl.m2021.0010

Bonfrate L, Krawczyk M, Lembo A, Grattagliano I, Lammert F, Portincasa P. Effects of dietary education, followed by a tailored fructose-restricted diet in adults with fructose malabsorption. Eur J Gastroenterol Hepatol. 2015; 27(7):785-96. doi: 10.1097/MEG.0000000000000374

Lambertz J, Weiskirchen S, Landert S, Weiskirchen R. Fructose: a dietary sugar in crosstalk with microbiota contributing to the development and progression of non-alcoholic liver disease. Front Immunol. 2017; 8:1159. doi: 10.3389/fimmu.2017.01159

Qi X, Tester RF. Fructose, galactose and glucose: in health and disease. Clin Nutr ESPEN. 2019; 33:18-28. doi: 10.1016/j.clnesp.2019.07.004

Bian X, Chi L, Gao B, Tu P, Ru H, Lu K. The artificial sweetener acesulfame potassium affects the gut microbiome and body weight gain in CD-1 mice. PLoS One. 2017; 12(6):e0178426. doi: 10.1371/journal.pone.0178426

Song M, Li X, Zhang X, Shi H, Vos MB et al. Dietary copper-fructose interactions alter gut microbial activity in male rats. Am J Physiol Gastrointest Liver Physiol. 2018; 314(1):G119-G130. doi: 10.1152/ajpgi.00378.2016

Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes. 2012; 3(4):279-88. doi: 10.4161/gmic.19625

Harvie R, Walmsley R, Schultz M. “We are what our bacteria eat”: the role of bacteria in personalizing nutrition therapy in gastrointestinal conditions. Journal of Gastroenterology and Hepatology. 2017; 32:352-7. doi: 10.1111/jgh.13462

Do MH, Lee E, Oh MJ, Kim Y, Park HY. High-glucose or -fructose diet cause changes of the gut microbiota and metabolic disorders in mice without body weight change. Nutrients. 2018; 10(6):761. doi: 10.3390/nu10060761

Heilpern D, Abbas RN, Gladman S, Menard M, Lee BH, Szilagyi A. High fructose intake fails to induce symptomatic adaptation but may induce intestinal carriers. Gastroenterol Insights. 2010; 2:8-12. doi: 10.4081/gi.2010.e3

Gonzalez-Granda A, Beisner J, Basrai M, Damms-Machado A, Bischoff SC. Fructose-induced intestinal microbiota shift following two types of short-term high fructose dietary phases: a microbiota analysis of a crossover intervention study in healthy women. Magazine Article. 2019; 140.

Alemán JO, Henderson WA, Walker JM, Ronning A, Jones DR et al. Excess dietary fructose does not alter gut microbiota or permeability in humans: a pilot randomized controlled study. J Clin Transl Sci. 2021; 5(1):e143. doi: 10.1017/cts.2021.801

Cuff C, Lin L, Mahurkar-Joshi S, Jacobs JP, Lagishetty V et al. Randomized controlled pilot study assessing fructose tolerance thresholds during fructose reintroduction in non-constipated IBS patients successfully treated with a low FODMAP diet. Gastroenterology. 2022; 162:S937-S938. doi: 10.1016/s0016-5085(22)62223-6

Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021; 372:n71. doi: 10.1136/bmj.n71

Sterne JAC, Savović J, Page MJ, Elbers RG, Blencowe NS et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ. 2019; 366:l4898. doi: 10.1136/bmj.l4898

Astbury S, Song A, Zhou M, Nielsen B, Hoedl A, Willing BP, et al. High fructose intake during pregnancy in rats influences the maternal microbiome and gut development in the offspring. Front Genet. 2018; 9:203. doi: 10.3389/fgene.2018.00203

Han X, Feng Z, Chen Y, Zhu L, Li X et al. Effects of high-fructose corn syrup on bone health and gastrointestinal microbiota in growing male mice. Front Nutr. 2022; 9:829396. doi: 10.3389/fnut.2022.829396

Shen Y, Sun Y, Wang X, Xiao Y, Ma L et al. Liver transcriptome and gut microbiome analysis reveals the effects of high fructose corn syrup in mice. Front Nutr. 2022; 9:921758. doi: 10.3389/fnut.2022.921758

Zoetendal EG, Rajilić-Stojanović M, De Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut. 2008; 57:1605-15. doi: 10.1136/gut.2007.133603

Stojanov S, Berlec A, Štrukelj B. The Influence of probiotics on the Firmicutes/Bacteroidetes ratio in the treatment of obesity and inflammatory bowel disease. Microorganisms. 2020;8(11):1715. doi: 10.3390/microorganisms8111715

Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S et al. The firmicutes/bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients. 2020; 12(5):1474. doi: 10.3390/nu12051474

Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015; 26:26050. doi: 10.3402/mehd.v26.26050

Nettleton JE, Reimer RA, Shearer J. Reshaping the gut microbiota: impact of low calorie sweeteners and the link to insulin resistance? Physiol Behav. 2016; 164:488-93. doi: 10.1016/j.physbeh.2016.04.029

Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015; 33:496-503. doi: 10.1016/j.tibtech.2015.06.011

Tan R, Dong H, Chen Z, Jin M, Yin J et al. Intestinal microbiota mediates high-fructose and high-fat diets to induce chronic intestinal inflammation. Front Cell Infect Microbiol. 2021; 11:654074. doi: 10.3389/fcimb.2021.654074

Ahn IS, Lang JM, Olson CA, Diamante G, Zhang G et al. Host genetic background and gut microbiota contribute to differential metabolic responses to fructose consumption in mice. J Nutr. 2020; 150(10):2716-28. doi: 10.1093/jn/nxaa239

Levine UY, Looft T, Allen HK, Stanton TB. Butyrate-producing bacteria, including mucin degraders, from the swine intestinal tract. Appl Environ Microbiol. 2013; 79:3879-81. doi:10.1128/AEM.00589-13

Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009; 139(9):1619-25. doi: 10.3945/jn.109.104638

Guo P, Wang H, Ji L, Song P, Ma X. Impacts of fructose on intestinal barrier function, inflammation and microbiota in a piglet model. Nutrients. 2021; 13(10):3515. doi: 10.3390/nu13103515

Luccia B, Crescenzo R, Mazzoli A, Cigliano L, Venditti P et al. Rescue of fructose-induced metabolic syndrome by antibiotics or faecal transplantation in a rat model of obesity. PLoS One 2015; 10(8):e0134893. doi: 10.1371/journal.pone.0134893

Hiippala K, Kainulainen V, Suutarinen M, Heini T, Bowers JR et al. Isolation of anti-inflammatory and epithelium reinforcing Bacteroides and Parabacteroides Spp. from a healthy fecal donor. Nutrients. 2020; 12(4):935. doi: 10.3390/nu12040935

Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH et al. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486:207-14. doi: 10.1038/nature11234

Simpson CA, Diaz-Arteche C, Eliby D, Schwartz OS, Simmons JG, Cowan CSM. The gut microbiota in anxiety and depression: a systematic review. Clin Psychol Rev. 2021; 83:101943. doi: 10.1016/j.cpr.2020.101943

Horne RG, Yu Y, Zhang R, Abdalqadir N, Rossi L et al. High fat-high fructose diet-induced changes in the gut microbiota associated with dyslipidemia in Syrian hamsters. Nutrients. 2020; 12:1-20. doi: 10.3390/nu12113557

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Publicado

2024-05-14

Como Citar

1.
Silva LL da, Lopes RR, Guilarducci MJ, Coelho OGL, Cândido FG, Guimarães NS, Gomes JMG. Effect of fructose on the intestinal microbiota: a systematic review of randomized clinical trials: Effect of fructose on the intestinal microbiota. HU Rev [Internet]. 14º de maio de 2024 [citado 21º de novembro de 2024];50:1-11. Disponível em: https://periodicos.ufjf.br/index.php/hurevista/article/view/42991

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