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A diet high in polyphenols is associated with a diversified gut microbiome. Tea is the second most consumed beverage in the world, after water. The health benefits of tea might be attributed to the presence of polyphenol compounds such as flavonoids (e.g., catechins and epicatechins), theaflavins, and tannins.
Studies on the relationship between gut microbiota and health have garnered much interest in recent years. The term “gut microbiota” is defined as the microbial ecosystem or community that resides within the human intestinal tract [1]. The gut ecosystem comprises microorganisms, mainly bacteria, and a small number of viruses, protozoa, and eukaryotic organisms such as fungi that are distributed throughout the gastrointestinal tract [2]. As stated by Nahoum et al., 2016, diversified microbiota are a crucial indicator of good health and well-being [3].
Gut microbiota play an important role in human health, and they are considered a “forgotten organ” and “super-organism” that maintains intestinal epithelium integrity [4][5][6]. The human gut contains an estimated 100 trillion microorganisms [7]; in addition, over 1000 different species of microbes colonize the human gut [8]. The dominant groups of bacteria phyla in the gut are Firmicutes, Bacteroidetes, Actinobacteria, and Proteobacteria [5][9]. Fusobacteria, Cyanobacteria, and Verrucomicrobia phyla are usually less well-represented [10].
Gut microbiota may also play a role in how drugs are metabolized in our body [11]. These commensal bacteria play important roles as key regulators of digestion, involving the extraction, synthesis, and absorption of many nutrients and metabolites, including bile acids, lipids, amino acids, vitamins, and short-chain fatty acids (SCFAs) [11]. The gut microbiota also have a crucial immune function against pathogenic bacteria colonization through many competition processes [12]. They inhibit pathogenic bacteria growth by consuming available nutrients, by pH modification, and by producing bacteriocins, which are a type of antimicrobial peptide secretion, affecting cell signaling pathways [13].
Gut microbiota imbalance (dysbiosis) is associated with the development of a series of diseases [14][15][16][17][18][19]. These diseases include diabetes, obesity, cardiovascular and liver diseases, cancers, multiple sclerosis, and neurodegenerative diseases [14][15][16][17][18][19]. Hence, the gut microbiota has been proposed as a promising therapeutic target for these diseases [20].
Research is still ongoing into the factors that modulate gut microbiota profiles, and diet could play a role [21][22][23]. However, studies suggest that diet only accounts for a low percentage of microbiome variation after adjusting for other contributing co-variates, such as genetics, age, ethnicity, geographic origins, body mass index (BMI), lifestyle, medication, and environmental factors [12][24].
Dietary intake varies from one individual to another, and there is a complex interaction between dietary intake and the gut microbiome [25]. The so-called “Western diet” is characterized as high-calorie and is associated with metabolic syndrome i.e., abnormal lipid profiles, elevated blood pressure, and impaired fasting glucose [2]. Evidence suggests that the so-called “Mediterranean diet,” which is high in the polyunsaturated fatty acids and polyphenols (from coffee, tea, or grapes), is associated with an increased gut microbiota diversity [26].
Tea (Camellia sinensis sp.) is one of the most widely consumed nonalcoholic beverages in the world [27]. There are different types of tea: green tea, oolong tea, black tea, Pu-erh tea, and dark tea. Each tea is produced differently using different fermentation processes. Tea is rich in polyphenols, possesses antioxidant properties, and offers multiple health benefits [28]. Flavonoids such as flavanols (catechins, gallocatechins, and epicatechins), flavonols (kaempferol and quercetin), and phenolic acids are the three major classes of polyphenols in tea [29].
Polyphenols are absorbed in the small intestine and may reach the colon [30]. These polyphenols may modulate the gut microbiota composition, and the gut microbiota may catabolize polyphenols into metabolites such as phenolic acids [31]. The metabolites are absorbed more efficiently compared with the parent polyphenols compounds. These metabolites might be further conjugated as O-methylated, sulphated, and glucuronidated in the liver before being excreted [32]. In vitro studies have shown that the polyphenols in tea are biotransformed to active metabolites by the gut microbiota through enzymatic activities and the increased bioavailability of polyphenols [33][34]. Polyphenols such as flavanols, including catechins, modulate the composition of the gut microbial community, mostly through the inhibition of pathogenic bacteria and the stimulation of beneficial bacteria species such as Bacteroides galacturonicus, Lactobacillus sp., Enterococcus caccae, Bifidobacterium catenulatum, Ruminococcus gauvreauii, and Escherichia coli [34][35]. Previous studies have shown that the synergistic effect of tea polyphenols and gut microbiota has subsequently influenced the host biochemical processes, establishing a system of mutual interaction and inter-dependency [36]. The presence of polyphenols could increase the host immune system and metabolic responses through the modulation of gut microbiota [36].
Evidence suggests that polyphenols may also modulate the gut microbiota in what is known as a prebiotic-like effect [20]. However, Ivey et al., 2019 reported that dietary flavanols produce a vast potential complexity of interactions when combined with the phylogenetic and functional diversity of the human gut microbiota [37]. This complexity is linked to the capacity of flavanols to promote beneficial bacteria or suppress pathogenic bacteria [38][39][40].
To the best of our knowledge, the effects of tea on gut microbiota were studied in cells (in vitro) and in mechanistic studies on animal models (in vivo) [41][42][43][44]. However, studies using cell lines or animal models to study gut microbiota have their own limitations. Casotta et al., 2020 showed that findings from animal models and cell cultures do not represent and are not translatable to humans [45]. The main limitation of in vivo studies is due to the host’s tolerance of microbial infections, which varies greatly across different species [46]. In vitro colonic fermentation models are cheaper, are more reproducible, and can be conducted in a shorter time compared with in vivo studies [47]. Pham et al., 2018 showed several limitations of cell studies, including the absence of human or animal cells and low pH, which reduces microbial activity [47].
Furthermore, it remains a challenge to translate findings obtained from cells and animal models to humans [48].
Oolong tea is also known as “semi-fermented” or “partially oxidized” tea. Catechins in oolong tea are oxidized into theaflavins, thearubigins, and theabrownins during partial fermentation, hence producing a slightly darker color than green tea [49]. Oolong tea was supplemented in two murine studies. Studies by Cheng et al. investigated the effects of oolong tea extracts in mice induced with human flora and given a high-fat diet [41][43]. Tea increased gut microbiota diversity after four to eight weeks of tea supplementation [41][43].
Black tea is a “fully fermented” tea and is characterized by a darker color and astringent taste due to a higher concentration of theaflavins, thearubigins, and theabrownins compared to other types of tea [49][50]. Polyphenol oxidase is a heat-labile enzyme present in black tea [50]. The activity of this enzyme is reduced by steam-heating during the fermentation of black tea, consequently reducing its antioxidant properties compared to green tea [50][51]. Human study demonstrated the effect of black tea on the gut microbiota. Black tea infusion was given to hypocholesterolemic volunteers in a double-blind, randomized crossover feeding trial for six weeks [52]. However, no significant changes were observed in the gut microbiota [52].
Pu-erh tea is a traditional Chinese tea. There are two types of Pu-erh tea, namely raw (unfermented) and ripe (after microbial fermentation) [53]. One human trial and four murine studies were done on Pu-erh tea. Huang et al., 2019 investigated the cholesterol-lowering activity of ripe Pu-erh tea in humans and animals [54]. In this study, male human subjects received 600 mL of tea infusion (approximately three cups) daily for four weeks, while the mice were provided with a daily dose of 450 mg of tea extracts per kg body weight in a high-fat diet for 26 weeks [54]. Hyper-cholesterol-enriching bacterial genera were significantly reduced compared to high-fat diet numbers in human and animal studies [54]. Three murine studies demonstrated the effects of raw and ripe Pu-erh tea in restoring the altered gut microbiota caused by a high-fat diet. Lu et al., 2019 and Xia et al., 2019 showed that Pu-erh tea at a dose between 0.1 to 0.4 g of tea extracts for five to eight weeks effectively increased gut microbiota diversity [55][56]. Gao et al., 2017 found that ripe Pu-erh tea extract and Pu-erh tea polyphenol components increased gut microbiota diversity in the high-fat diet group [57].
Fuzhuan brick tea is a type of dark tea known as fungal fermented tea [58]. The polyphenol content in Fuzhuan tea is lower compared to green tea, due to the process of microbial fermentation occurring in dark tea production [59][60]. A series of reactions, including degradation, oxidation, condensation, structural modification, methylation, and glycosylation, are catalyzed by microbial exo-enzymes or occur as a result of microbial metabolism, leading to the development of dark tea quality [61][62][63]. Studies by Chen et al., 2018 and Foster et al., 2016 incorporated two different dosages of Fuzhuan tea extracts in mice receiving a high-fat diet [42][64]. Daily supplementation of Fuzhuan tea extracts at doses of between 200 to 400 mg for eight weeks was able to reverse the altered dominant phyla bacteria in the gut and also increase the levels of Lactobacillus and Bifidobacteriaceae [42][64].
Two murine studies compared the modulating effects of multiple teas on the gut microbiota that were exposed to a high-fat diet [65][66]. Henning et al., 2017 showed that the supplementation of 0.5 g of decaffeinated green and black tea extract daily for four weeks increased the level of phylum Bacteroidetes while suppressing phyla Firmicutes and Actinobacteria [65]. The ratio of Firmicutes to Bacteroidetes was also reduced [65]. Liu et al., 2016 monitored the effects after feeding 100 mL of either green, oolong, or black tea liquid daily for 13 weeks, and they noted a reversed trend in the growth of bacteria, compared to those with only a high-fat diet [66].