Food Groups' Effects on Gut Microbiota and T2DM: Comparison
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Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Mihai Covașă.

Nutrition is one of the most influential environmental factors in both taxonomical shifts in gut microbiota as well as in the development of type 2 diabetes mellitus (T2DM). Considering the effects of macro- and micronutrients on gut microbiota and T2DM, food groups and dietary patterns are major determinants of the gut microbiota–metabolic disorder axis. 

  • gut bacteria
  • macronutrients
  • micronutrients
  • food groups
  • insulin resistance

1. Cereals and Cereal Products

Cereals are composed of whole grains, wheat, oats, rye, and barley, which have been shown to have beneficial effects on metabolic health and gut microbiota [261,262][1][2]. Over the years, an increasing number of studies have elucidated the effects of cereal products on T2DM, largely showing that the components within cereals decrease the risk of developing the disease and related sequelae [263,264,265,266][3][4][5][6]. Dietary recommendations for cereals in metabolic disease include increasing the intake of cereals with whole grains and limiting the intake of refined grains or cereals with processed sugars and artificial sweeteners [267][7]. Both whole wheat intake and the intake of barley, oat, and rye have been associated with improved blood glucose levels [268,269][8][9] and increased insulin sensitivity [270][10]. It should be noted that the beneficial effects of cereals appear when the intake is high, at least 4 g of β-glucans daily [269,271][9][11]. For example, a supplement of up to 50 g of whole grains per day was associated with a 25% decrease in the risk of T2DM [272][12]. Similarly, the consumption of two servings of whole grains per day was associated with a 21% decrease in the risk of T2DM [273][13], while a refined grain intake of 200–400 g per day was associated with a 6–14% increase in the risk of T2DM [272][12]. The composition of the whole grains such as magnesium, phytochemicals, isoflavins, and lignins was also associated with beneficial effects in T2DM [274][14]. Adding cereal fiber to meals reduced post-prandial insulin release, indicating the important roles of fiber in improving insulin sensitivity [266][6]. Taken together, these data provide strong evidence for cereal products in reducing the risk of T2DM development.
Further, cereal-based dietary approaches are shown to affect multiple metabolic parameters in individuals already diagnosed with T2DM, some of which may be related to changes in gut microbiota. For example, after a 3-month adherence to high dietary fiber-based cereals, there were favorable trends in lipids, HgbA1, body mass index (BMI), adipose distribution, and fasting C-peptide levels [263][3]. Similarly, high fiber rye, a component of healthy cereal, is shown to improve similar parameters when compared to refined wheats [264][4]. In addition to improving metabolic parameters, the high fiber rye diet produced important changes in gut microbiota, including elevated SCFA-producing Agathobacter and decreased Ruminococcus torques, with associated increases in plasma butyrate concentrations [264][4]. When compared to refined grains, the whole grain has immunomodulatory effects that were associated with microbial composition alterations [275][15]. For example, the introduction of wheat grains after a 2-week Western-style diet improved SCFAs, increased SCFA-producing Lachnospira, and reduced the pro-inflammatory Enterobacteriaceae family which correlated with positive changes in effector memory T-cell activity and acute innate immune response [275][15]. Other immunomodulatory effects of cereals have also been described in the literature, with the reduced activity of pro-inflammatory cytokines, TNF-α and IL-6, being observed after consumption [276,277][16][17]. In rodent studies, the effects of wheat also improved GPR41/43 receptor expression and enhanced GLP-1 secretion with concomitant increases in SCFA-producing bacteria, providing further insights into the multitude of effects that cereals have on metabolic disease [278][18].
In addition to the changes described above, it seems that a general increase in Bifidobacterium and Lactobacillus spp. is common after cereal consumption, an effect consistent with other recent studies [265][5]. Previous studies have also shown that diets rich in whole wheat compared to refined wheats exhibit an abundance of Bifidobacterium and relative decreases in Bacteroides after a 12-week intervention [279][19]. The type of cereal consumed is also important in determining microbiota shifts. For example, an increase in the abundance of Bifidobacterium and Lactobacillus was seen in the gut microbiota of people who consumed whole grain cereals for breakfast, compared to the microbiota of people who consumed cereals based on wheat bran [280][20]. A corn-based cereal diet increased the abundance of fecal Bifidobacteirum after a 3-week intervention, as compared to a refined-corn-based cereal [281][21]. These changes in the composition of the gut microbiota could be observed even at a low intake of whole corn (29.6% of the recommended total of 48 g [281][21]). However, the opposite is also true, with the sugar additives and processing seen in refined cereals having been shown to have negative effects on both gut microbial composition and related metabolites [282][22]. Therefore, it is evident that eating cereals with naturally occurring fibers can be beneficial in preventing or treating metabolic derangements in T2DM, while avoiding refined cereals and cereals with additives is also important.

2. Fruits and Vegetables

In general, some of the healthiest foods are considered vegetables and fruits, due to their content of dietary fiber, vitamins, minerals, and flavonoids [283][23]. Multiple studies have demonstrated the inverse associations between the consumption of green leafy vegetables and the risk of developing T2DM [67[24][25][26],284,285], the consumption of fruits and T2DM [286][27], as well as the intake of mixed fruits and vegetables and T2DM [287][28]. Specifically, an intake of 0.2 servings per day of green leafy vegetables reduced the risk for type 2 diabetes by 13% [284][25], with similar findings in another meta-analysis showing a risk reduction of 14% [285][26]. Changes in microbial shifts after the consumption of fruits and vegetables have also been described with study findings showing a decreased abundance of the Lachnospiraceae family, including Ruminococcus, and increased concentrations of Faecalibacterium and Lactobacillus [288][29]. Further metagenomic sequencing studies combining two large human cohorts have shown changes that include an increased abundance of Faecalibacterium prausnitzii, Akkermansia muciniphila, Ruminococcaceae, Clostridiales, and Acidaminococcus and a decrease in the abundance of Fusobacterium [289][30].
Vegetables and fruits are sources of antioxidants that have been associated with augmenting glucose metabolism, by improving oxidative stress [290][31], particularly given their high content of flavonoids and polyphenols [291][32]. Interestingly, flavonoids are shown to modulate gut microbiota-related metabolic processes, particularly through the suppression of lipogenesis and the upregulation of lipolysis, via the FXR pathway in bile acid metabolism [292][33]. These effects of flavonoids were corelated with increased Akkermansia and reductions in Lachnoclostridium, Desulfovibrio, Colidextribacter, and Blautia, all of which are strongly associated with metabolic parameters [292][33]. Further, flavonoid-based dietary interventions alleviated inflammation as measured through LPS/TLR-4, TNF-α, IL-6, and IL-10, while also improving insulin resistance, HgbA1c, and oral glucose tolerance [293][34]. Interestingly, GLP-1 release was also enhanced following flavonoid introduction. The beneficial effects of fruit and vegetable flavonoids also are shown by the improvement of intestinal barrier integrity, as well as promoting islet cell proliferation and the suppression of islet cell apoptosis [294][35]. Flavonoids also modulate glucose metabolism by the upregulation of the IRS/AKT signaling pathway to increase GLUT4 translocation and the synthesis of glycogen, while concomitantly improving the Firmicutes-to-Bacteroidetes ratio [295][36]. As such, flavonoids, a major component of fruits and vegetables, exert a multitude of metabolic benefits at the intersection between gut microbiota and glucose homeostasis.
In addition to flavonoids, fruits and vegetables are comprised of other beneficial bioactive phytochemical-based nutrients, including vitamin C and carotenoids, which contribute to insulin sensitivity [296,297][37][38]. Also, green leafy vegetables contain magnesium which is inversely associated with an increased risk for type 2 diabetes [298][39]. The association between fruit and vegetable intake and a reduced risk of type 2 diabetes may be due to their dietary fiber content [299][40] and the subsequent effects of weight loss in overweight individuals [300][41]. Fruit and vegetable juices, depending on their content, may have differing outcomes on both gut microbiota and T2DM [301,302,303,304][42][43][44][45]. Fruit juices that are altered by added sugar or artificial sweeteners pose harmful risks to the gut metabolic profile [301][42]. For example, the artificial sweetening of fruit beverages results in modest changes in gut microbiota, particularly in the ratio of Firmicutes to Bacteroidetes [301][42]. However, the introduction of natural fruit or vegetable extracts or juice generally has favorable effects [302,303,304][43][44][45]. In a prediabetic rodent model, blueberry juice improved the microbiota composition as well as metabolic parameters including insulin signaling, inflammation, ketogenesis, and fatty acid oxidation [303][44]. Similarly, pomegranate juice can reduce the post-prandial glycemic response after eating a high-carbohydrate meal, primarily breads [305][46]. Overall, fruits and vegetables are an important food group in maintaining a healthy microbiota profile because diets high in fruits, vegetables, legumes, and whole grains are accompanied by optimal body weight, reduced inflammation, and lower insulin resistance.

3. Milk and Dairy Products

Dairy products are rich in protein, B vitamins, and minerals, such as calcium, magnesium, potassium, phosphorus, and zinc, all of which have important effects on gut microbiota composition [306][47]. Dairy proteins, especially whey proteins, are associated with improved insulin sensitivity and a reduced risk of type 2 diabetes [307][48]. Interestingly, high quantities of dairy consumption (two servings per day) in adolescence were associated with a 38% decreased risk of developing T2DM in middle-aged women [308][49]. Further, an inverse correlation was observed between the intake of skimmed or semi-skimmed dairy products and the risk of type 2 diabetes [309][50]. This decreased risk was seen with 200 g of skimmed dairy product intake, with an improvement in risk up to 6% with every additional 200 g, up to a daily total of 600 g [272][12]. Another study has shown that one serving of dairy per day has beneficial effects on T2DM risk reduction of 9% in men and 4% in women [310,311][51][52]. Dairy consumption produces specific compositional changes in gut microbiota. For example, the introduction of dairy products or intake of yogurt for three weeks led to decreased Bacteroides fragilis [306][47] and an abundant growth of Lactobacillus and Bifidobacterium [312][53]. Similarly, the consumption of kefir, a yogurt-based drink, over the next 4 weeks increased the abundance of Lactobacillus [313[54][55],314], with associated elevated levels in fecal SCFAs [314][55]. Interestingly, in studies on murine models, yogurt-derived Lactobacillus plantarum has been shown to ameliorate the reduction in pancreatic β-cell mass with notable improvements in insulin resistance [315][56]. Taken together, these studies show that dairy consumption prompts significant changes in the composition of gut microbiota that are beneficial to the host in mitigating the deleterious effects of T2DM.

4. Meat and Meat Products

The recommendations for patients with type 2 diabetes regarding the intake of meat and meat products are similar to the recommendations for healthy individuals, i.e., one portion/day or the equivalent of 100–150 g of lean meat per day [316][57]. Lean meat and meat products are sources of protein with high biological value, but they are also important sources of iron and vitamin B12 [317][58]. However, red meats are shown to exert negative effects in both contributing to T2DM development and worsening the condition [316][57]. Several positive associations have been reported between the intake of processed red meats and increased blood glucose concentrations, insulin levels, and risk for obesity [318,319][59][60]. Moreover, the risk for type 2 diabetes was associated with the intake of red meat up to 100 g per day [272][12] but also with the intake of up to 50 g per day of processed meat products [272,320][12][61]. These effects have been attributed to the content of heterocyclic amines and nitrates affecting glucose metabolism [321,322][62][63]. These metabolites contribute to insulin resistance through adverse effects on pancreatic β-cell function and insulin-like growth factor (IGF-1) [323][64]. Further, these inorganic nitrates, present in processed meats, promote DNA damage through conversion to cytotoxic agents such as peroxy-nitrite as well as reactive oxygen species, which increase pro-inflammatory cytokine production and hamper glucose homeostasis [324][65]. Red meats also enhance the presence of dietary advanced glycosylated end products (dAGEs), the result of the Maillard reaction that occurs between amino acids and reducing sugars [325][66]. These dAGE products are shown to increase insulin resistance, while a restricted intake of dietary glycoxidation products improved insulin sensitivity in diabetic mice [326][67]. Additionally, it has been shown that hyperglycemia further enhances the glycation process, thus worsening the complications of uncontrolled diabetes. Therefore, red meats are a source of inorganic nitrates and substrates for the generation of dAGEs, which may contribute to the development of insulin resistance and complicate pre-existing diabetes.
Red meat may also be detrimental to gut microbial composition. It has been shown that red meat decreases Lactobacillus, Paralactobacillus, and Prevotella, while also decreasing SCFAs in animal models [327][68]. Further, the administration of beef, a red meat derivate, in mouse and rat study models led to an increase in the amount of Clostridium and Blautia and a decrease in the amount of Bifidobacterium and Akkermansia [328][69]. The addition of butyrate containing starch was shown to reverse the negative effects of red meat diet adherence through increased abundances of Clostridium coccoides, Clostridium leptum, Lactobacillus spp., Parabacteroides distasonis, and Ruminococcus bromii, but it also showed a decrease in the amount of Ruminococcus torques, Ruminococcus gnavus, and Escherichia coli [329][70]. However, the effects on gut microbial composition are dependent on the type of meat and proteins they contain [330][71]. For example, a study evaluating the gut microbiota of individuals consuming chicken meat is characterized by the highest proportion of Prevotella 9 (22.45%), followed by Dialister, Faecalibacterium, Megamonas, Prevotella, Roseburia, Alloprevotella, Ruminococcaceae, Eubacterium, and Succinivibrio, while the gut microbiota of individuals consuming pork is characterized by the highest proportion of Bacteroides (17.3%), followed by Faecalibacterium, Roseburia, Dialister, Ruminococcus, Blautia, Megamonas, Agathobacter, Subdoligranulum, and Eubacterium [331][72]. On the other hand, pork intake decreased the amount of Blautia, Bifidobacterium, and Alistipes and increased the amount of Akkermansia muciniphila and Ruminococcaceae [332][73]. Collectively, the intake of pork meat induced low-grade inflammation and induced oxidative stress and the upregulation of lipid metabolism genes such as PPAR-α and PPAR-γ [332][73]. Further, an increase in the abundance of Lactobacillus and a decrease in SCFA levels and SCFA-producing bacterial species such as Fusobacterium, Bacteroides, and Prevotella have been reported in laboratory mice fed beef, pork, or fish proteins, compared to mice that were given protein from sources other than meat, such as soy or casein [333][74]. Similarly, laboratory rats fed chicken meat had the highest abundance of Lactobacillus, compared to laboratory rats fed soy, which had the highest abundance of Ruminococcus and the lowest abundance of Lactobacillus [334][75]. The administration of beef in mouse and rat study models led to an increase in the amount of Clostridium and Blautia and a decrease in the amount of Bifidobacterium and Akkermansia [328][69]. Collectively, these changes indicate that meats derived from chicken have more favorable effects on gut microbiota and insulin resistance as compared to pork and red meats.

5. Nuts, Oils, and Oilseeds

Tree nuts have been shown to exert favorable effects on gut microbiota and metabolic parameters [335,336][76][77]. For example, replacing starchy foods with peanuts or almonds in patients with type 2 diabetes led to improvements in blood glucose, HgbA1c, and inflammatory markers [335][76]. In addition, the daily intake of raw or roasted almonds for 4 weeks promoted Bifidobacterium spp. and Lactobacillus spp. and inhibited the growth of Enterococcus spp. Interestingly, the administration of raw almonds had a greater Bifidobacteria-promoting effect than roasted almonds, with both roasted and raw almonds having a potential prebiotic effect, including regulating gut bacteria and improving metabolic activities [336][77]. Similarly, nut intake promotes an increase in the abundance of Faecalibacterium, Clostridium, Dialister, and Roseburia and a decrease in the abundance of Ruminococcus, Dorea, Oscillopira, and Bifidobacterium [337][78]. Pistachio consumption led to an increase in the abundance of potentially beneficial, butyrate-producing bacteria [338][79], while eating whole, roasted, or chopped almonds is associated with an increase in the abundance of Lachnospira and Roseburia [339][80]. These alterations in gut microbiota were associated with a concomitant decrease in pro-inflammatory secondary bile acid production and LDL cholesterol, two interrelated parameters in the development of hyperglycemia and insulin resistance [337][78]. Also, a diet enriched with 20% peanut protein was effective in increasing the amount of Bifidobacterium and reducing the amount of Enterobacteria and Clostridium perfringens in rats [340][81].
Oilseeds are important sources of polyunsaturated and monounsaturated fatty acids [341,342][82][83] and their consumption has been associated with a decreased risk for type 2 diabetes [343][84]. For example, dietary flaxseed oil, given its rich composition of omega-3, was associated with decreased Firmicutes and pro-inflammatory markers such as IL-1β, TNF-α, and IL-6 and increased Bacteroidetes and Alistipes that negatively correlate with LPS production [344][85]. Further, the direct markers of hyperglycemia showed significant improvement, particularly in fasting blood glucose and glycated hemoglobin. Interestingly, superoxide dismutase (SOD) activity was increased as well, with previous studies showing that SOD activity can improve diabetes-induced mitochondrial electron transport dysfunction and diabetes complications such as retinopathy [345][86]. Meta-analyses of human studies confirm these beneficial anti-inflammatory effects of oilseeds, with decreased CRP and IL-6 activity leading to improved endothelial function and metabolic activity [346][87]. Oilseeds cause significant changes in the gut composition profile, such as increased Lactobacillus spp. and SCFAs, with reduced production of harmful metabolites such as TMAO [347][88]. As such, oilseeds and nuts serve as healthy food sources that are intricate components of the Mediterranean diet and modulate important metabolic processes associated with T2DM. A summary of food groups and the mechanisms by which they impact T2DM is presented in Table 1.
Table 1.
Food groups and resulting effects on T2DM.
Food Group Study Period Outcome Measured Results/Implications Subject Type Reference
Cereals and Cereal Products Meta-Analysis Diabetes risk Two servings of whole grains decreased the risk of developing T2DM by 21%

Refined grain intake increased the risk of developing T2DM by 6–14%		 Humans [272][12]
3 months Metabolic Parameters Improvements in lipid quality, HgbA1c, BMI, adipose distribution, and fasting C-peptide levels Humans [263][3]
6 weeks Gut Microbiota and Inflammatory Markers Whole grains improved effector memory T-cell activity and acute innate immune response

Increased quantity of SCFAs and SCFA-producing genera including Lachnospira

Decreased relative abundances of pro-inflammatory bacterial family Enterobacteriaceae		 Humans [275][15]
9 weeks Gut Microbiota and Gut Hormones Increased SCFA-producing species

Increased GLP-1 secretion		 Mice [278][18]
12 weeks Gut Microbiota Increased Bifidobacterium and decreased Bacteroides Humans [279][19]
Fruits and Vegetables Meta-Analysis Diabetes risk Intake of 0.2 servings per day of green leafy vegetables reduced the risk for type 2 diabetes by 13% Humans [284][25]
  Gut Microbiota and Metabolic Parameters Increased Akkermansia

Reduced Lachnoclostridium, Desulfovibrio, Colidextribacter, and Blautia

Upregulation of lipolysis through the FXR, bile acid metabolism pathway		 Mice [292][33]
  Inflammatory Markers and Metabolic Parameters Reduced LPS/TLR-4 activity, TNF-α, and IL-6

Improved IL-10

Improved insulin resistance and HgbA1c

Increased GLP-1 secretion		 Mice [293][34]
  Glucose Metabolism and Gut Microbiota Upregulation of the IRS/AKT signaling pathway to increase GLUT4 translocation and synthesis of glycogen

Improved Firmicutes-to-Bacteroidetes ratio		 Mice [295][36]
Milk and Dairy Products   Diabetes risk One serving of dairy per day has beneficial effects on T2DM risk reduction of 9% in men and 4% in women Humans [310,311][51][52]
3 weeks Gut Microbiota Increased Bifidobacterium and Lactobacillus spp. Increased serum IgA

Decreased Bacteroides fragilis		 Humans [306,312][47][53]
  Gut Microbiota and Pancreatic Function Lactobacillus isolated from yogurt increased SCFA levels and SCFA receptors, GPR41/43

Increased SCFA-producing genera

Inhibited reduction of β-cell mass		 Mice [315][56]
Meat and Meat Products Meta-Analysis Diabetes Risk Risk for T2DM is increased with intake of 100 g of red meat per day

Risk for T2DM is increased with intake of 50 g of processed meat per day		 Humans [272,320][12][61]
  Gut Microbiota Red meat decreases Lactobacillus, Paralactobacillus, and Prevotella, while also decreasing SCFAs Dogs [327][68]
1–4 weeks Gut Microbiota Increased Clostridium and Blautia

Decreased Bifidobacterium and Akkermansia		 Mice [328][69]
3 months Gut Microbiota, Inflammatory and Metabolic parameters Pork meat decreased Blautia, Bifidobacterium, and Alistipes

Induced low-grade inflammation

Induced oxidative stress

Upregulated lipid metabolism genes including PPAR-α and PPAR-γ		 Mice [332][73]
Nuts, Oils and Oilseeds 3 months Parameters of T2DM Peanuts or almonds in patients with T2DM improved blood glucose, HgbA1c, and inflammatory markers like IL-6 expression Humans [335][76]
6 weeks Gut Microbiota and Metabolic Parameters Nut intake increased the abundance of Faecalibacterium, Clostridium, Dialister, and Roseburia and decreased the abundance of Ruminococcus, Dorea, Oscillopira, and Bifidobacterium

Decreased pro-inflammatory bile acid production and LDL cholesterol		 Humans [337][78]
5 weeks Gut Microbiota and Inflammatory Parameters Dietary flaxseed oil decreased severity of T2DM, improved the Firmicutes-to-Bacteroidetes ratio, while increasing Alistipes

Reduction in IL-1β, TNF-α, IL-6, and LPS production		 Rats [344][85]
Abbreviations: T2DM, type 2 diabetes mellitus, HgbA1c, Hemoglobin A1c; BMI, body mass index; SCFA, short-chain fatty acid; GLP-1, glucagon-like peptide 1; FXR, Farsenoid X Receptor; LPS, lipopolysaccharides; TLR-4, Toll-like receptor 4; TNF-α, Tumor Necrosis Factor alpha; IL, interleukin; GLUT4, Glucose Transporter 4; IRS, insulin receptor substrate; IgA, Immunoglobulin A; PPAR, peroxisome proliferator-activated receptor; LDL, low density lipoprotein.

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