Microbiome Changes after Type 2 Diabetes Treatment: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Eligibility Criteria
2.2. Search
2.3. Study Selection
2.4. Data Extraction
2.5. Risk of Bias and Quality
3. Results
3.1. Oral Anti-Diabetic Treatment
3.2. Surgery as Anti-Diabetic Treatment
3.3. Probiotics
3.4. Prebiotics
3.5. Synbiotics
3.6. Changes in Composition of Intestinal Microbiome
3.6.1. Phylum Level
3.6.2. Genus Level
3.6.3. Changes in Diversity
3.7. The Overall Significant Changes after All Types of Treatment
4. Discussion
4.1. Changes in Composition of Intestinal Microbiome
4.2. Changes in Diversity
4.3. Oral Anti-Diabetic Treatment
4.4. Surgery as Anti-Diabetic Treatment
4.5. Probiotics, Prebiotics, and Synbiotics
5. Limitations
6. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Source | No. of Subjects (Male) | Intervention Group | Control Group | Follow-Up | R | D | Mi | Me | S | O |
---|---|---|---|---|---|---|---|---|---|---|
Su et al. [16] | 95 (46) | T2D treatment with acarbose | T2D treatment without acarbose | 4 weeks | ||||||
Gu et al. [17] | 94 (58) | Acarbose | Glipizide | 12 weeks | ||||||
Tong et al. [18] | 200 (100) | Metformin with prebiotics (Chinese herbal formula) | Metformin without prebiotics | 12 weeks | ||||||
Wu et al. [19] | 40 (17) | Metformin | Placebo | 8 and 16 weeks | ||||||
Cortez et al. [20] | 21 (unspec.) | Surgery (DJB) | Optimal T2D treatment (metformin 2 g/day, gliclazide 30 mg) | 24 and 48 weeks | ||||||
Murphy et al. [21] | 14 (8) | Surgery (SG) | Surgery (RYGB) | 48 weeks | ||||||
Lee et al. [22] | 12 (0) | 3-arm study: surgery (AGB or RYGB) | Medical weight loss | Variable | ||||||
Mobini et al. [23] | 53 (35) | Probiotics (L. reuteri) | Placebo | 12 weeks | ||||||
Firouzi et al. [24] | 129 (67) | Probiotics (multi-strain) | Placebo | 6 and 12 weeks | ||||||
Sato et al. [25] | 68 (49) | Probiotics (L. casei) | Placebo | 8 and 16 weeks | ||||||
Hsieh et al. [26] | 68 (38) | 3-arm study: probiotics (L. reuteri ADR-1 or ADR-3) | Placebo | 12, 24, and 36 weeks | ||||||
Medina-Vera et al. [27] | 53 (19) | Prebiotics (non-specific functional foods) | Placebo | 12 weeks | ||||||
Pedersen et al. [28] | 29 (29) | Prebiotics (GOS) | Placebo | 12 weeks | ||||||
Shin et al. [29] | 12 (9) | Prebiotics (Scutellaria baicalensis) | Placebo | 8 weeks | ||||||
Balfego et al. [30] | 32 (15) | Standard T2D diet with prebiotics (non-specific functional foods) | Standard T2D diet without prebiotics | 24 weeks | ||||||
Zhang et al. [31] | 381 (245) | 4-arm study: probiotics (multi-strain) and/or prebiotics (berberine) | Placebo | 13 weeks |
Applied Intervention | RCT | Changes in Microbiome Composition | Changes in Microbiome Diversity | Anthropometric or Metabolic Improvements | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Phylum | Genera | Species | Alpha Diversity | Beta Diversity | A | G | I | C | L | |||
Oral antidiabetic pharmaceuticals | Su et al. [16] | – | – | ↑: B. Longum† ↓: E. faecalis | – | – | – | HbA1c, [glucose] | – | – | Ch, TG, LDL | |
Gu et al. [17] | – | – | (Acarbose) ↑: 36 mOTUs ↓: 33 mOTUs | ↓: Rarefaction, gene count, Shannon | – | BW, BMI | HbA1c, [glucose] | AUC | HOMA-IR | Ch, TG | ||
– | – | (Glipizide) No significant results | No significant results | – | – | HbA1c, [glucose] | – | – | – | |||
Tong et al. [18] | – | ↑: Megamonas, Escherichia/Shigella, Klebsiella, Blautia, Fusobacterium ↓: Alistipes, Bacteroidetes | – | ↑: Simpson | ↑: Bray-Curtis distance PCA, PCoA | BW, BMI | HbA1c, [glucose] | – | HOMA-B | Ch, LDL, HDL | ||
Wu et al. [19] | – | ↑: Escherichia, Bifidobacterium, Intestinibacter | ↑: 67 strains ↓: 18 strains | No significant results | No significant results | BMI | HbA1c, [glucose] | – | HOMA-IR, HOMA-B | HDL | ||
Surgery | Cortez et al. [20] | ↑: Bacteroidetes, Verrucomicrobia | ↑: Bacteroides, Akkermansia, Dialister | – | ↑: Shannon†, Chao1 estimator, Simpson§ | Unifrac distance: dispersion ‡ | BW | – | – | – | – | |
Murphy et al. [21] | (RYGB) ↑: Firmicutes, Actinobacteria ↓: Bacteroidetes | – | ↑: R. Intestinalis | ↑: species richness | – | BMI | HbA1c | – | HOMA-IR | – | ||
(SG) ↑: Bacteroidetes | – | ↑: R. Intestinalis | – | – | BMI | HbA1c | – | HOMA-IR | – | |||
Lee et al. [22] | (AGB) ↑: Proteobacteria | ↑: Akkermansia | ↑: 2 OTUs ↓: 2 OTUs | ↓: observed species¶, Chao1¶, PD¶ | Unifrac distance: no distant clustering | BMI | HbA1c | – | – | – | ||
(RYGB) ↑: Proteobacteria, Actinobacteria | ↑: Faecalibacterium†, Akkermansia | ↑: 10 OTUs ↓: 1 OTUs | ↑: observed species, Chao1, PD | BMI | HbA1c | – | – | – | ||||
Probiotics | Mobini et al. [23] | – | – | ↑: L. reuteri† | No significant results | No significant results | BW, BMI | – | ISI | – | – | |
Firouzi et al. [24] | – | ↑: Lactobacillus, Bifidobacterium† | – | – | – | – | HbA1c | fasting | – | – | ||
Sato et al. [25] | – | ↑: Lactobacillus†, Enterococcus | ↑: C. coccoides!†, C. leptum!†, L. gasseri, L. casei†, L. reuteri | – | – | – | HbA1c | – | – | Ch | ||
Hsieh et al. [26] | – | ↑: Bifidobacterium | ↑: L. reuteri† | – | – | – | – | – | – | Ch | LDL | |
Zhang et al. [31] | – | – | ↑: 12 strains | ↓: gene count | No significant results. | – | – | – | – | TG, HDL | ||
Prebiotics | Tong et al. [18] | – | ↑: Paraprevotella, Megamonas, Faecalibacterium, Klebsiella, Lachnospiraceae, Blautia ↓: Bacteroidetes, Parasutterella, Clostridiales, Alistipes, Clostridium | – | ↓: Rarefaction, Chao1 | ↑: Bray-Curtis distance PCA, PCoA. weighted and unweighted UniFrac distances†, abundance-weighted, binary Jaccard distances† | BW, BMI | HbA1c, [glucose] | – | HOMA-IR | Ch, TG, LDL | |
HOMA-B | HDL | |||||||||||
Medina-Vera et al. [27] | – | – | ↑: F. prausnitzii, A. muciniphila, B. longum, B. fragilis ↓: P. copri | ↑: Shannon† | – | – | HbA1c, AUC | ISI | – | Ch, TG, LDL | ||
Pedersen et al. [28] | – | ↑: Bifidobacterium | – | ↑: Shannon, inverse Simpson Richness | No significant results | – | GEZI | – | – | Ch, LDL | ||
Shin et al. [29] | – | ↑: Lactobacillus†, Akkermansia†, Megamonas, Mobilitalea, Acetivibrio ↓: Bifidobacterium†, Clostridium, Oscilibacter, Alloprevotella | – | No significant results | No significant results | – | AUC | – | – | – | ||
Balfego et al. [30] | ↓: Firmicutes | ↑: Bacteroides, Prevotella | ↑: E. Coli | – | – | – | – | fasting | HOMA-IR | – | ||
Zhang et al. [31] | – | – | ↑: 40 strains ↓: 30 strains | ↓: gene count†^, Shannon | ↑: Bray-Curtis distance PCoA† | – | HbA1c, [glucose], 2hPPG | – | HOMA-B | Ch, TG, LDL, HDL | ||
Syn. | Zhang et al. [31] | – | – | ↑: 41 strains ↓: 39 strains | ↓: gene count†^, Shannon†^ | ↑: Bray-Curtis distance PCoA† | – | HbA1c, [glucose], 2hPPG | – | HOMA-IR, HOMA-B | Ch, TG, LDL, HDL |
Alpha Diversity Indicator | Change | Changes in Beta Diversity | RCT | Metabolic Outcome Present |
---|---|---|---|---|
Shannon index | ↑ | Weighted, unweighted Unifrac: Dispersion | Cortez et al. [20] | ↓ Anthropometric results |
No significant results in PCoA | Medina-Vera et al. [27] | ↓ Glycemic, lipid profile, inflammatory results. ↓ FFAs | ||
No significant results in PCoA (Bray-Curtis distance) | Pedersen et al. [28] | ↓ Glycemic results | ||
↓ | – | Gu et al. (Acarbose arm) [17] | ↓ Glycemic, lipid profile, inflammatory results | |
Significant results in PcoA (↑: Bray-Curtis distance) | Zhang et al. (Symbiotic arm) [31] | ↓ Glycemic, lipid profile results | ||
Significant results in PcoA (↑: Bray-Curtis distance) | Zhang et al. (Prebiotic arm) [31] | ↓ Glycemic, lipid profile results | ||
Simpson index | ↑ | Weighted, unweighted Unifrac: Clustering | Cortez et al. (CG) [20] | – |
Significant results in PCA, PCoA (↑: Bray-Curtis distance) | Tong et al. (Metformin arm) [18] | ↓ Anthropometric, glycemic, lipid profile, inflammatory results | ||
Inverse Simpson index | ↑ | No significant results in PCoA (Bray-Curtis distance) | Pedersen et al. [28] | ↓ Glycemic results |
Chao1 index | ↑ | Weighted, unweighted Unifrac: Dispersion | Cortez et al. [20] | ↓ Anthropometric parameters |
Weighted, unweighted Unifrac: Clustering | Cortez et al. (CG) [20] | – | ||
No significant results in PCoA (UniFrac) | Lee et al. (RYGB arm) [22] | ↓ Anthropometric, glycemic results | ||
↓ | Significant results in: PCA, PcoA (↑: Bray-Curtis distance); ↑: weighted, unweighted UniFrac distances; abundance-weighted, ↑: binary Jaccard distances | Tong et al. (Prebiotic arm) [18] | ↓ Anthropometric, glycemic, lipid profile, inflammatory results, ↑ dBP | |
No significant results in PCoA (UniFrac) | Lee et al. (AGB arm) [22] | ↓ Glycemic, anthropometric results | ||
Species richness | ↑ | – | Murphy et al. (RYGB arm) [21] | ↓ Anthropometric, glycemic results |
No significant results in PCoA (Bray-Curtis distance) | Pedersen et al. [28] | ↓ Glycemic results | ||
Observed species | ↑ | No significant results in PCoA (UniFrac) | Lee et al. (RYGB arm) [22] | ↓ Anthropometric, glycemic results |
↓ | No significant results in PCoA (UniFrac) | Lee et al. (AGB arm) [22] | ↓ Glycemic, anthropometric results | |
Rarefaction | ↓ | – | Gu et al. (Acarbose arm) [17] | ↓ Glycemic, lipid profile, inflammatory results |
Significant results in: PCA, PcoA (↑: Bray-Curtis distance); ↑: weighted, unweighted UniFrac distances; abundance-weighted, ↑: binary Jaccard distances | Tong et al. (Prebiotic arm) [18] | ↓ Anthropometric, glycemic, lipid profile, inflammatory results | ||
Phylogenic diversity | ↑ | No significant results in PCoA (UniFrac) | Lee et al. (RYGB arm) [22] | ↓ Anthropometric, glycemic results |
↓ | No significant results in PCoA (UniFrac) | Lee et al. (AGB arm) [22] | ↓ Glycemic, anthropometric results | |
Gene count | ↓ | – | Gu et al. (Acarbosis arm) [17] | ↓ Glycemic, lipid profile, inflammatory results |
Significant results in PCoA (↑: Bray-Curtis distance) | Zhang et al. (Symbiotic arm) [31] | ↓ Glycemic, lipid profile results | ||
Significant results in PCoA (↑: Bray-Curtis distance) | Zhang et al. (Prebiotic arm) [31] | ↓ Glycemic, lipid profile results | ||
No significant results in PCoA (Bray-Curtis distance) | Zhang et al. (Probiotic arm) [31] | ↓ Lipid profile results |
More Abundant Phyla | Firmicutes | Bacteroidetes | Actinobacteria | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Intervention | Taxonomy | Phylum | Genus | Species | Overall | Phylum | Genus | Species | Overall | Phylum | Genus | Species | Overall |
Surgery | |||||||||||||
RYGB (3) | ↑ (1/1) | ↑ (2/2) | ↑ (1/1) | ↑ | → (1/2) | ↑ (1/1) | (0/0) | ? | ↑ (2/2) | (0/0) | (0/0) | ↑ | |
AGB (1) | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | |
SG (1) | (0/0) | (0/0) | ↑ (1/1) | → | ↑ (1/1) | (0/0) | (0/0) | ↑ | (0/0) | (0/0) | (0/0) | n/a | |
Oral anti-diabetic medication | |||||||||||||
Acarbose (2) | (0/0) | (0/0) | ↑ (20/36) | → | (0/0) | (0/0) | ↓ (14/16) | → | (0/0) | (0/0) | ↑ (6/7) | → | |
Metformin (2) | → (0/0) | ↑ (2/2) | ↑ (23/35) | ↑ | (0/0) | ↓ (2/2) | ↑ (5/5) | ? | (0/0) | (0/0) | ↑ (20/20) | → | |
Glipizide (1) | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | |
Probiotics (5) | → (0/0) | ↑ (3/3) | ↑ (17/17) | ↑ | (0/0) | (0/0) | ↑ (1/1) | → | (0/0) | ↑ (2/2) | ↑ (1/1) | ↑ | |
Prebiotics (6) | ↓ (1/1) | ↑ (8/12) | ↓ (16/28) | ? | (0/0) | ↑ (4/7) | ↑ (11/18) | ↑ | (0/0) | → (1/2) | ↓ (5/7) | ? | |
Symbiotics (1) | (0/0) | (0/0) | ↓ (24/41) | → | (0/0) | (0/0) | ↑ (10/19) | → | (0/0) | (0/0) | ↓ (5/6) | → | |
Less abundant phyla | Proteobacteria | Verrucomicrobia | Fusobacteria | ||||||||||
Surgery | |||||||||||||
RYGB (3) | ↑ (1/1) | (0/0) | (0/0) | ↑ | ↑ (1/1) | ↑ (2/2) | (0/0) | ↑ | (0/0) | (0/0) | (0/0) | n/a | |
AGB (1) | ↑ (1/1) | (0/0) | (0/0) | ↑ | (0/0) | ↑ (1/1) | (0/0) | ? | (0/0) | (0/0) | (0/0) | n/a | |
SG (1) | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | |
Oral anti-diabetic medication | |||||||||||||
Acarbose (2) | (0/0) | (0/0) | ↑ (3/3) | → | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | ↑ (1/1) | → | |
Metformin (2) | (0/0) | ↑ (2/2) | ↑ (18/22) | ↑ | (0/0) | (0/0) | (0/0) | n/a | (0/0) | ↑ (1/1) | ↓ (2/2) | ? | |
Glipizide (1) | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | |
Probiotics (5) | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | (0/0) | n/a | |
Prebiotics (6) | (0/0) | ↑ (1/1) | ↑ (10/11) | ↑ | (0/0) | ↑ (1/1) | ↑ (1/1) | ↑ | (0/0) | (0/0) | ↑ (1/1) | → | |
Symbiotics (1) | (0/0) | (0/0) | ↑ (12/13) | → | (0/0) | (0/0) | (0/0) | n/a | (0/0) | (0/0) | ↑ (1/1) | → |
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Merkevičius, K.; Kundelis, R.; Maleckas, A.; Veličkienė, D. Microbiome Changes after Type 2 Diabetes Treatment: A Systematic Review. Medicina 2021, 57, 1084. https://doi.org/10.3390/medicina57101084
Merkevičius K, Kundelis R, Maleckas A, Veličkienė D. Microbiome Changes after Type 2 Diabetes Treatment: A Systematic Review. Medicina. 2021; 57(10):1084. https://doi.org/10.3390/medicina57101084
Chicago/Turabian StyleMerkevičius, Kajus, Ričardas Kundelis, Almantas Maleckas, and Džilda Veličkienė. 2021. "Microbiome Changes after Type 2 Diabetes Treatment: A Systematic Review" Medicina 57, no. 10: 1084. https://doi.org/10.3390/medicina57101084