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Table 2 Effect of exercise and/or athletic diet on the gut microbiota: Characteristics of included articles (by publication date)

From: The athletic gut microbiota

Authors, year, countrySubjects characteristicsStudy design and gut microbiome analysisDiet and/or exerciseDurationKey outcome(s)
1. Clarke et al., 2014, Ireland [19]Professional male rugby players, n = 40, 29 ± 4 years; Healthy matched controls, n = 46, 29 ± 6 yearsCross-sectional
16S rRNA gene amplification of the V4 region
ObservationalCross-sectional• Athletes had a higher diversity of gut micro-organisms, representing 22 distinct phyla.
• GMa diversity indices were positively correlated with protein intake and serum creatine kinase in athletes.
2. Estaki et al., 2016, Canada [14]Healthy young males and females, n = 39, stratified by cardiorespiratory fitness, Low: 25.5 ± 3.3 years; Average: 24.3 ± 3.7 years; High: 26.2 ± 5.5 yearsCross-sectional
16S rRNA gene amplification of the V3 and V4 regions
ObservationalCross-sectional• VO2peakb, independent of diet, positively correlated with increased GM diversity.
• VO2peak explained significant variation in GM predicted metagenomic functions, aligning positively with genes related to bacterial chemotaxis, motility, and fatty acid biosynthesis.
• Increased production of fecal butyrate abundances of butyrate-producing taxa (Clostridiales, Roseburia, Lachnospiraceae, and Erysipelotrichaceae) amongst physically fit participants.
3. Yang et al., 2017, Finland [94]Premenopausal females with low, moderate and high-cardiorespiratory fitness (VO2max), n = 71, Low VO2max: 40.4 ± 3.5 years;
Moderate VO2max: 39.7 ± 4.2 years;
High VO2max: 30.6 ± 5 years
Cross-sectional
16S rRNA hybridization, DNA-staining, and flow
cytometry
ObservationalCross-sectional• Decreased Bacteroides, increased Eubacterium rectale-Clostridium coccoides in low VO2max participants vs high VO2max participants.
• VO2max inversely associated with Eubacterium rectale-C. coccoides but not with other bacteria.
4. Allen et al., 2018, USA [98]Sedentary lean males and females, n = 18, 25.1 ± 6.52 years; Obese males and females, n = 14, 31.14 ± 8.57 yearsLongitudinal design
16S rRNA gene amplification of the V4 region
30–60 min moderate-to-vigorous intensity (60–75% of HRRc) aerobic exercise, 3x per week6 weeks• Exercise induced shifts in SCFAd-producing taxa (Faecalibacterium and Lachnospira species) and genetic machinery (BCoATe) were more substantial in lean versus obese participants.
• A return to sedentary activity for 6 weeks led to a BMIf-dependent reversion in gut microbiome composition.
5. Barton et al., 2018, Ireland [13]Professional male rugby players, n = 40, 29 ± 4 years; Healthy matched controls, n = 46, 29 ± 6 yearsCross-sectional
Metagenomic whole genome shotgun sequencing and urine and fecal metabolomics
ObservationalCross-sectional• Relative increase in pathways (amino acid and antibiotic biosynthesis and carbohydrate metabolism) in athletes vs control.
• Increase in fecal metabolites (acetate, propionate and butyrate) in athletes vs control.
6. Cronin et al., 2018, Ireland [199]Sedentary overweight/obese males and females, n = 90, 18–40 yearsRandomized controlled trial,
parallel group design
Metagenomic whole genome shotgun sequencing and urine and fecal metabolomics
Groups:
• Protein-only; 30 g protein (24 g whey)
• Exercise-only; Combined aerobic and resistance training (aerobic training of moderate intensity and resistance training of 3 sets of 8 repetitions on 7 different resistance machines) 3 x per week
• Exercise + protein
8 weeks• Increase in alpha diversity in Exercise + Protein group vs Protein group.
• Decrease in beta diversity of the gut virome in participants consuming protein.
7. Moreno-Pérez et al., 2018, Spain [196]Endurance-trained
males, n = 18,
35.38 ± 9.0 years (control group), 34.90 ± 9.49 years (protein group)
Randomized controlled trial,
parallel group design
16S rRNA gene amplification of the V3 and V4 regions
Groups:
• Control: maltodextrin
• Protein: blend of whey isolate (10 g) and beef hydrolysate (10 g)
Minimum training frequency of 5 endurance training sessions per week; ≥240 min per week
10 weeks• Increase in Bacteroidetes in protein group.
• Decrease in Roseburia, Blautia, and Bifidobacterium longum in protein group.
8. Taniguchi et al., 2018, Japan [101]Healthy elderly Japanese males, n = 33, 62–76 yearsRandomized crossover trial
16S rRNA gene amplification of the V3 and V4 regions
5-week control period OR 5-week supervised, progressive aerobic exercise program. Cycle ergometer 3x per week. 60% of pre exercise VO2peak during week 1, 70% during weeks 2 and 3, and 75% during weeks 4 and 5. Duration was 30 min for weeks 1 and 2, and 45 min for weeks 3–5.5 weeks• Short-term endurance exercise did not appreciably influence diversity and composition of gut microbiota. Minor changes in the gut microbiota were associated with cardiometabolic risk factors.
• Decreased relative abundance of C. difficile significantly decreased, whereas Oscillospira significantly increased during exercise as compared to the control period.
9. Durk et al., 2019, USA [93]Healthy young males and females, n = 37, 25.7 ± 2.2 yearsCross-sectional
Quantitative Polymerase Chain Reaction (qPCR) that specifically measured the quantity of a target gene (16 s RNA) found in Firmicutes and Bacteroidetes
ObservationalCross-sectionalFirmicutes/Bacteroidetes ratio positively correlated to VO2max.
• VO2max explained ~ 22% of the variance of an individual’s relative gut bacteria as determined by Firmicutes/Bacteroidetes ratio.
10. Keohane et al., 2019, Ireland [99]Ultra-endurance male athletes, n = 4,
26.5 ± 1.3 years
A prospective, repeated-measures, within-subject report
Metagenomic whole genome shotgun sequencing
Observational33-day event; 3-month follow-up• Increased alpha diversity throughout event.
• Increased abundance of butyrate producing species (Roseburia hominis and members of the genus Subdoligranulum) and species associated with improved metabolic health (Dorea longicatena).
• Many of the adaptions in GM community structure and metaproteomics persisted at 3 months follow up.
11. Kern et al., 2019, Denmark [108]Overweight/obese males and females; n = 88; 20–45 yearsRandomized controlled trial,
parallel group design
16S rRNA gene amplification of the V4 region
Exercise groups:
• Habitual living (CON),
• Active commuting by bike (BIKE)
• Leisure-time exercise of moderate intensity (MOD)
• Vigorous intensity exercise (VIG)
6 months• Increase alpha diversity index in VIG at 3 months compared with CON.
• Beta diversity changed in all exercise groups compared with CON; VIG decreased heterogeneity.
• Increased inferred functional potential of microbiota in the exercise groups, primarily at 3 months and in MOD.
12. Morita et al., 2019, Japan [103]Healthy sedentary elderly females; n = 32; ≥ 65 yearsNon-randomized comparative trial
16S rRNA terminal restriction fragment length polymorphism
analyses
Exercise groups:
• Trunk muscle training group 1 h per week.
• Aerobic exercise training group, brisk walking at ≥3 METSg, 1 h daily.
12 weeks• Increased Bacteroides relative abundance in aerobic exercise group.
• Increased Bacteroides following exercise intervention associated with increased 6-min walk test.
13. Motiani et al., 2019, Finland [109]Obese sedentary, prediabetic/type 2 diabetic males and females; n = 26 (n = 9, n = 17 respectfully); 49 ± 4 yearsParallel group design
16S rRNA gene amplification of the V3 and V4 regions
Exercise groups:
• Sprint interval training group; 30 s exercise bouts (4–6) of all out cycling efforts with 4 min of recovery, 3x a week.
• Moderate intensity continuous training group; 40–60 min cycling at 60% of VO2peak intensity, 3x a week.
2 weeks• Increased Bacteroidetes in both groups.
• Decreased Firmicutes:Bacteroidetes ratio in both groups.
• Decreased Clostridium genus and Blautia.
• Colonic glucose uptake positively associated with Bacteroidetes and inversely with Firmicutes phylum, Firmicutes: Bacteroidetes ratio and Blautia genus.
14. Murtaza et al., 2019, Australia [230]Elite male endurance race walkers; n = 21; 20–35 yearsNon-randomized comparative trial
16S rRNA gene amplification of the V6-V8 regions
Diet groups:
• High-Carbohydrate
• Periodized Carbohydrate
• ketogenic LCHFh
Consumed during an intensified training program.
3 weeks• Microbiota profiles at baseline could be separated by Prevotella or Bacteroides dominated enterotype.
• LCHF diet resulted in increased relative abundance of Bacteroides and Dorea and decreased Faecalibacterium.
• Negative correlations between Bacteroides and fat oxidation, and between Dorea and economy test following LCHF intervention.
15. Scheiman et al., 2019, USA [16]Experiment 1:
• Athletes from the 2015 Boston Marathon (n = 15), sedentary controls (n = 10)
Experiment 2:
• Ultramarathoners and Olympic trial rowers (n = 87)
Observational
16S rRNA gene amplification of the V4 region for experiment 1
Metagenomic whole genome shotgun sequencing for experiment 2
Experiment 1:
• Marathon event
Experiment 2:
• Exercise bout
Experiment 1:
• Fecal samples collected 7 days before and after Marathon event
Experiment 2:
• Pre/post exercise
Experiment 1:
• Increased Veillonella relative abundance in marathon runners post marathon.
Veillonella was more prevalent among runner’s vs non-runners, although this was not statistically significant.
Experiment 2:
• Increased Veillonella abundance post exercise.
Veillonella methylmalonyl-CoA pathway was overrepresented in athlete metagenomic samples post exercise.
16. Liu et al., 2019, China [106]Overweight/obese prediabetic males; n = 39; 20–60 yearsRandomized controlled trial,
parallel group design
Metagenomic whole genome shotgun sequencing and fecal metabolomics
Groups:
• Control; No exercise.
• High-intensity exercise; 70 min combined aerobic and resistance interval training, 3x a week.
12 weeks• Microbiota profiles were differentially altered in exercise responders (n = 14) vs non-responders (n = 6).
• The microbiome of responders had increased functional capacity for SCFA biosynthesis and BCAAi catabolism.
• Exercise-induced gut microbiota changes were positively correlated with improvements in glucose homeostasis and insulin sensitivity.
• Baseline microbiome features accurately predicted personalized exercise responses.
• Fecal microbiota transplantation from responders conferred the metabolic benefits of exercise in mice.
  1. aGM Gut microbiota
  2. bVO2 Volume of oxygen utilization
  3. cHRR Heart rate reserve
  4. dSCFA Short-chain fatty acid
  5. eBCoAT Butyryl-CoA:acetate CoA-transferase, a butyrate-regulating gene
  6. fBMI Body mass index
  7. gMETS Metabolic equivalents
  8. hLCHF Low-Carbohydrate High-Fat
  9. iBCAA Branched-chain amino acid