Role of exercise in preventing and restoring gut dysbiosis in patients with inflammatory bowel diseases: A review

Table 1 Effect of exercise on the gut microbiome

Ref.	Study subject	Sample type	Exercise protocol	Exercise vs controls	Notes
Lambert et al[9]	Mouse, type 2 diabetic, (C57BL/KsJ-leprdb/leprdb)	Cecal matter	Treadmill, 5 d/wk, 66 min/d, 2.87 m/min	↑ Clostridium leptum	↑ Bifidobacterium with exercise in non-diabetic mice
				↑ Lactobacillus
				↓ Total bacteria
				↓ Bacteroides
				↓ Bifidobacterium
				↓ Methanobrevibacter
				↓ Prevotella
Campbell et al[19]	Mouse C57BL/6NTac, male	Fecal matter from the distal colon	Free running wheel	↑ Allobaculum	Normal-diet, not observed in a high-fat diet, except for Faecalibacterium prausnitzi
				↑ Clostridiales
				↑ Faecalibacterium prausnitzi
Denou et al[20]	Mouse, C57 BL/6, high-fat diet, obese	Feces from anal area, then full intestinal sampling	Treadmill, 6 wk total, 3 d/wk, 1 h/d, 17 m/min at 5% grade for 2 min + 2 min rest, increase by 1 m/min every week	↑ Bacteroidetes/Firmicutes ratio in the cecum	-
				↑ Bacteroidetes/Firmicutes ratio in the rectum
Carbajo-Pescador et al[8]	Juvenile male Wistar rats on early obesity and non-alcoholic fatty liver disease onset	Fecal matter	Treadmill, 11 wk total, 60 min/d combined aerobic and resistance training (10-min running; eight 2-min progressive incline run from 10°-25° at 20-25 cm/s /1 min rest; 30 min aerobic exercise)	↑ Parabacteroides
				↑ Bacteroides
				↑ Flavobacterium genera
				↓ Blautia
				↓ Dysgonomonas
				↓ Porphyromonas
Clarke et al[10]	Human, rugby player, male	Fecal matter, self-collected	Rugby training, capacity determined by EPIC-Norfolk questionnaire	↑ Akkermansia (than high-BMI controls)	-
				↓ Bacteroides (than low-BMI controls)
				↓ Lactobacillus (than low-BMI controls)
Bressa et al[24]	Human, female, premenopausal, BMI 20-25 kg/m2	Fecal matter, self-collected	No forced exercise, physical activity level gauged by accelerometers	↑ Akkermansia muciniphila	-
				↑ Faecalibacterium prausnitzii
				↑ Roseburia hominis
Munukka et al[26]	Human, female, sedentary, BMI > 27.5 kg/m2	Fecal matter, self-collected	Ergometer, Weeks 1-2: at 60 rpm, low intensity, 3 d/wk, 40 min/d	↑ Akkermansia	-
				↑ Anaerofilum
				↑ Bifidobacteriaceae
				↑ Dorea
				↑ Verrucomicrobiaceae
			Weeks 3-4: 3 d/wk, 50 min/d, every other session 3 10-min intervals of moderate-intensity cycling, the rest low intensity
				↓ Desulfovibrionaceae
				↓ Enterobacteriaceae
				↓ Odoribacter
				↓ Porphyromonadaceae
				↓ Proteobacteria
				↓ Streptococcus
			Weeks 5-6: 3 d/wk, 60 min/d, four 10-min moderate intensity intervals, the rest low intensity
Taniguchi et al[27]	Human, male, age > 60 yr, healthy	Fecal matter, self-collected	Cycling, Weeks 1-2: 3 d/wk, 30 min/d, 60% of VO2peak (week 1), 70% of VO2peak (week 2)	↓ Clostridium difficile	-
				↑ Oscillospora
			Weeks 3-5: 3 d/wk, 45 min/d, 70% of VO2max (week 3), 75% of VO2max (weeks 4-5)
Zhao et al[29]	Human, marathon runners	Fecal matter, self-collected	The 2016 Chongqing half marathon, before and after the race	↑ Acidobacteria	Post- vs pre-running
				↑ Lentisphaerae
Castellanos et al[23]	Human	Fecal matter, self-collected	No forced exercise, physical activity level gauged by accelerometers	↑ Blautia	-
				↑ Coprococcus
				↑ Eubacterium
				↓ Bacteroides
				↓ Parabacteroides
Keohane et al[30]	Human, male, athlete	Fecal matter, self-collected	Rowing race, 33 d 22 h, 151.8 km per day	↑ Roseburia hominis	Post-ultra-endurance exercise
				↑ Subdoligranulum
Liang et al[31]	Human, martial arts athlete	Fecal matter, self-collected	Martial arts, athletes, divided into higher- and lower-level based on General Administration of Sport of China criteria	↑ Bilophila	Higher- vs lower-level athletes
				↑ Oscillibacter
				↑ Parabacteroides
				↑ Phascolarctobacterium
				↓ Allisonella
				↓ Citrobacter
				↓ Megasphaera
Morita et al[25]	Human, female, age > 65 yr, sedentary	Fecal matter, self-collected	Trunk strengthening training, 12 wk, 1 h/wk: 5-10 min of warm-up + 45 min of targeted resistance training of trunk muscles + 5 – 10 cool-down and at-home exercise daily	↑ Bacteroides	After 12 wk of aerobic training
Hampton-Marcell et al[28]	Human, age 18-24 yr, swimmers	Cotton swab sample	Self-reporting of daily swimming distance and duration during daily practice	↑ Coprococcus	Before vs after reduction of training volume
				↑ Faecalibacterium
Quiroga et al[14]	Human, age 7-12 yr, obese	Fecal matter, self-collected	Strength and endurance training	↑ Blautia	After a 12-wk strength and endurance training program
				↑ Dialister
			12 wk, 2 d/wk:
			Warm-up on an ergometer for 7 min, low-medium load, 60 rpm	↑ Roseburia
			Third minute onwards, a sprint of 30s at 3’30”, 4’30”, 5’30”, and 6’30”
			Strength exercises for five muscle groups, initially 3 sets of 12 repetitions at 30% 1RM, up to 3 sets of 8 repetitions at 70% 1RM
			Cool-down at an elliptical cardiovascular device, 7 min, 50 rpm, 4 min low-medium load + 3 min high load
Rettedal et al[16]	Human, male, age 20-45 yr	Fecal matter, self-collected	9 sessions of high-intensity interval training on non-consecutive days over 3 wk: 60 s cycling at VO2peak 75 s rest	No significant changes in composition	Before and after high-intensity interval training
			8 intervals initially, up to 12 intervals by the end of the protocol

BMI: Body mass index.