Table 2.

Probiotic studies on physical performance, post-exercise recovery and cognitive outcomes.

Subjects	Design	Exercise Protocol and/or Intervention	Probiotic Supplementation	Main Results	Reference
Animal studies:
6-week-old male ICR mice 3 groups n = 8/group	Animal study	Forelimb grip strength Forced swim-to-exhaustion test, with loads 15-min swim test to determine recovery and fatigue-related biomarkers	L. plantarum TWK10 (LP10) Dosing per group: 0, 2.05 × 108; or 1.03 × 109 CFU/kg/day for 6 weeks	PRO improved forelimb grip strength and exhaustive swimming time. Blood lactate, ammonia, and CK levels were lower in PRO mice after a 15-min swim compared with those in control mice. Type I muscle fiber type increased, and relative muscle weight increased in PRO mice vs. control mice.	[88]
6-week-old male ICR mice 4 groups n = 8/group	Animal study	Forelimb grip strength Forced swim-to-exhaustion test with loads 10-min and 90-min swim tests, to determine recovery and fatigue-related biomarkers	A kefir drink with L. fermentum DSM 32,784 (LF26), L. helveticus DSM 32,787 (LH43), L. paracasei DSM 32,785 (LPC12), L. rhamnosus DSM 32,786 (LRH10), and S. thermophilus DSM 32,788 (ST30) Kefir dosing per group: 0, 2.15, 4.31, or 10.76 g/kg/day for 4 weeks	Kefir supplementation increased time-to exhaustion, and improved forelimb grip strength. Blood lactate, ammonia, blood urea nitrogen, and CK levels were lower after exercise in kefir-fed mice compared with control mice, in a dose-dependent manner. Glycogen contents in the liver and muscle were higher in kefir-supplemented mice compared with control mice.	[89]
11-week-old male Wistar rats 2 groups n = 13/group	Animal study	Incremental speed exercise on a treadmill, until exhaustion Treadmill chamber, coupled with gas-analyzer, to assess VO2max	Saccharomyces boulardii (strain not reported) 3 × 108 CFU/kg/day for 10 days	PRO supplementation moderately improved aerobic performance. PRO mice ran approx. 8 min longer than control mice (until exhaustion) and had higher maximal speed.	[90]
7-week-old male ICR mice 4 groups n = 10/group	Animal study	Forelimb grip strength Forced swim-to-exhaustion test, with loads 10-min and 90-min swim tests, to determine recovery and fatigue-related biomarkers	B. longum subsp. longum OLP-01 isolated from a female weightlifter Dosing per group: 0, 2.05 × 109, 4.10 × 109, or 1.03 × 1010 CFU/kg/day for 4 weeks	PRO improved forelimb grip strength and swim-to-exhaustion time, in a dose-dependent manner. Blood lactate and ammonia levels were lower after the acute swim test in PRO vs. control mice. After a 90-min swim test, blood urea nitrogen and CK levels were lower in PRO mice compared with those in control mice. PRO increased hepatic and muscular glycogen contents, observed at autopsy.	[98]
6-week-old male ICR mice 4 groups n = 10/group	Animal study	Forelimb grip strength Forced swim-to-exhaustion test, with loads 10-min and 90-min swim tests, to determine recovery and fatigue-related biomarkers	L. salivarius subsp. salicinius SA-03, isolated from a female weightlifter’s gut microbiota Dosing per group: 0, 2.05 × 109, 4.10 × 109, or 1.03 × 1010 CFU/kg/day for 4 weeks	PRO improved forelimb grip strength and swim-to-exhaustion time, in a dose-dependent manner. Blood lactate and ammonia levels were lower and blood glucose levels were higher after acute tests in the PRO groups vs. control group. After a 90-min swim, blood CK levels were lower in PRO groups compared to the control group. PRO increased hepatic and muscular glycogen contents, observed at autopsy.	[99]
Clinical studies:
Swimmers
Highly trained competitive swimmers n = 17, females Age not reported	Randomized, double-blind, placebo-controlled	6 weeks of intensified off-season training, including swimming and resistance exercise. Performance assessment: Vertical jump force plate test, aerobic and anaerobic swim performance test Cognitive assessment: stress and recovery during the intensified exercise training load (the Recovery-Stress Questionnaire for Athletes)	B. longum 35,624; 1 × 109 CFU bacteria/day for 6 weeks	No significant differences in exercise performance or systemic inflammation markers (at rest) between PRO and PLA. Differences in cognitive outcomes were detected showing more favorable sport recovery related scores in the PRO group.	[93]
Swimmers n = 46, females Age 13.8 ± 1.8 y	Randomized, placebo-controlled	Normal exercise regimen Performance assessment: 400-m free- swimming record, Harvard step test to, measure VO2max	L. acidophilus SPP, L. delbrueckii subsp. bulgaricus, B. bifidum, and S. salivarus subsp. thermophilus, strains not reported 400 mL of probiotic yogurt/day with 4 × 1010 CFU/mL for 8 weeks	Significant improvement in VO2max in the PRO group. No differences in 400-m swimming times between PRO and PLA groups.	[82]
Endurance runners
Elite distance runners n = 20, males Age 27.3 ± 6.4 y	Randomized, double-blind, placebo-controlled, crossover	Habitual winter-season training Performance assessment: A treadmill running test until exhaustion, at the start of the study period and the end of each study month	L. fermentum VRI-003; 1.2 × 1010 CFU bacteria/day for 4 weeks Cross-over study, with 1-month wash-out	No difference in performance outcomes with PRO compared to PLA. The number of illness days during PRO supplementation was significantly lower than with PLA (30 vs. 72 days). IFN-γ response was moderately higher with the PRO than with PLA.	[81]
Endurance-trained runners n = 8, males Age 26 ± 6 y	Randomized, blinded, placebo-controlled, cross-over	Habitual training Bout of exercise: 2-h running exercise at 60% VO2max in hot ambient conditions	L. casei (strain not reported) 1 × 1011 CFU/day for 7 days Cross-over study, with 1-month wash-out	No differences in hydration status between PRO and PLA. Inflammatory cytokine levels were not different between PRO and PLA, either pre-exercise or post-exercise (1, 2, 4, and 24 h after running).	[100]
Endurance-trained runners n = 8, males Age 26 ± 6 y	Randomized, blinded, placebo-controlled, cross-over	Habitual training Bout of exercise: 2-h running exercise, at 60% VO2max, in hot, ambient conditions	L. casei (strain not reported) 1 × 1011 CFU/day for 7 days Cross-over study with 1-month wash-out	PRO and PLA did not differ in salivary anti-microbial protein or serum cortisol responses during the post-exercise period (1, 2, 4, and 24 h after running).	[101]
Runners n = 10, males Age 27 ± 2 y	Randomized, double-blind, placebo-controlled, cross-over	Normal training Performance assessment: Running to fatigue, at 80% of ventilatory threshold, at 35 °C and 40% humidity	Multispecies probiotic, strains not specified; L. acidophilus, L. rhamnosus, L. casei, L. plantarum, L. fermentum, B. lactis, B. breve, B. bifidum, and S. thermophilus 45 × 109 CFU/day for 4 weeks, cross-over study with a 3-week wash-out	PRO increased run time to fatigue (PRO 37:44 vs. PLA 33:00 min:sec). A moderate, non-significant reduction in pre-exercise and post-exercise serum lipopolysaccharide (LPS) levels for PRO compared to PLA. No difference between PRO and PLA in plasma IL-6, IL-10, and IL-1Ra or GI permeability after exercise in the heat.	[77]
Marathon runners n = 42, males Age 39.5 ± 9.4 y	Randomized, double-blind, placebo-controlled	Usual training Bout of exercise: marathon run	L. casei Shirota 40 × 109 CFU/day for 30 days	PRO maintained salivary immune protection and increased anti-inflammatory response on the upper airways, immediately after the marathon. Serum TNF-α level was significantly lower immediately post-marathon in the PRO group compared to that in the PLA group	[102]
Marathon runners n = 119 (105/M, 14/F) Average age 40 y	Randomized, double-blind, placebo-controlled	3-month training period, 6-day preparation period Bout of exercise: marathon run	L. rhamnosus GG 4.0 × 1010 bacteria in drink/day (or 1 × 1010 in tablet/day) for 3 months	PRO did not differ from PLA in ox-LDL or antioxidant activity, pre- or post-marathon.	[103]
Marathon runners n = 24 (20/M, 4/F) Age 22–50 y	Randomized, double-blind, placebo- controlled, matched-pairs	Habitual training routine Performance assessment/Bout of exercise: Marathon race (no baseline assessment)	L. acidophilus CUL60, L. acidophilus CUL21, B. bifidum CUL20, and B. animalis subsp. lactis CUL34 2.5 × 1010 CFU/day for 28 days	No difference in marathon times between PRO and PLA. During the final third of the race, the reduction in average relative speed was greater in PLA compared to PRO. GI symptoms were lower in PRO compared to PLA during the final third. No difference in post-race serum IL-6, IL-8, IL-10, and cortisol levels between groups.	[104]
Ultramarathon runners n = 32 (26/M, 6/F) Age 23–53 y	Randomized, controlled (single-blind for glutamine supplementation)	Training for a marathon, ultra-marathon race of 294 km Performance assessment: A graded exercise test, to maximal exhaustion, on a motorized treadmill, VO2max test, pre-marathon, time-to-completion in ultra- marathon race	PRO: Multi-strain probiotic, daily dose 30 × 109 CFU comprising of 10 × 109 CFU L. acidophilus CUL-60 (NCIMB 30,157), 10 × 109 CFU L. acidophillus CUL-21 (NCIMB 30,156), 9.5 × 109 CFU B. bifidum CUL-20 (NCIMB 30,172), and 0.5 × 109 CFU B. animalis subsp. lactis CUL-34 (NCIMB 30,153 + 55.8 g fructooligosaccharides PRO + glutamine: Daily dose 2 × 109 CFU L. acidophilus CUL-60 (NCIMB 30,157), 2 × 109 CFU L. acidophilus CUL-21 (NCIMB 30156), 5 × 107 CFU B. bifidum CUL-20 (NCIMB 30,172), 9.5 × 108 CFU B. animalis subsp. lactis CUL-34 (NCIMB 30,153), and 5x 109 CFU L. salivarius CUL61 (NCIMB 30,211) + 0.9 g glutamine 12 weeks before the marathon	No difference in pre-race VO2max or in time-to-completion for ultra-marathon between PRO, PRO + glutamine, and control groups. PRO and PRO + glutamine had no effects on immune activation via extracellular heat-shock protein eHsp72 signaling at post-race.	[94]
Cyclists, triathletes
Competitive cyclists n = 99 (64/M, 35/F) Age 35 ± 9 y/M and 36 ± 9 y/F	Randomized, double-blind, placebo-controlled	Habitual training (physical activity recorded) Performance assessment: an incremental cycle ergometer performance test (peak power output, VO2max)	L. fermentum VRI-003 PC 1 × 109 CFU/day for 11 weeks	PRO did not affect training patterns or performance in VO2 max testing. Acute exercise-induced changes in anti- and pro-inflammatory cytokines were attenuated with PRO.	[71]
Triathletes Study I: n = 18, Study II: n = 16 Sex not reported Age 19–26 y	Randomized, double-blind, placebo-controlled	8 weeks of programmed training before a sprint triathlon (Study I) or full triathlon competition (Study II) Performance assessment: Wingate and 85% VO2max test (after full triathlon)	L. plantarum PS128 3 × 1010 CFU/day Study I: last 4 weeks of training Study II: last 3 weeks of training	In Study II, performance during recovery from a full triathlon was decreased in the PLA group and maintained at the pre-triathlon level in the PRO group. PRO group had lower blood TNF-α, IFN-γ, IL-6, and IL-8 levels compared to PLA, immediately after exercise (Study I/II), with levels significantly lower in PRO group 3 h after full triathlon (Study II). Anti-inflammatory IL-10 was higher in the PRO group, immediately after exercise (Study II) compared with that in the PLA group. No differences in muscle damage or fatigue markers detected between groups (Study I/II) except, lower CK in PRO vs. PLA, 3 h after full triathlon (Study II). Oxidative stress marker (MPO) was lower in PRO after exercise, with no differences 3 h post-exercise.	[105]
Elite athletes (badminton, triathlon, cycling, alpinism, karate, savate, kayak, judo, tennis, and swimming) n = 50 (36/M, 14/F) Age 18–28 y	Randomized, double-blind, placebo-controlled	Habitual training >11 h/week, self-reported training loads Performance assessment: VO2max, by a graded cardiopulmonary test, on a treadmill Cognitive assessment: Profile of mood and state (POMS) questionnaire	L. helveticus Lafti L10 2 × 1010 CFU/day for 14 weeks	No difference in VO2max and treadmill performance between PRO and PLA. Increase in the subjective feeling of vigor in the PRO group, but no difference in other cognitive scores between groups.	[84]
Recreational triathletes n = 30 (25/M, 5/F) Age 35 ± 1 y	Randomized, double-blind, placebo-controlled	Standardized training program for the previous 6 months Performance assessment/Bout of exercise: a long-distance triathlon (no baseline assessment)	Multistrain probiotic, daily dose 30 × 109 CFU (10 × 109 CFU L. acidophilus CUL-60 (NCIMB 30,157), 10 × 109 CFU L. acidophillus CUL-21 (NCIMB 30,156), 9.5 × 109 CFU B. bifidum CUL-20 (NCIMB 30,172), 0.5 × 109 CFU B. animalis subsp. lactis CUL-34 (NCIMB 30,153)) + 55.8 g fructo-oligosaccharides, alone or in combination with 600 mg N-acetyl carnitine + 400 mg α-lipoic acid for 12 weeks before and 6 days after triathlon	Non-significantly faster times were reported for PRO during swim and cycle stages, and a trend towards an overall faster time was reported compared to PLA (~86 min faster). No baseline measurements on performance were assessed. PRO reduced post-race plasma endotoxin levels, whereas PLA had no effect.	[73]
Team sports
Division I volleyball and soccer athletes n = 23, females Age 19.6 ± 1.0 y	Randomized, double-blind, placebo-controlled	Offseason resistance training protocol Performance assessment: 1RM testing (bench press, squat, deadlift), isometric midthigh pull, vertical jump height, pro-agility test	Bacillus subtilis DE111 5 × 109 CFU/day for 10 weeks	PRO had no effect on strength or athletic performance but significantly reduced percentage of body fat percentage.	[96]
Division I baseball athletes n = 25, males Age 20.1 ± 1.5 y	Randomized, double-blind, placebo-controlled	Resistance training program Performance assessment: 1RM testing (squat, deadlift), pro-agility test, 10-yard sprint, standing long jump	Bacillus subtilis DE111 1 × 109 CFU/day for 12 weeks	No differences between PRO and PLA in strength, performance, or body composition. PRO reduced TNF-α levels, but no differences in IL-10, cortisol, zonulin, or testosterone levels observed between PRO and PLA.	[95]
Highly trained athletes n = 29 (13/M, 16/F) Age 20–35 years	Randomized, double-blind, placebo-controlled	Normal training Performance assessment: Cycle ergometer exercise test until exhaustion	B. bifidum W23, B. lactis W51, Enterococcus faecium W54, L. acidophilus W22, L. brevis W63, and L. lactis W58 1 × 1010 CFU/day for 12 weeks	No difference in performance between groups. Weekly training loads were significantly higher in PRO compared to PLA (8.0 ± 2.3 vs. 6.6. ± 4.3 h/week). Exercise-induced reduction in tryptophan levels in PLA but not in the PRO group. PRO reduced the incidence of URT infections.	[85]
Active non-athletes
Resistance trained subjects n = 15, males Age 25 ± 4 y	Randomized, double-blind, placebo-controlled, crossover	Muscle-damaging eccentric exercise bout Performance assessment: isometric peak torque, after muscle damaging-exercise	S. thermophilus FP4, and B. breve BR03 5 × 109 CFU of each/day for 21 days	PRO attenuated performance decrements caused by muscle-damaging exercise during the recovery period. No effects of PRO on muscle soreness, range of motion, or plasma creatine kinase. PRO lowered resting IL-6 concentrations that were sustained until 48 h post-exercise.	[106]
Recreational exercisers n = 29, males Age 21.5 ± 2.8 y	Single-blind, crossover (casein first, after washout, PRO+casein)	Single-leg exercise bout Performance assessment: Anaerobic power by modified Wingate test, single-leg vertical jump, strength, by 1RM testing in the one-legged leg press, after muscle damaging-exercise	Bacillus coagulans BC30 1 × 109 CFU/day + 20 g casein for 14 days	PRO + casein increased perceived recovery status and reduced muscle soreness after exercise compared with casein alone. PRO + casein maintained post-exercise Wingate peak power at the pre-exercise level, whereas casein alone demonstrated reduced post-exercise performance. For 1RM leg-press and vertical jump power, no differences between groups in post-exercise performance.	[107]
Physically active subjects n = 27, females Age 18–25 y	Controlled, randomized	Habitual moderate exercise Performance assessment: treadmill running until exhaustion, VO2max test (Bruce test)	Probiotic not specified 450 g of probiotic yogurt/day for 2 weeks	No difference in VO2max between PRO and PLA. PRO yogurt increased antioxidant enzyme activities and reduced MMP2 and MMP9 levels before and after exhaustive exercise. No significant differences between PRO and PLA in high-sensitivity CRP, IL-6, and TNF-α after intense exercise.	[108]
Physically active students n = 11, sex not reported Age 22 ± 1 y	Non-controlled	Habitual training including endurance exercise Bout of exercise: 2-h cycling at 60% of VO2max	L. acidophilus, L. delbrueckii subsp. bulgaricus, Lactococcus lactis subsp. lactis, L. casei, L. helveticus, L. plantarum, L. rhamnosus, L. salivarius subsp. salivarius, B. breve, B. bifidum, B. infantis, B. longum, Bacillus subtilis, S. thermophilus minimum 2 × 109 CFU/capsule, 3 capsules/day for 30 days	Rating of perceived exertion during exercise was not different between PRO and PLA. PRO did not affect salivary antimicrobial proteins at rest or in response to an acute bout of prolonged exercise.	[109]
Students n = 67, males and females (n not specified by sex) Age 18–24 y	Controlled	The exercise groups completed structured, long-distance, endurance run training, whereas the active group maintained their usual exercise routine. Performance assessment: 1.5-mile (2.41 km) walk or run	Probiotic kefir, probiotic strain and dose not specified 15 weeks	No effect of PRO on 1.5-mile completion time. PRO attenuated exercise-induced inflammation, measured as serum CRP levels.	[110]
Students of physical education n = 30, males Average age: PRO 21.56 y, PLA 21.28 y	Randomized, matched pairs	Habitual training and training program by the study Performance assessment: Cooper test, maximum aerobic power, using Bulk test on a laboratory treadmill	Probiotic strains unspecified, included S. thermophilus and/or L. delbrueckii subsp. bulgaricus 1 × 105 CFU/g in 200 mL yogurt/day for 10 weeks	PRO improved VO2max and aerobic performance. PRO decreased serum high-sensitivity CRP and increased HDL levels.	[111]
Healthy participants n = 16, males Age 20–40 y	Randomized, double-blind, placebo-controlled	Habitual exercise Performance assessment: Treadmill running at 85% VO2max workload, until exhaustion.	L. plantarum TWK10 1 × 1011 CFU/day for 6 weeks	PRO improved time-to-exhaustion (PLA vs. PRO: 817 ± 79 s vs. 1292 ± 204 s). Blood glucose was higher in PRO vs. PLA after exhaustive exercise. No differences in post-exercise blood lactate, free fatty acid, CK levels between PRO and PLA.	[91]
Healthy participants n = 54, (27/M, 27/F) Age 20–30 y	Double-blind, placebo-controlled	Habitual exercise Performance assessment: treadmill running, at 60% VO2max and 85% VO2max workload, until exhaustion	L. plantarum TWK10 3 × 1010 CFU/day or 9 × 1010 CFU/day for 6 weeks	Exhaustion time was increased in both PRO groups and were longer compared to PLA. Improvement in exercise capacity was dose-dependent. PRO reduced serum lactate during and after exercise compared to PLA. Muscle mass increased in the high-dose PRO group.	[92]
Healthy sedentary individuals n = 41, males Age 19–26 y	Randomized, parallel, placebo-controlled	Circuit training protocol, including resistance exercises, 3 times a week Performance assessment: muscular strength (peak torque) and power via an isokinetic dynamometer	L. acidophilus BCMC 12,130, L. casei BCMC 12,313, L. lactis BCMC 12,451, B. bifidum BCMC 02,290, B. infantis BCMC 02,129 and B. longum BCMC 02,120 6 × 1010 CFU/day for 12 weeks	PRO did not show superior effects to PLA on muscular strength (peak torque) and power. PRO alone and exercise alone increased post-intervention serum IL-10 concentrations from pre-intervention levels. PRO and PLA with or without exercise, had no effects on serum IL-6 concentration.	[97]
Healthy elderly individuals with stretching experience n = 29 (14/M, 25/F) Age > 65 y	Randomized, double-blind, placebo-controlled	Moderate resistance exercise training, in instructed classes and at home Cognitive assessment: General cognitive performance (incl. tests for accuracy, reaction time), mental state (scoring for depression, anxiety, and overall mental state)	B. longum BB536, B. infantis M-63, B. breve M-16V and B. breve B-3 5 × 1010 CFU/day (1.25 × 1010 CFU each probiotic/day) for 12 weeks	An increase in the general cognitive function scores was observed in PRO and PLA groups, at 12 weeks. PRO group showed a decrease in anxiety-depression scores, body weight, BMI and body fat.	[112]

ICR mice, Institute of Cancer Research mice; L., Lactobacillus (or related genera); B., Bifidobacterium; S., Streptococcus; CFU, colony-forming units; PRO, probiotic supplementation; PLA, placebo supplementation; CK, creatine kinase; VO_2max, maximum rate of oxygen consumption; M, males, F, females; IFN-γ, interferon γ; IL, interleukin; GI, gastrointestinal; TNF-α = tumor necrosis factor α; ox-LDL, oxidized low-density lipoprotein; MPO, myeloperoxidase; 1RM, 1 repetition maximum; MMP2/9, matrix metalloproteinase 2/9; CRP, C-reactive protein; HDL, high-density lipoprotein; BMI, body mass index.