Table 3 Probiotic studies in an athletic population: performance, immune and GI health
From: International Society of Sports Nutrition Position Stand: Probiotics
Reference | Subject group | Sex and age (M ± SD) | Supplementation | Treatment duration | Exercise | Diet | Performance Benefit | Immune or GI Benefit |
|---|---|---|---|---|---|---|---|---|
Clancy et al. (2006) [53] | Healthy recreational athletes (n = 18), Fatigued recreational athletes (n = 9) | 11 M / 7 F 16–37 y 6 M / 3 F 17–40 y | L. acidophilus (LAFTI®L10), capsules, 2 × 1010 CFU Daily | 4 weeks | Not reported | Not reported | Not assessed | T cell deficit was reversed (increased secretion of IFNƴ from T cells) following probiotic supplementation |
Moreira et al. (2007) [54] | Non-elite Marathon runners (n = 141) | 62 M / 8 F in treatment group 39 ± 9 y | L. rhamnosus GG (LGG), milk-based drink, 4 × 1010 CFU Daily | 12 weeks | Running During pollen season & 2003 Helsinki City Marathon | Subjects instructed to refrain from eating food containing probiotics | Not assessed | No effects on symptoms of atopy or asthma |
Kekkonen et al. (2007)* [55] *Same subjects as Moreira et al (2007) [54] | Non-elite Marathon runners (n = 141) | 62 M / 8 F in treatment group 39 ± 9 y | L. rhamnosus GG (LGG), milk-based drink, 4 × 1010 CFU Daily | 12 weeks | Running During pollen season & 2003 Helsinki City Marathon | Subjects instructed to refrain from eating food containing probiotics | Not assessed | No effect on respiratory infections or GI episodes. Shortened GI stress post marathon |
Tiollier et al. (2007) [56] | French commando cadets (n = 47) | 47 M 21 ± 0.4 y | L. casei DN- 1 14 00 1, milk-based drink during training (dose not indicated) Daily | 3 weeks | Military training for 3 weeks followed by a 5-day combat course | Military ration. No fermented dairy products | Not assessed | No effect on respiratory tract infections |
Cox et al. (2010) [57] | Elite male distance runners (n = 20) | 20 M 27.3 ± 6.4 y | 1.2 × 1010 CFU L. fermentum VRI-003 (PCC) Daily | 16 weeks | Running (winter training) | Not reported | No changes in running performance | Significant reduction in respiratory episodes and severity |
Martarelli et al. (2011) [58] | Amateur cyclists (n = 24) | 24 M 32.03 ± 6.12 y | L. rhamnosus IMC 501®, L. paracasei IMC 502® 1 × 109 CFU Daily | 4 weeks | Intense physical activity | Diets proportionally equivalent in macro and micronutrient quantity, containing 100% of the RDA for all nutrients | Not assessed | Reduced exercise induced oxidative stress |
Recreationally active endurance athletes (n = 84) | 54 M / 30 F 27.0 ± 11.6 y | L. casei Shirota (LcS), 6.5 × 109 CFU 2x daily | 16 weeks | Running (winter training, normal training load) | Consumption of supplements, additional probiotics, or any fermented dairy products were not permitted during the study period | Not assessed | Significant reduction in frequency of URTI | |
West et al. (2011) [61] | Competitive cyclists (n = 80) | 64 M / 35 F 35 ± 9 and 36 ± 9 y | L. fermentum (PCC®) 1 × 109 CFU Daily | 11 weeks | Cycling (winter training, normal training load) | Subjects were asked to maintain a normal diet and refrain from eating probiotic or prebiotic enriched foods or supplements | No effect on peak power or VO2 max | Significant reduction in URTI (duration and severity) in males. No effect in females |
Välimäki et al. (2012) [62] | Marathon runners Placebo (n = 58), Probiotic (n = 61) | 105 M / 14 F 40 (23–69) y 40 (22–58) y | L. rhamnosus GG (LGG), 4 × 1010 CFU Daily | 12 weeks | Running training; marathon run | Instructed to refrain from eating food containing probiotics and advised to follow normal dietary habits | Not assessed | No effects on serum LDL or antioxidant levels |
Lamprecht et al. (2012) [63] | Endurance trained men (triathletes, runners, cyclists) (n = 23) | 23 M 37.6 ± 4.7 y | Multispecies probiotic (B. bifidum W23, B. lactis W51, E. faecium W54, L. acidophilus W22, L. brevis W63, and L. lactis W58, 1 × 1010 CFU Daily | 14 weeks | Normal training load | 7-dayfood record. Instructed to maintain their habitual diet | No effect on VO2 max, maximum performance | Significant reduction in Zonulin (marker of gut permeability) |
Gleeson et al. (2012) [64] | Highly active individuals (n = 66) | 28 M / 38 W 23.9 ± 4.7 y | L. salivarious, 2 × 1010 CFU Daily | 16 weeks | Endurance-based physical activities (spring training) | Consumption of supplements, additional probiotics, or any fermented dairy products was not permitted | Not assessed | No effect on frequency, severity and duration of upper respiratory tract infections |
Grobbelaar et al. (2012) [65] | Moderately active individuals (n = 50) | 50 M 18–30 y | Bifidobacterium and Lactobacillus strains (dose not indicated) Daily | 6 weeks | Moderately active as defined by ACSM and CDC | Nutritional supplementation prohibited | Not assessed | No significant increases in performance related blood markers |
West et al. (2012) [66] | Active individuals (n = 22) | 22 M 33.9 ± 6.5 y | Multi-strain probiotic (4.6 × 108 CFU L. paracasei subs paracasei (L. casei 431®), 6 × 108 CFU B. animalis ssp. lactis (BB-12®), 4.6 × 108 CFU L. acidophilus LA-5, 4.6 × 108 CFU L. rhamnosus GG Daily | 3 weeks | Recreational cycling | Not reported | Not assessed | No effect on measures of systemic or mucosal immunity including gut permeability |
Salarkia et al. (2013) [44] | Adolescent endurance swimmer (n = 46) | 46 F 13.8 ± 1.8 y | Multi-strain probiotic yoghurt (L. acidophilus SPP, L. delbrueckii bulgaricus, B. bifidum, and S. salivarus thermnophilus) 4 × 1010 CFU Daily | 8 weeks | Swimming | Advised to refrain from other probiotic products | Significant improvement in VO2 max. No effect on swim times | Significant reduction in respiratory and ear infections. No effect on GI episodes |
Charlesson et al. (2013) Abstract of 2012 IJSNEM Confer. | Male athletes (n = 8) (travelling to high risk travelers’ diarrhea countries) | 8 M Age not reported | L. acidophilus, B. lactis, L. rhamnosus (dose not indicated) Daily | 8 weeks | Normal training | Not reported | Not assessed | No effect on travelers’ diarrhea (TD). 50% of all athletes reported TD symptoms |
Sashihara et al. (2013) [67] | University-student athletes (n = 44) | 44 M Grp-1: 19.8 ± 0.9 y Grp-2: 19.9 ± 0.9 y | Grp-1: L. gasseri OLL2809 1 × 109 CFU. Grp-2: alpha-lactalbumin 900 mg +: L. gasseri OLL2809 1 × 109 CFU 3x daily | 4 weeks | Normal training load | Not reported | No improvement in 1 h of cycle ergometer exercise performance | Prevented reduced natural killer cell activity due to strenuous exercise and elevated mood from a depressed state (POMS) |
West et al. (2014) [68] | Active individuals (n = 465) | 241 M / 224 F 35 ± 12 y / 36 ± 12 y | B. animalis subsp. lactis BI-04 2 × 1010 CFU, or L. acidophilus NCFM and B. animalis subsp. lactis BI-07 5 × 109 CFU Daily | 150 days (21.42 weeks) | Normal activity load (approx. 6 h per week) | Refrain from consumption of non-study probiotic or prebiotic supplements or foods during the study. | Not assessed | BI-04 reduced upper respiratory tract infection frequency. BI-07 + LA NCFM showed no effect. Probiotic treatments delayed URTI ~ 0.8 months |
Haywood et al. (2014) [69] | Highly-trained rugby union players (n = 30) | 30 M 24.7 ± 3.6 y | L. gasseri 2.6 × 109 CFU, B. bifidum 0.2 × 109, and B. longum 0.2 × 109 CFU Daily | 4 weeks | Normal training load (during the winter months) | Asked to maintain a normal diet and refrain from consuming probiotic and prebiotic enriched foods or supplements | Not assessed | Significant reduction in episodes of illness. No effect on illness severity |
Shing et al. (2014) [46] | Runners (n = 10) | 10 M 27 ± 2 y | Multispecies probiotic (L. acidophilus, L. rhamnosus, L. casei, L. plantarum, L. fermentum, B. lactis, B. breve, B. bifidum, and S. thermophilus) 4.5 × 1010 CFU Daily | 4 weeks | Normal training load | Provided with a high glycemic index, low sucrose diet for the 26 h prior to each time to-fatigue run. | Significant increase in run time to fatigue in the heat | No effects on inflammation or GI markers |
Aghaee et al. (2014) [70] Abstract | Athletes (n = 16) | 16 M 19–25 y | Probiotic (type and dose not indicated) Daily | 30 days | Normal training load | Not reported | Not assessed | Probiotic treatment significantly increased monocyte levels in comparison to placebo control |
Georges et al. (2014) PILOT [71] | Resistance-trained individuals (n = 10) | 10 M 22.0 ± 2.4 y | B. coagulans GBI-30, 6086 (BC30), 5 × 108 CFU plus 20 g of casein 2x daily | 8 weeks | Periodized resistance training (4x per week) | Macronutrients were controlled to 50% carbohydrate, 25% protein, and 25% fat between groups. | Trend to increase vertical jump power (not significant). | Not assessed |
Narimani-Rad et al. (2014) [72] | Professional bodybuilding athletes (n = 14) | 14 M 20–55 y | Multi-strain probiotic (L. casei 5.1 × 109 CFU/g, L. acidophilus 2 × 109 CFU/g, L. C. 5.1 × 109 CFU/g, L. bulgaricus 2 × 108 CFU/g, B. breve 2 × 1010 CFU/g, B. longum 7 × 107 CFU/g, S. thermophilus 5.1 × 109 CFU/g) Daily | 30 days | Normal training load | Not reported | Not assessed | Stimulated thyroid activity. Significant increase in T4 and significant decrease TSH levels. No significant difference in T3 levels |
Muhamad & Gleeson (2014) [73] | Active University students (n = 11) | 11 (sex not reported) 22 ± 1 y | 14 strain probiotic (L. acidophilus, L. delbrueckii ssp. bulgaricus, L. lactis ssp. lactis, L. casei, L. helveticus, L. plantarum, L. rhamnosus, L. salivarius ssp. salivarius, B. breve, B. bifidum, B. infantis, B. longum, B. subtilis, and S. thermophilus.) 6 × 109 CFU Daily | 30 days | Not reported | Not reported | No significant change in rating of perceived exertion and HR | No significant change in salivary antimicrobial proteins (a measure of mucosal protection) |
Salehzadeh (2015) [45] | Endurance athletes (n = 30) | 30 M 21 y | 200 ml of probiotic yogurt drink S. thermophilus or L. delbrueckii ssp. bulgaricus 1 × 105 CFU/g Daily | 30 days | Intense aerobic training | Not reported | Significant increase in VO2 MAX and aerobic power | Significant decrease in serum CRP, significant increase in HDL |
O’Brien et al. (2015) [74] | Male and female runners (n = 67) | Not reported 18–24 y | Kefir beverage (probiotic strain and amount not indicated) 2x week | 15 weeks | Marathon training program | Not reported | No effect on 1.5 mile run test times | Attenuated increase in inflammation (serum CRP) |
Gill et al. (2016a) [75] | Endurance-trained runners (n = 8) | 8 M 26 ± 6 y | L. casei 10 × 1010 CFU Daily | 7 days | Running exercise in hot ambient temperature | Refrained from alcohol and caffeine for 72 h and exercise for 24 h before preliminary testing sessions and each experimental trial | No difference in exercise performance on a treadmill test and perception of effort | No improvement in salivary antimicrobial protein (mucosal immune protection) or cortisol status over placebo |
Gill et al. (2016b) [76] | Endurance-trained runners (n = 8) | 8 M 26 ± 6 y | L. casei 10 × 1010 CFU Daily | 7 days | Running exercise in hot ambient temperature | Consumption of other probiotics was prohibited outside the study protocol | Not reported | Did not prevent increases in external heat stress-induced circulatory endotoxin concentration or plasma cytokine profile compared with placebo |
Jäger et al. (2016) [42] | Recreationally-trained individuals (n = 29) | 29 M 21.5 ± 2.8 y | B. coagulans GBI-30, 6086 (BC30), 1 × 109 CFU plus 20 g of casein protein Daily | 2 weeks | Muscle-damaging single leg training bout | Subjects provided a standardized meal prior to exercise bout. Three-day dietary recalls were collected | Significantly increased recovery and decreased soreness. Non-significant trend to increase power | Not assessed |
Jäger et al. (2016) [43] | Resistance-trained men (n = 15) | 15 M 25 ± 4 y | B. breve BR03 5 × 109 live cells (AFU) & S. thermophilus FP4 5 × 109 live cells (AFU) Daily | 3 weeks | Normal training up until 72 h preceding muscle-damaging elbow flexor exercise challenge | Refrain from any nutritional supplements or ergogenic aids | Improved isometric average peak torque production and range-of-motion during acute recovery | Significant decrease in marker of inflammation (IL-6) |
Roberts et al. (2016) [77] | Recreational triathletes (n = 30) | 25 M / 5 F 35 ± 1 y | Multi-strain pro/prebiotic/antioxidant 30 × 109 CFU per day containing 10 × 109 CFU L. acidophilus CUL-60 (NCIMB 30157), 10 × 109 CFU L. acidophillus CUL-21 (NCIMB 30156), 9.5 × 109 CFU B. bifidum CUL-20 (NCIMB 30172) and 0.5 × 109 CFU B. animalis subsp. lactis CUL-34 (NCIMB 30153)/55.8 mg fructooligosaccharides/ 400 mg alpha-lipoic acid, 600 mg N-acetyl-carnitine Daily | 12 weeks | Progressive triathlon training program | Maintained habitual dietary intake. Required not to consume any other nutritional supplement | No significant difference in race times | Significant reduction in endotoxin levels |
Strasser et al. (2016) [78] | Trained athletes (n = 29) | 13 M / 16 F 26.7 ± 3.5 y | Multi-species probiotic (B. bifidum W23, B. lactis W51, E. faecium W54, L. acidophilus W22, L. brevis W63, and L. lactis W58) 1 × 1010 CFU/g Daily | 12 weeks | Winter training | Maintain normal diet and avoid anti-inflammatory drugs, antibiotics, additional probiotics and dietary supplements | Did not benefit athletic performance | Limited exercise-induced drops in tryptophan levels and reduced the incidence of URTI |
Michalickova et al. (2016) [79] | Elite athletes (badminton, triathlon, cycling, alpinism, karate, savate, kayak, judo, tennis and swimming) (n = 39) | 29 M / 10 F 23.15 ± 2.6 y | L. helveticus Lafti L10, 2 × 1010 CFU Daily | 14 weeks | Normal training load (during winter) | Subjects maintained normal diet and were asked to avoid fermented milk products and immunomodulatory supplements | No significant differences in exercise performance | Significant reduction in duration of URTI episodes and decreased symptoms in elite athletes |
Gleeson et al. (2016) [80] | College athletes (n = 243) | 142M / 101F 20.4 ± 0.2 y | Fermented milk beverage containing L. casei Shirota, 6.5 × 109 CFU 2x daily | 20 weeks | Normal training load | Supplements that might influence immune function and additional probiotics or fermented dairy were not permitted | Not assessed | Significant reduction in cytomegalovirus and Epstein Barr virus antibody titres, benefiting immune status |
Michalickova et al. (2017) | Elite athletes (badminton, triathlon, bicycling, athletics, karate, kayaking, and judo) (n = 30) | 24 M / 6 F 23.6 ± 1.9 y | L. helveticus Lafti L10, 2 × 1010 CFU Daily | 14 weeks | Normal training load (winter training) | Subjects maintained normal diet and were asked to avoid fermented milk products and immunomodulatory supplements | Not assessed | Supported humoral and mucosal immunity by preserving total salivary Immunoglobulin A level |
Gepner et al. (2017) | Soldiers from elite combat unit (n = 26) | 26 M 20.5 ± 0.8 y | B. coagulans GBI-30 (BC30) 1.0 × 109 CFU and HMB 3 g Daily | 40 days | Strenuous military training 40 days | No additional dietary supplements nor consumtion any androgens or other performance-enhancing drugs | Not assessed | Combined supplementation attenuated IL-6 and IL-10 response and maintained muscle integrity |
Marshall et al. (2017) [81] | Marathon competitors (n = 32) | 26 M / 6 F 23–53 y | PRO-grp: Multi-strain capsule; L. acidophilus CUL-60 10 × 109 CFU, and L. acidophillus CUL-21 (NCIMB 30156) 10 × 109 CFU), B. bifidum CUL-20 9.5 × 109 CFU and B. animalis subsp. lactis CUL-34 0.5 × 109 CFU, and 55.8 mg fructooligosaccharides. PGLn-grp: L. acidophilus CUL-60 (NCIMB 30157) 2 × 109 CFU, L. acidophilus CUL-21 (NCIMB 30156) 2 × 109, B. bifidum CUL-20 (NCIMB 30172) 0.5 × 109 CFU, B. animalis subsp. lactis CUL-34 (NCIMB 30153) 0.95 × 109 CFU, L. salivarius CUL61 (NCIMB 30211) 5 × 109 CFU, and each 5-g dose also contained 0.9 g L-glutamine. Daily | 12 weeks | Marathon training; Marathon race | Not permitted to consume any other commercial supplementation that conflicted with the study parameters | No difference in marathon time to completion compared to control group | No change in immuno-stimulatory heat shock protein (eHsp72) concentrations |
Toohey et al. (2018) [20] | Soccer and volleyball Division I college athletes (n = 23) | 23 F 19.6 ± 1.0 y | B. subtilis (DE111) 5 × 109 CFU Daily | 10 weeks | Offseason resistance training program | No dietary restrictions were placed on the athletes besides abstaining from other supplement use | No effect on physical performance parameters | Significant reduction in body fat percentage |
Brennan et al. (2018) [82] Abstract of 2018 ACSM Confer. | Endurance athletes (n = 7) | (sex not reported) 31 ± 6.1 y | L. salivarius (UCC118) (dose not indicated) Daily | 4 weeks | Not reported | Not reported | Not assessed | Exercise-induced intestinal hyperpermeability was attenuated |
Townsend et al. (2018) [83] | Division I Baseball Players (n = 25) | 25 M 20.1 ± 1.5 y | B. subtilis (DE111) 1 × 109 CFU Daily | 12 weeks | Offseason training | Three-day food logs collected on weeks 1, 9 and 12. | No effect on physical performance or body composition | TNF-α concentrations were significantly lower compared to placebo |
Antonio et al. (2018) [84] | Active men and women (n = 20) | 6 M/ 14 F 30 ± 8 y | B. breve BR03 5 × 109 CFU and S. thermophilus FP4 5 × 109 CFU Daily | 6 weeks | Normal training load (aerobic and/or resistance training) | Subjects were instructed to not alter their diet | No effect on body composition | Not assessed |
Huang et al. (2018) [85] | Healthy adults without professional athletic training (n = 16) | 16 M 20–40 y | L. plantarum TWK10 1 × 1011 CFU Daily | 6 weeks | Not reported | Normal diet maintained and no consumption of any other nutritional supplements | Improved endurance performance and blood glucose concentration in a maximal treadmill running test | Not assessed |
Carbuhn et al. (2018) [86] | Division I collegiate female swimmers (n = 17) | 17 F Age not reported | B. longum 35,624, 1 × 109 CFU Daily | 6 weeks | Offseason training | Three-day food logs collected at baseline and weeks 3 and 6. | No effect on aerobic/anaerobic swim time trials and force plate vertical jump | No effect on cytokine and gastrointestinal inflammatory markers and salivary IgA levels |
Huang et al. (2019) [87] | Healthy adult triathletes (n = 34) | Study 1: 18 M, 20.2 ± 0.7 y Study 2: 16 M, 22.3 ± 1.2 y | L. plantarum PS128 3 × 1010 CFU Daily | Study 1: 4 weeks Study 2: 3 weeks | Sprint triathlon (swimming 750 m, biking 20 km, running 5 km). | Before race: 595 kcal (24 g PRO, 16 g FAT, 90 g CHO). In race: 30–40 g CHO and 500–1000 ml water per hour. | Attenuated post-triathlon performance declines. No effect on body composition. | Reduced post-race inflammatory cytokines, reduced oxidative stress, increased plasma BCAA levels. |
Pugh et al. (2019) [88] | Health adult marathon runners (ran marathon race quicker than 5 h within the previous 2 years; n = 24) | 20 M / 4 F 34.8 ± 6.9 y | L. acidophilus (CUL60 and CUL21), B. bifidum (CUL20), B. animalis subs p. Lactis (CUL34) > 25 billion CFU daily in total, no information on individual strains | 4 weeks (pre-race) | Marathon race | Before race: standardized high CHO, low fiber diet. In race: 60 mL CHO gel with 200 mL (15 min before start, 40 min post and every 20 min for the remainder of the race. | No difference in race times. | GI symptom severity during the final third was significantly lower. |
Pumpa et al. (2019) [89] | Elite rugby union athletes (n = 19) | 19 M 27.0 ± 3.2 y | L. rhamnosus, L. casei, L. acidophilus, L. plantarum, L. fermentum, B. lactis, B. bifidum, S. thermophilus 120 billion CFU daily in total, no information on individual strains 500 mg S. boulardi (added during stage 3) | 17 weeks | 27-weeks, divided into three stages: 1) control period (10 weeks); 2) domestic competition (7 weeks); 3) international competition (10 weeks). | A national training camp and 3 domestic games (stage one), 6-weeks of domestic competition (stage two), and 8-weeks of international competition (stage three). | Not assessed | No effect on salivary Immunoglobulin A. Salivary cortisol increased. Increase in salivary alpha-amylase levels during stage 3. |
Vaisberg et al. (2019) [90] | Amateur marathon runners with previous history of post-race URTI (n = 42) | 42 M 39.5 ± 9.4 y | Fermented milk beverage containing L. casei Shirota, 4 × 1010 CFU Daily | 30 days (pre-race) | Marathon race | Unknown | Not assessed | Improved airway and systemic immune and inflammatory responses post-marathon. No significant effect on URTI. |