Probiotic consumption and inflammatory markers in athletes: a systematic review and meta-analysis

Figures & data

Figure 1. The flow diagram of study selection.

*The work of Huang et al. was divided into two different studies.

Table 1. Characteristics of included trials.

First author (publication year)	Year of publication	Country	Total Sample size (M/F)	Mean age (year)	Mean BMI (kg/m^2)	RCT design (blinding)	Duration	Intervention of experimental group	Intervention of control group	Number of bacteria	VO2max	Exercise mode	Measured outcomes	Quality score
Jager et al.^[Citation5]	2016	USA	15 M	25	25.66	Crossover (Yes)	3 wk	Probiotic capsule (Streptococcus thermophilus 5 × 10^19 CFU+ Bifidobacterium breve 5 × 10^19 CFU)	Placebo capsule	2	-	Anaerobic exercise	IL-6 ↔	Low
Townsend et al.^[Citation27]	2018	USA	25 M	20.1	25.07	Parallel (Yes)	12 wk	Probiotic capsule (Bacillis subtilis) 1.2 × 10^9 CFU	Placebo capsule	1	-	Anaerobic exercise	IL-10 ↔ TNF-α ↔	High
Brennan et al.^[Citation28]	2018	USA	5/2	31	24.55	Crossover (Yes)	4 wk	Probiotic capsule (Lactobacillus Salivarius)	Placebo capsule	1	57.9	Aerobic exercise	IL-6 ↓	High
Pugh et al.^[Citation21]	2019	UK	20/4	35.4	-	Parallel (Yes)	4 wk	Probiotic capsule (Lactobacillusacidophilus, Bifidobacterium bifidum, Bifidobacterium animalis) 25 × 10^9 CFU	Placebo capsule	4	57	Aerobic exercise	IL-6 ↔ IL-10 ↔ IL-8 ↔	High
Gleeson et al.^[Citation17]	2011	UK	54/30	27	23.25	Parallel (Yes)	16 wk	Probiotic drink (Lactobacillus casei shirota) 6.5 × 10^9 CFU	Placebo drink	1	-	Aerobic exercise	IL-6 ↓ IL-10 ↔ IFN-γ ↔ TNF-α ↔	High
Cox et al.^[Citation15]	2010	Australia	20 M	27.3	-	Crossover (Yes)	4 wk	Probiotic capsule (Lactobacillus fermentum) 2 × 10^9 CFU	Placebo capsule	1	67.1	Aerobic exercise	IFN-γ ↑	High
Shing et al.^[Citation22]	2014	Australia	10 M	27	-	Crossover (Yes)	4 wk	Probiotic capsule (Lactobacillusacidophilus, Lactobacillusrhamnosus, Lactobacillus casei, Lactobacillus plantarum, Lactobacillus fermentum, Bifidobacteriumlactis, Bifidobacterium breve, Bifidobacterium bifidum, Streptococcus thermophilus) 45 × 10^9 CFU	Placebo capsule	9	-	Anaerobic exercise	IL-6 ↔ IL-10 ↔ TNF-α ↔	High
Huang et al.^[Citation1,Citation29]	2019	Taiwan	18 M	20.65	22.3	Randomized (Yes)	4 wk	Probiotic capsule (Lactobacillus plantarum 1.5 × 10^10 CFU+ Bifidobacterium breve 5 × 10^19 CFU) twice/day	Placebo capsule	1	-	Aerobic exercise	IL-6 ↔ IL-10 ↔ IL-8 ↔ TNF-α ↔ IFN-γ ↔	High
Huang et al.^[Citation2,Citation29]	2019	Taiwan	16 M	21.2	22.4	Randomized (Yes)	3 wk	Probiotic capsule (Lactobacillus plantarum 1.5 × 10^10 CFU) twice/day	Placebo capsule	1	60.95	Aerobic exercise	IL-6 ↔ IL-10 ↔ IL-8 ↔ TNF-α ↓ IFN-γ ↔	High
Gepner et al.^[Citation16]	2017	Israel	26 M	20	-	Parallel (Yes)	6 wk	Probiotic capsule (Bacillus coagulans 1 × 10^9 CFU)	Placebo capsule	1	-	Anaerobic exercise	TNF-α ↔ IL-6 ↓ IL-10 ↔ IFN-γ ↔	Low
Marinkovic et al.^[Citation20]	2016	Serbia	36/14	23.15	22.9	Parallel (Yes)	14 wk	Probiotic capsule (Lactobacillus helveticus 2 × 10^10 CFU)	Placebo capsule	1	56.65	Aerobic exercise	IL-10 ↔ IFN-γ ↔	High
Mazani et al.^[Citation4]	2018	Iran	27 F	18–25	23.21	Parallel (Yes)	2 wk	Probiotic yogurt	Regular yogurt	NS	34.55	Anaerobic exercise	TNF-α ↔ IL-6 ↔	High
Lamprecht et al.^[Citation19]	2012	Austria	23 M	37.9	23.8	Parallel (Yes)	14 wk	Probiotic powder (Bifidobacterium bifidum, Bifidobacteriumlactis, Enterococcus faecium, Lactobacillusacidophilus, Lactobacillus brevis, Lactococcus lactis) 1 × 10^10 CFU	Placebo powder	6	50.75	Anaerobic exercise	TNF-α ↔ IL-6 ↔	High
Ibrahim et al.^[Citation18]	2018	Malaysia	48 M	22	21.52	Parallel (Yes)	12 wk	Probiotic powder (Lactobacillusacidophilus, Lactobacillus casei, Lactococcus lactis, Bifidobacterium bifidum, Bifidobacterium infantis, Bifidobacterium longum) 3 × 10^10 CFU	Placebo powder	6	-	Anaerobic exercise	IL-6 ↓ IL-10 ↔	High

M, male; F, female; RCT, randomized controlled trial; IL-6, interleukin-6; IL-10, interleukin-10; TNF-α, tumor necrosis factor-alpha; IFN-γ, interferon gamma; CFU, colony-forming unit

Table 2. Subgroup analysis to assess the effect of probiotic consumption on lipid inflammatory markers.

Sub-grouped by	No. of trials	Effect size	95% CI	I^2 (%)	P for heterogeneity	P for between subgroup heterogeneity
IFN-γ
Duration of intervention						0.029
<4 weeks	2	1.001	0.38, 1.61	94	˂0.001
≥4 weeks	2	0.18	−0.21, 0.58	0.0	0.75
Geographical location						0.15
Asian	3	0.71	0.2, 1.22	89.8	˂0.001
Non-Asian	1	0.21	−0.23, 0.65	-	-
IL-6
Duration of intervention						0.61
<4 weeks	4	−0.50	−0.91, −0.09	0.0	0.91
≥4 weeks	5	−0.65	−1.07, −0.23	48.8	0.09
Geographical location						0.28
Asian	5	−0.72	−1.13, −0.32	0.0	0.65
Non-Asian	4	−0.40	−0.83, 0.20	39.7	0.17
Number of used strain						0.30
Multi	5	−0.45	−0.83, −0.07	30.5	0.21
Single	4	−0.76	−1.24, −0.29	0.0	0.62
Gender						0.938
Male	6	−0.56	−0.92, −0.20	16.2	0.309
Female	1	−0.49	−1.26, 0.27	-	-
Both	2	−0.67	−1.37, 0.02	59.5	0.116
Exercise mode						0.473
Aerobic	4	−0.72	−1.21, −0.22	0.0	0.475
Anaerobic	5	−0.49	−0.86, −0.12	27.9	0.235
IL-10
Duration of intervention						0.99
<4 weeks	2	−0.04	−0.69, 0.59	0.0	0.58
≥4 weeks	4	−0.05	−0.38, 0.27	0.0	0.85
Geographical location						0.72
Asian	3	0.03	−0.50, 0.56	0.0	0.65
Non-Asian	3	−0.08	−0.43, 0.26	0.0	0.95
Number of used strain						0.39
Multi	2	−0.24	−0.85, 0.36	0.0	0.89
Single	4	0.008	−0.32, 0.34	0.0	0.91
Gender						0.741
Male	4	0.005	−0.43, 0.44	0.0	0.832
Female	0	-	-	-	-
Both	2	−0.09	−0.49, 0.29	0.0	0.777
Exercise mode						0.681
Aerobic	4	−0.01	−0.35, 0.32	0.0	0.865
Anaerobic	2	−0.15	−0.73, 0.42	0.0	0.693
TNF-α
Duration of intervention						0.85
<4 weeks	2	−0.76	−1.38, −0.14	0.0	0.58
≥4 weeks	3	−0.69	−1.18, −0.19	0.0	0.9
Geographical location						0.70
Asian	3	−0.78	−1.31, −0.26	0.0	0.85
Non-Asian	2	−0.63	−1.21, −0.05	0.0	0.78
Number of used strain						0.90
Multi	1	−0.72	−1.56, 0.12	-	-
Single	4	−0.71	−1.15, −0.27	0.0	0.9
Gender						0.803
Male	4	−0.74	−1.19, −0.29	0.0	0.923
Female	1	−0.63	−1.40, 0.14	-	-
Both	0	-	-	-	-
Exercise mode						0.516
Aerobic	2	−0.91	−1.62, −0.20	0.0	0.830
Anaerobic	3	−0.63	−1.09, −0.16	0.0	0.963

IL-6, interleukin-6; IL-10, interleukin-10; TNF-α, tumor necrosis factor-alpha; IFN-γ, interferon gamma

Figure 2. Forest plot of the effect of probiotic consumption on IFN-γ.

Figure 3. Forest plot of the effect of probiotic consumption on IL-6.

Figure 4. Forest plot of the effect of probiotic consumption on IL-8.

Figure 5. Forest plot of the effect of probiotic consumption on IL-10.

Figure 6. Forest plot of the effect of probiotic consumption on TNF-α.

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