Int J Sports Med 2021; 42(09): 769-781
DOI: 10.1055/a-1463-3303
Review

Effect of Probiotic Consumption on Immune Response in Athletes: A Meta-analysis

Rahele Tavakoly
1   Student Research Committee, Faculty of Public Health, Kerman University of Medical Sciences, Kerman, Iran (the Islamic Republic of)
2   Nutrition Research Center, School of Nutrition and Food Sciences, Shiraz University of Medical Sciences, Shiraz, Iran (the Islamic Republic of)
,
Amir Hadi
3   Department of Clinical Nutrition, School of Nutrition and Food Science, Food Security Research Center, Isfahan University of Medical Sciences, Isfahan, Iran (the Islamic Republic of)
,
Nahid Rafie
3   Department of Clinical Nutrition, School of Nutrition and Food Science, Food Security Research Center, Isfahan University of Medical Sciences, Isfahan, Iran (the Islamic Republic of)
,
Behrouz Talaei
1   Student Research Committee, Faculty of Public Health, Kerman University of Medical Sciences, Kerman, Iran (the Islamic Republic of)
4   Department of Nutrition, school of Public Health, Kerman University of Medical Sciences, Kerman, Iran (the Islamic Republic of)
,
Wolfgang Marx
5   Deakin University, IMPACT - the Institute for Mental and Physical Health and Clinical Translation, Food & Mood Centre, School of Medicine, Barwon Health, Geelong, Australia
,
Arman Arab
6   Department of Community Nutrition, School of Nutrition and Food Science, Food Security Research Center, Isfahan University of Medical Sciences, Isfahan, Iran (the Islamic Republic of)
› Author Affiliations

Abstract

The possible effect of probiotic interventions on immunological markers in athletes is inconclusive. Therefore, to synthesize and quantitatively analyze the existing evidence on this topic, systematic literature searches of online databases PubMed, Scopus, Cochrane Library, and ISI Web of Sciences was carried out up to February 2021 to find all randomized controlled trials (RCTs) concerning the immunological effects of probiotics in athletes. In the random-effects model, weighted mean difference (WMD) and 95% confidence interval (CI) explained the net effect. The authors assessed the likelihood of publication bias via Egger’s and Begg’s statistics. A total of 13 RCTs (836 participants) were retrieved. Probiotic consumption reduced lymphocyte T cytotoxic count significantly (WMD=−0.08 cells×109/L; 95% CI: −0.15 to −0.01; p=0.022) with evidence of moderate heterogeneity (I 2=59.1%, p=0.044) and monocyte count when intervention duration was ≤ 4 weeks (WMD=−0.08 cells×109/L; 95% CI: −0.16 to −0.001; I 2=0.0%). Furthermore, leukocyte count was significantly elevated (WMD=0.48 cells×109/L; 95% CI: 0.02 to 0.93; I 2=0.0%) when multi-strain probiotics were used. Probiotic supplements may improve immunological markers, including lymphocyte T cytotoxic, monocyte, and leukocyte in athletes. Further randomized controlled trials using diverse strains of probiotics and consistent outcome measures are necessary to allow for evidence-based recommendations.

Supplementary Material



Publication History

Received: 03 November 2020

Accepted: 17 March 2021

Article published online:
30 April 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Walsh NP, Gleeson M, Shephard RJ. et al. Position statement part one: immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63
  • 2 Nazari M, Faghfoori Z, As’Habi A. et al. Probiotic consumption and inflammatory markers in athletes: A systematic review and meta-analysis. Int J Food Prop 2020; 23: 1402-1415 doi:10.1080/10942912.2020.1807566
  • 3 As’Habi A, Nazari M, Hajianfar H. et al. A systematic review and meta-analysis of probiotic consumption and metabolic status of athletes. Int J Food Prop 2020; 23: 941-954 doi:10.1080/10942912.2020.1772286
  • 4 Soligard T, Steffen K, Palmer D. et al. Sports injury and illness incidence in the Rio de Janeiro 2016 Olympic Summer Games: A prospective study of 11274 athletes from 207 countries. Br J Sports Med 2017; 51: 1265-1271
  • 5 Hackney AC. Clinical management of immuno-suppression in athletes associated with exercise training: sports medicine considerations. Acta Med Iran 2013; 751-756
  • 6 Wang Y, Wu Y, Wang Y. et al. Antioxidant properties of probiotic bacteria. Nutrients 2017; 9: 521
  • 7 Granato D, Nazzaro F, Pimentel TC. et al. Probiotic food development : an updated review based on technological advancement. Ferranti P, Berry EM, Anderson JR. (Eds) robiotic food development : an updated review based on technological advancement Encyclopedia of Food Security and Sustainability. Elsevier: 2019: 422-428
  • 8 Brown AC, Valiere A. Probiotics and medical nutrition therapy. Nutr Clin Care: An official publication of Tufts University. 2004; 7: 56–58
  • 9 Szajewska H, Skorka A, Ruszczyński M. et al. Meta-analysis: L actobacillus GG for treating acute gastroenteritis in children–updated analysis of randomised controlled trials. Aliment Pharmacol Ther 2013; 38: 467-476
  • 10 Chan CK, Tao J, Chan OS. et al. Preventing respiratory tract infections by synbiotic interventions: A systematic review and meta-analysis of randomized controlled trials. Adv Nutr 2020; 11: 979-988 doi:10.1093/advances/nmaa003
  • 11 Pyne DB, West NP, Cox AJ. et al. Probiotics supplementation for athletes–clinical and physiological effects. Eur J Sport Sci 2015; 15: 63-72
  • 12 Gleeson M, Bishop NC, Oliveira M. et al. Daily probiotic’s (Lactobacillus casei Shirota) reduction of infection incidence in athletes. Int J Sport Nutr Exerc Metab 2011; 21: 55-64
  • 13 Gleeson M, Bishop NC, Oliveira M. et al. Effects of a Lactobacillus salivarius probiotic intervention on infection, cold symptom duration and severity, and mucosal immunity in endurance athletes. Int J Sport Nutr Exerc Metab 2012; 22: 235-242
  • 14 Fleming PS, Koletsi D, Pandis N. Blinded by PRISMA: Are systematic reviewers focusing on PRISMA and ignoring other guidelines?. PLoS One 2014; 9: e96407
  • 15 Harriss D, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
  • 16 Higgins JP, Altman DG, Gøtzsche PC. et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011; 343: d5928
  • 17 Ryan R, Hill S. How to GRADE the quality of the evidence. Cochrane Consumers and Communication Group, 2016. Available at http://cccrg.cochrane.org/author-resources
  • 18 McHugh ML. The odds ratio: calculation, usage and interpretation. Biochemia Medica 2009; 19: 120-126
  • 19 Follmann D, Elliott P, Suh I. et al. Variance imputation for overviews of clinical trials with continuous response. J Clin Epidemiol 1992; 45: 769-773
  • 20 Green S, Higgins J. Cochrane Handbook for Systematic Reviews of Interventions 4.2. 5. https://training.cochrane.org/handbook. May. 2005
  • 21 Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions. John Wiley & Sons; 2011
  • 22 Saltelli A, Aleksankina K, Becker W. et al. Why so many published sensitivity analyses are false: A systematic review of sensitivity analysis practices Environ Model. Softw 2019; 114: 29-39
  • 23 Augusteijn HE, van Aert R, van Assen MA. The effect of publication bias on the Q test and assessment of heterogeneity. Psychol Methods 2019; 24: 116–134
  • 24 Shing CM, Peake JM, Lim CL. et al. Effects of probiotics supplementation on gastrointestinal permeability, inflammation and exercise performance in the heat. Eur J Appl Physiol 2014; 114: 93-103 doi:10.1007/s00421-013-2748-y
  • 25 Cox AJ, Pyne DB, Saunders PU. et al. Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. Br J Sports Med 2010; 44: 222-226 doi:10.1136/bjsm.2007.044628
  • 26 Dönmez N, Kisadere I, Balaban C. et al. Effects of traditional homemade koumiss on some hematological and biochemical characteristics in sedentary men exposed to exercise. Biotech Histochem 2014; 89: 558-563 doi:10.3109/10520295.2014.915428
  • 27 Ibrahim NS, Ooi FK, Chen CK. et al. Effects of probiotics supplementation and circuit training on immune responses among sedentary young males. J Sports Med Phys Fitness 2018; 58: 1102-1109 doi:10.23736/s0022-4707.17.07742-8
  • 28 Pumpa KL, McKune AJ, Harnett J. A novel role of probiotics in improving host defence of elite rugby union athlete: A double blind randomised controlled trial. J Sci Med Sport 2019; 22: 876-881 doi:10.1016/j.jsams.2019.03.013
  • 29 Tiollier E, Chennaoui M, Gomez-Merino D. et al. Effect of a probiotics supplementation on respiratory infections and immune and hormonal parameters during intense military training. Mil Med 2007; 172: 1006-1011 doi:10.720 milmed.172.9.1006
  • 30 Townsend JR, Bender D, Vantrease WC. et al. Effects of Probiotic (Bacillus subtilis DE111) Supplementation on Immune Function, Hormonal Status, and Physical Performance in Division I Baseball Players. Sports (Basel) 2018; 6 doi:10.3390/sports6030070
  • 31 Sawada D, Kuwano Y, Tanaka H. et al. Daily intake of Lactobacillus gasseri CP2305 relieves fatigue and stress-related symptoms in male university Ekiden runners: A double-blind, randomized, and placebo-controlled clinical trial. J Funct Foods 2019; 57: 465-476
  • 32 Carbuhn AF, Reynolds SM, Campbell CW. et al. Effects of probiotic (Bifidobacterium longum 35624) supplementation on exercise performance, immune modulation, and cognitive outlook in Division I female swimmers. Sports (Basel) 2018; 6: 116
  • 33 Gleeson M, Bishop NC, Oliveira M. et al. Effects of a Lactobacillus salivarius probiotic intervention on infection, cold symptom duration and severity, and mucosal immunity in endurance athletes. Int J Sport Nutr Exerc Metab 2012; 22: 235-242
  • 34 Gleeson M, Bishop NC, Oliveira M. et al. Daily probiotic's (Lactobacillus casei Shirota) reduction of infection incidence in athletes. Int J Sport Nutr Exerc Metab 2011; 21: 55-64
  • 35 Gleeson M, Bishop NC, Struszczak L. Effects of Lactobacillus casei Shirota ingestion on common cold infection and herpes virus antibodies in endurance athletes: a placebo-controlled, randomized trial. Eur J Appl Physiol 2016; 116: 1555-1563 doi:10.1007/s00421-016-3415-x
  • 36 Michalickova D, Minic R, Dikic N. et al. Lactobacillus helveticus Lafti L10 supplementation reduces respiratory infection duration in a cohort of elite athletes: a randomized, double-blind, placebo-controlled trial. Appl Physiol Nutr Metab 2016; 41: 782-789 doi:10.1139/apnm-2015-0541
  • 37 Michalickova DM, Kostic-Vucicevic MM, Vukasinovic-Vesic MD. et al. Lactobacillus helveticus Lafti L10 Supplementation Modulates Mucosal and Humoral Immunity in Elite Athletes: A Randomized, Double-Blind, Placebo-Controlled Trial. J Strength Cond Res 2017; 31: 70-62 doi:10.1519/jsc.0000000000001456
  • 38 Moreira A, Kekkonen R, Korpela R. et al. Allergy in marathon runners and effect of Lactobacillus GG supplementation on allergic inflammatory markers. Respir Med 2007; 101: 1123-1131 doi:10.1016/j.rmed.2006.11.015
  • 39 Cox AJ, West NP, Horn PL. et al. Effects of probiotic supplementation over 5 months on routine haematology and clinical chemistry measures in healthy active adults. Eur J Clin Nutr 2014; 68: 1255-1257. doi:10.1038/ejcn.2014.137
  • 40 Morshedi M, Hashemi R, Moazzen S. et al. Immunomodulatory and anti-inflammatory effects of probiotics in multiple sclerosis: A systematic review. J Neuroinflammation 2019; 16: 231
  • 41 Aqaeinezhad Rudbane SM, Rahmdel S, Abdollahzadeh SM. et al. The efficacy of probiotic supplementation in rheumatoid arthritis: A meta-analysis of randomized, controlled trials. Inflammopharmacology 2018; 26: 67-76 doi:10.1007/s10787-017-0436-y
  • 42 Marteau P. Evidence of probiotic strain specificity makes extrapolation of results impossible from a strain to another, even from the same species. Annals of Gastroenterology and Hepatology 2011; 2: 1-3
  • 43 McFarland LV, Evans CT, Goldstein EJC. Strain-specificity and disease-specificity of probiotic efficacy: A systematic review and meta-analysis. Front Med (Lausanne) 2018; 5: 124. doi:10.3389/fmed.2018.00124
  • 44 Ibrahim NS, Ooi FK, Chen CK. et al. Effects of probiotics supplementation and circuit training on immune responses among sedentary young males. J Sports Med Phys Fitness 2018; 58: 1102-1109
  • 45 Shephard RJ. Development of the discipline of exercise immunology. Exerc Immunol Rev 2010; 16: 194-222
  • 46 Soligard T, Steffen K, Palmer D. et al. Sports injury and illness incidence in the Rio de Janeiro 2016 Olympic summer games: A prospective study of 11274 athletes from 207 countries. Br J Sports Med 2017; 51: 1265-1271
  • 47 Harris MD. Infectious disease in athletes. Curr Sports Med Rep 2011; 10: 84-89
  • 48 Ahmadinejad Z, Alijani N, Mansori S. et al. Common sports-related infections: A review on clinical pictures, management and time to return to sports. Asian J Sports Med 2014; 5: 1–9
  • 49 Bull-Otterson L, Feng W, Kirpich I. et al. Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of Lactobacillus rhamnosus GG treatment. PLoS One 2013; 8: e53028
  • 50 Möller GB, da Cunha Goulart MJV, Nicoletto BB. et al. Supplementation of probiotics and its effects on physically active individuals and athletes: Systematic review. Int J Sport Nutr Exerc Metab 2019; 29: 481-492
  • 51 Pyne DB, West NP, Cripps AW. Probiotics and immune response to exercise. Am J Lifestyle Med 2013; 7: 51-59
  • 52 Mack D, Ahrné S, Hyde L. et al. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 2003; 52: 827-833
  • 53 Forsyth CB, Farhadi A, Jakate SM. et al. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 2009; 43: 163-172
  • 54 Erridge C, Kennedy S, Spickett CM. et al. Oxidized phospholipid inhibition of toll-like receptor (TLR) signaling is restricted to TLR2 and TLR4 roles for cd14, lps-binding protein, and md2 as targets for specificity of inhibition. J Biol Chem 2008; 283: 24748-24759
  • 55 Hadi A, Ghaedi E, Khalesi S. et al. Effects of synbiotic consumption on lipid profile: a systematic review and meta-analysis of randomized controlled clinical trials. Eur J Nutr 2020; 59: 2857-2874 doi:10.1007/s00394-020-02248-7
  • 56 Kwon H-K, Kim G-C, Kim Y. et al. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin immunol 2013; 146: 217-227
  • 57 Tankou SK, Regev K, Healy BC. et al. Investigation of probiotics in multiple sclerosis. Mult Scler 2018; 24: 58-63
  • 58 Lavasani S, Dzhambazov B, Nouri M. et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One 2010; 5: e9009
  • 59 De Filippo C, Cavalieri D, Di Paola M. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci 2010; 107: 14691-14696
  • 60 O'Toole PW, Claesson MJ. Gut microbiota: changes throughout the lifespan from infancy to elderly. Int Dairy J 2010; 20: 281-291
  • 61 Turnbaugh PJ, Hamady M, Yatsunenko T. et al. A core gut microbiome in obese and lean twins. Nature 2480 457: 009
  • 62 Modi SR, Collins JJ, Relman DA. Antibiotics and the gut microbiota. J Clin Invest 2014; 124: 4212-4218
  • 63 Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13: 701–712
  • 64 Conlon M, Bird A. The impact of diet and lifestyle on gut microbiota and human health. Nutrients 2015; 7: 17-44
  • 65 David LA, Maurice CF, Carmody RN. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505: 559–563
  • 66 Devkota S. Prescription drugs obscure microbiome analyses. Science 2016; 351: 452-453