Skip to main content
Log in

The Effects of Supplementation with Probiotic on Biomarkers of Oxidative Stress in Adult Subjects: a Systematic Review and Meta-analysis of Randomized Trials

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Previous studies have supposed that probiotic supplementation led to a positive effect on different health outcomes. Furthermore, several studies indicated that probiotics supplementation improved antioxidant status, while some studies did not indicate these effects. Hence, current systematic review and meta-analysis study was conducted to determine the effect of probiotic supplementation on some oxidative stress biomarkers among adult subjects. We searched four electronic databases PubMed, SCOPUS, ISI Web of Science, and the Cochrane Library till November 2017. Clinical trials that compared the effects of probiotic supplementation with the control group were included. A random-effect model was used to pool weighted mean difference (WMD). Finding of 11 included studies (n = 577) indicated that probiotic supplementation increased total antioxidant capacity (TAC) (WMD 77.30 mmol/L; 95% confidence interval [CI] 2.60, 152.01; I2 = 88.3%) and reduced malondialdehyde (MDA) (WMD − 0.31 μmol/L; 95% CI − 0.54, − 0.08; I2 = 71.5%) significantly compared to the control group. However, its effects on glutathione (GSH) was not significant (WMD = 19.32 μmol/L; 95% CI − 18.70, 57.33; I2 = 64.9%). The current meta-analysis revealed that probiotic supplementation may result in increasing TAC and lowering MDA, which improve antioxidant status. However, due to high heterogeneity, findings should be interpreted with caution. Further investigations are required to elucidate the effect of supplementation with probiotics on biomarkers of antioxidants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Devasagayam TP, Tilak JC, Boloor KK, Sane KS, Ghaskadbi SS, Lele RD (2004) Free radicals and antioxidants in human health: current status and future prospects. J Assoc Physicians India 52:794–804

    CAS  PubMed  Google Scholar 

  2. Ceriello A, Motz E (2004) Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 24(5):816–823. https://doi.org/10.1161/01.atv.0000122852.22604.78

    Article  CAS  PubMed  Google Scholar 

  3. Sosa V, Moline T, Somoza R, Paciucci R, Kondoh H, ME LL (2013) Oxidative stress and cancer: an overview. Ageing Res Rev 12(1):376–390. https://doi.org/10.1016/j.arr.2012.10.004

    Article  CAS  PubMed  Google Scholar 

  4. Halliwell B, Gutteridge JM (1990) The antioxidants of human extracellular fluids. Arch Biochem Biophys 280(1):1–8

    Article  CAS  PubMed  Google Scholar 

  5. Mazidi M, Rezaie P, Kengne AP, Mobarhan MG, Ferns GA (2016) Gut microbiome and metabolic syndrome. Diabetes Metab Syndr 10(2 Suppl 1):S150–S157. https://doi.org/10.1016/j.dsx.2016.01.024

    Article  PubMed  Google Scholar 

  6. Zuccotti GV, Meneghin F, Raimondi C, Dilillo D, Agostoni C, Riva E, Giovannini M (2008) Probiotics in clinical practice: an overview. J Int Med Res 36:1A–53A. https://doi.org/10.1177/14732300080360s101

    Article  PubMed  Google Scholar 

  7. Alipour B, Homayouni-Rad A, Vaghef-Mehrabany E, Sharif SK, Vaghef-Mehrabany L, Asghari-Jafarabadi M, Nakhjavani MR, Mohtadi-Nia J (2014) Effects of Lactobacillus casei supplementation on disease activity and inflammatory cytokines in rheumatoid arthritis patients: a randomized double-blind clinical trial. Int J Rheum Dis 17(5):519–527. https://doi.org/10.1111/1756-185x.12333

    Article  CAS  PubMed  Google Scholar 

  8. Saez-Lara MJ, Robles-Sanchez C, Ruiz-Ojeda FJ, Plaza-Diaz J, Gil A (2016) Effects of probiotics and synbiotics on obesity, insulin resistance syndrome, type 2 diabetes and non-alcoholic fatty liver disease: a review of human clinical trials. Int J Mol Sci 17 (6). doi:https://doi.org/10.3390/ijms17060928

  9. Mishra V, Prasad DN (2005) Application of in vitro methods for selection of Lactobacillus casei strains as potential probiotics. Int J Food Microbiol 103(1):109–115. https://doi.org/10.1016/j.ijfoodmicro.2004.10.047

    Article  PubMed  Google Scholar 

  10. Moro-Garcia MA, Alonso-Arias R, Baltadjieva M, Fernandez Benitez C, Fernandez Barrial MA, Diaz Ruisanchez E, Alonso Santos R, Alvarez Sanchez M, Saavedra Mijan J, Lopez-Larrea C (2013) Oral supplementation with Lactobacillus delbrueckii subsp. bulgaricus 8481 enhances systemic immunity in elderly subjects. Age 35(4):1311–1326. https://doi.org/10.1007/s11357-012-9434-6

    Article  CAS  PubMed  Google Scholar 

  11. Roberfroid MB (2000) Prebiotics and probiotics: are they functional foods? Am J Clin Nutr 71(6 Suppl):1682S–1687S discussion 1688S–1690S

    Article  CAS  PubMed  Google Scholar 

  12. Ouwehand AC, Tölkkö S, Kulmala J, Salminen S, Salminen E (2000) Adhesion of inactivated probiotic strains to intestinal mucus. Lett Appl Microbiol 31(1):82–86. https://doi.org/10.1046/j.1472-765x.2000.00773.x

    Article  CAS  PubMed  Google Scholar 

  13. Bergmann RSO, Pereira MA, Veiga SMOM, Schneedorf JM, Oliveira NMS, Fiorini JE (2010) Microbial profile of a kefir sample preparations: grains in natura and lyophilized and fermented suspension. Food Sci Technol 30:1022–1026

    Article  Google Scholar 

  14. Holzapfel WH (2002) Appropriate starter culture technologies for small-scale fermentation in developing countries. Int J Food Microbiol 75(3):197–212

    Article  CAS  PubMed  Google Scholar 

  15. Peran L, Camuesco D, Comalada M, Nieto A, Concha A, Adrio JL, Olivares M, Xaus J, Zarzuelo A, Galvez J (2006) Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int J Color Dis 21(8):737–746. https://doi.org/10.1007/s00384-005-0773-y

    Article  Google Scholar 

  16. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative strains as promising probiotics. Int J Food Microbiol 72(3):215–224. https://doi.org/10.1016/S0168-1605(01)00674-2

    Article  CAS  PubMed  Google Scholar 

  17. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 4:1. https://doi.org/10.1186/2046-4053-4-1

    Article  PubMed  PubMed Central  Google Scholar 

  18. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, McQuay HJ (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17(1):1–12

    Article  CAS  PubMed  Google Scholar 

  19. Anderson R, Hay I, Wyk H, Theron A (1983) Ascorbic acid in bronchial asthma. S Afr Med J 63(17):649–652

    CAS  PubMed  Google Scholar 

  20. Asemi Z, Zare Z, Shakeri H, Sabihi S, Esmaillzadeh A (2013) Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 63(1–2):1–9. https://doi.org/10.1159/000349922

    Article  CAS  PubMed  Google Scholar 

  21. Mazloom Z, Yousefinejad A, Dabbaghmanesh MH (2013) Effect of probiotics on lipid profile, glycemic control, insulin action, oxidative stress, and inflammatory markers in patients with type 2 diabetes: a clinical trial. Iran J Med Sci 38(1):38–43

    PubMed  PubMed Central  Google Scholar 

  22. Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H, Taghizadeh M, Memarzadeh M, Asemi Z, Esmaillzadeh A (2016) Clinical and metabolic response to probiotic administration in patients with major depressive disorder: a randomized, double-blind, placebo-controlled trial. Nutrition 32(3):315–320. https://doi.org/10.1016/j.nut.2015.09.003

    Article  CAS  PubMed  Google Scholar 

  23. Jamilian M, Bahmani F, Vahedpoor Z, Salmani A, Tajabadi-Ebrahimi M, Jafari P, Hashemi Dizaji S, Asemi Z (2016) Effects of probiotic supplementation on metabolic status in pregnant women: a randomized, double-blind, placebo-controlled trial. Arch Iran Med 19(10):687–692

    PubMed  Google Scholar 

  24. Soleimani A, Zarrati MM, Bahmani F, Taghizadeh M, Ramezani M, Tajabadi-Ebrahimi M, Jafari P, Esmaillzadeh A, Asemi Z (2016) Probiotic supplementation in diabetic hemodialysis patients has beneficial metabolic effects. Kidney Int 91:435–442. https://doi.org/10.1016/j.kint.2016.09.040

    Article  CAS  PubMed  Google Scholar 

  25. Vaghef-Mehrabany E, Homayouni-Rad A, Alipour B, Sharif S, Vaghef-Mehrabany L, Alipour-Ajiry S (2016) Effects of probiotic supplementation on oxidative stress indices in women with rheumatoid arthritis: a randomized double-blind clinical trial. J Am Coll Nutr 35(4):291–299. https://doi.org/10.1080/07315724.2014.959208

    Article  PubMed  Google Scholar 

  26. Zamani B, Golkar HR, Farshbaf S, Emadi-Baygi M, Tajabadi-Ebrahimi M, Jafari P, Akhavan R, Taghizadeh M, Memarzadeh MR, Asemi Z (2016) Clinical and metabolic response to probiotic supplementation in patients with rheumatoid arthritis: a randomized, double-blind, placebo-controlled trial. Int J Rheum Dis 19(9):869–879. https://doi.org/10.1111/1756-185x.12888

    Article  CAS  PubMed  Google Scholar 

  27. Badehnoosh B, Karamali M, Zarrati M, Jamilian M, Bahmani F, Tajabadi-Ebrahimi M, Jafari P, Rahmani E, Asemi Z (2017) The effects of probiotic supplementation on biomarkers of inflammation, oxidative stress and pregnancy outcomes in journal of maternal-fetal & neonatal medicine. J Matern Fetal Neonatal Med 31:1128–1136. https://doi.org/10.1080/14767058.2017.1310193

    Article  CAS  PubMed  Google Scholar 

  28. Gomes A, Sousa R, Botelho P, Gomes T, Prada P, Mota J (2017) The additional effects of a probiotic mix on abdominal adiposity and antioxidant status: a double-blind, randomized trial. Obesity 25(1):30–38. https://doi.org/10.1002/oby.21671

    Article  CAS  PubMed  Google Scholar 

  29. Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, Tajabadi-Ebrahimi M, Jafari P, Asemi Z (2017) Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Clin Nutr 36(5):1245–1249. https://doi.org/10.1016/j.clnu.2016.08.015

    Article  CAS  PubMed  Google Scholar 

  30. Mohseni S, Bayani M, Bahmani F, Tajabadi-Ebrahimi M, Bayani MA, Jafari P, Asemi Z (2017) The effects of probiotic administration on wound healing and metabolic status in patients with diabetic foot ulcer: a randomized, double-blind, placebo-controlled trial. Diabetes Metab Res Rev. https://doi.org/10.1002/dmrr.2970

  31. Paneni F, Costantino S, Cosentino F (2015) Role of oxidative stress in endothelial insulin resistance. World J Diabetes 6(2):326–332. https://doi.org/10.4239/wjd.v6.i2.326

    Article  PubMed  PubMed Central  Google Scholar 

  32. White PA, Oliveira RC, Oliveira AP, Serafini MR, Araujo AA, Gelain DP, Moreira JC, Almeida JR, Quintans JS, Quintans-Junior LJ, Santos MR (2014) Antioxidant activity and mechanisms of action of natural compounds isolated from lichens: a systematic review. Molecules 19(9):14496–14527. https://doi.org/10.3390/molecules190914496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lobo V, Patil A, Phatak A, Chandra N (2010) Free radicals, antioxidants and functional foods: impact on human health. Pharmacogn Rev 4(8):118–126. https://doi.org/10.4103/0973-7847.70902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Heshmati J, Farsi F, Shokri F, Rezaeinejad M, Almasi-Hashiani A, Vesali S, Sepidarkish M (2018) A systematic review and meta-analysis of the probiotics and synbiotics effects on oxidative stress. J Funct Foods 46:66–84

    Article  CAS  Google Scholar 

  35. Mohammadi AA, Jazayeri S, Khosravi-Darani K, Solati Z, Mohammadpour N, Asemi Z, Adab Z, Djalali M, Tehrani-Doost M, Hosseini M, Eghtesadi S (2015) Effects of probiotics on biomarkers of oxidative stress and inflammatory factors in petrochemical workers: a randomized, double-blind, placebo-controlled trial. Int J Prev Med 6:82. https://doi.org/10.4103/2008-7802.164146

    Article  PubMed  PubMed Central  Google Scholar 

  36. Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63(14):3615–3626. https://doi.org/10.1021/jf506326t

    Article  CAS  PubMed  Google Scholar 

  37. Aqaeinezhad Rudbane SM, Rahmdel S, Abdollahzadeh SM, Zare M, Bazrafshan A, Mazloomi SM (2018) The efficacy of probiotic supplementation in rheumatoid arthritis: a meta-analysis of randomized, controlled trials. Inflammopharmacology 26(1):67–76. https://doi.org/10.1007/s10787-017-0436-y

    Article  CAS  PubMed  Google Scholar 

  38. Samah S, Ramasamy K, Lim SM, Neoh CF (2016) Probiotics for the management of type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetes Res Clin Pract 118:172–182. https://doi.org/10.1016/j.diabres.2016.06.014

    Article  CAS  PubMed  Google Scholar 

  39. Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V (2012) Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition 28(5):539–543. https://doi.org/10.1016/j.nut.2011.08.013

    Article  CAS  PubMed  Google Scholar 

  40. Chapman CM, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 50(1):1–17. https://doi.org/10.1007/s00394-010-0166-z

    Article  CAS  PubMed  Google Scholar 

  41. Fujimori S, Tatsuguchi A, Gudis K, Kishida T, Mitsui K, Ehara A, Kobayashi T, Sekita Y, Seo T, Sakamoto C (2007) High dose probiotic and prebiotic cotherapy for remission induction of active Crohn's disease. J Gastroenterol Hepatol 22(8):1199–1204. https://doi.org/10.1111/j.1440-1746.2006.04535.x

    Article  PubMed  Google Scholar 

  42. Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D (2015) Role of the normal gut microbiota. World J Gastroenterol 21(29):8787–8803. https://doi.org/10.3748/wjg.v21.i29.8787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Li P, Zhou Q, Gu Q (2016) Complete genome sequence of Lactobacillus plantarum LZ227, a potential probiotic strain producing B-group vitamins. J Biotechnol 234:66–70. https://doi.org/10.1016/j.jbiotec.2016.07.020

    Article  CAS  PubMed  Google Scholar 

  44. Ashoori M, Saedisomeolia A (2014) Riboflavin (vitamin B(2)) and oxidative stress: a review. Br J Nutr 111(11):1985–1991. https://doi.org/10.1017/s0007114514000178

    Article  CAS  PubMed  Google Scholar 

  45. Behnsen J, Deriu E, Sassone-Corsi M, Raffatellu M (2013) Probiotics: properties, examples, and specific applications. Cold Spring Harb Perspect Med 3:a010074. https://doi.org/10.1101/cshperspect.a010074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Osman N, Adawi D, Ahrné S, Jeppsson B, Molin G (2007) Endotoxin- and d-galactosamine-induced liver injury improved by the administration of Lactobacillus, Bifidobacterium and blueberry. Dig Liver Dis 39(9):849–856. https://doi.org/10.1016/j.dld.2007.06.001

    Article  CAS  PubMed  Google Scholar 

  47. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72(3):215–224

    Article  CAS  PubMed  Google Scholar 

  48. Gargari G, Taverniti V, Balzaretti S, Ferrario C, Gardana C, Simonetti P, Guglielmetti S (2016) Consumption of a Bifidobacterium bifidum strain for 4 weeks modulates dominant intestinal bacterial taxa and fecal butyrate in healthy adults. Appl Environ Microbiol 82(19):5850–5859. https://doi.org/10.1128/aem.01753-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yuan X, Wang L, Bhat OM, Lohner H, Li P-L (2018) Differential effects of short chain fatty acids on endothelial Nlrp3 inflammasome activation and neointima formation: antioxidant action of butyrate. Redox Biol 16:21–31. https://doi.org/10.1016/j.redox.2018.02.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Saiga A, Tanabe S, Nishimura T (2003) Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. J Agric Food Chem 51(12):3661–3667. https://doi.org/10.1021/jf021156g

    Article  CAS  PubMed  Google Scholar 

  51. Suetsuna K, Ukeda H, Ochi H (2000) Isolation and characterization of free radical scavenging activities peptides derived from casein. J Nutr Biochem 11(3):128–131

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The present study was supported by Tehran University of Medical Sciences (grant number : 97-03-161-40572 ).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leila Azadbakht.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zamani, B., Sheikhi, A., Namazi, N. et al. The Effects of Supplementation with Probiotic on Biomarkers of Oxidative Stress in Adult Subjects: a Systematic Review and Meta-analysis of Randomized Trials. Probiotics & Antimicro. Prot. 12, 102–111 (2020). https://doi.org/10.1007/s12602-018-9500-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-018-9500-1

Keywords

Navigation