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Published in: European Journal of Nutrition 2/2020

01-03-2020 | Probiotics | Original Contribution

The effect of probiotics on inflammatory biomarkers: a meta-analysis of randomized clinical trials

Authors: Alireza Milajerdi, Seyyed Mohammad Mousavi, Alireza Sadeghi, Asma Salari-Moghaddam, Mohammad Parohan, Bagher Larijani, Ahmad Esmaillzadeh

Published in: European Journal of Nutrition | Issue 2/2020

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Abstract

Purpose

No study has summarized earlier findings on the effect of probiotic supplementation on inflammatory biomarkers. This systematic review and meta-analysis was conducted to systematically review the available placebo-controlled clinical trials about the effect of probiotic supplementation on several inflammatory biomarkers in adults.

Methods

Relevant papers published up to March 2018 were searched up through PubMed, MEDLINE, SCOPUS, EMBASE, and Google Scholar, using following suitable keywords. Clinical trials that examined the effect of probiotic supplementation on inflammation in adults were included.

Results

Overall, 42 randomized clinical trials (1138 participants in intervention and 1120 participants in control groups) were included. Combining findings from included studies, we found a significant reduction in serum hs-CRP [standardized mean difference (SMD) − 0.46; 95% CI − 0.73, − 0.19], TNF-a (− 0.21; − 0.34, − 0.08), IL-6 (− 0.37; − 0.51, − 0.24), IL-12 (− 0.47; − 0.67, − 0.27), and IL-4 concentrations (− 0.48; − 0.76, − 0.20) after probiotic supplementation. Pooling effect sizes from 11 studies with 12 effect sizes, a significant increase in IL-10 concentrations was seen (0.21; 0.04, 0.38). We failed to find a significant effect of probiotic supplementation on serum IL-1B (− 0.17; − 0.37, 0.02), IL-8 (− 0.01; − 0.30, 0.28), and IFN-g (− 0.08; − 0.31, 0.15) and IL-17 concentrations (0.06; − 0.34, 0.46).

Conclusions

Probiotic supplementation significantly reduced serum concentrations of pro-inflammatory cytokines including, hs-CRP, TNF-a, IL-6, IL-12, and IL-4, but it did not influence IL-1B, IL-8, IFN-g, and IL-17 concentrations. A significant increase in serum concentrations of IL-10, as a anti-inflammatory cytokine was also documented after probiotic supplementation.
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Literature
1.
go back to reference Robertson CM, Coopersmith CM (2006) The systemic inflammatory response syndrome. Microbes Infect 8(5):1382–1389PubMed Robertson CM, Coopersmith CM (2006) The systemic inflammatory response syndrome. Microbes Infect 8(5):1382–1389PubMed
2.
go back to reference Huang Y, Chen Z (2016) Inflammatory bowel disease related innate immunity and adaptive immunity. Am J Transl Res 8(6):2490PubMedPubMedCentral Huang Y, Chen Z (2016) Inflammatory bowel disease related innate immunity and adaptive immunity. Am J Transl Res 8(6):2490PubMedPubMedCentral
3.
go back to reference Pradhan A (2007) Obesity, metabolic syndrome, and type 2 diabetes: inflammatory basis of glucose metabolic disorders. Nutr Rev 65(suppl_3):S152–S156PubMed Pradhan A (2007) Obesity, metabolic syndrome, and type 2 diabetes: inflammatory basis of glucose metabolic disorders. Nutr Rev 65(suppl_3):S152–S156PubMed
4.
go back to reference Guarner V, Rubio-Ruiz ME (2015) Low-grade systemic inflammation connects aging, metabolic syndrome and cardiovascular disease. Interdiscip Top Gerontol 40:99–106PubMed Guarner V, Rubio-Ruiz ME (2015) Low-grade systemic inflammation connects aging, metabolic syndrome and cardiovascular disease. Interdiscip Top Gerontol 40:99–106PubMed
5.
go back to reference Başaranoğlu M, Örmeci N (2014) Nonalcoholic fatty liver disease: diagnosis, pathogenesis, and management. Turk J Gastroenterol 25:127–132PubMed Başaranoğlu M, Örmeci N (2014) Nonalcoholic fatty liver disease: diagnosis, pathogenesis, and management. Turk J Gastroenterol 25:127–132PubMed
6.
go back to reference Speer K, Upton D, Semple S, McKune A (2018) Systemic low-grade inflammation in post-traumatic stress disorder: a systematic review. J Inflamm Res 11:111PubMedPubMedCentral Speer K, Upton D, Semple S, McKune A (2018) Systemic low-grade inflammation in post-traumatic stress disorder: a systematic review. J Inflamm Res 11:111PubMedPubMedCentral
7.
go back to reference Ashtary-Larky D, Lamuchi-Deli N, Milajerdi A, Salehi MB, Alipour M, Kooti W, Ashtary-Larky P, Alamiri F, Sheikhi A, Afrisham R (2017) Inflammatory and biochemical biomarkers in response to high intensity resistance training in trained and untrained men. Asian J Sports Med 8(2):1A–1A Ashtary-Larky D, Lamuchi-Deli N, Milajerdi A, Salehi MB, Alipour M, Kooti W, Ashtary-Larky P, Alamiri F, Sheikhi A, Afrisham R (2017) Inflammatory and biochemical biomarkers in response to high intensity resistance training in trained and untrained men. Asian J Sports Med 8(2):1A–1A
8.
go back to reference Kaluza J, Harris H, Melhus H, Michaëlsson K, Wolk A (2018) Questionnaire-based anti-inflammatory diet index as a predictor of low-grade systemic inflammation. Mary Ann Liebert, Inc., New Rochelle Kaluza J, Harris H, Melhus H, Michaëlsson K, Wolk A (2018) Questionnaire-based anti-inflammatory diet index as a predictor of low-grade systemic inflammation. Mary Ann Liebert, Inc., New Rochelle
9.
go back to reference Ozawa M, Shipley M, Kivimaki M, Singh-Manoux A, Brunner EJ (2017) Dietary pattern, inflammation and cognitive decline: the Whitehall II prospective cohort study. Clin Nutr 36(2):506–512PubMedPubMedCentral Ozawa M, Shipley M, Kivimaki M, Singh-Manoux A, Brunner EJ (2017) Dietary pattern, inflammation and cognitive decline: the Whitehall II prospective cohort study. Clin Nutr 36(2):506–512PubMedPubMedCentral
10.
go back to reference McLoughlin RF, Berthon BS, Jensen ME, Baines KJ, Wood LG (2017) Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis. Am J Clin Nutr 106(3):930–945PubMed McLoughlin RF, Berthon BS, Jensen ME, Baines KJ, Wood LG (2017) Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis. Am J Clin Nutr 106(3):930–945PubMed
11.
go back to reference Li M, van Esch BC, Wagenaar GT, Garssen J, Folkerts G, Henricks PA (2018) Pro-and anti-inflammatory effects of short chain fatty acids on immune and endothelial cells. Eur J Pharmacol 831:52–59PubMed Li M, van Esch BC, Wagenaar GT, Garssen J, Folkerts G, Henricks PA (2018) Pro-and anti-inflammatory effects of short chain fatty acids on immune and endothelial cells. Eur J Pharmacol 831:52–59PubMed
12.
go back to reference Campbell AW (2016) Inflammation and a solution: probiotics. Altern Ther Health Med 22(5):8PubMed Campbell AW (2016) Inflammation and a solution: probiotics. Altern Ther Health Med 22(5):8PubMed
13.
go back to reference Wang Z-J, Chen X-F, Zhang Z-X, Li Y-C, Deng J, Tu J, Song Z-Q, Zou Q-H (2017) Effects of anti-Helicobacter pylori concomitant therapy and probiotic supplementation on the throat and gut microbiota in humans. Microb Pathog 109:156–161PubMed Wang Z-J, Chen X-F, Zhang Z-X, Li Y-C, Deng J, Tu J, Song Z-Q, Zou Q-H (2017) Effects of anti-Helicobacter pylori concomitant therapy and probiotic supplementation on the throat and gut microbiota in humans. Microb Pathog 109:156–161PubMed
14.
go back to reference Goldin B, Gorbach S (2008) Clinical indications for probiotics: an overview. Clin Infect Dis 46(Supplement_2):S96–S100PubMed Goldin B, Gorbach S (2008) Clinical indications for probiotics: an overview. Clin Infect Dis 46(Supplement_2):S96–S100PubMed
15.
go back to reference Kaur IP, Kuhad A, Garg A, Chopra K (2009) Probiotics: delineation of prophylactic and therapeutic benefits. J Med Food 12(2):219–235PubMed Kaur IP, Kuhad A, Garg A, Chopra K (2009) Probiotics: delineation of prophylactic and therapeutic benefits. J Med Food 12(2):219–235PubMed
16.
go back to reference Alberda C, Gramlich L, Meddings J, Field C, McCargar L, Kutsogiannis D, Fedorak R, Madsen K (2007) Effects of probiotic therapy in critically ill patients: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr 85(3):816–823PubMed Alberda C, Gramlich L, Meddings J, Field C, McCargar L, Kutsogiannis D, Fedorak R, Madsen K (2007) Effects of probiotic therapy in critically ill patients: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr 85(3):816–823PubMed
17.
go back to reference Han SH, Suk KT, Kim DJ, Kim MY, Baik SK, Kim YD, Cheon GJ, Choi DH, Ham YL, Shin DH (2015) Effects of probiotics (cultured Lactobacillus subtilis/Streptococcus faecium) in the treatment of alcoholic hepatitis: randomized-controlled multicenter study. Eur J Gastroenterol Hepatol 27(11):1300–1306PubMed Han SH, Suk KT, Kim DJ, Kim MY, Baik SK, Kim YD, Cheon GJ, Choi DH, Ham YL, Shin DH (2015) Effects of probiotics (cultured Lactobacillus subtilis/Streptococcus faecium) in the treatment of alcoholic hepatitis: randomized-controlled multicenter study. Eur J Gastroenterol Hepatol 27(11):1300–1306PubMed
18.
go back to reference Pineda Mde L, Thompson SF, Summers K, de Leon F, Pope J, Reid G (2011) A randomized, double-blinded, placebo-controlled pilot study of probiotics in active rheumatoid arthritis. Med Sci Monit 17(6):CR347–C354PubMed Pineda Mde L, Thompson SF, Summers K, de Leon F, Pope J, Reid G (2011) A randomized, double-blinded, placebo-controlled pilot study of probiotics in active rheumatoid arthritis. Med Sci Monit 17(6):CR347–C354PubMed
19.
go back to reference Bajaj JS, Heuman DM, Hylemon PB, Sanyal AJ, Puri P, Sterling RK, Luketic V, Stravitz RT, Siddiqui MS, Fuchs M, Thacker LR, Wade JB, Daita K, Sistrun S, White MB, Noble NA, Thorpe C, Kakiyama G, Pandak WM, Sikaroodi M, Gillevet PM (2014) Randomised clinical trial: Lactobacillus GG modulates gut microbiome, metabolome and endotoxemia in patients with cirrhosis. Aliment Pharmacol Ther 39(10):1113–1125. https://doi.org/10.1111/apt.12695 CrossRefPubMedPubMedCentral Bajaj JS, Heuman DM, Hylemon PB, Sanyal AJ, Puri P, Sterling RK, Luketic V, Stravitz RT, Siddiqui MS, Fuchs M, Thacker LR, Wade JB, Daita K, Sistrun S, White MB, Noble NA, Thorpe C, Kakiyama G, Pandak WM, Sikaroodi M, Gillevet PM (2014) Randomised clinical trial: Lactobacillus GG modulates gut microbiome, metabolome and endotoxemia in patients with cirrhosis. Aliment Pharmacol Ther 39(10):1113–1125. https://​doi.​org/​10.​1111/​apt.​12695 CrossRefPubMedPubMedCentral
20.
go back to reference Maslova E, Bhattacharya S, Lin S-W, Michels KB (2010) Caffeine consumption during pregnancy and risk of preterm birth: a meta-analysis. Am J Clin Nutr 92(5):1120–1132PubMedPubMedCentral Maslova E, Bhattacharya S, Lin S-W, Michels KB (2010) Caffeine consumption during pregnancy and risk of preterm birth: a meta-analysis. Am J Clin Nutr 92(5):1120–1132PubMedPubMedCentral
21.
go back to reference Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H, Taghizadeh M, Memarzadeh MR, 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):315–320PubMed Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H, Taghizadeh M, Memarzadeh MR, 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):315–320PubMed
22.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
28.
go back to reference Ebrahimi-Mameghani M, Sanaie S, Mahmoodpoor A, Hamishehkar H (2013) Effect of a probiotic preparation (VSL#3) in critically ill patients: a randomized, double-blind, placebo-controlled trial (pilot study). Pak J Med Sci 29(2):490–494PubMedPubMedCentral Ebrahimi-Mameghani M, Sanaie S, Mahmoodpoor A, Hamishehkar H (2013) Effect of a probiotic preparation (VSL#3) in critically ill patients: a randomized, double-blind, placebo-controlled trial (pilot study). Pak J Med Sci 29(2):490–494PubMedPubMedCentral
29.
go back to reference Firouzi S, Majid HA, Ismail A, Kamaruddin NA, Barakatun-Nisak MY (2017) Effect of multi-strain probiotics (multi-strain microbial cell preparation) on glycemic control and other diabetes-related outcomes in people with type 2 diabetes: a randomized controlled trial. Eur J Nutr 56(4):1535–1550. https://doi.org/10.1007/s00394-016-1199-8 CrossRefPubMed Firouzi S, Majid HA, Ismail A, Kamaruddin NA, Barakatun-Nisak MY (2017) Effect of multi-strain probiotics (multi-strain microbial cell preparation) on glycemic control and other diabetes-related outcomes in people with type 2 diabetes: a randomized controlled trial. Eur J Nutr 56(4):1535–1550. https://​doi.​org/​10.​1007/​s00394-016-1199-8 CrossRefPubMed
30.
go back to reference Flichy-Fernández A, Ata-Ali J, Alegre-Domingo T, Candel-Martí E, Ata-Ali F, Palacio J, Peñarrocha-Diago M (2015) The effect of orally administered probiotic Lactobacillus reuteri-containing tablets in peri-implant mucositis: a double-blind randomized controlled trial. J Periodontal Res 50(6):775–785PubMed Flichy-Fernández A, Ata-Ali J, Alegre-Domingo T, Candel-Martí E, Ata-Ali F, Palacio J, Peñarrocha-Diago M (2015) The effect of orally administered probiotic Lactobacillus reuteri-containing tablets in peri-implant mucositis: a double-blind randomized controlled trial. J Periodontal Res 50(6):775–785PubMed
31.
34.
go back to reference Hatakka K, Martio J, Korpela M, Herranen M, Poussa T, Laasanen T, Saxelin M, Vapaatalo H, Moilanen E, Korpela R (2003) Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis—a pilot study. Scand J Rheumatol 32(4):211–215PubMed Hatakka K, Martio J, Korpela M, Herranen M, Poussa T, Laasanen T, Saxelin M, Vapaatalo H, Moilanen E, Korpela R (2003) Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis—a pilot study. Scand J Rheumatol 32(4):211–215PubMed
37.
go back to reference Jones M, Martoni C, Prakash S (2012) Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. Eur J Clin Nutr 66(11):1234PubMed Jones M, Martoni C, Prakash S (2012) Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. Eur J Clin Nutr 66(11):1234PubMed
40.
go back to reference Mohseni S, Bayani M, Bahmani F, Tajabadi-Ebrahimi M, Bayani MA, Jafari P, Asemi Z (2017) The beneficial 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 CrossRefPubMed Mohseni S, Bayani M, Bahmani F, Tajabadi-Ebrahimi M, Bayani MA, Jafari P, Asemi Z (2017) The beneficial 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 CrossRefPubMed
44.
go back to reference Pinto-Sanchez MI, Hall GB, Ghajar K, Nardelli A, Bolino C, Lau JT, Martin FP, Cominetti O, Welsh C, Rieder A, Traynor J, Gregory C, De Palma G, Pigrau M, Ford AC, Macri J, Berger B, Bergonzelli G, Surette MG, Collins SM, Moayyedi P, Bercik P (2017) Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology 153(2):448–459 e448. https://doi.org/10.1053/j.gastro.2017.05.003 CrossRefPubMed Pinto-Sanchez MI, Hall GB, Ghajar K, Nardelli A, Bolino C, Lau JT, Martin FP, Cominetti O, Welsh C, Rieder A, Traynor J, Gregory C, De Palma G, Pigrau M, Ford AC, Macri J, Berger B, Bergonzelli G, Surette MG, Collins SM, Moayyedi P, Bercik P (2017) Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology 153(2):448–459 e448. https://​doi.​org/​10.​1053/​j.​gastro.​2017.​05.​003 CrossRefPubMed
45.
go back to reference Rajkumar H, Mahmood N, Kumar M, Varikuti SR, Challa HR, Myakala SP (2014) Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized, controlled trial. Mediat Inflamm 2014:348959. https://doi.org/10.1155/2014/348959 CrossRef Rajkumar H, Mahmood N, Kumar M, Varikuti SR, Challa HR, Myakala SP (2014) Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized, controlled trial. Mediat Inflamm 2014:348959. https://​doi.​org/​10.​1155/​2014/​348959 CrossRef
46.
go back to reference Redondo N, Nova E, Gheorghe A, Díaz LE, Hernández A, Marcos A (2017) Evaluation of Lactobacillus coryniformis CECT5711 strain as a coadjuvant in a vaccination process: a randomised clinical trial in healthy adults. Nutr Metab 14(1):2 Redondo N, Nova E, Gheorghe A, Díaz LE, Hernández A, Marcos A (2017) Evaluation of Lactobacillus coryniformis CECT5711 strain as a coadjuvant in a vaccination process: a randomised clinical trial in healthy adults. Nutr Metab 14(1):2
47.
51.
go back to reference Sierra S, Lara-Villoslada F, Sempere L, Olivares M, Boza J, Xaus J (2010) Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults. Anaerobe 16(3):195–200PubMed Sierra S, Lara-Villoslada F, Sempere L, Olivares M, Boza J, Xaus J (2010) Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults. Anaerobe 16(3):195–200PubMed
55.
go back to reference Wang I-K, Wu Y-Y, Yang Y-F, Ting I-W, Lin C-C, Yen T-H, Chen J-H, Wang C-H, Huang C-C, Lin H-C (2015) The effect of probiotics on serum levels of cytokine and endotoxin in peritoneal dialysis patients: a randomised, double-blind, placebo-controlled trial. Benef Microbes 6(4):423–430PubMed Wang I-K, Wu Y-Y, Yang Y-F, Ting I-W, Lin C-C, Yen T-H, Chen J-H, Wang C-H, Huang C-C, Lin H-C (2015) The effect of probiotics on serum levels of cytokine and endotoxin in peritoneal dialysis patients: a randomised, double-blind, placebo-controlled trial. Benef Microbes 6(4):423–430PubMed
56.
go back to reference Xiao J (2006) Effect of probiotic Bifidobacterium longum BBS36 in relieving clinical symptoms and modulating plasma cytokine levels of Japanese cedar pollinosis during the pollen season. A randomized double-blind, placebocontrolled trial. J Investig Allergol Clin Immunol 16:86–93PubMed Xiao J (2006) Effect of probiotic Bifidobacterium longum BBS36 in relieving clinical symptoms and modulating plasma cytokine levels of Japanese cedar pollinosis during the pollen season. A randomized double-blind, placebocontrolled trial. J Investig Allergol Clin Immunol 16:86–93PubMed
57.
go back to reference Yamamoto K, Yokoyama K, Matsukawa T, Kato S, Kato S, Yamada K, Hirota T (2016) Efficacy of prolonged ingestion of Lactobacillus acidophilus L-92 in adult patients with atopic dermatitis. J Dairy Sci 99(7):5039–5046PubMed Yamamoto K, Yokoyama K, Matsukawa T, Kato S, Kato S, Yamada K, Hirota T (2016) Efficacy of prolonged ingestion of Lactobacillus acidophilus L-92 in adult patients with atopic dermatitis. J Dairy Sci 99(7):5039–5046PubMed
58.
go back to reference 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. https://doi.org/10.1111/1756-185x.12888 CrossRefPubMed 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. https://​doi.​org/​10.​1111/​1756-185x.​12888 CrossRefPubMed
59.
go back to reference Mazidi M, Rezaie P, Ferns GA, Vatanparast H (2017) Impact of probiotic administration on serum C-reactive protein concentrations: systematic review and meta-analysis of randomized control trials. Nutrients 9(1):20PubMedCentral Mazidi M, Rezaie P, Ferns GA, Vatanparast H (2017) Impact of probiotic administration on serum C-reactive protein concentrations: systematic review and meta-analysis of randomized control trials. Nutrients 9(1):20PubMedCentral
60.
go back to reference Ma Y-Y, Li L, Yu C-H, Shen Z, Chen L-H, Li Y-M (2013) Effects of probiotics on nonalcoholic fatty liver disease: a meta-analysis. World J Gastroenterol 19(40):6911PubMedPubMedCentral Ma Y-Y, Li L, Yu C-H, Shen Z, Chen L-H, Li Y-M (2013) Effects of probiotics on nonalcoholic fatty liver disease: a meta-analysis. World J Gastroenterol 19(40):6911PubMedPubMedCentral
61.
go back to reference Liu D, Jiang X-Y, Zhou L-S, Song J-H, Zhang X (2016) Effects of probiotics on intestinal mucosa barrier in patients with colorectal cancer after operation: meta-analysis of randomized controlled trials. Medicine 95(15):e3342PubMedPubMedCentral Liu D, Jiang X-Y, Zhou L-S, Song J-H, Zhang X (2016) Effects of probiotics on intestinal mucosa barrier in patients with colorectal cancer after operation: meta-analysis of randomized controlled trials. Medicine 95(15):e3342PubMedPubMedCentral
62.
go back to reference 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 26:67–76PubMed 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 26:67–76PubMed
63.
go back to reference Tam CS, Redman LM (2013) Adipose tissue inflammation and metabolic dysfunction: a clinical perspective. Horm Mol Biol Clin Investig 15(1):19–24PubMedPubMedCentral Tam CS, Redman LM (2013) Adipose tissue inflammation and metabolic dysfunction: a clinical perspective. Horm Mol Biol Clin Investig 15(1):19–24PubMedPubMedCentral
64.
go back to reference Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, Mizumachi K, Kurisaki J (2002) Adhesion of lactic acid bacteria to caco-2 cells and their effect on cytokine secretion. Microbiol Immunol 46(4):293–297PubMed Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, Mizumachi K, Kurisaki J (2002) Adhesion of lactic acid bacteria to caco-2 cells and their effect on cytokine secretion. Microbiol Immunol 46(4):293–297PubMed
65.
go back to reference He F, Ouwehand AC, Isolauri E, Hashimoto H, Benno Y, Salminen S (2001) Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. Pathog Dis 30(1):43–47 He F, Ouwehand AC, Isolauri E, Hashimoto H, Benno Y, Salminen S (2001) Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. Pathog Dis 30(1):43–47
66.
go back to reference Pankevich E, Astakhova A, Chistyakov D, Sergeeva M (2017) Antiinflammatory effect of rosiglitazone via modulation of mRNA stability of interleukin 10 and cyclooxygenase 2 in astrocytes. Biochemistry 82(11):1276–1284PubMed Pankevich E, Astakhova A, Chistyakov D, Sergeeva M (2017) Antiinflammatory effect of rosiglitazone via modulation of mRNA stability of interleukin 10 and cyclooxygenase 2 in astrocytes. Biochemistry 82(11):1276–1284PubMed
67.
go back to reference Calcinaro F, Dionisi S, Marinaro M, Candeloro P, Bonato V, Marzotti S, Corneli R, Ferretti E, Gulino A, Grasso F (2005) Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia 48(8):1565–1575PubMed Calcinaro F, Dionisi S, Marinaro M, Candeloro P, Bonato V, Marzotti S, Corneli R, Ferretti E, Gulino A, Grasso F (2005) Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia 48(8):1565–1575PubMed
68.
go back to reference Kaji R, Kiyoshima-Shibata J, Tsujibe S, Nanno M, Shida K (2018) Probiotic induction of interleukin-10 and interleukin-12 production by macrophages is modulated by co-stimulation with microbial components. J Dairy Sci 101(4):2838–2841PubMed Kaji R, Kiyoshima-Shibata J, Tsujibe S, Nanno M, Shida K (2018) Probiotic induction of interleukin-10 and interleukin-12 production by macrophages is modulated by co-stimulation with microbial components. J Dairy Sci 101(4):2838–2841PubMed
69.
go back to reference Icaza-Chávez M (2013) Gut microbiota in health and disease. Revista de Gastroenterología de México 78(4):240–248 (English edition) PubMed Icaza-Chávez M (2013) Gut microbiota in health and disease. Revista de Gastroenterología de México 78(4):240–248 (English edition) PubMed
70.
go back to reference Shacklett BL, Cox CA, Sandberg JK, Stollman NH, Jacobson MA, Nixon DF (2003) Trafficking of human immunodeficiency virus type 1-specific CD8+ T cells to gut-associated lymphoid tissue during chronic infection. J Virol 77(10):5621–5631PubMedPubMedCentral Shacklett BL, Cox CA, Sandberg JK, Stollman NH, Jacobson MA, Nixon DF (2003) Trafficking of human immunodeficiency virus type 1-specific CD8+ T cells to gut-associated lymphoid tissue during chronic infection. J Virol 77(10):5621–5631PubMedPubMedCentral
71.
go back to reference Malin M, Verronen P, Korhonen H, Syväoja E-L, Salminen S, Mykkänen H, Arvilommi H, Eerola E, Isolauri E (1997) Dietary therapy with Lactobacillus GG, bovine colostrum or bovine immune colostrum in patients with juvenile chronic arthritis: evaluation of effect on gut defence mechanisms. Inflammopharmacology 5(3):219–236PubMed Malin M, Verronen P, Korhonen H, Syväoja E-L, Salminen S, Mykkänen H, Arvilommi H, Eerola E, Isolauri E (1997) Dietary therapy with Lactobacillus GG, bovine colostrum or bovine immune colostrum in patients with juvenile chronic arthritis: evaluation of effect on gut defence mechanisms. Inflammopharmacology 5(3):219–236PubMed
72.
go back to reference Vitaliti G, Pavone P, Guglielmo F, Spataro G, Falsaperla R (2014) The immunomodulatory effect of probiotics beyond atopy: an update. J Asthma 51(3):320–332PubMed Vitaliti G, Pavone P, Guglielmo F, Spataro G, Falsaperla R (2014) The immunomodulatory effect of probiotics beyond atopy: an update. J Asthma 51(3):320–332PubMed
73.
go back to reference Rautava S, Kalliomäki M, Isolauri E (2005) New therapeutic strategy for combating the increasing burden of allergic disease: probiotics—a Nutrition, Allergy, Mucosal Immunology and Intestinal Microbiota (NAMI) Research Group report. J Allergy Clin Immunol 116(1):31–37PubMed Rautava S, Kalliomäki M, Isolauri E (2005) New therapeutic strategy for combating the increasing burden of allergic disease: probiotics—a Nutrition, Allergy, Mucosal Immunology and Intestinal Microbiota (NAMI) Research Group report. J Allergy Clin Immunol 116(1):31–37PubMed
Metadata
Title
The effect of probiotics on inflammatory biomarkers: a meta-analysis of randomized clinical trials
Authors
Alireza Milajerdi
Seyyed Mohammad Mousavi
Alireza Sadeghi
Asma Salari-Moghaddam
Mohammad Parohan
Bagher Larijani
Ahmad Esmaillzadeh
Publication date
01-03-2020
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 2/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-019-01931-8

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