Abstract
Objective
Despite the increasing evidence for probiotics’ anti-inflammatory effects, the results of meta-analyses remain inconsistent. The present umbrella meta-analysis aimed to investigate the effects of probiotic supplementation on inflammatory biomarkers.
Methods
We performed a wide-ranging systematic search in several databases, including PubMed, Web of Science, Scopus, EMBASE, and Google Scholar up to April 2023. The overall effect sizes were calculated using effect size (ES) values and their corresponding confidence intervals (CI).
Results
Out of a total of 580 related articles, 39 studies were qualified for inclusion in the analysis. The results of the analysis revealed a significant reduction of C-reactive protein (CRP) (ES = −1.02; 95% CI: −1.23, −0.80, p < 0.001; I2: 94.1%, p < 0.001), TNF-α (ES = −0.35; 95% CI: −0.50, −0.20, p < 0.001; I2: 75.6%, p < 0.001), and interleukin-6 (IL-6) levels (ES = −0.36; 95% CI: −0.59, −0.13, p = 0.002; I2: 85.6%, p < 0.001), following probiotic supplementation.
Conclusion
Probiotic supplementation significantly reduced serum concentrations of TNF-a, CRP, and IL-6. Thus, probiotic supplementation can be considered adjuvant therapy to alleviate inflammation in various inflammatory conditions.
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Code availability
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References
AbdelQadir YH, Hamdallah A, Sibaey EA, Hussein AS, Abdelaziz M, AbdelAzim A et al (2020) Efficacy of probiotic supplementation in patients with diabetic nephropathy: a systematic review and meta-analysis. Clin Nutr ESPEN 40:57–67. https://doi.org/10.1016/j.clnesp.2020.06.019
Alipour B, Homayouni-Rad A, Vaghef-Mehrabany E, Sharif SK, Vaghef-Mehrabany L, Asghari-Jafarabadi M, 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
Amirani E, Milajerdi A, Mirzaei H, Jamilian H, Mansournia MA, Hallajzadeh J, Ghaderi A (2020) The effects of probiotic supplementation on mental health, biomarkers of inflammation and oxidative stress in patients with psychiatric disorders: a systematic review and meta-analysis of randomized controlled trials. Complement Ther Med 49:102361. https://doi.org/10.1016/j.ctim.2020.102361
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
Arango Duque G, Descoteaux A (2014) Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol 5. https://doi.org/10.3389/fimmu.2014.00491
Askari G, Ghavami A, Shahdadian F, Moravejolahkami AR (2021) Effect of synbiotics and probiotics supplementation on autoimmune diseases: a systematic review and meta-analysis of clinical trials. Clin Nutr 40:3221–3234. https://doi.org/10.1016/j.clnu.2021.02.015
Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y et al (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331(6015):337–341
Badehnoosh B, Karamali M, Zarrati M, Jamilian M, Bahmani F, Tajabadi-Ebrahimi M et al (2018) The effects of probiotic supplementation on biomarkers of inflammation, oxidative stress and pregnancy outcomes in gestational diabetes. J Matern Fetal Neonatal Med 31(9):1128–1136. https://doi.org/10.1080/14767058.2017.1310193
Basso FG, Pansani TN, Turrioni AP, Soares DG, de Souza Costa CA, Hebling J (2016) Tumor necrosis factor-α and interleukin (IL)-1β, IL-6, and IL-8 impair in vitro migration and induce apoptosis of gingival fibroblasts and epithelial cells, delaying wound healing. J Periodontol 87(8):990–996. https://doi.org/10.1902/jop.2016.150713
Bohlouli J, Namjoo I, Borzoo-Isfahani M, Hojjati Kermani MA, Balouch Zehi Z, Moravejolahkami AR (2021) Effect of probiotics on oxidative stress and inflammatory status in diabetic nephropathy: a systematic review and meta-analysis of clinical trials. Heliyon 7(1):e05925. https://doi.org/10.1016/j.heliyon.2021.e05925
Brusselle G, Bracke K (2014) Targeting immune pathways for therapy in asthma and chronic obstructive pulmonary disease. Ann Am Thorac Soc 11(Suppl 5):S322-328. https://doi.org/10.1513/AnnalsATS.201403-118AW
Chan KY, Wong MMH, Pang SSH, Lo KKH (2021) Dietary supplementation for gestational diabetes prevention and management: a meta-analysis of randomized controlled trials. Arch Gynecol Obstet 303(6):1381–1391. https://doi.org/10.1007/s00404-021-06023-9
Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J et al (2017) Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 9(6):7204–7218. https://doi.org/10.18632/oncotarget.23208
Chen Y, Yue R, Zhang B, Li Z, Shui J, Huang X (2020) Effects of probiotics on blood glucose, biomarkers of inflammation and oxidative stress in pregnant women with gestational diabetes mellitus: a meta-analysis of randomized controlled trials. Med Clin (barc) 154(6):199–206. https://doi.org/10.1016/j.medcli.2019.05.041
Custodero C, Mankowski RT, Lee SA, Chen Z, Wu S, Manini TM et al (2018) Evidence-based nutritional and pharmacological interventions targeting chronic low-grade inflammation in middle-age and older adults: a systematic review and meta-analysis. Ageing Res Rev 46:42–59. https://doi.org/10.1016/j.arr.2018.05.004
Dai Y, Quan J, Xiong L, Luo Y, Yi B (2022) Probiotics improve renal function, glucose, lipids, inflammation and oxidative stress in diabetic kidney disease: a systematic review and meta-analysis. Ren Fail 44(1):862–880
Den H, Dong X, Chen M, Zou Z (2020) Efficacy of probiotics on cognition, and biomarkers of inflammation and oxidative stress in adults with Alzheimer’s disease or mild cognitive impairment—a meta-analysis of randomized controlled trials. Aging (albany NY) 12(4):4010
Eckersall PD, Bell R (2010) Acute phase proteins: biomarkers of infection and inflammation in veterinary medicine. Vet J 185(1):23–27. https://doi.org/10.1016/j.tvjl.2010.04.009
Eslami S, Hadjati J, Motevaseli E, Mirzaei R, Farashi Bonab S, Ansaripour B, Khoramizadeh MR (2016) Lactobacillus crispatus strain SJ-3C-US induces human dendritic cells (DCs) maturation and confers an anti-inflammatory phenotype to DCs. APMIS 124(8):697–710
Furman D, Campisi J, Verdin E, Carrera-Bastos P, Targ S, Franceschi C et al (2019) Chronic inflammation in the etiology of disease across the life span. Nat Med 25(12):1822–1832. https://doi.org/10.1038/s41591-019-0675-0
Gudkov AV, Komarova EA (2016) p53 and the carcinogenicity of chronic inflammation. Cold Spring Harb Perspect Med 6(11):a026161. https://doi.org/10.1101/cshperspect.a026161
Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, Schünemann HJ (2008) GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 336(7650):924–926
Hadi A, Moradi S, Ghavami A, Khalesi S, Kafeshani M (2020) Effect of probiotics and synbiotics on selected anthropometric and biochemical measures in women with polycystic ovary syndrome: a systematic review and meta-analysis. Eur J Clin Nutr 74(4):543–547
Hage FG, Szalai AJ (2007) C-reactive protein gene polymorphisms, C-reactive protein blood levels, and cardiovascular disease risk. J Am Coll Cardiol 50(12):1115–1122
Hajifaraji M, Jahanjou F, Abbasalizadeh F, Aghamohammadzadeh N, Abbasi MM, Dolatkhah N (2018) Effect of probiotic supplements in women with gestational diabetes mellitus on inflammation and oxidative stress biomarkers: a randomized clinical trial. Asia Pac J Clin Nutr 27(3):581–591. https://doi.org/10.6133/apjcn.082017.03
He B, Hoang TK, Tian X, Taylor CM, Blanchard E, Luo M et al (2019) Lactobacillus reuteri reduces the severity of experimental autoimmune encephalomyelitis in mice by modulating gut microbiota. Front Immunol 10:385
Ishizaki A, Bi X, Nguyen LV, Matsuda K, Pham HV, Phan CTT et al (2017) Effects of short-term probiotic ingestion on immune profiles and microbial translocation among HIV-1-infected Vietnamese children. Int J Mol Sci 18(10):2185. https://doi.org/10.3390/ijms18102185
Jia L, Jia Q, Yang J, Jia R, Zhang H (2018) Efficacy of probiotics supplementation on chronic kidney disease: a systematic review and meta-analysis. Kidney Blood Press Res 43(5):1623–1635. https://doi.org/10.1159/000494677
Jiang J, Chu C, Wu C, Wang C, Zhang C, Li T et al (2021) Efficacy of probiotics in multiple sclerosis: a systematic review of preclinical trials and meta-analysis of randomized controlled trials. Food Funct 12(6):2354–2377. https://doi.org/10.1039/d0fo03203d
Kamath DY, Xavier D, Sigamani A, Pais P (2015) High sensitivity C-reactive protein (hsCRP) & cardiovascular disease: an Indian perspective. Indian J Med Res 142(3):261–268. https://doi.org/10.4103/0971-5916.166582
Kasińska MA, Drzewoski J (2015) Effectiveness of probiotics in type 2 diabetes: a meta-analysis. Pol Arch Med Wewn 125(11):803–813. https://doi.org/10.20452/pamw.3156
Khan MY, Mihali AB, Rawala MS, Aslam A, Siddiqui WJ (2019) The promising role of probiotic and synbiotic therapy in aminotransferase levels and inflammatory markers in patients with nonalcoholic fatty liver disease—a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 31(6):703–715
Kieper WC, Troy A, Burghardt JT, Ramsey C, Lee JY, Jiang HQ et al (2005) Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J Immunol 174(6):3158–3163. https://doi.org/10.4049/jimmunol.174.6.3158
Kocsis T, Molnár B, Németh D, Hegyi P, Szakács Z, Bálint A et al (2020) Probiotics have beneficial metabolic effects in patients with type 2 diabetes mellitus: a meta-analysis of randomized clinical trials. Sci Rep 10(1):11787. https://doi.org/10.1038/s41598-020-68440-1
Li S-C, Hsu W-F, Chang J-S, Shih C-K (2019) Combination of Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis shows a stronger anti-inflammatory effect than individual strains in HT-29 cells. Nutrients 11(5):969
Li Z, Li Y, Pan B, Wang X, Wu Y, Guo K et al (2022) The effects of oral probiotic supplementation in postmenopausal women with overweight and obesity: a systematic review and meta-analysis of randomized controlled trials. Probiot Antimicrob Proteins. https://doi.org/10.1007/s12602-022-10037-3
Liu X, Zou Q, Zeng B, Fang Y, Wei H (2013) Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol 67(2):170–176. https://doi.org/10.1007/s00284-013-0338-1
Liu T, Zhang L, Joo D, Sun S-C (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2(1):17023. https://doi.org/10.1038/sigtrans.2017.23
Liu Y, Alookaran JJ, Rhoads JM (2018) Probiotics in autoimmune and inflammatory disorders. Nutrients 10(10):1537. https://doi.org/10.3390/nu10101537
Liu T, Wang X, Li R, Zhang ZY, Fang J, Zhang X (2021) Effects of probiotic preparations on inflammatory cytokines in chronic kidney disease patients: a systematic review and meta-analysis. Curr Pharm Biotechnol 22(10):1338–1349. https://doi.org/10.2174/1389201021666201119124058
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):6911–6918. https://doi.org/10.3748/wjg.v19.i40.6911
Macpherson AJ, Uhr T (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303(5664):1662–1665
Maia LP, Levi YLAS, do Prado RL, dos Santos SantinoniC, Marsicano JA (2019) Effects of probiotic therapy on serum inflammatory markers: a systematic review and meta-analysis. J Funct Foods 54:466–478
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):20. https://doi.org/10.3390/nu9010020
Milajerdi A, Mousavi SM, Sadeghi A, Salari-Moghaddam A, Parohan M, Larijani B, Esmaillzadeh A (2020) The effect of probiotics on inflammatory biomarkers: a meta-analysis of randomized clinical trials. Eur J Nutr 59(2):633–649. https://doi.org/10.1007/s00394-019-01931-8
Mirtaheri E, Pourghassem Gargari B, Kolahi S, Dehghan P, Asghari-Jafarabadi M, Hajalilou M et al (2015) Effects of alpha-lipoic acid supplementation on inflammatory biomarkers and matrix metalloproteinase-3 in rheumatoid arthritis patients. J Am Coll Nutr 34(4):310–317
Mohammed AT, Khattab M, Ahmed AM, Turk T, Sakr N et al (2017) The therapeutic effect of probiotics on rheumatoid arthritis: a systematic review and meta-analysis of randomized control trials. Clin Rheumatol 36(12):2697–2707. https://doi.org/10.1007/s10067-017-3814-3
Mousavi SN, Saboori S, Asbaghi O (2020) Effect of daily probiotic yogurt consumption on inflammation: a systematic review and meta-analysis of randomized controlled clinical trials. Obes Med 18:100221
Murata H, Shimada N, Yoshioka M (2004) Current research on acute phase proteins in veterinary diagnosis: an overview. Vet J 168(1):28–40. https://doi.org/10.1016/s1090-0233(03)00119-9
Musazadeh V, Roshanravan N, Mohammadizadeh M, Kavyani Z, Dehghan P, Mosharkesh E (2022) Curcumin as a novel approach in improving lipid profile: an umbrella meta-analysis. Nutr Metab Cardiovasc Dis 32(11):2493–2504
Naseri K, Saadati S, Ghaemi F, Ashtary-Larky D, Asbaghi O, Sadeghi A et al (2023) The effects of probiotic and synbiotic supplementation on inflammation, oxidative stress, and circulating adiponectin and leptin concentration in subjects with prediabetes and type 2 diabetes mellitus: a GRADE-assessed systematic review, meta-analysis, and meta-regression of randomized clinical trials. Eur J Nutr 62(2):543–561
Nguyen TTU, Kim HW, Kim W (2021) Effects of probiotics, prebiotics, and synbiotics on uremic toxins, inflammation, and oxidative stress in hemodialysis patients: a systematic review and meta-analysis of randomized controlled trials. J Clin Med 10(19):4456
NIH (2021) Probiotics—health professional fact sheet. Retrieved from https://ods.od.nih.gov/factsheets/Probiotics-HealthProfessional/
Okesene-Gafa KA, Moore AE, Jordan V, McCowan L, Crowther CA (2020) Probiotic treatment for women with gestational diabetes to improve maternal and infant health and well-being. Cochrane Database Syst Rev 6(6): Cd012970. https://doi.org/10.1002/14651858.CD012970.pub2
Pan H, Li R, Li T, Wang J, Liu L (2017) Whether probiotic supplementation benefits rheumatoid arthritis patients: a systematic review and meta-analysis. Engineering 3(1):115–121
Park JS, Lee EJ, Lee JC, Kim WK, Kim HS (2007) Anti-inflammatory effects of short chain fatty acids in IFN-gamma-stimulated RAW 264.7 murine macrophage cells: involvement of NF-kappaB and ERK signaling pathways. Int Immunopharmacol 7(1):70–77. https://doi.org/10.1016/j.intimp.2006.08.015
Sagheddu V, Uggeri F, Belogi L, Remollino L, Brun P, Bernabè G et al (2020) The biotherapeutic potential of Lactobacillus reuteri characterized using a target-specific selection process. Front Microbiol 11:532–532. https://doi.org/10.3389/fmicb.2020.00532
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
Shamasbi SG, Ghanbari-Homayi S, Mirghafourvand M (2020) The effect of probiotics, prebiotics, and synbiotics on hormonal and inflammatory indices in women with polycystic ovary syndrome: a systematic review and meta-analysis. Eur J Nutr 59(2):433–450
Shea BJ, Reeves BC, Wells G, Thuku M, Hamel C, Moran J et al (2017) AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ 358:j4008
Sproston NR, Ashworth JJ (2018) Role of C-reactive protein at sites of inflammation and infection. Front Immunol. https://doi.org/10.3389/fimmu.2018.00754
Sun J, Buys N (2015) Effects of probiotics consumption on lowering lipids and CVD risk factors: a systematic review and meta-analysis of randomized controlled trials. Ann Med 47(6):430–440. https://doi.org/10.3109/07853890.2015.1071872
Tabrizi R, Ostadmohammadi V, Lankarani KB, Akbari M, Akbari H, Vakili S et al (2019) The effects of probiotic and synbiotic supplementation on inflammatory markers among patients with diabetes: a systematic review and meta-analysis of randomized controlled trials. Eur J Pharmacol 852:254–264. https://doi.org/10.1016/j.ejphar.2019.04.003
Tamtaji OR, Milajerdi A, Reiner Ž, Asemi Z, Dadgostar E, Heidari-Soureshjani R et al (2020) A systematic review and meta-analysis: the effects of probiotic supplementation on metabolic profile in patients with neurological disorders. Complement Ther Med 53:102507. https://doi.org/10.1016/j.ctim.2020.102507
Tang Y, Huang J, Zhang WY, Qin S, Yang YX, Ren H et al (2019) Effects of probiotics on nonalcoholic fatty liver disease: a systematic review and meta-analysis. Therapeutic Adv Gastroenterol 12:1756284819878046
Thakur BK, Saha P, Banik G, Saha DR, Grover S, Batish VK, Das S (2016) Live and heat-killed probiotic Lactobacillus casei Lbs2 protects from experimental colitis through Toll-like receptor 2-dependent induction of T-regulatory response. Int Immunopharmacol 36:39–50. https://doi.org/10.1016/j.intimp.2016.03.033
Thongprayoon C, Kaewput W, Hatch ST, Bathini T, Sharma K, Wijarnpreecha K et al (2019) Effects of probiotics on inflammation and uremic toxins among patients on dialysis: a systematic review and meta-analysis. Dig Dis Sci 64(2):469–479. https://doi.org/10.1007/s10620-018-5243-9
Tzang BS, Liu CH, Hsu KC, Chen YH, Huang CY, Hsu TC (2017) Effects of oral Lactobacillus administration on antioxidant activities and CD4 + CD25 + forkhead box P3 (FoxP3) + T cells in NZB/W F1 mice. Br J Nutr 118(5):333–342. https://doi.org/10.1017/s0007114517002112
Venkatesh M, Mukherjee S, Wang H, Li H, Sun K, Benechet AP et al (2014) Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 41(2):296–310
Vinolo MA, Rodrigues HG, Hatanaka E, Sato FT, Sampaio SC, Curi R (2011) Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J Nutr Biochem 22(9):849–855. https://doi.org/10.1016/j.jnutbio.2010.07.009
Wang H, Wang D, Song H, Zou D, Feng X, Ma X et al (2021) The effects of probiotic supplementation on renal function, inflammation, and oxidative stress in diabetic nephropathy: a systematic review and meta-analysis of randomized controlled trials. Mater Exp 11(7):1122–1131
Wojdasiewicz P, Poniatowski ŁA, Szukiewicz D (2014) The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediators Inflamm 2014:561459–561459. https://doi.org/10.1155/2014/561459
Xiao M-W, Lin S-X, Shen Z-H, Luo W-W, Wang X-Y (2019) Systematic review with meta-analysis: the effects of probiotics in nonalcoholic fatty liver disease. Gastroenterol Res Prac. https://doi.org/10.1155/2019/1484598
Yao K, Zeng L, He Q, Wang W, Lei J, Zou X (2017) Effect of probiotics on glucose and lipid metabolism in type 2 diabetes mellitus: a meta-analysis of 12 randomized controlled trials. Med Sci Monit 23:3044–3053. https://doi.org/10.12659/msm.902600
Zarezadeh M, Musazadeh V, Faghfouri AH, Roshanravan N, Dehghan P (2021) Probiotics act as a potent intervention in improving lipid profile: an umbrella systematic review and meta-analysis. Crit Rev Food Sci Nutr 63(2):145–158
Zarezadeh M, Musazadeh V, Faghfouri AH, Sarmadi B, Jamilian P, Jamilian P et al (2022) Probiotic therapy, a novel and efficient adjuvant approach to improve glycemic status: an umbrella meta-analysis. Pharmacol Res 183:106397. https://doi.org/10.1016/j.phrs.2022.10639
Zhang D, Sun M, Samols D, Kushner I (1996) STAT3 participates in transcriptional activation of the C-reactive protein gene by interleukin-6 (∗). J Biol Chem 271(16):9503–9509
Zheng HJ, Guo J, Jia Q, Huang YS, Huang WJ, Zhang W et al (2019) The effect of probiotic and synbiotic supplementation on biomarkers of inflammation and oxidative stress in diabetic patients: a systematic review and meta-analysis of randomized controlled trials. Pharmacol Res 142:303–313. https://doi.org/10.1016/j.phrs.2019.02.016
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The protocol of this study was endorsed by the Student Research Committee, Tabriz University of Medical Sciences, Tabriz, Iran (Registration code: 69599).
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VM and AHF designed the research; ZK, ZSN, and VM conducted systematic search; AHF, VM, and MJ screened the articles; LGMPA, ZK, and VM extracted data; AHF analyzed and interpreted data; VM and ZK drew tables; LGMPA, MJ, VM, and AHF wrote the paper. PD had primary responsibility for the final content. All authors read and approved the final manuscript.
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Faghfouri, A.H., Afrakoti, L.G.M.P., Kavyani, Z. et al. The role of probiotic supplementation in inflammatory biomarkers in adults: an umbrella meta-analysis of randomized controlled trials. Inflammopharmacol 31, 2253–2268 (2023). https://doi.org/10.1007/s10787-023-01332-8
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DOI: https://doi.org/10.1007/s10787-023-01332-8