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Treating asthma patients with probiotics: a systematic review and meta-analysis.
Xie, Q, Yuan, J, Wang, Y
Nutricion hospitalaria. 2023;40(4):829-838
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Asthma is a common chronic inflammatory respiratory disease, with high morbidity and mortality. Recently, the efficacy of probiotics in allergic diseases has received special attention. Experiments have shown that probiotics have a clear effect on allergic diseases. The aim of this study was to study the efficacy of probiotics in the treatment of asthma and evaluate it, so as to provide a reference for the selection of treatment options for asthma patients. This study was a systematic review and meta-analysis of ten randomised controlled trials. Results showed that probiotics can improve symptoms and airway inflammation in patients with asthma, reduce acute exacerbation of asthma, and have no significant improvement in lung function. Authors concluded that the use of probiotics in patients with asthma can improve lung inflammation and asthma symptoms, as well as reduce the number of asthma attacks.
Abstract
Objective: To evaluate the role of probiotics in the treatment of asthma patients by meta-analysis. Methods: PubMed, Embase, The Cochrane Library, Web of Science, and other databases were searched by computer, and the relevant literature on the treatment of asthma by probiotics that met the inclusion criteria was screened by manual retrieval. Meta-analysis was performed using Revman 5.4 software and the combined effect was evaluated by odds ratio (OR) or mean difference (MD) and 95 % confidence interval (CI). Results: a total of ten references were included, all of which were randomized controlled studies, and a total of 1,101 people were investigated. Fractional exhaled nitric oxide (FeNO) (MD = -7.17, 95 % CI: -12.81, -1.54), asthma symptom severity (MD = -0.07, 95 % CI: -0.10, -0.04), Childhood Asthma Control Test (CACT) (MD = 2.26, 95 % CI: 1.14, 3.39), and the number of acute episodes of asthma (OR = 0.30, 95 % CI: 0.19, 0.47) in the probiotics group were better than those in the control group. There was no significant difference in forced expiratory volume in the first second (FEV1) (MD = 0.11, 95 % CI: -0.05, 0.26) and FEV1/FVC (%) (MD = 0.32, 95 % CI: -1.48, 2.12). Conclusion: the use of probiotics in patients with asthma can improve lung inflammation and asthma symptoms, reduce the number of asthma attacks, and have no effect on lung function. Objetivo: evaluar el papel de los probióticos en el tratamiento de pacientes con asma mediante metaanálisis. Métodos: se realizaron búsquedas informáticas en PubMed, Embase, The Cochrane Library, Web of Science y otras bases de datos, y se examinó la literatura relevante sobre el tratamiento del asma con probióticos que cumplía con los criterios de inclusión mediante recuperación manual. El metaanálisis se realizó con el software Revman 5.4 y el efecto combinado se evaluó mediante la razón de probabilidades (OR) o diferencia media (MD) y el intervalo de confianza (IC) del 95 %. Resultados: se incluyó un total de diez referencias, todas ellas estudios controlados aleatorios, y se investigó un total de 1.101 personas. El óxido nítrico exhalado (FeNO) (MD = -7,17, IC 95 %: -12,81, -1,54), la gravedad de los síntomas del asma (MD = -0,07, IC 95 %: -0,10, -0,04), la Prueba de Control del Asma (CACT-ACT) (MD = 2,26, IC 95 %: 1,14, 3,39) y el número de episodios agudos de asma (OR = 0,30, IC 95 %: 0,19, 0,47) en el grupo de probióticos fueron mejores que en el grupo de control. No hubo diferencia significativa en volumen espiratorio forzado en el primer segundo (FEV1) (DM = 0,11, IC 95 %: -0,05, 0,26) y FEV1/FVC (%) (DM = 0,32, IC 95 %: -1,48, 2,12). Conclusión: el uso de probióticos en pacientes con asma puede mejorar la inflamación pulmonar y los síntomas del asma, reducir el número de ataques de asma y no tener efecto sobre la función pulmonar.
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Meta-Analysis Reveals Compositional and Functional Microbial Changes Associated with Osteoporosis.
Akinsuyi, OS, Roesch, LFW
Microbiology spectrum. 2023;11(3):e0032223
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Osteoporosis (OP) is the most common metabolic bone disease associated with aging. Microbiome dysbiosis leading to impaired intestinal immune responses and subsequent production of osteoclastogenic cytokines has been proposed as the mechanism by which gut microbes are associated with osteoporosis. The aim of this study was to identify gut bacteria consistently associated with osteoporosis across different cohorts. This study was a meta-analysis of five studies. Results showed that gut microbial dysbiosis in osteoporosis patients is associated with functional changes, which result in significant changes in metabolites that play a key role in bone metabolism. Authors concluded that their findings set the stage for future studies to provide more comprehensive knowledge on how dysbiosis in the gut microbiome contributes to osteoporosis.
Abstract
Over the past decade, the role of the gut microbiota in many disease states has gained a great deal of attention. Mounting evidence from case-control and observational studies has linked changes in the gut microbiota to the pathophysiology of osteoporosis (OP). Nonetheless, the results of these studies contain discrepancies, leaving the literature without a consensus on osteoporosis-associated microbial signatures. Here, we conducted a comprehensive meta-analysis combining and reexamining five publicly available 16S rRNA partial sequence data sets to identify gut bacteria consistently associated with osteoporosis across different cohorts. After adjusting for the batch effect associated with technical variation and heterogeneity of studies, we observed a significant shift in the microbiota composition in the osteoporosis group. An increase in the relative abundance of opportunistic pathogens Clostridium sensu stricto, Bacteroides, and Intestinibacter was observed in the OP group. Moreover, short-chain-fatty-acid (SCFA) producers, including members of the genera Collinsella, Megasphaera, Agathobaculum, Mediterraneibacter, Clostridium XIV, and Dorea, were depleted in the OP group relative to the healthy control (HC) group. Lactic acid-producing bacteria, including Limosilactobacillus, were significantly increased in the OP group. The random forest algorithm further confirmed that these bacteria differentiate the two groups. Furthermore, functional prediction revealed depletion of the SCFA biosynthesis pathway (glycolysis, tricarboxylic acid [TCA] cycle, and Wood-Ljungdahl pathway) and amino acid biosynthesis pathway (methionine, histidine, and arginine) in the OP group relative to the HC group. This study uncovered OP-associated compositional and functional microbial alterations, providing robust insight into OP pathogenesis and aiding the possible development of a therapeutic intervention to manage the disease. IMPORTANCE Osteoporosis is the most common metabolic bone disease associated with aging. Mounting evidence has linked changes in the gut microbiota to the pathophysiology of osteoporosis. However, which microbes are associated with dysbiosis and their impact on bone density and inflammation remain largely unknown due to inconsistent results in the literature. Here, we present a meta-analysis with a standard workflow, robust statistical approaches, and machine learning algorithms to identify notable microbial compositional changes influencing osteoporosis.
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Elucidation of Prebiotics, Probiotics, Postbiotics, and Target from Gut Microbiota to Alleviate Obesity via Network Pharmacology Study.
Oh, KK, Gupta, H, Min, BH, Ganesan, R, Sharma, SP, Won, SM, Jeong, JJ, Lee, SB, Cha, MG, Kwon, GH, et al
Cells. 2022;11(18)
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The prevalence of obesity and associated comorbidities, such as diabetes, heart attack, hypertension, and cancer, is increasing worldwide. Microbes in the gut may play a significant role in the management of obesity by fermenting dietary fibres and producing metabolites such as short-chain fatty acids and flavonoids. In this meta-analysis, data were retrieved about gut microbial metabolites from the gutMGene database to evaluate the beneficial effects of prebiotics, probiotics, and postbiotics on key targets of obesity. Tryptophan was converted into beneficial metabolites such as indole by Escherichia coli, and isoflavones were converted into equol by Lactobacillus paracasei JS1. A positive effect may be exerted by these metabolites on the treatment of obesity. According to this meta-analysis, equol can reduce the levels of Interleukin-6, one of the inflammatory cytokines associated with obesity. Prebiotic isoflavone is fermented by probiotic Lactobacillus paracasei JS1 to produce equol, a postbiotic that inhibits the action of interleukin-6 and exerts a beneficial effect on obesity. In addition to understanding the relationship between prebiotics, probiotics, and postbiotics, healthcare professionals can use the results of this study to modulate the pathophysiology of obesity. It is necessary to conduct further rigorous research in order to evaluate the pharmacological value of the elements.
Abstract
The metabolites produced by the gut microbiota have been reported as crucial agents against obesity; however, their key targets have not been revealed completely in complex microbiome systems. Hence, the aim of this study was to decipher promising prebiotics, probiotics, postbiotics, and more importantly, key target(s) via a network pharmacology approach. First, we retrieved the metabolites related to gut microbes from the gutMGene database. Then, we performed a meta-analysis to identify metabolite-related targets via the similarity ensemble approach (SEA) and SwissTargetPrediction (STP), and obesity-related targets were identified by DisGeNET and OMIM databases. After selecting the overlapping targets, we adopted topological analysis to identify core targets against obesity. Furthermore, we employed the integrated networks to microbiota-substrate-metabolite-target (MSMT) via R Package. Finally, we performed a molecular docking test (MDT) to verify the binding affinity between metabolite(s) and target(s) with the Autodock 1.5.6 tool. Based on holistic viewpoints, we performed a filtering step to discover the core targets through topological analysis. Then, we implemented protein-protein interaction (PPI) networks with 342 overlapping target, another subnetwork was constructed with the top 30% degree centrality (DC), and the final core networks were obtained after screening the top 30% betweenness centrality (BC). The final core targets were IL6, AKT1, and ALB. We showed that the three core targets interacted with three other components via the MSMT network in alleviating obesity, i.e., four microbiota, two substrates, and six metabolites. The MDT confirmed that equol (postbiotics) converted from isoflavone (prebiotics) via Lactobacillus paracasei JS1 (probiotics) can bind the most stably on IL6 (target) compared with the other four metabolites (3-indolepropionic acid, trimethylamine oxide, butyrate, and acetate). In this study, we demonstrated that the promising substate (prebiotics), microbe (probiotics), metabolite (postbiotics), and target are suitable for obsesity treatment, providing a microbiome basis for further research.
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The Clinical, Microbiological, and Immunological Effects of Probiotic Supplementation on Prevention and Treatment of Periodontal Diseases: A Systematic Review and Meta-Analysis.
Gheisary, Z, Mahmood, R, Harri Shivanantham, A, Liu, J, Lieffers, JRL, Papagerakis, P, Papagerakis, S
Nutrients. 2022;14(5)
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Periodontal disease is preventable and reversible in its early stages; however, it can progress to chronic, irreversible states with significant destruction of the tooth-supporting tissues. The cause of periodontal disease is multifactorial with modifiable risk factors, including smoking, unhealthy diet (e.g., a western diet with high sugars and saturated fats), poor oral hygiene, hormonal changes, stress, various medications, and poorly managed comorbidities (e.g., type 2 diabetes), while non-modifiable risk factors include age, sex, and genetics. The aim of this study was to assess the effects on the clinical, microbiological, and immunological outcomes related to periodontal disease prevention and management. This study is systematic review and meta-analysis of randomized clinical trials involving adults with periodontal diseases or healthy volunteers receiving probiotic supplementation (control groups did not receive probiotic supplementation). Results show that probiotic supplementation improved the clinical parameters, reduced the subgingival bacterial counts of specific periodontopathogens, and reduced the gingival crevicular fluid levels of some proinflammatory mediators in periodontal disease patients. Authors conclude that further research is required to better assess the therapeutic and preventive value of probiotic supplementation in patients with gingivitis (early disease), as well as in healthy (without periodontal disease) individuals.
Abstract
(1) Background: Periodontal diseases are a global health concern. They are multi-stage, progressive inflammatory diseases triggered by the inflammation of the gums in response to periodontopathogens and may lead to the destruction of tooth-supporting structures, tooth loss, and systemic health problems. This systematic review and meta-analysis evaluated the effects of probiotic supplementation on the prevention and treatment of periodontal disease based on the assessment of clinical, microbiological, and immunological outcomes. (2) Methods: This study was registered under PROSPERO (CRD42021249120). Six databases were searched: PubMed, MEDLINE, EMBASE, CINAHL, Web of Science, and Dentistry and Oral Science Source. The meta-analysis assessed the effects of probiotic supplementation on the prevention and treatment of periodontal diseases and reported them using Hedge's g standardized mean difference (SMD). (3) Results: Of the 1883 articles initially identified, 64 randomized clinical trials were included in this study. The results of this meta-analysis indicated statistically significant improvements after probiotic supplementation in the majority of the clinical outcomes in periodontal disease patients, including the plaque index (SMD = 0.557, 95% CI: 0.228, 0.885), gingival index, SMD = 0.920, 95% CI: 0.426, 1.414), probing pocket depth (SMD = 0.578, 95% CI: 0.365, 0.790), clinical attachment level (SMD = 0.413, 95% CI: 0.262, 0.563), bleeding on probing (SMD = 0.841, 95% CI: 0.479, 1.20), gingival crevicular fluid volume (SMD = 0.568, 95% CI: 0.235, 0.902), reduction in the subgingival periodontopathogen count of P. gingivalis (SMD = 0.402, 95% CI: 0.120, 0.685), F. nucleatum (SMD = 0.392, 95% CI: 0.127, 0.658), and T. forsythia (SMD = 0.341, 95% CI: 0.050, 0.633), and immunological markers MMP-8 (SMD = 0.819, 95% CI: 0.417, 1.221) and IL-6 (SMD = 0.361, 95% CI: 0.079, 0.644). (4) Conclusions: The results of this study suggest that probiotic supplementation improves clinical parameters, and reduces the periodontopathogen load and pro-inflammatory markers in periodontal disease patients. However, we were unable to assess the preventive role of probiotic supplementation due to the paucity of studies. Further clinical studies are needed to determine the efficacy of probiotic supplementation in the prevention of periodontal diseases.
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The Efficacy and Safety of Probiotics for Allergic Rhinitis: A Systematic Review and Meta-Analysis.
Luo, C, Peng, S, Li, M, Ao, X, Liu, Z
Frontiers in immunology. 2022;13:848279
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Allergic rhinitis (AR) is characterized by a nasal sensitive inflammation. Common symptoms of AR are nasal itching, sneezing, rhinorrhoea, and nasal congestion. In addition, some patients experience symptoms of allergic rhinoconjunctivitis, such as watery or itchy or red eyes. The aim of this study was to address the effect and safety of probiotics on AR and to explore the possible causes of between-study heterogeneity via subgroup. This study is a systematic review and meta-analysis of twenty-eight randomised controlled trials. Results showed that probiotics supplementation for patients with AR can ameliorate AR symptoms and improve the quality of life. Probiotics supplementation can correct the T helper cell 1/ T helper cell 2 balance. Furthermore, there was no significant change in overall or antigen-specific immunoglobulin E levels between probiotic-treated and placebo-treated subjects. Authors conclude that in spite of the positive results of some outcomes, there is weak evidence that probiotics have a potential benefit in the treatment of AR.
Abstract
Background: Probiotics have proven beneficial in a number of immune-mediated and allergic diseases. Several human studies have evaluated the efficacy and safety of probiotics in allergic rhinitis; however, evidence for their use has yet to be firmly established. Objective: We undertook a systematic review and meta-analysis aiming to address the effect and safety of probiotics on allergic rhinitis. Methods: We systematically searched databases [MEDLINE (PubMed), Embase, and the Cochrane Central Register of Controlled Trials] from inception until June 1, 2021. Qualified literature was selected according to inclusion and exclusion criteria, the data were extracted, and a systematic review and meta-analysis was conducted. Results: Twenty-eight studies were included. The results showed that probiotics significantly relieved allergic rhinitis symptoms (standardized mean difference [SMD], -0.29, 95% confidence interval (CI) [-0.44, -0.13]; p = 0.0003, I 2 = 89%), decreased Rhinoconjunctivitis Quality of Life Questionnaire (RQLQ) scores compared with the control group (SMD, -0.64, 95% CI [-0.79, -0.49], p < 0.00001, I 2 = 97%), and increased T helper cell 1(Th1)/Th2 ratio (mean difference [MD], -2.47, 95% CI [-3.27, -1.68], p < 0.00001, I 2 = 72%). There was no significant change in overall or specific IgE levels between probiotic-treated and placebo-treated subjects (SMD, 0.09, 95% CI [-0.16, 0.34], I 2 = 0%, and SMD, -0.03, 95% CI [-0.18, 0.13], p = 0.72, I 2 = 0%, respectively). Conclusions: To sum up, probiotic supplement seems to be effective in ameliorating allergic rhinitis symptoms and improving the quality of life, but there is high heterogeneity in some results after subgroup analysis and clinicians should be cautious when recommending probiotics in treating allergic rhinitis. Systematic Review Registration: https://www.crd.york.ac.uk/PROSPERO/, PROSPERO (CRD42021242645).
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The Effects of Exercise on Indirect Markers of Gut Damage and Permeability: A Systematic Review and Meta-analysis.
Chantler, S, Griffiths, A, Matu, J, Davison, G, Jones, B, Deighton, K
Sports medicine (Auckland, N.Z.). 2021;51(1):113-124
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Gut permeability and intestinal cell damage are often observed in various gastrointestinal and metabolic conditions. Based on recent findings, exercise appears to cause damage to intestinal cells, leading to an increase in gut permeability. The aim of this review was to determine the effect of an acute bout of exercise on gut damage and permeability and explore the plausible mechanisms underlying these effects. This review analysed 34 studies that evaluated biomarkers of gut permeability and cell damage in response to exercise compared to resting controls. These findings revealed a significant impact of exercise on gut damage and permeability, and the markers were exacerbated when exercise was performed in hot conditions. The duration of exercise did not have any impact on cell damage or permeability. Based on these results, the authors conclude a single bout of exercise increases gut damage and permeability and they encourage further investigation into nutritional strategies to prevent adverse effects during the post-exercise period. Future research should consider the efficacy nutritional interventions to minimize these negative effects to optimise athletic health and performance.
Abstract
AIM: Exercise appears to cause damage to the endothelial lining of the human gastrointestinal tract and elicit a significant increase in gut permeability. OBJECTIVE The aim of this review was to determine the effect of an acute bout of exercise on gut damage and permeability outcomes in healthy populations using a meta-analysis. METHODS PubMed, The Cochrane Library as well as MEDLINE, SPORTDiscus and CINHAL, via EBSCOhost were searched through February 2019. Studies were selected that evaluated urinary (ratio of disaccharide/monosaccharide excretion) or plasma markers [intestinal Fatty Acid Binding Protein (i-FABP)] of gut permeability and gut cell damage in response to a single bout of exercise. RESULTS A total of 34 studies were included. A random-effects meta-analysis was performed, and showed a large and moderate effect size for markers of gut damage (i-FABP) (ES 0.81; 95% CI 0.63-0.98; n = 26; p < 0.001) and gut permeability (Disaccharide Sugar/Monosaccharide Sugar) (ES 0.70; 95% CI 0.29-1.11; n = 17; p < 0.001), respectively. Exercise performed in hot conditions (> 23 °C) further increased markers of gut damage compared with thermoneutral conditions [ES 1.06 (95% CI 0.88-1.23) vs. 0.66 (95% CI 0.43-0.89); p < 0.001]. Exercise duration did not have any significant effect on gut damage or permeability outcomes. CONCLUSIONS These findings demonstrate that a single bout of exercise increases gut damage and gut permeability in healthy participants, with gut damage being exacerbated in hot environments. Further investigation into nutritional strategies to minimise gut damage and permeability after exercise is required. PROSPERO database number (CRD42018086339).
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Effect of Probiotics on Metabolic Outcomes in Pregnant Women with Gestational Diabetes: A Systematic Review and Meta-Analysis of Randomized Controlled Trials.
Taylor, BL, Woodfall, GE, Sheedy, KE, O'Riley, ML, Rainbow, KA, Bramwell, EL, Kellow, NJ
Nutrients. 2017;9(5)
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The gut microbiota is an important ecosystem consisting of both residential and pathogenic bacteria. The microbiota produce bioactive compounds shown to benefit host metabolism. A variety of factors influence the gut microbiome, including host genetics, illness, antibiotic use, dietary patterns, weight loss and pregnancy. Throughout pregnancy the gut microbiota undergoes significant changes. The aim of this study is to determine the effect of 6-8-week probiotic supplementation versus placebo on glucose homeostasis, lipid levels and gestational weight gain in pregnant women diagnosed with gestational diabetes mellitus. This study is a systemic review based on four randomised controlled trials involving 288 participants. All studies included healthy pregnant women, age range between 18 – 40 years, who were diagnosed with gestational diabetes mellitus at 24 – 30 weeks gestation by oral glucose tolerance test. The study found that a 6 – 8-week probiotic intervention did not improve fasting blood glucose or LDL-cholesterol levels. However, probiotic supplementation in women with gestational diabetes mellitus was associated with significant reductions in insulin resistance. Authors conclude that while probiotic supplementation resulted in a significant reduction in insulin resistance in pregnant women with gestational diabetes mellitus, there was no significant effect on fasting blood glucose or LDL-cholesterol.
Abstract
The metabolic effects of probiotic administration in women with gestational diabetes mellitus (GDM) is unknown. The objective of this review was to investigate the effect of probiotics on fasting plasma glucose (FPG), insulin resistance (HOMA-IR) and LDL-cholesterol levels in pregnant women diagnosed with GDM. Seven electronic databases were searched for RCTs published in English between 2001 and 2017 investigating the metabolic effects of a 6-8 week dietary probiotic intervention in pregnant women following diagnosis with GDM. Eligible studies were assessed for risk of bias and subjected to qualitative and quantitative synthesis using a random effects model meta-analyses. Four high quality RCTs involving 288 participants were included in the review. Probiotic supplementation was not effective in decreasing FBG (Mean Difference = -0.13; 95% CI -0.32, 0.06, p = 0.18) or LDL-cholesterol (-0.16; 95% CI -0.45, 0.13, p = 0.67) in women with GDM. However, a significant reduction in HOMA-IR was observed following probiotic supplementation (-0.69; 95% CI -1.24, -0.14, p = 0.01). There were no significant differences in gestational weight gain, delivery method or neonatal outcomes between experimental and control groups, and no adverse effects of the probiotics were reported. Probiotic supplementation for 6-8 weeks resulted in a significant reduction in insulin resistance in pregnant women diagnosed with GDM. The use of probiotic supplementation is promising as a potential therapy to assist in the metabolic management of GDM. Further high quality studies of longer duration are required to determine the safety, optimal dose and ideal bacterial composition of probiotics before their routine use can be recommended in this patient group.
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Impact of Probiotic Administration on Serum C-Reactive Protein Concentrations: Systematic Review and Meta-Analysis of Randomized Control Trials.
Mazidi, M, Rezaie, P, Ferns, GA, Vatanparast, H
Nutrients. 2017;9(1)
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C-reactive protein (CRP) is a blood marker of inflammation and is frequently elevated in chronic conditions such as heart disease, obesity and Type 2 diabetes. Some strains of probiotics (bacteria that exert health benefits) are thought to act as anti-inflammatory agents through various mechanisms. This systematic review and meta-analysis of 20 randomised controlled trials (RCTs) aimed to investigate the effects of probiotic supplementation on CRP levels as one measure of inflammation. The meta-analysis indicates that probiotic supplementation with various strains of bacteria has a significant impact on serum CRP levels, with a weighted mean difference of -1.35mg/l. Whilst positive impacts were also seen for interleukin-10 and tumour necrosis factor-alpha (other markers of inflammation) with probiotics, these did not reach significance. The authors of this study point out that the results need to be interpreted with caution owing to the wide variety of study types, study size, probiotic strains and health outcomes measured in the included RCTs. However, Nutrition Practitioners working with clients with raised CRP levels may want to investigate the use of certain probiotic strains as part of an anti-inflammatory protocol.
Abstract
We conducted this systematic review and meta-analysis of prospective studies to determine the effect of probiotic administration on serum C-reactive protein (CRP) concentrations. We searched PubMed-Medline, Web of Science, the Cochrane, and Google Scholar databases (until May 2016) to identify prospective studies evaluating the impact of probiotic administration on CRP. We used a random effects models and generic inverse variance methods to synthesize quantitative data, followed by a leave-one-out method for sensitivity analysis. The systematic review registration number was: CRD42016039457. From a total of 425 entries identified via searches, 20 studies were included in the final analysis. The meta-analysis indicated a significant reduction in serum CRP following probiotic administration with a weighted mean difference (WMD) of -1.35 mg/L, (95% confidence interval (CI) -2.15 to -0.55, I² 65.1%). The WMDs for interleukin 10 (IL10) was -1.65 pg/dL, (95% CI -3.45 to 0.14, I² 3.1%), and -0.45 pg/mL, (95% CI -1.38 to 0.48, I² 10.2%) for tumor necrosis factor alpha (TNF-α). These findings were robust in sensitivity analyses. This meta-analysis suggests that probiotic administration may significantly reduce serum CRP while having no significant effect on serum IL10 and TNF-α.