Probiotics Can Further Reduce Waist Circumference in Adults with Morbid Obesity after Bariatric Surgery: A Systematic Review and Meta-Analysis of Randomized Controlled Trials

Yu Zhang, Tong Yan, Chenxin Xu, Huawu Yang, Tongtong Zhang, Yanjun Liu, Yu Zhang, Tong Yan, Chenxin Xu, Huawu Yang, Tongtong Zhang, Yanjun Liu

Abstract

Whether probiotics could be used as an adjunct to bariatric surgery is controversial. This meta-analysis aimed to evaluate the effects of probiotics on body weight, body mass index (BMI), percentage of the excess weight loss (%EWL), waist circumference (WC), and C-reactive protein (CRP) in adults with obesity after bariatric surgery (BS). PUBMED, EMBASE, and the Cochrane Central Registry of Controlled Trials were searched from the earliest record to March 2020. All randomized controlled trials (RCTs) on the effects of probiotics in adults with obesity after bariatric surgery were analyzed according to the eligibility criteria. Four RCTs, including 172 participants, were analyzed. There was a statistically significant difference in probiotics in the reduction of waist circumference at 12 months after bariatric surgery. However, probiotics were not effective in weight, BMI, %EWL, WC, and CRP both within 3 months and at 12 months postoperation. Probiotics aid adults with morbid obesity in achieving further waist circumference improvement after BS, with no significant effect on weight, BMI, %EWL, and CRP. More quality clinical studies are needed to confirm the efficacy and safety of probiotics, and address a number of practical issues before the routine clinical use of probiotics in adults with obesity undergoing BS.

Conflict of interest statement

The authors declare no conflicts of interest.

Copyright © 2021 Yu Zhang et al.

Figures

Figure 1
Figure 1
PRISMA flowchart of the process for searching and selecting studies.
Figure 2
Figure 2
(a) Risk of bias summary: judgements about each risk of bias item for included studies. The green circle represents a low risk, and yellow represents an unclear risk, which means that no evidence was found. (b) Risk of bias graph: judgements about each risk of bias item presented as percentages across all included studies. The risk of bias is relatively low.
Figure 3
Figure 3
Forest plot presenting the effects of probiotic supplementation on the changes of weight in patients at 3 months after bariatric surgery.
Figure 4
Figure 4
Forest plot presenting the effects of probiotic supplementation on the changes of BMI in patients at (a) 3 months and (b) 12 months after bariatric surgery, respectively.
Figure 5
Figure 5
Forest plot presenting the effects of probiotic supplementation on the changes of %EWL in patients at (a) 3 months and (b) 12 months after bariatric surgery, respectively.
Figure 6
Figure 6
Forest plot presenting the effects of probiotic supplementation on the changes of WC in patients at (a) 3 months and (b) 12 months after bariatric surgery, respectively.
Figure 7
Figure 7
Forest plot presenting the effects of probiotic supplementation on the changes of CRP in patients at (a) 3 months and (b) 12 months after bariatric surgery, respectively.

References

    1. Bluher M. Obesity: global epidemiology and pathogenesis. Nature Reviews Endocrinology. 2019;15(5):288–298. doi: 10.1038/s41574-019-0176-8.
    1. Sweeney T. E., Morton J. M. The human gut microbiome: a review of the effect of obesity and surgically induced weight loss. JAMA Surgery. 2013;148(6):563–569. doi: 10.1001/jamasurg.2013.5.
    1. Liu R., Hong J., Xu X., et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nature Medicine. 2017;23(7):859–868. doi: 10.1038/nm.4358.
    1. Liou A. P., Paziuk M., Luevano J. M., Jr., Machineni S., Turnbaugh P. J., Kaplan L. M. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Science Translational Medicine. 2013;5(178) doi: 10.1126/scitranslmed.3005687.178ra141
    1. Aron-Wisnewsky J., Prifti E., Belda E., et al. Major microbiota dysbiosis in severe obesity: fate after bariatric surgery. Gut. 2019;68(1):70–82. doi: 10.1136/gutjnl-2018-316103.
    1. Schulman A. R., Thompson C. C. Complications of bariatric surgery: what you can expect to see in your GI practice. American Journal of Gastroenterology. 2017;112(11):1640–1655. doi: 10.1038/ajg.2017.241.
    1. Qiu J., Lundberg P. W., Javier Birriel T., Claros L., Stoltzfus J., El Chaar M. Revisional bariatric surgery for weight regain and refractory complications in a single MBSAQIP accredited center: what are we dealing with? Obesity Surgery. 2018;28(9):2789–2795. doi: 10.1007/s11695-018-3245-5.
    1. Bal B. S., Finelli F. C., Shope T. R., Koch T. R. Nutritional deficiencies after bariatric surgery. Nature Reviews Endocrinology. 2012;8(9):544–556. doi: 10.1038/nrendo.2012.48.
    1. Mischke M., Arora T., Tims S., et al. Specific synbiotics in early life protect against diet-induced obesity in adult mice. Diabetes, Obesity and Metabolism. 2018;20(6):1408–1418. doi: 10.1111/dom.13240.
    1. Cani P. D., Possemiers S., Van de Wiele T., et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58(8):1091–1103. doi: 10.1136/gut.2008.165886.
    1. Choi B. R., Kwon E. Y., Kim H. J., Choi M. S. Role of synbiotics containing d-allulose in the alteration of body fat and hepatic lipids in diet-induced obese mice. Nutrients. 2018;10(11) doi: 10.3390/nu10111797.
    1. Tunapong W., Apaijai N., Yasom S., et al. Chronic treatment with prebiotics, probiotics and synbiotics attenuated cardiac dysfunction by improving cardiac mitochondrial dysfunction in male obese insulin-resistant rats. European Journal of Nutrition. 2018;57(6):2091–2104. doi: 10.1007/s00394-017-1482-3.
    1. Kim J., Yun J. M., Kim M. K., Kwon O., Cho B. Lactobacillus gasseri BNR17 supplementation reduces the visceral fat accumulation and waist circumference in obese adults: a randomized, double-blind, placebo-controlled trial. Journal of Medicinal Food. 2018;21(5):454–461. doi: 10.1089/jmf.2017.3937.
    1. Lau E., Neves J. S., Ferreira-Magalhaes M., Carvalho D., Freitas P. Probiotic ingestion, obesity, and metabolic-related disorders: results from NHANES, 1999–2014. Nutrients. 2019;11(7) doi: 10.3390/nu11071482.
    1. Szulinska M., Loniewski I., van Hemert S., Sobieska M., Bogdanski P. Dose-dependent effects of multispecies probiotic supplementation on the lipopolysaccharide (LPS) level and cardiometabolic profile in obese postmenopausal women: a 12-week randomized clinical trial. Nutrients. 2018;10(6) doi: 10.3390/nu10060773.
    1. Szulinska M., Loniewski I., Skrypnik K., et al. Multispecies probiotic supplementation favorably affects vascular function and reduces arterial stiffness in obese postmenopausal women-A 12-week placebo-controlled and randomized clinical study. Nutrients. 2018;10(11) doi: 10.3390/nu10111672.
    1. Mohammadi-Sartang M., Bellissimo N., Totosy de Zepetnek J. O., et al. The effect of daily fortified yogurt consumption on weight loss in adults with metabolic syndrome: a 10-week randomized controlled trial. Nutrition, Metabolism and Cardiovascular Diseases. 2018;28(6):565–574. doi: 10.1016/j.numecd.2018.03.001.
    1. Shamseer L., Moher D., Clarke M., et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ. 2015;350 doi: 10.1136/bmj.i4086.g7647
    1. De Vrese M., Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Advances in Biochemical Engineering/Biotechnology. 2018;111:1–66. doi: 10.1007/10_2008_097.
    1. Higgins J. P., Altman D. G., Gotzsche P. C., et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343 doi: 10.1136/bmj.d5928.d5928
    1. Higgins J. P. T., Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 2011. .
    1. Mokhtari Z., Karbaschian Z., Pazouki A., et al. The effects of probiotic supplements on blood markers of endotoxin and lipid peroxidation in patients undergoing gastric bypass surgery; a randomized, double-blind, placebo-controlled, clinical trial with 13 Months follow-up. Obesity Surgery. 2019;29(4):1248–1258. doi: 10.1007/s11695-018-03667-6.
    1. Fernandes R., Beserra B. T., Mocellin M. C., et al. Effects of prebiotic and synbiotic supplementation on inflammatory markers and anthropometric indices after roux-en-Y gastric bypass: a randomized, triple-blind, placebo-controlled pilot study. Journal of Clinical Gastroenterology. 2016;50(3):208–217. doi: 10.1097/mcg.0000000000000328.
    1. Woodard G. A., Encarnacion B., Downey J. R., et al. Probiotics improve outcomes after Roux-en-Y gastric bypass surgery: a prospective randomized trial. Journal of Gastrointestinal Surgery. 2009;13(7):1198–1204. doi: 10.1007/s11605-009-0891-x.
    1. Sherf-Dagan S., Zelber-Sagi S., Zilberman-Schapira G., et al. Probiotics administration following sleeve gastrectomy surgery: a randomized double-blind trial. International Journal of Obesity. 2018;42(2):147–155. doi: 10.1038/ijo.2017.210.
    1. Weiss R., Dziura J., Burgert T. S., et al. Obesity and the metabolic syndrome in children and adolescents. New England Journal of Medicine. 2004;350(23):2362–2374. doi: 10.1056/nejmoa031049.
    1. Choi J., Joseph L., Pilote L. Obesity and C-reactive protein in various populations: a systematic review and meta-analysis. Obesity Reviews. 2013;14(3):232–244. doi: 10.1111/obr.12003.
    1. Suzumura E. A., Bersch-Ferreira A. C., Torreglosa C. R., et al. Effects of oral supplementation with probiotics or synbiotics in overweight and obese adults: a systematic review and meta-analyses of randomized trials. Nutrition Reviews. 2019;77(6):430–450. doi: 10.1093/nutrit/nuz001.
    1. Gomes A. C., de Sousa R. G., Botelho P. B., Gomes T. L., Prada P. O., Mota J. F. The additional effects of a probiotic mix on abdominal adiposity and antioxidant Status: a double-blind, randomized trial. Obesity. 2017;25(1):30–38. doi: 10.1002/oby.21671.
    1. Famouri F., Shariat Z., Hashemipour M., Keikha M., Kelishadi R. Effects of probiotics on nonalcoholic fatty liver disease in obese children and adolescents. Journal of Pediatric Gastroenterology & Nutrition. 2017;64(3):413–417. doi: 10.1097/mpg.0000000000001422.
    1. Ross R., Neeland I. J., Yamashita S., et al. Waist circumference as a vital sign in clinical practice: a consensus statement from the IAS and ICCR working group on visceral obesity. Nature Reviews Endocrinology. 2020;16(3):177–189. doi: 10.1038/s41574-019-0310-7.
    1. Hou X., Chen S., Hu G., et al. Stronger associations of waist circumference and waist-to-height ratio with diabetes than BMI in Chinese adults. Diabetes Research and Clinical Practice. 2019;147:9–18. doi: 10.1016/j.diabres.2018.07.029.
    1. He M., Shi B. Gut microbiota as a potential target of metabolic syndrome: the role of probiotics and prebiotics. Cell & Bioscience. 2017;7:p. 54. doi: 10.1186/s13578-017-0183-1.
    1. Park D. Y., Ahn Y. T., Huh C. S., Jeon S. M., Choi M. S. The inhibitory effect of Lactobacillus plantarum KY1032 cell extract on the adipogenesis of 3T3-L1 Cells. Journal of Medicinal Food. 2011;14(6):670–675. doi: 10.1089/jmf.2010.1355.
    1. Zhang Z., Zhou Z., Li Y., Zhou L., Ding Q., Xu L. Isolated exopolysaccharides from Lactobacillus rhamnosus GG alleviated adipogenesis mediated by TLR2 in mice. Scientific Reports. 2016;6 doi: 10.1038/srep36083.36083
    1. Sorrenti V., Randazzo C. L., Caggia C., et al. Beneficial effects of pomegranate peel extract and probiotics on pre-adipocyte differentiation. Frontiers in Microbiology. 2019;10:p. 660. doi: 10.3389/fmicb.2019.00660.
    1. Lee E., Jung S. R., Lee S. Y., Lee N. K., Paik H. D., Lim S. I. Lactobacillus plantarum strain Ln4 attenuates diet-induced obesity, insulin resistance, and changes in hepatic mRNA levels associated with glucose and lipid metabolism. Nutrients. 2018;10:5. doi: 10.3390/nu10050643.
    1. Choi W. J., Dong H. J., Jeong H. U., et al. Lactobacillus plantarum LMT1-48 exerts anti-obesity effect in high-fat diet-induced obese mice by regulating expression of lipogenic genes. Scientific Reports. 2020;10(1):p. 869. doi: 10.1038/s41598-020-57615-5.
    1. Lee Y., Ba Z., Roberts R. F., et al. Effects of Bifidobacterium animalis subsp. lactis BB-12((R)) on the lipid/lipoprotein profile and short chain fatty acids in healthy young adults: a randomized controlled trial. Nutrition Journal. 2017;16(1):p. 39. doi: 10.1186/s12937-017-0261-6.
    1. Hernandez M. A. G., Canfora E. E., Jocken J. W. E., Blaak E. E. The short-chain fatty acid acetate in body weight control and insulin sensitivity. Nutrients. 2019;11(8) doi: 10.3390/nu11081943.
    1. Lu Y., Fan C., Li P., Lu Y., Chang X., Qi K. Short chain fatty acids prevent high-fat-diet-induced obesity in mice by regulating G protein-coupled receptors and gut microbiota. Scientific Reports. 2016;6 doi: 10.1038/srep37589.37589
    1. Mohammadi H., Ghavami A., Hadi A., Askari G., Symonds M., Miraghajani M. Effects of pro-/synbiotic supplementation on anthropometric and metabolic indices in overweight or obese children and adolescents: a systematic review and meta-analysis. Complementary Therapies in Medicine. 2019;44:269–276. doi: 10.1016/j.ctim.2019.05.008.
    1. Hadi A., Alizadeh K., Hajianfar H., Mohammadi H., Miraghajani M. Efficacy of synbiotic supplementation in obesity treatment: a systematic review and meta-analysis of clinical trials. Critical Reviews in Food Science and Nutrition. 2020;60(4):584–596. doi: 10.1080/10408398.2018.1545218.
    1. Liu L., Li P., Liu Y., Zhang Y. Efficacy of probiotics and synbiotics in patients with nonalcoholic fatty liver disease: a meta-analysis. Digestive Diseases and Sciences. 2019;64(12):3402–3412. doi: 10.1007/s10620-019-05699-z.
    1. Koutnikova H., Genser B., Monteiro-Sepulveda M., et al. Impact of bacterial probiotics on obesity, diabetes and non-alcoholic fatty liver disease related variables: a systematic review and meta-analysis of randomised controlled trials. BMJ Open. 2019;9(3) doi: 10.1136/bmjopen-2017-017995.e017995
    1. Michael D. R., Jack A. A., Masetti G., et al. A randomised controlled study shows supplementation of overweight and obese adults with lactobacilli and bifidobacteria reduces bodyweight and improves well-being. Scientific Reports. 2020;10(1):p. 4183. doi: 10.1038/s41598-020-60991-7.
    1. Dowd J. B., Zajacova A. Long-term obesity and cardiovascular, inflammatory, and metabolic risk in U.S. adults. American Journal of Preventive Medicine. 2014;46(6):578–584. doi: 10.1016/j.amepre.2014.01.016.
    1. Hou X., Chen P., Hu G., et al. Distribution and related factors of cardiometabolic disease stage based on body mass index level in Chinese adults-The National Diabetes and Metabolic Disorders Survey. Diabetes/Metabolism Research and Reviews. 2018;34(2) doi: 10.1002/dmrr.2963.
    1. Song E. J., Han K., Lim T. J., et al. Effect of probiotics on obesity-related markers per enterotype: a double-blind, placebo-controlled, randomized clinical trial. EPMA Journal. 2020;11(1):31–51. doi: 10.1007/s13167-020-00198-y.
    1. Sun J., Buys N. Effects of probiotics consumption on lowering lipids and CVD risk factors: a systematic review and meta-analysis of randomized controlled trials. Annals of Medicine. 2015;47(6):430–440. doi: 10.3109/07853890.2015.1071872.
    1. Zhang Q., Wu Y., Fei X. Effect of probiotics on body weight and body-mass index: a systematic review and meta-analysis of randomized, controlled trials. International Journal of Food Sciences and Nutrition. 2016;67(5):571–580. doi: 10.1080/09637486.2016.1181156.
    1. Borgeraas H., Johnson L. K., Skattebu J., Hertel J. K., Hjelmesaeth J. Effects of probiotics on body weight, body mass index, fat mass and fat percentage in subjects with overweight or obesity: a systematic review and meta-analysis of randomized controlled trials. Obesity Reviews. 2018;19(2):219–232. doi: 10.1111/obr.12626.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere