Impact of exercise on epithelial injury of gastrointestinal membrane associated with levels of circulating I-FABP - A systematic review and meta-analysis of randomized control trial
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Aim: Intense exercise promotes intestinal injury in the gastrointestinal tract of humans and a substantial upsurge in intestinal permeability indicating gut barrier dysfunction. Design: Systematic review and meta-analysis Objective: The goal line for this systematic review and meta-analysis was to investigate the consequence of a strenuous workout session on Intestinal epithelial cells (IECs) injury of gastrointestinal membrane and permeability in healthy persons. Methods: Through May 2023, PubMed, EMBASE, Scopus, and Web of Science were searched. Studies were included evaluating intestinal Fatty Acid Binding Protein (I-FABP) of gut permeability and gut cell injury following a solitary strenuous workout. Results: 18 studies showed a mean difference of 488.36 [ 95% CI 280.35; 696.37] in I-FABP post-exercise using a random effects model. The studies were heterogeneous, with a 95% prediction interval of − 427.52 to 1404.24. I-FABP, as a measure of gut injury, had a significant and moderate impact magnitude in disturbing the epithelial lining of the intestinal membrane. Conclusion: This project's decisions establish that a sole strenuous exercise session elevates gut permeability and damage to healthy contributors. The study has been registered with PROSPERO (CRD42023387126).
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1. van Wijck K, Wijnands KA, Meesters DM, Boonen B, van Loon LJ, Buurman WA, et al. L-citrulline improves splanchnic perfusion and reduces gut injury during exercise. Med Sci Sports Exerc. 2014;46(11):2039-46. DOI: https://doi.org/10.1249/MSS.0000000000000332
2. Wallett A, Périard JD, Saunders P, McKune A. Effect of Exercising in the Heat on Intestinal Fatty Acid-Binding Protein, Endotoxins, and Lipopolysaccharide-Binding Protein Markers in Trained Athletic Populations: A Systematic Literature Review. Int J Sport Nutr Exerc Metab. 2021;31(4):359-68. DOI: https://doi.org/10.1123/ijsnem.2021-0040
3. Kung S, Vakula MN, Kim Y, England DL, Bergeson J, Bressel E, et al. No effect of a dairy-based, high flavonoid pre-workout beverage on exercise-induced intestinal injury, permeability, and inflammation in recreational cyclists: A randomized controlled crossover trial. PLoS One. 2022;17(11):e0277453. DOI: https://doi.org/10.1371/journal.pone.0277453
4. Wang F, Wang X, Liu Y, Zhang Z. Effects of Exercise-Induced ROS on the Pathophysiological Functions of Skeletal Muscle. Oxid Med Cell Longev. 2021;2021:3846122. DOI: https://doi.org/10.1155/2021/3846122
5. JanssenDuijghuijsen LM, Mensink M, Lenaerts K, Fiedorowicz E, van Dartel DA, Mes JJ, et al. The effect of endurance exercise on intestinal integrity in well-trained healthy men. Physiol Rep. 2016;4(20). DOI: https://doi.org/10.14814/phy2.12994
6. E. Shaaban A, E. Alfqy O, K. Shaaban H, A. Maqsoud Y, Assar E. Potential role of serum intestinal fatty acid-binding protein as a marker for early prediction and diagnosis of necrotizing enterocolitis in preterm neonates. Journal of Indian Association of Pediatric Surgeons. 2021;26(6):393-400. DOI: https://doi.org/10.4103/jiaps.JIAPS_218_20
7. Zhong J, Chen J, Cao M, Fang L, Wang Z, Liao J, et al. Elevated plasma intestinal fatty acid binding protein and aberrant lipid metabolism predict post-stroke depression. Heliyon. 2022;8(11):e11848. DOI: https://doi.org/10.1016/j.heliyon.2022.e11848
8. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. DOI: https://doi.org/10.1136/bmj.n71
9. McGowan J, Sampson M, Salzwedel DM, Cogo E, Foerster V, Lefebvre C. PRESS Peer Review of Electronic Search Strategies: 2015 Guideline Statement. J Clin Epidemiol. 2016;75:40-6. DOI: https://doi.org/10.1016/j.jclinepi.2016.01.021
10. Watkins JD, Carter S, Atkinson G, Koumanov F, Betts JA, Holst JJ, et al. Glucagon-like peptide-1 secretion in people with versus without type 2 diabetes: a systematic review and meta-analysis of cross-sectional studies. Metabolism. 2023;140:155375. DOI: https://doi.org/10.1016/j.metabol.2022.155375
11. Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Medical Research Methodology. 2014;14(1):135. DOI: https://doi.org/10.1186/1471-2288-14-135
12. Higgins JP, Savović J, Page MJ, Elbers RG, Sterne JA. Assessing risk of bias in a randomized trial. Cochrane handbook for systematic reviews of interventions. 2019:205-28. DOI: https://doi.org/10.1002/9781119536604.ch8
13. Rücker G, Schwarzer G. Beyond the forest plot: The drapery plot. Res Synth Methods. 2021;12(1):13-9. DOI: https://doi.org/10.1002/jrsm.1410
14. Shamim MA, Dwivedi P, Padhi BK. Beyond the funnel plot: The advantages of Doi plots and prediction intervals in meta-analyses. Asian J Psychiatr. 2023;84:103550. DOI: https://doi.org/10.1016/j.ajp.2023.103550
15. Furuya-Kanamori L, Barendregt JJ, Doi SAR. A new improved graphical and quantitative method for detecting bias in meta-analysis. Int J Evid Based Healthc. 2018;16(4):195-203. DOI: https://doi.org/10.1097/XEB.0000000000000141
16. Willis BH, Riley RD. Measuring the statistical validity of summary meta-analysis and meta-regression results for use in clinical practice. Stat Med. 2017;36(21):3283-301. DOI: https://doi.org/10.1002/sim.7372
17. Karhu E, Forsgård RA, Alanko L, Alfthan H, Pussinen P, Hämäläinen E, et al. Exercise and gastrointestinal symptoms: running-induced changes in intestinal permeability and markers of gastrointestinal function in asymptomatic and symptomatic runners. Eur J Appl Physiol. 2017;117(12):2519-26. DOI: https://doi.org/10.1007/s00421-017-3739-1
18. Kartaram S, Mensink M, Teunis M, Schoen E, Witte G, Janssen Duijghuijsen L, et al. Plasma citrulline concentration, a marker for intestinal functionality, reflects exercise intensity in healthy young men. Clin Nutr. 2019;38(5):2251-8. DOI: https://doi.org/10.1016/j.clnu.2018.09.029
19. McKenna Z, Berkemeier Q, Naylor A, Kleint A, Gorini F, Ng J, et al. Bovine colostrum supplementation does not affect plasma I-FABP concentrations following exercise in a hot and humid environment. European Journal of Applied Physiology. 2017;117(12):2561-7. DOI: https://doi.org/10.1007/s00421-017-3743-5
20. Morrison S, Cheung S, Cotter J. Bovine colostrum, training status, and gastrointestinal permeability during exercise in the heat: A placebo-controlled double-blind study. Applied Physiology, Nutrition, and Metabolism. 2014;39:1-13. DOI: https://doi.org/10.1139/apnm-2013-0583
21. Pugh JN, Sage S, Hutson M, Doran DA, Fleming SC, Highton J, et al. Glutamine supplementation reduces markers of intestinal permeability during running in the heat in a dose-dependent manner. European Journal of Applied Physiology. 2017;117(12):2569-77. DOI: https://doi.org/10.1007/s00421-017-3744-4
22. Pugh J, Impey S, Doran D, Fleming S, Morton J, Close G. Acute high-intensity interval running increases markers of gastrointestinal damage and permeability but not gastrointestinal symptoms. Applied Physiology Nutrition and Metabolism. 2017;42. DOI: https://doi.org/10.1139/apnm-2016-0646
23. Sheahen BL, Fell JW, Zadow EK, Hartley TF, Kitic CM. Intestinal damage following short-duration exercise at the same relative intensity is similar in temperate and hot environments. Appl Physiol Nutr Metab. 2018;43(12):1314-20. DOI: https://doi.org/10.1139/apnm-2018-0057
24. Snipe RMJ, Khoo A, Kitic CM, Gibson PR, Costa RJS. Carbohydrate and protein intake during exertional heat stress ameliorates intestinal epithelial injury and small intestine permeability. Appl Physiol Nutr Metab. 2017;42(12):1283-92. DOI: https://doi.org/10.1139/apnm-2017-0361
25. Snipe RMJ, Costa RJS. Does the temperature of water ingested during exertional-heat stress influence gastrointestinal injury, symptoms, and systemic inflammatory profile? J Sci Med Sport. 2018;21(8):771-6. DOI: https://doi.org/10.1016/j.jsams.2017.12.014
26. Snipe RMJ, Khoo A, Kitic CM, Gibson PR, Costa RJS. The impact of exertional-heat stress on gastrointestinal integrity, gastrointestinal symptoms, systemic endotoxin and cytokine profile. European Journal of Applied Physiology. 2018;118(2):389-400. DOI: https://doi.org/10.1007/s00421-017-3781-z
27. Snipe RMJ, Khoo A, Kitic CM, Gibson PR, Costa RJS. The Impact of Mild Heat Stress During Prolonged Running On Gastrointestinal Integrity, Gastrointestinal Symptoms, Systemic Endotoxin and Cytokine Profiles. Int J Sports Med. 2018. DOI: https://doi.org/10.1055/s-0043-122742
28. Szymanski MC, Gillum TL, Gould LM, Morin DS, Kuennen MR. Short-term dietary curcumin supplementation reduces gastrointestinal barrier damage and physiological strain responses during exertional heat stress. J Appl Physiol (1985). 2018;124(2):330-40. DOI: https://doi.org/10.1152/japplphysiol.00515.2017
29. van Wijck K, Lenaerts K, van Loon LJ, Peters WH, Buurman WA, Dejong CH. Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men. PLoS One. 2011;6(7):e22366. DOI: https://doi.org/10.1371/journal.pone.0022366
30. Van Wijck K, Lenaerts K, Van Bijnen AA, Boonen B, Van Loon LJC, Dejong CHC, et al. Aggravation of exercise-induced intestinal injury by Ibuprofen in athletes. Med Sci Sports Exerc. 2012;44(12):2257-62. DOI: https://doi.org/10.1249/MSS.0b013e318265dd3d
31. Tataka Y, Haramura M, Hamada Y, Ono M, Toyoda S, Yamada T, et al. Effects of oral cystine and glutamine on exercise-induced changes in gastrointestinal permeability and damage markers in young men. Eur J Nutr. 2022;61(5):2331-9. DOI: https://doi.org/10.1007/s00394-022-02806-1
32. Costa RJS, Mika AS, McCubbin AJ. The impact of exercise modality on exercise-induced gastrointestinal syndrome and associated gastrointestinal symptoms. J Sci Med Sport. 2022;25(10):788-93. DOI: https://doi.org/10.1016/j.jsams.2022.07.003
33. March DS, Marchbank T, Playford RJ, Jones AW, Thatcher R, Davison G. Intestinal fatty acid-binding protein and gut permeability responses to exercise. Eur J Appl Physiol. 2017;117(5):931-41. DOI: https://doi.org/10.1007/s00421-017-3582-4
34. March DS, Jones AW, Thatcher R, Davison G. The effect of bovine colostrum supplementation on intestinal injury and circulating intestinal bacterial DNA following exercise in the heat. Eur J Nutr. 2019;58(4):1441-51. DOI: https://doi.org/10.1007/s00394-018-1670-9
35. Ribeiro FM, Petriz B, Marques G, Kamilla LH, Franco OL. Is There an Exercise-Intensity Threshold Capable of Avoiding the Leaky Gut? Front Nutr. 2021;8:627289. DOI: https://doi.org/10.3389/fnut.2021.627289
36. Sadowska-Krępa E, Rozpara M, Rzetecki A, Bańkowski S, Żebrowska A, Pilch W. Strenuous 12-h run elevates circulating biomarkers of oxidative stress, inflammation and intestinal permeability in middle-aged amateur runners: A preliminary study. PLoS One. 2021;16(4):e0249183. DOI: https://doi.org/10.1371/journal.pone.0249183
37. Lau E, Marques C, Pestana D, Santoalha M, Carvalho D, Freitas P, et al. The role of I-FABP as a biomarker of intestinal barrier dysfunction driven by gut microbiota changes in obesity. Nutrition & Metabolism. 2016;13(1):31. DOI: https://doi.org/10.1186/s12986-016-0089-7
38. Costa RJS, Snipe RMJ, Kitic CM, Gibson PR. Systematic review: exercise-induced gastrointestinal syndrome-implications for health and intestinal disease. Aliment Pharmacol Ther. 2017;46(3):246-65. DOI: https://doi.org/10.1111/apt.14157
39. Adriaanse MP, Tack GJ, Passos VL, Damoiseaux JG, Schreurs MW, van Wijck K, et al. Serum I-FABP as marker for enterocyte damage in coeliac disease and its relation to villous atrophy and circulating autoantibodies. Aliment Pharmacol Ther. 2013;37(4):482-90. DOI: https://doi.org/10.1111/apt.12194
40. Chantler S, Griffiths A, Phibbs P, Roe G, Ramírez-López C, Davison G, et al. The effect of rugby training on indirect markers of gut permeability and gut damage in academy level rugby players. Eur J Appl Physiol. 2022;122(12):2545-54. DOI: https://doi.org/10.1007/s00421-022-05027-w
41. Snipe RMJ, Khoo A, Kitic CM, Gibson PR, Costa RJS. The impact of exertional-heat stress on gastrointestinal integrity, gastrointestinal symptoms, systemic endotoxin and cytokine profile. Eur J Appl Physiol. 2018;118(2):389-400. DOI: https://doi.org/10.1007/s00421-017-3781-z