Correlation between Gut Microbiota, its Metabolic Products, and their Association with Liver Enzymes among Sample of Egyptian Females

Authors

  • Nayera E. Hassan Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Sahar A. El-Masry Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Ayat Nageeb Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt https://orcid.org/0000-0003-0260-0395
  • Mohamed S. El Hussieny Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Aya Khalil Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt https://orcid.org/0000-0003-2727-0126
  • Manal Mouhamed Aly Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Mahmoud A. S. Afify Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Ahmed Ismail Department of Biological Anthropology, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Gamila El-Saeed Department of Medical Biochemistry, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt
  • Adel Hashish Department of Children with Special Needs, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt https://orcid.org/0000-0001-9549-2973
  • Mohamed Selim Department Researches and Applications of Complementary Medicine, Medical Research and Clinical Studies Institute, National Research Centre, Giza, Egypt

DOI:

https://doi.org/10.3889/oamjms.2022.7909

Keywords:

Gut microbiota, Obesity, Liver enzymes, Egyptian females

Abstract

BACKGROUND: Gut microbiota plays critical role in pathogenesis of obesity, liver metabolism and associated diseases.

AIM: The present study aimed to identify existing gut microbiota enterotypes and their metabolic products profiles, and investigate correlation between gut microbiota; body mass index (BMI); and liver enzymes among sample of normal weight and obese Egyptian females.

METHODS: A case-control cross-sectional study included 112 Egyptian females; 82 obese and 30 normal weights; aged 25–60 years. For each  participant, anthropometric measurements (weight, height, and BMI), laboratory investigations (Aspartate amino transferase [AST], Alanine amino transferase [ALT], Short-chain fatty acids [SCFA], and C-reactive protein [CRP]) and microbiota analysis were done.

RESULTS: Obese females had higher significant values of CRP, AST, ALT, SCFA, log Bacteroidetes, Firmicutes, Firmicutes/Bacteroidetes ratio, and Lactobacillus. Among normal weight group, Lactobacillus had significant positive correlations with SCFA, Bifidobacteria, and Firmicutes, and significant negative correlations with AST, ALT, and CRP. While Bifidobacteria had significant negative correlations with height and ALT, Bacteroidetes bacteria had significant positive correlations with SCFA, and significant negative correlations with age and height, Firmicutes bacteria had significant negative  correlations with AST and ALT, and Firmicutes/Bacteroidetes ratio had significant negative correlations with AST, ALT, and SCFA. Among obese group, Lactobacillus and Bifidobacteria had significant negative correlations with Firmicutes/Bacteroidetes ratio, and Firmicutes bacteria had significant negative correlations with ALT.

CONCLUSION: The beneficial Lactobacillus and Bifidobacteria have their good impact on improving obesity status and liver functions.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Plum Analytics Artifact Widget Block

References

Scheithauer TP, Rampanelli E, Nieuwdorp M, Vallance BA, Verchere CB, van Raalte DH, et al. Gut microbiota as a trigger for metabolic inflammation in obesity and Type 2 diabetes. Front Immunol. 2020;11:571731. https://doi.org/10.3389/fimmu.2020.571731 PMid:33178196

Khan MJ, Gerasimidis K, Edwards CA, Shaikh MG. Role of gut microbiota in the aetiology of obesity: Proposed mechanisms and review of the literature. J Obes. 2016;2016:7353642. https://doi.org/10.1155/2016/7353642 PMid:27703805

Thaiss CA, Zmora N, Levy M, Elinav E. Themicrobiome and innate immunity. Nature. 2016;535(7610):65-74. https://doi.org/10.1038/nature18847 PMid:27383981

Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577-91. https://doi.org/10.1038/nrendo.2015.128 PMid:26260141

Hu GX, Chen GR, Xu H, Ge RS, Lin J. Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. Med Hypotheses. 2010;74(1):123-6. https://doi.org/10.1016/j.mehy.2009.07.022 PMid:19665312

Muscogiuri G, Cantone E, Cassarano S, Tuccinardi D, Barrea L, Savastano S, et al. Gut microbiota: A new path to treat obesity. Int J Obes Suppl. 2019;9(1):10-9. https://doi.org/10.1038/s41367-019-0011-7 PMid:31391921

Hoyles L, Fernández-Real JM, Federici M, Serino M, Abbott J, Charpentier J, et al. Molecular phenomics and metagenomics of hepatic steatosis in non-diabetic obese women. Nat Med. 2018;24(7):1070-80. https://doi.org/10.1038/s41591-018-0061-3. PMid:29942096

Li R, Mao Z, Ye X, Zuo T. Human gut microbiome and liver diseases: From correlation to causation. Microorganisms. 2021;9(5):1017. https://doi.org/10.3390/microorganisms9051017 PMid:34066850

Steinvil A, Shapira I, Ben-Bassat OK, Cohen M, Vered Y, Berliner S, et al. The association of higher levels of within-normal-limits liver enzymes and the prevalence of the metabolic syndrome. Cardiovasc Diabetol. 2010;9:30. https://doi.org/10.1186/1475-2840-9-30 PMid:20633271

Mostafa SA, Khunti K, Morris DH, Webb D, Srinivasan BT, Davies MJ. Can liver enzymes predict progression from prediabetes to Type 2 diabetes independent of factors associated with the metabolic syndrome in white Europeans and South Asians? Diabetologia. 2012;55:S135.

Noronha JA, Medeiros CC, Ada SC, Gonzaga NC, Ramos AT, Ramos AL. C-reactive protein and its relation to high blood pressure in overweight or obese children and adolescents. Rev Paul Pediatr. 2013;31(3):331-7. https://doi.org/10.1590/S0103-05822013000300009 PMid:24142315

Faam B, Zarkesh M, Daneshpour MS, Azizi F, Hedayati M. The association between inflammatory markers and obesity-related factors in Tehranian adults: Tehran lipid and glucose study. Iran J Basic Med Sci. 2014;17(8):577-82. PMid:25422750

Hiernaux J, Tanner J. Growth and physical studies. In: Weiner JS, Lourie SA, editors. Human Biology: A Guide to Field Methods. United Kingdom: Blackwell Scientific Publications; 1969.

Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325-40. https://doi.org/10.1194/jlr.R036012 PMid:23821742

Mitra B, Panja M. High sensitive C-reactive protein: A novel biochemical markers and its role in coronary artery disease. J Assoc Physicians India. 2005;53:25-32. PMid:15857009

Wheeler HE, Shah KP, Brenner J, Garcia T, Aquino-Michaels K, GTEx Consortium, et al. Survey of the heritability and sparse architecture of gene expression traits across human tissues. PLoS Genet. 2016;12(11):e1006423. https://doi.org/10.1371/journal.pgen.1006423 PMid:27835642

Leung C, Rivera L, Furness JB, Angus PW. The role of the gut microbiota in NAFLD. Nat Rev Gastroenterol Hepatol. 2016;13(7):412-25. https://doi.org/10.1038/nrgastro.2016.85 PMid:27273168

Aoun A, Darwish F, Hamod N. The influence of the gut microbiome on obesity in adults and the role of probiotics, prebiotics, and synbiotics for weight loss. Prev Nutr Food Sci. 2020;25(2):113-23. https://doi.org/10.3746/pnf.2020.25.2.113 PMid:32676461

Dao MC, Clément K. Gut microbiota and obesity: Concepts relevant to clinical care. Eur J Intern Med. 2018;48:18-24. https://doi.org/10.1016/j.ejim.2017.10.005 PMid:29110901

Aron-Wisnewsky J, Prifti E, Belda E, Ichou F, Kayser BD, Dao MC, et al. Major microbiota dysbiosis in severe obesity: Fate after bariatric surgery. Gut. 2018;68(1):70-82. https://doi.org/10.1136/gutjnl-2018-316103 PMid:29899081

Ignacio A, Fernandes MR, Rodrigues VA, Groppo FC, Cardoso AL, Avila-Campos MJ, et al. Correlation between body mass index and faecalmicrobiota from children. Clin Microbiol Infect. 2016;22(3):258.e1-8. https://doi.org/10.1016/j.cmi.2015.10.031 PMid:26551842

Jin J, Cheng R, Ren Y, Shen X, Wang J, Xue Y, et al. Distinctive gut microbiota in patients with overweight and obesity with dyslipidemia and its responses to long-term orlistat and ezetimibe intervention: A randomized controlled open-label trial. Front Pharmacol. 2021;12:732541. https://doi.org/10.3389/ fphar.2021.732541 PMid:34512358

Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond). 2008;32(11):1720-4. https://doi.org/10.1038/ijo.2008.155 PMid:18779823

Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TM, Comelli EM. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes. 2014;4(6):e121. https://doi.org/10.1038/nutd.2014.23 PMid:24979150

Koliada A, Syzenko G, Moseiko V, Budovska L, Puchkov K, Perederiy V, Gavalko Y, Dorofeyev A, Romanenko M, Tkach S, Sineok L, Lushchak O, Vaiserman A. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17(1):120. https://doi.org/10.1186/s12866-017-1027-1 PMid:28532414

Palmas, V., Pisanu, S., Madau, V., Casula E, Deledda A, Cusano R, et al. Gut microbiota markers associated with obesity and overweight in Italian adults. Sci Rep. 2021;11(1):5532. https://doi.org/10.1038/s41598-021-84928-w PMid:33750881

Duan M, Wang Y, Zhang Q, Zou R, Guo M, Zheng H. Characteristics of gut microbiota in people with obesity. PLoS One. 2021;16(8):e0255446. https://doi.org/10.1371/journal.pone.0255446 PMid:34375351

Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, et al. The Firmicutes/Bacteroidetes ratio: A relevant marker of gut dysbiosis in obese patients? Nutrients. 2020;12(5):1474. https://doi.org/10.3390/nu12051474 PMid:32438689

Lê KA, Li Y, Xu X, Yang W, Liu T, Zhao X, et al. Alterations in fecal Lactobacillus and Bifidobacterium species in Type 2 diabetic patients in Southern China population. Front Physiol. 2013;3:496. https://doi.org/10.3389/fphys.2012.00496 PMid:23386831

Long J, Cai Q, Steinwandel M, Hargreaves MK, Bordenstein SR, Blot WJ, et al. Association of oral microbiome with Type 2 diabetes risk. J Periodontal Res. 2017;52(3):636-43. https://doi.org/10.1111/jre.12432 PMid:28177125

Collado MC, Isolauri E, Laitinen K, Salminen S. Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: A prospective follow-up study initiated in early pregnancy. Am J Clin Nutr. 2010;92(5):1023-30. https://doi.org/10.3945/ajcn.2010.2987 PMid:20844065

Begley M, Hill C, Gahan CG. Bile salt hydrolase activity in probiotics. Appl Environ Microbiol. 2006;72(3):1729-38. https://doi.org/10.1128/AEM.72.3.1729-1738.2006 PMid:16517616

Kikuchi K, Ben Othman M, Sakamoto K. Sterilized Bifidobacteria suppressed fat accumulation and blood glucose level. Biochem Biophys Res Commun. 2018;501(4):1041-7. https://doi.org/10.1016/j.bbrc.2018.05.105 PMid:29777696

Ji YS, Kim HN, Park HJ, Lee JE, Yeo SY, Yang JS, et al. Modulation of the murine microbiome with a concomitant anti-obesity effect by Lactobacillus rhamnosus GG and Lactobacillus sakei NR28. Benef Microbes. 2012;3(1):13-22. https://doi.org/10.3920/BM2011.0046 PMid:22348905

Ji Y, Park S, Park H, Hwang E, Shin H, Pot B, et al. Modulation of Active Gut Microbiota by Lactobacillus rhamnosus GG in a diet induced obesity murine model. Front Microbiol. 2018;9:710. https://doi.org/10.3389/fmicb.2018.00710 PMid:29692770

Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, et al. Gut microbiota functions: Metabolism of nutrients and other food components. Eur J Nutr. 2018;57(1):1-24. https://doi.org/10.1007/s00394-017-1445-8 PMid:28393285

Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun. 2013;4:1829. https://doi.org/10.1038/ncomms2852 PMid:23652017

Tseng CH, Wu CY. The gut microbiome in obesity. J Formos Med Assoc. 2019;118 Suppl 1:S3-9. https://doi.org/10.1016/j.jfma.2018.07.009 PMid:30057153

Shoaie S, Karlsson F, Mardinoglu A, Nookaew I, Bordel S, Nielsen J. Understanding the interactions between bacteria in the human gut through metabolic modeling. Sci Rep. 2013;3:2532. https://doi.org/10.1038/srep02532 PMid:23982459

Wilmanski T, Diener C, Rappaport N, Patwardhan S, Wiedrick J, Lapidus J, et al. Gut microbiome pattern reflects healthy ageing and predicts survival in humans. Nat Metab. 2021;3(2):274-86. https://doi.org/10.1038/s42255-021-00348-0 PMid:33619379

Albhaisi SA, Bajaj JS, Sanyal AJ. Role of gut microbiota in liver disease. Am J Physiol Gastrointest Liver Physiol. 2020;318(1):G84-98. https://doi.org/10.1152/ajpgi.00118.2019 PMid:31657225

Kirpich IA, Solovieva NV, Leikhter SN, Shidakova NA, Lebedeva OV, Sidorov PI, et al. Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: A pilot study. Alcohol. 2008;42(8):675-82. https://doi.org/10.1016/j.alcohol.2008.08.006 PMid:19038698

Gao X, Zhu Y, Wen Y, Liu G, Wan C. Efficacy of probiotics in non-alcoholic fatty liver disease in adult and children: A meta-analysis of randomized controlled trials. Hepatol Res. 2016;46(12):1226-33. https://doi.org/10.1111/hepr.12671. PMid:26866817

Sproston NR, Ashworth JJ. Role of C-reactive protein at sites of inflammation and infection. Front Immunol. 2018;9:754. https://doi.org/10.3389/fimmu.2018.00754. PMid:29706967

Rajkumar H, Mahmood N, Kumar M, Varikuti SR, Challa HR, Myakala SP. 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. Mediators Inflamm. 2014;2014:348959. https://doi.org/10.1155/2014/348959 PMid:24795503

Mazidi M, Rezaie P, Ferns GA, Vatanparast H. Impact of probiotic administration on serum C-reactive protein concentrations: Systematic review and meta-analysis of randomized control trials. Nutrients. 2017;9(1):20. https://doi.org/10.3390/nu9010020 PMid:28054937

Downloads

Published

2021-12-19

How to Cite

1.
Hassan NE, El-Masry SA, Nageeb A, El Hussieny MS, Khalil A, Aly MM, Afify MAS, Ismail A, El-Saeed G, Hashish A, Selim M. Correlation between Gut Microbiota, its Metabolic Products, and their Association with Liver Enzymes among Sample of Egyptian Females. Open Access Maced J Med Sci [Internet]. 2021 Dec. 19 [cited 2026 Oct. 17];10(B):1797-804. Available from: https://oamjms.eu/index.php/mjms/article/view/7909

Issue

Section

Gastroenterohepatology

Categories