Review
BibTex RIS Cite

Can the gastrointestinal system alter liver damage caused by COVID-19?

Year 2024, Volume: 41 Issue: 2, 397 - 406, 19.05.2024

Abstract

Our gastrointestinal system, often referred to as our "second brain," is grappling with the devastating effects of COVID-19, a disease that has plagued recent years. Researchers are investigating how bacteria in the intestinal microflora may contribute to or mitigate liver damage caused by COVID-19. Despite the limited number of studies, the fight against liver organ damage by the gastrointestinal system, which is our second brain is important. All original articles published in English until March 01, 2020, were retrieved via a library-assisted literature search from PubMed/MEDLINE, Excerpta Medica Database (EMBASE), and Web of Science. A total of nine articles (2.188 patients) were found eligible for inclusion. Effect size and 95% confidence interval were evaluated in this study. The randomized trials exhibit a noteworthy level of heterogeneity (p<0.05), and upon scrutinizing the funnel plot, there is no discernible indication of publication bias. According to the meta-analysis tree graph, the weights of the studies are significantly to the right of the 2 vertical lines. The confidence interval of each study has significant weights. According to the study findings, the interaction of the intestinal flora and the immune system showed us that there is an area that we need to investigate against the COVID-19 disease. For many years, research has tried to explain how the signaling pathways in the intestinal tract are related to the brain. The study revealed that our digestive system plays a crucial role as an auxiliary component of our brain. Future studies should uncover the main ways of this communication.

References

  • Matijašić M., Meštrović T., Paljetak HČ, Perić M, Barešić A. & Verbanac D. (2020). Gut Microbiota beyond Bacteria-Mycobiome, Virome, Archaeome, and Eukaryotic Parasites in IBD. International journal of molecular sciences, 11;21(8):2668. https://doi.org/ 10.3390/ijms21082668
  • Vemuri R., Shankar E.M., Chieppa M., Eri R. & Kavanagh K. (2020). Beyond Just Bacteria: Functional Biomes in the Gut Ecosystem Including Virome, Mycobiome, Archaeome and Helminths. Microorganisms, 8(4):483. https://doi.org/ 10.3390/microorganisms8040483
  • Davis C.D. (2016). The Gut Microbiome and Its Role in Obesity. Nutrition today, 51(4):167-174. https://doi.org/ 10.1097/NT.0000000000000167
  • Tomasello G., Mazzola M., Jurjus A., Cappello F., Carini F. & Damiani P. (2017). The fingerprint of the human gastrointestinal tract microbiota: a hypothesis of molecular mapping. Journal of Biological Regulators and Homeostatic Agents, 31(1):245-249. https://doi.org/ 28337900
  • Dill-McFarland K.A., Tang Z.Z., Kemis J.H., Kerby R.L., Chen G. & Palloni A. (2019). Close social relationships correlate with human gut microbiota composition. Scientific reports, 24;9(1):703. https://doi.org/ 10.1038/s41598-018-37298-9
  • Rees T., Bosch T. & Douglas A.E. (2018). How the microbiome challenges our concept of self. PLoS Biology, 9;16(2):e2005358. https://doi.org/ 10.1371/journal.pbio.2005358
  • Conlon M.A. & Bird A.R. (2014). The impact of diet and lifestyle on gut microbiota and human health. Nutrients, 24;7(1):17-44. https://doi.org/ 10.3390/nu7010017
  • Krajmalnik-Brown R., Ilhan Z.E., Kang D.W. & DiBaise J.K. (2012). Effects of gut microbes on nutrient absorption and energy regulation. Nutrition in Clinical Practice, 27(2):201-14. https://doi.org/ 10.1177/0884533611436116
  • Morowitz M.J., Carlisle E.M. & Alverdy J.C. (2011). Contributions of intestinal bacteria to nutrition and metabolism in the critically ill. Surgical oncology clinics of North America, 91(4):771-85, https://doi.org/ 10.1016/j.suc.2011.05.001
  • Clapp M., Aurora N., Herrera L., Bhatia M., Wilen E. & Wakefield S. (2017). Gut microbiota's effect on mental health: The gut-brain axis. International journal of clinical practice. 15;7(4):987. https://doi.org/ 10.4081/cp.2017.987
  • Butler M.I., Mörkl S., Sandhu K.V., Cryan J.F. & Dinan T.G. (2019). The Gut Microbiome and Mental Health: What Should We Tell Our Patients?: Le microbiote Intestinal et la Santé Mentale : que Devrions-Nous dire à nos Patients? The Canadian Journal of Psychiatry, 64(11):747-760. https://doi.org/ 10.1177/0706743719874168
  • Taylor V.H. (2019). The microbiome and mental health: Hope or hype? Journal of Psychiatry and Neuroscience, 1;44(4):219-222. https://doi.org/ 10.1503/jpn.190110
  • Dantzer R. (2018). Neuroimmune Interactions: From the Brain to the Immune System and Vice Versa. Physiological reviews, 1;98(1):477-504. https://doi.org/ 10.1152/physrev.00039.2016
  • Rivest S. (2009). Regulation of innate immune responses in the brain. Nature reviews immunology, 9(6):429-39. https://doi.org/ 10.1038/nri2565
  • Hanke M.L. & Kielian T. (2011). Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clinical science, 121(9):367-87. https://doi.org/ 10.1042/CS20110164
  • Nobel Y.R., Phipps M. & Verna E.C. (2021). COVID-19 and Effect on Liver Transplant. Current treatment options in gastroenterology,19(3):483-499. https://doi.org/ 10.1007/s11938-021-00355-w
  • Choudhary N.S., Dhampalwar S., Saraf N. & Soin A.S. (2021). Outcomes of COVID-19 in Patients with Cirrhosis or Liver Transplantation. Journal of Clinical and Experimental Hepatology, 11(6):713-719. https://doi.org/ 10.1016/j.jceh.2021.05.003
  • Schult D., Reitmeier S., Koyumdzhieva P., Lahmer T., Middelhoff M. & Erber J. (2022). Gut bacterial dysbiosis and instability is associated with the onset of complications and mortality in COVID-19. Gut Microbes, 14(1):2031840. https://doi.org/ 10.1080/19490976.2022.2031840
  • Cheemerla S. & Balakrishnan M. (2021). Global Epidemiology of Chronic Liver Disease. Clin Liver Dis (Hoboken), 4;17(5):365-370. https://doi.org/ 10.1002/cld.1061
  • Mallet V., Beeker N., Bouam S., Sogni P. & Pol S. (2021). Demosthenes research group. Prognosis of French COVID-19 patients with chronic liver disease: A national retrospective cohort study for 2020. Journal of hepatology, 75(4):848-855. https://doi.org/ 10.1016/j.jhep.2021.04.052
  • Chadalavada P., Padbidri V., Garg R., Alomari M., Babar A., Kewan T. Et al. (2020). Transaminases are Potential Biomarkers of Disease Severity in COVID-19 Patients: A Single-Center Experience. Cureus, 18;12(11):e11555. https://doi.org/ 10.7759/cureus.11555
  • Kaneko S., Kurosaki M., Nagata K., Taki R., Ueda K. & Hanada S. (2020). Liver injury with COVID-19 based on gastrointestinal symptoms and pneumonia severity. PLoS One, 4;15(11):e0241663. https://doi.org/ 10.1371/journal.pone.0241663
  • Pott-Junior H., Bittencourt N.Q.P., Chacha S.F.G., Luporini R.L., Cominetti M.R. & Anibal F.F. (2021). Elevations in Liver Transaminases in COVID-19: (How) Are They Related? Frontiers of medicine, 15;8:705247. https://doi.org/ 10.3389/fmed.2021.705247
  • Schnabl B. & Brenner D.A. Interactions between the intestinal microbiome and liver diseases. Gastroenterology, 146(6):1513-24. https://doi.org/ 10.1053/j.gastro.2014.01.020
  • Belkaid Y. & Hand T.W. (2014). Role of the microbiota in immunity and inflammation. Cell, 27;157(1):121-41. https://doi.org/ 10.1016/j.cell.2014.03.011
  • Newsome R.C., Gauthier J., Hernandez M.C., Abraham G.E., Robinson T.O., Williams H.B. Et al. (2021). The gut microbiome of COVID-19 recovered patients returns to uninfected status in a minority-dominated United States cohort. Gut Microbes, 13(1):1-15. https://doi.org/10.1080/19490976.2021.1926840
  • Carabotti M., Scirocco A., Maselli M.A. & Severi C. (2015). The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Annals of gastroenterology, 28(2):203-209. https://doi.org/ 25830558
  • Martin C.R., Osadchiy V., Kalani A. & Mayer E.A. (2018). The Brain-Gut-Microbiome Axis. Cellular and Molecular Gastroenterology and Hepatology, 12;6(2):133-148. https://doi.org/ 10.1016/j.jcmgh.2018.04.003
  • Fung T.C., Olson C.A. & Hsiao E.Y. (2017). Interactions between the microbiota, immune and nervous systems in health and disease. Nature neuroscience, 20(2):145-155. https://doi.org/ 10.1038/nn.4476
  • Wang Y. & Kasper L.H. (2014). The role of microbiome in central nervous system disorders. Brain, Behavior, and Immunity, 38:1-12. https://doi.org/ 10.1016/j.bbi.2013.12.015
  • Maeda Y., Motooka D., Kawasaki T., Oki H., Noda Y. & Adachi Y. (2022). Longitudinal alterations of the gut mycobiota and microbiota on COVID-19 severity. BMC infectious diseases, 24;22(1):572. https://doi.org/ 10.1186/s12879-022-07358-7
  • Galland L. (2014). The gut microbiome and the brain. Journal of medicinal food. 17(12):1261-72. https://doi.org/ 10.1089/jmf.2014.7000
  • Madison A. & Kiecolt-Glaser J.K. (2019). Stress, depression, diet, and the gut microbiota: human-bacteria interactions at the core of psychoneuroimmunology and nutrition. Current Opinion in Behavioral Sciences, 28:105-110. https://doi.org/ 10.1016/j.cobeha.2019.01.011
  • Napolitano M. & Covasa M. (2020). Microbiota Transplant in the Treatment of Obesity and Diabetes: Current and Future Perspectives. Frontiers in microbiology, 12;11:590370. https://doi.org/ 10.3389/fmicb.2020.590370
  • Chinna Meyyappan A., Forth E., Wallace C.J.K. & Milev R. (2020). Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review. BMC Psychiatry, 15;20(1):299. https://doi.org/ 10.1186/s12888-020-02654-5
  • Sharon G., Sampson T.R., Geschwind D.H. & Mazmanian S.K. (2016). The Central Nervous System and the Gut Microbiome. Cell, 3;167(4):915-932. https://doi.org/ 10.1016/j.cell.2016.10.027
  • Wiertsema S.P., van Bergenhenegouwen J., Garssen J. & Knippels L.M.J. (2021). The Interplay between the Gut Microbiome and the Immune System in the Context of Infectious Diseases throughout Life and the Role of Nutrition in Optimizing Treatment Strategies. Nutrients, 13(3):886. https://doi.org/ 10.3390/nu13030886
  • Kho Z.Y. & Lal SK. (2018). The Human Gut Microbiome - A Potential Controller of Wellness and Disease. Frontiers in microbiology, 14;9:1835. https://doi.org/ 10.3389/fmicb.2018.01835
  • Martin A.M., Sun E.W., Rogers G.B. & Keating D.J. (2019). The Influence of the Gut Microbiome on Host Metabolism Through the Regulation of Gut Hormone Release. Frontiers in Physiology, 16;10:428. https://doi.org/ 10.3389/fphys.2019.00428
  • Gilbert J.A., Blaser MJ, Caporaso JG, Jansson JK, Lynch SV & Knight R. (2018). Current understanding of the human microbiome. Nature medicine, 10;24(4):392-400. https://doi.org/ 10.1038/nm.4517
  • Conlon M.A. & Bird A.R. (2014). The impact of diet and lifestyle on gut microbiota and human health. Nutrients, 24;7(1):17-44. https://doi.org/ 10.3390/nu7010017
  • Kelly S.A., Nzakizwanayo J., Rodgers A.M., Zhao L., Weiser R. & Tekko I.A. (2021). Antibiotic Therapy and the Gut Microbiome: Investigating the Effect of Delivery Route on Gut Pathogens. ACS infectious diseases, 14;7(5):1283-1296. https://doi.org/ 10.1021/acsinfecdis.1c00081
  • Ramirez J., Guarner F., Bustos Fernandez L., Maruy A., Sdepanian V.L. & Cohen H. (2020). Antibiotics as Major Disruptors of Gut Microbiota. Frontiers in cellular and infection microbiology, 24;10:572912. https://doi.org/ 10.3389/fcimb.2020.572912
  • Ceccarelli G., Borrazzo C., Pinacchio C., Santinelli L., Innocenti G.P., Cavallari E.N. et al. (2021). Oral Bacteriotherapy in Patients With COVID-19: A Retrospective Cohort Study. Frontiers in Nutrition, 11;7:613928. https://doi.org/ 10.3389/fnut.2020.613928
  • Looft T. & Allen H.K. (2012). Collateral effects of antibiotics on mammalian gut microbiomes. Gut Microbes, 3(5):463-7. https://doi.org/ 10.4161/gmic.21288
  • Khlevner J., Park Y. & Margolis K.G. (2018). Brain-Gut Axis: Clinical Implications. Gastrointestinal endoscopy clinics of North America, 47(4):727-739. https://doi.org/ 10.1016/j.gtc.2018.07.002
  • Sasselli V., Pachnis V. & Burns A.J. (2012). The enteric nervous system. (2014). Dev Biol, 366(1): 64-73. https://doi.org/ 10.1016/j.ydbio.2012.01.012
  • Furness J.B., Callaghan B.P., Rivera L.R. & Cho H.J. (2014). The enteric nervous system and gastrointestinal innervation: integrated local and central control. Advances in Experimental Medicine and Biology, 817:39-71. https://doi.org/ 10.1007/978-1-4939-0897-4_3
  • Li J.H., Duan R., Li L., Wood J.D., Wang X.Y. & Shu Y. [Unique characteristics of "the second brain" - The enteric nervous system]. Sheng Li Xue Bao, 2020 Jun 25;72(3):382-390. https://doi.org/ 10.3389/fnagi.2021.698988
  • Arneth B.M. (2018). Gut-brain axis biochemical signalling from the gastrointestinal tract to the central nervous system: gut dysbiosis and altered brain function. Postgraduate medical journal, 94(1114):446-452. https://doi.org/ 10.1136/postgradmedj-2017-135424
  • D'Agata A.L., Wu J., Welandawe MKV, Dutra SVO, Kane B & Groer MW. (2019). Effects of early life NICU stress on the developing gut microbiome. Developmental psychobiology. 61(5):650-660. https://doi.org/ 10.1002/dev.21826
  • Shen H.H. News Feature: Microbes on the mind. (2015). The Proceedings of the National Academy of Sciences, 28;112(30):9143-5. https://doi.org/ 10.1073/pnas.1509590112
  • Gutiérrez-Castrellón P., Gandara-Martí T., Abreu A.T., Nieto-Rufino C.D., López-Orduña E. & Jiménez-Escobar I. (2022). Probiotic improves symptomatic and viral clearance in COVID19 outpatients: a randomized, quadruple-blinded, placebo-controlled trial. Gut Microbes, 14(1):2018899. https://doi.org/ 10.1080/19490976.2021.2018899.
  • Bathina S. & Das U.N. (2015). Brain-derived neurotrophic factor and its clinical implications. Archives of medical sciences, 10;11(6):1164-78. https://doi.org/ 10.5114/aoms.2015.56342
  • Binder D.K. & Scharfman H.E. (2004). Brain-derived neurotrophic factor. Growth Factors, 22(3):123-31. https://doi.org/ 10.1080/08977190410001723308
  • Rodriguez D.M., Benninghoff A.D., Aardema N.D.J., Phatak S. & Hintze K.J. (2019). Basal Diet Determined Long-Term Composition of the Gut Microbiome and Mouse Phenotype to a Greater Extent than Fecal Microbiome Transfer from Lean or Obese Human Donors. Nutrients, 17;11(7):1630. https://doi.org/ 10.3390/nu11071630
  • Luo Y., Zeng B., Zeng L., Du X., Li B. & Huo R. (2018). Gut microbiota regulates mouse behaviors through glucocorticoid receptor pathway genes in the hippocampus. Translational psychiatry, 7;8(1):187. https://doi.org/ 10.1038/s41398-018-0240-5
  • Argou-Cardozo I. & Zeidán-Chuliá (2018). F. Clostridium Bacteria and Autism Spectrum Conditions: A Systematic Review and Hypothetical Contribution of Environmental Glyphosate Levels. Medical Sciences, 4;6(2):29. https://doi.org/10.3390/medsci6020029
  • Wasilewska J. & Klukowski M. (2015). Gastrointestinal symptoms and autism spectrum disorder: links and risks- a possible new overlap syndrome. Pediatric Health, Medicine and Therapeutics, 6:153-166. https://doi.org/ 10.2147/PHMT.S85717
  • Dunn A.B., Jordan S., Baker B.J. & Carlson N.S. (2017). The Maternal Infant Microbiome: Considerations for Labor and Birth. MCN The American Journal of Maternal Child Nursing, 42(6):318-325. https://doi.org/ 10.1097/NMC.0000000000000373
  • Suganya K. & Koo B.S. (2020). Gut-Brain Axis: Role of Gut Microbiota on Neurological Disorders and How Probiotics/Prebiotics Beneficially Modulate Microbial and Immune Pathways to Improve Brain Functions. International journal of molecular sciences, 21(20):7551. https://doi.org/ 10.3390/ijms21207551
  • Chowdhury M.A., Hossain N., Kashem M.A., Shahid M.A. & Alam A. (2020). Immune response in COVID-19: A review. Journal of infection prevention, 13(11):1619-1629. https://doi.org/ 10.1016/j.jiph.2020.07.001
  • Farsi Y., Tahvildari A., Arbabi M., Vazife F., Sechi L.A. & Shahidi Bonjar A.H. (2022). Diagnostic, Prognostic, and Therapeutic Roles of Gut Microbiota in COVID-19: A Comprehensive Systematic Review. Frontiers in cellular and infection microbiology, 4;12:804644. https://doi.org/ 10.3389/fcimb.2022.804644
  • Gagliardi A., Totino V., Cacciotti F., Iebba V., Neroni B. & Bonfiglio G. (2018). Rebuilding the Gut Microbiota Ecosystem. International journal of environmental health research, 7;15(8):1679. https://doi.org/
  • Sun Z., Song Z.G., Liu C., Tan S., Lin S., Zhu J. Et al. (2022). Gut microbiome alterations and gut barrier dysfunction are associated with host immune homeostasis in COVID-19 patients. BMC Medicine, 20;20(1):24. https://doi.org/ 10.1186/s12916-021-02212-0
  • Somsouk M., Estes J.D., Deleage C., Dunham R.M., Albright R. & Inadomi J.M. (2015). Gut epithelial barrier and systemic inflammation during chronic HIV infection. AIDS, 29(1):43-51. https://doi.org/
  • Gold J.E., Okyay R.A., Licht W.E. & Hurley D.J. (2021). Investigation of Long COVID Prevalence and Its Relationship to Epstein-Barr Virus Reactivation. Pathogens, 17;10(6):763. https://doi.org/ 10.3390/pathogens10060763
  • Carvalho T., Krammer F. & Iwasaki A. (2021). The first 12 months of COVID-19: a timeline of immunological insights. Nature reviews Immunology, 21(4):245-256. https://doi.org/ 10.1038/s41577-021-00522-1
  • D'Andrea G. (2015). Quercetin: A flavonol with multifaceted therapeutic applications? Fitoterapia, 106:256-71. https://doi.org/ 10.1016/j.fitote.2015.09.018
  • Górski A., Międzybrodzki R., Żaczek M. & Borysowski J. (2020). Phages in the fight against COVID-19? Future Microbiol, 15:1095-1100. https://doi.org/ 10.2217/fmb-2020-0082
  • Sharma J.N., Al-Omran A. & Parvathy S.S. (2007). Role of nitric oxide in inflammatory diseases. Inflammopharmacology, 15(6):252-9. https://doi.org/ 10.1007/s10787-007-0013-x
  • Vázquez-Torres A. & Bäumler A.J. (2016). Nitrate, nitrite and nitric oxide reductases: from the last universal common ancestor to modern bacterial pathogens. Current Opinion in Microbiology, 29:1-8. https://doi.org/ 10.1016/j.mib.2015.09.002
  • Thota R.N., Acharya S.H. & Garg M.L. (2019). Curcumin and/or omega-3 polyunsaturated fatty acids supplementation reduces insulin resistance and blood lipids in individuals with high risk of type 2 diabetes: a randomised controlled trial. Lipids in Health and Disease, 18(1):31. https://doi.org/ 10.1186/s12944-019-0967-x
  • Davie J.R. (2003). Inhibition of histone deacetylase activity by butyrate. The Journal of Nutrition, 133(7 Suppl):2485S-2493S. https://doi.org/ 10.1093/jn/133.7.2485S
  • Wei Y. & Melas P.A. Wegener G, Mathé A.A., Lavebratt C. (2014). Antidepressant-like effect of sodium butyrate is associated with an increase in TET1 and in 5-hydroxymethylation levels in the Bdnf gene. International Journal of Neuropsychopharmacology, 31;18(2). https://doi.org/ 10.1093/ijnp/pyu032
  • Madempudi R.S., Ahire JJ, Neelamraju J, Tripathi A. & Nanal S. (2019). Randomized clinical trial: the effect of probiotic Bacillus coagulans Unique IS2 vs. placebo on the symptoms management of irritable bowel syndrome in adults. Scientific reports, 21;9(1):12210. https://doi.org/ 10.1038/s41598-019-48554-x
  • Liu Q., Mak J.W.Y., Su Q., Yeoh Y.K., Lui G.C. & Ng S.S.S. (2022). Gut microbiota dynamics in a prospective cohort of patients with post-acute COVID-19 syndrome. Gut, 71(3):544-552. https://doi.org/ 10.1136/gutjnl-2021-325989
  • Hrncir T. (2022). Gut Microbiota Dysbiosis: Triggers, Consequences, Diagnostic and Therapeutic Options. Microorganisms. 10(3):578-643. doi: 10.3390/microorganisms10030578.
  • Tilg H, Adolph TE, Trauner M (2022). Gut-liver axis: Pathophysiological concepts and clinical implications. Microorganism. 34(11):1700-1718. doi: 10.1016/j.cmet.2022.09.017.
  • An C, Chon H, Ku W, Eom S, Seok M, Kim S et al., (2022). Bile Acids: Major Regulator of the Gut Microbiome. Microorganisms. 10(9):1792. doi: 10.3390/microorganisms10091792.
  • Arias N, Arboleya S, Allison J, Kaliszewska A, Higarza SG, Gueimonde M et al., (2020). The Relationship between Choline Bioavailability from Diet, Intestinal Microbiota Composition, and Its Modulation of Human Diseases. Nutrients. 12(8):2340. doi: 10.3390/nu12082340.
  • Latif A, Shehzad A, Niazi S, Zahid A, Ashraf W, Iqbal MW et al., (2023). Probiotics: mechanism of action, health benefits and their application in food industries. Frontiers in Microbiology. 14(1): 21-67. doi: 10.3389/fmicb.2023.1216674.
  • Bax L., Yu L.M., Ikeda N & Moons KGA. (2007). systematic comparison of software dedicated to meta-analysis of causal studies. BMC medical research methodology, 10;7:40. https://doi.org/ 10.1186/1471-2288-7-40
  • Chelakkot C., Ghim J. & Ryu S.H. (2018). Mechanisms regulating intestinal barrier integrity and its pathological implications. Experimental and Molecular Medicine, 16;50(8):1-9. https://doi.org/ 10.1038/s12276-018-0126-x
  • Chowdhury M.A., Hossain N., Kashem M.A., Shahid M.A. & Alam A. (2020). Immune response in COVID-19: A review. Journal of infection prevention, 13(11):1619-1629. https://doi.org/ 10.1016/j.jiph.2020.07.001
  • Dill-McFarland K.A., Tang Z.Z., Kemis J.H., Kerby R.L., Chen G. & Palloni A. (2019). Close social relationships correlate with human gut microbiota composition. Scientific reports, 24;9(1):703. https://doi.org/ 10.1038/s41598-018-37298-9
  • Jin X., Lian J.S., Hu J.H., Gao J., Zheng L. & Zhang Y.M. (2020). Epidemiological, clinical and virological characteristics of 74 cases of coronavirus-infected disease 2019 (COVID-19) with gastrointestinal symptoms. Gut, 69(6):1002-1009. https://doi.org/ 10.1136/gutjnl-2020-320926
  • Suárez-Reyes A. & Villegas-Valverde C.A. (2021). Implications of Low-grade Inflammation in SARS-CoV-2 Immunopathology. MEDICC Review, 23(2):42. https://doi.org/ 10.37757/MR2021.V23.N2.4
  • Yeoh Y.K., Zuo T., Lui G.C., Zhang F. & Liu Q. (2021). Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut, 70(4):698-706. https://doi.org/10.1136/gutjnl-2020-323020
Year 2024, Volume: 41 Issue: 2, 397 - 406, 19.05.2024

Abstract

References

  • Matijašić M., Meštrović T., Paljetak HČ, Perić M, Barešić A. & Verbanac D. (2020). Gut Microbiota beyond Bacteria-Mycobiome, Virome, Archaeome, and Eukaryotic Parasites in IBD. International journal of molecular sciences, 11;21(8):2668. https://doi.org/ 10.3390/ijms21082668
  • Vemuri R., Shankar E.M., Chieppa M., Eri R. & Kavanagh K. (2020). Beyond Just Bacteria: Functional Biomes in the Gut Ecosystem Including Virome, Mycobiome, Archaeome and Helminths. Microorganisms, 8(4):483. https://doi.org/ 10.3390/microorganisms8040483
  • Davis C.D. (2016). The Gut Microbiome and Its Role in Obesity. Nutrition today, 51(4):167-174. https://doi.org/ 10.1097/NT.0000000000000167
  • Tomasello G., Mazzola M., Jurjus A., Cappello F., Carini F. & Damiani P. (2017). The fingerprint of the human gastrointestinal tract microbiota: a hypothesis of molecular mapping. Journal of Biological Regulators and Homeostatic Agents, 31(1):245-249. https://doi.org/ 28337900
  • Dill-McFarland K.A., Tang Z.Z., Kemis J.H., Kerby R.L., Chen G. & Palloni A. (2019). Close social relationships correlate with human gut microbiota composition. Scientific reports, 24;9(1):703. https://doi.org/ 10.1038/s41598-018-37298-9
  • Rees T., Bosch T. & Douglas A.E. (2018). How the microbiome challenges our concept of self. PLoS Biology, 9;16(2):e2005358. https://doi.org/ 10.1371/journal.pbio.2005358
  • Conlon M.A. & Bird A.R. (2014). The impact of diet and lifestyle on gut microbiota and human health. Nutrients, 24;7(1):17-44. https://doi.org/ 10.3390/nu7010017
  • Krajmalnik-Brown R., Ilhan Z.E., Kang D.W. & DiBaise J.K. (2012). Effects of gut microbes on nutrient absorption and energy regulation. Nutrition in Clinical Practice, 27(2):201-14. https://doi.org/ 10.1177/0884533611436116
  • Morowitz M.J., Carlisle E.M. & Alverdy J.C. (2011). Contributions of intestinal bacteria to nutrition and metabolism in the critically ill. Surgical oncology clinics of North America, 91(4):771-85, https://doi.org/ 10.1016/j.suc.2011.05.001
  • Clapp M., Aurora N., Herrera L., Bhatia M., Wilen E. & Wakefield S. (2017). Gut microbiota's effect on mental health: The gut-brain axis. International journal of clinical practice. 15;7(4):987. https://doi.org/ 10.4081/cp.2017.987
  • Butler M.I., Mörkl S., Sandhu K.V., Cryan J.F. & Dinan T.G. (2019). The Gut Microbiome and Mental Health: What Should We Tell Our Patients?: Le microbiote Intestinal et la Santé Mentale : que Devrions-Nous dire à nos Patients? The Canadian Journal of Psychiatry, 64(11):747-760. https://doi.org/ 10.1177/0706743719874168
  • Taylor V.H. (2019). The microbiome and mental health: Hope or hype? Journal of Psychiatry and Neuroscience, 1;44(4):219-222. https://doi.org/ 10.1503/jpn.190110
  • Dantzer R. (2018). Neuroimmune Interactions: From the Brain to the Immune System and Vice Versa. Physiological reviews, 1;98(1):477-504. https://doi.org/ 10.1152/physrev.00039.2016
  • Rivest S. (2009). Regulation of innate immune responses in the brain. Nature reviews immunology, 9(6):429-39. https://doi.org/ 10.1038/nri2565
  • Hanke M.L. & Kielian T. (2011). Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clinical science, 121(9):367-87. https://doi.org/ 10.1042/CS20110164
  • Nobel Y.R., Phipps M. & Verna E.C. (2021). COVID-19 and Effect on Liver Transplant. Current treatment options in gastroenterology,19(3):483-499. https://doi.org/ 10.1007/s11938-021-00355-w
  • Choudhary N.S., Dhampalwar S., Saraf N. & Soin A.S. (2021). Outcomes of COVID-19 in Patients with Cirrhosis or Liver Transplantation. Journal of Clinical and Experimental Hepatology, 11(6):713-719. https://doi.org/ 10.1016/j.jceh.2021.05.003
  • Schult D., Reitmeier S., Koyumdzhieva P., Lahmer T., Middelhoff M. & Erber J. (2022). Gut bacterial dysbiosis and instability is associated with the onset of complications and mortality in COVID-19. Gut Microbes, 14(1):2031840. https://doi.org/ 10.1080/19490976.2022.2031840
  • Cheemerla S. & Balakrishnan M. (2021). Global Epidemiology of Chronic Liver Disease. Clin Liver Dis (Hoboken), 4;17(5):365-370. https://doi.org/ 10.1002/cld.1061
  • Mallet V., Beeker N., Bouam S., Sogni P. & Pol S. (2021). Demosthenes research group. Prognosis of French COVID-19 patients with chronic liver disease: A national retrospective cohort study for 2020. Journal of hepatology, 75(4):848-855. https://doi.org/ 10.1016/j.jhep.2021.04.052
  • Chadalavada P., Padbidri V., Garg R., Alomari M., Babar A., Kewan T. Et al. (2020). Transaminases are Potential Biomarkers of Disease Severity in COVID-19 Patients: A Single-Center Experience. Cureus, 18;12(11):e11555. https://doi.org/ 10.7759/cureus.11555
  • Kaneko S., Kurosaki M., Nagata K., Taki R., Ueda K. & Hanada S. (2020). Liver injury with COVID-19 based on gastrointestinal symptoms and pneumonia severity. PLoS One, 4;15(11):e0241663. https://doi.org/ 10.1371/journal.pone.0241663
  • Pott-Junior H., Bittencourt N.Q.P., Chacha S.F.G., Luporini R.L., Cominetti M.R. & Anibal F.F. (2021). Elevations in Liver Transaminases in COVID-19: (How) Are They Related? Frontiers of medicine, 15;8:705247. https://doi.org/ 10.3389/fmed.2021.705247
  • Schnabl B. & Brenner D.A. Interactions between the intestinal microbiome and liver diseases. Gastroenterology, 146(6):1513-24. https://doi.org/ 10.1053/j.gastro.2014.01.020
  • Belkaid Y. & Hand T.W. (2014). Role of the microbiota in immunity and inflammation. Cell, 27;157(1):121-41. https://doi.org/ 10.1016/j.cell.2014.03.011
  • Newsome R.C., Gauthier J., Hernandez M.C., Abraham G.E., Robinson T.O., Williams H.B. Et al. (2021). The gut microbiome of COVID-19 recovered patients returns to uninfected status in a minority-dominated United States cohort. Gut Microbes, 13(1):1-15. https://doi.org/10.1080/19490976.2021.1926840
  • Carabotti M., Scirocco A., Maselli M.A. & Severi C. (2015). The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Annals of gastroenterology, 28(2):203-209. https://doi.org/ 25830558
  • Martin C.R., Osadchiy V., Kalani A. & Mayer E.A. (2018). The Brain-Gut-Microbiome Axis. Cellular and Molecular Gastroenterology and Hepatology, 12;6(2):133-148. https://doi.org/ 10.1016/j.jcmgh.2018.04.003
  • Fung T.C., Olson C.A. & Hsiao E.Y. (2017). Interactions between the microbiota, immune and nervous systems in health and disease. Nature neuroscience, 20(2):145-155. https://doi.org/ 10.1038/nn.4476
  • Wang Y. & Kasper L.H. (2014). The role of microbiome in central nervous system disorders. Brain, Behavior, and Immunity, 38:1-12. https://doi.org/ 10.1016/j.bbi.2013.12.015
  • Maeda Y., Motooka D., Kawasaki T., Oki H., Noda Y. & Adachi Y. (2022). Longitudinal alterations of the gut mycobiota and microbiota on COVID-19 severity. BMC infectious diseases, 24;22(1):572. https://doi.org/ 10.1186/s12879-022-07358-7
  • Galland L. (2014). The gut microbiome and the brain. Journal of medicinal food. 17(12):1261-72. https://doi.org/ 10.1089/jmf.2014.7000
  • Madison A. & Kiecolt-Glaser J.K. (2019). Stress, depression, diet, and the gut microbiota: human-bacteria interactions at the core of psychoneuroimmunology and nutrition. Current Opinion in Behavioral Sciences, 28:105-110. https://doi.org/ 10.1016/j.cobeha.2019.01.011
  • Napolitano M. & Covasa M. (2020). Microbiota Transplant in the Treatment of Obesity and Diabetes: Current and Future Perspectives. Frontiers in microbiology, 12;11:590370. https://doi.org/ 10.3389/fmicb.2020.590370
  • Chinna Meyyappan A., Forth E., Wallace C.J.K. & Milev R. (2020). Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review. BMC Psychiatry, 15;20(1):299. https://doi.org/ 10.1186/s12888-020-02654-5
  • Sharon G., Sampson T.R., Geschwind D.H. & Mazmanian S.K. (2016). The Central Nervous System and the Gut Microbiome. Cell, 3;167(4):915-932. https://doi.org/ 10.1016/j.cell.2016.10.027
  • Wiertsema S.P., van Bergenhenegouwen J., Garssen J. & Knippels L.M.J. (2021). The Interplay between the Gut Microbiome and the Immune System in the Context of Infectious Diseases throughout Life and the Role of Nutrition in Optimizing Treatment Strategies. Nutrients, 13(3):886. https://doi.org/ 10.3390/nu13030886
  • Kho Z.Y. & Lal SK. (2018). The Human Gut Microbiome - A Potential Controller of Wellness and Disease. Frontiers in microbiology, 14;9:1835. https://doi.org/ 10.3389/fmicb.2018.01835
  • Martin A.M., Sun E.W., Rogers G.B. & Keating D.J. (2019). The Influence of the Gut Microbiome on Host Metabolism Through the Regulation of Gut Hormone Release. Frontiers in Physiology, 16;10:428. https://doi.org/ 10.3389/fphys.2019.00428
  • Gilbert J.A., Blaser MJ, Caporaso JG, Jansson JK, Lynch SV & Knight R. (2018). Current understanding of the human microbiome. Nature medicine, 10;24(4):392-400. https://doi.org/ 10.1038/nm.4517
  • Conlon M.A. & Bird A.R. (2014). The impact of diet and lifestyle on gut microbiota and human health. Nutrients, 24;7(1):17-44. https://doi.org/ 10.3390/nu7010017
  • Kelly S.A., Nzakizwanayo J., Rodgers A.M., Zhao L., Weiser R. & Tekko I.A. (2021). Antibiotic Therapy and the Gut Microbiome: Investigating the Effect of Delivery Route on Gut Pathogens. ACS infectious diseases, 14;7(5):1283-1296. https://doi.org/ 10.1021/acsinfecdis.1c00081
  • Ramirez J., Guarner F., Bustos Fernandez L., Maruy A., Sdepanian V.L. & Cohen H. (2020). Antibiotics as Major Disruptors of Gut Microbiota. Frontiers in cellular and infection microbiology, 24;10:572912. https://doi.org/ 10.3389/fcimb.2020.572912
  • Ceccarelli G., Borrazzo C., Pinacchio C., Santinelli L., Innocenti G.P., Cavallari E.N. et al. (2021). Oral Bacteriotherapy in Patients With COVID-19: A Retrospective Cohort Study. Frontiers in Nutrition, 11;7:613928. https://doi.org/ 10.3389/fnut.2020.613928
  • Looft T. & Allen H.K. (2012). Collateral effects of antibiotics on mammalian gut microbiomes. Gut Microbes, 3(5):463-7. https://doi.org/ 10.4161/gmic.21288
  • Khlevner J., Park Y. & Margolis K.G. (2018). Brain-Gut Axis: Clinical Implications. Gastrointestinal endoscopy clinics of North America, 47(4):727-739. https://doi.org/ 10.1016/j.gtc.2018.07.002
  • Sasselli V., Pachnis V. & Burns A.J. (2012). The enteric nervous system. (2014). Dev Biol, 366(1): 64-73. https://doi.org/ 10.1016/j.ydbio.2012.01.012
  • Furness J.B., Callaghan B.P., Rivera L.R. & Cho H.J. (2014). The enteric nervous system and gastrointestinal innervation: integrated local and central control. Advances in Experimental Medicine and Biology, 817:39-71. https://doi.org/ 10.1007/978-1-4939-0897-4_3
  • Li J.H., Duan R., Li L., Wood J.D., Wang X.Y. & Shu Y. [Unique characteristics of "the second brain" - The enteric nervous system]. Sheng Li Xue Bao, 2020 Jun 25;72(3):382-390. https://doi.org/ 10.3389/fnagi.2021.698988
  • Arneth B.M. (2018). Gut-brain axis biochemical signalling from the gastrointestinal tract to the central nervous system: gut dysbiosis and altered brain function. Postgraduate medical journal, 94(1114):446-452. https://doi.org/ 10.1136/postgradmedj-2017-135424
  • D'Agata A.L., Wu J., Welandawe MKV, Dutra SVO, Kane B & Groer MW. (2019). Effects of early life NICU stress on the developing gut microbiome. Developmental psychobiology. 61(5):650-660. https://doi.org/ 10.1002/dev.21826
  • Shen H.H. News Feature: Microbes on the mind. (2015). The Proceedings of the National Academy of Sciences, 28;112(30):9143-5. https://doi.org/ 10.1073/pnas.1509590112
  • Gutiérrez-Castrellón P., Gandara-Martí T., Abreu A.T., Nieto-Rufino C.D., López-Orduña E. & Jiménez-Escobar I. (2022). Probiotic improves symptomatic and viral clearance in COVID19 outpatients: a randomized, quadruple-blinded, placebo-controlled trial. Gut Microbes, 14(1):2018899. https://doi.org/ 10.1080/19490976.2021.2018899.
  • Bathina S. & Das U.N. (2015). Brain-derived neurotrophic factor and its clinical implications. Archives of medical sciences, 10;11(6):1164-78. https://doi.org/ 10.5114/aoms.2015.56342
  • Binder D.K. & Scharfman H.E. (2004). Brain-derived neurotrophic factor. Growth Factors, 22(3):123-31. https://doi.org/ 10.1080/08977190410001723308
  • Rodriguez D.M., Benninghoff A.D., Aardema N.D.J., Phatak S. & Hintze K.J. (2019). Basal Diet Determined Long-Term Composition of the Gut Microbiome and Mouse Phenotype to a Greater Extent than Fecal Microbiome Transfer from Lean or Obese Human Donors. Nutrients, 17;11(7):1630. https://doi.org/ 10.3390/nu11071630
  • Luo Y., Zeng B., Zeng L., Du X., Li B. & Huo R. (2018). Gut microbiota regulates mouse behaviors through glucocorticoid receptor pathway genes in the hippocampus. Translational psychiatry, 7;8(1):187. https://doi.org/ 10.1038/s41398-018-0240-5
  • Argou-Cardozo I. & Zeidán-Chuliá (2018). F. Clostridium Bacteria and Autism Spectrum Conditions: A Systematic Review and Hypothetical Contribution of Environmental Glyphosate Levels. Medical Sciences, 4;6(2):29. https://doi.org/10.3390/medsci6020029
  • Wasilewska J. & Klukowski M. (2015). Gastrointestinal symptoms and autism spectrum disorder: links and risks- a possible new overlap syndrome. Pediatric Health, Medicine and Therapeutics, 6:153-166. https://doi.org/ 10.2147/PHMT.S85717
  • Dunn A.B., Jordan S., Baker B.J. & Carlson N.S. (2017). The Maternal Infant Microbiome: Considerations for Labor and Birth. MCN The American Journal of Maternal Child Nursing, 42(6):318-325. https://doi.org/ 10.1097/NMC.0000000000000373
  • Suganya K. & Koo B.S. (2020). Gut-Brain Axis: Role of Gut Microbiota on Neurological Disorders and How Probiotics/Prebiotics Beneficially Modulate Microbial and Immune Pathways to Improve Brain Functions. International journal of molecular sciences, 21(20):7551. https://doi.org/ 10.3390/ijms21207551
  • Chowdhury M.A., Hossain N., Kashem M.A., Shahid M.A. & Alam A. (2020). Immune response in COVID-19: A review. Journal of infection prevention, 13(11):1619-1629. https://doi.org/ 10.1016/j.jiph.2020.07.001
  • Farsi Y., Tahvildari A., Arbabi M., Vazife F., Sechi L.A. & Shahidi Bonjar A.H. (2022). Diagnostic, Prognostic, and Therapeutic Roles of Gut Microbiota in COVID-19: A Comprehensive Systematic Review. Frontiers in cellular and infection microbiology, 4;12:804644. https://doi.org/ 10.3389/fcimb.2022.804644
  • Gagliardi A., Totino V., Cacciotti F., Iebba V., Neroni B. & Bonfiglio G. (2018). Rebuilding the Gut Microbiota Ecosystem. International journal of environmental health research, 7;15(8):1679. https://doi.org/
  • Sun Z., Song Z.G., Liu C., Tan S., Lin S., Zhu J. Et al. (2022). Gut microbiome alterations and gut barrier dysfunction are associated with host immune homeostasis in COVID-19 patients. BMC Medicine, 20;20(1):24. https://doi.org/ 10.1186/s12916-021-02212-0
  • Somsouk M., Estes J.D., Deleage C., Dunham R.M., Albright R. & Inadomi J.M. (2015). Gut epithelial barrier and systemic inflammation during chronic HIV infection. AIDS, 29(1):43-51. https://doi.org/
  • Gold J.E., Okyay R.A., Licht W.E. & Hurley D.J. (2021). Investigation of Long COVID Prevalence and Its Relationship to Epstein-Barr Virus Reactivation. Pathogens, 17;10(6):763. https://doi.org/ 10.3390/pathogens10060763
  • Carvalho T., Krammer F. & Iwasaki A. (2021). The first 12 months of COVID-19: a timeline of immunological insights. Nature reviews Immunology, 21(4):245-256. https://doi.org/ 10.1038/s41577-021-00522-1
  • D'Andrea G. (2015). Quercetin: A flavonol with multifaceted therapeutic applications? Fitoterapia, 106:256-71. https://doi.org/ 10.1016/j.fitote.2015.09.018
  • Górski A., Międzybrodzki R., Żaczek M. & Borysowski J. (2020). Phages in the fight against COVID-19? Future Microbiol, 15:1095-1100. https://doi.org/ 10.2217/fmb-2020-0082
  • Sharma J.N., Al-Omran A. & Parvathy S.S. (2007). Role of nitric oxide in inflammatory diseases. Inflammopharmacology, 15(6):252-9. https://doi.org/ 10.1007/s10787-007-0013-x
  • Vázquez-Torres A. & Bäumler A.J. (2016). Nitrate, nitrite and nitric oxide reductases: from the last universal common ancestor to modern bacterial pathogens. Current Opinion in Microbiology, 29:1-8. https://doi.org/ 10.1016/j.mib.2015.09.002
  • Thota R.N., Acharya S.H. & Garg M.L. (2019). Curcumin and/or omega-3 polyunsaturated fatty acids supplementation reduces insulin resistance and blood lipids in individuals with high risk of type 2 diabetes: a randomised controlled trial. Lipids in Health and Disease, 18(1):31. https://doi.org/ 10.1186/s12944-019-0967-x
  • Davie J.R. (2003). Inhibition of histone deacetylase activity by butyrate. The Journal of Nutrition, 133(7 Suppl):2485S-2493S. https://doi.org/ 10.1093/jn/133.7.2485S
  • Wei Y. & Melas P.A. Wegener G, Mathé A.A., Lavebratt C. (2014). Antidepressant-like effect of sodium butyrate is associated with an increase in TET1 and in 5-hydroxymethylation levels in the Bdnf gene. International Journal of Neuropsychopharmacology, 31;18(2). https://doi.org/ 10.1093/ijnp/pyu032
  • Madempudi R.S., Ahire JJ, Neelamraju J, Tripathi A. & Nanal S. (2019). Randomized clinical trial: the effect of probiotic Bacillus coagulans Unique IS2 vs. placebo on the symptoms management of irritable bowel syndrome in adults. Scientific reports, 21;9(1):12210. https://doi.org/ 10.1038/s41598-019-48554-x
  • Liu Q., Mak J.W.Y., Su Q., Yeoh Y.K., Lui G.C. & Ng S.S.S. (2022). Gut microbiota dynamics in a prospective cohort of patients with post-acute COVID-19 syndrome. Gut, 71(3):544-552. https://doi.org/ 10.1136/gutjnl-2021-325989
  • Hrncir T. (2022). Gut Microbiota Dysbiosis: Triggers, Consequences, Diagnostic and Therapeutic Options. Microorganisms. 10(3):578-643. doi: 10.3390/microorganisms10030578.
  • Tilg H, Adolph TE, Trauner M (2022). Gut-liver axis: Pathophysiological concepts and clinical implications. Microorganism. 34(11):1700-1718. doi: 10.1016/j.cmet.2022.09.017.
  • An C, Chon H, Ku W, Eom S, Seok M, Kim S et al., (2022). Bile Acids: Major Regulator of the Gut Microbiome. Microorganisms. 10(9):1792. doi: 10.3390/microorganisms10091792.
  • Arias N, Arboleya S, Allison J, Kaliszewska A, Higarza SG, Gueimonde M et al., (2020). The Relationship between Choline Bioavailability from Diet, Intestinal Microbiota Composition, and Its Modulation of Human Diseases. Nutrients. 12(8):2340. doi: 10.3390/nu12082340.
  • Latif A, Shehzad A, Niazi S, Zahid A, Ashraf W, Iqbal MW et al., (2023). Probiotics: mechanism of action, health benefits and their application in food industries. Frontiers in Microbiology. 14(1): 21-67. doi: 10.3389/fmicb.2023.1216674.
  • Bax L., Yu L.M., Ikeda N & Moons KGA. (2007). systematic comparison of software dedicated to meta-analysis of causal studies. BMC medical research methodology, 10;7:40. https://doi.org/ 10.1186/1471-2288-7-40
  • Chelakkot C., Ghim J. & Ryu S.H. (2018). Mechanisms regulating intestinal barrier integrity and its pathological implications. Experimental and Molecular Medicine, 16;50(8):1-9. https://doi.org/ 10.1038/s12276-018-0126-x
  • Chowdhury M.A., Hossain N., Kashem M.A., Shahid M.A. & Alam A. (2020). Immune response in COVID-19: A review. Journal of infection prevention, 13(11):1619-1629. https://doi.org/ 10.1016/j.jiph.2020.07.001
  • Dill-McFarland K.A., Tang Z.Z., Kemis J.H., Kerby R.L., Chen G. & Palloni A. (2019). Close social relationships correlate with human gut microbiota composition. Scientific reports, 24;9(1):703. https://doi.org/ 10.1038/s41598-018-37298-9
  • Jin X., Lian J.S., Hu J.H., Gao J., Zheng L. & Zhang Y.M. (2020). Epidemiological, clinical and virological characteristics of 74 cases of coronavirus-infected disease 2019 (COVID-19) with gastrointestinal symptoms. Gut, 69(6):1002-1009. https://doi.org/ 10.1136/gutjnl-2020-320926
  • Suárez-Reyes A. & Villegas-Valverde C.A. (2021). Implications of Low-grade Inflammation in SARS-CoV-2 Immunopathology. MEDICC Review, 23(2):42. https://doi.org/ 10.37757/MR2021.V23.N2.4
  • Yeoh Y.K., Zuo T., Lui G.C., Zhang F. & Liu Q. (2021). Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut, 70(4):698-706. https://doi.org/10.1136/gutjnl-2020-323020
There are 89 citations in total.

Details

Primary Language English
Subjects Respiratory Diseases
Journal Section Review Articles
Authors

Kayhan Özkan 0000-0002-5956-093X

Şerif Demir

Publication Date May 19, 2024
Submission Date December 21, 2023
Acceptance Date April 17, 2024
Published in Issue Year 2024 Volume: 41 Issue: 2

Cite

APA Özkan, K., & Demir, Ş. (2024). Can the gastrointestinal system alter liver damage caused by COVID-19?. Journal of Experimental and Clinical Medicine, 41(2), 397-406.
AMA Özkan K, Demir Ş. Can the gastrointestinal system alter liver damage caused by COVID-19?. J. Exp. Clin. Med. May 2024;41(2):397-406.
Chicago Özkan, Kayhan, and Şerif Demir. “Can the Gastrointestinal System Alter Liver Damage Caused by COVID-19?”. Journal of Experimental and Clinical Medicine 41, no. 2 (May 2024): 397-406.
EndNote Özkan K, Demir Ş (May 1, 2024) Can the gastrointestinal system alter liver damage caused by COVID-19?. Journal of Experimental and Clinical Medicine 41 2 397–406.
IEEE K. Özkan and Ş. Demir, “Can the gastrointestinal system alter liver damage caused by COVID-19?”, J. Exp. Clin. Med., vol. 41, no. 2, pp. 397–406, 2024.
ISNAD Özkan, Kayhan - Demir, Şerif. “Can the Gastrointestinal System Alter Liver Damage Caused by COVID-19?”. Journal of Experimental and Clinical Medicine 41/2 (May 2024), 397-406.
JAMA Özkan K, Demir Ş. Can the gastrointestinal system alter liver damage caused by COVID-19?. J. Exp. Clin. Med. 2024;41:397–406.
MLA Özkan, Kayhan and Şerif Demir. “Can the Gastrointestinal System Alter Liver Damage Caused by COVID-19?”. Journal of Experimental and Clinical Medicine, vol. 41, no. 2, 2024, pp. 397-06.
Vancouver Özkan K, Demir Ş. Can the gastrointestinal system alter liver damage caused by COVID-19?. J. Exp. Clin. Med. 2024;41(2):397-406.