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References

  1. Heilig M, Egli M. 2006. Pharmacological treatment of alcohol dependence: target symptoms and target mechanisms. Pharmacol. Ther. 111: 855-876.
    Pubmed CrossRef
  2. Thoma P, Friedmann C, Suchan B. 2013. Empathy and social problem solving in alcohol dependence, mood disorders and selected personality disorders. Neurosci. Biobehav. Rev. 37: 448-470.
    Pubmed CrossRef
  3. de Timary P, Leclercq S, Stärkel P, Delzenne N. 2015. A dysbiotic subpopulation of alcohol-dependent subjects. Gut. Microbes 6: 388-391.
    Pubmed PMC CrossRef
  4. Rehm J, Dawson D, Frick U, Gmel G, Roerecke M, Shield KD, et al. 2014. Burden of disease associated with alcohol use disorders in the United States. Alcohol Clin. Exp. Res. 38:1068-1077.
    Pubmed PMC CrossRef
  5. Levey DF, Leniculescu H, Frank J, Ayalew M, Jain N, Kirlin B, et al. 2014. Genetic risk prediction and neurobiological understanding of alcoholism. Transl. Psychiatry 4: e391.
    Pubmed CrossRef
  6. Salvatore JE, Aliev F, Edwards AC, Evans DM, Macleod J, Hickman M, et al. 2014. Polygenic scores predict alcohol problems in an independent sample and show moderation by the environment. Genes 5: 330-346.
    Pubmed PMC CrossRef
  7. Whelan R, Watts R, Orr CA, Althoff RR, Artiges E, Banaschewski T, et al. 2014. Neuropsychosocial profiles of current and future adolescent alcohol misusers. Nature 512:185-189.
    Pubmed PMC CrossRef
  8. Gilpin NW, Koob GF. 2008. Neurobiology of alcohol dependence: focus on motivational mechanisms. Alcohol Res. Health 31: 185-195.
    Pubmed PMC
  9. Freeman K, Staehle MM, Vadigepalli R, Gonye GE, Ogunnaike BA, Hoek JB, et al. 2013. Coordinated dynamic gene expression changes in the central nucleus of the amygdala during alcohol withdrawal. Alcohol Clin. Exp. Res. 37(suppl): E88-E100.
    Pubmed PMC CrossRef
  10. Gorky J, Schwaber J. 2016. The role of the gut-brain axis in alcohol use disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 4: 234-241.
    Pubmed PMC CrossRef
  11. Leclercq S,de Timary P, Delzenne NM, Stärkel P. 2017. The link between inflammation, bugs, the intestine and the brain in alcohol dependence. Transl. Psychiatry 7: e1048.
    Pubmed PMC CrossRef
  12. Leo Galland. 2014. The Gut Microbiome and the Brain. J. Med. Food 17: 1-12.
    Pubmed PMC CrossRef
  13. Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. 2016. The Central Nervous System and the Gut Microbiome. Cell 167: 915-932.
    Pubmed PMC CrossRef
  14. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. 2012. A meta genome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55-60.
    Pubmed CrossRef
  15. Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, Laatikainen T, et al. 2012. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl. Acad. Sci. USA 109: 8334-8339.
    Pubmed PMC CrossRef
  16. Dalal SR, Chang EB. 2014. The microbial basis of inflammatory bowel diseases, J. Clin. Invest. 124: 4190-4196.
    Pubmed PMC CrossRef
  17. Jess T. 2014. Microbiota, antibiotics, and obesity. N. Engl. J. Med. 371: 2526-2528.
    Pubmed CrossRef
  18. Rogers GB, Keating DJ, Young RL, Wong ML, Licinio J, Wesselingh S. 2016. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol. Psychiatry 21: 738-748.
    Pubmed PMC CrossRef
  19. Foster JA, McVey Neufeld KA. 2013. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36: 305-312.
    Pubmed CrossRef
  20. Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. 2016. The central nervous system and the gut microbiome. Cell 167: 915-932.
    Pubmed PMC CrossRef
  21. Vuong HE, Hsiao EY. 2017. Emerging roles for the gut microbiome in autism spectrum disorder. Biol. Psychiatry 81:411-423.
    Pubmed PMC CrossRef
  22. Cani PD, Everard A. 2015. Harnessing genes and diet to fine-tune the gut microbial fitness. Cell Metab. 22: 754-756.
    Pubmed CrossRef
  23. Hollister EB, Gao C, Versalovic J. 2014. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 146: 14491458.
    Pubmed PMC CrossRef
  24. Mutlu EA, Gillevet PM, Rangwala H, Sikaroodi M, Naqvi A, Engen PA, Kwasny M, et al. 2012. Colonic microbiome is altered in alcoholism. Am. J. Physiol. Gastrointest Liver Physiol. 302: G966-G978.
    Pubmed PMC CrossRef
  25. Engen PA, Green SJ, Voigt RM, Forsyth CB, Keshavarzian A. 2015. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res. 37: 223-236.
    Pubmed PMC
  26. Bishehsari F, Magno E, Swanson G, Desai V, Voigt RM, Forsyth CB, et al. 2017. Alcohol and gut-derived inflammation. Alcohol Res. 38: 163-171.
    Pubmed PMC
  27. Bull-Otterson L, Feng W, Kirpich I, Wang Y, Qin X, Liu Y, et al. 2013. Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of Lactobacillus rhamnosus GG treatment. PLoS One 8: e53028.
    Pubmed PMC CrossRef
  28. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. 2008. Highthroughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57: 1605-1615.
    Pubmed CrossRef
  29. Zhao WJ, Wang YP, Liu SY, Huang JJ, Zhai ZX, He C, et al. 2015. The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. PLoS One 10: e0117441.
    Pubmed PMC CrossRef
  30. Erden BF, Ozdemirci S, Yildiran G, Utkan T, Gacar N, Ulak G. 1999. Dextromethorphan attenuates ethanol withdrawal syndrome in rats. Pharmacol. Biochem. Behav. 62: 537-541.
    CrossRef
  31. Chen Y, Yang F, Lu H, Wang B, Chen Y, Lei D, et al. 2011. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54: 562-572.
    Pubmed CrossRef
  32. Queipo-Ortuño MI, Boto-Ordóñez M, Murri M, GomezZumaquero JM, Clemente-Postigo M, Estruch R, et al. 2012. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am. J. Clin. Nutr. 95: 1323-1334.
    Pubmed CrossRef
  33. Mutlu E, Keshavarzian A, Engen P, Forsyth CB, Sikaroodi M, Gillevet P. 2009. Intestinal dysbiosis: a possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol Clin. Exp. Res. 33: 1836-1846.
    Pubmed PMC CrossRef
  34. Yan AW, Fouts DE, Brandl J, Stärkel P, Torralba M, Schott E, et al. 2011. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 53: 96-105.
    Pubmed PMC CrossRef
  35. Mu C, Yang Y, Su Y, Zoetendal EG, Zhu W. 2017. Differences in microbiota membership along the gastrointestinal tract of piglets and their differential alterations following an earlylife antibiotic intervention. Front. Microbiol. 8: 797.
    Pubmed PMC CrossRef
  36. Xiao HW, Ge C, Feng GX, Li Y, Luo D, Dong JL, et al. 2018. Gut microbiota modulates alcohol withdrawal-induced anxiety in mice. Toxicol. Lett. 287: 23-30.
    Pubmed CrossRef
  37. Peterson VL, Jury NJ, Cabrera-Rubio R, Draper LA, Crispie F, Cotter PD, et al. 2017. Drunk bugs: chronic vapour alcohol exposure induces marked changes in the gut microbiome in mice. Behav. Brain Res. 323: 172-176.
    Pubmed PMC CrossRef
  38. Levitt MD, Li R, DeMaster EG, Elson M, Furne J, Levitt DG. 1997. Use of measurements of ethanol absorption from stomach and intestine to assess human ethanol metabolism. Am. J. Physiol. 273: G951-G957.
    Pubmed
  39. Norberg A, Jones AW, Hahn RG, Gabrielsson JL. 2003. Role of variability in explaining ethanol pharmacokinetics: research and forensic applications. Clin. Pharmacokinet 42: 1-31.
    Pubmed CrossRef
  40. Zakhari S . 2006. O verview: h ow i s alc ohol m etabolized by the body? Alcohol Res. Health 29: 245-254.
    Pubmed
  41. Nosova T, Jousimies-Somer H, Jokelainen K, Heine R, Salaspuro M. 2000. Acetaldehyde production and metabolism by human indigenous and probiotic Lactobacillus and Bifidobacterium strains. Alcohol Alcohol 35: 561-568.
    Pubmed CrossRef
  42. Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, et al. 2014. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc. Natl. Acad. Sci. USA 111: E4485-E4493.
    Pubmed PMC CrossRef
  43. Leclercq S, De Saeger C, Delzenne N, de Timary P, Stärkel P. 2014. Role of inflammatory pathways, blood mononuclear cells, and gut-derived bacterial products in alcohol dependence. Biol. Psychiatry 76: 725-733.
    Pubmed CrossRef
  44. Kirpich IA, Solovieva NV, Leikhter SN, Shidakova NA, Lebedeva OV, Sidorov PI, et al. 2008. Probiotics restore bowel flora and improve liver enzymes in human alcoholinduced liver injury: a pilot study. Alcohol 42: 675-682.
    Pubmed PMC CrossRef
  45. Dubinkina VB, Tyakht AV, Odintsova VY, Yarygin KS, Kovarsky BA, Pavlenko AV, et al. 2017. Links of gut microbiota composition with alcohol dependence syndrome and alcoholic liver disease. Microbiome 5: 141.
    Pubmed PMC CrossRef
  46. Nimgampalle M, Kuna Y. 2017. Anti-Alzheimer Properties of Probiotic, Lactobacillus plantarum MTCC 1325 in Alzheimer’s disease induced Albino Rats. J. Clin. Diagn. Res. 11: KC01-KC05.
    CrossRef
  47. Wang H, Lee IS, Braun C, Enck P. 2016. Effect of probiotics on central nervous system functions in animals and humans:a systematic review. J. Neurogastroenterol Motil 22: 589-605.
    Pubmed PMC CrossRef
  48. Leclercq S, Cani PD, Neyrinck AM, Stärkel P, Jamar F, Mikolajczak M, et al. 2012. Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects. Brain Behav. Immun. 26: 911-918.
    Pubmed CrossRef
  49. Parlesak A, S c häfer C, S c hütz T , Bode JC, B ode C. 2 000. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J. Hepatol. 32: 742-747.
    CrossRef
  50. Bode C, Bode JC. 2003. Effect of alcohol consumption on the gut. Best Pract Res. Clin. Gastroenterol 17: 575-592.
    CrossRef
  51. Keshavarzian A, Farhadi A, Forsyth CB, Rangan J, Jakate S, Shaikh M, et al. 2009. Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J. Hepatol 50: 538-547.
    Pubmed PMC CrossRef
  52. de Timary P, Stärkel P, Delzenne NM, Leclercq S. 2017. A role for the peripheral immune system in the development of alcohol use disorders? Neuropharmacology 122: 148-160.
    Pubmed CrossRef
  53. Donnadieu-Rigole H, Pansu N, Mura T, Pelletier S, Alarcon R, Gamon L, et al. 2018. Beneficial effect of alcohol withdrawal on gut permeability and microbial translocation in patients with alcohol use disorder. Alcohol. Clin. Exp. Res. 42: 32-40.
    Pubmed CrossRef
  54. Stärkel P, Leclercq S, de Timary P, Schnabl B. 2018. Intestinal dysbiosis and permeability: the yin and yang in alcohol dependence and alcoholic liver disease. Clin. Sci. (Lond) 132: 199-212.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2018; 28(11): 1883-1895

Published online November 28, 2018 https://doi.org/10.4014/jmb.1806.06050

Copyright © The Korean Society for Microbiology and Biotechnology.

Comparison of Microbial Diversity and Composition in Jejunum and Colon of the Alcohol-dependent Rats

Yang Fan 1, 2, Zhao Ya-E 1*, Wei Ji-Dong 2, Lu Yu-fan 2, Zhang Ying 2, Sun Ya-lun 2, Ma Meng-Yu 2 and Zhang Rui-ling 3

1Department of Immunology and Pathogen Biology, School of Basic Medical Science, Xi’an Jiaotong University, No. 76 Yanta West Road, Xi’an, China 710061, 2Department of microbiology, School of Basic Medical Science, Xinxiang Medical University, Xinxiang, China 453003, 3The Second Affiliated Hospital, Xinxiang Medical University, Xinxiang, China 453000

Received: June 22, 2018; Accepted: September 11, 2018

Abstract

Alcohol dependence was a global public health problem, yet the mechanisms of alcohol dependence has incompletely understood. The traditional view consider ethanol alter various neurotransmitters and their receptors in brain and develop the addiction. However, an increasing experimental evidences suggest that gut microbiota also influence brain functions via gut-to-brain interactions, and may therefore induce the development of alcohol use disorders. In this study, a rat model of alcohol dependence and withdrawal was employed, the gut microbiota composition was analyzed by high-throughput 16S rRNA gene sequencing, and the metagenome function was predicted by PICRUSt software. The results suggested that chronic alcohol consumption did not significant alter the diversity and richness of gut microbiota in jejunum and colon, but markedly changed the microbiota composition structure in colon. The phyla Bacteroidetes and eight genera including Bacteroidales S24-7, Ruminococcaceae, Parabacteroides, Butyricimonas, et al were drastically increased, however the genus Lactobacillus and gauvreauii were significantly decreased in alcohol dependence group compared with other two groups in the colon. The microbial functional prediction analysis revealed that the proportions of amino acid metabolism, polyketide sugar unit biosynthesis and peroxisome were significantly increased in AD group. This study demonstrated that the chronic alcohol consumption has a dramatic effect on the microbiota composition structure in the colon but few effects on the jejunum. Alcohol abuse induce the colonic microbiota dysbiosis seems to be a factor of alcohol dependence, which suggested that modulated the colonic microbiota composition might be a potentially new target for treating alcohol addiction.

Keywords: Alcohol dependence, gut microbiota, dysbiosis, jejunum, colon

References

  1. Heilig M, Egli M. 2006. Pharmacological treatment of alcohol dependence: target symptoms and target mechanisms. Pharmacol. Ther. 111: 855-876.
    Pubmed CrossRef
  2. Thoma P, Friedmann C, Suchan B. 2013. Empathy and social problem solving in alcohol dependence, mood disorders and selected personality disorders. Neurosci. Biobehav. Rev. 37: 448-470.
    Pubmed CrossRef
  3. de Timary P, Leclercq S, Stärkel P, Delzenne N. 2015. A dysbiotic subpopulation of alcohol-dependent subjects. Gut. Microbes 6: 388-391.
    Pubmed KoreaMed CrossRef
  4. Rehm J, Dawson D, Frick U, Gmel G, Roerecke M, Shield KD, et al. 2014. Burden of disease associated with alcohol use disorders in the United States. Alcohol Clin. Exp. Res. 38:1068-1077.
    Pubmed KoreaMed CrossRef
  5. Levey DF, Leniculescu H, Frank J, Ayalew M, Jain N, Kirlin B, et al. 2014. Genetic risk prediction and neurobiological understanding of alcoholism. Transl. Psychiatry 4: e391.
    Pubmed CrossRef
  6. Salvatore JE, Aliev F, Edwards AC, Evans DM, Macleod J, Hickman M, et al. 2014. Polygenic scores predict alcohol problems in an independent sample and show moderation by the environment. Genes 5: 330-346.
    Pubmed KoreaMed CrossRef
  7. Whelan R, Watts R, Orr CA, Althoff RR, Artiges E, Banaschewski T, et al. 2014. Neuropsychosocial profiles of current and future adolescent alcohol misusers. Nature 512:185-189.
    Pubmed KoreaMed CrossRef
  8. Gilpin NW, Koob GF. 2008. Neurobiology of alcohol dependence: focus on motivational mechanisms. Alcohol Res. Health 31: 185-195.
    Pubmed KoreaMed
  9. Freeman K, Staehle MM, Vadigepalli R, Gonye GE, Ogunnaike BA, Hoek JB, et al. 2013. Coordinated dynamic gene expression changes in the central nucleus of the amygdala during alcohol withdrawal. Alcohol Clin. Exp. Res. 37(suppl): E88-E100.
    Pubmed KoreaMed CrossRef
  10. Gorky J, Schwaber J. 2016. The role of the gut-brain axis in alcohol use disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 4: 234-241.
    Pubmed KoreaMed CrossRef
  11. Leclercq S,de Timary P, Delzenne NM, Stärkel P. 2017. The link between inflammation, bugs, the intestine and the brain in alcohol dependence. Transl. Psychiatry 7: e1048.
    Pubmed KoreaMed CrossRef
  12. Leo Galland. 2014. The Gut Microbiome and the Brain. J. Med. Food 17: 1-12.
    Pubmed KoreaMed CrossRef
  13. Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. 2016. The Central Nervous System and the Gut Microbiome. Cell 167: 915-932.
    Pubmed KoreaMed CrossRef
  14. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. 2012. A meta genome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55-60.
    Pubmed CrossRef
  15. Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, Laatikainen T, et al. 2012. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl. Acad. Sci. USA 109: 8334-8339.
    Pubmed KoreaMed CrossRef
  16. Dalal SR, Chang EB. 2014. The microbial basis of inflammatory bowel diseases, J. Clin. Invest. 124: 4190-4196.
    Pubmed KoreaMed CrossRef
  17. Jess T. 2014. Microbiota, antibiotics, and obesity. N. Engl. J. Med. 371: 2526-2528.
    Pubmed CrossRef
  18. Rogers GB, Keating DJ, Young RL, Wong ML, Licinio J, Wesselingh S. 2016. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol. Psychiatry 21: 738-748.
    Pubmed KoreaMed CrossRef
  19. Foster JA, McVey Neufeld KA. 2013. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36: 305-312.
    Pubmed CrossRef
  20. Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. 2016. The central nervous system and the gut microbiome. Cell 167: 915-932.
    Pubmed KoreaMed CrossRef
  21. Vuong HE, Hsiao EY. 2017. Emerging roles for the gut microbiome in autism spectrum disorder. Biol. Psychiatry 81:411-423.
    Pubmed KoreaMed CrossRef
  22. Cani PD, Everard A. 2015. Harnessing genes and diet to fine-tune the gut microbial fitness. Cell Metab. 22: 754-756.
    Pubmed CrossRef
  23. Hollister EB, Gao C, Versalovic J. 2014. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 146: 14491458.
    Pubmed KoreaMed CrossRef
  24. Mutlu EA, Gillevet PM, Rangwala H, Sikaroodi M, Naqvi A, Engen PA, Kwasny M, et al. 2012. Colonic microbiome is altered in alcoholism. Am. J. Physiol. Gastrointest Liver Physiol. 302: G966-G978.
    Pubmed KoreaMed CrossRef
  25. Engen PA, Green SJ, Voigt RM, Forsyth CB, Keshavarzian A. 2015. The gastrointestinal microbiome: alcohol effects on the composition of intestinal microbiota. Alcohol Res. 37: 223-236.
    Pubmed KoreaMed
  26. Bishehsari F, Magno E, Swanson G, Desai V, Voigt RM, Forsyth CB, et al. 2017. Alcohol and gut-derived inflammation. Alcohol Res. 38: 163-171.
    Pubmed KoreaMed
  27. Bull-Otterson L, Feng W, Kirpich I, Wang Y, Qin X, Liu Y, et al. 2013. Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of Lactobacillus rhamnosus GG treatment. PLoS One 8: e53028.
    Pubmed KoreaMed CrossRef
  28. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. 2008. Highthroughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57: 1605-1615.
    Pubmed CrossRef
  29. Zhao WJ, Wang YP, Liu SY, Huang JJ, Zhai ZX, He C, et al. 2015. The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. PLoS One 10: e0117441.
    Pubmed KoreaMed CrossRef
  30. Erden BF, Ozdemirci S, Yildiran G, Utkan T, Gacar N, Ulak G. 1999. Dextromethorphan attenuates ethanol withdrawal syndrome in rats. Pharmacol. Biochem. Behav. 62: 537-541.
    CrossRef
  31. Chen Y, Yang F, Lu H, Wang B, Chen Y, Lei D, et al. 2011. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54: 562-572.
    Pubmed CrossRef
  32. Queipo-Ortuño MI, Boto-Ordóñez M, Murri M, GomezZumaquero JM, Clemente-Postigo M, Estruch R, et al. 2012. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am. J. Clin. Nutr. 95: 1323-1334.
    Pubmed CrossRef
  33. Mutlu E, Keshavarzian A, Engen P, Forsyth CB, Sikaroodi M, Gillevet P. 2009. Intestinal dysbiosis: a possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol Clin. Exp. Res. 33: 1836-1846.
    Pubmed KoreaMed CrossRef
  34. Yan AW, Fouts DE, Brandl J, Stärkel P, Torralba M, Schott E, et al. 2011. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 53: 96-105.
    Pubmed KoreaMed CrossRef
  35. Mu C, Yang Y, Su Y, Zoetendal EG, Zhu W. 2017. Differences in microbiota membership along the gastrointestinal tract of piglets and their differential alterations following an earlylife antibiotic intervention. Front. Microbiol. 8: 797.
    Pubmed KoreaMed CrossRef
  36. Xiao HW, Ge C, Feng GX, Li Y, Luo D, Dong JL, et al. 2018. Gut microbiota modulates alcohol withdrawal-induced anxiety in mice. Toxicol. Lett. 287: 23-30.
    Pubmed CrossRef
  37. Peterson VL, Jury NJ, Cabrera-Rubio R, Draper LA, Crispie F, Cotter PD, et al. 2017. Drunk bugs: chronic vapour alcohol exposure induces marked changes in the gut microbiome in mice. Behav. Brain Res. 323: 172-176.
    Pubmed KoreaMed CrossRef
  38. Levitt MD, Li R, DeMaster EG, Elson M, Furne J, Levitt DG. 1997. Use of measurements of ethanol absorption from stomach and intestine to assess human ethanol metabolism. Am. J. Physiol. 273: G951-G957.
    Pubmed
  39. Norberg A, Jones AW, Hahn RG, Gabrielsson JL. 2003. Role of variability in explaining ethanol pharmacokinetics: research and forensic applications. Clin. Pharmacokinet 42: 1-31.
    Pubmed CrossRef
  40. Zakhari S . 2006. O verview: h ow i s alc ohol m etabolized by the body? Alcohol Res. Health 29: 245-254.
    Pubmed
  41. Nosova T, Jousimies-Somer H, Jokelainen K, Heine R, Salaspuro M. 2000. Acetaldehyde production and metabolism by human indigenous and probiotic Lactobacillus and Bifidobacterium strains. Alcohol Alcohol 35: 561-568.
    Pubmed CrossRef
  42. Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, et al. 2014. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc. Natl. Acad. Sci. USA 111: E4485-E4493.
    Pubmed KoreaMed CrossRef
  43. Leclercq S, De Saeger C, Delzenne N, de Timary P, Stärkel P. 2014. Role of inflammatory pathways, blood mononuclear cells, and gut-derived bacterial products in alcohol dependence. Biol. Psychiatry 76: 725-733.
    Pubmed CrossRef
  44. Kirpich IA, Solovieva NV, Leikhter SN, Shidakova NA, Lebedeva OV, Sidorov PI, et al. 2008. Probiotics restore bowel flora and improve liver enzymes in human alcoholinduced liver injury: a pilot study. Alcohol 42: 675-682.
    Pubmed KoreaMed CrossRef
  45. Dubinkina VB, Tyakht AV, Odintsova VY, Yarygin KS, Kovarsky BA, Pavlenko AV, et al. 2017. Links of gut microbiota composition with alcohol dependence syndrome and alcoholic liver disease. Microbiome 5: 141.
    Pubmed KoreaMed CrossRef
  46. Nimgampalle M, Kuna Y. 2017. Anti-Alzheimer Properties of Probiotic, Lactobacillus plantarum MTCC 1325 in Alzheimer’s disease induced Albino Rats. J. Clin. Diagn. Res. 11: KC01-KC05.
    CrossRef
  47. Wang H, Lee IS, Braun C, Enck P. 2016. Effect of probiotics on central nervous system functions in animals and humans:a systematic review. J. Neurogastroenterol Motil 22: 589-605.
    Pubmed KoreaMed CrossRef
  48. Leclercq S, Cani PD, Neyrinck AM, Stärkel P, Jamar F, Mikolajczak M, et al. 2012. Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects. Brain Behav. Immun. 26: 911-918.
    Pubmed CrossRef
  49. Parlesak A, S c häfer C, S c hütz T , Bode JC, B ode C. 2 000. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J. Hepatol. 32: 742-747.
    CrossRef
  50. Bode C, Bode JC. 2003. Effect of alcohol consumption on the gut. Best Pract Res. Clin. Gastroenterol 17: 575-592.
    CrossRef
  51. Keshavarzian A, Farhadi A, Forsyth CB, Rangan J, Jakate S, Shaikh M, et al. 2009. Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J. Hepatol 50: 538-547.
    Pubmed KoreaMed CrossRef
  52. de Timary P, Stärkel P, Delzenne NM, Leclercq S. 2017. A role for the peripheral immune system in the development of alcohol use disorders? Neuropharmacology 122: 148-160.
    Pubmed CrossRef
  53. Donnadieu-Rigole H, Pansu N, Mura T, Pelletier S, Alarcon R, Gamon L, et al. 2018. Beneficial effect of alcohol withdrawal on gut permeability and microbial translocation in patients with alcohol use disorder. Alcohol. Clin. Exp. Res. 42: 32-40.
    Pubmed CrossRef
  54. Stärkel P, Leclercq S, de Timary P, Schnabl B. 2018. Intestinal dysbiosis and permeability: the yin and yang in alcohol dependence and alcoholic liver disease. Clin. Sci. (Lond) 132: 199-212.
    Pubmed CrossRef