Skip to main content

Advertisement

SpringerLink
Log in

Are Probiotics Effective in Targeting Alcoholic Liver Diseases?

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Alcoholic liver disease (ALD) encompasses a broad spectrum of disorders including steatosis, steatohepatitis, fibrosis, and cirrhosis. Despite intensive research in the last two decades, there is currently no Food and Drug Administration-approved therapy for treating ALD. Several studies have demonstrated the importance of the gut-liver axis and gut microbiome on the pathogenesis of ALD. Alcohol may induce intestinal dysbiosis and increased intestinal permeability, which in turn result in increased levels of pathogen-associated molecular patterns such as lipopolysaccharide (LPS) and translocation of microbial products from the gut to the liver (bacterial translocation). LPS is an inflammatory signal that activates toll-like receptor 4 on Kupffer cells, contributing to the inflammation observed in ALD. Recently, probiotics have been shown to be effective in reducing or preventing the progression of ALD. A potential mechanism is that the probiotics transforms the composition of intestinal microbiota, which leads to reductions in alcohol-induced dysbiosis, intestinal permeability, bacterial translocation, endotoxemia, and consequently, the development of ALD. While transformation of intestinal microbiota by probiotics appears to be a promising therapeutic strategy for the treatment of intestinal barrier dysfunction, there is a scarcity of research that studies probiotics in the context of ALD. In this review, we discuss the potential therapeutic applications of probiotics in the treatment of ALD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

ALD:

alcoholic liver disease

LPS:

lipopolysaccharide

TLR:

Toll-like receptor

TNF:

tumor necrosis factor

IL:

interleukin

FMT:

fecal microbiota transplantation

GG:

Gorbach-Goldin

CDI:

Clostridium difficile infection

CRP:

C-reactive protein

AST:

aspartate aminotransferase

ALT:

alanine aminotransferase

References

  1. Room R, Babor T, Rehm J (2005) Alcohol and public health. Lancet 365(9458):519–530. https://doi.org/10.1016/S0140-6736(05)17870-2

    Article  PubMed  Google Scholar 

  2. Sanyal AJ (2011) NASH: a global health problem. Hepatol Res 41(7):670–674. https://doi.org/10.1111/j.1872-034X.2011.00824.x

    Article  PubMed  Google Scholar 

  3. Moreau R (2016) Acute-on-chronic liver failure: a new syndrome in cirrhosis. Clin Mol Hepatol 22(1):1–6. https://doi.org/10.3350/cmh.2016.22.1.1

    Article  PubMed  PubMed Central  Google Scholar 

  4. Pares A, Caballeria J, Bruguera M et al (1986) Histological course of alcoholic hepatitis. Influence of abstinence, sex and extent of hepatic damage. J Hepatol 2(1):33–42

    Article  CAS  PubMed  Google Scholar 

  5. Stewart S, Jones D, Day CP (2001) Alcoholic liver disease: new insights into mechanisms and preventative strategies. Trends Mol Med 7(9):408–413

    Article  CAS  PubMed  Google Scholar 

  6. Thurman RG (1998) II. Alcoholic liver injury involves activation of Kupffer cells by endotoxin. Am J Phys 275(4 Pt 1):G605–G611

    CAS  Google Scholar 

  7. Ji SB, Lee SS, Jung HC et al (2016) A Korean patient with Guillain-Barre syndrome following acute hepatitis E whose cholestasis resolved with steroid therapy. Clin Mol Hepatol 22(3):396–399. https://doi.org/10.3350/cmh.2015.0039

    Article  PubMed  PubMed Central  Google Scholar 

  8. Veldt BJ, Laine F, Guillygomarc'h A et al (2002) Indication of liver transplantation in severe alcoholic liver cirrhosis: quantitative evaluation and optimal timing. J Hepatol 36(1):93–98

    Article  PubMed  Google Scholar 

  9. European Association for the Study of The Liver (2012) EASL clinical practical guidelines: management of alcoholic liver disease. J Hepatol 57(2):399–420. https://doi.org/10.1016/j.jhep.2012.04.004

  10. Wheeler MD, Kono H, Yin M, Nakagami M, Uesugi T, Arteel GE, Gäbele E, Rusyn I, Yamashina S, Froh M, Adachi Y, Iimuro Y, Bradford BU, Smutney OM, Connor HD, Mason RP, Goyert SM, Peters JM, Gonzalez FJ, Samulski RJ, Thurman RG (2001) The role of Kupffer cell oxidant production in early ethanol-induced liver disease. Free Radic Biol Med 31(12):1544–1549

    Article  CAS  PubMed  Google Scholar 

  11. Enomoto N, Ikejima K, Bradford BU et al (2000) Role of Kupffer cells and gut-derived endotoxins in alcoholic liver injury. J Gastroenterol Hepatol 15 Suppl(D20–25)

  12. Petrasek J, Csak T, Szabo G (2013) Toll-like receptors in liver disease. Adv Clin Chem 59:155–201

    Article  CAS  PubMed  Google Scholar 

  13. Shah VH (2015) Managing alcoholic liver disease. Clin Mol Hepatol 21(3):212–219. https://doi.org/10.3350/cmh.2015.21.3.212

    Article  PubMed  PubMed Central  Google Scholar 

  14. Uesugi T, Froh M, Arteel GE, Bradford BU, Thurman RG (2001) Toll-like receptor 4 is involved in the mechanism of early alcohol-induced liver injury in mice. Hepatology 34(1):101–108. https://doi.org/10.1053/jhep.2001.25350

    Article  CAS  PubMed  Google Scholar 

  15. Petrasek J, Mandrekar P, Szabo G (2010) Toll-like receptors in the pathogenesis of alcoholic liver disease. Gastroenterol Res Pract 2010:1–12. https://doi.org/10.1155/2010/710381

    Article  Google Scholar 

  16. Szabo G (2015) Gut-liver axis in alcoholic liver disease. Gastroenterology 148(1):30–36. https://doi.org/10.1053/j.gastro.2014.10.042

    Article  CAS  PubMed  Google Scholar 

  17. Gabbard SL, Lacy BE, Levine GM, Crowell MD (2013) The impact of alcohol consumption and cholecystectomy on small intestinal bacterial overgrowth. Dig Dis Sci 59:638–644. https://doi.org/10.1007/s10620-013-2960-y

    Article  CAS  PubMed  Google Scholar 

  18. Chen P, Torralba M, Tan J, Embree M, Zengler K, Stärkel P, van Pijkeren JP, DePew J, Loomba R, Ho SB, Bajaj JS, Mutlu EA, Keshavarzian A, Tsukamoto H, Nelson KE, Fouts DE, Schnabl B (2015) Supplementation of saturated long-chain fatty acids maintains intestinal eubiosis and reduces ethanol-induced liver injury in mice. Gastroenterology 148(1):203–214 e216. https://doi.org/10.1053/j.gastro.2014.09.014

    Article  CAS  PubMed  Google Scholar 

  19. Kirpich IA, Petrosino J, Ajami N, Feng W, Wang Y, Liu Y, Beier JI, Barve SS, Yin X, Wei X, Zhang X, McClain CJ (2016) Saturated and unsaturated dietary fats differentially modulate ethanol-induced changes in gut microbiome and metabolome in a mouse model of alcoholic liver disease. Am J Pathol 186(4):765–776. https://doi.org/10.1016/j.ajpath.2015.11.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Cope K, Risby T, Diehl AM (2000) Increased gastrointestinal ethanol production in obese mice: implications for fatty liver disease pathogenesis. Gastroenterology 119(5):1340–1347

    Article  CAS  Google Scholar 

  21. Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, Baker RD, Gill SR (2013) Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57(2):601–609. https://doi.org/10.1002/hep.26093

    Article  CAS  Google Scholar 

  22. Zhu L, Baker RD, Zhu R, Baker SS (2016) Gut microbiota produce alcohol and contribute to NAFLD. Gut 65(7):1232. https://doi.org/10.1136/gutjnl-2016-311571

    Article  CAS  Google Scholar 

  23. Sookoian S, Pirola CJ (2017) Genetic predisposition in nonalcoholic fatty liver disease. Clin Mol Hepatol 23(1):1–12. https://doi.org/10.3350/cmh.2016.0109

    Article  PubMed  PubMed Central  Google Scholar 

  24. Sherman PM, Ossa JC, Johnson-Henry K (2009) Unraveling mechanisms of action of probiotics. Nutr Clin Pract 24(1):10–14. https://doi.org/10.1177/0884533608329231

    Article  PubMed  Google Scholar 

  25. Mizock BA (2015) Probiotics. Dis Mon 61(7):259–290. https://doi.org/10.1016/j.disamonth.2015.03.011

    Article  PubMed  Google Scholar 

  26. Schnabl B, Brenner DA (2014) Interactions between the intestinal microbiome and liver diseases. Gastroenterology 146(6):1513–1524. https://doi.org/10.1053/j.gastro.2014.01.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Szabo G, Bala S (2010) Alcoholic liver disease and the gut-liver axis. World J Gastroenterol 16(11):1321–1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hartmann P, Chen P, Wang HJ, Wang L, McCole DF, Brandl K, Stärkel P, Belzer C, Hellerbrand C, Tsukamoto H, Ho SB, Schnabl B (2013) Deficiency of intestinal mucin-2 ameliorates experimental alcoholic liver disease in mice. Hepatology 58(1):108–119. https://doi.org/10.1002/hep.26321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yan AW, Fouts DE, Brandl J et al (2011) Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 53(1):96–105. https://doi.org/10.1002/hep.24018

    Article  CAS  PubMed  Google Scholar 

  30. Bull-Otterson L, Feng W, Kirpich I, Wang Y, Qin X, Liu Y, Gobejishvili L, Joshi-Barve S, Ayvaz T, Petrosino J, Kong M, Barker D, McClain C, Barve S (2013) Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of lactobacillus rhamnosus GG treatment. PLoS One 8(1):e53028. https://doi.org/10.1371/journal.pone.0053028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Chiu WC, Huang YL, Chen YL, Peng HC, Liao WH, Chuang HL, Chen JR, Yang SC (2015) Synbiotics reduce ethanol-induced hepatic steatosis and inflammation by improving intestinal permeability and microbiota in rats. Food Funct 6(5):1692–1700. https://doi.org/10.1039/c5fo00104h

    Article  CAS  PubMed  Google Scholar 

  32. Bajaj JS, Heuman DM, Hylemon PB, Sanyal AJ, White MB, Monteith P, Noble NA, Unser AB, Daita K, Fisher AR, Sikaroodi M, Gillevet PM (2014) Altered profile of human gut microbiome is associated with cirrhosis and its complications. J Hepatol 60(5):940–947. https://doi.org/10.1016/j.jhep.2013.12.019

    Article  CAS  Google Scholar 

  33. Gabbard SL, Lacy BE, Levine GM, Crowell MD (2014) The impact of alcohol consumption and cholecystectomy on small intestinal bacterial overgrowth. Dig Dis Sci 59(3):638–644. https://doi.org/10.1007/s10620-013-2960-y

    Article  CAS  PubMed  Google Scholar 

  34. Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, Windey K, Tremaroli V, Bäckhed F, Verbeke K, de Timary P, Delzenne NM (2014) Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci U S A 111(42):E4485–E4493. https://doi.org/10.1073/pnas.1415174111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kirpich IA, Solovieva NV, Leikhter SN, Shidakova NA, Lebedeva OV, Sidorov PI, Bazhukova TA, Soloviev AG, Barve SS, McClain CJ, Cave M (2008) Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: a pilot study. Alcohol 42(8):675–682. https://doi.org/10.1016/j.alcohol.2008.08.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tuomisto S, Pessi T, Collin P, Vuento R, Aittoniemi J, Karhunen PJ (2014) Changes in gut bacterial populations and their translocation into liver and ascites in alcoholic liver cirrhotics. BMC Gastroenterol 14:40. https://doi.org/10.1186/1471-230X-14-40

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mutlu EA, Gillevet PM, Rangwala H, Sikaroodi M, Naqvi A, Engen PA, Kwasny M, Lau CK, Keshavarzian A (2012) Colonic microbiome is altered in alcoholism. Am J Physiol Gastrointest Liver Physiol 302(9):G966–G978. https://doi.org/10.1152/ajpgi.00380.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Llopis M, Cassard AM, Wrzosek L, Boschat L, Bruneau A, Ferrere G, Puchois V, Martin JC, Lepage P, le Roy T, Lefèvre L, Langelier B, Cailleux F, González-Castro AM, Rabot S, Gaudin F, Agostini H, Prévot S, Berrebi D, Ciocan D, Jousse C, Naveau S, Gérard P, Perlemuter G (2016) Intestinal microbiota contributes to individual susceptibility to alcoholic liver disease. Gut 65(5):830–839. https://doi.org/10.1136/gutjnl-2015-310585

    Article  CAS  PubMed  Google Scholar 

  39. Kakiyama G, Hylemon PB, Zhou H, Pandak WM, Heuman DM, Kang DJ, Takei H, Nittono H, Ridlon JM, Fuchs M, Gurley EC, Wang Y, Liu R, Sanyal AJ, Gillevet PM, Bajaj JS (2014) Colonic inflammation and secondary bile acids in alcoholic cirrhosis. Am J Physiol Gastrointest Liver Physiol 306(11):G929–G937. https://doi.org/10.1152/ajpgi.00315.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tsai CC, Hsih HY, Chiu HH, Lai YY, Liu JH, Yu B, Tsen HY (2005) Antagonistic activity against Salmonella infection in vitro and in vivo for two lactobacillus strains from swine and poultry. Int J Food Microbiol 102(2):185–194. https://doi.org/10.1016/j.ijfoodmicro.2004.12.014

    Article  PubMed  Google Scholar 

  41. Younts-Dahl SM, Osborn GD, Galyean ML et al (2005) Reduction of Escherichia coli O157 in finishing beef cattle by various doses of lactobacillus acidophilus in direct-fed microbials. J Food Prot 68(1):6–10

    Article  PubMed  Google Scholar 

  42. Peterson RE, Klopfenstein TJ, Moxley RA et al (2007) Efficacy of dose regimen and observation of herd immunity from a vaccine against Escherichia coli O157:H7 for feedlot cattle. J Food Prot 70(11):2561–2567

    Article  CAS  PubMed  Google Scholar 

  43. Roselli M, Finamore A, Britti MS, Mengheri E (2006) Probiotic bacteria Bifidobacterium animalis MB5 and lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br J Nutr 95(6):1177–1184

    Article  CAS  PubMed  Google Scholar 

  44. Segawa S, Wakita Y, Hirata H, Watari J (2008) Oral administration of heat-killed lactobacillus brevis SBC8803 ameliorates alcoholic liver disease in ethanol-containing diet-fed C57BL/6N mice. Int J Food Microbiol 128(2):371–377. https://doi.org/10.1016/j.ijfoodmicro.2008.09.023

    Article  CAS  PubMed  Google Scholar 

  45. Forsyth CB, Farhadi A, Jakate SM, Tang Y, Shaikh M, Keshavarzian A (2009) Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43(2):163–172. https://doi.org/10.1016/j.alcohol.2008.12.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Arora S, Kaur IP, Chopra K et al (2014) Efficiency of double layered microencapsulated probiotic to modulate proinflammatory molecular markers for the management of alcoholic liver disease. Mediators Inflamm 2014:715130. https://doi.org/10.1155/2014/715130

  47. Wang Y, Liu Y, Kirpich I, Ma Z, Wang C, Zhang M, Suttles J, McClain C, Feng W (2013) Lactobacillus rhamnosus GG reduces hepatic TNFalpha production and inflammation in chronic alcohol-induced liver injury. J Nutr Biochem 24(9):1609–1615. https://doi.org/10.1016/j.jnutbio.2013.02.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wang Y, Kirpich I, Liu Y, Ma Z, Barve S, McClain CJ, Feng W (2011) Lactobacillus rhamnosus GG treatment potentiates intestinal hypoxia-inducible factor, promotes intestinal integrity and ameliorates alcohol-induced liver injury. Am J Pathol 179(6):2866–2875. https://doi.org/10.1016/j.ajpath.2011.08.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhang M, Wang C, Wang C, Zhao H, Zhao C, Chen Y, Wang Y, McClain C, Feng W (2015) Enhanced AMPK phosphorylation contributes to the beneficial effects of lactobacillus rhamnosus GG supernatant on chronic-alcohol-induced fatty liver disease. J Nutr Biochem 26(4):337–344. https://doi.org/10.1016/j.jnutbio.2014.10.016

    Article  CAS  PubMed  Google Scholar 

  50. Wang Y, Liu Y, Sidhu A, Ma Z, McClain C, Feng W (2012) Lactobacillus rhamnosus GG culture supernatant ameliorates acute alcohol-induced intestinal permeability and liver injury. Am J Physiol Gastrointest Liver Physiol 303(1):G32–G41. https://doi.org/10.1152/ajpgi.00024.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Chang B, Sang L, Wang Y et al (2013) The protective effect of VSL#3 on intestinal permeability in a rat model of alcoholic intestinal injury. BMC Gastroenterol 13:151. https://doi.org/10.1186/1471-230X-13-151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Bang CS, Hong SH, Suk KT, Kim JB, Han SH, Sung H, Kim EJ, Kim MJ, Kim MY, Baik SK, Kim DJ (2014) Effects of Korean red ginseng (Panax ginseng), urushiol (Rhus vernicifera Stokes), and probiotics (lactobacillus rhamnosus R0011 and lactobacillus acidophilus R0052) on the gut-liver axis of alcoholic liver disease. J Ginseng Res 38(3):167–172. https://doi.org/10.1016/j.jgr.2014.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hong M, Kim SW, Han SH, Kim DJ, Suk KT, Kim YS, Kim MJ, Kim MY, Baik SK, Ham YL (2015) Probiotics (lactobacillus rhamnosus R0011 and acidophilus R0052) reduce the expression of toll-like receptor 4 in mice with alcoholic liver disease. PLoS One 10(2):e0117451. https://doi.org/10.1371/journal.pone.0117451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Stadlbauer V, Mookerjee RP, Hodges S, Wright GAK, Davies NA, Jalan R (2008) Effect of probiotic treatment on deranged neutrophil function and cytokine responses in patients with compensated alcoholic cirrhosis. J Hepatol 48(6):945–951. https://doi.org/10.1016/j.jhep.2008.02.015

    Article  CAS  PubMed  Google Scholar 

  55. Koga H, Tamiya Y, Mitsuyama K, Ishibashi M, Matsumoto S, Imaoka A, Hara T, Nakano M, Ooeda K, Umezaki Y, Sata M (2013) Probiotics promote rapid-turnover protein production by restoring gut flora in patients with alcoholic liver cirrhosis. Hepatol Int 7(2):767–774. https://doi.org/10.1007/s12072-012-9408-x

    Article  PubMed  Google Scholar 

  56. Kwak DS, Jun DW, Seo JG, Chung WS, Park SE, Lee KN, Khalid-Saeed W, Lee HL, Lee OY, Yoon BC, Choi HS (2014) Short-term probiotic therapy alleviates small intestinal bacterial overgrowth, but does not improve intestinal permeability in chronic liver disease. Eur J Gastroenterol Hepatol 26(12):1353–1359. https://doi.org/10.1097/MEG.0000000000000214

    Article  PubMed  Google Scholar 

  57. Borody TJ, Campbell J (2012) Fecal microbiota transplantation: techniques, applications, and issues. Gastroenterol Clin North Am 41(4):781–803. https://doi.org/10.1016/j.gtc.2012.08.008

    Article  PubMed  Google Scholar 

  58. Sidhu SS, Goyal O, Kishore H, Sidhu S (2017) New paradigms in management of alcoholic hepatitis: a review. Hepatol Int 11:255–267. https://doi.org/10.1007/s12072-017-9790-5

    Article  PubMed  Google Scholar 

  59. Smits LP, Bouter KE, de Vos WM et al (2013) Therapeutic potential of fecal microbiota transplantation. Gastroenterology 145(5):946–953. https://doi.org/10.1053/j.gastro.2013.08.058

    Article  PubMed  Google Scholar 

  60. Konturek PC, Koziel J, Dieterich W, Haziri D, Wirtz S, Glowczyk I, Konturek K, Neurath MF, Zopf Y (2016) Successful therapy of Clostridium difficile infection with fecal microbiota transplantation. J Physiol Pharmacol 67(6):859–866

    CAS  PubMed  Google Scholar 

  61. Di Luccia B, Crescenzo R, Mazzoli A et al (2015) Rescue of Fructose-Induced Metabolic Syndrome by antibiotics or Faecal transplantation in a rat model of obesity. PLoS One 10(8):e0134893. https://doi.org/10.1371/journal.pone.0134893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ferrere G, Wrzosek L, Cailleux F, Turpin W, Puchois V, Spatz M, Ciocan D, Rainteau D, Humbert L, Hugot C, Gaudin F, Noordine ML, Robert V, Berrebi D, Thomas M, Naveau S, Perlemuter G, Cassard AM (2017) Fecal microbiota manipulation prevents dysbiosis and alcohol-induced liver injury in mice. J Hepatol 66(4):806–815. https://doi.org/10.1016/j.jhep.2016.11.008

    Article  CAS  PubMed  Google Scholar 

  63. Philips CA, Pande A, Shasthry SM, Jamwal KD, Khillan V, Chandel SS, Kumar G, Sharma MK, Maiwall R, Jindal A, Choudhary A, Hussain MS, Sharma S, Sarin SK (2017) Healthy donor fecal microbiota transplantation in steroid-ineligible severe alcoholic hepatitis: a pilot study. Clin Gastroenterol Hepatol 15(4):600–602. https://doi.org/10.1016/j.cgh.2016.10.029

    Article  PubMed  Google Scholar 

  64. Ren YD, Ye ZS, Yang LZ et al (2016) Fecal microbiota transplantation induces hepatitis B virus e-antigen (HBeAg) clearance in patients with positive HBeAg after long-term antiviral therapy. Hepatology. https://doi.org/10.1002/hep.29008

  65. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125(6):1401–1412

    Article  CAS  Google Scholar 

  66. Watanabe A, Sakai T, Sato S, Imai F, Ohto M, Arakawa Y, Toda G, Kobayashi K, Muto Y, Tsujii T, Kawasaki H, Okita K, Tanikawa K, Fujiyama S, Shimada S (1997) Clinical efficacy of lactulose in cirrhotic patients with and without subclinical hepatic encephalopathy. Hepatology 26(6):1410–1414. https://doi.org/10.1053/jhep.1997.v26.pm0009397979

    Article  CAS  PubMed  Google Scholar 

  67. Tang Y, Forsyth CB, Banan A, Fields JZ, Keshavarzian A (2009) Oats supplementation prevents alcohol-induced gut leakiness in rats by preventing alcohol-induced oxidative tissue damage. J Pharmacol Exp Ther 329(3):952–958. https://doi.org/10.1124/jpet.108.148643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Burokas A, Arboleya S, Moloney RD et al (2017) Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry 82(7):472–487. https://doi.org/10.1016/j.biopsych.2016.12.031

  69. Ohshima T, Kojima Y, Seneviratne CJ, Maeda N (2016) Therapeutic application of Synbiotics, a fusion of probiotics and prebiotics, and Biogenics as a new concept for oral Candida infections: a mini review. Front Microbiol 7:10. https://doi.org/10.3389/fmicb.2016.00010

    Article  PubMed  PubMed Central  Google Scholar 

  70. Olveira G, Gonzalez-Molero I (2016) An update on probiotics, prebiotics and symbiotics in clinical nutrition. Endocrinol Nutr 63(9):482–494. https://doi.org/10.1016/j.endonu.2016.07.006

    Article  PubMed  Google Scholar 

  71. Ianiro G, Tilg H, Gasbarrini A (2016) Antibiotics as deep modulators of gut microbiota: between good and evil. Gut 65(11):1906–1915. https://doi.org/10.1136/gutjnl-2016-312297

    Article  CAS  PubMed  Google Scholar 

  72. Sung H, Kim SW, Hong M, Suk KT (2016) Microbiota-based treatments in alcoholic liver disease. World J Gastroenterol 22(29):6673–6682. https://doi.org/10.3748/wjg.v22.i29.6673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Reijnders D, Goossens GH, Hermes GD et al (2016) Effects of gut microbiota manipulation by antibiotics on host metabolism in obese humans: a randomized double-blind placebo-controlled trial. Cell Metab 24(1):63–74. https://doi.org/10.1016/j.cmet.2016.06.016

    Article  CAS  PubMed  Google Scholar 

  74. Bergheim I, Weber S, Vos M, Krämer S, Volynets V, Kaserouni S, McClain CJ, Bischoff SC (2008) Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol 48(6):983–992. https://doi.org/10.1016/j.jhep.2008.01.035

    Article  CAS  PubMed  Google Scholar 

  75. Gangarapu V, Ince AT, Baysal B, Kayar Y, Klç U, Gök Ö, Uysal Ö, Şenturk H (2015) Efficacy of rifaximin on circulating endotoxins and cytokines in patients with nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 27(7):840–845. https://doi.org/10.1097/MEG.0000000000000348

    Article  CAS  PubMed  Google Scholar 

  76. Vlachogiannakos J, Saveriadis AS, Viazis N et al (2009) Intestinal decontamination improves liver haemodynamics in patients with alcohol-related decompensated cirrhosis. Aliment Pharmacol Ther 29(9):992–999. https://doi.org/10.1111/j.1365-2036.2009.03958.x

    Article  CAS  Google Scholar 

  77. Vlachogiannakos J, Viazis N, Vasianopoulou P, Vafiadis I, Karamanolis DG, Ladas SD (2013) Long-term administration of rifaximin improves the prognosis of patients with decompensated alcoholic cirrhosis. J Gastroenterol Hepatol 28(3):450–455. https://doi.org/10.1111/jgh.12070

    Article  CAS  Google Scholar 

  78. Gupta N, Kumar A, Sharma P, Garg V, Sharma BC, Sarin SK (2013) Effects of the adjunctive probiotic VSL#3 on portal haemodynamics in patients with cirrhosis and large varices: a randomized trial. Liver Int 33(8):1148–1157. https://doi.org/10.1111/liv.12172

    Article  CAS  Google Scholar 

  79. Bass NM, Mullen KD, Sanyal A, Poordad F, Neff G, Leevy CB, Sigal S, Sheikh MY, Beavers K, Frederick T, Teperman L, Hillebrand D, Huang S, Merchant K, Shaw A, Bortey E, Forbes WP (2010) Rifaximin treatment in hepatic encephalopathy. N Engl J Med 362(12):1071–1081. https://doi.org/10.1056/NEJMoa0907893

    Article  CAS  Google Scholar 

  80. Madrid AM, Hurtado C, Venegas M, Cumsille F, Defilippi C (2001) Long-term treatment with cisapride and antibiotics in liver cirrhosis: effect on small intestinal motility, bacterial overgrowth, and liver function. Am J Gastroenterol 96(4):1251–1255. https://doi.org/10.1111/j.1572-0241.2001.03636.x

    Article  CAS  PubMed  Google Scholar 

  81. Chen H, Shen F, Sherban A, Nocon A, Li Y, Wang H, Xu MJ, Rui X, Han J, Jiang B, Lee D, Li N, Keyhani-Nejad F, Fan JG, Liu F, Kamat A, Musi N, Guarente L, Pacher P, Gao B, Zang M (2018) DEPTOR suppresses lipogenesis and ameliorates hepatic steatosis and acute-on-chronic liver injury in alcoholic liver disease. Hepatology. https://doi.org/10.1002/hep.29849

Download references

Funding

This research was supported by Hallym University Research Fund, Korea National Research Foundation (NRF-2015R1C1A1A01053232 and NRF-2018M3A9F3020956), and Hallym University Research Fund 2016 (HURF-2016-60).

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Hallym University Chuncheon Sacred Heart Hospital, Hallym University College of Medicine, Gyo-dong, Chuncheon, 24253, South Korea

    Meegun Hong, Dae Hee Han, Jitaek Hong, Dong Joon Kim & Ki Tae Suk

Authors
  1. Meegun Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dae Hee Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jitaek Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Joon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ki Tae Suk
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Meegun Hong: analysis and interpretation of the data, collection and assembly of data, drafting of the article. Ki Tae Suk: conception and design, critical revision of the article for important intellectual content, final approval of the article. Dae Hee Han and Jitaek Hong: critical revision of the article for important intellectual content. Dong Joon Kim: provision of study materials.

Corresponding author

Correspondence to Ki Tae Suk.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Meegun Hong, Dae Hee Han, and Jitaek Hong share co-first author.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hong, M., Han, D.H., Hong, J. et al. Are Probiotics Effective in Targeting Alcoholic Liver Diseases?. Probiotics & Antimicro. Prot. 11, 335–347 (2019). https://doi.org/10.1007/s12602-018-9419-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-018-9419-6

Keywords

Search

Navigation