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Intestinal permeability, microbial translocation, changes in duodenal and fecal microbiota, and their associations with alcoholic liver disease progression in humans
Open accessAbstract
Background Animal data suggest a role of the gut-liver axis in progression of alcoholic liver disease (ALD), but human data are scarce especially for early disease stages.Methods We included patients with alcohol use disorder (AUD) who follow a rehabilitation program and matched healthy controls. We determined intestinal epithelial and vascular permeability (IP) (using urinary excretion of 51Cr-EDTA, fecal albumin content, and immunohistochemistry in distal duodenal biopsies), epithelial damage (histology, serum iFABP, and intestinal gene expression), and microbial translocation (Gram – and Gram + serum markers by ELISA). Duodenal mucosa-associated microbiota and fecal microbiota were analyzed by 16 S rRNA sequencing. ALD was staged by Fibroscan® (liver stiffness, controlled attenuation parameter) in combination with serum AST, ALT, and CK18-M65.Results Only a subset of AUD patients had increased 51Cr-EDTA and fecal albumin together with disrupted tight junctions and vasculature expression of plasmalemma Vesicle-Associated Protein-1. The so-defined increased intestinal permeability was not related to changes of the duodenal microbiota or alterations of the intestinal epithelium but associated with compositional changes of the fecal microbiota. Leaky gut alone did not explain increased microbial translocation in AUD patients. By contrast, duodenal dysbiosis with a dominance shift toward specific potential pathogenic bacteria genera (Streptococcus, Shuttleworthia, Rothia), increased IP and elevated markers of microbial translocation characterized AUD patients with progressive ALD (steato-hepatitis, steato-fibrosis).Conclusion Progressive ALD already at early disease stages is associated with duodenal mucosa-associated dysbiosis and elevated microbial translocation. Surprisingly, such modifications were not linked with increased IP. Rather, increased IP appears related to fecal microbiota dysbiosis.
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“Alcoholic liver disease (ALD) is associated with gut microbial dysbiosis,113, 114, 115”
From Regulation of Intestinal Barrier Function by Microbial Metabolites (2021) · cites this paper as [113]
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Role of ER Stress in Xenobiotic‐Induced Liver Diseases and Hepatotoxicity
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“ALD attributed to long-term alcohol consumption is one of the major causes of chronic liver disease [17], a ff ecting millions of patients around the world.”
Zhao, L., Wang, S., Zhang, N., Zhou, J., Mehmood, A., Raka, R. N., Zhou, F. L., & Zhao, L. (2022) · Antioxidants · doi:10.3390/antiox11061211 · Cited by 23
“Therefore, increased intestinal permeability caused by microbial dysregulation is an important prerequisite for the progression of ALD [57,58].”
BackgroundGut Microbiota Modulation of Short Bowel Syndrome and the Gut–Brain Axis
Carter, J., Bettag, J., Morfin, S., Manithody, C., Nagarapu, A., Jain, A., Nazzal, H., Prem, S., Unes, M., McHale, M., et al. (2023) · Nutrients · doi:10.3390/nu15112581 · Cited by 21
“An increase in permeability can also drive endotoxin mediated hepatic and systemic inflammatory responses [53,54].”
BackgroundBetaine regulates the gut-liver axis: a therapeutic approach for chronic liver diseases
Perumal, S. K., Arumugam, M. K., Osna, N. A., Rasineni, K., & Kharbanda, K. K. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1478542 · Cited by 22
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“Alcohol (ethanol) also changes the composition of the microbiome in ALD [31,42–45], even at the early stages of ALD, causing dysbiosis and bacterial translocation [45].”
BackgroundMaccioni, L., Guan, Y., Kim, M., Parra, M. A., Peiffer, B., Fu, Y., Wang, Y., Lin, Y.-H., Mackowiak, B., Feng, D., et al. (2025) · Gut · doi:10.1136/gutjnl-2024-334412 · Cited by 21
Self-citationGut microbiome and liver diseases
Xu, J., Chen, N., Zhou, L., & Liu, Y. (2024) · Fundamental Research · doi:10.1016/j.fmre.2024.09.007 · Cited by 20
“Additionally, microbial translocation into the liver directly leads to immunological disturbances, dysbiosis of hepatic triglyceride metabolism, and NAFLD progression [ 39 , 41 ].”
Gut Microbiota as Emerging Players in the Development of Alcohol-Related Liver Disease
Li, W., Gao, W., Yan, Q. S., Yang, L., Zhu, Q., & Chu, H. (2024) · Biomedicines · doi:10.3390/biomedicines13010074 · Cited by 19
“The intestinal barrier is disrupted in ALD, allowing pathogens and microbial products to be transferred into the circulation [16,22,48].”
Fuke, N., Yamashita, T., Shimizu, S., Matsumoto, M., Sawada, K., Jung, S., Tokuda, I., Misawa, M., Suzuki, S., Ushida, Y., et al. (2023) · Metabolites · doi:10.3390/metabo13020250 · Cited by 22
“Patients with alcoholic liver disease have a higher composition ratio of Streptococcus in the fecal flora, intestinal permeability, and blood LBP concentration compared to healthy subjects [97].”
BackgroundChen, D., Xiong, J., CHEN, G., ZHANG, Z., LIU, Y., XU, J., & XU, H. (2023) · In Vivo · doi:10.21873/invivo.13308 · Cited by 18
Liu, L., Zhao, Z., Liu, H., Xia, X., Ai, C., Song, S., & Yan, C. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.133014 · Cited by 17
Targeting the gut microbiota to treat alcoholic liver diseases: evidence and promises.
Leclercq, S., de Timary, P., & Stärkel, P. (2020) · PubMed · Cited by 17
Self-citationImmune cells in alcohol-related liver disease
Xu, H., & Wang, H. (2022) · Liver Research · doi:10.1016/j.livres.2022.01.001 · Cited by 17
Insights into the gut-liver axis: mechanisms and emerging therapies in hepatocellular carcinoma
Hu, Y., Gao, M., Chenghuang, J., & Bao, R. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1595853 · Cited by 16
Activation of intestinal endogenous retroviruses by alcohol exacerbates liver disease
Cabré, N., Fondevila, M. F., Wei, W., Yamazaki, T., Tonetti, F. R., Eguileor, Á., Garcia‐Carbonell, R., Meijnikman, A. S., Miyamoto, Y., Mayo, S. L., et al. (2025) · Journal of Clinical Investigation · doi:10.1172/jci188541 · Cited by 15
Self-citationPuhakka, E., Ahmed, H., Haikonen, R., Leclercq, S., Hanhineva, K., Maccioni, L., Amadieu, C., Lehtonen, M., Männistö, V., Rysä, J., et al. (2025) · Liver International · doi:10.1111/liv.70128 · Cited by 14
Self-citationXiang, M., Zheng, L., Pu, D., Lin, F., Ma, X., Ye, H., Pu, D., Zhang, Y., Wang, D., Wang, X., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.909729 · Cited by 14
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“In addition, alcohol abuse alters the composition and function of intestinal microorganisms, leading to disorders of hepatic lipid metabolism and increased hepatic fats deposition; the accumulation of these fats in the liver may lead to the development of fatty liver and other liver diseases [8].”
BackgroundIntestinal ELF4 Deletion Exacerbates Alcoholic Liver Disease by Disrupting Gut Homeostasis
Liu, T., Yu, H., Zhang, Z., Xie, Y., Yang, L., & You, F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094825 · Cited by 14
“Reported results indicate that increased intestinal permeability is related to fecal microbiota dysbiosis [15].”
BackgroundBalakrishnan, J., Kannan, S., Arivazhagan, G., Ramachandran, N., & Sundarasamy, V. G. (2025) · Medicine in Microecology · doi:10.1016/j.medmic.2025.100154 · Cited by 15
Implications of the Liver-Gut Axis in Liver Disease: From Mechanisms to Therapeutic Targets
Ramírez-Mejía, M. M., Ponciano‐Rodríguez, G., & Méndez‐Sánchez, N. (2025) · Archives of Medical Research · doi:10.1016/j.arcmed.2025.103335 · Cited by 15
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Yak milk protects against alcohol-induced liver injury in rats
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Role of the Gut Microbiome in Metabolic Dysfunction-Associated Steatotic Liver Disease
Maher, S., Rajapakse, J., El-Omar, E. M., & Zekry, A. (2024) · Seminars in Liver Disease · doi:10.1055/a-2438-4383 · Cited by 14
Liu, S., Zhao, Y., Liu, Y., Tang, Y., Xu, X., Wang, M., Tao, X., & Xu, H. (2021) · Toxicological Sciences · doi:10.1093/toxsci/kfab127 · Cited by 12
Gao, B., Zhu, Y., Gao, N., Shen, W., Stärkel, P., & Schnabl, B. (2021) · Metabolites · doi:10.3390/metabo11110766 · Cited by 11
Self-citationImmune dysregulation and pathophysiology of alcohol consumption and alcoholic liver disease
Martínez‐Castillo, M., Altamirano-Mendoza, I., Sánchez-Valle, S., García-Islas, L., Sánchez-Barragán, M., Hernandez-Santillan, M., Hernández-Barragán, A., Pérez-Hernández, J. L., la Tijera, F. H., & Gutiérrez‐Reyes, G. (2023) · Revista de Gastroenterología de México (English Edition) · doi:10.1016/j.rgmxen.2023.03.003 · Cited by 11
Alcohol-associated liver disease: Emerging therapeutic strategies
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“A systematic review of 13 studies [5 randomized controlled trial (RCTs)] of the impact of psychosocial studies in 1945 patients with chronic liver disease observed that only an integrated approach combining cognitive behavioral therapy, motivational enhancement therapy, and medical care, provided…”
Gao, H., Bai, H., Su, Y., Gao, Y., Fang, H., Li, D., Yu, Y., Xing, L., Xia, D., Mao, D., et al. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06573-5 · Cited by 11
“1F), all of which have been implicated in the pathogenesis of ALD [37, 38].”
Probiotics attenuate alcohol-induced muscle mechanical hyperalgesia: Preliminary observations
Green, P. G., Álvarez, P., & Levine, J. D. (2022) · Molecular Pain · doi:10.1177/17448069221075345 · Cited by 12
“It is well established that chronic alcohol consumption has a marked impact on the gastrointestinal (gut) microbiome, as well as increasing gut permeability.(12,13) Given the recent appreciation of the ability of gut microbiota to modulate chronic pain, and that gut microbial diversity is markedly affected by alcohol…”
BackgroundMaccioni, L., Kasavuli, J., Leclercq, S., Pirlot, B., Laloux, G., Horsmans, Y., Leclercq, I. A., Schnabl, B., & Stärkel, P. (2023) · Hepatology Communications · doi:10.1097/hc9.0000000000000107 · Cited by 12
“Conclusions: Our results point to the contribution of activated monocytes to systemic inflammation and ALD.”
BackgroundInfluentialSelf-citationHuang, J., Yu, Y., Feng, Z., Yin, Y., Liu, Y., Liu, X., & Yu, R. (2025) · International Journal of Nanomedicine · doi:10.2147/ijn.s548624 · Cited by 10
Yang, W., Xi, C., Yao, H., Yuan, Q., Zhang, J., Chen, Q., Wu, G., & Hu, J. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1304218 · Cited by 11
Joon, A., Sharma, A., Jalandra, R., Bayal, N., Dhar, R., & Karmakar, S. (2024) · Journal of Translational Gastroenterology · doi:10.14218/jtg.2023.00018 · Cited by 11
Gut cannabinoid receptor 1 regulates alcohol binge-induced intestinal permeability
Maccioni, L., Dvorácskó, S., Godlewski, G., Çınar, R., Iyer, M. R., Gao, B., & Kunos, G. (2025) · eGastroenterology · doi:10.1136/egastro-2024-100173 · Cited by 12
Self-citation
Metadata
- Authors
- Maccioni, L., Gao, B., Leclercq, S., Pirlot, B., Horsmans, Y., De Timary, P., Leclercq, I., Fouts, D., Schnabl, B., & Stärkel, P.
- Affiliations
- UCLouvain (BE)
- University of California San Diego (US)
- Cliniques Universitaires Saint-Luc (BE)
- Department of Adult Psychiatry, Cliniques Universitaires Saint-Luc, Brussels, Belgium
- J. Craig Venter Institute (US)
- Corresponding author
- Stärkel, Peter
- ORCID
- Venue
- Gut Microbes
- Publisher
- Informa UK Limited
- Published
- 2020-06-26
- Volume
- 12
- Issue
- 1
- Pages
- 1782157
- ISSN
- 1949-0976 (ISSN-L)
- 1949-0984
- PMC
- PMC7524402
- OpenAlex
- W3037663071
- Cited by
- 174
- References
- 58
- Citations by year
- 2026: 25 · 2025: 33 · 2024: 31 · 2023: 29 · 2022: 27 · 2021: 22 · 2020: 7
- FWCI
- 6.86
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Gut Microbes (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Fonds De La Recherche Scientifique - FNRS (J.0146.17, T.0217.18)
- National Institutes of Health (U01 AA026939, R01 AA24726)
- Université Catholique de Louvain (ARC 2018)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Pathology and Forensic Medicine › Alcohol Consumption and Health Effects
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- alcoholic liver disease, alcoholism, intestinal permeability, leaky gut, microbial translocation, gut-liver axis, duodenal microbiota, duodenal mucosa, tight junctions, intestinal epithelial damage, Streptococcus, Shuttleworthia, Rothia, liver fibrosis, steatohepatitis
- MeSH terms
- Gastrointestinal Microbiome, Adult, Alcoholism, Bacteria, Capillary Permeability, Duodenum, Feces, Female, Humans, Intestinal Mucosa, Liver, Liver Diseases, Alcoholic, Male, Middle Aged, RNA, Ribosomal, 16S, Dysbiosis
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