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Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects
Abstract
BACKGROUND AND AIMS Mood and cognition alterations play a role in the motivation for alcohol-drinking. Lipopolysaccharides are known to stimulate inflammation that was shown to induce mood and cognitive changes in rodents and humans. Enhanced intestinal permeability and elevated blood LPS characterize alcohol-dependent mice. However, no data have been published in non-cirrhotic humans. Our first goal was to test whether intestinal permeability, blood LPS and cytokines are increased in non-cirrhotic alcohol-dependent subjects before withdrawal and if they recover after withdrawal. Our second goal was to test correlations between these biochemical and the behavioral variables to explore the possibility of a role for a gut-brain interaction in the development of alcohol-dependence. METHODS Forty alcohol-dependent-subjects hospitalized for a 3-week detoxification program were tested at onset (T1) and end (T2) of withdrawal and compared for biological and behavioral markers with 16 healthy subjects. Participants were assessed for gut permeability, systemic inflammation (LPS, TNFα, IL-6, IL-10, hsCRP) and for depression, anxiety, alcohol-craving and selective attention. RESULTS Intestinal permeability and LPS were largely increased in alcohol-dependent subjects at T1 but recovered completely at T2. A low-grade inflammation was observed at T1 that partially decreased during withdrawal. At T1, pro-inflammatory cytokines were positively correlated with craving. At T2 however, the anti-inflammatory cytokine IL-10 was negatively correlated with depression, anxiety and craving. CONCLUSION Leaky gut and inflammation were observed in non-cirrhotic alcohol-dependent subjects and inflammation was correlated to depression and alcohol-craving. This suggests that the gut-brain axis may play a role in the pathogenesis of alcohol-dependence.
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“Given the links between impaired gastrointestinal health and neuroinflammation (145), targeted nutrition interventions may ameliorate neuroinflammation, which has been identified as a potential treatment for OUD (78).”
From A Biopsychosocial Overview of the Opioid Crisis: Considering Nutrition and Gastrointestinal Health (2019) · cites this paper as [145]
Citations
Cites
Atherosclerosis--an inflammatory disease
Ross, R. (1999) · New England Journal of Medicine · doi:10.1056/nejm199901143400207 · Cited by 21,725
Beck, A. T., Steer, R. A., & Brown, G. (2011) · PsycTESTS Dataset · doi:10.1037/t00742-000 · Cited by 7,535
From inflammation to sickness and depression: when the immune system subjugates the brain
Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., & Kelley, K. W. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2297 · Cited by 7,395
Metabolic Endotoxemia Initiates Obesity and Insulin Resistance
Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A. M., Fava, F., Tuohy, K. M., Chabo, C., et al. (2007) · Diabetes · doi:10.2337/db06-1491 · Cited by 6,638
Self-citationCani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819
Self-citationA Meta-Analysis of Cytokines in Major Depression
Dowlati, Y., Herrmann, N., Swardfager, W., Liu, H., Sham, L., Reim, E. K., & Lanctôt, K. L. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.033 · Cited by 4,729
Interleukin-10-deficient mice develop chronic enterocolitis
Kühn, R., Löhler, J., Rennick, D. M., Rajewsky, K., & Müller, W. (1993) · Cell · doi:10.1016/0092-8674(93)80068-p · Cited by 4,248
An Algorithm for the Grading of Activity in Chronic Hepatitis C
Bédossa, P., & Poynard, T. (1996) · Hepatology · doi:10.1002/hep.510240201 · Cited by 4,107
de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G., & de Vries, J. E. (1991) · The Journal of experimental medicine · doi:10.1084/jem.174.5.1209 · Cited by 3,762
The anti-inflammatory effect of exercise
Petersen, A. M. W., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00164.2004 · Cited by 3,100 · cited 1×
“These results permit us to conclude that alcohol-dependent subjects indeed present with a low-grade inflammation, which is defined by a 2- to 3-fold increase in inflammatory cytokines and acute phase proteins (Petersen and Pedersen, 2005; Ross, 1999).”
Cani, P. D., Possemiers, S., Van de Wiele, T., Guiot, Y., Everard, A., Rottier, O., Geurts, L., Naslain, D., Neyrinck, A., Lambert, D. M., et al. (2009) · Gut · doi:10.1136/gut.2008.165886 · Cited by 2,518
Self-citationGrant, B. F., Dawson, D. A., Stinson, F. S., Chou, S. P., Dufour, M. C., & Pickering, R. P. (2004) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2004.02.004 · Cited by 1,509
Twenty years of research on cytokine-induced sickness behavior
Dantzer, R., & Kelley, K. W. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2006.09.006 · Cited by 1,420
Cytokine-Associated Emotional and Cognitive Disturbances in Humans
Reichenberg, A., Yirmiya, R., Schuld, A., Kraus, T., Haack, M., Morag, A., & Pollmächer, T. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.5.445 · Cited by 1,365
Recognition of pathogen-associated molecular patterns by TLR family
Akira, S., & Hemmi, H. (2003) · Immunology Letters · doi:10.1016/s0165-2478(02)00228-6 · Cited by 1,162
Everard, A., Lazarevic, V., Derrien, M., Girard, M., Muccioli, G. G., Neyrinck, A. M., Possemiers, S., Van Holle, A., François, P., de Vos, W. M., et al. (2011) · Diabetes · doi:10.2337/db11-0227 · Cited by 1,076
Self-citationCytokine-induced sickness behaviour: mechanisms and implications
Konsman, J. P., Parnet, P., & Dantzer, R. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)02088-9 · Cited by 999
Sabat, R., Grütz, G., Warszawska, K., Kirsch, S., Witte, E., Wolk, K., & Geginat, J. (2010) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2010.09.002 · Cited by 977
Intestinal permeability: an overview
Bjarnason, I., Macpherson, A., & Hollander, D. (1995) · Gastroenterology · doi:10.1016/0016-5085(95)90708-4 · Cited by 927
Targeting gut microbiota in obesity: effects of prebiotics and probiotics
Delzenne, N. M., Neyrinck, A. M., Bäckhed, F., & Cani, P. D. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.126 · Cited by 805
Self-citationAntibiotics prevent liver injury in rats following long-term exposure to ethanol
Adachi, Y., Moore, L. E., Bradford, B. U., Gao, W., & Thurman, R. G. (1995) · Gastroenterology · doi:10.1016/0016-5085(95)90027-6 · Cited by 692
The endocannabinoid system links gut microbiota to adipogenesis
Muccioli, G. G., Naslain, D., Bäckhed, F., Reigstad, C. S., Lambert, D. M., Delzenne, N. M., & Cani, P. D. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.46 · Cited by 691
Self-citationAnton, R. F., Moak, D. H., & Latham, P. K. (1995) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1995.tb01475.x · Cited by 679
Parlesak, A., Schäfer, C., Schütz, T., Bode, J. C., & Bode, C. (2000) · Journal of Hepatology · doi:10.1016/s0168-8278(00)80242-1 · Cited by 647
Major Depression and Activation of The Inflammatory Response System
Maes, M. (1999) · Advances in Experimental Medicine and Biology · doi:10.1007/978-0-585-37970-8_2 · Cited by 617
Structure of bacterial lipopolysaccharides
Caroff, M., & Karibian, D. (2003) · Carbohydrate Research · doi:10.1016/j.carres.2003.07.010 · Cited by 562
Fukui, H., Brauner, B., Bode, J. C., & Bode, C. (1991) · Journal of Hepatology · doi:10.1016/0168-8278(91)90933-3 · Cited by 461
Nuclear factor‐κB and the hepatic inflammation‐fibrosis‐cancer axis†
Elsharkawy, A. M., & Mann, D. A. (2007) · Hepatology · doi:10.1002/hep.21802 · Cited by 400
Effect of alcohol consumption on the gut.
Bode, C., & Christian Bode, J. (2003) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/s1521-6918(03)00034-9 · Cited by 379
Mutlu, E., Keshavarzian, A., Engen, P. A., Forsyth, C. B., Sikaroodi, M., & Gillevet, P. M. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.01022.x · Cited by 371
Keshavarzian, A., Farhadi, A., Forsyth, C. B., Rangan, J., Jakate, S. M., Shaikh, M. W., Banan, A., & Fields, J. Z. (2008) · Journal of Hepatology · doi:10.1016/j.jhep.2008.10.028 · Cited by 359
Rao, R. K., Seth, A., & Sheth, P. (2004) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00006.2004 · Cited by 340
Bourque, P. E., & Beaudette, D. (1982) · Canadian Journal of Behavioural Science/Revue canadienne des sciences du comportement · doi:10.1037/h0081254 · Cited by 338
Sparkman, N. L., Buchanan, J. B., Heyen, J. R. R., Chen, J., Beverly, J. L., & Johnson, R. W. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3376-06.2006 · Cited by 307
Exacerbation of Alcoholic Liver Injury by Enteral Endotoxin in Rats
Mathurin, P., Deng, Q.-G., Keshavarzian, A., Choudhary, S., HOLMES, E. W., & Tsukamoto, H. (2000) · Hepatology · doi:10.1053/jhep.2000.19621 · Cited by 297
The turnover and shedding of epithelial cells
Creamer, B., Shorter, R. G., & Bamforth, J. S. (1961) · Gut · doi:10.1136/gut.2.2.110 · Cited by 297
What is craving? Models and implications for treatment.
Anton, R. F. (1999) · PubMed Central · Cited by 289
Structural and functional analyses of bacterial lipopolysaccharides
Caroff, M., Karibian, D., Cavaillon, J., & Haeffner‐Cavaillon, N. (2002) · Microbes and Infection · doi:10.1016/s1286-4579(02)01612-x · Cited by 210
Renal Tubular Dysfunction in Chronic Alcohol Abuse -- Effects of Abstinence
Marchi, S. D., Cecchin, E., Basile, A., Bertotti, A., Nardini, R., & Bartoli, E. (1993) · New England Journal of Medicine · doi:10.1056/nejm199312233292605 · Cited by 188
Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats
Bluthé, R.-M., Castanon, N., Pousset, F., Bristow, A., Ball, C., Lestage, J., Michaud, B., KELLEY, K. W., & Dantzer, R. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00077-8 · Cited by 179
IL-10 modulates depressive-like behavior
Mesquita, A. R., Correia‐Neves, M., Roque, S., Castro, A. G., Vieira, P., Pedrosa, J., Palha, J. A., & Sousa, N. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.02.004 · Cited by 159
Circulating antiinflammatory cytokine IL-10 in patients with inflammatory bowel disease (IBD)
Kucharzik, T. F., Stoll, R., Lügering, N., & Domschke, W. (1995) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.1995.tb03721.x · Cited by 158
Endotoxin and Kupffer cell activation in alcoholic liver disease.
Wheeler, M. D. (2003) · Europe PMC (PubMed Central) · Cited by 155
In Situ Expression of Interleukin-10 in Noninflamed Human Gut and in Inflammatory Bowel Disease
Autschbach, F., Braunstein, J., Helmke, B. M., ZUNA, I., Schürmann, G., Niemir, Z. I., Wallich, R., Otto, H. F., & Meuer, S. C. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65552-6 · Cited by 151
Medication treatment of different types of alcoholism
Johnson, B. A. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.08101500 · Cited by 151 · cited 2×
“Indeed current pharmacological approaches of alcohol-dependence that only target brain neurotransmitters have proved so far to be modestly efficient (Johnson, 2010), eventually because they fail to take into account of intestinal permeability and inflammation as a driving force for the…”
Alcohol in Europe – Public Health Perspective: Report summary
Anderson, P., & Geiger, B. B. (2006) · Drugs Education Prevention and Policy · doi:10.1080/09687630600902477 · Cited by 145
de Timary, P., Luts, A., Hers, D., & Luminet, O. (2007) · Psychiatry Research · doi:10.1016/j.psychres.2006.12.008 · Cited by 136
Cognitive deficits in interleukin-10-deficient mice after peripheral injection of lipopolysaccharide
Richwine, A. F., Sparkman, N. L., Dilger, R. N., Buchanan, J. B., & Johnson, R. W. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.02.020 · Cited by 118
Allez, M., & Mayer, L. (2004) · Inflammatory Bowel Diseases · doi:10.1097/00054725-200409000-00027 · Cited by 114
Luoto, R., Kalliomäki, M. A., Laitinen, K., Delzenne, N. M., Cani, P. D., Salminen, S., & Isolauri, E. (2010) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181f3457f · Cited by 110
Self-citationAlcohol and depression: a clinical perspective
Schuckit, M. A. (1994) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1994.tb05798.x · Cited by 104
Intestinal mucosal alterations in experimental cirrhosis in the rat: Role of oxygen free radicals
Ramachandran, A., Ramamoorthy, P., Thomas, S., Reddy, J. B., Pulimood, A. B., & Balasubramanian, K. A. (2002) · Hepatology · doi:10.1053/jhep.2002.31656 · Cited by 100
Endotoxemia-induced inflammation and the effect on the human brain
van den Boogaard, M., Ramakers, B. P., van Alfen, N., van der Werf, S. P., Fick, W. F., Hoedemaekers, C. W., Verbeek, M. M., Schoonhoven, L., van der Hoeven, J. G., & Pickkers, P. (2010) · Critical Care · doi:10.1186/cc9001 · Cited by 84
Bode, C., Kolepke, R., Schäfer, K., & Bode, J. C. (1993) · PubMed · Cited by 79
Effect of Detoxification on Liver Stiffness Assessed by Fibroscan® in Alcoholic Patients
Gelsi, È., Dainese, R., Truchi, R., Mariné–Barjoan, E., Anty, R., Autuori, M., Burroni, S., Vanbiervliet, G., Evesque, L., Chérikh, F., et al. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01374.x · Cited by 78
Ansseau, M., Besson, J., Lejoyeux, M., Pinto, E., Landry, U., Cornes, M., Deckers, F., Potgieter, A. S., & Adès, J. (2000) · European Addiction Research · doi:10.1159/000019010 · Cited by 66
Uva, M. C. D. S., Luminet, O., Cortesi, M., Constant, E., Derely, M., & de Timary, P. (2010) · Alcohol and Alcoholism · doi:10.1093/alcalc/agq012 · Cited by 65
Krzyszton, C. P., Sparkman, N. L., Grant, R. W., Buchanan, J. B., Broussard, S. R., Woods, J. A., & Johnson, R. W. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90302.2008 · Cited by 64
Santo, E. D., Sironi, M., Pozzi, P., Gnocchi, P., Isetta, A. M., Delvaux, A., Goldman, M., Marchant, A., & Ghezzi, P. (1995) · NeuroImmunoModulation · doi:10.1159/000096885 · Cited by 51
Peeters, M., Hiele, M. I., Ghoos, Y. F., Huysmans, V., Geboes, K. J., Vantrappen, G. R., & Rutgeerts, P. (1994) · Gut · doi:10.1136/gut.35.10.1404 · Cited by 42
Research works printed but not linked: 2
- Andersohn, 2004, Depressive mood and craving during alcohol withdrawal: association and interaction, German J. Psychiatry, 7, 6
- Spielberger, C.D., Gorsuch, R.L., Lushene, R., Vagg, P.R., Jacobs, G.A., 1983. Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press, Palo Alto. CA.
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Leclercq, S., Matamoros, S., Cani, P. D., Neyrinck, A. M., Jamar, F., Stärkel, P., Windey, K., Tremaroli, V., Bäckhed, F., Verbeke, K., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415174111 · Cited by 972
Self-citationGut–Liver Axis in Alcoholic Liver Disease
Szabo, G. (2015) · Gastroenterology · doi:10.1053/j.gastro.2014.10.042 · Cited by 754
Alcohol and Gut-Derived Inflammation
Bishehsari, F. (2017) · Alcohol research · doi:10.35946/arcr.v38.2.02 · Cited by 380
Microbiota-liver axis in hepatic disease
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Metadata
- Authors
- Leclercq, S., Cani, P. D., Neyrinck, A. M., Stärkel, P., Jamar, F., Mikolajczak, M., Delzenne, N. M., & de Timary, P.
- Affiliations
- UCLouvain (BE)
- Cliniques Universitaires Saint-Luc (BE)
- Corresponding author
- Delzenne, Nathalie M.
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 26
- Issue
- 6
- Pages
- 911-918
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W1705992573
- Semantic Scholar
- 0e7b0f2e0da0290af9f83f26dab1524da03a8e77
- Cited by
- 310
- References
- 61
- Citations by year
- 2026: 17 · 2025: 27 · 2024: 28 · 2023: 20 · 2022: 25 · 2021: 41 · 2020: 30 · 2019: 29 · 2018: 27 · 2017: 20 · 2016: 18 · 2015: 10 · 2014: 12 · 2013: 4 · 2012: 2
- FWCI
- 6.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
- Alcohol and Alcoholism
- Funders
- Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Alcohol Consumption and Health Effects
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- alcoholism, intestinal permeability, leaky gut, lipopolysaccharide, systemic inflammation, gut-brain axis, alcohol craving, depression, anxiety, cytokines, IL-10, TNF-α, interleukin-6, alcohol withdrawal, selective attention, non-cirrhotic patients
- MeSH terms
- Alcoholism, Anxiety, Attention, C-Reactive Protein, Chromium Radioisotopes, Depression, Edetic Acid, Enteritis, Female, Humans, Intestines, Lipopolysaccharides, Male, Middle Aged, Neuropsychological Tests, Obsessive Behavior, Permeability, Reaction Time, Substance Withdrawal Syndrome, Body Mass Index, Cytokines, Diagnostic and Statistical Manual of Mental Disorders
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