Incubation of neural alcohol cue reactivity after withdrawal and its blockade by naltrexone.
alcohol addiction
cue reactivity
fMRI
naltrexone
relapse
Journal
Addiction biology
ISSN: 1369-1600
Titre abrégé: Addict Biol
Pays: United States
ID NLM: 9604935
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
28
09
2018
revised:
15
12
2018
accepted:
08
01
2019
pubmed:
13
2
2019
medline:
11
2
2021
entrez:
13
2
2019
Statut:
ppublish
Résumé
During the first weeks of abstinence, alcohol craving in patients may increase or "incubate." We hypothesize that Naltrexone (NTX) blocks this incubation effect. Here, we compared NTX effects on neural alcohol cue reactivity (CR) over the first weeks of abstinence and on long-term clinical outcomes to standard treatment. Male alcohol-dependent patients (n = 55) and healthy controls (n = 35) were enrolled. Participants underwent baseline psychometric testing and functional magnetic resonance imaging (fMRI) assessment of mesolimbic alcohol CR. Patients participated in a standard treatment program with the option of adjuvant NTX. They received another scan after 2 weeks of treatment. We found higher CR in several brain regions in patients versus healthy controls. CR significantly increased over 2 weeks in the standard treatment group (n = 13) but not in the NTX group (n = 22). NTX significantly attenuated CR in the left putamen and reduced relapse risk to heavy drinking within 3 months of treatment. Additionally, increased CR in the left putamen and its course over time predicted both NTX response and relapse risk. Carrier status for the functional OPRM1 variant rs1799971:A > G was considered but had no effect on NTX efficacy. In conclusion, NTX was most effective in patients with high CR in the left putamen. While the results from our naturalistic study await further confirmation from prospective randomized trials, they support a potential role of neural CR as a biomarker in the development of precision medicine approaches with NTX.
Substances chimiques
Narcotic Antagonists
0
Naltrexone
5S6W795CQM
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12717Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : SFB636
Pays : International
Organisme : Horizon 2020 Framework Programme
ID : 668863-SyBil-AA
Pays : International
Organisme : ERA-Net NEURON program
ID : FKZ 01EW1112-TRANSALC
Pays : International
Organisme : European Union's Horizon 2020 research and innovation program
ID : 668863-SyBil-AA
Pays : International
Informations de copyright
© 2019 Society for the Study of Addiction.
Références
World Health Organization (2018) Global Status Report on Alcohol and Health.
Jonas DE, Amick HR, Feltner C, Bobashev G, Thomas K, Wines R, Kim MM, Shanahan E, Gass CE, Rowe CJ, Garbutt JC (2014) In: Pharmacotherapy for Adults With Alcohol-Use Disorders in Outpatient Settings: Rockville (MD).
Heilig M, Sommer WH, Spanagel R. The need for treatment responsive translational biomarkers in alcoholism research. Curr Top Behav Neurosci. 2016;28:151-171.
Mann K, Roos CR, Hoffmann S, Nakovics H, Leménager T, Heinz A. Witkiewitz K (2018) precision medicine in alcohol dependence: a controlled trial testing pharmacotherapy response among reward and relief drinking phenotypes. Neuropsychopharmacology. 2018;43(4):891-899.
Hansson AC, Gründer G, Hirth N, Noori HR, Spanagel R, Sommer WH. Dopamine and Opioid Systems Adaptation in Alcoholism Revisited: Convergent Evidence from Positron Emission Tomography and Postmortem Studies. Neuroscience and Biobehavioral Reviews InPress; 2018.
Hendershot CS, Wardell JD, Samokhvalov AV, Rehm J. Effects of naltrexone on alcohol self-administration and craving: meta-analysis of human laboratory studies. Addict Biol. 2017;22(6):1515-1527.
Schacht JP, Anton RF, Voronin KE, et al. Interacting effects of naltrexone and OPRM1 and DAT1 variation on the neural response to alcohol cues. Neuropsychopharmacology: official publication of the American college of Neuropsychopharmacology. 2013;38(3):414-422.
Vollstadt-Klein S, Loeber S, Richter A, et al. Validating incentive salience with functional magnetic resonance imaging: association between mesolimbic cue reactivity and attentional bias in alcohol-dependent patients. Addict Biol. 2012;17(4):807-816.
Yalachkov Y, Kaiser J, Naumer MJ. Functional neuroimaging studies in addiction: multisensory drug stimuli and neural cue reactivity. Neurosci Biobehav Rev. 2012;36(2):825-835.
Mann K, Vollstadt-Klein S, Reinhard I, et al. Predicting naltrexone response in alcohol-dependent patients: the contribution of functional magnetic resonance imaging. Alcohol Clin Exp Res. 2014;38(11):2754-2762.
Reinhard I, Lemenager T, Fauth-Buhler M, et al. A comparison of region-of-interest measures for extracting whole brain data using survival analysis in alcoholism as an example. J Neurosci Methods. 2015;242:58-64.
Schacht JP, Anton RF, Myrick H. Functional neuroimaging studies of alcohol cue reactivity: a quantitative meta-analysis and systematic review. Addict Biol. 2013b;18(1):121-133.
Schacht JP, Randall PK, Latham PK, et al. Predictors of naltrexone response in a randomized trial: reward-related brain activation, OPRM1 genotype, and smoking status. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology. 2017;42(13):2640-2653.
Lukas SE, Lowen SB, Lindsey KP, et al. Extended-release naltrexone (XR-NTX) attenuates brain responses to alcohol cues in alcohol-dependent volunteers: a bold FMRI study. Neuroimage. 2013;78:176-185.
Grimm JW, Hope BT, Wise RA, Shaham Y. Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature. 2001;412(6843):141-142.
Pickens CL, Airavaara M, Theberge F, Fanous S, Hope BT, Shaham Y. Neurobiology of the incubation of drug craving. Trends Neurosci. 2011;34(8):411-420.
Bienkowski P, Rogowski A, Korkosz A, et al. Time-dependent changes in alcohol-seeking behaviour during abstinence. Eur Neuropsychopharmacol. 2004;14(5):355-360.
Li P, Wu P, Xin X, et al. Incubation of alcohol craving during abstinence in patients with alcohol dependence. Addict Biol. 2015;20(3):513-522.
Dong Y, Taylor JR, Wolf ME, Shaham Y. Circuit and synaptic plasticity mechanisms of drug relapse. J Neurosci Off J Soc Neurosci. 2017;37(45):10867-10876.
Luis C, Cannella N, Spanagel R, Kohr G. Persistent strengthening of the prefrontal cortex - nucleus accumbens pathway during incubation of cocaine-seeking behavior. Neurobiol Learn Mem. 2017;138:281-290.
Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961;4(6):561-571.
Fagerstrom KO, Schneider NG. Measuring nicotine dependence: a review of the Fagerstrom tolerance questionnaire. J Behav Med. 1989;12(2):159-182.
Kivlahan DR, Sher KJ, Donovan DM. The alcohol dependence scale: a validation study among inpatient alcoholics. J Stud Alcohol. 1989;50(2):170-175.
Saunders JB, Aasland OG, Babor TF, De la Fuente JR, Grant M. Development of the alcohol use disorders identification test (AUDIT): WHO collaborative project on early detection of persons with harmful alcohol consumption-II. Addiction. 1993;88(6):791-804.
Mann K. Die OCDS-G: Psychometrische Kennwerte der deutschen Version der Obsessive Compulsive Drinking Scale. Sucht. 2000;46:10.
Sullivan JT, Sykora K, Schneiderman J, Naranjo CA, Sellers EM. Assessment of alcohol withdrawal: the revised clinical institute withdrawal assessment for alcohol scale (CIWA-Ar). Br J Addict. 1989;84(11):1353-1357.
Tonigan JS, Miller WR, Brown JM. The reliability of form 90: an instrument for assessing alcohol treatment outcome. J Stud Alcohol. 1997;58(4):358-364.
Loeber S, Kiefer F, Wagner F, Mann K, Croissant B. Treatment outcome after inpatient alcohol withdrawal: impact of motivational interventions: a comparative study. Nervenarzt. 2009;80(9):1085-1092.
Bach P, Vollstädt-Klein S, Kirsch M, et al. Increased mesolimbic cue-reactivity in carriers of the mu-opioid-receptor gene OPRM1 A118G polymorphism predicts drinking outcome: a functional imaging study in alcohol dependent subjects. Eur Neuropsychopharmacol. 2015;25(8):1128-1135.
Jorde A, Bach P, Witt SH, et al. Genetic variation in the atrial natriuretic peptide transcription factor GATA4 modulates amygdala responsiveness in alcohol dependence. Biol Psychiatry. 2014;75(10):790-797.
Kiefer F, Witt SH, Frank J, et al. Involvement of the atrial natriuretic peptide transcription factor GATA4 in alcohol dependence, relapse risk and treatment response to acamprosate. Pharmacogenomics J. 2011;11(5):368-374.
Anton RF, Oroszi G, O'Malley S, et al. An evaluation of mu-opioid receptor (OPRM1) as a predictor of naltrexone response in the treatment of alcohol dependence: results from the combined pharmacotherapies and behavioral interventions for alcohol dependence (COMBINE) study. Arch Gen Psychiatry. 2008;65(2):135-144.
Chamorro AJ, Marcos M, Miron-Canelo JA, Pastor I, Gonzalez-Sarmiento R, Laso FJ. Association of micro-opioid receptor (OPRM1) gene polymorphism with response to naltrexone in alcohol dependence: a systematic review and meta-analysis. Addict Biol. 2012;17(3):505-512.
Oslin DW, Berrettini W, Kranzler HR, et al. A functional polymorphism of the mu-opioid receptor gene is associated with naltrexone response in alcohol-dependent patients. Neuropsychopharmacology. 2003;28(8):1546-1552.
Ramchandani VA, Umhau J, Pavon FJ, et al. A genetic determinant of the striatal dopamine response to alcohol in men. Mol Psychiatry. 2011;16(8):809-817.
Bennett CM, Wolford GL, Miller MB. The principled control of false positives in neuroimaging. Soc Cogn Affect Neurosci. 2009;4(4):417-422.
Noori HR, Cosa Linan A, Spanagel R. Largely overlapping neuronal substrates of reactivity to drug, gambling, food and sexual cues: a comprehensive meta-analysis. Eur Neuropsychopharmacol. 2016;26(9):1419-1430.
Sjoerds Z, de Wit S, van den Brink W, et al. Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients. Transl Psychiatry. 2013;3(12):e337.
Altman DG, Andersen PK. Calculating the number needed to treat for trials where the outcome is time to an event. BMJ (Clinical Research Ed). 1999;319(7223):1492-1495.
Vollstadt-Klein S, Loeber S, Kirsch M, et al. Effects of cue-exposure treatment on neural cue reactivity in alcohol dependence: a randomized trial. Biol Psychiatry. 2011;69(11):1060-1066.
Koob GF, Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science. 1997;278(5335):52-58.
Bujarski S, Ray LA. Subjective response to alcohol and associated craving in heavy drinkers vs. alcohol dependents: an examination of Koob's allostatic model in humans. Drug Alcohol Depend. 2014;140:161-167.
Bujarski S, Hutchison KE, Prause N, Ray LA. Functional significance of subjective response to alcohol across levels of alcohol exposure. Addict Biol. 2017;22(1):235-245.
Sinha R. How does stress lead to risk of alcohol relapse? Alcohol Res. 2012;34(4):432-440.
Smith KS, Tindell AJ, Aldridge JW, Berridge KC. Ventral pallidum roles in reward and motivation. Behav Brain Res. 2009;196(2):155-167.
Grusser SM, Wrase J, Klein S, et al. Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics. Psychopharmacology (Berl). 2004;175(3):296-302.
Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci. 2005;8(11):1481-1489.
Kranzler HR, Stephenson JJ, Montejano L, Wang S, Gastfriend DR. Persistence with oral naltrexone for alcohol treatment: implications for health-care utilization. Addiction. 2008;103(11):1801-1808.
Swift R, Oslin DW, Alexander M, Forman R. Adherence monitoring in naltrexone pharmacotherapy trials: a systematic review. J Stud Alcohol Drugs. 2011;72(6):1012-1018.
Magill M, Ray LA. Cognitive-behavioral treatment with adult alcohol and illicit drug users: a meta-analysis of randomized controlled trials. J Stud Alcohol Drugs. 2009;70(4):516-527.
Bernardi RE, Zohsel K, Hirth N, et al. A gene-by-sex interaction for nicotine reward: evidence from humanized mice and epidemiology. Transl Psychiatry. 2016;6(7):e861.