Cited by 1,638Substance Abuse Treatment and OutcomesNeurotransmitter Receptor Influence on BehaviorGambling Behavior and Treatments

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Meta‐analysis of cue‐reactivity in addiction research

Carter, Brian L., Tiffany, Stephen T.·1999·Addiction

DOI 10.1046/j.1360-0443.1999.9433273.x

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Abstract

Aims. The cue‐reactivity procedure exposes addicts to a variety of drug‐related stimuli while self‐report of craving and physiological responses are monitored. The present review sought to determine the magnitude and overall pattern of responses typically found in cue‐reactivity research and which, if any, learning‐based model of cue reactivity is best supported by the findings. Design. Meta‐analytical techniques were used to select and evaluate results from 41 cue‐reactivity studies that compared responses of alcoholics, cigarette smokers, cocaine addicts or heroin addicts to drug‐related versus neutral stimuli. Effect sizes were calculated, separately by addict type, for self‐report of craving and physiological responses (heart rate, sweat gland activity and skin temperature). Findings. Across all addict groups, the effect size for craving was +0.92. Alcoholics had a significantly smaller craving effect size (+0.53) compared to other addict groups (+1.18 to +1.29). Relatively smaller effect sizes were found for physiological responses. The general profile of effect sizes across all addict groups was increased heart rate (+0.26) and sweat gland activity (+0.40) and decreased skin temperature (‐0.24) when addicts were presented with drug‐related stimuli. Conclusions. The cuereactivity paradigm can produce a stable profile of significant effects and, therefore, has a number of potential applications for investigating addictive phenomena. The implications of these findings for conditioning‐based models of cue‐reactivity phenomena are discussed.

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Background
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Method
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Result
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“…that cues paired with alcohol or nicotine can induce physiological responses, subjective cravings, and drug seeking behavior (i.e., cue reactivity; Carter & Tiffany 1999; Glautier, Drummond, & Remington, 1994; Hogarth, Mogg, Bradley, Duka, & Dickinson, 2003; Thewissen, Havermans, Geschwind, Van…”
Background
Behavioral momentum of cocaine self-administration: effects of frequency of reinforcement on resistance to extinction
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“Empirically, discrete drug cues and contexts previously associated with drug taking are known to produce craving in substance abusers and can produce relapse to drug seeking in animal drug self-administration procedures (see Carter and Tiffany, 1999; Drummond, 2000; Crombag et al., 2008).”
Background
Craving and illicit heroin use among patients in heroin-assisted treatment
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IMAGING STUDY: Exposure to smoking cues during an emotion recognition task can modulate limbic fMRI activation in cigarette smokers
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“As SCs are supposed to enhance craving during this time period (Carter & Tiffany 1999), the exposure to SCs should have exacerbated craving in our smokers.”
Background
Generalized craving, self-report of arousal, and cue reactivity after brief abstinence
Carter, B. L., Lam, C. Y., Robinson, J. D., Paris, M. M., Waters, A. J., Wetter, D. W., & Cinciripini, P. M. (2009) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntp068 · Cited by 23
“For permissions, please e-mail: journals.permissions@oxfordjournals.org Introduction In numerous laboratory studies, smokers have shown increased craving and physiological arousal when exposed to cigarette stimuli ( Carter & Tiffany, 1999 ).”
BackgroundSelf-citation
Nondaily smokers’ experience of craving on days they do not smoke.
Shiffman, S. S., Dunbar, M. S., Tindle, H. A., & Ferguson, S. G. (2015) · Journal of Abnormal Psychology · doi:10.1037/abn0000063 · Cited by 23
“Laboratory experiments using cue reactivity methods (Carter & Tiffany, 1999) have also documented the role of cueing stimuli in eliciting craving and smoking.”
BackgroundMethod
Constituents of craving in a clinical alcohol sample
Westerberg, V. S. (2000) · Journal of Substance Abuse · doi:10.1016/s0899-3289(01)00051-7 · Cited by 23
Effects of a body image challenge on smoking motivation among college females.
Lopez, E., Drobes, D. J., Thompson, J. K., & Brandon, T. H. (2008) · Health Psychology · doi:10.1037/0278-6133.27.3(suppl.).s243 · Cited by 23
“The most robust indices of cue-reactivity have been self-reported urge to smoke and skin conductance response (Carter & Tiffany, 1999).”
BackgroundResult
Effects of standardised cigarette packaging on craving, motivation to stop and perceptions of cigarettes and packs
Brose, L. S., Chong, C. B., Aspinall, E., Michie, S., & McEwen, A. (2014) · Psychology and Health · doi:10.1080/08870446.2014.896915 · Cited by 22
“Studies on reaction to cues commonly use ‘proximal cues’ that are universally present during smoking (Carter & Tiffany, 1999); however, to date, no study appears to have assessed the effect of branded and standardised packaging as cues on craving or the association of packaging with smokers’…”
Background
Bidirectional Influences Between Parents and Children in Smoking Behavior: A Longitudinal Full-Family Model
Schuck, K., Otten, R., Engels, R. C. M. E., Barker, E. D., & Kleinjan, M. (2012) · Nicotine & Tobacco Research · doi:10.1093/ntr/nts082 · Cited by 24
Sleep rebound attenuates context-dependent behavioural sensitization induced by amphetamine
Calzavara, M. B., Andersen, M. L., Fukushiro, D. F., Lopez, G. B., Abílio, V. C., Tufik, S., & Frussa‐Filho, R. (2008) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2008.04.001 · Cited by 22
“…paired with drug effects on the development of both behavioural sensitization in rodents (Battisti et al., 2000; Cabib, 1993; Chinen et al., 2006; Crombag et al., 2001; Fraioli et al., 1999) and drug craving in humans (Carter and Tiffany, 1999; Childress et al., 1986; Niaura et al., 1988).”
Background
Anxiety and explicit alcohol-related memory in problem drinkers
Zack, M. H., Toneatto, T., & MacLeod, C. M. (2002) · Addictive Behaviors · doi:10.1016/s0306-4603(01)00233-7 · Cited by 22
“These findings demonstrate a consistent effect of cue exposure on addictive motivation and addictive behavior (Carter & Tiffany, 1999).”
Background
Electrophysiological correlates of associative learning in smokers: a higher-order conditioning experiment
Littel, M., & Franken, I. H. A. (2012) · BMC Neuroscience · doi:10.1186/1471-2202-13-8 · Cited by 23
Frontal asymmetry and alcohol cue reactivity: Influence of core personality systems
Mechin, N., Gable, P. A., & Hicks, J. A. (2016) · Psychophysiology · doi:10.1111/psyp.12659 · Cited by 22
Alcohol Craving and Relapse Prediction
Heinz, A., Beck, A., Mir, J., Grüsser, S. M., Grace, A. A., & Wrase, J. (2010) · Frontiers in neuroscience · doi:10.1201/9781420007350-c4 · Cited by 20
Female rats display higher methamphetamine-primed reinstatement and c-Fos immunoreactivity than male rats
Pittenger, S. T., Chou, S., Murawski, N. J., Barrett, S. T., Loh, O., Duque, J. F., Li, M., & Bevins, R. A. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173089 · Cited by 22
Pharmacological evidence of a cholinergic contribution to elevated impulsivity and risky decision-making caused by adding win-paired cues to a rat gambling task
Betts, G., Hynes, T. J., & Winstanley, C. A. (2021) · Journal of Psychopharmacology · doi:10.1177/0269881120972421 · Cited by 25
“Increased sensitivity to reward-predictive cues is fairly well established as a risk factor for substance use disorder (Carter and Tiffany, 1999; Childress et al., 1992; Robinson and Berridge, 1993; Saunders and Robinson, 2010), and is associated with other pro-addiction cognitive traits such as…”
Background
fMRI of the brain’s response to stimuli experimentally paired with alcohol intoxication
Kareken, D. A., Grahame, N. J., Džemidžić, M., Walker, M. J., Lehigh, C. A., & O’Connor, S. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2526-7 · Cited by 23
“Stimuli that become classically conditioned to alcohol by repeated pairing with drinking induce craving (Carter and Tiffany 1999), shift implicit attention toward alcohol-related stimuli (Field and Duka 2002), and promote relapse (Cooney et al.”
Examining the effect of perceived availability on craving for alcohol: A quasi-experimental approach
MacKillop, J. M., & Lisman, S. A. (2007) · Addiction Research & Theory · doi:10.1080/16066350701407104 · Cited by 22
Regulating task-monitoring systems in response to variable reward contingencies and outcomes in cocaine addicts
Morie, K. P., Sanctis, P. D., Garavan, H., & Foxe, J. J. (2016) · Psychopharmacology · doi:10.1007/s00213-015-4191-8 · Cited by 22
Craving for sweet carbohydrate and fat‐rich foods – possible triggers and impact on nutritional intake
Christensen, L. (2007) · Nutrition Bulletin · doi:10.1111/j.1467-3010.2007.00615.x · Cited by 22
The observing-response procedure: A novel method to study drug-associated conditioned reinforcement.
Shahan, T. A. (2002) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.10.1.3 · Cited by 22
Positive and instructive anti-smoking messages speak to older smokers: a focus group study
Cataldo, J., Hunter, M. M., Petersen, A., & Sheon, N. (2015) · Tobacco Induced Diseases · doi:10.1186/s12971-015-0027-x · Cited by 21
“The results of our study support the premise that when anti-smoking messages include smoking-related cues in order to illustrate the negative consequences of smoking they can trigger cravings to smoke and may play a role in relapse [34,35].”
Result
Extinction of gambling cue-reactivity: A pilot study in a problem gambling treatment setting
Riley, B. J., Baigent, M. F., Harris, S., Larsen, A., Nye, T., & Battersby, M. (2018) · Journal of Addiction and Recovery · doi:10.33582/2637-4528/1010 · Cited by 21
“A conditioning model of addiction has been applied widely to substance use disorders [3].”
Method
Virtual Environments for Substance Abuse Assessment and Treatment
Bordnick, P. S., & Washburn, M. (2019) · Virtual reality technologies for health and clinical applications · doi:10.1007/978-1-4939-9482-3_6 · Cited by 26
Memory biases in alcohol use disorder: enhanced memory for contexts associated with alcohol prospectively predicts alcohol use outcomes
Goldfarb, E. V., Fogelman, N., & Sinha, R. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0650-y · Cited by 21
“Alcohol-related items are highly affectively salient for heavy drinkers [29] and patients with AUD [30], and limited evidence indicates that these patients have better memory for alcohol-related items after a short delay [20, 21] (but see ref.”
Background
Developing a theoretical marketing framework to analyse JUUL and compatible e-cigarette product promotion on Instagram
Kostygina, G., Tran, H., Czaplicki, L., Perks, S. N., Vallone, D., Emery, S., & Hair, E. C. (2022) · Tobacco Control · doi:10.1136/tobaccocontrol-2021-057120 · Cited by 23
Emotional distress and pain catastrophizing predict cue-elicited opioid craving among chronic pain patients on long-term opioid therapy
Parisi, A. B., Landicho, H. L., Hudak, J., Leknes, S., Froeliger, B., & Garland, E. L. (2022) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2022.109361 · Cited by 23
Food Addiction: a Deep Dive into ‘Loss of Control’ and ‘Craving’
Whatnall, M. C., Skinner, J. A., Leary, M., & Burrows, T. L. (2022) · Current Addiction Reports · doi:10.1007/s40429-022-00431-w · Cited by 26
A Comparison of Gambling Behavior, Problem Gambling Indices, and Reasons for Gambling Among Smokers and Nonsmokers Who Gamble: Evidence from a Provincial Gambling Prevalence Study
McGrath, D. S., Barrett, S. P., Stewart, S. H., & McGrath, P. R. (2012) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntr294 · Cited by 21
‘Cue reward salience’ predicts craving in response to alcohol cues
Kambouropoulos, N., & Staiger, P. K. (2008) · Personality and Individual Differences · doi:10.1016/j.paid.2008.08.023 · Cited by 21
Real‐Time Craving Differences between Black and White Smokers
Carter, B. L., Paris, M. M., Lam, C. Y., Robinson, J. D., Traylor, A. C., Waters, A. J., Wetter, D. W., & Cinciripini, P. M. (2010) · American Journal on Addictions · doi:10.1111/j.1521-0391.2009.00020.x · Cited by 25
Self-citation
Effectiveness of Ceftriaxone Treatment in Preventing Relapse-like Drinking Behavior Following Long-term Ethanol Dependence in P Rats
Sari, Y. (2014) · Journal of Addiction Research & Therapy · doi:10.4172/2155-6105.1000183 · Cited by 21
Differences in ERP topographies during color matching of smoking-related and neutral pictures in smokers and non-smokers
Fehr, T., Wiedenmann, P., & Herrmann, M. (2007) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2007.05.006 · Cited by 21
“Numerous studies have shown that behavioral and/or environmental cueing, using specific aspects of drug consumption, can produce changes in the feeling of craving and physiological parameters, such as skin conductance, heart rate and EEGrelated parameters (Carter and Tiffany, 1999).”
Background
The strength of aversive and appetitive associations and maladaptive behaviors
Itzhak, Y., Perez‐Lanza, D., & Liddie, S. (2014) · IUBMB Life · doi:10.1002/iub.1310 · Cited by 22
Alcohol consumption as a predictor of reactivity to smoking and stress cues presented in the natural environment of smokers
Tomko, R. L., Saladin, M. E., McClure, E. A., Squeglia, L. M., Carpenter, M. J., Tiffany, S. T., Baker, N. L., & Gray, K. M. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4472-x · Cited by 21
Self-citation
Callous-Unemotional Traits Modulate Brain Drug Craving Response in High-Risk Young Offenders
Vincent, G. M., Cope, L. M., King, J. A., Nyalakanti, P. K., & Kiehl, K. A. (2017) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-017-0364-8 · Cited by 26
“…abuse history increases the likelihood of obtaining a higher prevalence of psychopathic traits due to their relatively greater proclivity towards cocaine abuse (Smith and Newman 1990; Walsh et al. 2007), and b) stimulants and cocaine elicit a strong craving response (Carter and Tiffany 1999).”

Authors: Carter, B. L., & Tiffany, S. T.
Affiliations: Purdue University West Lafayette (US)
Venue: Addiction
Publisher: Wiley
Published: 1999-03
Volume: 94
Issue: 3
Pages: 327-340
ISSN: 0965-2140 (ISSN-L)
1360-0443
DOI: 10.1046/j.1360-0443.1999.9433273.x
OpenAlex: W1988132969
Cited by: 1,638
References: 0
Citations by year: 2026: 41 · 2025: 50 · 2024: 38 · 2023: 59 · 2022: 53 · 2021: 73 · 2020: 145 · 2019: 61 · 2018: 59 · 2017: 58 · 2016: 83 · 2015: 85 · 2014: 90 · 2013: 86 · 2012: 97
FWCI: 16.64
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 1159 d)
Locations: Addiction (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (2r01da004050-09a2)
National Institute on Drug Abuse (R01DA04050)
Topics: Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Social Sciences › Psychology › Clinical Psychology › Gambling Behavior and Treatments
Keywords: cue reactivity, drug craving, alcoholism, cigarette smoking, cocaine dependence, heroin addiction, physiological responses, heart rate, sweat gland activity, skin temperature
MeSH terms: Adult, Cues, Female, Heart Rate, Humans, Male, Research, Skin Temperature, Sweating, Randomized Controlled Trials as Topic, Substance-Related Disorders

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Meta‐analysis of cue‐reactivity in addiction research

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