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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Method
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Background
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Smoking Abstinence and Neurocognition: Implications for Cessation and Relapse
McClernon, F. J., Addicott, M. A., & Sweitzer, M. M. (2015) · Current topics in behavioral neurosciences · doi:10.1007/978-3-319-13665-3_8 · Cited by 39
“Exposure to smoking-related stimuli increases self-reported craving to smoke (Carter and Tiffany 1999) and has long been theorized to precipitate relapse among smokers trying to quit (Shiffman et al.”
Background
Attenuation of brain response to heroin correlates with the reinstatement of heroin-seeking in rats by fMRI
Luo, F. R., Xi, Z., Wu, G., Liu, C., Gardner, E. L., & Li, S. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.03.017 · Cited by 38
Reactivity to smoking cues in adolescent cigarette smokers
Upadhyaya, H. P., Drobes, D. J., & Thomas, S. E. (2004) · Addictive Behaviors · doi:10.1016/j.addbeh.2004.02.040 · Cited by 38
“Adult smoking-cue-reactivity studies have utilized various paradigms to examine subjective and physiological reactions to salient smoking-related stimuli (see review by Carter & Tiffany, 1999).”
Background
Cue-induced craving and physiological reactions in recently and long-abstinent heroin-dependent patients
Zhao, M., Fan, C., Du, J., Jiang, H., Chen, H., & Sun, H. (2012) · Addictive Behaviors · doi:10.1016/j.addbeh.2011.11.030 · Cited by 37
“Drugrelated cue-induced response is presumed to consist of physiological and/or subjective reactions (Carter & Tiffany, 1999; Robbins, Ehrman, Childress, & O'Brien, 1997).”
Background
A reward and incentive-sensitization perspective on compulsive use of social networking sites – Wanting but not liking predicts checking frequency and problematic use behavior
Ihssen, N., & Wadsley, M. G. (2020) · Addictive Behaviors · doi:10.1016/j.addbeh.2020.106808 · Cited by 42
Cigarette smoking, illicit drug use, and routes of administration among heroin and cocaine users
Harrell, P. T., Trenz, R. C., Scherer, M., Pacek, L. R., & Latimer, W. W. (2012) · Addictive Behaviors · doi:10.1016/j.addbeh.2012.01.011 · Cited by 36
“Cues for drug intake are associated with increased craving among substance users (Carter & Tiffany, 1999) and stimulus generalization predisposes individuals to relapse (Siegel & Ramos, 2002).”
Background
Accumbens D2-MSN hyperactivity drives antipsychotic-induced behavioral supersensitivity
Kruyer, A., Parrilla-Carrero, J., Powell, C., Brandt, L., Gutwinski, S., Angelis, A., Chalhoub, R., Jhou, T. C., Kalivas, P. W., & Amato, D. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01235-6 · Cited by 37
“6D, S9C, D), a widely accepted model of cue reactivity [68] linked to drug relapse in human patients [69].”
Background
Tetrodotoxin alleviates acute heroin withdrawal syndrome: A multicentre, randomized, double-blind, placebo-controlled study
Song, H., li, J., Lu, C., Kang, L., Xie, L., Zhang, Y., Zhou, X., & Zhong, S. (2011) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2011.05539.x · Cited by 36
Reward expectancy promotes generalized increases in attentional bias for rewarding stimuli
Jones, A., Hogarth, L., Christiansen, P., Rose, A. K., Martinović, J., & Field, M. (2012) · Quarterly Journal of Experimental Psychology · doi:10.1080/17470218.2012.686513 · Cited by 36
Evidence for greater cue reactivity among low-dependent vs. high-dependent smokers
Watson, N. L., Carpenter, M. J., Saladin, M. E., Gray, K. M., & Upadhyaya, H. P. (2010) · Addictive Behaviors · doi:10.1016/j.addbeh.2010.02.010 · Cited by 36
“Cue-specific craving is most commonly measured with various selfreport indices of craving (Carter and Tiffany, 1999; Ferguson and Shiffman, 2009) and is commonly viewed as a form of stimulus control (i.e., the ability of environmental cues to elicit craving) that develops following repeated…”
Background
Pain or nociception? Subjective experience mediates the effects of acute noxious heat on autonomic responses - corrected and republished
Mischkowski, D., Palacios‐Barrios, E. E., Banker, L., Dildine, T. C., & Atlas, L. Y. (2019) · Pain · doi:10.1097/j.pain.0000000000001573 · Cited by 40
Reward‐related regions form a preferentially coupled system at rest
Huckins, J. F., Adeyemo, B., Miezin, F. M., Power, J. D., Gordon, E. M., Laumann, T. O., Heatherton, T. F., Petersen, S. E., & Kelley, W. M. (2018) · Human Brain Mapping · doi:10.1002/hbm.24377 · Cited by 34
Smoking cue reactivity in schizophrenia: Effects of a nicotinic receptor antagonist
Fonder, M. A., Sacco, K. A., Termine, A., Boland, B. S., Seyal, A. A., Dudas, M. M., Vessicchio, J. C., & George, T. P. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.027 · Cited by 36
Do People Serve as Cues to Smoke?
Conklin, C. A., Salkeld, R. P., Perkins, K. A., & Robin, N. (2013) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntt104 · Cited by 36
“…with significant changes in subjective (e.g., self-reported craving) and physiological (e.g., heart rate [HR]) indices of responding when exposed to cues most proximal to drug administration (e.g., heroin needles, lit cigarettes, drug use paraphernalia; see Carter & Tiffany, 1999, for review).”
Background
Pavlovian conditioning of an approach bias in low-dependent smokers
Thewissen, R., Havermans, R. C., Geschwind, N., van den Hout, M., & Jansen, A. T. M. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0819-7 · Cited by 35
“Cue reactivity comprises subjective responses (e.g. craving), psychophysiological responses (e.g. changes in heart rate and skin conductance level) and behavioural responses (e.g. drug-seeking behaviour; Carter and Tiffany 1999; Drummond 2000; Drummond et al. 2000).”
Background
Individual and Combined Effects of Multiple High-Risk Triggers on Postcessation Smoking Urge and Lapse
Lam, C. Y., Businelle, M. S., Aigner, C. J., McClure, J. B., Cofta-Woerpel, L. M., Cinciripini, P. M., & Wetter, D. W. (2013) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntt190 · Cited by 36
“The presence of others smoking exposes smokers to smoking-related cues, which has been shown to increase craving (Carter & Tiffany, 1999) and may signal the availability of cigarettes and/or acceptability of smoking.”
Background
Facial reactions to smoking cues relate to ambivalence about smoking.
Griffin, K. M., & Sayette, M. A. (2008) · Psychology of Addictive Behaviors · doi:10.1037/0893-164x.22.4.551 · Cited by 36
“Keywords: ambivalence, smoking cue reactivity, facial expression, FACS An extensive literature reveals that smokers show increased reactivity to laboratory smoking cues (see Carter & Tiffany, 1999).”
Subjective and physiological responses to smoking cues in smokers with schizophrenia
Tidey, J. W., Rohsenow, D. J., Kaplan, G. B., & Swift, R. M. (2005) · Nicotine & Tobacco Research · doi:10.1080/14622200500125724 · Cited by 35
Impact on smoking of England's 2012 partial tobacco point of sale display ban: a repeated cross-sectional national study
Kuipers, M. A. G., Beard, E., Hitchman, S. C., Brown, J., Stronks, K., Kunst, A. E., McNeill, A. D., & West, R. (2016) · Tobacco Control · doi:10.1136/tobaccocontrol-2015-052724 · Cited by 36
Adolescents' behavioral and neural responses to e‐cigarette advertising
Chen, Y., Fowler, C. H., Papa, V. B., Lepping, R. J., Brucks, M. G., Fox, A. T., & Martin, L. E. (2017) · Addiction Biology · doi:10.1111/adb.12510 · Cited by 37
“…a smoker sees cigarette images); the individual’s responses to the cues may then be compared with their responses to neutral cues (e.g. non-smoking images such as a pack of pencils), or their peak self-reported responses to the cues may be measured (Carter & Tiffany 1999; Sayette & Tiffany 2013).”
Background
Cue-induced reinstatement of alcohol-seeking behavior is associated with increased CaMKII T286 phosphorylation in the reward pathway of mice
Salling, M. C., Hodge, C. J., Psilos, K. E., Eastman, V. R., Faccidomo, S., & Hodge, C. W. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.10.011 · Cited by 29
Combined Smoking Cues Enhance Reactivity and Predict Immediate Subsequent Smoking
Conklin, C. A., McClernon, F. J., Vella, E. J., Joyce, C. J., Salkeld, R. P., Parzynski, C. S., & Bennett, L. (2018) · Nicotine & Tobacco Research · doi:10.1093/ntr/nty009 · Cited by 35
An Acute Psychosocial Stressor Does Not Potentiate Alcohol Cue Reactivity in Non-Treatment-Seeking Alcoholics
Thomas, S. E., Randall, P. K., Brady, K. T., See, R. E., & Drobes, D. J. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01363.x · Cited by 34
“Because others have found that self-reported craving induced by drug cues can clearly exceed this (Carter and Tiffany, 1999; MacKillop, 2006), ceiling effects in these measures were unlikely.”
Background
Attentional bias is associated with incentive-related physiological and subjective measures.
Waters, A. J., Carter, B. L., Robinson, J. D., Wetter, D. W., Lam, C. Y., Kerst, W. F., & Cinciripini, P. M. (2009) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0016658 · Cited by 37
“Responses to drug cues can be assessed from self-report and from physiological responses (e.g., Carter & Tiffany, 1999).”
BackgroundSelf-citation
Urge to Gamble in a Simulated Gambling Environment
Kushner, M. G., Thurus, P., Sletten, S., Frye, B., Abrams, K. B., Adson, D. E., Demark, J. V., Maurer, E. W., & Donahue, C. (2007) · Journal of Gambling Studies · doi:10.1007/s10899-007-9083-3 · Cited by 35
“These early observations stimulated enough research for Carter and Tiffany (1999) to review the literature related to cue reactivity among problem users of alcohol, cigarettes, cocaine and heroin.”
Background
Marijuana craving trajectories in an adolescent marijuana cessation pharmacotherapy trial
Roten, A. T., Baker, N. L., & Gray, K. M. (2012) · Addictive Behaviors · doi:10.1016/j.addbeh.2012.11.003 · Cited by 35
“…a paradigm that measures cue-induced craving, a cue (a picture, an imagery script, or a drug-related object for example) is introduced to the participant and subsequent craving is measured by self-reports and/or possible physiological measures of craving (Carter & Tiffany, 1999; Gray et al., 2008).”
Method
Pharmacological enhancement of drug cue extinction learning: translational challenges
Kantak, K. M., & Dhonnchadha, B. Á. N. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05899.x · Cited by 35
Effects of cortisol administration on craving in heroin addicts
Walter, M., Bentz, D., Schicktanz, N., Milnik, A., Aerni, A., Gerhards, C., Schwegler, K., Vogel, M., Blum, J., Schmid, O., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.101 · Cited by 36
Cue Exposure Therapy for Alcohol Use Disorders: What Can Be Learned from Exposure Therapy for Anxiety Disorders?
Byrne, S., Haber, P., Baillie, A., Giannopolous, V., & Morley, K. C. (2019) · Substance Use & Misuse · doi:10.1080/10826084.2019.1618328 · Cited by 37
“There is evidence that CET to alcohol cues reduces cue reactivity (Carter & Tiffany, 1999; Conklin & Tiffany, 2002).”
Background

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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