Experimental and Clinical Psychopharmacology 2015, Vol. 23, No. 2, 90 –96
© 2015 American Psychological Association 1064-1297/15/$12.00 http://dx.doi.org/10.1037/a0038826
Examining the Relationship Between Cue-Induced Craving and Actual Smoking Cynthia A. Conklin
Elizabeth J. Vella
University of Pittsburgh
University of Southern Maine
Christopher J. Joyce, Ronald P. Salkeld, Kenneth A. Perkins, and Craig S. Parzynski This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
University of Pittsburgh Smoking cue-reactivity studies have consistently demonstrated heightened self-report craving, as well as moderate autonomic reactivity, among smokers exposed to salient drug-related cues. However, significantly fewer studies have examined whether exposure to smoking cues affects smokers’ actual smoking, or examined the predictive relationship between cue-induced craving and smoking behavior. Using our well-tested pictorial cues in a cue-reactivity paradigm, we investigated the impact of smoking-related cues relative to neutral cues on subjective craving and smoking behavior (assessed via CReSS; Plowshare Technologies, Baltimore, MD) measures of latency to smoke, puff volume, and number of puffs). Further, we examined the predictive value of cue-induced craving on subsequent smoking behavior. Sixty nondeprived daily smokers completed 2 experimental sessions involving exposure to either smokingrelated or neutral pictorial cues. Following initial exposure to cues, smokers rated their craving and were then allowed to smoke freely if they chose to during a subsequent 6-min cue exposure period. Result showed that exposure to smoking cues relative to neutral predicted significantly greater craving and increases in smoking behavior. Likewise, the magnitude of the difference in cue-induced craving when exposed to smoking cues relative to neutral cues (i.e., the cue-reactivity effect) was highly predictive of shorter latency to smoke, as well as increased number of puffs and puff volume. Keywords: smoking, cue reactivity, cue-induced craving, smoking behavior
several theories anticipate a tight relationship between the two. For example, the dual-affect model purports that as urge networks become more fully activated, measures of craving and physiological responding should become more strongly intercorrelated (e.g., Baker, Morse, & Sherman, 1986). Moreover, other theories suggest that stimuli and/or situations that evoke strong craving should also evoke coherent physiological increases (Tiffany, 1990). However, given the complexity of both cue-induced craving and physiological reactivity, a direct correlation between these measures may be too simplistic to expect. Compared with the wealth of studies investigating subjective and physiological responses to smoking cues, very few studies have examined if smoking-related cues affect actual smoking behavior. In theory, if a smoker is craving and has access to cigarettes in an environment permissive of smoking, the expectation is that he or she, barring any attempt to quit, will choose to smoke (Tiffany, 1990). Indeed, this relationship holds well among nonquitting smokers experiencing abstinence-induced craving brought on by intermittent nicotine deprivation (Schuh & Stitzer, 1995; Zacny & Stitzer, 1985). However, cue-induced craving appears to behave differently and seemingly more independently of nicotine. For example, nicotine replacement studies have shown that NRT directly reduces abstinence-induced craving but fails to attenuate cue-induced craving (Hutchison et al., 1999; Tiffany, Cox, & Elash, 2000; Waters et al., 2004). Likewise, even in sated smokers, exposure to smoking-related cues evokes strong increases in self-reported craving (e.g., Carter et al., 2006). So, although an autonomic response to cues may not
It is well established that smokers react with robust increases in self-reported craving, and moderate changes in autonomic reactivity (e.g., heart rate, skin conductance, blood pressure) when exposed to smoking-related stimuli (Carter & Tiffany, 1999). Although significant changes in these various indices of responding have been seen across cue studies, correlations between measures are consistently very weak or absent. See (Carter & Tiffany, 1999, for review). The lack of coherence between self-report and autonomic responses to drug-related cues is somewhat surprising, as
This article was published Online First March 2, 2015. Cynthia A. Conklin, Department of Psychiatry, University of Pittsburgh; Elizabeth J. Vella, Department of Psychology, University of Southern Maine; Christopher J. Joyce, Ronald P. Salkeld, Kenneth A. Perkins, and Craig S. Parzynski, Department of Psychiatry, University of Pittsburgh. Craig S. Parzynski is now at Yale University, Department of Internal Medicine. This research was supported by National Institute on Drug Abuse Grants DA023646 and DA027508. The funding source had no role in the research other than financial support. We have contributed significantly to the article and have read and approved the final manuscript. We do not have a conflict of interest that may inappropriately impact or influence the research or interpretation of the findings. We thank Bethany Preston for her assistance with this research. Correspondence concerning this article should be addressed to Cynthia A. Conklin, 3811 O’Hara Street, Room 1620, Pittsburgh, PA 15213. E-mail: [email protected] 90
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CRAVING AND SMOKING BEHAVIOR
strongly track how an individual reports thinking and feeling, one might expect a person’s self-reported desire and intention to immediately engage in a reinforcing appetitive behavior to better map on to how they subsequently behave. Specifically, if a nonquitting smoker reports heightened craving after seeing salient smoking stimuli and is immediately offered a chance to smoke, a reasonable assumption is that the majority of the time, smoking will follow. In fact, the assumption of a predictive relationship between cue-induced craving and subsequent smoking is commonly held, yet review of the cuereactivity smoking literature finds limited empirical evidence to support it. This may be due in part to challenges noted by several researchers that drug-use behaviors are complex and finding a single smoking behavior that adequately functions as an index of smoking motivation or likelihood of use may be difficult or unlikely (e.g., Carter & Tiffany, 1999; Glautier & Tiffany, 1995; Tiffany, 1990), as well as the fact that behavioral reactivity is more difficult to assess. Specifically, examining the impact of cues on smoking requires lengthier studies, given that once a participant has smoked, all manipulation thereafter are confounded by smoking, necessitating individual sessions for different cue manipulations. There is some evidence that the majority of lapses and relapses to smoking during quit attempts occur in the presence self-reported cue exposure and/or cue-induced craving (Shiffman, Paty, Gnys, Kassel, & Hickox, 1996). And, a few experimental studies directly examining smoking behavior in response to smoking cue exposure in the lab have been conducted and shown promising but inconclusive support for this relationship. In perhaps the first study, Herman (1974) found that when confronted with high versus low salience smoking cues (a light directed on participants ashtrays and cigarettes vs. no light on these stimuli), light smokers reported greater craving, were quicker to initiate smoking, and smoked more. Similarly, Droungas et al. (1995) found that smokers who were told they would be able to smoke in session, responded to smoking cues relative to nonsmoking cues with greater craving, withdrawal, and quicker latency to smoke. Another study involving the manipulation of both affect and smoking cues (Payne et al., 1991) found that smokers sitting in a room containing multiple smoking-related cues lit up quicker and increased their puff duration compared with those in a room devoid of any visible smoking stimuli. On balance, these studies demonstrate a clear link between exposure to smoking-related cues and subsequent smoking behavior. However, none of these studies examined the predictive relationship between cue-induced craving and subsequent smoking behavior. More recent cue-reactivity studies examining craving and behavior have been conducted by Shiffman et al. (2013a, 2013b). The first study, examining differences in cue reactivity and behavioral responding in intermittent and daily smokers, found that although craving intensity predicted smoking, cues (e.g., smoking, neutral, alcohol, mood) had little influence on smoking (Shiffman et al., 2013a). Background, or abstinence-induced, craving was related to smoking, but smoking variables were equivalent for each cue type. A second study using the same cues (Shiffman et al., 2013b) again found no evidence of main effects of cues on any measures of smoking behavior. In both of these studies, the authors note that the level of cue reactivity evoked was modest, and suggest that their cues may not have induced strong enough craving to allow specificity as a function of cue type to emerge. Likewise, they note their use of visual ratings of topography measures as a possible limitation. Thus, whether cues affect actual
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smoking and the extent to which greater cue-induced craving can predict subsequent smoking behavior remain uncertain and more controlled studies are clearly needed (Perkins, 2009; Shiffman, 2009; Tiffany & Wray, 2009). We have developed well-tested pictorial smoking cues that reliably evoke robust cue-induced craving from smokers (e.g., Conklin, Parzynski, Salkeld, Perkins, & Fonte, 2012; Conklin, Robin, Perkins, Salkeld, & McClernon, 2008). Using these stimuli in a computer-automated cue-reactivity study, we aimed to further examine the impact of cues on craving and smoking behavior, as well as to determine the predictive value of cue-induced craving on multiple objective smoking topography variables (latency to smoke, puff volume, and number of puffs) among nondeprived nontreatment-seeking daily smokers. We assessed subjective craving and behavioral responses to pictorial smoking and neutral cues across two separate sessions. We hypothesized that exposure to these highly salient pictorial smoking cues, relative to neutral cues, would evoke enhanced cue-induced self-report craving, as well as greater smoking intensity evidenced by quicker latency to smoke and greater puff volume and number of puffs compared with neutral cues. Most important, we anticipated a strong predictive relationship between these self-report and behavioral indices of cue reactivity.
Method Participants Newspaper advertisements and flyers were used to recruit 60 smokers (30 men and 30 women) for the study. Advertisements invited, “healthy men and women smokers, ages 18 – 65 [to participate in] a research study investigating smoking cues.” Participants were on average 36.9 years old and smoked 19.72 cigarettes per day. They had to have been smoking regularly for at least a year (M ⫽ 10.21 years; SD ⫽ 10.18; range ⫽ 1–33 years), and have a baseline carbon monoxide concentration ⬎8 ppm (M ⫽ 21.68, SD ⫽ 11.4). Participants had an average Fagerström Test of Nicotine Dependence (FTND; Heatherton, Kozlowski, Frecker, & Fagerström, 1991) score of 5.7 (SD ⫽ 1.8; range ⫽ 1–9). Each participant was paid $100 for completing the study. All methods used in this study were approved by the Institutional Review Board of the University of Pittsburgh.
Stimulus Materials Pictorial cue stimuli used in the present study included three smoking cues (lit cigarette in ashtray, lighters, pack of cigarettes) and three neutral cues (notepad and pen, lip balms, bar of soap) shown from four angles each, for a total of 24 cue pictures (12 smoking, 12 neutral). All of these pictorial cues were initially piloted and have been used in several past cue-reactivity smoking studies (e.g., Conklin et al., 2008; 2012).
Procedure Each participant attended two experimental sessions on two separate days. The 2 sessions varied only in the cues presented (smoking or neutral, the order of which was counterbalanced and stratified by gender). Additionally, Session 1 included informed
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consent and initial questionnaires including a Smoking History Form, the FTND scale, and the Balanced Inventory of Desired Responding—Impression Management section (BIDR⫺IM; Paulhus, 1991.) The BIDR⫺IM is a factor-analytically derived questionnaire of the extent to which an individual engages in conscious attempts to create favorable responses. Its inclusion allowed for investigation of possible associations between impression management and participants’ answers on self-report measures. During each session, the participant sat in front of a 21-inch computer screen in a dimly lit room and viewed the stimulus pictures. To standardize time since last cigarette, the participant smoked one cigarette at the beginning of each session, using the CReSS (Plowshare Technologies, Baltimore, MD) hand-held smoking device, which allows for assessment of smoking topography measures (i.e., puff volume, latency to first puff, and number of puffs). This also allowed for training on how to use the CReSS device, which would be utilized for ad lib smoking later in the computer-automated cue-reactivity sessions. Following the baseline cigarette, the participant rested and read magazines for 30 minutes. A screen prompt then indicated that the picture trials would start, the experimenter turned down the lights, left the room, and the participant was prompted to complete a baseline craving rating before the computer-automated cue reactivity began. Cue exposure then began (2 min of exposure to the 12 picture cues, 10 s each, of either smoking or neutral objects, depending on session). The participant was instructed to focus intently on each object pictured as if he or she had the actual item with him/her. Cueinduced subjective craving was collected following that initial cue exposure. A screen then appeared informing the participant that at any time from that point on he or she could smoke as much or little as desired. All participants who chose to smoke did so through the hand-held CReSS cigarette holder. Exposure to the 12 picture cues continued for a 6-min ad lib period during which topography measures were collected. During the 6-min ad lib period, each picture was presented for 10 s and repeated three times in a counterbalanced order. The presentation of the pictorial stimuli was controlled by Microsoft PowerPoint, 2000 software (Microsoft Corporation; Redwood, WA) on a Compaq Evo computer (Hewlett Packard Company; Palo Alto, CA) and displayed on a 22-inch monitor (ViewSonic Corporation; Walnut, CA). After the ad lib period, the experimenter returned to the room, and if it was the second session, debriefed the participant before paying him/her.
Analytic Strategy The analyses for the current study focused on the impact of cue type (smoking vs. neutral) on self-reported craving and behavioral indices of cue reactivity. The primary analyses reported in the current study were evaluated via mixed model regression with SAS PROC MIXED (SAS Institute, Inc, 2010). Mixed model regression features advantages over traditional forms of regression, because of the ability to handle repeated assessments of both predictor variables (e.g., stimulus condition of neutral cues vs. smoking cues) and outcome variables (e.g., craving scores and smoking topography measure of latency to smoke, number of puffs, and total puff volume) in combination with betweensubjects predictors (e.g., trait scores of impression management and nicotine dependence).
Analyses of mixed model regressions tested the main effects of cue trial (1 ⫽ neutral cue, 2 ⫽ smoking cue) on craving and smoking topography variables. Separate models were evaluated for the following outcome variables: craving, latency to smoke, total number of puffs, and total puff volume. Baseline craving levels were entered into models evaluating posttrial craving prior to the inclusion of the independent variable of cue type, to control for their predictive influence on this outcome variable. A second set of mixed model regressions examined whether magnitude of cue-induced craving (postexposure craving minus baseline craving) predicted smoking topography variables, with separate models evaluating the dependent variables of total puff volume, total number of puffs, and latency to smoke. For each of these models, cue-induced Craving ⫻ Trial interaction effects were tested to ascertain, for example, whether latency to smoke was quickest amid those who displayed elevated craving exclusive to smoking cues. In accordance with recommendations by Aiken and West (1991), significant interactions were followed up by simple slopes analyses.
Results Craving and Behavioral Responses to Experimental Cues Ancillary exploratory analyses tested whether between-subjects variables of age, gender, number of cigarettes smoked per day, and trait levels of impression management and nicotine dependence predicted any of the craving and smoking topography dependent variables under study. All these between-subjects predictors were nonsignificant and as such were excluded from the mixed model regressions reported here. However, an order effect was apparent exclusive to the total puff volume dependent variable, B ⫽ ⫺194.69, SE ⫽ 87.73; t(60) ⫽ ⫺2.2, p ⫽ .03, indicating participants demonstrated larger inhalations if receiving smoking cues first, neutral cues second. Consequently, presentation order was entered as a covariate for all analyses predicting total puff volume. It is important to note that the McNemar test for repeated measures on dichotomous variables indicated that participants were significantly more likely to smoke following exposure to smoking cues (54/60 ⫽ 90%) relative to following neutral cues (43/60 ⫽ 72%), p ⬍ .001. In accord with expectation, experimental cue type (neutral, smoking) was a significant predictor of postexposure craving, after controlling for baseline craving, B ⫽ 25.13, SE ⫽ 2.86; t(59) ⫽ 8.78, p ⬍ .001, indicating smoking cue exposure predicted a significant increase in craving relative to neutral cues (i.e., strong cue-induced craving). A similar pattern of relationship emerged with the smoking topography variables, whereby exposure to smoking cues predicted greater subsequent total number of puffs, B ⫽ 4.03, SE ⫽ .812; t(59) ⫽ 4.93, p ⬍ .001, and total puff volume post trial, B ⫽ 267, SE ⫽ 67.97; t(59) ⫽ 3.93, p ⬍ .001, compared with smoking after neutral cue exposure. Finally, a significant inverse association was evident between cue type and latency to smoke in milliseconds, B ⫽ ⫺79,557, SE ⫽ 15,304; t(59) ⫽ ⫺5.2, p ⬍ .001, with smoking cue exposure predicting quicker latency to smoke relative to neutral cues. Taken together, these findings indicate that relative to neutral cues, smoking cues predicted significant increases in craving, total number of puffs,
CRAVING AND SMOKING BEHAVIOR
Craving Reactivity X Cue Type on # of Puffs
Table 1 Descriptive Statistics of Sample Characteristics and Main Effects for Primary Analyses
Age Number cigarettes smoked/day Fagerström test of nicotine dependence Gender Male Female Ethnicity African American Caucasian Biracial Native American Education African American Caucasian Biracial Native American Some graduate school Graduate degree
Baseline craving Baseline number of puffs Total puff volume (mL) Posttrial craving Posttrial number of puffs Posttrial puff volume (mL) Posttrial latency to smoke (ms)
M
SD
36.9 19.7
12.9 7.1
5.7
1.8
30 (50%) 30 (50%)
Total Number of Puffs
Frequency (%)
14 12 10
-1SD Craving Reactivity
8 6
*AVG Craving Reactivity
4
*+1SD Craving Reactivity
2 0 Neutral Cues Smoking Cues *p < .001
19 (31.7%) 38 (63.3%) 2 (3.3%) 1 (1.7%)
Figure 1. Mixed model regression interaction between Craving Reactivity ⫻ Cue Type on total number of puffs. Simple slopes represent total number of puffs at one standard deviation above and below the centered mean of craving reactivity.
2 (3.3%) 17 (28.3%) 29 (48.3%) 8 (13.3%) 2 (3.3%) 2 (3.3%)
Discussion
Neutral cue
Smoking cue
M
SD
M
SD
37.7 11.2 567.12 28.54 8.02 379.0 182,773
25.6 4.6 239.58 26.1 6.70 327.9 137,964
37.1 12.1 586.90 53.13 12.10 645.9 103,215
23.6 5.1 240.98 27.10ⴱ 6.05ⴱ 535.9ⴱ 102,25ⴱ
Note. n ⫽ 60. ⴱ p ⬍ .001.
and total puff volume, coupled with shorter latencies to smoke. See Table 1 for descriptive statistics pertaining to these analyses.
Craving Reactivity as a Predictor of Smoking Behavior A second set of mixed model regressions indicated cue-induced craving (postexposure craving minus baseline craving) to be a significant predictor of subsequent number of puffs, B ⫽ .08, SE ⫽ 0.24; t(59) ⫽ 3.2, p ⫽ .002, and total puff volume, B ⫽ 4.44, SE ⫽ 1.86; t(59) ⫽ 2.4, p ⫽ .02. Further, as predicted, magnitude of cue-induced craving was inversely related to smoking latency: B ⫽ ⫺1,727, SE ⫽ 434; t(59) ⫽ ⫺3.98, p ⫽ .002. It is important to note that all cue-induced Craving ⫻ Trial interactions were significant: total number of puffs, B ⫽ .197, SE ⫽ .063; t(57) ⫽ 3.11, p ⫽ .003; total puff volume, B ⫽ 11.34, SE ⫽ 4.79; t(57) ⫽ 2.37, p ⫽ .02; and latency to smoke; B ⫽ ⫺3,137, SE ⫽ 1,206; t(57) ⫽ ⫺2.6, p ⫽ .02. Simple slopes analyses indicated significant effects at the centered mean of craving reactivity and at one standard deviation above the mean, whereby smoking cue exposure predicted significant increases in total number of puffs and total puff volume and significant decreases in latency to smoke relative to neutral cue exposure (see Figures 1, 2, and 3).
Results of the present study directly inform our understanding of how cues impact actual smoking behavior, as well as the relationship between cue-induced craving and smoking behavior. As noted, there have been numerous cue studies demonstrating that confrontation with smoking cues significantly increases cueinduced craving among smokers and moderately alters autonomic reactivity (see Carter & Tiffany, 1999, for review), but few demonstrating an increase in actual smoking in direct response to smoking cue exposure. Likewise, there has been little empirical evidence of a predictive relationship between cue-induced craving and subsequent smoking. The present findings offer direct evidence of both. Similar to past research investigating the impact of proximal smoking cues on smokers’ subjective reactivity (e.g., Conklin et al., 2008), the present study confirmed that exposure to these smoking-related cues predicts not only robust self-reported craving but also increases in subsequent smoking behavior as well. Specifically, smoking cue exposure predicted elevated craving, shorter latency to smoke, and greater number of puffs and puff volume
Total Puff Volume (mL)
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Variable
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Craving Reactivity X Cue Type on Total Puff Volume 900 800 700 600 -1SD Craving 500 Reactivity 400 *AVG Craving 300 Reactivity 200 *+1SD Craving 100 Reactivity 0 Neutral Cues Smoking Cues *p < .005
Figure 2. Mixed model regression interaction between Craving Reactivity ⫻ Cue Type on total puff volume. Simple slopes represent total puff volume at one standard deviation above and below the centered mean of craving reactivity.
CONKLIN ET AL.
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Latency to Smoke in Minutes
Craving Reactivity X Cue Type on Latency to Smoke 4 3.5 3 2.5 2 1.5 1 0.5 0
-1SD Craving Reactivity *AVG Craving Reactivity *+1SD Craving Reactivity Neutral Cues Smoking Cues *p < .005
Figure 3. Mixed model regression interaction between Craving Reactivity ⫻ Cue Type on latency to smoke. Simple slopes represent latency to smoke in minutes at one standard deviation above and below the centered mean of craving reactivity.
relative to neutral cues. So, a cue that induced strong craving to smoke also increased the speed with which the individual subsequently lit up a cigarette, as well as the amount he or she smoked. This finding partly replicates early cue-reactivity investigations of craving and smoking behavior, which demonstrated increases in craving as a function of smoking cue exposure (Droungas et al., 1995; Herman, 1974), as well as increases in measures of smoking topography (Droungas et al., 1995; Herman, 1974; Payne et al., 1991). Unlike those studies, the present investigation controlled for baseline preexposure craving, and although Payne et al. (1991) included neutral cue exposure as a comparison, the others relied on the presence or absence of smoking cues rather than a neutral comparison cue. With our more tightly controlled design, the impact of craving and smoking topography still emerged robustly. However, these results stand in contrast to recent findings by Shiffman et al. (2013a, 2013b). Although the authors’ found that noncue-related craving, background craving, was associated with the probability and amount of smoking post cue exposure, no main effects of cue type on any smoking topography variables were revealed. Similar to those results, the present study did find that baseline craving, self-report craving prior to any cue exposure, was predictive of smoking during the later in-session ad lib period. So, as Shiffman et al. (2013a, 2013b) found, smokers who carry higher background craving may be more likely to smoke when given the opportunity. However, in contrast to their findings, we saw a highly significant increase in both cue-induced craving and smoking topography variables when smokers were exposed to smoking versus neutral cues, as well as a predictive relationship between cue-induced craving and immediate smoking behavior. Although the basic cue-reactivity paradigm was similar between our study and those of Shiffman et al. (2013a, 2013b), there are several methodological differences that may account for the contrast in findings. First, Shiffman et al. (2013a, 2013b) used multiple cues (i.e., smoking, neutral, alcohol, and mood) during independent cue-reactivity sessions. Perhaps reactivity was tempered by increased demand on attention and focus on various cues across the study. However, as the authors noted, there is little evidence that smokers’ habituate to cues or to the cue-reactivity paradigm after several sessions. A second, more likely, explanation for differing results is the actual smoking and neutral cues used.
Shiffman et al., 2013a pointed to the cues they used as a possible limitation stating that “the absolute magnitude of reactivity observed here was modest; perhaps other cues or study procedures would have elicited stronger responses” (p. 331). Unlike their studies, cue-induced craving as a function of our smoking and neutral cues was robust and highly significant differences emerged. We have used these cues across past studies (although not to examine smoking behavior) and found a cue-induced craving effect size of d ⫽ 1.40 (e.g., Conklin et al., 2008), which by Cohen’s (1988) estimation (effect sizes at or greater than d ⫽ .8) can be considered large. The heightened magnitude of cue-induced craving evoked by our pictorial cues may be what allowed the impact of cues on craving and smoking behavior to emerge in the present study relative to past studies. The robustness of our cue effects may also account for the emergence of a strong predictive relationship between cue-induced craving and subsequent smoking behavior. This relationship has not been revealed in past studies, because of either an absence of examining it (Droungas, 1995; Herman, 1974; Payne, 1991) or to nonsignificant results (Shiffman et al., 2013a, 2013b). We found that unlike investigations of the relationship between cue-induced craving and physiological reactivity, between which associations have been limited or nonsignificant, cue-induced craving in the present study was highly predictive of increases in immediate smoking behavior. The overall change in baseline craving to postexposure craving significantly predicted ad lib number of puffs, puff volume, and shorter latency to smoke. Further, when cue-induced craving was indexed as the difference between smoking and neutral cues (i.e., controlling for background craving), a greater difference predicted a greater number of puffs, total puff volume, and quicker latency to smoke. Overall, these findings are some of the first to reveal evidence of a predictive relationship between cue-induced craving and immediate smoking behavior, and show strong specificity of cue-induced craving brought on by smoking cues relative to neutral cues as a predictor of immediate smoking behavior. Results of this study also suggest that, more than previously thought, cue-induced craving may reflect how cues influence smoking behavior in the real world. Although the present results stand in contrast to laboratory cue studies recently conducted by Shiffman et al. (2013a, 2013b), they cohere tightly with the authors’ ecological momentary assessment (EMA) study findings demonstrating that situational stimuli are indentified in smokers’ diaries as clear antecedents of smoking (Shiffman et al., 2002), as well as triggers for relapse (Shiffman et al., 1996). Moreover, given that studying actual smoking is not possible in cessation studies, for which abstinence is the goal, the present work suggests that cue-induced craving may serve as a useful measure of desire to smoke and likelihood of lapsing among those trying to quit, and might be used to track treatment progress. However, more research is needed to understand how cue reactivity functions among quitting smokers, as some recent studies have shown higher cueinduced craving as a predictor success in initiating a quit attempt (Conklin et al., 2012; Powell, Dawkins, West, Powell, & Pickering, 2011) and longer time to lapse (Niaura et al., 1999). Therefore, although in nonquitting smokers increased cue-induced craving predicted immediate smoking in the present study, among quitting smokers reactivity to cues may index heightened anticipation or intention to soon initiate abstinence (Conklin et al., 2012). Clearly,
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CRAVING AND SMOKING BEHAVIOR
more studies are needed investigating how cues function across a variety of smoking and quitting scenarios. The present study also suggests that laboratory-based cueelicited craving may be an efficient method of testing the efficacy of novel medications for smoking cessation (Ditre et al., 2012). Whereas nicotine replacement therapy significantly reduces abstinence-induced craving, or background craving, no medications for attenuating cue-induced craving have been discovered. Therefore, using the present study cue paradigm, a medication that reduces or inhibits cue-induced craving may in turn decrease the likelihood or amount of subsequent smoking. This suggests a positive effect on smoking cessation. However, further support of the validity of cue-induced craving as a clinical measure predictive of subsequent smoking is needed, particularly in quitting smokers. A few limitations of the present study should be noted. First, the ad lib period was only 6 min. It may be that smokers in the neutral condition would have eventually smoked, but needed longer than 6 min to do so. However, with increasing time, the decision to smoke may be motivated more by abstinence-induced, not cueinduced, craving. Second, as is the case with all laboratory studies, the extent to which these results parallel confrontations and decisions to smoke when confronted with smoking-related cues in the real world is speculative. As noted, these results map onto past EMA study findings that smokers report exposure to real-world cues preceding smoking and relapse (Shiffman et al., 1996; Shiffman et al., 2002). Still, real-world exposure to cues is clearly less static and controlled. Thus, studies that incorporate more of the cues smokers typically encounter (e.g., multiple cues, personal cues from smokers’ own experiences, social cues) may provide a more complete and accurate picture of how real-world cue confrontations actually affect smokers’ behavior (Conklin, 2006). Within these limitations, the present study demonstrates that discrete smoking cues capable of inducing robust craving from smokers also increase their immediate smoking behavior. Moreover, it provides novel evidence that cue-induced craving is highly predictive of immediate smoking. Thus, unlike several past investigations showing limited coherence between subjective and physiological reactivity to smoking cues, the present study found a strong predictive relationship between self-reported cue-induced craving and subsequent smoking behavior. Although this relationship between cues, craving, and actual smoking has been long assumed, the present study offers some of the first evidence that it is empirically supported.
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Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum. Conklin, C. A. (2006). Environments as cues to smoke: Implications for human extinction-based research and treatment. Experimental and Clinical Psychopharmacology, 14, 12–19. http://dx.doi.org/10.1037/10641297.14.1.12 Conklin, C. A., Parzynski, C. S., Salkeld, R. P., Perkins, K. A., & Fonte, C. A. (2012). Cue reactivity as a predictor of successful abstinence initiation among adult smokers. Experimental and Clinical Psychopharmacology, 20, 473– 478. http://dx.doi.org/10.1037/a0029599 Conklin, C. A., Robin, N., Perkins, K. A., Salkeld, R. P., & McClernon, F. J. (2008). Proximal versus distal cues to smoke: The effects of environments on smokers’ cue-reactivity. Experimental and Clinical Psychopharmacology, 16, 207–214. http://dx.doi.org/10.1037/10641297.16.3.207 Conklin, C. A., Salkeld, R. P., Perkins, K. A., & Robin, N. (2013). Do people serve as cues to smoke? Nicotine & Tobacco Research, 15, 2081–2087. http://dx.doi.org/10.1093/ntr/ntt104 Ditre, J. W., Oliver, J. A., Myrick, H., Henderson, S., Saladin, M. E., & Drobes, D. J. (2012). Effects of divalproex on smoking cue reactivity and cessation outcomes among smokers achieving initial abstinence. Experimental and Clinical Psychopharmacology, 20, 293–301. http://dx .doi.org/10.1037/a0027789 Droungas, A., Ehrman, R. N., Childress, A. R. & O’Brien, C. P. (1995). Effect of smoking cues and cigarette availability on craving and smoking behavior. Addictive Behaviors, 20, 657– 673. Glautier, S., & Tiffany, S. T. (1995). Methodological issues in cue reactivity research. In D. C. Drummond, S. T. Tiffany, S. Glautier, & B. Remington (Eds.), Addictive behaviour: Cue exposure theory and practice, pp. 75–97. Chichester: John Wiley & Sons. Heatherton, T. F., Kozlowski, L. T., Frecker, R. C., & Fagerström, K. O. (1991). The Fagerström Test for Nicotine Dependence: A revision of the Fagerström Tolerance Questionnaire. British Journal of Addiction, 86, 1119 –1127. http://dx.doi.org/10.1111/j.1360-0443.1991.tb01879.x Herman, C. P. (1974). External and internal cues as determinants of the smoking behavior of light and heavy smokers. Journal of Personality and Social Psychology, 30, 664 – 672. Hutchison, K. E., Monti, P. M., Rohsenow, D. J., Swift, R. M., Colby, S. M., Gnys, M., . . . Sirota, A. D. (1999). Effects of naltrexone with nicotine replacement on smoking cue reactivity: Preliminary results. Psychopharmacology, 142, 139 –143. http://dx.doi.org/10.1007/ s002130050872 Niaura, R., Abrams, D. B., Shadel, W. G., Rohsenow, D. J., Monti, P. M., & Sirota, A. D. (1999). Cue exposure treatment for smoking relapse prevention: A controlled clinical trial. Addiction, 94, 685– 695. http://dx .doi.org/10.1046/j.1360-0443.1999.9456856.x Paulhus, D. L. (1991). Measurement and control of response bias. In J. P. Robinson & P. R. Shaver (Eds.), Measures of personality and social psychological attitudes (Vol. 1, pp. 17–59). San Diego, CA: Academic Press, Inc. http://dx.doi.org/10.1016/B978-0-12-590241-0.50006-X Payne, T. J., Schare, M. L., Levis, D. J., & Colletti, G. (1991). Exposure to smoking-relevant cues: Effects on desire to smoke and topographical components of smoking behavior. Addictive Behaviors, 16, 467– 479. Perkins, K. A. (2009). Does smoking cue-induced craving tell us anything important about nicotine dependence? Addiction, 104, 1610 –1616. http://dx.doi.org/10.1111/j.1360-0443.2009.02550.x Powell, J., Dawkins, L., West, R., Powell, J., & Pickering, A. (2011). Erratum to: Relapse to smoking during unaided cessation: Clinical, cognitive and motivational predictors. Psychopharmacology, 215, 607. http://dx.doi.org/10.1007/s00213-011-2300-x Schuh, K. J., & Stitzer, M. L. (1995). Desire to smoke during spaced smoking intervals. Psychopharmacology, 120, 289 –295. http://dx.doi .org/10.1007/BF02311176
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Shiffman, S. (2009). Responses to smoking cues are relevant to smoking and relapse. Addiction, 104, 1617–1618. http://dx.doi.org/10.1111/j .1360-0443.2009.02580.x Shiffman, S., Dunbar, M. S., Kirchner, T. R., Li, X., Tindle, H. A., Anderson, S. J., . . . Ferguson, S. G. (2013a). Cue reactivity in non-daily smokers: Effects on craving and on smoking behavior. Psychopharmacology, 226, 321–333. http://dx.doi.org/10.1007/s00213-012-2909-4 Shiffman, S., Dunbar, M., Kirchner, T., Li, X., Tindle, H., Anderson, S., & Scholl, S. (2013b). Smoker reactivity to cues: Effects on craving and on smoking behavior. Journal of Abnormal Psychology, 122, 264 –280. http://dx.doi.org/10.1037/a0028339 Shiffman, S., Gwaltney, C. J., Balabanis, M. H., Liu, K. S., Paty, J. A., Kassel, J. D., . . . Gnys, M. (2002). Immediate antecedents of cigarette smoking: An analysis from ecological momentary assessment. Journal of Abnormal Psychology, 111, 531. Shiffman, S., Paty, J. A., Gnys, M., Kassel, J. A., & Hickcox, M. (1996). First lapses to smoking: Within-subjects analysis of real-time reports. Journal of Consulting and Clinical Psychology, 64, 366. Tiffany, S. T. (1990). A cognitive model of drug urges and drug-use behavior: Role of automatic and nonautomatic processes. Psychological Review, 97, 147–168. http://dx.doi.org/10.1037/0033-295X.97.2.147 Tiffany, S. T., & Conklin, C. A. (2000). A cognitive processing model of alcohol craving and compulsive alcohol use. Addiction, 95, 145–153. http://dx.doi.org/10.1080/09652140050111717
Tiffany, S. T., Cox, L. S., & Elash, C. A. (2000). Effects of transdermal nicotine patches on abstinence-induced and cue-elicited craving in cigarette smokers. Journal of Consulting and Clinical Psychology, 68, 233–240. http://dx.doi.org/10.1037/0022-006X.68.2.233 Tiffany, S. T., & Wray, J. (2009). The continuing conundrum of craving. Addiction, 104, 1618 –1619. http://dx.doi.org/10.1111/j.1360-0443.2009 .02588.x Waters, A. J., Shiffman, S., Sayette, M. A., Paty, J. A., Gwaltney, C. J., & Balabanis, M. H. (2004). Cue-provoked craving and nicotine replacement therapy in smoking cessation. Journal of Consulting and Clinical Psychology, 72, 1136 –1143. http://dx.doi.org/10.1037/0022-006X.72.6 .1136 Zacny, J. P., & Stitzer, M. L. (1985). Effects of smoke deprivation interval on puff topography. Clinical Pharmacology and Therapeutics, 38, 109 – 115. http://dx.doi.org/10.1038/clpt.1985.143
Received July 9, 2014 Revision received December 23, 2014 Accepted January 5, 2015 䡲
© 2015 American Psychological Association 1064-1297/15/$12.00 http://dx.doi.org/10.1037/a0038826
Examining the Relationship Between Cue-Induced Craving and Actual Smoking Cynthia A. Conklin
Elizabeth J. Vella
University of Pittsburgh
University of Southern Maine
Christopher J. Joyce, Ronald P. Salkeld, Kenneth A. Perkins, and Craig S. Parzynski This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
University of Pittsburgh Smoking cue-reactivity studies have consistently demonstrated heightened self-report craving, as well as moderate autonomic reactivity, among smokers exposed to salient drug-related cues. However, significantly fewer studies have examined whether exposure to smoking cues affects smokers’ actual smoking, or examined the predictive relationship between cue-induced craving and smoking behavior. Using our well-tested pictorial cues in a cue-reactivity paradigm, we investigated the impact of smoking-related cues relative to neutral cues on subjective craving and smoking behavior (assessed via CReSS; Plowshare Technologies, Baltimore, MD) measures of latency to smoke, puff volume, and number of puffs). Further, we examined the predictive value of cue-induced craving on subsequent smoking behavior. Sixty nondeprived daily smokers completed 2 experimental sessions involving exposure to either smokingrelated or neutral pictorial cues. Following initial exposure to cues, smokers rated their craving and were then allowed to smoke freely if they chose to during a subsequent 6-min cue exposure period. Result showed that exposure to smoking cues relative to neutral predicted significantly greater craving and increases in smoking behavior. Likewise, the magnitude of the difference in cue-induced craving when exposed to smoking cues relative to neutral cues (i.e., the cue-reactivity effect) was highly predictive of shorter latency to smoke, as well as increased number of puffs and puff volume. Keywords: smoking, cue reactivity, cue-induced craving, smoking behavior
several theories anticipate a tight relationship between the two. For example, the dual-affect model purports that as urge networks become more fully activated, measures of craving and physiological responding should become more strongly intercorrelated (e.g., Baker, Morse, & Sherman, 1986). Moreover, other theories suggest that stimuli and/or situations that evoke strong craving should also evoke coherent physiological increases (Tiffany, 1990). However, given the complexity of both cue-induced craving and physiological reactivity, a direct correlation between these measures may be too simplistic to expect. Compared with the wealth of studies investigating subjective and physiological responses to smoking cues, very few studies have examined if smoking-related cues affect actual smoking behavior. In theory, if a smoker is craving and has access to cigarettes in an environment permissive of smoking, the expectation is that he or she, barring any attempt to quit, will choose to smoke (Tiffany, 1990). Indeed, this relationship holds well among nonquitting smokers experiencing abstinence-induced craving brought on by intermittent nicotine deprivation (Schuh & Stitzer, 1995; Zacny & Stitzer, 1985). However, cue-induced craving appears to behave differently and seemingly more independently of nicotine. For example, nicotine replacement studies have shown that NRT directly reduces abstinence-induced craving but fails to attenuate cue-induced craving (Hutchison et al., 1999; Tiffany, Cox, & Elash, 2000; Waters et al., 2004). Likewise, even in sated smokers, exposure to smoking-related cues evokes strong increases in self-reported craving (e.g., Carter et al., 2006). So, although an autonomic response to cues may not
It is well established that smokers react with robust increases in self-reported craving, and moderate changes in autonomic reactivity (e.g., heart rate, skin conductance, blood pressure) when exposed to smoking-related stimuli (Carter & Tiffany, 1999). Although significant changes in these various indices of responding have been seen across cue studies, correlations between measures are consistently very weak or absent. See (Carter & Tiffany, 1999, for review). The lack of coherence between self-report and autonomic responses to drug-related cues is somewhat surprising, as
This article was published Online First March 2, 2015. Cynthia A. Conklin, Department of Psychiatry, University of Pittsburgh; Elizabeth J. Vella, Department of Psychology, University of Southern Maine; Christopher J. Joyce, Ronald P. Salkeld, Kenneth A. Perkins, and Craig S. Parzynski, Department of Psychiatry, University of Pittsburgh. Craig S. Parzynski is now at Yale University, Department of Internal Medicine. This research was supported by National Institute on Drug Abuse Grants DA023646 and DA027508. The funding source had no role in the research other than financial support. We have contributed significantly to the article and have read and approved the final manuscript. We do not have a conflict of interest that may inappropriately impact or influence the research or interpretation of the findings. We thank Bethany Preston for her assistance with this research. Correspondence concerning this article should be addressed to Cynthia A. Conklin, 3811 O’Hara Street, Room 1620, Pittsburgh, PA 15213. E-mail: [email protected] 90
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CRAVING AND SMOKING BEHAVIOR
strongly track how an individual reports thinking and feeling, one might expect a person’s self-reported desire and intention to immediately engage in a reinforcing appetitive behavior to better map on to how they subsequently behave. Specifically, if a nonquitting smoker reports heightened craving after seeing salient smoking stimuli and is immediately offered a chance to smoke, a reasonable assumption is that the majority of the time, smoking will follow. In fact, the assumption of a predictive relationship between cue-induced craving and subsequent smoking is commonly held, yet review of the cuereactivity smoking literature finds limited empirical evidence to support it. This may be due in part to challenges noted by several researchers that drug-use behaviors are complex and finding a single smoking behavior that adequately functions as an index of smoking motivation or likelihood of use may be difficult or unlikely (e.g., Carter & Tiffany, 1999; Glautier & Tiffany, 1995; Tiffany, 1990), as well as the fact that behavioral reactivity is more difficult to assess. Specifically, examining the impact of cues on smoking requires lengthier studies, given that once a participant has smoked, all manipulation thereafter are confounded by smoking, necessitating individual sessions for different cue manipulations. There is some evidence that the majority of lapses and relapses to smoking during quit attempts occur in the presence self-reported cue exposure and/or cue-induced craving (Shiffman, Paty, Gnys, Kassel, & Hickox, 1996). And, a few experimental studies directly examining smoking behavior in response to smoking cue exposure in the lab have been conducted and shown promising but inconclusive support for this relationship. In perhaps the first study, Herman (1974) found that when confronted with high versus low salience smoking cues (a light directed on participants ashtrays and cigarettes vs. no light on these stimuli), light smokers reported greater craving, were quicker to initiate smoking, and smoked more. Similarly, Droungas et al. (1995) found that smokers who were told they would be able to smoke in session, responded to smoking cues relative to nonsmoking cues with greater craving, withdrawal, and quicker latency to smoke. Another study involving the manipulation of both affect and smoking cues (Payne et al., 1991) found that smokers sitting in a room containing multiple smoking-related cues lit up quicker and increased their puff duration compared with those in a room devoid of any visible smoking stimuli. On balance, these studies demonstrate a clear link between exposure to smoking-related cues and subsequent smoking behavior. However, none of these studies examined the predictive relationship between cue-induced craving and subsequent smoking behavior. More recent cue-reactivity studies examining craving and behavior have been conducted by Shiffman et al. (2013a, 2013b). The first study, examining differences in cue reactivity and behavioral responding in intermittent and daily smokers, found that although craving intensity predicted smoking, cues (e.g., smoking, neutral, alcohol, mood) had little influence on smoking (Shiffman et al., 2013a). Background, or abstinence-induced, craving was related to smoking, but smoking variables were equivalent for each cue type. A second study using the same cues (Shiffman et al., 2013b) again found no evidence of main effects of cues on any measures of smoking behavior. In both of these studies, the authors note that the level of cue reactivity evoked was modest, and suggest that their cues may not have induced strong enough craving to allow specificity as a function of cue type to emerge. Likewise, they note their use of visual ratings of topography measures as a possible limitation. Thus, whether cues affect actual
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smoking and the extent to which greater cue-induced craving can predict subsequent smoking behavior remain uncertain and more controlled studies are clearly needed (Perkins, 2009; Shiffman, 2009; Tiffany & Wray, 2009). We have developed well-tested pictorial smoking cues that reliably evoke robust cue-induced craving from smokers (e.g., Conklin, Parzynski, Salkeld, Perkins, & Fonte, 2012; Conklin, Robin, Perkins, Salkeld, & McClernon, 2008). Using these stimuli in a computer-automated cue-reactivity study, we aimed to further examine the impact of cues on craving and smoking behavior, as well as to determine the predictive value of cue-induced craving on multiple objective smoking topography variables (latency to smoke, puff volume, and number of puffs) among nondeprived nontreatment-seeking daily smokers. We assessed subjective craving and behavioral responses to pictorial smoking and neutral cues across two separate sessions. We hypothesized that exposure to these highly salient pictorial smoking cues, relative to neutral cues, would evoke enhanced cue-induced self-report craving, as well as greater smoking intensity evidenced by quicker latency to smoke and greater puff volume and number of puffs compared with neutral cues. Most important, we anticipated a strong predictive relationship between these self-report and behavioral indices of cue reactivity.
Method Participants Newspaper advertisements and flyers were used to recruit 60 smokers (30 men and 30 women) for the study. Advertisements invited, “healthy men and women smokers, ages 18 – 65 [to participate in] a research study investigating smoking cues.” Participants were on average 36.9 years old and smoked 19.72 cigarettes per day. They had to have been smoking regularly for at least a year (M ⫽ 10.21 years; SD ⫽ 10.18; range ⫽ 1–33 years), and have a baseline carbon monoxide concentration ⬎8 ppm (M ⫽ 21.68, SD ⫽ 11.4). Participants had an average Fagerström Test of Nicotine Dependence (FTND; Heatherton, Kozlowski, Frecker, & Fagerström, 1991) score of 5.7 (SD ⫽ 1.8; range ⫽ 1–9). Each participant was paid $100 for completing the study. All methods used in this study were approved by the Institutional Review Board of the University of Pittsburgh.
Stimulus Materials Pictorial cue stimuli used in the present study included three smoking cues (lit cigarette in ashtray, lighters, pack of cigarettes) and three neutral cues (notepad and pen, lip balms, bar of soap) shown from four angles each, for a total of 24 cue pictures (12 smoking, 12 neutral). All of these pictorial cues were initially piloted and have been used in several past cue-reactivity smoking studies (e.g., Conklin et al., 2008; 2012).
Procedure Each participant attended two experimental sessions on two separate days. The 2 sessions varied only in the cues presented (smoking or neutral, the order of which was counterbalanced and stratified by gender). Additionally, Session 1 included informed
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consent and initial questionnaires including a Smoking History Form, the FTND scale, and the Balanced Inventory of Desired Responding—Impression Management section (BIDR⫺IM; Paulhus, 1991.) The BIDR⫺IM is a factor-analytically derived questionnaire of the extent to which an individual engages in conscious attempts to create favorable responses. Its inclusion allowed for investigation of possible associations between impression management and participants’ answers on self-report measures. During each session, the participant sat in front of a 21-inch computer screen in a dimly lit room and viewed the stimulus pictures. To standardize time since last cigarette, the participant smoked one cigarette at the beginning of each session, using the CReSS (Plowshare Technologies, Baltimore, MD) hand-held smoking device, which allows for assessment of smoking topography measures (i.e., puff volume, latency to first puff, and number of puffs). This also allowed for training on how to use the CReSS device, which would be utilized for ad lib smoking later in the computer-automated cue-reactivity sessions. Following the baseline cigarette, the participant rested and read magazines for 30 minutes. A screen prompt then indicated that the picture trials would start, the experimenter turned down the lights, left the room, and the participant was prompted to complete a baseline craving rating before the computer-automated cue reactivity began. Cue exposure then began (2 min of exposure to the 12 picture cues, 10 s each, of either smoking or neutral objects, depending on session). The participant was instructed to focus intently on each object pictured as if he or she had the actual item with him/her. Cueinduced subjective craving was collected following that initial cue exposure. A screen then appeared informing the participant that at any time from that point on he or she could smoke as much or little as desired. All participants who chose to smoke did so through the hand-held CReSS cigarette holder. Exposure to the 12 picture cues continued for a 6-min ad lib period during which topography measures were collected. During the 6-min ad lib period, each picture was presented for 10 s and repeated three times in a counterbalanced order. The presentation of the pictorial stimuli was controlled by Microsoft PowerPoint, 2000 software (Microsoft Corporation; Redwood, WA) on a Compaq Evo computer (Hewlett Packard Company; Palo Alto, CA) and displayed on a 22-inch monitor (ViewSonic Corporation; Walnut, CA). After the ad lib period, the experimenter returned to the room, and if it was the second session, debriefed the participant before paying him/her.
Analytic Strategy The analyses for the current study focused on the impact of cue type (smoking vs. neutral) on self-reported craving and behavioral indices of cue reactivity. The primary analyses reported in the current study were evaluated via mixed model regression with SAS PROC MIXED (SAS Institute, Inc, 2010). Mixed model regression features advantages over traditional forms of regression, because of the ability to handle repeated assessments of both predictor variables (e.g., stimulus condition of neutral cues vs. smoking cues) and outcome variables (e.g., craving scores and smoking topography measure of latency to smoke, number of puffs, and total puff volume) in combination with betweensubjects predictors (e.g., trait scores of impression management and nicotine dependence).
Analyses of mixed model regressions tested the main effects of cue trial (1 ⫽ neutral cue, 2 ⫽ smoking cue) on craving and smoking topography variables. Separate models were evaluated for the following outcome variables: craving, latency to smoke, total number of puffs, and total puff volume. Baseline craving levels were entered into models evaluating posttrial craving prior to the inclusion of the independent variable of cue type, to control for their predictive influence on this outcome variable. A second set of mixed model regressions examined whether magnitude of cue-induced craving (postexposure craving minus baseline craving) predicted smoking topography variables, with separate models evaluating the dependent variables of total puff volume, total number of puffs, and latency to smoke. For each of these models, cue-induced Craving ⫻ Trial interaction effects were tested to ascertain, for example, whether latency to smoke was quickest amid those who displayed elevated craving exclusive to smoking cues. In accordance with recommendations by Aiken and West (1991), significant interactions were followed up by simple slopes analyses.
Results Craving and Behavioral Responses to Experimental Cues Ancillary exploratory analyses tested whether between-subjects variables of age, gender, number of cigarettes smoked per day, and trait levels of impression management and nicotine dependence predicted any of the craving and smoking topography dependent variables under study. All these between-subjects predictors were nonsignificant and as such were excluded from the mixed model regressions reported here. However, an order effect was apparent exclusive to the total puff volume dependent variable, B ⫽ ⫺194.69, SE ⫽ 87.73; t(60) ⫽ ⫺2.2, p ⫽ .03, indicating participants demonstrated larger inhalations if receiving smoking cues first, neutral cues second. Consequently, presentation order was entered as a covariate for all analyses predicting total puff volume. It is important to note that the McNemar test for repeated measures on dichotomous variables indicated that participants were significantly more likely to smoke following exposure to smoking cues (54/60 ⫽ 90%) relative to following neutral cues (43/60 ⫽ 72%), p ⬍ .001. In accord with expectation, experimental cue type (neutral, smoking) was a significant predictor of postexposure craving, after controlling for baseline craving, B ⫽ 25.13, SE ⫽ 2.86; t(59) ⫽ 8.78, p ⬍ .001, indicating smoking cue exposure predicted a significant increase in craving relative to neutral cues (i.e., strong cue-induced craving). A similar pattern of relationship emerged with the smoking topography variables, whereby exposure to smoking cues predicted greater subsequent total number of puffs, B ⫽ 4.03, SE ⫽ .812; t(59) ⫽ 4.93, p ⬍ .001, and total puff volume post trial, B ⫽ 267, SE ⫽ 67.97; t(59) ⫽ 3.93, p ⬍ .001, compared with smoking after neutral cue exposure. Finally, a significant inverse association was evident between cue type and latency to smoke in milliseconds, B ⫽ ⫺79,557, SE ⫽ 15,304; t(59) ⫽ ⫺5.2, p ⬍ .001, with smoking cue exposure predicting quicker latency to smoke relative to neutral cues. Taken together, these findings indicate that relative to neutral cues, smoking cues predicted significant increases in craving, total number of puffs,
CRAVING AND SMOKING BEHAVIOR
Craving Reactivity X Cue Type on # of Puffs
Table 1 Descriptive Statistics of Sample Characteristics and Main Effects for Primary Analyses
Age Number cigarettes smoked/day Fagerström test of nicotine dependence Gender Male Female Ethnicity African American Caucasian Biracial Native American Education African American Caucasian Biracial Native American Some graduate school Graduate degree
Baseline craving Baseline number of puffs Total puff volume (mL) Posttrial craving Posttrial number of puffs Posttrial puff volume (mL) Posttrial latency to smoke (ms)
M
SD
36.9 19.7
12.9 7.1
5.7
1.8
30 (50%) 30 (50%)
Total Number of Puffs
Frequency (%)
14 12 10
-1SD Craving Reactivity
8 6
*AVG Craving Reactivity
4
*+1SD Craving Reactivity
2 0 Neutral Cues Smoking Cues *p < .001
19 (31.7%) 38 (63.3%) 2 (3.3%) 1 (1.7%)
Figure 1. Mixed model regression interaction between Craving Reactivity ⫻ Cue Type on total number of puffs. Simple slopes represent total number of puffs at one standard deviation above and below the centered mean of craving reactivity.
2 (3.3%) 17 (28.3%) 29 (48.3%) 8 (13.3%) 2 (3.3%) 2 (3.3%)
Discussion
Neutral cue
Smoking cue
M
SD
M
SD
37.7 11.2 567.12 28.54 8.02 379.0 182,773
25.6 4.6 239.58 26.1 6.70 327.9 137,964
37.1 12.1 586.90 53.13 12.10 645.9 103,215
23.6 5.1 240.98 27.10ⴱ 6.05ⴱ 535.9ⴱ 102,25ⴱ
Note. n ⫽ 60. ⴱ p ⬍ .001.
and total puff volume, coupled with shorter latencies to smoke. See Table 1 for descriptive statistics pertaining to these analyses.
Craving Reactivity as a Predictor of Smoking Behavior A second set of mixed model regressions indicated cue-induced craving (postexposure craving minus baseline craving) to be a significant predictor of subsequent number of puffs, B ⫽ .08, SE ⫽ 0.24; t(59) ⫽ 3.2, p ⫽ .002, and total puff volume, B ⫽ 4.44, SE ⫽ 1.86; t(59) ⫽ 2.4, p ⫽ .02. Further, as predicted, magnitude of cue-induced craving was inversely related to smoking latency: B ⫽ ⫺1,727, SE ⫽ 434; t(59) ⫽ ⫺3.98, p ⫽ .002. It is important to note that all cue-induced Craving ⫻ Trial interactions were significant: total number of puffs, B ⫽ .197, SE ⫽ .063; t(57) ⫽ 3.11, p ⫽ .003; total puff volume, B ⫽ 11.34, SE ⫽ 4.79; t(57) ⫽ 2.37, p ⫽ .02; and latency to smoke; B ⫽ ⫺3,137, SE ⫽ 1,206; t(57) ⫽ ⫺2.6, p ⫽ .02. Simple slopes analyses indicated significant effects at the centered mean of craving reactivity and at one standard deviation above the mean, whereby smoking cue exposure predicted significant increases in total number of puffs and total puff volume and significant decreases in latency to smoke relative to neutral cue exposure (see Figures 1, 2, and 3).
Results of the present study directly inform our understanding of how cues impact actual smoking behavior, as well as the relationship between cue-induced craving and smoking behavior. As noted, there have been numerous cue studies demonstrating that confrontation with smoking cues significantly increases cueinduced craving among smokers and moderately alters autonomic reactivity (see Carter & Tiffany, 1999, for review), but few demonstrating an increase in actual smoking in direct response to smoking cue exposure. Likewise, there has been little empirical evidence of a predictive relationship between cue-induced craving and subsequent smoking. The present findings offer direct evidence of both. Similar to past research investigating the impact of proximal smoking cues on smokers’ subjective reactivity (e.g., Conklin et al., 2008), the present study confirmed that exposure to these smoking-related cues predicts not only robust self-reported craving but also increases in subsequent smoking behavior as well. Specifically, smoking cue exposure predicted elevated craving, shorter latency to smoke, and greater number of puffs and puff volume
Total Puff Volume (mL)
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Variable
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Craving Reactivity X Cue Type on Total Puff Volume 900 800 700 600 -1SD Craving 500 Reactivity 400 *AVG Craving 300 Reactivity 200 *+1SD Craving 100 Reactivity 0 Neutral Cues Smoking Cues *p < .005
Figure 2. Mixed model regression interaction between Craving Reactivity ⫻ Cue Type on total puff volume. Simple slopes represent total puff volume at one standard deviation above and below the centered mean of craving reactivity.
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Latency to Smoke in Minutes
Craving Reactivity X Cue Type on Latency to Smoke 4 3.5 3 2.5 2 1.5 1 0.5 0
-1SD Craving Reactivity *AVG Craving Reactivity *+1SD Craving Reactivity Neutral Cues Smoking Cues *p < .005
Figure 3. Mixed model regression interaction between Craving Reactivity ⫻ Cue Type on latency to smoke. Simple slopes represent latency to smoke in minutes at one standard deviation above and below the centered mean of craving reactivity.
relative to neutral cues. So, a cue that induced strong craving to smoke also increased the speed with which the individual subsequently lit up a cigarette, as well as the amount he or she smoked. This finding partly replicates early cue-reactivity investigations of craving and smoking behavior, which demonstrated increases in craving as a function of smoking cue exposure (Droungas et al., 1995; Herman, 1974), as well as increases in measures of smoking topography (Droungas et al., 1995; Herman, 1974; Payne et al., 1991). Unlike those studies, the present investigation controlled for baseline preexposure craving, and although Payne et al. (1991) included neutral cue exposure as a comparison, the others relied on the presence or absence of smoking cues rather than a neutral comparison cue. With our more tightly controlled design, the impact of craving and smoking topography still emerged robustly. However, these results stand in contrast to recent findings by Shiffman et al. (2013a, 2013b). Although the authors’ found that noncue-related craving, background craving, was associated with the probability and amount of smoking post cue exposure, no main effects of cue type on any smoking topography variables were revealed. Similar to those results, the present study did find that baseline craving, self-report craving prior to any cue exposure, was predictive of smoking during the later in-session ad lib period. So, as Shiffman et al. (2013a, 2013b) found, smokers who carry higher background craving may be more likely to smoke when given the opportunity. However, in contrast to their findings, we saw a highly significant increase in both cue-induced craving and smoking topography variables when smokers were exposed to smoking versus neutral cues, as well as a predictive relationship between cue-induced craving and immediate smoking behavior. Although the basic cue-reactivity paradigm was similar between our study and those of Shiffman et al. (2013a, 2013b), there are several methodological differences that may account for the contrast in findings. First, Shiffman et al. (2013a, 2013b) used multiple cues (i.e., smoking, neutral, alcohol, and mood) during independent cue-reactivity sessions. Perhaps reactivity was tempered by increased demand on attention and focus on various cues across the study. However, as the authors noted, there is little evidence that smokers’ habituate to cues or to the cue-reactivity paradigm after several sessions. A second, more likely, explanation for differing results is the actual smoking and neutral cues used.
Shiffman et al., 2013a pointed to the cues they used as a possible limitation stating that “the absolute magnitude of reactivity observed here was modest; perhaps other cues or study procedures would have elicited stronger responses” (p. 331). Unlike their studies, cue-induced craving as a function of our smoking and neutral cues was robust and highly significant differences emerged. We have used these cues across past studies (although not to examine smoking behavior) and found a cue-induced craving effect size of d ⫽ 1.40 (e.g., Conklin et al., 2008), which by Cohen’s (1988) estimation (effect sizes at or greater than d ⫽ .8) can be considered large. The heightened magnitude of cue-induced craving evoked by our pictorial cues may be what allowed the impact of cues on craving and smoking behavior to emerge in the present study relative to past studies. The robustness of our cue effects may also account for the emergence of a strong predictive relationship between cue-induced craving and subsequent smoking behavior. This relationship has not been revealed in past studies, because of either an absence of examining it (Droungas, 1995; Herman, 1974; Payne, 1991) or to nonsignificant results (Shiffman et al., 2013a, 2013b). We found that unlike investigations of the relationship between cue-induced craving and physiological reactivity, between which associations have been limited or nonsignificant, cue-induced craving in the present study was highly predictive of increases in immediate smoking behavior. The overall change in baseline craving to postexposure craving significantly predicted ad lib number of puffs, puff volume, and shorter latency to smoke. Further, when cue-induced craving was indexed as the difference between smoking and neutral cues (i.e., controlling for background craving), a greater difference predicted a greater number of puffs, total puff volume, and quicker latency to smoke. Overall, these findings are some of the first to reveal evidence of a predictive relationship between cue-induced craving and immediate smoking behavior, and show strong specificity of cue-induced craving brought on by smoking cues relative to neutral cues as a predictor of immediate smoking behavior. Results of this study also suggest that, more than previously thought, cue-induced craving may reflect how cues influence smoking behavior in the real world. Although the present results stand in contrast to laboratory cue studies recently conducted by Shiffman et al. (2013a, 2013b), they cohere tightly with the authors’ ecological momentary assessment (EMA) study findings demonstrating that situational stimuli are indentified in smokers’ diaries as clear antecedents of smoking (Shiffman et al., 2002), as well as triggers for relapse (Shiffman et al., 1996). Moreover, given that studying actual smoking is not possible in cessation studies, for which abstinence is the goal, the present work suggests that cue-induced craving may serve as a useful measure of desire to smoke and likelihood of lapsing among those trying to quit, and might be used to track treatment progress. However, more research is needed to understand how cue reactivity functions among quitting smokers, as some recent studies have shown higher cueinduced craving as a predictor success in initiating a quit attempt (Conklin et al., 2012; Powell, Dawkins, West, Powell, & Pickering, 2011) and longer time to lapse (Niaura et al., 1999). Therefore, although in nonquitting smokers increased cue-induced craving predicted immediate smoking in the present study, among quitting smokers reactivity to cues may index heightened anticipation or intention to soon initiate abstinence (Conklin et al., 2012). Clearly,
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CRAVING AND SMOKING BEHAVIOR
more studies are needed investigating how cues function across a variety of smoking and quitting scenarios. The present study also suggests that laboratory-based cueelicited craving may be an efficient method of testing the efficacy of novel medications for smoking cessation (Ditre et al., 2012). Whereas nicotine replacement therapy significantly reduces abstinence-induced craving, or background craving, no medications for attenuating cue-induced craving have been discovered. Therefore, using the present study cue paradigm, a medication that reduces or inhibits cue-induced craving may in turn decrease the likelihood or amount of subsequent smoking. This suggests a positive effect on smoking cessation. However, further support of the validity of cue-induced craving as a clinical measure predictive of subsequent smoking is needed, particularly in quitting smokers. A few limitations of the present study should be noted. First, the ad lib period was only 6 min. It may be that smokers in the neutral condition would have eventually smoked, but needed longer than 6 min to do so. However, with increasing time, the decision to smoke may be motivated more by abstinence-induced, not cueinduced, craving. Second, as is the case with all laboratory studies, the extent to which these results parallel confrontations and decisions to smoke when confronted with smoking-related cues in the real world is speculative. As noted, these results map onto past EMA study findings that smokers report exposure to real-world cues preceding smoking and relapse (Shiffman et al., 1996; Shiffman et al., 2002). Still, real-world exposure to cues is clearly less static and controlled. Thus, studies that incorporate more of the cues smokers typically encounter (e.g., multiple cues, personal cues from smokers’ own experiences, social cues) may provide a more complete and accurate picture of how real-world cue confrontations actually affect smokers’ behavior (Conklin, 2006). Within these limitations, the present study demonstrates that discrete smoking cues capable of inducing robust craving from smokers also increase their immediate smoking behavior. Moreover, it provides novel evidence that cue-induced craving is highly predictive of immediate smoking. Thus, unlike several past investigations showing limited coherence between subjective and physiological reactivity to smoking cues, the present study found a strong predictive relationship between self-reported cue-induced craving and subsequent smoking behavior. Although this relationship between cues, craving, and actual smoking has been long assumed, the present study offers some of the first evidence that it is empirically supported.
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Received July 9, 2014 Revision received December 23, 2014 Accepted January 5, 2015 䡲
