Experimental and Clinical Psychopharmacology 2014, Vol. 22, No. 6, 502–510

© 2014 American Psychological Association 1064-1297/14/$12.00 http://dx.doi.org/10.1037/a0038250

Alcohol and Tobacco Cue Effects on Craving in Non-Daily Smokers Marcel P. J. Peloquin

Daniel S. McGrath

Dalhousie University

University of Calgary

Dessislava Telbis and Sean P. Barrett

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Dalhousie University Non-daily smokers commonly smoke cigarettes following the consumption of alcohol, yet the reason(s) for this remains poorly understood. The present study examined the impact of alcohol consumption on responses in tobacco salient cues 49 male and 50 female non-daily smokers. After the administration of an alcohol, placebo, or control beverage, participants were exposed to series neutral video clips and tobacco smoking salient video clips, and their subjective states and heart rates were monitored. The timing of the exposure to the tobacco smoking clips was randomly determined to coincide with the timing of either the ascending limb or the descending limb of the blood alcohol concentration (BAC) curve of the alcohol beverage condition. The tobacco smoking clips were found to increase cigarette craving regardless of beverage condition or timing of exposure (p ⫽ .002). Alcohol consumption was associated with increased ratings of intoxication (p ⬍ .001), increased heart rate across participants (p ⬍ .001), and increased cigarette craving in female participants specifically (p ⫽ .017). Alcohol did not influence responses to the smoking videos. These results suggest that smoking salient cues and alcohol may impact cigarette craving in non-daily smokers through independent processes. Keywords: cue reactivity, tobacco, alcohol, cigarette, sex difference

Stewart, Barrett, 2013) and smoking behavior (Barrett, Campbell, Roach, Stewart, & Darredeau, 2013; King et al., 2009; McKee et al., 2010). NNS are also believed to be more sensitive to the cravinginducing effects of smoking cues (Davies, Willner, & Morgan, 2000; Hogarth, Mogg, Bradley, Duka, & Dickinson, 2003; Watson, Carpenter, Saladin, Gray, & Upadhyaya, 2010). A number of investigations have assessed the effects of tobacco cue exposure on cigarette craving (e.g., Shiffman et al., 2013) including following the receipt of alcohol (e.g., King & Epstein, 2005). In such studies, participants are typically exposed to both neutral and tobacco salient stimuli, and subjective and/or physiological responses are monitored (Carter & Tiffany, 1999). These reactions are thought to be a form of environmental stimulus control (Shiffman & Paty, 2006), and the degree and type of craving induced by a substancerelated cue indicates how well the individual has learned that the conditioned stimulus predicts subsequent substance-use as well as other future outcomes. For dependent smokers, tobacco dependence and withdrawal is thought to play the substantive role in maintaining smoking behavior (Stolerman & Jarvis, 1995), and as a consequence, craving may not always be directly under environmental stimulus control. Although smoking cues have been shown to increase craving in dependent smokers in laboratory environments (Lazev, Herzog, & Brandon, 1999; Shiffman et al., 2013), level of dependence appears to be inversely related to the degree of smoking cue reactivity (Watson et al., 2010). Additionally, exposure to environmental stimuli does not seem to be a strong predictor of subsequent smoking behavior in natural settings for dependent smokers (Shiffman & Paty, 2006; Shiffman, Tindle et al., 2012; Shiffman et al., 2014). This may be due to a transition toward compulsive and idiographic smoking patterns as their level

Alcohol and tobacco are commonly coadministered. Although this is the case for both dependent, daily smokers (Jackson, Sher, & Wood, 2000) and nondependent, non-daily smokers (NNS; Campbell, Bozec, McGrath, & Barrett, 2012; Shiffman, Tindle et al., 2012), growing evidence suggests that this relationship may be particularly strong among NNS. For instance, epidemiological evidence suggests that compared with dependent smokers, NNS consume a greater proportion of their tobacco while drinking alcohol (Epstein, Sher, Young, & King, 2007; Harrison, Desai, & McKee, 2008; King, McNamara, Angstadt, & Phan, 2010; McKee, Harrison, & Shi, 2010; Shiffman et al., 2014). Experimental evidence suggests a similar pattern, with NNS appearing to be particularly sensitive to alcohol’s effects on cigarettes craving (King, McNamara, Conrad, & Cao, 2009; Peloquin, Hecimovic, Sardinha,

Marcel P. J. Peloquin, Department of Psychology and Neuroscience, Dalhousie University; Daniel S. McGrath, Department of Psychology, University of Calgary; Dessislava Telbis and Sean P. Barrett, Department of Psychology and Neuroscience, Dalhousie University. This research was financed by a grant through The Natural Sciences and Engineering Research Council of Canada. There are no known conflicts of interest, including financial, personal, or other relationships with other organizations or pharmaceutical/biomedical companies. The authors would also like to acknowledge the valuable assistance of Erin Wagner and Karen Hecimovic in our data collection, as well as our many volunteers. Correspondence concerning this article should be addressed to Sean P. Barrett, Department of Psychology and Neuroscience, and Department of Psychiatry, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4R2. E-mail: [email protected] 502

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ALCOHOL AND TOBACCO CUE EFFECTS ON CRAVING

of dependence increases (Edwards, 1986; Shiffman & Paty, 2006; Shiffman, Waters, & Hickcox, 2004). Moreover, evidence suggests that NNS may be more reactive to smoking cues than daily smokers (e.g., Hogarth et al., 2003; Lazev et al., 1999), and that exposure to smoking cues can increase NNSs’ subsequent smoking behavior (Schane, Glantz, & Ling, 2009; Shiffman & Paty, 2006). To date, only a few investigations have examined the extent to which acute alcohol administration affects smoking cue reactivity. An early study by Burton and Tiffany (1997) reported that alcohol increased craving in dependent smokers, and that smoking cues did not appear to further increase craving. King et al. (2010) found in NNS that tobacco cues activated the ventral striatum when given an acute dose of alcohol versus a placebo beverage, further suggesting that alcohol may function as a conditioned stimulus when paired with other substances known to release dopamine. Among a sample of dependent smokers, Field, Mogg, and Bradley (2005) found that acute alcohol administration significantly increased gaze duration toward smoking-related cues compared with a placebo beverage. The authors suggest that alcohol may selectively potentiate the maintenance of overt attention toward smoking cues, causing dependent smokers to gaze longer at cues once detected in their environment. Lastly, Sayette, Martin, Wertz, Perrott, and Peters (2005) found that both actual alcohol consumption as well as the belief that one has consumed alcohol increased the urge to smoke in both daily and NNS smokers, and that alcohol consumption itself was also associated with increased positive affect following smoking cue exposure. However alcohol did not differentially impact smoking urges in response to neutral and smoke cues. Collectively, these findings are mixed with some studies suggesting that alcohol consumption may augment tobacco cue-reactivity in NNS and others suggesting no impact. One potential concern when studying the effects of alcohol in a laboratory setting is that the consumption of a placebo beverage can produce expectancy effects related to the belief that one is consuming alcohol, a phenomenon known to influence tobacco craving (e.g., Niaura et al., 1988). Although the aforementioned studies that examined alcohol effects on smoking cue reactivity did not use a nonexpectant control group, there is evidence that at least among dependent female smokers that alcohol related changes in smoking may be linked to the perception of alcohol ingestion rather than to the pharmacological effects of alcohol (Kahler et al., 2012). In addition, neither Field et al. (2005); King et al. (2010), nor Sayette et al. (2005) distinguished alcohol effects at different points during the BAC curve. When BAC levels are rising, alcohol has stimulant-like properties, whereas sedative effects are observed at higher BAC or when levels drop during the descending limb (Pohorecky, 1977). King and Epstein (2005) found that when NNS were given either 0.4g/kg or 0.8g/kg of alcohol (approximating BACs of 0.04% and 0.08%, respectively), craving for a cigarette increased postbeverage until BAC levels peaked and were maintained up to 165 min; suggesting that alcohol continues to potentiate the desire for tobacco as BAC levels drop. Finally, some (e.g., King, Epstein, Conrad, McNamara, & Cao, 2008), though not all (e.g., Sayette et al., 2005), research findings suggest that there may be sex differences in alcohol’s effects on tobacco cue reactivity. Past research also suggests that women may be more sensitive to nonpharmacological smoking factors (Niaura et al., 1998; Perkins, Donny, & Caggiula, 1999), including visual smoking cues (Field & Duka, 2004; Heishman, Lee, Taylor, & Single-

503

ton, 2010; Knott et al., 2009; Schlagintweit, Good, & Barrett, 2014; Waters et al., 2004), yet it remains unclear the extent to which this increased sensitivity is affected by alcohol consumption. The current study examined the effects of smoking cues on craving indices in NNS following the consumption of an alcohol beverage, a placebo, and a nonexpectant control beverage. To our knowledge, it is the first to attempt to smoking cue reactivity during both the ascending and descending limbs of the BAC. We hypothesized that: (a) alcohol would increase participants’ desire to smoke cigarettes versus a placebo or control beverage, (b) the presentation of smoking cues would be associated with increased cigarette craving compared with neutral cues, (c) alcohol would potentiate the effect of smoking cues on craving, and (d) females would be more sensitive to the craving-inducing effects of smoking cues.

Materials and Methods Participants NNS were recruited via advertisement on community and Internet bulletin boards. All participants were required to score a 0 on the Fagerström Test of Cigarette Dependence (FTCD; Fagerström, 2012), be an NNS for a minimum of 6 months, smoke at least five cigarettes over the past week, and not be trying to quit smoking. They also were required to be moderate consumers of alcohol (defined as consuming a minimum of 5 drinks for men and 4 drinks for women on at least one occasion per week) and score lower than 3 on the Short Michigan Alcoholism Screening Test (SMAST; Selzer, Vinokur, & van Rooijen, 1975). Lastly, participants, who were at risk of being or becoming pregnant, who had a medical condition that alcohol use could adversely affect, or who were taking any psychiatric medications were excluded. All requirements were verified via a telephone interview prior to participation. Potential participants were informed that the study would take place over two sessions, and that for the second session, a minimum of 12-hr abstinence from both smoking and drinking alcohol prior would be required. Participants were also informed that they would receive $10 per hour as compensation.

Design The protocol consisted of a double-blind, randomized session with a 3 (beverage condition: alcohol, placebo, or control) ⫻ 2 (video condition: early smoking video or late smoking video) and time (T1 through T5) between-within subjects design. In the “early smoking video condition,” participants viewed smoking-related content during the second video showing. In the “late smoking video condition,” participants saw smoking-related content during the fourth video showing. All sessions were identical in procedure, except that participants received a different beverage-video combination. Participants were each randomly assigned to a beverage condition (3) and video condition (2) until each beverage-video combination had a minimum of 6 participants. The remaining participants were then randomly assigned to alcohol or placebo beverage conditions. The experimenter remained blind to all conditions.

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PELOQUIN, MCGRATH, AND TELBIS

Beverages. Participants were assigned to receive an alcohol, placebo, or control beverage. In the alcohol condition, participants received a beverage with 2.28 ml 50% USP units of alcohol per kilogram of body weight for women and 2.73 ml 50% USP units of alcohol per kilogram of body weight for men mixed with four parts cranberry juice (MacDonald, Baker, Stewart, & Skinner, 2000) to target a peak BAC of 0.06%. A small amount of alcohol was also smeared on the rim of their glasses on the serving tray. In the placebo beverage condition, participants’ beverage was made with five parts cranberry juice, and the glasses and tray were similarly smeared with alcohol. This was done to ensure participants in both conditions experienced the odor of alcohol and to give both beverages a similar taste. In the control condition, participants received a beverage with five parts cranberry juice with no alcohol smeared on the glasses or tray and were told that they were assigned to the control condition. To maintain integrity of the blind, research personnel, not otherwise involved with data collection, prepared and served all beverages and recorded all breath alcohol measurements. Videos. Participants were exposed to two types of 2-min long video clips; neutral or smoking. Neutral video clips contained scenes of individuals of different ages and races receiving/giving haircuts and contained no smoking or drinking imagery, and the smoking video contained scenes of individuals smoking alone or with others in a variety of different settings (e.g., office, outdoors, at a bar). Both the smoking and neutral videos have been previously used together to examine smoking cue reactivity (McBride, Barrett, Kelly, Aw, & Dagher, 2006; Schlagintweit et al., 2014). Each participant viewed three neutral clips and one smoking clip in their experimental session. Each clip was designed to match the others in terms of induced valence (McBride et al., 2006). Participants were assigned to one of two video conditions; an early video condition (where the smoking video was the second video shown, and videos 1, 3, and 4 were neutral clips), and a later video condition (where the smoking video was the final (fourth) video shown, and the first, second, and third videos were neutral clips). The timing of the videos was selected so the smoking clip would occur either during the ascending or descending limb of the BAC curve during the alcohol beverage condition. To minimize potential carryover effects, there was a 40-min lapse between the end of the early video and the start of the late video presentations (Heishman et al., 2010). To maintain blinding, all videos commenced following a short delay after the experimenter left the testing room.

Measures Subjective rating scale. An author-compiled Subjective Ratings Scale (SRS) was used to assess subjective states (head rush, stimulated, jittery, dizzy, crave cigarette, and intoxicated, relaxed, pleasant, irritable, trouble concentrating, anxious, and frustrated). Each item was rated on a 10-cm horizontal line labeled with the integers 1 to 10 and anchored with the endpoints “Not at all” and “Extremely.” Similar scales have been widely used to collect information about subjective drug effects, and this method of assessment has been shown to be reliable and valid (e.g., Wewers & Lowe, 1990) as well as sensitive to the acute effects of alcohol and tobacco (e.g., Barrett et al., 2013; Barrett, Tichauer, Leyton, & Pihl, 2006).

Questionnaire of Smoking Urges-Brief. The Questionnaire of Smoking Urges-Brief (QSU-B; Cox, Tiffany, & Christen, 2001) is a 10-item self-report measure used to assess tobacco craving across two dimensions (factor 1: intention to smoke; factor 2: withdrawal/negative affect relief), each with five Likert-scale questions with seven-point scoring sets ranging from “Strongly disagree” to “Strongly agree.” The QSU-B has been demonstrated to be sensitive for measuring nicotine, tobacco and abstinencerelated effects (e.g., Heffner, Mingione, Blom, & Anthenelli, 2011) and has been found to be an effective measure to assess tobacco craving in NNS (Davies et al., 2000). Brief Biphasic Alcohol Effects Scale. The Brief Biphasic Alcohol Effects Scale (B-BAES; Martin, Earleywine, Musty, Perrine, & Swift, 1993) is a six-item self-report measure used to assess the subjective stimulating effects of alcohol associated with rising BAC levels (factor1), and the subjective sedating effects associated with descending BAC levels (factor 2; e.g., Rueger, McNamara, & King, 2009), and has been previously shown to be sensitive to the effects of alcohol in NNS (Peloquin et al., 2013). Heart rate. Heart rate was measured using a RS-100 Polar Heart Rate Monitor (Polar Electro Canada; Lachine, Canada), and was included to verify a pharmacologic effect of alcohol (e.g., Brunelle, Barrett, & Pihl, 2007)

Procedure Prior to the experimental session, participants completed a session to provide informed consent, to complete a demographic and smoking/drinking pattern questionnaire as well to provide a nonabstinent carbon monoxide (CO) measurement. Participants were also informed that they were required to refrain from consuming alcohol or tobacco for 12 hr prior to their experimental session, as well as food and caffeine for 2 hr beforehand. An outline of experimental procedures is presented in Figure 1. Upon arrival, participants were brought into the laboratory and asked to confirm that they followed the required substance use restrictions before the session. Abstinence from alcohol was confirmed with a BAC reading of 0.00% (AK Solutions; Lansdale, PA), and abstinence from smoking with a CO reading of ⬎10 ppm (ppm; Vitalograph; Lenexa, KS). Although to our knowledge there is no known reliable CO cutoff to verify abstinence in NNS, a cutoff of ⬎10 ppm would expect to exclude those who engaged in a heavy smoking episode within 12 hr of their session (Benowitz et al., 2002). The participant was asked to complete the SRS, QSU-B, and B-BAES measures, and their average and maximum heart rate over 2 min were recorded and subsequently acted as their baseline scores [T1]. Next the participant consumed their beverage over 15 min, followed by 20 min for beverage absorption. The research assistant returned at the end of the 20 min to record the participant’s BAC. Next, the participant watched the first video clip. During the video presentation, the experimenter remotely recorded the participant’s heart rate. Once the video finished, the experimenter returned and administered the QSU-B, B-BAES, and SRS [T2]. This process was then repeated for the second video. If the participant was assigned to the early video condition, the second video would be the smoking video. After the participant viewed the second video and completed their measures [T3], they were allowed to relax in the room for 40 min. During this 40-min break, the research assistant recorded their BAC at the start of the break,

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ALCOHOL AND TOBACCO CUE EFFECTS ON CRAVING

Figure 1.

505

Timeline of experimental session in minutes.

at 20 min, and then at the end of the break. Following the break, the participant watched two more sets of videos. During each video, average heart rate was recorded, and participants completed the measures again [T4, T5]. If the participant was in the later video condition, the final video would be the smoking video. Once the participant completed their measures, they were provided a snack and required to remain in the laboratory for at least an hour (until their BAC reached 0.04%). They were then sent home via taxi or experimenter escort and compensated. The experimental sessions lasted approximately 3 hr.

Statistical Analysis A repeated measure analysis of variances (ANOVA) with an experimental alpha of .05 was used to determine if demographic, alcohol, and/or tobacco use differences existed between male and female participants assigned to each beverage condition. The remaining data were analyzed using linear mixed models (LMM) in SPSS version 20.0 for Windows (SPSS Inc.; Chicago, IL). In contrast with general linear model repeated-measures ANOVA, the LLM method calculates F-statistics using a restricted maximum-likelihood approach, which permits deviations from compound symmetry and the inclusion of cases with missing values (Gueorguieva & Krystal, 2004). An appropriate covariance structure was selected for each variable on the basis of model simplicity and of the likelihood ratio test. Tests of simple main effects were conducted on linearly independent pairwise comparisons between the estimated marginal means. For interactions, the simple main effects of variables within each level combination of the other variable(s) were tested. The measures analyzed were the aggregates of QSU-B factor 1 scores, QSU-B factor 2 scores, B-BAES factor 1 scores, B-BAES factor 2 scores, each of the SRS items, and average heart rate. Data was analyzed using sex, beverage (alcohol, placebo, or control), and video (early, late) as fixed factors; time as a repeated and fixed factor; and subject as a random factor, with baseline scores serving as time-varying covariates for the remaining time points. Effects of interest were the main effects of beverage and interactions with sex, beverage, and video with time. For interactions, the simple effects of variables within each level combination of the other variable(s) were tested. BAC levels in the alcohol beverage condition were also analyzed using similar LMM analyses, with the exception that video and

beverage conditions were not included as factors in the analyses, and main effects and interactions involving time and sex were the outcomes of interest. To account for multiple testing, family wise Bonferroni corrections were applied.

Results Participants Forty-nine male and 50 female NNS who were moderate drinkers completed the experiment. Participant demographic and tobacco and alcohol use history data are recorded in Table 1. The only differences that were evident were weekly number of alcohol drinks F(2, 99) ⫽ 7.572, p ⫽ .007 (M ⫽ 23.2, SE ⫽ 1.8 for males and M ⫽ 16.1, SE ⫽ 1.8 for females) between males and females. Table 2 presents the distribution of participants across the different video/beverage conditions.

Baseline Abstinence and Alcohol Administration Verification All participants reported being abstinent from tobacco for at least 12 hr before their experimental session. The average nonabstinent CO reading was 4.41 ppm (SE ⫽ 0.70) during the baseline session, and 2.79 (SE ⫽ 0.22) at the start of the experimental session, reflecting a significant decrease t(98) ⫽ 2.46, p ⫽ .016. All participants had a BAC of 0.00% at the beginning of the experimental session. Two male participants had post alcohol BAC readings greater than 3 standard deviations above the sample mean and were thus excluded from the BAC analysis. Although these participants’ BAC readings disproportionately impacted the BAC curve, none of the other reported findings were significantly impacted by their inclusion/exclusion of these participants from the analyses. Average BAC at 20 min was 0.053 (SE ⫽ 0.004), 0.050 (SE ⫽ 0.004) at 40 min, 0.049 (SE ⫽ 0.004) at 60 min, and 0.047 (SE ⫽ 0.004) at 80 min for participants assigned to the alcohol condition. A significant effect of time F(3, 96.674) ⫽ 4.121, p ⫽ .009 showed that BAC levels at 40 and 60 min were significantly greater (ps ⬍ .006) than at 20 min, and that levels at 80 min were lower than at 60 min (p ⫽ .049). No main effect of sex

PELOQUIN, MCGRATH, AND TELBIS

506 Table 1 Sample Characteristics

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Males

N Age Age of first smoking Days smoked in past 30 Cigarettes per smoking day Cigarettes in the past week Age of first drinking Drinking episodes per week Drinks per week

Females

Bev

Alcohol

Placebo

Control

Alcohol

Placebo

Control

Sex

p

Sex ⫻ Bev

17 23.2 (1.6) 15.1 (0.7) 15.1 (1.6) 1.5 (0.3) 10.5 (2.4) 15.0 (0.6) 2.7 (0.3) 22.2 (3.1)

20 26.0 (1.5) 15.2 (0.7) 14.6 (1.5) 2.1 (0.3) 14.5 (2.2) 14.4 (0.6) 2.9 (0.3) 21.4 (2.8)

12 22.6 (2.0) 13.7 (0.9) 14.9 (1.9) 1.8 (0.4) 12.6 (2.8) 13.0 (0.7) 3.0 (0.4) 26.1 (3.7)

20 21.8 (1.5) 16.2 (0.7) 14.6 (1.5) 1.8 (0.3) 12.6 (2.2) 14.5 (0.6) 2.8 (0.3) 19.6 (2.8)

18 25.1 (1.6) 15.2 (0.7) 13.7 (1.6) 1.7 (0.3) 12.2 (2.3) 13.2 (0.6) 2.1 (0.3) 13.0 (3.0)

12 24.3 (2.0) 15.5 (0.9) 14.3 (1.9) 2.1 (0.4) 14.5 (2.8) 13.8 (0.7) 3.1 (0.4) 15.7 (3.7)

.873 .123 .616 .804 .786 .554 .520 .007ⴱ

.157 .445 .903 .626 .642 .089 .246 .373

.651 .492 .988 .559 .557 .360 .357 .441

Note. Mean group demographic values separated by sex and beverage condition (SE). No group differences were detected between participants assigned to each beverage condition, and only the number of alcoholic drinks per week differed between men and women. ⴱ p ⬍ .05.

(p ⫽ .534) or interaction with time (p ⫽ .082) detected any difference between male and female BAC levels at each time point (see Figure 2).

Heart Rate A main effect for beverage F(2, 79.072) ⫽ 9.478, p ⬍ .001 was found for average heart rate, with individuals assigned to the alcohol condition having higher postbeverage average heart rates throughout the experiment. No main effects or interactions involving time, video condition, or sex were evident.

Subjective Responses Cigarette craving. Cigarette craving was assessed using the SRS item “crave cigarette,” as well as two craving factors from the QSU-Brief (factor 1: intention to smoke; factor 2: withdrawal/ negative affect relief). An interaction of video ⫻ time was detected for SRS crave cigarette F(3, 87) ⫽ 5.164, p ⫽ .002, where craving was rated higher at T5 in the later video condition (M ⫽ 5.0, SE ⫽ 0.35) than the early smoking video condition (M ⫽ 3.9, SE ⫽ 0.33; p ⫽ .037). As well, in the early smoking video, participants reported higher crave cigarette scores at T3 (during the smoking video; M ⫽ 4.2, SE ⫽ 0.28) than at T2 (M ⫽ 3.8, SE ⫽ 0.28; p ⫽ .022). In the later smoking video, participants reported greater scores at T5 (during the smoking video; M ⫽ 5.0, SE ⫽ 0.35) than at T2 (M ⫽ 4.0, SE ⫽ 0.29; p ⬍ .001), T3 (M ⫽ 4.0, SE ⫽ 0.29; p ⫽ .001), and T4 (M ⫽ 3.9, SE ⫽ 0.31; p ⬍ .001). A beverage ⫻ sex interaction F(2, 86.166) ⫽ 4.255, p ⫽ .017 indicated that

females assigned to the alcohol condition reported greater crave cigarette levels (M ⫽ 5.3, SE ⫽ 0.41) compared with females assigned to the placebo (M ⫽ 3.8, SE ⫽ 0.42; p ⫽ .013) and control (M ⫽ 3.5, SE ⫽ 0.53; p ⫽ .006) conditions, as well as males assigned to the alcohol condition (M ⫽ 3.6, SE ⫽ 0.45; p ⫽ .005; Figure 3a). An interaction of video ⫻ time was detected for QSU-B factor 1 craving (intension to smoke) F(3, 87) ⫽ 5.201, p ⫽ .002 indicating that participants in the early video condition reported higher factor 1 craving at T3 (M ⫽ 19.9, SE ⫽ 0.89) compared with T2 (M ⫽ 17.6, SE ⫽ 0.76; p ⬍ .001) or T4 (M ⫽ 18.2, SE ⫽ 0.86; p ⫽ .018), and those assigned to the later video condition reported higher factor 1 craving at T5 (M ⫽ 20.0, SE ⫽ 1.01) compared with T2 (M ⫽ 18.0, SE ⫽ 0.80; p ⫽ .014), T3 (M ⫽ 17.8, SE ⫽ 0.94; p ⫽ .007), or T4 (M ⫽ 18.2, SE ⫽ 0.86; p ⬍ .001). A trend was also detected for beverage ⫻ sex F(2, 86.240) ⫽ 3.460, p ⫽ .036, where females assigned to the alcohol beverage condition (M ⫽ 22.0, SE ⫽ 1.21) reported higher factor 1 craving than females assigned to the placebo (M ⫽ 17.5, SE ⫽ 1.28; p ⫽ .013) and control (M ⫽ 19.4, SE ⫽ 1.57, p ⫽ .002; Figure 3b). No effects of beverage or interactions of time with beverage, video, and/or sex were evident for QSU-B factor 2 craving (negative affect/withdrawal relief).

Post---beverage BAC

0.058 0.056

Average

0.054

Males

0.052

Females

0.05 0.048

Table 2 Number of Participants in Each Condition

0.046 0.044 0.042

Beverage condition Video condition Video 1 Video 2

Sex Sex

Male Female Total Male Female Total

0.04

Alcohol

Placebo

Control

Total

9 10 19 8 10 18

12 10 22 8 8 16

6 6 12 6 6 12

27 26 53 22 24 46

0

20

40

60

80

Minutes post beverage

Figure 2. Average BAC levels for participants assigned to the alcohol condition postbeverage, as well as average BAC levels for males and females. BAC readings remained at 0.00% throughout both placebo and control beverage conditions. Error bars (SEM) for average BAC values at each time point are displayed.

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ALCOHOL AND TOBACCO CUE EFFECTS ON CRAVING

507

Figure 3. Interactions of beverage ⫻ sex for both “crave cigarette” and QSU-B factor 1 craving. Note. ⴱ p ⬍ .36.

Alcohol effects. Prototypic effects of alcohol were examined by using the B-BAES factor 1 (stimulating) and factor 2 (sedating) scores, as well as the SRS item “intoxicated.” A video ⫻ time interaction F(3, 87) ⫽ 3.810, p ⫽ .013 revealed that participants reported greater B-BAES factor 2 scores at T2 (neutral video) (M ⫽ 11.7, SE ⫽ 0.58) compared with T3 (smoking video) in the early smoking video condition (M ⫽ 10.5, SE ⫽ 0.65; p ⫽ .006). Participants also reported higher factor 2 scores at T3 (neural video) and T4 (neural video; M ⫽ 11.8, SE ⫽ 0.81) compared with T5 (smoking video) in the later smoking video condition (M ⫽ 9.9, SE ⫽ 0.75; p ⫽ .017, p ⫽ .001, respectively). No significant effects for B-BAES factor 1 scores were detected. A main effect of beverage was detected for “intoxicated” F (2, 86.140) ⫽ 31.522, p ⬍ .001, with participants in the alcohol condition (M ⫽ 3.5, SE ⫽ 0.20) reporting being more intoxicated than those in the placebo (M ⫽ 2.1, SE ⫽ 0.20; p ⬍ .001) and control (M ⫽ 1.1, SE ⫽ 0.20; p ⬍ .001) conditions. Participants in the placebo condition reported being more intoxicated than those in the control condition (p ⫽ .003). A Beverage ⫻ time interaction was found F(6,87) ⫽ 7.736, p ⬍ .001 where at T2, participants assigned to the alcohol condition (M ⫽ 4.6, SE ⫽ 0.24) report

being more intoxicated than those in the placebo (M ⫽ 2.3, SE ⫽ 0.24; p ⬍ .001) and control condition (M ⫽ 1.2, SE ⫽ 0.30; p ⬍ .001), and those in the placebo condition also report being more intoxicated than those in the control condition at T2 (p ⫽ .003). At T3, participants in the alcohol condition (M ⫽ 4.2, SE ⫽ 0.24) reported being more intoxicated than those in the placebo condition (M ⫽ 2.5, SE ⫽ 0.24; p ⬍ .001) or the control condition (M ⫽ 1.2, SE ⫽ 0.30; p ⬍ .001). As well, those in the placebo condition also reported being more intoxicated than those in the control condition (p ⫽ .001). At T4, those in the alcohol condition (M ⫽ 2.9, SE ⫽ 0.21) reported being more intoxicated than those in the placebo (M ⫽ 1.7, SE ⫽ 0.21; p ⬍ .001) or control (M ⫽ 1.0, SE ⫽ 0.26; p ⬍ .001) conditions. As well, at T5 participants in the alcohol condition (M ⫽ 2.4, SE ⫽ 0.20) reported being more intoxicated than those in the placebo (M ⫽ 1.7, SE ⫽ 0.20; p ⫽ .008) or control (M ⫽ 1.0, SE ⫽ 0.25; p ⬍ .001) conditions. Additionally, participants in the alcohol condition reported feeling more intoxicated at T2 compared with T3 (p ⫽ .004), T4 (p ⬍ .001), or T5 (p ⬍ .001), at T3 compared with T4 (p ⬍ .001) or T5 (p ⬍ .001), as well as at T4 compared with T5 (p ⫽ .003). Participants in the placebo condition reported feeling more intox-

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icated at T2 compared with T4 (p ⫽ .002) and T5 (p ⫽ .002), as well as at T3 compared with T4 (p ⬍ .001) and T5 (p ⬍ .001). Other subjective effects. A video ⫻ time interaction for relaxed revealed that relaxed ratings at T5 were lower in the late video condition (M ⫽ 5.9, SE ⫽ 0.26) compared with the early video condition (M ⫽ 6.7, SE ⫽ 0.25; p ⫽ .034). Relaxed ratings were also lower at T5 during the early video condition compared with T4 (M ⫽ 7.0, SE ⫽ 0.23; p ⫽ .036), and relaxed scores were lower at T5 during the late video condition compared with T2 (M ⫽ 7.1, SE ⫽ 0.21; p ⬍ .001), T3 (M ⫽ 7.1, SE ⫽ 0.19; p ⬍ .001), or T4 (M ⫽ 6.8, SE ⫽ 0.25; p ⬍ .001) late condition scores. No significant main effects of beverage or additional interactions involving time were detected for any SRS items.

Discussion The purpose of our study was to further examine alcohol’s influence on cue-induced craving in NNS. Overall, participants experienced increased intentions to smoke as well as a general craving to smoke— but not withdrawal-related craving—when they were exposed to videos of other people smoking. This result is consistent with the findings of Davies et al. (2000) that NNSs displayed an increased desire to smoke for positively reinforcing properties, but not negatively reinforcing properties, when they were exposed to a lit cigarette. Moreover, consistent with the findings of Burton and Tiffany (1997) and Sayette and colleagues (2005), no interactions between alcohol and presentation of the smoking cues on cigarette craving were evident in the present study. This suggests that alcohol likely impacts tobacco craving through mechanisms beyond its effects on smoking-salient stimuli processing. Perhaps, somewhat more surprisingly, our findings also suggest that women may be especially susceptible to alcohol’s effects on cigarette craving regardless of smoking video presentation. Previous research suggests that alcohol should increase NNS’ cigarette craving throughout the BAC. For instance, King and Epstein (2005) gave NNS either a high dose (0.8g/kg) or a low dose (0.4g/kg) of alcohol versus a placebo beverage without exposure to smoking cues, and then asked participants to rate their cigarette craving during both the ascending and descending limb of the BAC curve. They found that both alcohol groups showed an increase in their intention to smoke, which was maintained throughout the BAC. Epstein and colleagues (2007) also found the same effect when light and heavy tobacco chippers were given either a low or high dose of alcohol. However, neither of these studies simultaneously presented participants with smoking cues during the alcohol challenge, nor noted if there were any sex differences. When Sayette et al. (2005) exposed tobacco chippers to a smoking cue post- alcohol or placebo beverage, they found that both beverages increased ratings of desire to smoke before the smoking cue, and that postcue craving ratings increased while BAC levels were rising. Sayette and colleagues also reported on the effects of sex, and none were evident. It is possible that differences in alcohol doses, sample characteristics, cue properties, or other methodological factors (e.g., use of a control beverage) account for these discrepant findings. King and colleagues (2008) compared men and women’s alcohol-induced tobacco craving and

found stronger associations in women. They speculated that women may be more sensitive to exteroceptive factors to smoke than men. This is consistent with evidence that among dependent female smokers, alcohol related craving appears to be more affected by the belief that alcohol has been consumed rather than the pharmacological properties of alcohol itself (Kahler et al., 2012). One potential explanation for the present finding of an alcohol effect in female smokers specifically is that alcohol and tobacco associations may be more rapidly acquired in women than in men. A stronger association between contextual factors such as drinking with smoking in females may in part be why women have greater difficulty quitting smoking than men(McDermott, Dobson, & Owen, 2009). Another reason for the difference may be hormonal, as animal models suggest that high estrogen levels facilitate acquisition of substance pairings (for a review, see Dalla & Shors, 2009); however, examining these factors are beyond the scope our study. Regardless of the specific mechanisms involved, the present findings suggest a continued need to examine potential sex differences in alcohol-tobacco co-use. It is also worth noting that we did not find differences in craving during different time points during BAC. Individual differences in the effects of alcohol are known to be both dose and time dependent (Holdstock & Wit, 1998). In the present study, participants’ BAC peaked during the break, and began to drop before being exposed the second set of video cues. Although increases in subjective effects of stimulation are often conceptualized as being exclusive to the ascending BAC, stimulating effects have been shown to remain throughout the curve with the peak occurring approximately by 40 – 45 min postbeverage (at the time of the break) and remain elevated for at least another hour, whereas sedative effects are known to slowly emerge over a 90-min period (Brunelle et al., 2007); Hendler, Ramchandani, Gilman, & Hommer, 2013). Since our final BAC level is sampled 80 min postbeverage consumption, it is possible that we did not adequately capture true descending limb effects. There are several potential limitations to consider when interpreting the results of the current study. First, the experiment took place in a controlled research environment instead of a setting where participants would normally smoke, thereby reducing ecological validity. In addition, beverages were consumed over 15 min without the opportunity to consume additional beverages, which is not typical of normal drinking behavior. It is also unknown how the level of social contact in the study would have affected cigarette craving, but NNS frequently consume alcohol and tobacco in the presence of others (Shiffman, Dunbar, Scholl, & Tindle, 2012; Shiffman et al., 2014). Our experiment also lacked an opportunity for participants to smoke during the study. Smoking throughout the experiment would be expected to impact subsequent cue exposures, and therefore was not included in our design. However, King and colleages (2009) reported that while alcohol increased cigarette craving across male and female smokers, it only increased actual smoking behavior in males. Such findings suggest that the present craving findings may not generalize to actual smoking behavior. As well, increasing the length of time participants waited between the second and third video would have ensured that all participants’ BAC had increased, plateaued, and subsequently begun to descend. However, doing so may have increased participants’ boredom, which is also known to increase cigarette cravings (Copeland, Brandon, & Quinn, 1995). Addition-

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ALCOHOL AND TOBACCO CUE EFFECTS ON CRAVING

ally, our experiment lacked a dependent smoker comparison group. Past research suggests that NNS may be more sensitive than dependent smokers to the effects of alcohol (e.g., Peloquin et al., 2013) and tobacco cues (e.g., Watson et al., 2010) on craving; however, we are unable to make inferences about such potential group differences in the present study given our sample. Last, it is possible that the experiment was underpowered to detect complex interaction effects, and a larger sample size may have revealed more subtle effects. In conclusion, the most novel outcome of our study was the finding that female NNS appear to be more strongly influenced by alcohol-induced tobacco craving than males. It is possible that either biological differences (e.g., hormonal influences) or gender differences related to social aspects of smoking and drinking co-use may have contributed to these differences. Future work should further explore these possibilities.

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Received June 13, 2014 Revision received September 13, 2014 Accepted September 15, 2014 䡲