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Explicit and implicit heroin-related cognitions and heroin use among patients receiving methadone maintenance treatment
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ScienceDirect Comprehensive Psychiatry 56 (2015) 155 – 160 www.elsevier.com/locate/comppsych
Explicit and implicit heroin-related cognitions and heroin use among patients receiving methadone maintenance treatment Peng-Wei Wang a, b , Huang-Chi Lin a, b , Hung-Chi Wu d , Chih-Yao Hsu d , Kuan-Sheng Chung d , Chih-Hung Ko a, b, c,⁎, 1 , Cheng-Fang Yen a, b,⁎, 1 a
Department of Psychiatry, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan Department of Psychiatry, Faculty of Medicine and Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan c Department of Psychiatry, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan d Departments of Addiction Science, Kai-Suan Psychiatric Hospital, Kaohsiung, Taiwan
b
Abstract Background: Craving is an important issue in substance use disorder. To achieve a better understanding of the cognitive processing systems of craving, the cognitive processes of craving have been considered as two distinct processes. One system, based on rule-based inferences and named explicit cognition, is more conscious and effortful. The other system, based on prior learned association and named implicit cognition, is unconscious and effortless. How explicit and implicit cognitions are associated with heroin use in patients with methadone maintenance treatment (MMT) is not clear. This study aimed to explore the relationship between explicit and implicit cognition and heroin use in patients undergoing MMT. Method: This study recruited one-hundred forty intravenous heroin users. The participants were invited to provide social–demographic data, the severity of substance dependence and explicit cognition with regard to heroin. Then, participants completed a computerized test to assess implicit cognition with regards to heroin. Results: This study found that explicit and implicit heroin-related cognitions were associated with the frequency of heroin use. There was an interaction effect between implicit and explicit cognition on the frequency of heroin use. This study also found that higher explicit heroin-related cognition was a risk factor for continuing heroin use. Conclusion: Both explicit and implicit cognitions were associated with the frequency of heroin use in patients undergoing MMT, but only explicit cognition was associated with whether patients could stop using heroin during MMT. Therefore, the status of heroin use in patients undergoing MMT may be related to different cognitive processes. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Craving is becoming more and more important in terms of conceptualizing and treating substance use disorder because it can destabilize patients seeking treatment for substance abuse [1] and has been used as a criterion of substance use disorder in the DSM-5 [2]. To achieve a better understanding of the cognitive processing systems of craving involved in initiation and escalation of substance use, scholars have ⁎ Corresponding authors at: Department of Psychiatry, Kaohsiung Medical University Hospital, 100 Tzyou 1st Road, Kaohsiung 807, Taiwan. Tel.: +886 7 312 4941; fax: +886 7 3134761. E-mail address: [email protected] (C.-F. Yen). 1 Cheng-Fang Yen, MD., PhD and Chih-Hung Ko, MD., PhD contributed equally to the work. http://dx.doi.org/10.1016/j.comppsych.2014.08.047 0010-440X/© 2014 Elsevier Inc. All rights reserved.
considered the cognitive processes of craving as two distinct processes [3–5]. One system, based on rule-based inferences and named explicit cognition, enables quickly learning the representation of unique or novel event and is more conscious and effortful. The other system, based on prior learned association and named implicit cognition, enables slow learning of general regularities and is unconscious as well as effortless. A meta-analysis study by Rooke and colleagues showed that implicit substance-related cognition is significantly associated with substance use [6]. Research has also found that explicit heroin-related cognition may be associated with illicit heroin use in patients receiving methadone maintenance treatment (MMT) [7]. Furthermore, a previous study on former heroin users demonstrated that the level of explicit heroin-related cognition did not increase after exposure to
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heroin-related and neutral cues, but the blood oxygen-level dependence intensity on MRI increased when the participants were exposed to heroin-related, not neutral, cues [8]. The results of previous studies imply that not only explicit heroin-related cognition but also implicit cognition may play a role in heroin-related craving in heroin users. Heroin use is an important clinical issue because heroin users usually suffer from a chronic relapsing course, as well as a lots of adverse social and health consequences, criminal activities, reliance on social services, and blood-borne infections [9,10]. MMT can improve heroin users' quality of life [11] and reduce their criminal activities [12]. However, although MMT can reduce the severity and frequency of heroin use, 30 to 70% of heroin users receiving MMT still cannot stop using heroin [13–16]. Because of the significant associations of both explicit and implicit cognitions with substance use found in previous studies [6,7,17], further study of the relationship of explicit and implicit cognition with continuous heroin use among heroin users receiving MMT is important. This study aimed to explore the relationships of explicit and implicit heroin-related cognitions with continuous heroin use and without heroin use among heroin users receiving MMT in Taiwan. We also explored whether the interaction between explicit and implicit cognition is associated with current heroin use and abstinence of heroin. We hypothesized that among heroin users receiving MMT: (a) explicit and implicit heroin-related cognitions that are unfavorable to heroin use are associated with whether patients can keep abstinence of heroin or not; (b) explicit and implicit unfavorable heroin-related attitudes may interact with each other in terms of their relationship with abstinence from heroin use; (c) explicit and implicit heroin related cognitions that are unfavorable to heroin use are associated with frequency of current heroin use in patients with MMT and continuing heroin use; (d) the relationships of explicit and implicit unfavorable heroin-related cognitions with frequency of heroin use may interact with each other in the continuing heroin use group.
2. Methods 2.1. Participants This study recruited intravenous heroin users who visited the MMT clinics of Kaohsiung Medical University Hospital and Kai-Suan Psychiatric Hospital. All were opioiddependent: psychiatrists conducted a diagnostic interview based on the Structured Clinical Interview for DSM-IV for Axis I Disorders (SCID) to determine the diagnosis of heroin dependence. They also must have been taking a stable dosage of methadone for more than 1 month. Heroin users who conformed to the criteria described above were recruited into this study. The Institutional Review Board of Kaohsiung Medical University and Kai-Suan Psychiatric Hospital approved the study protocol.
2.2. Measures 2.2.1. Socio-demographic characteristics Participants' sex, age and age of initial heroin use were recorded. 2.2.2. The Chinese version of the Severity of Dependence Scale (SDS [Ch]) The 5-item SDS [Ch] was used to evaluate participants' severity of heroin dependence [18,19]. Each item is scored on a four-point scale (scored 0 to 3). The total SDS score ranges from 0 to 15, higher scores indicating a greater degree of dependence. Cronbach's α of the SDS [Ch] in this study was 0.78. 2.2.3. Visual Analogue Scale (VAS) This study used a VAS with scores from 0 to 100 (none to very much) to measure explicit heroin-related cognition. The VAS includes the following question modified from Cullbertson et al. [20] and Sinha et al. [21]: “How much do you crave/desire/want heroin right now? “ 2.2.4. The Computerized Implicit Association Test (IAT) for heroin cues In presenting the IAT to the participants, we closely followed the procedure described by Greenwald [22]. The target discrimination is heroin-related cues vs. neutral cues, and the attribute discrimination is pleasure vs. aversion. We used liked vs. disliked as attribute labels because these categories are strongly associated with inner motivation. The stimulus material consisted of 6 heroin-related cues (pictures) and 6 neutral cues (pictures) as well as 6 liked (e.g., “lucky, relaxed, pleasure, beauty, active, optimistic”) and 6 disliked words (e.g., “doom, stress, depression, ugly, passive, pessimistic”). Phase 1 consisted of 24 trials in which heroin-related and neutral pictures were presented. During phase 2, liked and disliked words were presented in 24 trials. Phase 3 consisted of two blocks of 48 trials, during which each word or picture was presented twice. The liked word and heroin-related pictures were classified to the left side in the 48 trials. Phase 4 was identical to 2, except that the heroin-related pictures were classified to the right side and neutral pictures were classified to the left side. Phase 5 consisted of two blocks of 48 trials, during which each word or picture was presented twice. The liked words and neutral pictures were classified to the left side in the 48 trials. The IAT score was calculated as the difference in score between the mean response times of the heroin-liked/neutral-disliked block and the neutral-liked/heroin-disliked block, with larger scores indicating stronger automatic approach motivation toward heroin. The IAT score was calculated according to the D-measure algorithm suggested by Greenwald [23]. 2.2.5. Heroin use and methadone treatment characteristics The current dosage of methadone, result of morphine urine examination and self-reported heroin use were recorded. Those who have abstained and did not abstain from heroin use during MMT were classified as the abstinent
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and non-abstinent groups, respectively. The frequency of heroin use was also collected for the non-abstinent group. 2.3. Procedure and statistical analysis Trained research assistants introduced the purpose and procedures of the present study to those who agreed to participate in this study. Informed consent was obtained from all participants prior to commencement of the study. Participants were invited to complete the research questionnaires described above first. Then, the participants completed the computerized test to assess implicit heroinrelated cognition. The abstinent groups were patients without self-reported heroin use and negative heroin urine test. The background characteristics of the participants were compared between the abstinent and non-abstinent groups during MMT using the χ 2 test and Student's t test. The paired t test was used to examine the differences between the reaction time to the heroin + liked words and heroin + disliked words. Student's t test was used to determine the difference in the reaction time of the IAT between the abstinent and non-abstinent groups during MMT. We used a generalized linear model to determine the relationship (1) between explicit heroinrelated cognition and frequency of current heroin use for non-abstinent patients; (2) between explicit heroin-related cognition and abstinence from heroin; (3) between implicit heroin-related cognition and frequency of heroin use for nonabstinent patients; and (4) between implicit heroin-related cognition and abstinence from heroin. We also explored the associations of the interactions between explicit and implicit cognition and frequency of current heroin use and abstinence from heroin. We made inferences at the 0.05 level of significance for inferential statistical procedures and used Holm–Bonferroni method to counteract the problem of multiple comparisons [24].
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3. Results One-hundred forty users receiving MMT participated in this study. Of them, 8 patients (5.70%) were female heroin users. According to current heroin use or not, the participants were classified into the abstinent (n = 48, 34.30%) and nonabstinent (n = 92, 65.70%) groups. In addition, the average frequency of heroin use for the past week was 17.17 (15.75) times per week. None of abstinent patients and one of nonabstinent patients (2.1%) had cocaine use. There was no group difference in cocaine use (χ 2 = 1.930; p = .165). The patients with tetrahydrocannabinol (THC) use were four in abstinent (8.33%) and seven in non-abstinent (7.61%). The rate of THC use did not differ from each group (χ 2 = 0.023; p = .880). Eleven of abstinent patients had alcohol use (22.92%) at least once per week and thirty of the non-abstinent patients had used alcohol one or more times per week. The rate of alcohol use did not differ between groups (χ 2 = 1.431; p = .232). Smoking was common in both groups (97.92% for abstinent and 97.83% for non-abstinent) without group difference (χ 2 = 0.001; p = .972). The results of comparing gender, age, age of first heroin use, severity of heroin dependence on the SDS [Ch], explicit cognition with regards to heroin on the VAS, and implicit cognition with regards to heroin determined by the reaction time to the heroin + liked words and to the heroin + disliked words between the abstinent and non-abstinent groups are shown in Table 1. The mean (standard deviation [SD]) of the severity of heroin dependence measured by the SDS in the abstinent and non-abstinent groups was 5.35 (3.33) and 7.98 (2.89), respectively. The result showed that the severity of heroin dependence was higher in the non-abstinent than in the abstinent group (t = −4.822, df = 137, p b .001). The mean (SD) of the level of explicit attitudes to heroin measured by the VAS in the abstinent and non-abstinent groups was 11.67 (15.48) and 38.88 (26.35), respectively. There was a more
Table 1 The comparisons of social–demographic, severity of dependence, explicit and implicit cognitions between abstinence and non-abstinence group.
Sex (female)
Age (years) Age at first heroin use (years) Severity of heroin dependence a Methadone dosage (mg) Reaction time to heroin pictures and liked items (seconds) b Reaction time to heroin pictures and disliked items (seconds) b Explicit cognition c Implicit cognition b (D score) a b c
Measured by the Substance Dependence Scale. Measured by the Implicit Association Test. Measured by the Visual Analog Scale.
Abstinence group (n = 48) n (%) 5 (10.42)
Non-abstinence group (n = 92) n (%) 3 (3.30)
Mean (SD)
Mean (SD)
42.86 (7.73) 25.85 (6.48) 5.35 (3.33) 55.57 (28.39) 1.13 (0.45) 1.20 (0.49) 11.67 (15.48) 0.18 (1.06)
42.00 (6.25) 26.44 (7.71) 7.98 (2.89) 41.06 (37.78) 1.03 (0.40) 1.12 (0.41) 38.88 (26.35) 0.08 (0.98)
p value
.124
.479 .654 b.001 .021 .203 .335 b.001 .553
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positive explicit attitude in the non-abstinent group than in the abstinent group (t = −6.57, df = 137, p b .001). The difference in the mean reaction time to the heroin pictures + liked items and the heroin pictures + disliked items for the abstinent group was not significant (paired t = −1.44, df = 47, p = .156). However, the mean reaction time of the heroin pictures + liked items was significantly shorter than that of the heroin pictures + disliked items for the non-abstinent group (paired t = −2.27, df = 90, p = .026). There was no significant correlation between implicit heroin related cognition and VAS for the non-abstinent group (Pearson correlation coefficient = −0.05, p = .619) and for the abstinent group (Pearson correlation coefficient = −0.224, p = .126). The frequency of heroin use was significantly positively related to the severity of heroin dependence (Spearman correlation coefficient = 0.266, p = .011) and negatively related to the dosage of methadone (Spearman correlation coefficient = −0.299, p = .004) in the non-abstinent group after corrections of multiple comparisons. There was a significant positive correlation between the frequency of heroin use and implicit heroin-related cognition (D values) (Spearman correlation coefficient = 0.237, p = .024) after corrections of multiple comparisons. Furthermore, the correlation between frequency of heroin use and explicit heroin-related cognition tended to be significant (Spearman correlation coefficient = 0.204, p = .052) after corrections of multiple comparisons. The results of examining the relationships of explicit and implicit cognition with abstinence from heroin use in heroin users receiving MMT are shown in Table 2. The results indicated that more favorable explicit but not implicit cognition toward heroin use was significantly associated with non-abstinence from heroin (continuing heroin use) during MMT. There was no interaction effect between explicit and implicit cognition on abstinence from heroin. Furthermore, the results of examining the relationships of explicit and implicit cognition with the frequency of current Table 2 The associations of explicit and implicit cognition with abstinence from heroin use in heroin users receiving methadone maintenance treatment. Model I OR Sex (0: female; 1: male) Age at first heroin use Severity of heroin dependence a Methadone dosage Explicit cognition b Implicit cognition c Explicit × implicit cognition
Model II
p value OR
1.550 .680 1.059 .106 1.252 .008 .987 .070 1.067 b.001
Model III
p value OR
3.095 .209 1.023 .424 1.343 b.001 .993
.183
.908
.635
OR: odds ratio. a Measured by the Substance Dependence Scale. b Measured by the Visual Analog Scale. c Measured by the Implicit Association Test.
1.253 1.057 1.249
p value .835 .128 .009
.987 .061 1.070 b.001 .920 .811 1.013 .294
heroin use in the non-abstinent group are shown in Table 3. The results indicated that both explicit and implicit heroinrelated cognitions were positively associated with the frequency of heroin use. There was a positive interaction effect between implicit and explicit heroin-related cognition.
4. Discussion There were several important findings in this study. The first was that heroin users receiving MMT who have more favorable explicit cognition toward heroin use were less likely to maintain abstinence. Second, both heroin-related explicit and implicit cognitions were positively associated with frequencies of heroin use in non-abstinent patients. Third, regarding the frequencies of heroin use, the heroin-related explicit and implicit cognitions interacted with each other in a synergic way. Explicit cognition, and not implicit cognition, was associated with whether heroin users were able to stop using heroin or not. Furthermore, implicit cognition did not change the association between the explicit attitude to and abstinence from heroin because there was no interaction effect between implicit and explicit cognition. Robinson et al. [25] suggested that the explicit or implicit cognitive process that the substance user chooses to apply can influence their substance-using behavior. Based on incentive sensitization theory, explicit cognition is essential to explain why substance users engage in behavior to procure a drug [26]. Tiffany argued that implicit cognition is involved in consuming a drug, not procuring a drug [27]. Therefore, explicit attitude plays a major role in whether patients can maintain abstinence or not. Our results also supported this idea, because only explicit attitudes were associated with whether the participant was abstinent or not. Our results also showed that the levels of implicit heroinrelated cognition were not different between the nonabstinent and abstinent heroin users during MMT. The results of the study by Marhe et al. [28] showed that the level of implicit heroin-related cognition did not differ between non-abstinent and abstinent heroin users during inpatient detoxification treatment. Geng et al. [29] showed that the level of implicit heroin-related cognition was not different between heroin users who received and did not receive MMT. The results of this and previous studies imply that MMT may not influence the level of implicit cognition with regards to heroin use. Furthermore, this study found that non-abstinent heroin users had a more favorable explicit cognition toward heroin use than the abstinent participants during MMT in the outpatient setting; meanwhile, after controlling for the effects of age, gender, level of education and severity of heroin dependence, more favorable explicit cognition was associated with a higher frequency of heroin use in non-abstinent heroin users during MMT in the outpatient setting. The result of this study was not in line with that of Marhe et al. [28], in which it was shown that
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Table 3 The relationships of explicit and implicit cognition with the frequency of current heroin use in heroin users receiving methadone maintenance treatment. Model I
Sex (0: female; 1: male) Age at first heroin use Severity of heroin dependence a Methadone dosage Explicit cognition b Implicit cognition c Explicit × implicit cognition a b c
Model II
Model III
Coefficient
p value
Coefficient
p value
Coefficient
p value
2.356 .994 1.053 .990 1.008
b.001 .066 b.001 b.001 b.001
2.361 .989 1.077 .990
b.001 .001 b.001 b.001
1.202
b.001
1.972 .989 1.044 .990 1.007 1.107 1.002
b.001 .002 b.001 b.001 b.001 .040 .022
Measured by the Substance Dependence Scale. Measured by the Visual Analog Scale. Measured by the Implicit Association Test.
there was no difference in explicit heroin-related cognition between non-abstinent and abstinent heroin users during inpatient detoxification treatment. The possible reason for this discrepancy is the difference in the treatment setting between the present study and the study of Marhe and colleagues. Explicit attitude is more subjective compared with implicit attitude, and thus explicit attitude may be biased by the psychosocial desirability perceived by heroin users in controlled environments such as inpatient treatment settings [30]. It is also possible that abstinence from heroin use when receiving MMT indicates that the heroin users have a good treatment response to methadone, because methadone can decrease the explicit attitude to heroin in heroin users [31]. Blanken et al. [7] showed that stronger explicit heroinrelated cognition was associated with more heroin use in patients with and without heroin use during MMT. Our study further found that, for non-abstinent heroin users during MMT, stronger explicit heroin-related cognition was also associated with more frequent heroin use. The possible reason for why patients with stronger explicit-related cognition were associated with more frequent heroin use was that explicit heroin-related cognition makes abusers seek and use heroin [26] because heroin use is an effective way to reduce explicit heroin-related cognition [32]. It is also interesting that the implicit attitude was associated with more frequent heroin use for non-abstinent heroin users during MMT. Few studies have explored the association between frequency of heroin use and implicit heroin-related cognition. A previous study regarding frequency of alcohol use showed that implicit cognition was associated with more drinking episodes during the past month and higher drinking per occasion [33]. Our study showed that, similar to alcohol users, implicit cognition was positively related to the frequency of heroin use. Our results imply that explicit and implicit heroin-related cognitions measured in this study may indicate different aspects of heroin-related cognition and may represent different aspects of craving for heroin use because there was no significant association between explicit and implicit cognition found in this study. The result was similar to that of
a previous study that used methadone-related stimulus as the reference in the IAT [29]. In addition, our results showed that regarding the frequency of heroin use, explicit cognition and implicit cognition did interact with each other in a synergic way. The dual process decision model showed that explicit and implicit cognitions may cooperate with each other to control individuals' actions [34]. Furthermore, a synergic effect can develop if explicit and implicit cognitions are congruent [35]. Our results also supported the idea that if explicit and implicit cognitions are congruent, the associations between frequency of heroin use and explicit/ implicit cognition are stronger than just the summation of the effect of explicit and implicit cognition. This synergic effect may be associated with a stronger subjective desirability, which may be related to risk-seeking behavior such as drug use [36]. There were several limitations in this study. First, abstinence or not and the frequency of heroin use in nonabstinent heroin users were self-reported. However, a previous study showed that heroin users receiving MMT report the extent of current heroin use truthfully [2]. Second, we did not examine how explicit and implicit attitudes changed with time. Third, we assessed the implicit attitude before assessing the explicit attitude in every participant. Therefore, we could not exclude the possibility that the implicit attitude may influence the results of the explicit attitude. In conclusion, our results showed that both explicit and implicit heroin-related cognitions are associated with the level of heroin use in non-abstinent heroin users receiving MMT, but only explicit heroin-related cognition is associated with whether heroin users can stop using heroin during MMT. Therefore, different cognitive processes toward heroin use may have different influences on heroin users' drug-using behaviors.
Acknowledgment This study was supported by grant NSC101-2314-B-037-057MY3 awarded by the National Science Council, Taiwan (ROC) and the grant KMUH101-1R58.
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Explicit and implicit heroin-related cognitions and heroin use among patients receiving methadone maintenance treatment Peng-Wei Wang a, b , Huang-Chi Lin a, b , Hung-Chi Wu d , Chih-Yao Hsu d , Kuan-Sheng Chung d , Chih-Hung Ko a, b, c,⁎, 1 , Cheng-Fang Yen a, b,⁎, 1 a
Department of Psychiatry, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan Department of Psychiatry, Faculty of Medicine and Graduate Institute of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan c Department of Psychiatry, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan d Departments of Addiction Science, Kai-Suan Psychiatric Hospital, Kaohsiung, Taiwan
b
Abstract Background: Craving is an important issue in substance use disorder. To achieve a better understanding of the cognitive processing systems of craving, the cognitive processes of craving have been considered as two distinct processes. One system, based on rule-based inferences and named explicit cognition, is more conscious and effortful. The other system, based on prior learned association and named implicit cognition, is unconscious and effortless. How explicit and implicit cognitions are associated with heroin use in patients with methadone maintenance treatment (MMT) is not clear. This study aimed to explore the relationship between explicit and implicit cognition and heroin use in patients undergoing MMT. Method: This study recruited one-hundred forty intravenous heroin users. The participants were invited to provide social–demographic data, the severity of substance dependence and explicit cognition with regard to heroin. Then, participants completed a computerized test to assess implicit cognition with regards to heroin. Results: This study found that explicit and implicit heroin-related cognitions were associated with the frequency of heroin use. There was an interaction effect between implicit and explicit cognition on the frequency of heroin use. This study also found that higher explicit heroin-related cognition was a risk factor for continuing heroin use. Conclusion: Both explicit and implicit cognitions were associated with the frequency of heroin use in patients undergoing MMT, but only explicit cognition was associated with whether patients could stop using heroin during MMT. Therefore, the status of heroin use in patients undergoing MMT may be related to different cognitive processes. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Craving is becoming more and more important in terms of conceptualizing and treating substance use disorder because it can destabilize patients seeking treatment for substance abuse [1] and has been used as a criterion of substance use disorder in the DSM-5 [2]. To achieve a better understanding of the cognitive processing systems of craving involved in initiation and escalation of substance use, scholars have ⁎ Corresponding authors at: Department of Psychiatry, Kaohsiung Medical University Hospital, 100 Tzyou 1st Road, Kaohsiung 807, Taiwan. Tel.: +886 7 312 4941; fax: +886 7 3134761. E-mail address: [email protected] (C.-F. Yen). 1 Cheng-Fang Yen, MD., PhD and Chih-Hung Ko, MD., PhD contributed equally to the work. http://dx.doi.org/10.1016/j.comppsych.2014.08.047 0010-440X/© 2014 Elsevier Inc. All rights reserved.
considered the cognitive processes of craving as two distinct processes [3–5]. One system, based on rule-based inferences and named explicit cognition, enables quickly learning the representation of unique or novel event and is more conscious and effortful. The other system, based on prior learned association and named implicit cognition, enables slow learning of general regularities and is unconscious as well as effortless. A meta-analysis study by Rooke and colleagues showed that implicit substance-related cognition is significantly associated with substance use [6]. Research has also found that explicit heroin-related cognition may be associated with illicit heroin use in patients receiving methadone maintenance treatment (MMT) [7]. Furthermore, a previous study on former heroin users demonstrated that the level of explicit heroin-related cognition did not increase after exposure to
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heroin-related and neutral cues, but the blood oxygen-level dependence intensity on MRI increased when the participants were exposed to heroin-related, not neutral, cues [8]. The results of previous studies imply that not only explicit heroin-related cognition but also implicit cognition may play a role in heroin-related craving in heroin users. Heroin use is an important clinical issue because heroin users usually suffer from a chronic relapsing course, as well as a lots of adverse social and health consequences, criminal activities, reliance on social services, and blood-borne infections [9,10]. MMT can improve heroin users' quality of life [11] and reduce their criminal activities [12]. However, although MMT can reduce the severity and frequency of heroin use, 30 to 70% of heroin users receiving MMT still cannot stop using heroin [13–16]. Because of the significant associations of both explicit and implicit cognitions with substance use found in previous studies [6,7,17], further study of the relationship of explicit and implicit cognition with continuous heroin use among heroin users receiving MMT is important. This study aimed to explore the relationships of explicit and implicit heroin-related cognitions with continuous heroin use and without heroin use among heroin users receiving MMT in Taiwan. We also explored whether the interaction between explicit and implicit cognition is associated with current heroin use and abstinence of heroin. We hypothesized that among heroin users receiving MMT: (a) explicit and implicit heroin-related cognitions that are unfavorable to heroin use are associated with whether patients can keep abstinence of heroin or not; (b) explicit and implicit unfavorable heroin-related attitudes may interact with each other in terms of their relationship with abstinence from heroin use; (c) explicit and implicit heroin related cognitions that are unfavorable to heroin use are associated with frequency of current heroin use in patients with MMT and continuing heroin use; (d) the relationships of explicit and implicit unfavorable heroin-related cognitions with frequency of heroin use may interact with each other in the continuing heroin use group.
2. Methods 2.1. Participants This study recruited intravenous heroin users who visited the MMT clinics of Kaohsiung Medical University Hospital and Kai-Suan Psychiatric Hospital. All were opioiddependent: psychiatrists conducted a diagnostic interview based on the Structured Clinical Interview for DSM-IV for Axis I Disorders (SCID) to determine the diagnosis of heroin dependence. They also must have been taking a stable dosage of methadone for more than 1 month. Heroin users who conformed to the criteria described above were recruited into this study. The Institutional Review Board of Kaohsiung Medical University and Kai-Suan Psychiatric Hospital approved the study protocol.
2.2. Measures 2.2.1. Socio-demographic characteristics Participants' sex, age and age of initial heroin use were recorded. 2.2.2. The Chinese version of the Severity of Dependence Scale (SDS [Ch]) The 5-item SDS [Ch] was used to evaluate participants' severity of heroin dependence [18,19]. Each item is scored on a four-point scale (scored 0 to 3). The total SDS score ranges from 0 to 15, higher scores indicating a greater degree of dependence. Cronbach's α of the SDS [Ch] in this study was 0.78. 2.2.3. Visual Analogue Scale (VAS) This study used a VAS with scores from 0 to 100 (none to very much) to measure explicit heroin-related cognition. The VAS includes the following question modified from Cullbertson et al. [20] and Sinha et al. [21]: “How much do you crave/desire/want heroin right now? “ 2.2.4. The Computerized Implicit Association Test (IAT) for heroin cues In presenting the IAT to the participants, we closely followed the procedure described by Greenwald [22]. The target discrimination is heroin-related cues vs. neutral cues, and the attribute discrimination is pleasure vs. aversion. We used liked vs. disliked as attribute labels because these categories are strongly associated with inner motivation. The stimulus material consisted of 6 heroin-related cues (pictures) and 6 neutral cues (pictures) as well as 6 liked (e.g., “lucky, relaxed, pleasure, beauty, active, optimistic”) and 6 disliked words (e.g., “doom, stress, depression, ugly, passive, pessimistic”). Phase 1 consisted of 24 trials in which heroin-related and neutral pictures were presented. During phase 2, liked and disliked words were presented in 24 trials. Phase 3 consisted of two blocks of 48 trials, during which each word or picture was presented twice. The liked word and heroin-related pictures were classified to the left side in the 48 trials. Phase 4 was identical to 2, except that the heroin-related pictures were classified to the right side and neutral pictures were classified to the left side. Phase 5 consisted of two blocks of 48 trials, during which each word or picture was presented twice. The liked words and neutral pictures were classified to the left side in the 48 trials. The IAT score was calculated as the difference in score between the mean response times of the heroin-liked/neutral-disliked block and the neutral-liked/heroin-disliked block, with larger scores indicating stronger automatic approach motivation toward heroin. The IAT score was calculated according to the D-measure algorithm suggested by Greenwald [23]. 2.2.5. Heroin use and methadone treatment characteristics The current dosage of methadone, result of morphine urine examination and self-reported heroin use were recorded. Those who have abstained and did not abstain from heroin use during MMT were classified as the abstinent
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and non-abstinent groups, respectively. The frequency of heroin use was also collected for the non-abstinent group. 2.3. Procedure and statistical analysis Trained research assistants introduced the purpose and procedures of the present study to those who agreed to participate in this study. Informed consent was obtained from all participants prior to commencement of the study. Participants were invited to complete the research questionnaires described above first. Then, the participants completed the computerized test to assess implicit heroinrelated cognition. The abstinent groups were patients without self-reported heroin use and negative heroin urine test. The background characteristics of the participants were compared between the abstinent and non-abstinent groups during MMT using the χ 2 test and Student's t test. The paired t test was used to examine the differences between the reaction time to the heroin + liked words and heroin + disliked words. Student's t test was used to determine the difference in the reaction time of the IAT between the abstinent and non-abstinent groups during MMT. We used a generalized linear model to determine the relationship (1) between explicit heroinrelated cognition and frequency of current heroin use for non-abstinent patients; (2) between explicit heroin-related cognition and abstinence from heroin; (3) between implicit heroin-related cognition and frequency of heroin use for nonabstinent patients; and (4) between implicit heroin-related cognition and abstinence from heroin. We also explored the associations of the interactions between explicit and implicit cognition and frequency of current heroin use and abstinence from heroin. We made inferences at the 0.05 level of significance for inferential statistical procedures and used Holm–Bonferroni method to counteract the problem of multiple comparisons [24].
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3. Results One-hundred forty users receiving MMT participated in this study. Of them, 8 patients (5.70%) were female heroin users. According to current heroin use or not, the participants were classified into the abstinent (n = 48, 34.30%) and nonabstinent (n = 92, 65.70%) groups. In addition, the average frequency of heroin use for the past week was 17.17 (15.75) times per week. None of abstinent patients and one of nonabstinent patients (2.1%) had cocaine use. There was no group difference in cocaine use (χ 2 = 1.930; p = .165). The patients with tetrahydrocannabinol (THC) use were four in abstinent (8.33%) and seven in non-abstinent (7.61%). The rate of THC use did not differ from each group (χ 2 = 0.023; p = .880). Eleven of abstinent patients had alcohol use (22.92%) at least once per week and thirty of the non-abstinent patients had used alcohol one or more times per week. The rate of alcohol use did not differ between groups (χ 2 = 1.431; p = .232). Smoking was common in both groups (97.92% for abstinent and 97.83% for non-abstinent) without group difference (χ 2 = 0.001; p = .972). The results of comparing gender, age, age of first heroin use, severity of heroin dependence on the SDS [Ch], explicit cognition with regards to heroin on the VAS, and implicit cognition with regards to heroin determined by the reaction time to the heroin + liked words and to the heroin + disliked words between the abstinent and non-abstinent groups are shown in Table 1. The mean (standard deviation [SD]) of the severity of heroin dependence measured by the SDS in the abstinent and non-abstinent groups was 5.35 (3.33) and 7.98 (2.89), respectively. The result showed that the severity of heroin dependence was higher in the non-abstinent than in the abstinent group (t = −4.822, df = 137, p b .001). The mean (SD) of the level of explicit attitudes to heroin measured by the VAS in the abstinent and non-abstinent groups was 11.67 (15.48) and 38.88 (26.35), respectively. There was a more
Table 1 The comparisons of social–demographic, severity of dependence, explicit and implicit cognitions between abstinence and non-abstinence group.
Sex (female)
Age (years) Age at first heroin use (years) Severity of heroin dependence a Methadone dosage (mg) Reaction time to heroin pictures and liked items (seconds) b Reaction time to heroin pictures and disliked items (seconds) b Explicit cognition c Implicit cognition b (D score) a b c
Measured by the Substance Dependence Scale. Measured by the Implicit Association Test. Measured by the Visual Analog Scale.
Abstinence group (n = 48) n (%) 5 (10.42)
Non-abstinence group (n = 92) n (%) 3 (3.30)
Mean (SD)
Mean (SD)
42.86 (7.73) 25.85 (6.48) 5.35 (3.33) 55.57 (28.39) 1.13 (0.45) 1.20 (0.49) 11.67 (15.48) 0.18 (1.06)
42.00 (6.25) 26.44 (7.71) 7.98 (2.89) 41.06 (37.78) 1.03 (0.40) 1.12 (0.41) 38.88 (26.35) 0.08 (0.98)
p value
.124
.479 .654 b.001 .021 .203 .335 b.001 .553
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positive explicit attitude in the non-abstinent group than in the abstinent group (t = −6.57, df = 137, p b .001). The difference in the mean reaction time to the heroin pictures + liked items and the heroin pictures + disliked items for the abstinent group was not significant (paired t = −1.44, df = 47, p = .156). However, the mean reaction time of the heroin pictures + liked items was significantly shorter than that of the heroin pictures + disliked items for the non-abstinent group (paired t = −2.27, df = 90, p = .026). There was no significant correlation between implicit heroin related cognition and VAS for the non-abstinent group (Pearson correlation coefficient = −0.05, p = .619) and for the abstinent group (Pearson correlation coefficient = −0.224, p = .126). The frequency of heroin use was significantly positively related to the severity of heroin dependence (Spearman correlation coefficient = 0.266, p = .011) and negatively related to the dosage of methadone (Spearman correlation coefficient = −0.299, p = .004) in the non-abstinent group after corrections of multiple comparisons. There was a significant positive correlation between the frequency of heroin use and implicit heroin-related cognition (D values) (Spearman correlation coefficient = 0.237, p = .024) after corrections of multiple comparisons. Furthermore, the correlation between frequency of heroin use and explicit heroin-related cognition tended to be significant (Spearman correlation coefficient = 0.204, p = .052) after corrections of multiple comparisons. The results of examining the relationships of explicit and implicit cognition with abstinence from heroin use in heroin users receiving MMT are shown in Table 2. The results indicated that more favorable explicit but not implicit cognition toward heroin use was significantly associated with non-abstinence from heroin (continuing heroin use) during MMT. There was no interaction effect between explicit and implicit cognition on abstinence from heroin. Furthermore, the results of examining the relationships of explicit and implicit cognition with the frequency of current Table 2 The associations of explicit and implicit cognition with abstinence from heroin use in heroin users receiving methadone maintenance treatment. Model I OR Sex (0: female; 1: male) Age at first heroin use Severity of heroin dependence a Methadone dosage Explicit cognition b Implicit cognition c Explicit × implicit cognition
Model II
p value OR
1.550 .680 1.059 .106 1.252 .008 .987 .070 1.067 b.001
Model III
p value OR
3.095 .209 1.023 .424 1.343 b.001 .993
.183
.908
.635
OR: odds ratio. a Measured by the Substance Dependence Scale. b Measured by the Visual Analog Scale. c Measured by the Implicit Association Test.
1.253 1.057 1.249
p value .835 .128 .009
.987 .061 1.070 b.001 .920 .811 1.013 .294
heroin use in the non-abstinent group are shown in Table 3. The results indicated that both explicit and implicit heroinrelated cognitions were positively associated with the frequency of heroin use. There was a positive interaction effect between implicit and explicit heroin-related cognition.
4. Discussion There were several important findings in this study. The first was that heroin users receiving MMT who have more favorable explicit cognition toward heroin use were less likely to maintain abstinence. Second, both heroin-related explicit and implicit cognitions were positively associated with frequencies of heroin use in non-abstinent patients. Third, regarding the frequencies of heroin use, the heroin-related explicit and implicit cognitions interacted with each other in a synergic way. Explicit cognition, and not implicit cognition, was associated with whether heroin users were able to stop using heroin or not. Furthermore, implicit cognition did not change the association between the explicit attitude to and abstinence from heroin because there was no interaction effect between implicit and explicit cognition. Robinson et al. [25] suggested that the explicit or implicit cognitive process that the substance user chooses to apply can influence their substance-using behavior. Based on incentive sensitization theory, explicit cognition is essential to explain why substance users engage in behavior to procure a drug [26]. Tiffany argued that implicit cognition is involved in consuming a drug, not procuring a drug [27]. Therefore, explicit attitude plays a major role in whether patients can maintain abstinence or not. Our results also supported this idea, because only explicit attitudes were associated with whether the participant was abstinent or not. Our results also showed that the levels of implicit heroinrelated cognition were not different between the nonabstinent and abstinent heroin users during MMT. The results of the study by Marhe et al. [28] showed that the level of implicit heroin-related cognition did not differ between non-abstinent and abstinent heroin users during inpatient detoxification treatment. Geng et al. [29] showed that the level of implicit heroin-related cognition was not different between heroin users who received and did not receive MMT. The results of this and previous studies imply that MMT may not influence the level of implicit cognition with regards to heroin use. Furthermore, this study found that non-abstinent heroin users had a more favorable explicit cognition toward heroin use than the abstinent participants during MMT in the outpatient setting; meanwhile, after controlling for the effects of age, gender, level of education and severity of heroin dependence, more favorable explicit cognition was associated with a higher frequency of heroin use in non-abstinent heroin users during MMT in the outpatient setting. The result of this study was not in line with that of Marhe et al. [28], in which it was shown that
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Table 3 The relationships of explicit and implicit cognition with the frequency of current heroin use in heroin users receiving methadone maintenance treatment. Model I
Sex (0: female; 1: male) Age at first heroin use Severity of heroin dependence a Methadone dosage Explicit cognition b Implicit cognition c Explicit × implicit cognition a b c
Model II
Model III
Coefficient
p value
Coefficient
p value
Coefficient
p value
2.356 .994 1.053 .990 1.008
b.001 .066 b.001 b.001 b.001
2.361 .989 1.077 .990
b.001 .001 b.001 b.001
1.202
b.001
1.972 .989 1.044 .990 1.007 1.107 1.002
b.001 .002 b.001 b.001 b.001 .040 .022
Measured by the Substance Dependence Scale. Measured by the Visual Analog Scale. Measured by the Implicit Association Test.
there was no difference in explicit heroin-related cognition between non-abstinent and abstinent heroin users during inpatient detoxification treatment. The possible reason for this discrepancy is the difference in the treatment setting between the present study and the study of Marhe and colleagues. Explicit attitude is more subjective compared with implicit attitude, and thus explicit attitude may be biased by the psychosocial desirability perceived by heroin users in controlled environments such as inpatient treatment settings [30]. It is also possible that abstinence from heroin use when receiving MMT indicates that the heroin users have a good treatment response to methadone, because methadone can decrease the explicit attitude to heroin in heroin users [31]. Blanken et al. [7] showed that stronger explicit heroinrelated cognition was associated with more heroin use in patients with and without heroin use during MMT. Our study further found that, for non-abstinent heroin users during MMT, stronger explicit heroin-related cognition was also associated with more frequent heroin use. The possible reason for why patients with stronger explicit-related cognition were associated with more frequent heroin use was that explicit heroin-related cognition makes abusers seek and use heroin [26] because heroin use is an effective way to reduce explicit heroin-related cognition [32]. It is also interesting that the implicit attitude was associated with more frequent heroin use for non-abstinent heroin users during MMT. Few studies have explored the association between frequency of heroin use and implicit heroin-related cognition. A previous study regarding frequency of alcohol use showed that implicit cognition was associated with more drinking episodes during the past month and higher drinking per occasion [33]. Our study showed that, similar to alcohol users, implicit cognition was positively related to the frequency of heroin use. Our results imply that explicit and implicit heroin-related cognitions measured in this study may indicate different aspects of heroin-related cognition and may represent different aspects of craving for heroin use because there was no significant association between explicit and implicit cognition found in this study. The result was similar to that of
a previous study that used methadone-related stimulus as the reference in the IAT [29]. In addition, our results showed that regarding the frequency of heroin use, explicit cognition and implicit cognition did interact with each other in a synergic way. The dual process decision model showed that explicit and implicit cognitions may cooperate with each other to control individuals' actions [34]. Furthermore, a synergic effect can develop if explicit and implicit cognitions are congruent [35]. Our results also supported the idea that if explicit and implicit cognitions are congruent, the associations between frequency of heroin use and explicit/ implicit cognition are stronger than just the summation of the effect of explicit and implicit cognition. This synergic effect may be associated with a stronger subjective desirability, which may be related to risk-seeking behavior such as drug use [36]. There were several limitations in this study. First, abstinence or not and the frequency of heroin use in nonabstinent heroin users were self-reported. However, a previous study showed that heroin users receiving MMT report the extent of current heroin use truthfully [2]. Second, we did not examine how explicit and implicit attitudes changed with time. Third, we assessed the implicit attitude before assessing the explicit attitude in every participant. Therefore, we could not exclude the possibility that the implicit attitude may influence the results of the explicit attitude. In conclusion, our results showed that both explicit and implicit heroin-related cognitions are associated with the level of heroin use in non-abstinent heroin users receiving MMT, but only explicit heroin-related cognition is associated with whether heroin users can stop using heroin during MMT. Therefore, different cognitive processes toward heroin use may have different influences on heroin users' drug-using behaviors.
Acknowledgment This study was supported by grant NSC101-2314-B-037-057MY3 awarded by the National Science Council, Taiwan (ROC) and the grant KMUH101-1R58.
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