Behavioral addictions in euthymic patients with bipolar I disorder: a comparison to controls

It has been suggested (Depue and Iacono 1989; Alloy and Abramson 2010) that bipolar disorder is associated with a hypersensitive behavioral approach system (BAS). According to this model (Gray 1973; Gray and McNaughton 2004), there are three brain systems which affect behavior and emotion. The fight/flight/freeze system (FFFS) organizes behavior in the face of aversive stimuli which can be avoided or escaped. The behavioral inhibition system (BIS) is activated by association with punishment or termination of reward, while the BAS is activated in response to reward or the termination of punishment (Franken et al. 2006). Once activated, the BAS initiates motor activity, positive affect, and motivation for reward; the BAS has been related to the activation of several dopamine pathways and brain regions including the nucleus accumbens, the orbitofrontal cortex, the anterior cingulated cortex, and the dorsolateral prefrontal cortex (Depue and Collins 1999; Berns et al. 2001).

Alloy and Abramson (2010) offered a dysregulation perspective to explain how hypersensitivity in the BAS system is expressed in individuals vulnerable to bipolar spectrum disorders. It would appear that a sensitive BAS, hyper-reactive to cues involving reward or termination of punishment, becomes dysregulated easily. Such sensitivity may lead to great variability in BAS activation over time and across situations in response to stimuli. An overactive BAS could result in manic-like behavior (hyperactivity, enhanced appetitive behavior, euphoric or irritable mood), whereas an underactive BAS could result in depression-like behavior (anhedonia, lack of motivation, passivity) (Urosevic et al. 2008).

A possible role for BAS dysregulation in the bipolar spectrum in general and in patients with bipolar I specifically has been supported in several studies using the self-report BIS/BAS scale (Carver and White 1994). Alloy et al. (2009c) and Meyer et al. (2001) found higher BAS scores in euthymic bipolar I patients as compared to healthy controls. Similar results were reported by Salavert et al. (2007) using a different self-report measure of BAS sensitivity. In two studies comparing bipolar spectrum participants (bipolar II and cyclothymic) to demographically matched controls, the bipolar spectrum group reported higher total scores in the BAS (Alloy et al. 2008; Alloy et al. 2009b). In one prospective high-risk design study, adolescents with high BAS scores, over 12 to 13 years of follow-up, had a higher probability and a shorter time to onset of bipolar spectrum disorders than did a group with moderate scores (Alloy et al. 2012).

Assuming that bipolar disorder (BP) is related to a hypersensitive BAS and therefore to increased reward sensitivity, it would seem logical to predict unusually high rates of substance use, abuse, and addiction among patients with BP disorder. In fact, studies have shown prevalence of substance abuse among patients diagnosed with bipolar I disorder to range between 35% and 60%, approximately three to nine times the prevalence in the general population (Lagerberg et al. 2010; Merikangas et al. 2007; ten Have et al. 2002). Additionally, there is higher lifetime prevalence of substance use disorders (SUDs) in bipolar disorder as compared to other mood disorders (Quello et al. 2005).

Possible specific links between the BAS and SUDs have been explored in non-patient as well as in patient samples. Franken and Muris (2005) found that the BAS dimension of fun seeking correlated positively with a number of illegal substances which undergraduate students had used, frequency of binge drinking, and overall quantity of alcohol consumed; the BAS dimension of drive also correlated (weakly) with the amount of illegal substances used. In patients with bipolar spectrum disorders, Alloy et al. (2009a) found that high BAS sensitivity predicted greater substance use problems at follow-up, even after controlling for lifetime SUDs.

These findings suggest that BAS hypersensitivity is related to both vulnerability to SUDs and to mood symptoms. Interestingly, the sensitivity of the reward system is hypothesized to involve dopaminergic projections (Urosevic et al. 2008) which are also involved in the neurobiology of both substance and behavioral addictions (Grant et al. 2006).

Substance use is one element of the larger phenotype of behavioral addiction. Behavioral addictions (BAs) are similar to substance addiction in exhibiting diminished control, but the main expression of the addiction is its behavioral focus - it does not necessarily include the ingestion of a psychoactive substance. BAs are experienced as pleasurable and give relief and excitement whether the addiction is to music, exercise, gambling, or drugs (Meyer et al. 2007).

Substance abuse and behavioral addictions have much in common, including ‘natural history, phenomenology, tolerance, co-morbidity, overlapping genetic contribution, neurobiological mechanisms, and response to treatment’ (Grant et al. 2010, p. 233). It is not surprising, therefore, that the prevalence of behavioral addictions has been found to be higher in patients with bipolar disorder than among healthy controls - 33% vs. 13% - in one study (Di Nicola et al. 2010).

It is not clear what role personality factors may play in the relationship between BP disorder and BAs. In particular, traits related to disinhibition or behavioral undercontrol may mediate the diathesis to both bipolar disorder and behavioral addictions. The psychobiological model of personality, developed by Cloninger (Cloninger et al. 1993; Cloninger and Svrakic 1997), is a two-tier system. The first tier, the temperament traits, includes Harm Avoidance (HA), Novelty Seeking (NS), Reward Dependence (RD), and Persistence (PS). The second tier, the character traits, includes Self-directedness (SD), Cooperativeness (CO), and Self-transcendence (ST). Mardaga and Hansenne (2007) explored the connection between these two models in an undergraduate sample of 150 participants and found that BAS scores were predicted by high novelty seeking and high persistence scores. We decided to further explore the interrelationships between bipolar disorder, behavioral addictions, and personality/temperament traits by comparing responses on two self-report questionnaires, one for behavioral addictions and one a measure of personality according to Cloninger’s model, administered to euthymic adult bipolar patients and to a matched healthy control group. This study was approved by the BGU Institutional Review Board.

The patient group consisted of 50 adult (ages 18 to 65) euthymic patient volunteers diagnosed as having bipolar I disorder as diagnosed by DSM-IV criteria based on chart review and clinical interview and were recruited from the well-defined bipolar patient population of the ambulatory Mood Disorders Clinic of the Beer Sheva Mental Health Center. Every patient recruited was well known to the clinic staff, and some have been treated by the same team for over 20 years. (Osher et al. 2010). Exclusion criteria were dementia or language skills inadequate for comprehension of the questionnaires in available languages. The control group was recruited from the community and consisted of 50 healthy volunteers matched with patients for age (±5 years), sex, gender, and educational level. The participants aged 40 and older were recruited in the Sharon area in Israel and were drawn from an ongoing longitudinal study of personality (Cloninger and Zohar 2011). The younger participants were recruited using a snowball technique.

There were no significant differences between the patient and control groups with respect to age (42.2 ± 11.92 vs. 43.2 ± 16.23; t = 0.18, p = 0.85) or sex (27 females, 23 males in each group). Control participants were slightly more educated than patients on average (15.1 ± 2.85 vs. 13.6 ± 2.36; t = −2.94, p = 0.005).

Bipolar patients had an average age of onset of 23.6 years (SD = 7.3, range 12 to 47) and had been ill for an average of 19.3 years (SD = 10.8, range 1 to 47). All patients were receiving psychotropic medication, with 35 on lithium, 14 on anticonvulsants, 26 on atypical antipsychotics, and another 6 on typical antipsychotics; five patients received an antidepressant. The total is more than 50 patients as only 18 patients were on monotherapy, while 28 patients received two medications and 4 patients received three or more.

Behavioral addictions

Repeated measures ANOVA with BA domains as within-subject factors showed a significant group X domain interaction [F (11,1078) = 6.0, p < 0.0001]. Post-hoc (LSD test) comparisons revealed significant differences (p < 0.05) on several individual BAs, with BP patients showing higher scores on two benign BAs (music and shopping) and higher scores on smoking. Control group participants showed higher scores on two harmful BAs (drugs (p = 0.06) and alcohol (p < 0.05)). Results are presented in Figure 1.

The hypersensitive behavioral approach system model of bipolar disorder would predict higher levels of various addictions in bipolar patients as compared to controls, and in this study, we tested this hypothesis by looking at behavioral addictions in addition to the more commonly studied substance addictions. Euthymic bipolar patients did in fact show significantly elevated levels of two benign behavioral addictions (shopping and music) as well as smoking. Bipolar patients’ levels of drug- and alcohol-related addiction were, surprisingly, lower than those reported by healthy controls. We discuss possible explanations for this below.

The finding of higher tobacco use among BP patients as compared to healthy controls is consistent with other reports (Diaz et al. 2009; Leonard et al. 2001; Itkin et al. 2001). High rates of substance abuse are also often reported among bipolar patients (Lagerberg et al. 2010; Strakowski and DelBello 2000; Swann 2010). We suspect that our finding of lower levels of substance abuse (i.e., illicit drugs and alcohol) among the bipolar subjects may be related to the fact that the bipolar subjects in this study were stable and euthymic and, as a group, have received considerable psychoeducational exposure and are relatively adherent to medication recommendations, as indicated by frequent tests of medication blood levels (see Osher et al. 2010). It also became clear during the testing sessions that many of the bipolar patients had (ab)used drugs and/or alcohol in the past but had modified these behaviors since beginning treatment in the clinic.

This study also explored the relationships between behavioral addictions and personality factors (temperament and character as measured by the TCI-R). In both BP patients and controls, novelty seeking was positively correlated to harmful addictions. This finding is consistent with findings in non-clinical samples regarding consumption of both multiple substances, including illicit drugs and alchohol (Chakroun et al. 2004), and cigarettes (Dinn et al. 2004). The character trait of cooperativeness was found to be negatively related to harmful addictions in both groups. Overall, these findings suggest that temperament and character traits may play roles both as risk factors and as protective factors regarding BAs in euthymic bipolar patients as well as in healthy controls.

One limitation of this study is that the BP patient group consisted mostly of residents of southern Israel, while the control group was recruited mostly from the Sharon area, Israel. Although the distance between the regions is not great, there may be some social or socio-economic differences between the two groups.

The hypersensitive BAS model of bipolar disorder provides a possible framework for the integration of biological, behavioral, and neurological aspects of this devastating illness. Our findings are largely consistent with this model and contribute to a growing literature, suggesting the importance of continued elucidation of the role of a hypersensitive BAS in the pathogenesis of bipolar affective disorder.