Abstract
Objective
Increased impulsivity has been demonstrated to be a trait feature of adults with bipolar disorder (BD), yet impulsivity has received little study in adolescents with BD. Thus, it is unknown whether it is a trait feature that is present early in the course of the disorder. We tested the hypotheses that self-reported impulsiveness is increased in adolescents with BD, and that it is present during euthymia, supporting impulsiveness as an early trait feature of the disorder.
Methods
Impulsiveness was assessed in 23 adolescents with BD and 23 healthy comparison (HC) adolescents using the self-report measure of impulsivity, the Barratt Impulsiveness Scale (BIS), comprised by attentional, motor and nonplanning subscale scores. Effects of subscale scores and associations of scores with mood state and course features were explored.
Results
Total and subscale BIS scores were significantly higher in adolescents with BD than HC adolescents. Total, attentional and motor subscale BIS scores were also significantly higher in the subset of adolescents with BD who were euthymic, compared to HC adolescents. Adolescents with BD with rapid-cycling and chronic mood symptoms had significantly higher total and motor subscale BIS scores than adolescents with BD without these course features.
Conclusion
These results suggest increased self-reported impulsiveness is a trait feature of adolescents with BD. Elevated impulsivity may be especially prominent in adolescents with rapid-cycling and chronic symptoms.
Keywords: Bipolar Disorder, Adolescents, Impulsivity
Impulsivity is a prominent feature of bipolar disorder (BD) (1–3). Heightened impulsiveness is a characteristic feature of mania (3,4) and has also been associated with depressive episodes of BD (3,5). Using a self-report measure of trait impulsivity, the Barratt Impulsiveness Scale [BIS, (6)], adults with BD demonstrate elevated impulsivity during both acute mania and depression as well as in euthymic periods (2,3,7–10). These findings support impulsivity as a trait feature of BD. Impulsivity is elevated in adults with rapid-cycling bipolar disorder and suicidality, suggesting that impulsivity may be associated with poorer prognosis (11,12). Additionally, total and attentional impulsivity scores are related to an earlier age of onset in adult BD (12), suggesting impulsivity may be a characteristic of BD presenting during adolescence. However, little work has focused on impulsivity in adolescent BD and thus, it is not clear whether impulsivity is a trait feature of the adolescent epoch.
To our knowledge, demonstration of trait impulsiveness across the attentional, motor, and nonplanning domains assessed by the BIS has not been reported previously in adolescents with BD. Increased impulsiveness in adolescents with BD is implicated by studies demonstrating impaired response inhibition in tasks requiring inhibition of prepotent responses and adaptation of responses to changing reinforcement contingencies (13–16). Moreover, impulsiveness could contribute to deficits in adaptive set shifting and cognitive flexibility in BD, demonstrated in euthymic adolescents with BD and in adolescent BD without comorbid attention-deficit/hyperactivity disorder (13–16).
We assessed self-reported trait impulsivity in adolescents with BD using the BIS (6). We hypothesized that adolescents with BD would show increased impulsiveness compared to healthy comparison (HC) adolescents, and that this increase would be present in euthymic, in addition to symptomatic, adolescents with BD. We also explored the relationship between impulsivity and clinical features of BD, including rapid-cycling, comorbidity with ADHD, and suicidality.
Materials and Methods
Subjects
Participants included adolescents ages 11–17 years, twenty-three with BD I (43.4% female, mean (M) age 14.7 years ±SD 1.32) and twenty-three HC adolescents (47.8% female, M=14.2±1.91). Adolescents with BD were recruited from the Yale School of Medicine medical center and surrounding community; HC participants were recruited from the community. The presence or absence of DSM-IV Axis I disorders were confirmed by administration of the revised schedule for Affective Disorders and Schizophrenia for School-Age Children- Present and Lifetime Version (K-SADS-PL) (22) to participants and a parent or guardian. Exclusion criteria included history of neurological disorders, loss of consciousness over five minutes and significant medical illness. Additionally, HC adolescents did not meet DSM-IV criteria (23) for an Axis I disorder, nor had a first degree relative with a history of psychiatric illness, as measured by the Family History Screen for Epidemiological Studies (24).
At the time of assessment, fifteen (65%) adolescents with BD were euthymic and eight (35%) were in a current mood episode: three (16%) depressed, two (11%) manic, and three (16%) in mixed states. Owing to the small number of participants in a mood episode, they were combined into a BD “acute” subgroup for analyses. Six adolescents (26%) met criteria for rapid-cycling and five adolescents (22%) reported chronic mixed symptoms. These two groups were combined for analysis into a “rapid-cycling” subgroup to compare adolescents who experience more time in clinically symptomatic states to the non-rapid-cycling BD subgroup who experience acute symptoms less frequently; secondary analyses also assessed the subgroup that met criteria for rapid-cycling separately from the chronic symptom subgroup. Current comorbidities in adolescents with BD included attention deficit hyperactivity disorder (ADHD) (N=7, 30%), oppositional defiant disorder (N=3, 13%), anxiety disorders (N=3, 13%: separation anxiety disorder N=1, generalized anxiety disorder and post traumatic stress disorder N=1, specific phobia N=1), substance abuse (N=1, 4%), and enuresis (N= 1, 4%). Psychotropic medications prescribed to adolescents with BD included atypical antipsychotics (N=15, 65%), anticonvulsants (N=11, 48%), lithium (N=6, 26%), antidepressants (N=4, 17%), stimulants (N=5,22%), and benzodiazepines (N=1, 4%). Three (13%) adolescents with BD were unmedicated at assessment.
Prior to study, written informed consent from the parent/guardian and written assent from participants were obtained. The study was approved by the Yale School of Medicine Institutional Review Board.
Instruments
Current mood episode and history of suicidal behaviors were assessed using the K-SADS-PL (22). The Child Depression Rating Scale (CDRS) (25) and Young Mania Rating Scale (YMRS) (26) assessed current mood symptoms. To measure impulsivity, the BIS version 11a (27) was used. The total score on the BIS self-report measure of impulsivity is the sum of three subscale scores: attentional impulsivity (inability to focus or concentrate), motor impulsivity (acting on the spur of the moment) and nonplanning impulsivity (lack of sense of future). Total BIS scores, as well as the three subscale scores, were calculated from the BIS-11a and prorated to BIS-11 scores (27,28).
Statistical Analysis
Analyses were performed in SAS version 9.1 (SAS Institute, Cary, North Carolina) using BIS total and subscale scores as dependent variables. Independent sample t-tests were performed to compare the HC group to the BD group. ANOVA was used to further assess differences between the euthymic BD subgroup, acute BD subgroup, and HC group, followed by Tukey’s multiple comparison procedure testing all pair-wise differences. Age and sex were considered in the comparisons above using ANCOVA, but were not significant and dropped for parsimony. Within the overall BD group, effects of clinical factors were assessed one at a time using independent samples t-tests, including the presence/absence of rapid-cycling/chronic symptoms, ADHD comorbidity, history of suicide attempts, and medication (on/off for any psychotropic medication and individually for atypical antipsychotic, anticonvulsant, lithium, antidepressants and stimulant subclasses).
Results
There were no significant differences between the HC and BD groups, or across HC, BD euthymic, and BD acute groups, in age [t(44)= −1.08, p>.05] or gender [χ2(1)= .088, p>.05]. BIS total and all subscale scores were significantly higher in the BD group compared to the HC group (Table 1).
Table 1.
HC (n=23) | All BD (n=23) | Euthymic BD (n=15) | Acute BD (n=8) | |
---|---|---|---|---|
Age | 14.2 (±1.91) | 14.7 (±1.32) | 14.5 (±1.41) | 15.1 (±1.13) |
Gender (% F) | 48% | 43% | 45% | 50% |
BIS Total | 61.7 (8.59) | 74.2 (11.07)*** | 72.7 (12.99)** | 77.0 (5.86)*** |
BIS Attentional | 16.4 (4.58) | 21.1 (4.21)*** | 20.9 (4.85)** | 21.5 (2.88)** |
BIS Motor | 19.4 (3.69) | 24.0 (5.58)* | 24.1 (6.71)* | 23.9 (2.75) |
BIS Nonplanning | 25.4 (4.73) | 29.2 (5.50)* | 27.8 (6.17) | 31.8 (2.71)** |
Note. HC= Healthy Comparison Adolescents, BD= Adolescents with Bipolar Disorder, BIS=Barratt Impulsiveness Scale Score.
Significantly different from HC group (p<0.05)
Significantly different from HC group (p<0.01)
Significant different from HC group (p<0.001)
No significant differences between Euthymic BD and Acute BD groups
Values are group means (SE) unless otherwise indicated.
Comparing the euthymic BD, acute mood BD, and HC groups using ANOVA, significant effects of group for total BIS scores [F( 2,43)= 9.66, p<.001] and all subscale scores [attentional: F(2,43)= 8.37, p<.001; motor: F(2,43)= 5.35 p<.01; nonplanning: F(2,43)=4.81, p<.05] were observed. Tukey’s post hoc tests demonstrated the euthymic BD subgroup and acute BD subgroup each displayed significantly higher total scores than the HC group on total and attentional subscale scores (Table 1). Significantly higher scores on the motor subscale were only found for the euthymic BD subgroup, compared to the HC group. Conversely, only the acute BD subgroup differed from the HC group on the nonplanning subscale. No differences were observed between the two BD subgroups. Controlling for CDRS and YMRS scores in the models above did not affect results, nor did total BIS scores correlate with current manic [r=.22, p>.05] or depressive [r=.28, p>.05] symptoms.
The subgroups of BD adolescents with rapid-cycling/chronic symptoms had higher BIS total scores [t(21)= 2.9, p<.05], and motor subscale scores [t(21)= −2.96 p<.05], than adolescents with BD without these course features. Secondary analyses assessing adolescents with rapid-cycling and adolescents with chronic symptoms separately showed the rapid cycling subgroup differed significantly from the HC group on both the total [t(16)= −2.48, p<.05] and motor subscale [t(16)= −3.15, p<.05] scores while differences between the chronic symptom subgroup and the HC group on total [t(15)= −1.98, p=.06] and motor subscale [t(15)= −1.94, p=.07] scores were at the trend level. No significant effects were detected for the presence or absence of ADHD comorbidity, history of suicidal behavior, or medication use (overall use or for subclass of medication)
Discussion
Impulsivity, as measured by the BIS, was significantly higher in adolescents with BD compared with HC adolescents. Consistent with findings in adult samples, (2,3,9,12), impulsivity was elevated within the euthymic subgroup of BD adolescents. This supports self-reported impulsiveness as a trait feature of BD that is present by adolescence. Additionally, previous reports show the attentional subscale to be associated with a more severe course of the disorder and an earlier age of onset (12). Similarly, in the current sample, the attentional subscale was the only subscale to show significant elevations in both the euthymic and acute mood subsamples compared with the HC adolescents. This is potentially consistent with reports of diminished performance on tasks requiring sustained attention and inhibition of inappropriate responses and deficits in prefrontal regions subserving impulse regulation reported in euthymic BD adolescents (13,15–21).
Neuroimaging studies of BD demonstrate structural and functional abnormalities in ventral prefrontal cortex (vPFC) neural systems that subserve impulse regulation (17–20), suggesting a neural difference that might mediate the increased impulsiveness of BD. Decreases in vPFC volume, and deficits in vPFC engagement during tasks that require inhibition of prepotent responses, have been reported in symptomatic and euthymic adults with BD (17,18). Preliminary evidence suggests these abnormalities emerge and progress during adolescence (18–20) and are associated with impaired behavioral inhibition (21).
Consistent with reported associations between more frequent episodes in adults with BD and elevated impulsivity (12), adolescents with BD with rapid-cycling and chronic symptoms demonstrated elevated self-reported impulsivity, especially on the motor subscale, compared with BD adolescents with fewer episodes. We previously noted greater decreases in vPFC volume in adolescents and adults with BD with rapid-cycling, compared to those with BD without rapid-cycling (18), suggesting structural brain differences that may mediate the increased impulsivity in this population. Consistent with the findings, vPFC abnormalities in adolescents with BD have been linked to motor disinhibition (21). It is possible that greater abnormalities in the development of vPFC may lead to impulsivity and cycling phenotypic features of an adolescent subgroup with BD; however, it is also possible that episodes have neurotoxic effect in vPFC. Research to bridge the neurobiological findings, impulsivity, and clinical course features of adolescents with BD is warranted.
Although increased suicidality has been associated with increased impulsivity in adults with BD (11,12), we did not detect this relationship in the adolescents. The additional diagnosis of ADHD also did not influence levels of impulsivity. ADHD not in conjunction with BD has been associated with increased BIS scores (29); however, our finding is consistent with reports of similar levels of difficulty in response inhibition in BD adolescents with and without comorbid ADHD (13,16). It should be noted though that the small subsample sizes in the subgroups with suicidality and comorbid ADHD may have reduced ability to detect associations. Substance abuse is also associated with increased impulsivity in adult BD (1,8,11). However, this sample included only one adolescent who met criteria for a substance use disorder so associations could not be assessed. More sensitive measures of substance misuse may help to elucidate associations to substance use initiation and early misuse with impulsivity in adolescents with BD. Associations between total impulsivity and psychotropic medication status for any medication use and for use of subclasses of medications were not detected, although assessments may have been limited by small sample sizes.
To our knowledge, this is the first study to demonstrate trait impulsiveness in adolescents with BD using the BIS. Given the small sample size, the results should be considered preliminary. Future research should include larger samples and more systematic assessment of clinical features and medication. Future prospective studies of adolescents at risk for BD and assessment of structural brain differences associated with BIS scores will further aid in elucidating mechanisms underlying the development of impulsivity in the disorder.
Acknowledgments
We wish to thank Kathleen Colonese, Susan Quatrano and Allison McDonough for their work with the adolescents and organization of the data, and the adolescents and their families for their participation. Funding for this study was provided by the National Institute of Health grants RC1MH088366 (HPB) and R01MH69747 (HPB), UL1DE19586, the Roadmap for Medical Research/Common Fund and RL1DA024856 (HPB, JHK, SN-H), T32MH14276 (JHK), the National Alliance for Research in Schizophrenia and Depression (HPB, JHK), the Attias Family Foundation (HPB), Marcia Simon Kaplan (JHK), Women’s Health Research at Yale (HPB) and the Klingenstein Foundation (JHK). These funding sources had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.
Footnotes
All authors declare they have no conflict of interest.
References
- 1.Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC. Psychiatric Aspects of Impulsivity. American Journal of Psychiatry. 2001;158:1783–1793. doi: 10.1176/appi.ajp.158.11.1783. [DOI] [PubMed] [Google Scholar]
- 2.Swann AC, Anderson JC, Dougherty DM, Moeller FG. Measurement of the inter-episode impulsivity in bipolar disorder. Psychiatry Research. 2001;101:195–197. doi: 10.1016/s0165-1781(00)00249-3. [DOI] [PubMed] [Google Scholar]
- 3.Swann AC, Pazzaglia PJ, Nicholls A, Dougherty DM, Moeller FG. Impulsivity and phase of illness in bipolar disorder. Journal of Affective Disorders. 2003;73:105–111. doi: 10.1016/s0165-0327(02)00328-2. [DOI] [PubMed] [Google Scholar]
- 4.Harmon-Jones E, Barratt ES, Wigg C. Impulsiveness, aggression, reading, and the P300 of the event-related potential. Personality and Individual Differences. 1997;22:439–445. [Google Scholar]
- 5.Corruble E, Benyamina A, Bayle F, Falissard B, Hardy P. Understanding impulsivity in severe depression? A psychometrical contribution. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 2003;27:829–833. doi: 10.1016/S0278-5846(03)00115-5. [DOI] [PubMed] [Google Scholar]
- 6.Barratt ES, Patton JH. Impulsivity: Cognitive, behavioral, and psychophysiological correlates. In: Zuckerman M, editor. Biological Basis of Sensation-Seeking, Impulsivity, and Anxiety. Lawrence Erlbaum Associates; 1983. pp. 77–116. [Google Scholar]
- 7.Swann AC, Moeller FG, Steinberg JL, Schneider L, Barratt ES, Dougherty DM. Manic Symptoms and impulsivity during bipolar depressive episodes. Bipolar Disorders. 2007;9:206–212. doi: 10.1111/j.1399-5618.2007.00357.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Swann AC, Steinberg JL, Lijffijt F, Moeller FG. Impulsivity: Differential relationship to depression and mania in bipolar disorder. Journal of Affective Disorders. 2008;206:241–248. doi: 10.1016/j.jad.2007.07.011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Peluso MAM, Hatch JP, Glahn DC, Monkul ES, Sanches M, Najt P, Bowden CL, Barratt ES, Soares JC. Trait impulsivity in patients with mood disorders. Journal of Affective Disorders. 2007;100:227–231. doi: 10.1016/j.jad.2006.09.037. [DOI] [PubMed] [Google Scholar]
- 10.Holmes MK, Bearden CE, Barguil M, Fonseca M, Monkul ES, Nery FG, Soares JC, Mintz J, Glahn DC. Conceptualizing impulsivity and risk taking in bipolar disorder: Importance of history of alcohol abuse. Bipolar Disorders. 2009;11:33–40. doi: 10.1111/j.1399-5618.2008.00657.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Swann AC, Dougherty DM, Pazzaglia PJ, Pham M, Steinberg JL, Moeller FG. Increased Impulsivity Associated with Severity of Suicide Attempt History in Patients with Bipolar Disorder. American Journal of Psychiatry. 2005;162:1680–1687. doi: 10.1176/appi.ajp.162.9.1680. [DOI] [PubMed] [Google Scholar]
- 12.Swann AC, Lijffijt M, Lane SD, Steinberg JL, Moeller FG. Increased trait-like impulsivity and course of illness in bipolar disorder. Bipolar Disorders. 2009;11:280–288. doi: 10.1111/j.1399-5618.2009.00678.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Dickstein DP, Treland JE, Snow J, McClure EB, Mehta MS, Towbin KE, Pine DS, Leibenluft E. Neuropsychological performance in pediatric bipolar disorder. Biological Psychiatry. 2004;55:32–39. doi: 10.1016/s0006-3223(03)00701-7. [DOI] [PubMed] [Google Scholar]
- 14.Dickstein DP, Nelson EE, McClure EB, Grimley ME, Knopf L, Brotman MA, Rich BA, Pine DS, Leibenluft E. Cognitive Flexibility in Phenotypes of Pediatric Bipolar Disorder. Journal of American Academy of Child and Adolescent Psychiatry. 2007;46:341–355. doi: 10.1097/chi.0b013e31802d0b3d. [DOI] [PubMed] [Google Scholar]
- 15.Gorrindo T, Blair RJ, Budhani S, Dickstein DP, Pine DS, Leibenlulft E. Deficits on a probabilistic response-reversal task in patients with pediatric bipolar disorder. American Journal of Psychiatry. 2005;162:1975–1977. doi: 10.1176/appi.ajp.162.10.1975. [DOI] [PubMed] [Google Scholar]
- 16.McClure EB, Treland JE, Snow J, Schmajuk M, Dickstein DP, Towbin KE, Charney DS, Pine DS, Leibenluft E. Deficits in social cognition and response flexibility in pediatric bipolar disorder. American Journal of Psychiatry. 2005;162:1644–1651. doi: 10.1176/appi.ajp.162.9.1644. [DOI] [PubMed] [Google Scholar]
- 17.Blumberg HP, Hoi-Chung L, Skudlarski P, Lacadie CM, Fredericks CA, Harris BC, Charney DS, Gore JC, Krystal JH, Peterson BS. A Functional Magnetic Resonance Imaging Study of Bipolar Disorder; State- and trait-related dysfunction in ventral prefrontal cortices. Archives of General Psychiatry. 2003;60:601–609. doi: 10.1001/archpsyc.60.6.601. [DOI] [PubMed] [Google Scholar]
- 18.Blumberg HP, Krystal JH, Bansal R, Martin A, Dziura J, Durkin K, Martin L, Gerard E, Charney DS, Peterson BS. Age, rapid-cycling, and pharmacotherapy effects on ventral prefrontal cortex in bipolar disorder: A cross sectional study. Biological Psychiatry. 2006;59:611–618. doi: 10.1016/j.biopsych.2005.08.031. [DOI] [PubMed] [Google Scholar]
- 19.Blumberg HP, Martin A, Kaufman J, Leung HC, Skudlarski P, Lacadie C, Fulbright RK, Gore JC, Charney DS, Krystal JH, Peterson BS. Frontostriatal abnormalities in adolescents with bipolar disorder: Preliminary observations from functional MRI. American Journal of Psychiatry. 2003;160:1345–1347. doi: 10.1176/appi.ajp.160.7.1345. [DOI] [PubMed] [Google Scholar]
- 20.Kalmar JH, Wang F, Chepenik LG, Womer FY, Jones MM, Pittman B, Shah MP, Martin A, Constable RT, Blumberg HP. Relation between amygdala structure and function in adolescents with bipolar disorder. Journal of American Academy of Child and Adolescent Psychiatry. 2009;48:636–642. doi: 10.1097/CHI.0b013e31819f6fbc. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Leibenluft E, Rich BA, Vinton DT, Nelson EE, Fromm SJ, Berghorst LH, Joshi P, Robb A, Schacher RJ, Dickstein DP, McClure EB, Pine DS. Neural circuitry engaged during unsuccessful motor inhibition in pediatric bipolar disorder. American Journal of Psychiatry. 2007;164:152–160. doi: 10.1176/ajp.2007.164.1.A52. [DOI] [PubMed] [Google Scholar]
- 22.Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Paula M, Williamson D, Ryan N. Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. Journal of American Academy of Child and Adolescent Psychiatry. 1997;36:980–988. doi: 10.1097/00004583-199707000-00021. [DOI] [PubMed] [Google Scholar]
- 23.American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4. Washington DC: 2000. text revision. [Google Scholar]
- 24.Lish JD, Weissman MM, Adams PB, Hoven CW, Bird H. Family psychiatric screening instruments for epidemiologic studies: Pilot testing and validation. Psychiatry Research. 1995;57:169–180. doi: 10.1016/0165-1781(95)02632-7. [DOI] [PubMed] [Google Scholar]
- 25.Emslie GJ, Weinberg WA, Rush AJ, Adams RM, Rintelmann JW. Depressive symptoms by self-report in adolescents: Phase I of the development of a questionnaire for depression by self-report. Journal of Child Neurology. 1990;5:449–453. doi: 10.1177/088307389000500208. [DOI] [PubMed] [Google Scholar]
- 26.Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: Reliability, validity and sensitivity. British Journal of Psychiatry. 1978;133:429–435. doi: 10.1192/bjp.133.5.429. [DOI] [PubMed] [Google Scholar]
- 27.Barratt ES. Impulsiveness and aggression. In: Monahan J, Steadman HJ, editors. Violence and Mental Disorder: Developments in Risk Assessment. University of Chicago; Chicago: 1994. pp. 61–79. [Google Scholar]
- 28.Patton JH, Stanford MS, Barratt ES. Factor Structure of the Barratt Impulsiveness Scale. Journal of Clinical Psychology. 1995;51:768–774. doi: 10.1002/1097-4679(199511)51:6<768::aid-jclp2270510607>3.0.co;2-1. [DOI] [PubMed] [Google Scholar]
- 29.Malloy-Diniz L, Fuentes D, Leite WB, Correa H, Bechara A. Impulsive behavior in adults with attention deficit/hyperactivity disorder: Characterization of attentional, motor, and cognitive impulsiveness. Journal of the International Neuropsychological Society. 2007;13:693–698. doi: 10.1017/S1355617707070889. [DOI] [PubMed] [Google Scholar]