Impulsivity as an Endophenotype in ADHD: Negative Findings

Abstract

Impulsivity has a strong genetic component and is considered an endophenotype in many psychiatric disorders. Impulsivity in adult ADHD has become a focus of interest more recently because of its suggested prominence in this age. Objective: This study aimed to access self-reported impulsivity levels in biological parents of ADHD offspring, according to their status: non-ADHD (controls), remitted, nonremitted. Method: Impulsivity levels of 155 parents of ADHD children were compared according to their status using the Barratt Impulsiveness Scale (BIS-11). Results: The ADHD group presented the highest levels of impulsivity compared with all other groups. The remitted ADHD and control groups showed no significant differences in impulsivity levels. Conclusion: Impulsivity tended to remit alongside ADHD symptoms in remitters and to persist in those presenting with the residual form of adult ADHD suggesting it should not be considered as an endophenotype. Only the attentional dimension was impaired, cautioning against Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5) impulsivity proposed criteria.

Keywords

implusivity adult ADHD parental ADHD ADHD subtypes ADHD-associated problems

Introduction

Impulsivity has been defined as unplanned actions that lead to thoughtless behaviors and to a tendency to act with a lower level of planning compared with people of similar intellectual level (Moeller, Barratt, Dougherty, Schmitz, & Swann, 2001). Some degree of impulsivity may be considered to be a key component of human nature as it may be advantageous in situations where it is crucial to act quickly either to avoid danger or take opportunities (Bevilacqua & Goldman, 2013). Its overexpression is seen in many psychiatric disorders and higher levels of impulsivity have been linked to outcomes in bipolar disorder, substance use, and ADHD (Stanger et al., 2012).

ADHD is a neurodevelopmental disorder affecting children, adolescents, and adults worldwide (Polanczyk, de Lima, Horta, Biederman, & Rohde, 2007) where impulsivity has long been considered to be central to the disorder (Barkley, 1997) among its other defining symptoms of inattention and hyperactivity. It is the most common psychiatric disorder in children, and often persists into adulthood (Kessler et al., 2005). The Barratt Impulsiveness Scale (BIS-11) is the most commonly used psychometric tool used to measure impulsivity in both clinical and research contexts. The scale involves 18 items, which can be subdivided in three dimensions: motor impulsivity (BIS-MOT), planning deficit (BIS-PLA), and attentional impulsivity (BIS-AT). Although impulsivity is a heterogeneous construct with different clinical components (Malloy-Diniz et al., 2015; Sedyiama et al., 2017), only items about motor impulsivity is addressed by DSM (Diagnostic and Statistical Manual of Mental Disorders, 5th, 2013) diagnostic criteria. A previous study (Malloy-Diniz, Fuentes, Leite, Correa, & Bechara, 2007), however, found that adult ADHD is associated with increased impulsiveness scores in both self-reported and neuropsychological measures of motor, nonplanning, and attentional impulsivity.

In children, impulsivity is related to an impaired ability to interact with peers, including inappropriate interruptions, difficulties in listening to others and difficulty in waiting one’s turn. Impulsive behavior is related to behavioral problems with relatives and school peers, particularly during adolescence. In adulthood, impulsivity is associated with diverse negative consequences, such as unemployment, interpersonal conflicts, driving accidents, and criminality (Nigg, 2013). In addition, studies have suggested that although impulsivity is not directly associated with aggressiveness, it contributes to less overall tolerance (Spencer, Biederman, & Mick, 2007).

There is evidence that impulsive behavior has a strong genetic influence and, therefore, it is expected that first-degree relatives of psychiatric patients present with higher impulsivity expression than controls. Bora, Yucel, and Pantelis (2009) found that first-degree relatives of bipolar patients tend to present worse response inhibition than controls. In ADHD, however, the results seem to be controversial. Pauli-Pottt, Neidhard, Heinzel-Gutenbrunner, and Becker (2014) found that unaffected preschoolers with a positive family history of ADHD presented worse scores in delay aversion tasks. Opposite results were found by Pironti et al. (2016), who did not find increased impulsivity in ADHD first-degree relatives, although using a different methodology. To the best of our knowledge, there are no studies exploring impulsivity traits in unaffected ADHD parents.

It has been well established that parents with ADHD offspring have elevated symptoms themselves (Starck, Grünwald, & Schlarb, 2016). In their pioneering study, Alberts-Corush, Firestone, and Goodman (1986) reported a prevalence of 15% to 20% in mothers and 20% to 30% in fathers of children with the disorder. Because impulsivity, in addition to being part of the ADHD clinical symptomatology, has a strong genetic component, it is plausible to expect an increase of impulsivity traits in ADHD parents, qualifying it as an endophenotype (Almasy & Blangero, 2001). Phenotypic heterogeneity is characteristic of ADHD, such as in several other psychiatric disorders, favoring endophenotype-based models of the disorder (Castellanos & Tannock, 2002; Doyle et al., 2005) in line with Research Domain Criteria (RDoC). From this perspective, the aims of this study were to investigate the impulsivity levels in a sample of biological parents of ADHD offspring and analyze the profile of impulsivity, according to the parents’ ADHD status (non-ADHD [controls], remitted, ADHD subjects).

Method

We recruited biological parents of children and adolescents 7 years to 18 years old referred to an ADHD outpatient unit at the Institute of Psychiatry of the Federal University of Rio de Janeiro (IPUB/UFRJ). The present study is part of a larger family based study; detailed methodology can be found elsewhere (Segenreich et al., 2015). All individuals signed an informed consent, and the study was approved by the Ethics Committee at the Institute of Psychiatry of the Federal University of Rio de Janeiro.

A total of 180 adults (biological parents of 90 children with ADHD) were invited to the study but only 155 (86.1%) were willing to participate in the entire protocol, which included extensive clinical and neuropsychological evaluations of all family members throughout the day. ADHD was diagnosed according to the Diagnostic and Statistical Manual of Mental Disorders (5th ed.; DSM-5; American Psychiatric Association, 2013) criteria, using a semistructured interview (K-SADS for children and adolescents and K-SADS adapted for adults). All diagnoses were done by board-certified psychiatrists.

Barratt’s self-response scale 11th version (BIS-11) was used to measure impulsivity levels in parents. The parent sample was sorted into four groups: (a) Group I, individuals who met the current DSM-5 criteria for ADHD; (b) Group II, individuals who met the DSM-5 criteria in childhood, but who presented with fewer than five current symptoms in each DSM domain (remitted ADHD); (c) Group III, individuals who did not meet the criteria for ADHD either in childhood or in adulthood (controls); and (d) individuals who did not meet childhood criteria but presented current ADHD diagnosis (late-onset). We chose to aggregate subjects with late-onset ADHD in Group I due to the small number of individuals with this profile (n = 9).

Thirty-six subjects were allocated in Group I, 21 in Group II, and 98 in Group III. The prevalence of ADHD in the sample was 17.4% (13 fathers and 14 mothers)—subjects with current and past symptoms indicative of ADHD, meeting the criteria required by DSM-5. ADHD current presentation (predominantly inattentive, hyperactive, and combined) was also investigated after the allocation of individuals in their respective groups.

Statistical analysis was performed using SPSS IBM Version 23.0. To compare impulsivity level between the groups, data were analyzed using one-way MANOVA, followed by univariate ANOVAs to explore the effects of the independent variable (IV) on each dependent variable (DV). The GROUP was the IV, and the BIS subscores (attention, planning, and motor activity) were the DVs. The level of significance was set at p < .05 for the MANOVA, and Scheffé’s post hoc criterion for significance was used for the univariate ANOVAs. All tests were two tailed.

Results

Table 1 presents clinical data for all groups. Among parents with ADHD (Group I), approximately half of individuals had current hyperactive presentation, although it represented only one third of past presentations. This result contrasts to findings from a large study (Vitola et al., 2017) in our country, which demonstrated a much lower percentage of hyperactive presentation in adult ADHD. There is some evidence that the presence and magnitude of hyperactive behavior in ADHD may be influenced to a considerable extent by environmental factors (Kofler et al., 2016). Among the individuals with remitted ADHD (Group II), almost two thirds of cases had inattentive presentation in the past.

Table 1.

Prevalence of Current and Past ADHD Presentations in Parents.

	Past	Current
Group I (ADHD; n = 36)	Inattentive = 07 (25.9%) Hyperactive = 09 (33.3%) Combined = 11 (40.7%)	Inattentive = 07 (19.4%) Hyperactive = 20 (55.5%) Combined = 09 (25%)
Group II (ADHD remitted; n = 21)	Inattentive = 14 (66.6%) Hyperactive = 03 (14.2%) Combined = 04 (19%)	—

Descriptive statistics and bivariate correlations for the DVs are shown in Table 2. Results for normality assumption (K-S test displayed no significant statistics for each measure and level), homogeneity of variance–covariance matrices (Box’ M test, p = .15), linearity, and multicollinearity (variance inflation factors [VIFs] < 1.34) were satisfactory. Considering unequal sample sizes across the groups, we reported Pillai’s trace statistic (Tabachnick & Fidell, 2012). A one-way MANOVA revealed a significant multivariate main effect for GROUP, Pillai’s trace = .21 F (6, 300) = 5.88, p <. 001, η² = .11, observed power (for α = .05) = .99. Given the significance of the overall test, we performed univariate F tests for each DV to further explore the multivariate effect. The univariate tests indicated significant differences across the groups for the BIS-AT, F(2, 151) = 18.36; p < .001, η² = 0.20, observed power (for α = .05) = .99, as well as marginally significant differences on the BIS-PLA, F(2, 151) = 3.03; p = .051, η² = .04, observed power (for α = .05) = .58, and no differences for the BIS-MOT, F(2, 151) = .78; p = .459, η² = .01, observed power (for α = .05) = .18. Post hoc analyses of the effect on the BIS-AT, using the Scheffé’s post hoc criterion for significance, indicated that Group I scored higher than Group II, mean difference = 2.99, 95% CI = [0.43, 5.55], p = .017, and Group III (mean difference = 4.46, 95% CI = [2.64, 6.23], p < .001; Figure 1a). Post hoc analyses for the BIS-PLA indicated a marginally significant higher score for Group I compared with Group III (mean difference = 2.38, 95% CI = [–.03, 4.78], p = .053; Figure 1b).

Table 2.

Zero-Order Correlations and Descriptive Statistics for Each BIS Subscores (Variables) Across Groups.

ADHD (n = 36)
BIS variables	1	2	3	4
1. Attentional factor		.36*	.42*	.71**
2. Motor factor			.61**	.81**
3. Nonplanning factor				.88**
4. BIS total score
M	16.51	19.06	26.97	62.51
SD	3.92	3.88	5.24	10.55
Remitted ADHD (n = 21)
BIS variables	1	2	3	4
1. Attentional factor		−.10	.46*	.67**
2. Motor factor			−.07	.48*
3. Nonplanning factor				.74**
4. BIS total score
M	13.52	17.52	24.86	55.91
SD	3.34	4.02	3.97	7.08
Controls (n = 98)
BIS variables	1	2	3	4
1. Attentional factor		.16	.12	.70**
2. Motor factor			.48**	.30**
3. Nonplanning factor				.34**
4. BIS total score
M	12.05	18.36	24.59	53.05
SD	3.76	4.75	5.02	12.20

Note. BIS = Barrat Impulsivity Scale.

p < .05. **p < .001 (two tailed).

Figure 1.

The BIS-11 subscores for each group. (a) Box plots and data points for each group on BIS attention subscore; (b) box plots and data points for each group on BIS motor subscore; (c) box plots and data points for each group on BIS nonplanning subscore.

There was a decreasing pattern of impulsivity between groups, with a significant difference between total impulsivity scores between Groups I and III.

Analysis of Barratt’s scale (BIS-11) dimensions from the one-way ANOVA, revealed a statistically significant difference only in attentional scores comparing Groups I and II and Groups I and III. Comparisons between other dimensions did not reveal any statistical significance (Table 2).

Discussion

In this sample, we found a prevalence of adult ADHD in parents of ADHD offspring similar to other studies (Nigg, 2013). Our results support the idea that impulsivity is associated with ADHD symptoms using the gold-standard diagnosis, a semistructured interview. Adults with nonremitted ADHD presented higher levels of impulsivity (measured by BIS) compared with adults with remitted ADHD and controls. Adults with remitted ADHD showed nearly the same levels of impulsivity as the control group. The results described here are in accordance with Pironti et al. (2016), and do not support the idea that impulsive behavior is overexpressed in unaffected relatives of ADHD children. Kim et al. (2017) found similar results using a different methodology. Our results also suggest that impulsivity has a parallel course to other ADHD symptoms as individuals mature and no longer meet the diagnostic criteria, indicating that impulsivity does not qualify for and endophenotype.

Karam et al. (2017) have demonstrated that impulsivity persists through adulthood and even increase in a subgroup of adult ADHD patients. Two studies have addressed the relevance of impulsivity and ADHD in adulthood: Chamberlain et al. (2017) investigated a sample of patients who gambled more than 5 times during a year, and a total of 20.3% patients presented with ADHD symptoms at a clinical level. A significant correlation was observed between the three BIS subscales and ADHD symptoms. Agnew-Blais et al. (2016) compared adults with ADHD with their relatives and a control group. Higher levels of impulsivity were observed in the ADHD group compared with the other groups.

Parents with ADHD had higher levels of impulsivity compared with all other groups, as expected, with a predominance of the hyperactive presentation. At first, this result was considered to be unexpected due to the classic assumption of decreasing hyperactivity levels with aging; however, it was consistent with a recent study (Adler et al., 2017).

The remitted group (Group II) presented a more prevalent inattentive subtype in childhood. It is not clear if there is a greater probability of remission in this group, the design of our study does not allow the investigation of this aspect. Although a few other studies investigated the course according to subtypes of ADHD (for example, Larsson, Dilshad, Lichstenstein, & Barker, 2011) we used a different methodology, making it difficult to compare results. Our outcomes differed from those of Srebinick, Kolakowski, and Wolanczyk (2012) who found higher rates of remission in the combined presentation. More than half of nonremitted individuals in our sample presented a current hyperactive presentation; this rate was increased by the aggregation of subjects classified as late-onset ADHD. This result may indicate an increase in hyperactivity/impulsivity symptoms throughout the years, but it is not possible to exclude memory bias toward them.

Previous analyses have suggested that the risk of ADHD persistence is related to the severity of the symptoms in childhood (Lara et al., 2009; Cherkasova, Sulla, Dalena, Pondé, & Hechtman, 2013), and few studies have investigated impulsivity as an independent construct for remission. Our results indicate an impulsivity profile with greater impairment of attentional dimension only, according to BIS-11 subscores independently of ADHD subtype. This finding is in contrast to previous results from another study in our country (Malloy-Diniz et al., 2007) and brings an important issue into focus: DSM-5 impulsivity items address only motor impulsivity and no other impulsivity domains. In fact, much debate occurred prior to the publishing of DSM-5 concerning not only the number but also the dimensions of impulsivity items to be included in this last edition (Ünsel Bolat et al., 2016). Our results suggest that previous impulsivity items, first aimed at childhood and later adapted to adulthood in other DSM editions may not portray impulsivity in adult ADHD.

Late-onset ADHD (a subsample of Group I) has been recently described in a group of adults presenting the clinical picture of ADHD but with no history of ADHD during childhood (Agnew-Blais et al., 2016). Although this diagnosis remains controversial, some authors suggest the existence of two syndromes that have distinct developmental trajectories (adult form of ADHD [nonremitted] vs. late-onset young adult ADHD; Caye, Rocha, & Anselmi, 2016). Impulsivity has already been associated with the adult form of ADHD. We did not find any differences between late-onset ADHD and nonremitted ADHD, although there was a trend toward high levels of impulsivity in the former; the subjects with late-onset ADHD profile also had higher hyperactivity–impulsivity symptoms compared with the remitted and control groups but not higher inattention levels. However, this group size is a major limitation to making any conclusions concerning those individuals.

There are some limitations inherent to our study. First, it is a cross-sectional study; therefore, we can only suggest that impulsivity parallels the remission of other symptoms that characterize ADHD, and prospective studies are needed to corroborate this hypothesis. Because past ADHD symptoms were retrospectively collected in a semistructured interview (K-SADS), potential memory bias (in the form of either overvaluation or neglect) must be taken into account because we did not include collateral information. However, comparisons between self-reports and collateral reports do not provide significant differences (Breda et al., 2016). Because impulsivity by a self-report inventory does not necessarily mirror the findings from neuropsychological testing (Malloy-Diniz et al., 2015), further studies should be performed to assess impulsive behavior in the relatives of children with ADHD.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Author Biographies

Tiago Figueiredo, MD, is a psychiatrist and PhD student at D’Or Institute of Research and Education, Brazil. His research area is impulsivity and social abilities in ADHD.

Dídia Fortes, MD, is a psychiatrist at D’Or Institute of Research and Education, Brazil. Her research area is ADHD-associated impairment.

Pilar Erthal is a neuropsychologist and PhD student at D’Or Institute of Research and Education, Brazil. Her research area is decision-making in ADHD.

Tiago Bortolini, PhD, is a researcher at D’Or Institute of Research and Education, Brazil. His research area is the neural basis of group belongingness and in-group favouritism. He contribute with statistical analysis.

Daniel Segenreich, PhD, is a psychiatrist and his research area is ADHD genetics.

Leandro Malloy-Diniz, PhD, is a neuropsychologist and professor at Federal University of Minas Gerais, Brazil. His research area is ADHD and genetics.

Paulo Mattos, PhD, is a psychiatrist and professor at the Federal University of Rio de Janeiro, Brazil. He is the coordinator of neuroscience at D’Or Institute of Research and Education, Brazil.

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