Detection of Adult Attention Deficit Hyperactivity Disorder With Cognitive Complaint Experience of A French Memory Center
Detection of Adult Attention Deficit Hyperactivity Disorder With Cognitive Complaint Experience of A French Memory Center
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General review
M. Pierre a,e,f,*, J. Cogez b,e, P. Lebain c,e, N. Loisel b,e, C. Lalevée b,e,f,
A.L. Bonnet d,e, V. De La Sayette b,e,f, F. Viader b,e,f
a
Service de gériatrie, centre hospitalier universitaire, 14000 Caen, France
b
Service de neurologie, centre hospitalier universitaire, 14000 Caen, France
c
Service de psychiatrie, centre hospitalier universitaire, 14000 Caen, France
d
Service de neurologie, centre hospitalier mémorial France États-Unis, 50000 Saint-Lô, France
e
Centre mémoire Ressources et recherche, centre hospitalier universitaire, 14000 Caen, France
f
Inserm, U1077, EPHE, UNICAEN, Normandie université, PSL research university, 14000 Caen, France
Article history: Introduction. – Attention deficit hyperactivity disorder (ADHD) is a frequent neurodevelop-
Received 13 March 2018 mental mental disorder. It can persist in adulthood and be expressed as a cognitive
Received in revised form complaint.
13 July 2018 Methods. – We conducted a descriptive study in a French memory center concerning
Accepted 13 September 2018 patients seen over a period of two years. All patients for whom the final diagnosis was
Available online 2 May 2019 ADHD were included. All patients benefited from standard neuropsychological tests and a
psychiatric specific consultation.
Keywords: Results. – Thirteen patients were included with an average age of 50.2 19 years. Main
Attention deficit hyperactivity complaints related to memory, attention, focusing and organizational functioning. These
disorder difficulties had negative social, professional and academic consequences. ADHD history in
Adult descendants was noted in 46% of patients. More than 20% of subjects had motor, verbal or
Cognitive impairment mental restlessness. Neuropsychological assessment highlighted impaired performances in
Neuropsychological tests executive functions (38%), sustained attention (67%), divided attention (45%), working
Psychiatry memory (46%) and information processing speed (75%). A psychiatric history or comorbi-
dities were present in 85% of patients, mostly of the anxio-depressive type. The more
prevalent presentations of ADHD were the combined (38%) and inattentive (38%) types.
Discussion. – Adult ADHD can masquerade as a cognitive impairment, including a stable
cognitive complaint from infancy to old age. Inattentive, hyperactive and impulsive symp-
toms change with time and become more internalized (such as concentration difficulties or
mental restlessness). No neuropsychological pattern has been reported but fluctuating
* Corresponding author. Pôle médecine de spécialité-SSR, service de gériatrie, CHRU, avenue Côte-de-Nacre, 14033 Caen cedex 9, France.
E-mail address: [email protected] (M. Pierre).
https://doi.org/10.1016/j.neurol.2018.09.021
0035-3787/# 2019 Elsevier Masson SAS. All rights reserved.
revue neurologique 175 (2019) 358–366 359
deficits in sustained, divided attention, working memory and information processing speed
are frequently observed in adult ADHD. A specific psychiatric expertise is essential in
diagnosis and care for ADHD and its commonly associated psychiatric comorbidities.
# 2019 Elsevier Masson SAS. All rights reserved.
The American Psychiatric Association Diagnostic and Statis- 2.1. Outline of study
tical Manual of Mental Disorders [1] (DSM-V) defines attention
deficit disorder with or without hyperactivity (ADHD) as a We carried out a retrospective descriptive study in a French
syndrome occurring during childhood and which consists of MRRC (Memory Resources and Research Center) between
three symptoms: hyperactivity, inattention and impulsivity. January 1st, 2013 and December 31st, 2015. We included
In the absence of a specific biomarker, this triad is the sole consecutively all patients for whom the diagnosis retained at
element for the diagnosis of ADHD. The variable combinations the end of the investigations concluded an attention deficit
of these symptoms, their educational and social repercus- disorder with or without hyperactivity. We excluded patients
sions, are the cause of the different clinical presentations: a diagnosed with ADHD since childhood. Patients were initially
predominantly attentional subcategory, a predominantly evaluated by one of the three neurologists working in the
hyperactive subcategory and finally a mixed subcategory that memory center and all underwent neuropsychological assess-
associates both inattention and hyperactivity symptoms. ment. The neurologist determined what complementary
ADHD is the most frequent neurodevelopmental disorder examinations were appropriate. After neurological disease
with an estimated global prevalence in children of between 5 was excluded, all patients were referred to the referral
and 6% which has been steadily increasing (an increase of 33% psychiatrist for diagnostic confirmation.
between 1997–1999 and 2006–2008) [2,3].
Historically described as a disorder restricted to the 2.2. Data collection
childhood period, its diagnosis in adulthood was long
controversial [3]. Many longitudinal studies have now confir- Using a standardized sheet for data collection, we found and
med the chronic nature of ADHD symptoms throughout life, gathered the following demographic data: age at first
including at an older age [4]. The persistence of the symptoms appointment, gender, family status, level of education as
after adolescence is observed depending on the clinical form defined by French institute for national statistics (INSEE),
considered, in 50% to 80% of the cases [3,5]. Thus, the family history (including occurrences of ADHD). Elements
prevalence of ADHD in adulthood is estimated between 2– related to childhood development, presence of motor rest-
5% and 3–4% worldwide [3,6]. The typical presentation of lessness or attention disorders during this period were also
ADHD in adults meets different criteria from those observed in noted.
children. Symptoms associated with hyperactivity/impulsi- We collected the data concerning the reason for seeking
vity decrease and are expressed by disorganization and care: existence of a cognitive complaint, duration of disease
restlessness (motor or mental), while those associated with course and presence of a triggering factor, domain concerned
an attention deficit persist and now tend to become more by the complaint (memory, attention, concentration, organi-
prevalent [5,7]. Over time, the target symptoms of ADHD thus zation, language, sleep, and emotion), repercussions (school,
become more ‘‘cognitive’’ than ‘‘behavioral’’. professional, social, acts of everyday life). Clinical examina-
Compared to healthy young adults, these patients appear tion and interrogation sought the existence of motor, mental
to exhibit more attentional, executive and/or memory or verbal restlessness.
difficulties [8,9]. Probably because of the age of the subjects, In terms of neuropsychological evaluation, verbal episodic
these anomalies are not found in common practice and there memory was measured by the French version of the Free
is currently no specific neuropsychological pattern for adult and Cued Selective Reminding Test (RL-RI16) or the
patients with ADHD [10]. Moreover, depending on the personal California Verbal Learning Test (CVLT) and visual episodic
environment, more frequent comorbidities in this population memory using Recall of the Complex Figure of Rey-Osterrieth
and compensatory strategies spontaneously implemented, (ROCF). ThExecutive functions were evaluated using the
certain signs can be integrated into the overall functioning of Wisconsin card sorting test: flexibility by the number of
the patient and make the diagnosis procedure more complex. categories completed and the number of persistent errors,
Although it is not uncommon today for psychiatrists to make inhibition by the number of perseverative errors and
late diagnosis, it is, on the contrary, little known by other adult maintenance of set.
care centers, particularly for memory [11,12]. Yet the pre- Concerning attention mechanisms: working memory was
dominant cognitive expression can be the reason for seeking evaluated using digit-spans and the Brown-Peterson para-
care in a memory center. In this study, we wanted to evaluate digm, K-T test sustained attention, Brown-Peterson paradigm
specifically the clinical and neuropsychological elements divided attention, and K-T test information processing speed.
allowing memory-based screening of adults with ADHD. Language, more specifically the creation of categories, was
360 revue neurologique 175 (2019) 358–366
[(Figure_1)TD$IG]
Table 1 – Demographic and general data of patients.
Demographic data
Age at first consultation 50.2 19 [22; 75]
(mean SD) [min; max]
Sex (M/F) 3/10
Marital status n (%)
Married 11 (85)
Divorced 1 (8)
Single 1 (8)
Education level – Insee (mean SD) 4.2 0.8
Family history: dementia, psychiatric 7 (54)
disorders n (%)
Including ADHD n (%) 6 (46)
Reason for consultation
Cognitive complaint n (%) 13 (100)
Duration n (%)
< 5 years 3 (23)
5–10 years 4 (31)
> 10 years 6 (46)
Triggering factor n (%) 5 (38)
Domain concerned n (%)
Memory 11 (85)
Attention 9 (69)
Concentration 10 (77)
Organization 7 (54)
Language 6 (46)
Sleep insomnia 4 (31)
Emotional regulation 1 (8)
Clinical sign
Figure 1 – Flowchart of patient selection. Motor restlessness n (%) 3 (23)
Verbal restlessness n (%) 3 (23)
Excessive mind-wandering n (%) 4 (31)
Childhood
Motor restlessness n (%) 6 (46)
evaluated using semantic and formal verbal fluencies. Visio- Attentional disorders n (%) 5 (38)
Repercussions
constructive capacities were evaluated using a copy of the
Academic n (%) 11 (79)
Complex Rey-Osterrieth Figure. We noted impaired perfor-
Professional n (%) 10 (71)
mances and defined as ‘‘frailty’’ in subjects for whom the Social n (%) 7 (50)
results were within age and level standards but nevertheless Acts of everyday life n (%) 4 (29)
showed qualitative abnormalities. Sleep insomnia n (%) 4 (31)
The psychiatric analysis sought the presence of comorbi- Emotional instability n (%) 1 (8)
dities and psychiatric antecedents: addiction, mood disorders,
anxiety and neurotic/psychotic disorders.
Screening for ADHD was conducted using two question-
naires. The Adult Self-Report Scale (ASRS-v1.1) [13] 3. Results
(Appendix A) is a self-report scale of symptoms very similar
to ADHD which are present at the time of consultation. The Of the 583 new patients who consulted with the MRRC over a
short version consists of six questions. If at least four answers period of three years, 13 were diagnosed with ADHD after
were in line with an ADHD symptom, a long 18-item version explorations (Fig. 1). Their demographic and general data are
was systematically suggested. presented in Table 1. The sample consisted of 10 women and
The Wender Utah Rating Scale (WURS) [14] (Appendix B) is a three men, with an average age of 50.2 19 years with values
scale that retrospectively assesses the presence of symptoms ranging from 22 to 75 years. A family history of ADHD was
during childhood according to four criteria (emotional and present in 46% of them, in all cases of offspring (children or
affective, impulsivity-conduct disorders, impulsivity/hyper- grandchildren). The reason for consultation was a cognitive
activity and attention deficits.). The scores can vary between 0 complaint in the 13 patients. This complaint affected memory
and 100. A critical threshold of 46 has been suggested by some for 85% of them. Attention difficulties were noted in 69% of the
authors but remains only a possibility [15]. cases, 77% exhibited a lack of concentration, and 54% a lack of
The diagnosis of ADHD was based on a structured interview organization. An important change in work or family life for
tool, either the WSR (Weiss Symptom Record) [16], or the DIVA two and three of them respectively was the factor revealing the
2.0 (Diagnostic Interview Voor ADHD) [17]. These two inter- cognitive complaint. Motor, verbal or mental restlessness was
views allowed the assessment of the presence or absence of noted in more than 20% of patients at the time of the memory
the 18 diagnosis criteria according to DSM-IV. At the end of the consultation. Cerebral magnetic resonance imaging was per-
psychiatric assessment, patients were prescribed medication formed in six patients and CT in two patients; none showed any
or not. abnormality that could explain the symptomatology.
revue neurologique 175 (2019) 358–366 361
Table 2 – Neuropsychological test results of ADHD Table 3 – Data collected after psychiatric expertise.
patients. Psychiatric history and comorbidities
Episodic memory Psychiatric history 11 (85)
Verbal (n = 17) Depressive episode n (%) 7 (54)
Impaired n (%) 3 (23) Anxiety n (%) 5 (38)
Frailty n (%) 1 (8) Phobia n (%) 2 (15)
Visual (n = 17) Psychiatric comorbidities 11 (85)
Impaired n (%) 1 (8) Addiction n (%) 6 (46)
Frailty n (%) 2 (15) Depressive episode n (%) 6 (46)
Executive functions Anxiety and neurotic disorders n (%) 4 (31)
Flexibility (n = 17) Psychotic disorders n (%) 1 (8)
Impaired n (%) 4 (31) ADHD diagnosis
Frailty n (%) 0 (0) ASRS-v1.1 (mean SD)
Inhibition (n = 17) Short version/6 4.54 1.3
Impaired n (%) 5 (38) Long version/18 12.3 2.9
Frailty n (%) 0 (0) WURSS 25 (mean SD) 51.9 18.7
Maintenance of set (n = 17) DSM-IV n (%)
Impaired n (%) 4 (31) Predominant attentional type 5 (38)
Frailty n (%) 2 (15) Predominant hyperactive type 2 (15)
Attention Combined type 5 (38)
Working memory (n = 17) Residual syndrome 1 (8)
Impaired n (%) 6 (46) Therapeutics
Frailty n (%) 2 (15) Methylphenidate n (%) 3 (23)
Sustained attention (n = 13) Psychoeducation n (%) 10 (77)
Impaired n (%) 6 (67) Cognitive behavioral therapy n (%) 3 (38)
Frailty n (%) 2 (22) ASRS: Adult Self-Report Scale; WURSS: Wender Utah Rating Scale;
Divided attention (n = 15) DSM: diagnostic and statistical manual of mental disorders.
Impaired n (%) 5 (45)
Frailty n (%) 1 (9)
Processing speed treatment (n = 16)
Impaired n (%) 9 (75)
Frailty n (%) 0 (0)
Language hyperactive type. One patient had a probable residual
Verbales fluencies (n = 9) syndrome. Therapeutically, 23% of patients received methyl-
Impaired n (%) 2 (13) phenidate drug therapy, 38% cognitive behavioral therapy and
Frailty n (%) 0 (0)
77% psychoeducation.
Visuoconstructional abilities
Copy of ROCF (n = 16)
Impaired n (%) 0 (0)
4. Discussion
Frailty n (%) 0 (0)
a neurodegenerative disease. In this context, certain clinical which is not the case in megalomania experienced in manic
features noted in the patient’s past and present history may episodes.
guide the clinician towards the diagnosis of ADHD. Inattention is the central symptom in adult ADHD [5,7].
The sex ratio for children is four to nine boys for one girl [1]. This disorder brings together a very rich set of manifestations
In our population, this sex ratio was reversed (10 women for which constitute the main part of the complaint. In our
three men). This change could be partly explained by the population, attention disorders were at the center of the
underestimation of the number of girls with childhood onset. complaint in 69% of the cases, dealing with commonplace
Indeed, the latter mostly present predominantly the inat- things like loss of objects, forgetting appointments or
tentive type, which is the most difficult type to diagnose [17]. difficulties in reading. More specifically, attention disorders
In adulthood, these attention disorders can become more were manifested by difficulties in concentration in 77% of
disabling and constitute a reason for consultation in memory patients and organization in 54% of patients. These difficulties
centers. No patient was aware of symptoms that had begun in are frequently reported in adults with ADHD when faced with
childhood. Interrogation should, however, focus on specific new demands and responsibilities [20]. One of the particula-
symptoms of inattention or restlessness during childhood, rities of ADHD attention disorders is its fluctuating nature.
often referred to schools. Contrary to usual practices in Conners et al. report that, usually, symptoms worsen
memory consultation, the search for a family history will in situations lacking intrinsic attractiveness or novelty, in
focus more on the descendants than on the ascendants. In our monotonous and repetitive tasks. On the contrary, the
population, 46% had at least one child or grandchild with symptomatology diminishes or even disappears if the subject
ADHD. ADHD has, in fact, a major genetic component with an is in a new or particularly interesting environment [20]. It is
estimated heritability of 0.8 [5]. The genes involved seem to be thus rarer to observe these attention disorders during
coding for proteins, a significant element in the regulation of consultation.
dopaminergic and serotonergic pathways. Retrieving the patient’s life history may reveal additional
This early and non-progressive complaint was always elements resulting from the association of several of these
cognitive and concerned mainly memory, attention and symptoms. In the school setting, 79% of patients were
concentration abilities. Some subjects had difficulty finding affected, mostly with delays in acquisitions, repetition and
words in conversation. Each of these cognitive complaints children judged as ‘‘stunned’’ in class. The number of years of
may be the expression, in adulthood, of the syndromic triad study is often lower than in the general population [18]. On the
hyperactivity/impulsivity/inattention. social level, we noted interpersonal difficulties in 50% of our
Restlessness or hyperactivity seems to decrease by 50% patients, associating conflicts with the environment, pro-
between childhood and adulthood [18]. Although characte- blems of insertion and relational or couple stability [19]. The
ristic, motor restlessness (‘‘incessant fidget’’) was noted only family network is often reduced, especially among people
in three of our patients. In adulthood, restlessness seems to be over the age of 60 [21]. Initial sleep insomnia was found in four
more internalized [19]: in verbal form (over-talkativeness to of our patients. If it does not represent a diagnostic criterion, it
logorrhea) as in three of our patients or in the form of more is present in more than 70% of adults with ADHD [3]. Although
subjective elements (feeling of motor impatience, nervous- only one of our patients had an emotional complaint,
ness, voltage. . .). Another form this time of psychic nature emotional dysregulation is a common associated feature of
concerned 31% of our patients: excessive mind-wandering. ADHD with frustration intolerance (aggravated by agitation),
This form of mental hyperactivity, classically described in irritability and high mood lability [1,3,22]. For all these
adults with ADHD, is defined by ‘‘a mind that drifts away from reasons, adult ADHD can have a major socio-economic
a task and focuses on internal thoughts and images that are impact [23].
unrelated to the task or situation at hand’’ [3]. Restlessness can
also be expressed in everyday life by a rapid loss of interest in 4.2. Neuropsychological evaluation
various activities leading to the multiplication of activities
(leisure or work), procrastination, the avoidance of sedentary ADHD is a clinical diagnosis. The DSM-V unambiguously
trades and a craze for social relations [2]. states that the results obtained in neuropsychological tests do
Impulsivity appears to decrease by 40% in adulthood. Like not have diagnostic value. Although the literature highlights
restlessness, it takes over time a form which tends to be more some profiles, these results are not always reliable on an
verbal than motor (20). In our population the three patients individual scale [9]; they can be a valuable aid in the diagnostic
who complained of verbal impulsivity also complained of process.
verbal restlessness; these signs are easily spotted at inter- In our population, all attention aspects were disrupted by
rogation. Language is presented as disconnected, with many neuropsychological tests. These results are similar to those
digressions with patients who speak without thinking, answer found in the literature, where alterations in sustained
before the question is fully posed, interrupt their interlocutor, attention, vigilance, working memory, speed of mental
lose the thread of discourse. . . Motor impulsivity can be processes, mental flexibility. . . [9,24–26]. The working memory
integrated for a long time in the personality of the patient who evaluated by the backward digit-span task and the Brown
is described as passionate and unreflective. In our population, Peterson paradigm was altered in 46% of our patients. One of
restlessness had not resulted in any of the dangerous the most common findings in the literature [8,27] is that it is
consequences conventionally reported in this syndrome: easy to seek in consultation. According to some authors, poor
offenses, reckless expenditures, dangerous driving. . . [19]. performances on digit-span task are associated with a lack of
The patients are aware of all these facts and suffer from them, attention resources, which is responsible for impaired
revue neurologique 175 (2019) 358–366 363
encoding [28]. Information processing speed was the most caffeine. After qualitative analysis, non-significant errors
impaired component in our sample. This process appears to were noted.
often be deficient in ADHD patients and this deficit seems to
increase with the complexity of the task [29]. Sustained 4.3. Psychiatric expertise
attention and divided attention were impaired in 67% and 45%
of patients, respectively. These attention deficits, which define As recommended by the European consensus, all patients
ADHD, are correlated with the severity of the disorder and the were given psychiatric expertise to diagnose ADHD, evaluate
presence of symptoms in childhood [30]. psychiatric comorbidities and develop appropriate therapeu-
In our population during the Wisconsin test, 38% of tic management [17]. Screening is based on self-assessment
patients had impaired performances in flexibility, inhibition scales made up of items that put these difficulties in a
or strategy maintenance. Although the majority of studies situation; they are filled in by the patient and by means of
show at least one executive dysfunction in this population, it directed interviews. The presence of a family member is
seems to concern mainly the tests requiring attention control strongly recommended. ASRS-V1.1 looks for already present
[26,31]. Attention deficit can be a major contributor to signs. In our population, the mean score for the short version
executive difficulties such as planning, inhibition, flexibility, was 4.5/6 (above the threshold of 4) and the average score for
problem solving and decision-making on a regular basis in the long version was high (12.3/18). The presence of
these children and adults [25,29]. At the individual level, it is diagnostic signs (before seven years according to the DSM-
less systematic to highlight a deficit in executive functioning. IV, before 12 years according to the DSM-V) was detected
The implementation of compensatory mechanisms under- using the WURSS questionnaire completed by the patient.
pinned by executive control processes whose maturation Because of its retrospective nature, the presence of a family
differs from one person to another seems to be one of the member is strongly recommended by the DSM, as well as
explanations for the heterogeneity of the results and by bringing school records books. These scales have a sup-
extension of the late diagnosis [3]. Another explanation lies in plementary role, but the diagnosis is finally established with
the controversial hypothesis that hyperactive forms have less the DSM-IV (now V). The diagnosis of ADHD requires having
executive performance, whereas attention forms are more five to seven symptoms in two areas of inattention/hyper-
likely to be deficient in memory, attention spots and in the activity/impulsivity. It also requires significant clinical or
speed of information processing [26]. psychosocial repercussions and must be present in at least
Intellectual functioning, perception, memory, language, two areas of daily life. In our study, five subjects had an
praxis, and visuo-constructive abilities are generally well attention type, five a combined type and only two had a
preserved. However, the impact of executive and attention predominantly hyperactive type. These results are consistent
difficulties on other cognitive functions can lead to disorga- with the established notion of a decrease in hyperactive type
nized speech or the presence of intrusions into memory tasks over time.
[24]. Despite the memory complaint, only three patients had During the consultation, the search for medical history or
difficulties in verbal episodic memory and one in visual psychiatric comorbidities is essential. It is not reserved to
modality. From a qualitative point of view, these abnorma- psychiatric expertise only (although less specific), it is
lities were not related to a genuine episodic memory deficit necessary for the diagnostic procedure, for the interpretation
(hippocampal) but more related to a deficit in the recovery of of neuropsychological tests and can lead to specific and
an executive or attention alteration [26]. Concerning language, adapted medical care. In our population, 85% of patients had at
a ‘‘word-finding’’ problem can be linked to learning lags in least one psychiatric comorbidity. The presence of psychiatric
childhood in these patients. In our study, language was comorbidities is very high in patients with ADHD [5,34]. In the
evaluated by the verbal fluency test, which requires executive large cohorts, the three most frequent were found to be similar
capabilities both for the recovery and for categorizing to those observed in our sample: addiction, generalized
knowledge [32]. However, only two patients were deficient anxiety and mood disorders [5,6,34,35]. Depression in more
in this test, one of them suffering from developmental than half of the cases in the elderly suffering from ADHD
dyslexia. constitutes the main pejorative factor of this disorder [23,36].
The presence of comorbidities must be integrated in the One of the difficulties with the diagnosis of ADHD is the
consideration of these results. Indeed, most psychiatric presence of common symptoms observed in this disorder and
comorbidities (mood disorders, addiction, schizophrenia) those observed in many other psychiatric diseases. Unlike the
have neuropsychological deficits, mainly executive and latter, the symptoms of ADHD are typically early and
attention, which interfere with the correct interpretation persistent over time. There is no sudden change in behavior
of the results [26,33]. Similarly, low level of education and [3].
possible learning disabilities must also be taken into The current recommendations indicate that the first
account. treatment focuses on comorbidities and psycho-education,
Finally, three patients had no deficit score. This apparent the aim of which is to obtain adaptive strategies. On the
normality of the tests could be explained by the attention and medicinal level, although the reference treatment is currently
motivational fluctuations usual in ADHD. Indeed, attention 80% efficient (as in children) [2,16,17], only three of our
can vary on the order of seconds, fluctuating from one trial to patients have been treated with psychostimulants (methyl-
the next of a cognitive task; minutes, declining over the course phenidate). Some people did not want to take this treatment,
of a taxing or monotonous task; and hours, varying throu- others were not able to take it because of a history of high
ghout the day with the circadian rhythm and drugs like blood pressure. The abuse of addictive substances which was
364 revue neurologique 175 (2019) 358–366
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