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Journal of Anxiety Disorders 28 (2014) 741746

Contents lists available at ScienceDirect

Journal of Anxiety Disorders

The relationships among separation anxiety disorder, adult


attachment style and agoraphobia in patients with panic disorder
Stefano Pini a, , Marianna Abelli a , Alfonso Troisi c , Alberto Siracusano c ,
Giovanni B. Cassano a , Katherine M. Shear b , David Baldwin d
a
Department of Clinical and Experimental Medicine, Section of Psychiatry, University of Pisa, via Roma 65, I-56100 Pisa, Italy
b
Columbia University, Department of Social Work, School of Social Work, Columbia University, New York, NY, USA
c
Department of Neurosciences, University of Rome Tor Vergata, Via Montpellier 1, 00133 Rome, Italy
d
Department of Psychiatry, University of Southampton, Faculty of Medicine, Academic Centre, College Keep, 4-12 Terminus Terrace, Southampton SO14
3DT, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: Epidemiological studies indicate that separation anxiety disorder occurs more frequently in adults than
Received 19 May 2012 children. It is unclear whether the presence of adult separation anxiety disorder (ASAD) is a manifestation
Received in revised form 20 June 2014 of anxious attachment, or a form of agoraphobia, or a specic condition with clinically signicant con-
Accepted 30 June 2014
sequences. We conducted a study to examine these questions. A sample of 141 adult outpatients with
Available online 11 July 2014
panic disorder participated in the study. Participants completed standardized measures of separation
anxiety, attachment style, agoraphobia, panic disorder severity and quality of life. Patients with ASAD
Keywords:
(49.5% of our sample) had greater panic symptom severity and more impairment in quality of life than
Panic disorder
Separation anxiety disorder
those without separation anxiety. We found a greater rate of symptoms suggestive of anxious attachment
Adult attachment style among panic patients with ASAD compared to those without ASAD. However, the relationship between
Agoraphobia ASAD and attachment style is not strong, and adult ASAD occurs in some patients who report secure
attachment style. Similarly, there is little evidence for the idea that separation anxiety disorder is a form
of agoraphobia. Factor analysis shows clear differentiation of agoraphobic and separation anxiety symp-
toms. Our data corroborate the notion that ASAD is a distinct condition associated with impairment in
quality of life and needs to be better recognized and treated in patients with panic disorder.
2014 Published by Elsevier Ltd.

1. Introduction disorder, and avoidance behaviors may occur in the workplace as


well as at school. Also, in contrast to DSM-IV, the diagnostic criteria
Separation anxiety disorder is a well-established diagnostic cat- no longer specify that age at onset must be before 18 years, because
egory in the psychiatric nomenclature (Shear, Jin, Ruscio, Walters, a substantial number of adults report onset of separation anxiety
& Kessler, 2006). However, most studies of this condition pertain to after age 18 (Marnane & Silove, 2013). The disturbance must cause
childhood. By contrast, little attention has been paid to the occur- clinically signicant distress or impairment in social, academic, or
rence of adult separation anxiety disorder (ASAD). Although in other important areas of functioning. Adults with a diagnosis of
DSM-IV, separation anxiety disorder was classied in the section ASAD report extreme anxiety about separations from major attach-
Disorders Usually First Diagnosed in Infancy, Childhood, or Ado- ment gures (partner, children, or parents), fear that harm would
lescence, criteria for the disorder are now described in the DSM-5 befall those close to them and need to maintain proximity to them.
section on anxiety disorders (APA, 2013). The core features remain These symptoms may affect the individuals behavior and lead to
mostly unchanged, although the wording of the criteria has been severe impairment in social relationships. It is important to dis-
modied to more adequately represent the expression of sepa- tinguish between symptoms of ASAD and dependent personality
ration anxiety symptoms in adulthood. For example, attachment traits. Dependency is a pervasive and indiscriminate tendency to
gures may include the children of adults with separation anxiety rely excessively on others, whereas ASAD refers to a limited array of
concern about the proximity and safety of key attachment gures.
Initially, Manicavasagar, Silove, and Curtis (1997) highlighted
Corresponding author at: Department of Psychiatry, University of Pisa, Via Roma the clinical signicance of ASAD as a distinct diagnosis. This group
67, 56100 Pisa, Italy. Tel.: +39 050 993559; fax: +39 050 21581. raised the possibility that the most common pathological out-
E-mail address: stefano.pini@med.unipi.it (S. Pini). come for children with separation anxiety may be adult separation

http://dx.doi.org/10.1016/j.janxdis.2014.06.010
0887-6185/ 2014 Published by Elsevier Ltd.
742 S. Pini et al. / Journal of Anxiety Disorders 28 (2014) 741746

anxiety disorder (Manicavasagar, Silove, Curtis, & Wagner, 2000; breathing and separation distress in decreasing the suffocation
Manicavasagar, Silove, & Hadzi-Pavlovic, 1998) and documented alarm threshold.
the occurrence of ASAD in adults (Wijeratne & Manicavasagar, Given the dearth of research concerning ASAD, we have under-
2003). Our group (Cyranowski et al., 2002; Fagiolini, Shear, Cassano, taken a series of investigations to better understand this condition
& Frank, 1998; Pini, Abelli, et al., 2005; Pini et al., 2010) also found among help-seeking individuals diagnosed with other DSM IV diag-
ASAD to be surprisingly common in a large clinical population of noses (Costa et al., 2009; Pini, Abelli, et al., 2005; Pini, Martini,
outpatients with anxiety and mood disorders. The high prevalence et al., 2005; Pini et al., 2010). In the current paper, we report
of ASAD in the general population (6.6%) was also conrmed in the the results of a clinical study aimed at ascertaining whether adult
NCS-R data (Shear et al., 2006). separation anxiety can be distinguished from agoraphobia and
Another unresolved question is the nature of the relationship from anxious attachment style. In addition, we aimed at clarify-
linking separation anxiety disorder to insecure attachment in gen- ing whether the occurrence of ASAD is associated with distinctive
eral and to anxious attachment in particular (Troisi & DArgenio, features of the PD clinical picture. These data may contribute to
2004). Theoretically, it is possible that not all individuals with the current debate whether ASAD is a distinct clinical entity or
anxious attachment meet criteria for separation anxiety disor- merely a variant/subtype of PD. In addition, differential assessment
der. It is also possible that separation anxiety disorder occurs of ASAD, agoraphobia or anxious attachment style may have impor-
even in the context of secure attachment. In other words, it is tant therapeutical implications for patients with panic disorder
not known whether all individuals with separation anxiety dis- (Milrod et al., 2014).
order also engage in other anxious attachment behaviors. To our
knowledge, no empirical study has been undertaken to answer this 2. Methods
question.
Manicavasagar, Silove, Marnane, and Wagner (2009) tried The study sample included 141 consecutive adult psychiatric
to clarify the link between attachment styles and panic disor- outpatients with a diagnosis of panic disorder with or without
der/agoraphobia (PD-Ag). They studied 83 patients with PD-Ag and agoraphobia as a primary diagnosis. Participants were recruited
ASAD, highlighting that the style of anxious attachment, using the from the adult psychiatric outpatient clinics of the Department
Attachment Style Questionnaire (ASQ) (Feeney, Noller, & Hanrahan, of Psychiatry, University of Pisa. Patients with psychotic disor-
1994), was more prevalent in patients with separation anxiety and ders or substance use disorder prior to the index assessment were
panic disorder than in patients with only panic attacks. excluded. This investigation was carried out in accordance with
Similarly, the relationship between adult separation anxiety the Declaration of Helsinki. The University of Pisa Ethical Commit-
disorder, panic disorder (PD) and agoraphobia has not been well tee reviewed the study design and all subjects were informed of the
claried (Mian, Godoy, Briggs-Gowan, & Carter, 2012; Wittchen nature of study procedures and provided written informed consent
et al., 2008; Wittchen, Gloster, Beesdo-Baum, Fava, & Craske, 2010). prior to participation. Experienced residents in psychiatry per-
A prominent theme in the literature pertains to the relationship formed interviews. Subjects completed self-report questionnaires
between childhood separation anxiety and adult PD (Bruckl et al., and structured clinical interviews over 2 days.
2007). Some investigators found evidence that childhood separa-
tion anxiety disorder is associated with an increased risk of PD, with
or without agoraphobia, in adulthood (De Ruiter & Van Ijzendoorn, 2.1. Panic disorder diagnosis
1992; Klein, 1964, 1980). However, other studies have not sup-
ported this association (Aschenbrand, Kendall, Webb, Safford, & All subjects were assessed with the Structured Clinical Inter-
Flannery-Schroeder, 2003; Warner, Mufson, & Weissman, 1995). view for the DSM-IV (SCID-I) (First, Spitzer, Gibbon, & Williams,
Lipsitz et al. (1994) found a high rate of childhood separation anx- 2002) to establish DSM IV axis I primary diagnosis and comorbidity.
iety among adults with different anxiety disorders and questioned We used the Panic Disorder Severity Scale (PDSS) to assess cur-
whether childhood separation anxiety disorder is selectively linked rent severity of PD (Shear et al., 1997; Shear, Rucci, et al., 2001).
to adult PD or, alternatively, constitutes a risk factor for adult anx- We also examined current severity of depression using the Hamil-
iety disorders more generally. Findings from the NCS-R supported ton Depression Rating Scale (Hamilton, 1960). Quality of life was
the latter hypothesis. In the NCS-R, ASAD was highly comorbid with assessed by the Medical Outcomes Study Short Form (SF-36) (Ware
PD, but such a comorbidity rate was not different from the rates & Gandek, 1998).
with other anxiety or mood disorders. Thus, neither childhood nor
adult ASAD was preferentially associated with PD. 2.2. Separation anxiety
This hypothesis has been further corroborated by ndings
arguing against the notion that separation anxiety and anxious We conducted clinical interviews for adult and childhood his-
attachment are relevant to panic disorder with agoraphobia in tory of separation anxiety disorder. To do this, we used the
general, suggesting instead that that constellation is conned to Structured Clinical Interview for Separation Anxiety Symptoms
a separate group, namely that of adult separation anxiety disorder. (SCI-SAS) (Cyranowski et al., 2002). This semi-structured interview
Preter and Klein (2008) proposed a model that amplied the evaluates each of the 8 DSM IV criterion symptoms of separation
original suffocation false alarm theory (Klein, 1993). The observa- anxiety, separately for childhood and adult symptoms. Each ques-
tion of respiratory abnormalities in patients with PD was in line tion was scored as 0 (not at all), 1 (sometimes), 2 (often) or ? (dont
with the hypothesis that panic may be provoked by indicators of recall). In keeping with the DSM-IV guidelines, endorsement of
potential suffocation, such as uctuations in pCO2 and brain lac- three or more of the eight criterion symptoms (symptoms rated
tate, as well as environmental circumstances. However, the fact as 2 (often)) was used as a threshold to determine categorical
that sudden loss, bereavement and childhood separation anxiety (yes/no) diagnosis of separation anxiety disorder in childhood and
are also antecedents of spontaneous panic required an integra- adulthood. In addition, criterion B (i.e., duration of at least 4 weeks)
tive explanation. Within this framework, the authors reappraised and C (i.e., the disturbance causes clinically signicant distress or
a developmental pathophysiological link between separation anxi- impairment in social, academic, occupational), or other important
ety and PD and subsequent agoraphobia, coupled with attachment areas of functioning were required. Scores on the 8 items of each
theory and ethological views of anxiety. Central opioid system dys- subscale were also summed to produce a continuous measure of
function has been claimed to play a key role in both disordered separation anxiety symptoms (range for each subscale = 016).
S. Pini et al. / Journal of Anxiety Disorders 28 (2014) 741746 743

We further assessed separation anxiety using the Adult Separa- using the t-test for independent samples. Comparisons of categori-
tion Anxiety Questionnaire (ASA-27), a 27-item inventory, which cal variables between groups were conducted using the chi-square
rates symptoms of ASAD. This scale has been shown to display test. In particular, rates of Axis I psychiatric comorbidity were
good internal reliability as well as concurrent validity with clinical compared between the two groups with or without ASAD, before
assessments of ASAD (Manicavasagar et al., 1997; Manicavasagar, proceeding to factor analysis and attachment comparisons. The p-
Silove, Wagner, & Drobny, 2003). value was set at .05. The association of demographic and clinical
variables with ASAD was estimated using crude odds ratios (ORs)
2.3. Attachment style with 95% condence intervals (CIs). The factor structure of the adult
SCI-SAS scale and PAS-SR agoraphobia subscale was evaluated by
Attachment style was assessed using two different self-report using a generalized least square factor analysis. For this analysis
instruments. The Relationship Questionnaire (RQ) (Bartholomew the SCI-SAS items were dichotomized (0, 1 = absent, 2 = present) to
& Horowitz, 1991) is a single-item measure made up of four short have the same measurement level as PAS-SR items.
paragraphs, each describing a prototypical attachment pattern as it Statistical analyses were conducted using IBM SPSS Statistics,
applies in close adult peer relationships. Participants are asked to version 20.0 (IBM SPSS Inc., 2011).
rate degree of t for each prototype on a 7-point scale. The RQ was
designed to obtain continuous ratings of each of the four attach- 4. Results
ment patterns, and can also be used to categorize individuals into
their best tting attachment pattern. The highest of the four attach- 4.1. Characteristics of sub-groups with and without adult
ment prototype ratings can be used to classify participants into separation anxiety disorder (ASAD)
an attachment category designated A (secure), B (fearful-avoidant
attachment), C (preoccupied) and D (dismissing-avoidant) (Grifn Overall, ASAD was diagnosed in 70/141 (49.5%) of our sample,
& Bartholomew, 1994). The instrument has shown good psycho- and was more likely to occur in females (52/91; 57.1%) com-
metric properties (Picardi et al., 2002). In this study, the RQ data pared with males (18/50; 36%) (OR = 2.37, 95% CI: 1.174.83.) Age,
were used to assign each participant to an attachment style cate- educational level and marital status were similar between sub-
gory. Attachment style was determined by assigning each subject jects with or without ASAD (age: 39.45 12.60 with ASAD and
to the category with the maximum score among the four items 41.65 13.07 without ASAD; t-test = 1.013, p = .313; educational
described by the RQ (data available for 107 subjects). level: 10.76 3.71 with ASAD and 11.20 4.36 without ASAD, t-
In addition, we used the Attachment Style Questionnaire (ASQ) test = .652, p = .516; married: 31 (45.6%) and 33 (46.5%), in each
(Feeney et al., 1994) as a dimensional measure of attachment group respectively, chi-square = .11, p = .916). Subjects with ASAD
style (data available for 104 subjects). The ASQ is a 40-item self- were less likely to be employed (58.8% vs. 72.9%) although this
report questionnaire in which items are rated on a 6-point scale difference did not reach statistical signicance (chi-square = 3.03,
from 1 (totally disagree) to 6 (totally agree). Based on both the- p = .082).
oretical expectations and principal components analysis, the 40 Thirty-eight (54.3%) of the 70 participants with ASAD also
items can be assigned to ve scales: Condence, Discomfort with reported a history of childhood separation anxiety disorder, while
Closeness, Need for Approval, Preoccupation with Relationships, only 13/71 (18.3%) of those without ASAD recalled these symptoms
and Relationships as Secondary. Discomfort with Closeness maps in childhood (OR = 5.30, CI 2.4711.37 for those with ASAD com-
onto conceptualizations of avoidant attachment (Hazan & Shaver, pared with those without). Overall, 58/141 (41%) of the sample did
1987). Need for Approval reects respondents need for acceptance not meet criteria for child or adult separation anxiety disorder.
and conrmation from others that characterizes fearful avoidant
and anxious preoccupied groups. Preoccupation with Relation- 4.2. Clinical correlates of adult separation anxiety disorder
ships also maps to anxious attachment (sometimes also called (ASAD)
anxious/ambivalent attachment). The Relationships as Secondary
scale identies dismissing attachment (Bartholomew, 1990). Con- As shown in Table 1, ASAD was associated with higher frequency
dence (in Self and Others) reects a secure attachment orientation. of agoraphobia (p = .046), more panic attacks during last month
When the ASQ was administered to a large sample of university (p = .008), greater severity of panic disorder symptoms (p = .008),
students, the ve scales showed good internal consistency, with and earlier age of onset of agoraphobia (p = .018). Patients with
Cronbachs alpha coefcients ranging from .76 to .84; further, the ASAD endorsed lower scores on quality of life as assessed by SF-
10-week retest reliability coefcients of the scales ranged from .67 36 in terms of physical functioning (p = .007), role emotional
to .78 (Feeney et al., 1994). (p = .048), mental health (p = .003) and general health (p = .008.)

2.4. Agoraphobia 4.3. Adult separation anxiety and agoraphobia

Agoraphobia was assessed using the Panic-Agoraphobic Spec- ASA-27 total score signicantly correlated with SCI-PAS ago-
trum Self-Report (PAS-SR) (Cassano et al., 1999). This 114-item raphobia subscale score (r = .31.) Factor analysis including items
questionnaire was developed to assess lifetime panic-agoraphobic from both scales revealed that a two-factor model ts the data
spectrum symptoms and displays good psychometric properties well (chi-square = 163.6, df = 151, p = .228). The factor loadings are
(Frank et al., 2002; Shear, Frank, et al., 2001). Items are orga- shown in Table 2. Two items from the agoraphobia scale load on
nized into eight panic-agoraphobic symptom domains including the separation anxiety factor. These items rate feeling nervous or
a domain comprising 25 items for assessing agoraphobia. Items uncomfortable when alone outside home or somewhere far from
are rated dichotomously (yes/no). Domain scores are obtained by home or when home alone.
counting the number of positive responses.
4.4. Adult separation anxiety disorder and attachment style
3. Statistical analyses
The relationship between ASAD and attachment style has been
The mean values of continuous variables such as age and scale investigated by the RQ and the ASQ. About 20% of the sample was
scores were compared between subjects with and without ASAD not willing to complete the attachment evaluation. However, these
744 S. Pini et al. / Journal of Anxiety Disorders 28 (2014) 741746

Table 1 Table 2
Clinical and quality of life (QOL) characteristics in subjects with panic disorder (PD) Rotated factor matrix of PAS-SRa typical agoraphobia subscale and the 8 SCI-SASb
with and without adult separation anxiety disorder (ASADa ). adult section items.

Patients Patients Chi-square p Factor


with PD with with PD
no ASAD with ASAD 1 (agoraphobia) 2 (separation
(n = 71) (n = 70) anxiety)

Lifetime comorbidity Did you avoid, feel nervous or


Agoraphobia 37 (52.1%) 48 (68.6%) 3.988 .046 uncomfortable. . .a
Social phobia 14 (19.7%) 10 (14.3%) .737 .391 . . .when you were alone outside your .382 .416
OCD 13 (18.3%) 10 (14.3%) .418 .518 home or somewhere far from home?
Specic phobia 18 (25.4%) 22 (31.4%) .640 .424 . . .when home alone? .394 .415
Bipolar I 8 (11.3%) 11 (15.7%) .598 .439 . . .when you were in a crowded place? .462 .056
Bipolar II 19 (26.8%) 18 (25.7%) .020 .888 . . .when on a bridge or in a ski .421 .318
Major depression 23 (32.4%) 17 (24.3%) 1.140 .286 gondola?
. . .when you were in closed places .578 .385
(such as tunnels, subways,
Patients Patients t-Test p
underground, or in a theater)?
with PD with PD
. . .when you were in an elevator? .508 .215
with no with
. . .driving a car other than on a .692 .035
ASAD ASAD
highway? I never drove
(n = 71) (n = 70)
. . .driving a car on the highway? I .651 .150
Severity of PD never drove
Past month panic 3.98 7.95 9.62 14.74 2.695 .008 . . .being in an open place like a town .590 .200
attacks square or a wide street?
Number of panic 7.55 2.83 10.09 2.43 5.709 .008 . . .traveling as a passenger by car, bus, .510 .132
symptoms train or plane? Note: Not because of
ASA-27 20.82 11.61 45.31 12.23 12.197 .0001 fear of crashing
SASI-tot 11.445 7.90 18.81 9.82 4.918 .0001 . . .standing in line? .587 .181
Age at onset of PD 29.76 12.37 28.20 12.22 .723 .471 . . .in situations or places in which you .330 .089
Tot Hamilton 12.23 7.43 13.50 9.35 .897 .371 thought you might be embarrassed
Age at onset of 33.97 14.14 27.28 11.17 2.411 .018 by the symptoms previously
agoraphobia described?
As a child or an adult, did you ever
SF36 QOL
experience. . .b
Physical 88.57 16.76 77.58 26.43 2.767 .007
A lot of distress if you were separated .089 .664
Functioning or anticipated separation from home
Role physical 58.33 45.12 59.16 45.55 .102 .919
or loved ones
Role emotional 36.50 42.63 22.22 36.13 2.000 .048 A lot of distress because of thoughts .139 .689
Mental health 48.17 23.52 35.58 22.08 3.018 .003
that you might lose someone close to
General health 61.16 22.18 49.68 25.12 2.690 .008
you or some harm might come to
Social functioning 49.40 12.38 49.16 9.45 .119 .905
them
Vitality 43.22 23.54 35.97 23.95 1.671 .097
Persistent and excessive worry that an .194 .454
Bodily pain 71.77 30.91 68.79 32.93 .511 .610
untoward event will lead to
a
ASAD = 3 or more items scored 2 (often) at structured clinical interview for separation from a major attachment
separation anxiety disorder adult (SCI-SAS). gure (e.g., getting lost or being
kidnapped)
Persistent reluctance or refusal to go to .071 .352
school or elsewhere because of fear
individuals did not differ from those who completed the assess- of separation
ment on socio-demographic or clinical characteristics. Persistently and excessively fearful or .011 .538
There were no signicant differences in the distribution of the reluctant to be alone or without
major attachment gures at home or
four RQ-rated attachment styles among panic disorder patients
without signicant adults in other
with vs without ASAD (Anxious, 35.8% vs 26.8%; Avoidant 26.4% settings
vs 22.2%; Dismissing 26.4% vs 25.9%, Secure 11.3% vs 24.1%). Persistent reluctance or refusal to go to .003 .505
The dimensional measure ASQ revealed that the group with sleep without being near a major
ASAD scored signicantly higher on preoccupation with rela- attachment gure or to sleep away
from home
tionships (32.22 8.43 vs 28.56 7.40; t = 2.308, p = .023) and
Repeated nightmares involving the .015 .262
showed a trend toward greater need for approval (25.00 7.89 vs theme of separation
22.40 7.44, t = 1.702, p = .092), i.e. on both the scales indicative Repeated complaints of physical .201 .207
of anxious attachment. symptoms (such as headaches,
stomachaches, nausea, or vomiting)
when separation from major
5. Discussion attachment gures occurs or is
anticipated

Our study of panic disorder patients examined questions related Bold values dene items tting in the same factor.
a
to the distinctiveness of the syndrome of adult separation anxiety PAS-SR: panic-agoraphic Spectrum self-report questionnaire.
b
SCI-SAS: structured Clinical Interview for Separation Anxiety Disorder.
disorder. Results of our study support the idea that adult sepa-
ration anxiety disorder is different from anxious attachment or
agoraphobia. We found a greater rate of symptoms suggestive of agoraphobia. Factor analysis shows clear differentiation of agora-
anxious attachment among panic patients with ASAD compared to phobic and separation anxiety symptoms.
those without ASAD. However, the relationship between ASAD and Previous studies reported that ASAD is an impairing condition
attachment style is not strong, and ASAD occurs in some patients that leads to long term difculties in different areas of functioning
who report secure attachment style. Similarly, there is little evi- (Milrod et al., 2014; Pini et al., 2010; Shear et al., 2006). We found
dence for the idea that separation anxiety disorder is a form of that panic disorder patients with ASAD had greater severity of panic
S. Pini et al. / Journal of Anxiety Disorders 28 (2014) 741746 745

disorder and more impairment in quality of life than those without. to be aware of separation anxiety disorder in adults and consider
These ndings corroborate the notion that it is important for clini- the possibility that specic treatment strategies may be needed.
cians and researchers to focus on ASAD, when co-occurring with
other psychiatric disorders, as an independent source of disability. Acknowledgements
We highlight the importance of distinguishing between separation
anxiety as a symptom and separation anxiety as a disorder. Both This work was supported by grants from the Italian Ministry
ASAD and anxious attachment share separation anxiety symptoms of University and Scientic Research (prot. 2005069159) and Fon-
(Shear, 1996; Dozie, Chase Stovall, & Albus, 1999). However, our dazione IDEA (Institute for Research and Prevention of Depression
results suggest that separation anxiety, as a symptom, is not nec- and Anxiety).
essarily indicative of separation anxiety disorder. The latter is a
specic constellation of symptoms in adults, resembling the well-
described childhood condition, to which it is often related. In this References
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