Article

Prevalence, Comorbidity and Heritability of Hoarding Symptoms in Adolescence: A Population Based Twin Study in 15-Year Olds

Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
PLoS ONE (Impact Factor: 3.23). 07/2013; 8(7):e69140. DOI: 10.1371/journal.pone.0069140
Source: PubMed
ABSTRACT
Hoarding Disorder (HD) is often assumed to be an 'old age' problem, but many individuals diagnosed with HD retrospectively report first experiencing symptoms in childhood or adolescence. We examined the prevalence, comorbidity and etiology of hoarding symptoms in adolescence.
To determine the presence of clinically significant hoarding symptoms, a population-based sample of 15-year old twins (N = 3,974) completed the Hoarding Rating Scale-Self Report. Co-occurring Obsessive Compulsive Disorder (OCD), Autism Spectrum Disorders (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) were estimated from parental report. Model-fitting analyses divided hoarding symptom scores into additive genetic, shared, and non-shared environmental effects.
The prevalence of clinically significant hoarding symptoms was 2% (95% CI 1.6-2.5%), with a significantly higher prevalence in girls than boys. Exclusion of the clutter criterion (as adolescents do not have control over their environment) increased the prevalence rate to 3.7% (95% CI 3.1-4.3%). Excessive acquisition was reported by 30-40% among those with clinically significant hoarding symptoms. The prevalence of co-occurring OCD (2.9%), ASD (2.9%) and ADHD (10.0%) was comparable in hoarding and non-hoarding teenagers. Model-fitting analyses suggested that, in boys, additive genetic (32%; 95% CI 13-44%) and non-shared environmental effects accounted for most of the variance. In contrast, among girls, shared and non-shared environmental effects explained most of the variance, while additive genetic factors played a negligible role.
Hoarding symptoms are relatively prevalent in adolescents, particularly in girls, and cause distress and/or impairment. Hoarding was rarely associated with other common neurodevelopmental disorders, supporting its DSM-5 status as an independent diagnosis. The relative importance of genetic and shared environmental factors for hoarding differed across sexes. The findings are suggestive of dynamic developmental genetic and environmental effects operating from adolescence onto adulthood.

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Prevalence, Comorbidity and Heritability of Hoarding
Symptoms in Adolescence: A Population Based Twin
Study in 15-Year Olds
Volen Z. Ivanov
1,2
*, David Mataix-Cols
3
, Eva Serlachius
1
, Paul Lichtenstein
2
, Henrik Anckarsa
¨
ter
4
,
Zheng Chang
2
, Clara Hellner Gumpert
1
, Sebastian Lundstro
¨
m
4,5
, Niklas La
˚
ngstro
¨
m
2
, Christian Ru
¨
ck
1
1 Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden, 2 Department of Medical Epidemiology and Biostatistics, Karolinska Institutet,
Stockholm, Sweden, 3 Departments of Psychosis Studies and Psychology, King’s College London, Institute of Psychiatry, London, England, 4 Centre for Ethics Law and
Mental Health, University of Gothenburg, Gothenburg, Sweden, 5 Gillberg Neuropsychiatry Centre, Institution of Neuroscience and Physiology, University of Gothenburg,
Gothenburg, Sweden
Abstract
Background:
Hoarding Disorder (HD) is often assumed to be an ‘old age’ problem, but many individuals diagnosed with HD
retrospectively report first experiencing symptoms in childhood or adolescence. We examined the prevalence, comorbidity
and etiology of hoarding symptoms in adolescence.
Methods:
To determine the presence of clinically significant hoarding symptoms, a population-based sample of 15-year old
twins (N = 3,974) completed the Hoarding Rating Scale-Self Report. Co-occurring Obsessive Compulsive Disorder (OCD),
Autism Spectrum Disorders (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) were estimated from parental report.
Model-fitting analyses divided hoarding symptom scores into additive genetic, shared, and non-shared environmental
effects.
Results:
The prevalence of clinically significant hoarding symptoms was 2% (95% CI 1.6–2.5%), with a significantly higher
prevalence in girls than boys. Exclusion of the clutter criterion (as adolescents do not have control over their environment)
increased the prevalence rate to 3.7% (95% CI 3.1–4.3%). Excessive acquisition was reported by 30–40% among those with
clinically significant hoarding symptoms. The prevalence of co-occurring OCD (2.9%), ASD (2.9%) and ADHD (10.0%) was
comparable in hoarding and non-hoarding teenagers. Model-fitting analyses suggested that, in boys, additive genetic (32%;
95% CI 13–44%) and non-shared environmental effects accounted for most of the variance. In contrast, among girls, shared
and non-shared environmental effects explained most of the variance, while additive genetic factors played a negligible
role.
Conclusions:
Hoarding symptoms are relatively prevalent in adolescents, particularly in girls, and cause distress and/or
impairment. Hoarding was rarely associated with other common neurodevelopmental disorders, supporting its DSM-5
status as an independent diagnosis. The relative importance of genetic and shared environmental factors for hoarding
differed across sexes. The findings are suggestive of dynamic developmental genetic and environmental effects operating
from adolescence onto adulthood.
Citation: Ivanov VZ, Mataix-Cols D, Serlachius E, Lichtenstein P, Anckarsa
¨
ter H, et al. (2013) Prevalence, Comorbidi ty and Heritability of Hoarding Symptoms in
Adolescence: A Population Based Twin Study in 15-Year Olds. PLoS ONE 8(7): e69140. doi:10.1371/journal.pone.0069140
Editor: Stacey Cherny, University of Hong Kong, Hong Kong
Received March 27, 2013; Accepted June 4, 2013; Published July 10, 2013
Copyright: ß 2013 Ivanov et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by the Swedish Council for Working Life (http://www.fas.se/en/), the Research Council of the Swedish National Alcohol
Monopoly, funds under the Agreement on Medical Training and Research Agreement, the Swedish Research Council (http://www.vr.se/inenglish.4 .
12fff4451215cbd83e 4800015152.html) and the Swedish Society of Medicine (Stiftelsen So
¨
derstro
¨
m-Ko
¨
nigska Sjukhemmet)(http://www.sls.se/Om-SLS/In-
English/) and Riksbankens Jubileumsfond (http://www.rj.se/english/). The funders had no role in study design, data collection and analysis, decision to publish,
or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: volen.ivanov@ki.se
Introduction
Hoarding has been defined as the acquisition of and failure to
discard a large number of possessions, difficulties using living
spaces due to clutter and significant impairment and/or emotional
distress due to the hoarding behavior [1]. Hoarding can be a
serious health problem and may result in social isolation, family
burden, eviction, and even death in extreme cases [2]. Although
traditionally studied in the context of Obsessive-Compulsive
Disorder (OCD), mounting research indicates that hoarding is in
fact seldom OCD-related [3]. The idea that hoarding might be a
separate psychopathological entity has led to the inclusion of a new
disorder in DSM-5 named Hoarding Disorder (HD) [4]. The
diagnostic criteria for HD have been empirically tested and found
to be valid, reliable and perceived as useful and acceptable by both
professionals and sufferers alike [5,6].
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Hoarding is often considered a problem of old age; most
clinically referred samples consist of adults or older adults.
However, anecdotal evidence and some retrospective studies
suggest that the origins of hoarding may be in childhood or
adolescence [7,8]. Indeed, many patients report specific events in
childhood (such as parents forcefully discarding possessions) as the
origin of their current problematic behavior [9]. HD is thought to
follow a chronic and progressively deteriorating course over time,
with a retrospectively reported onset between ages 11 and 15 [8].
In adults, hoarding may be highly prevalent with estimates of point
prevalence ranging from 2% to almost 6% [10,11]. The actual
prevalence of hoarding symptoms during childhood and adoles-
cence in the general population remains unknown. Because
parental control over the living space may limit the extent and
consequences of hoarding in young people, any prevalence
estimates should take this into account.
The most commonly reported psychiatric comorbidities of HD
are Major Depressive Disorder, Generalized Anxiety Disorder,
Social Phobia and Attention Deficit Hyperactivity Disorder
(ADHD), whereas OCD is less frequently associated with hoarding
[6,12]. Several studies have examined the presence and correlates
of hoarding symptoms among children and adolescents with OCD
[13–15]. Hoarding in children with OCD is associated with lower
insight and higher levels of externalizing disorders compared to
children with OCD who do not hoard [16]. Hoarding symptoms
have also been described in clinical samples of youth and adults
with Autism Spectrum Disorder (ASD) [17] and ADHD [18].
However, it seems important to establish to what extent hoarding
symptoms in childhood/adolescence are associated with these
common neuropsychiatric disorders in the general population, free
from the selection biases involved with clinically ascertained
samples.
Research into the etiology of HD is still in its infancy.
Uncontrolled clinical studies suggest that hoarding runs in families,
[19–21] and twin studies indicate that approximately 50% of the
liability to hoarding symptoms can be attributed to genetic factors
whereas unique (or non-shared) environmental factors explain the
remaining variance [10,22,23]. While the largest twin study was
conducted in adult females [10,22], Taylor et al. [23] found no
evidence of gender differences in the heritability of hoarding.
However, it is well known that heritability estimates of behavioral
traits can change substantially with age, and that gender
differences in heritability patterns may be present in adolescents
but not in adults [24–27]. Thus, data on the heritability of
hoarding symptoms in younger people could potentially increase
our knowledge of the dynamic etiological factors that may be at
play across the lifespan.
The first aim of this study was to elucidate prevalence and
comorbidity of hoarding symptoms in a large twin sample of
adolescents. The second aim was to estimate the relative
contributions of genetic and environmental factors to hoarding
symptoms and to test whether sex-differences in heritability
patterns exist in this age group.
Methods
Participants
Participants were 15-year old monozygotic (MZ) or dizygotic
(DZ) twins enrolled in the Swedish Twin Registry and taking part
in the ongoing Child and Adolescent Twin Study in Sweden
(CATSS). CATSS is a prospective, longitudinal study of all twins
born in Sweden since 1992 whose parents were first contacted and
interviewed when twins reached the age of 9 or 12 years [28]. We
used data on hoarding symptoms from the follow-up at age 15,
when twins themselves were contacted and asked to fill out a
measure of hoarding symptoms. This age group is ideal to study
the development of hoarding symptoms given the available
retrospective accounts of adolescent symptom onset given by
adult patients with HD [8,29].
The current study sample is comprised of (1) twins who,
according to parental interviews, screened negative for neurode-
velopmental disorders at age 9/12 (n = 3,713) and (2) twins from
the same cohort, who screened positive for a neurodevelopmental
disorder and age-matched random healthy twins (n = 261). Twins
from the latter group were invited to participate in a clinical face-
to-face examination at age 15 and hoarding symptoms were
captured with the same questionnaire but in connection to the
clinical examination. Twin zygosity was determined either by
using single nucleotide polymorphisms (SNPs) [30] or (if DNA was
unavailable) an algorithm based on twin similarity with predictive
value greater than 95% compared to DNA testing [31].
Ethical approval was obtained from the Regional Ethics Review
Board in Stockholm under contracts Dnr 02–289, 2009–793 and
03–672. In accordance with the board’s decision and Swedish
regulations, written informed consent was obtained directly from
the 15-year olds involved in this study and not from their parents.
However, parents were informed about the study and what was
being collected. Parents provided written informed consent
regarding their own participation in the parental interviews when
twins were 9 and 12 years old.
A total of 3,974 participants (response rate = 47% of all Swedish
twins in the age group) were included in the current study. Of
these, 45% (n = 1,805) were boys and 55% (n = 2,169) girls.
Furthermore, 30% (n = 1,210) were monozygotic (MZ) twins, 30%
(n = 1,119) dizygotic same-sex (DZ), 26% (n = 1,022) dizygotic
opposite sex (DZOS) twins and 14% (n = 543) had unknown
zygosity. There were no significant differences between partici-
pants who responded to the hoarding questionnaire in the
CATSS-battery compared to those who did not (n = 218) in terms
of dwelling area (in both groups, 69% lived in a city rather than a
rural area), having a mother born abroad (9% vs.10%, respec-
tively), a father born abroad (8% vs. 11%), parental income, or
paternal educational level. However, a larger proportion of
mothers to responders had a university education compared to
non-responders (47 vs. 39%, z = 22.12, df = 1, p,0.05). Co-
occurring OCD at age 9/12 was also equally common in both
groups (1% among responders vs. 3% among non-responders;
x2 = , 2.00, df = 1, p = 0.20), whereas more non-responders
screened for ASD (2% vs. 6%; x2 = 8.62, df = 1, p,0.01) and
ADHD (7% versus 17%; x2 = 22.28, df = 1, p,0.001). Further, a
larger proportion of the responders were girls (55% vs. 45%;
x2 = 5.05, df = 1, p,0.05), and monozygotic (35% vs. 27%;
x2 = 4.71, df = 1, p,0.05) than non-responders.
Measures
All study participants filled out the Hoarding Rating Scale-Self
Report (HRS-SR) [32]. The HRS-SR consists of five items
measured on a 9-point Likert type scale ranging from 0 (none) to 8
(extreme). The HRS-SR items reflect the proposed DSM-5 criteria
for HD: clutter in the rooms of one’s home, difficulty discarding
possessions, excessive acquisition and perceived distress and
impairment. To address adolescents’ limited control over their
entire homes and parental control, we rephrased the clutter item
in the questionnaire to refer solely to clutter in the young person’s
own room (rather than the entire home).
In the current study, the HRS-SR displayed acceptable internal
consistency (Cronbach’s alpha = 0.70) and a principal component
analysis revealed a single factor structure explaining 46.2% of the
Hoarding Symptoms in Adolescence
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variance, with factor loadings ranging from 0.65 (clutter in room)
to 0.71 (emotional distress).
Presence of clinically significant hoarding symptoms was defined
as scoring at least moderately (4 or more out of 8) on items
measuring clutter, difficulties discarding and distress and/or
impairment. This has previously been described as criteria for
clinically significant hoarding [33,34] and approximately corre-
sponds to the proposed core criteria for DSM-5 [3]. Although it is
currently unclear whether the DSM-5 diagnostic criteria are
suitable for adolescents [35], a recent taxometric exploration of the
latent structure of hoarding symptoms [36] supported a similar
dimensional structure of hoarding in adults and young adults
(mean age = 19). However, since the phenomenology of hoarding
in adolescence is largely unknown, we also calculated an additional
prevalence estimate. For this, we used the above-described criteria
but excluded the clutter criterion since clutter, or the lack thereof,
could be heavily influenced by familial factors, such as parents or
siblings discarding items. Additionally, since excessive acquisition
is a prominent feature of hoarding (but not a core criterion in
DSM-5) we also calculated the proportion of participants reporting
excessive acquisition among those endorsing clinically significant
hoarding symptoms.
Co-occurring neurodevelopmental disorders were assessed at
age 9/12 with the ‘Autism-Tics, AD/HD and other Comorbid-
ities inventory’ (A-TAC) [37,38] specifically developed for parental
interviewing in CATSS. Parents to twins underwent telephone
interviews answering questions regarding lifetime symptoms of
ADHD and ASD closely mapped after the corresponding DSM-
IV-TR-criteria [39]. The A-TAC is structured in different
modules, which in turn consist of several items: Language (6 items),
Social interaction (6 items), and Flexibility (5 items) for ASD and
Concentration/Attention (9 items) and Impulsiveness/Activity (10 items)
for ADHD. In each module, parents are first reminded that the
items refer to a life-time perspective and subsequently asked to
answer either by stating No (Score 0), Yes, to some extent (Score 0.5)
or Yes (Score 1). Additionally, parents are given the alternatives Do
not know or Do not wish to answer. To be defined as screening positive
for ASD in this study, a cut-off score of 4.5 was required.
Conversely, for ADHD, a cut-off score of 6 was used. These cut-
offs have been validated and provide high sensitivity/specificity
(0.91/0.80) for ASD and (0.91/0.73) ADHD as well as excellent
inter-rater agreement (ICC.0.90) [38]. Furthermore, predictive
validity, measured by receiver operating characteristics (ROC) is
excellent with areas under the curve (AUC) of 0.96 for ASD and
0.94 for ADHD. OCD symptoms were ascertained with two A-
TAC items, modeled after DSM-IV-TR-criteria for OCD,
addressing obsessions and compulsions. Examples of typical
obsessions concerning dirt, contamination or catastrophes and
compulsions consisting of washing, touching, repeating, arranging
or counting were provided. The cut-off score for OCD was
determined to 1.
Statistical Analyses
Internal consistency and factor analysis of the HRS-SR as well
as prevalence estimates and demographic differences were
estimated using SAS version 9.2 [40]. For continuous variables
we used t-tests, whereas ordinal and nominal data were analyzed
with x2-tests (Fischer’s exact test) and Wilcoxon’s test. In the
prevalence estimates, we controlled for the clustering of twins
within families. All parameter estimates in the twin analyses were
obtained from maximum-likelihood estimates in MX [41].
Twin Analyses
Twin analyses are based on the differing genetic relatedness of
MZ twins, sharing all of their genes and DZ twins, which share on
average 50% of their co-segregating genes. The assumption that
both twin types grow up under equal environments leads to the
conclusion that an accentuated resemblance within MZ compared
to DZ pairs on a given trait is due to a genetic influence on that
trait. To estimate the magnitude of this within-twin pair
resemblance, we calculated intraclass correlations for HRS-SR
total scores by zygosity. Since total scores were positively skewed
(skewness = 1.55), they were successfully logarithmically trans-
formed using the natural logarithm (skewness = 20.14). Next, we
undertook maximum-likelihood univariate model-fitting [42] and
fitted our raw data to different models to identify that with the best
fit by comparing the chi-square statistic of the 22 Log likelihood
(22LL) statistics. Twin models decompose the variance of
phenotypes to additive genetic factors (A), shared environmental
factors (C; which make twins within a pair alike), and non-shared
environmental factors (E; which make twins within a pair
dissimilar). The correlational pattern showed that the MZ twins
were more alike compared to DZ twins among males but not
among females, suggesting possible sex differences in genetic and
environmental influences on hoarding symptoms. Therefore we
fitted several sex-limitation models to our data. Initially, however,
data was fitted to the saturated model where variances and means
of the first and second born MZ and DZ twin were allowed to vary
freely
. Next, we fitted data to the General Sex Limitation Model
(GSM) [42] which allows for qualitative and quantitative sex
effects on a trait (i.e., we tested whether the same genes influenced
hoarding symptoms in both sexes and if the magnitude of this
genetic effect was equal across sexes). Additionally, the genetic
correlation between DZOS twins was allowed to vary freely and so
were the effects of A, C and E on males and females. We also
tested a similar model where the shared environmental correlation
in DZOS twins was allowed to vary freely to test if qualitative
differences in the shared environment could be influential across
sexes. In striving for parsimony by using as few parameters in a
model as possible, we subsequently tested the more restrained
Common Effects Sex Limitation Model (CESM) [42] and
compared this to the full GSM. In CESM only the magnitude
of the genetic effect is allowed to vary whereas the genes affecting
the trait are common to both sexes by restraining the DZOS
genetic correlation to 0.5. Finally, we also tested a No Sex Effects
Model (NESM) [42] in which A, C and E effects are all restrained
to be equally influential on both sexes and compared this to the
CESM.
Results
Prevalence
A total of 2% (N = 79; 95% CI 1.6%22.5%; Mean HRS-SR
score = 19.7; min = 12, max = 40; SD = 4.9) of the entire sample of
15-year olds had clinically significant hoarding symptomatology
based on the above-described criteria. The prevalence was
significantly higher in girls (2.6%; 95% CI 2.0%23.5%) than in
boys (1.2%; 95% CI 0.8%21.8%) (x2 = 15.5, df = 1, p,0.01).
After excluding the clutter criterion, the prevalence rate increased
to 3.7% (N = 145; 95% CI 3.1%24.3%; Mean HRS-SR
score = 17.0; min = 8, max = 40; SD = 5.3).
Excessive acquisition was endorsed by 38% (n = 30) of
participants with clinically significant hoarding symptoms (includ-
ing clutter) and by 28% (n = 41) of participants when the clutter
criterion was excluded from the prevalence estimates.
Hoarding Symptoms in Adolescence
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Demographic Characteristics and Comorbidity
Socio-demographic and clinical characteristics of hoarding and
non-hoarding groups are shown in Table 1. Adolescents with
hoarding symptoms were more likely to be female (72% vs. 54%).
The two groups were similar regarding urban area of living,
parental education, income and immigrant status. Among
hoarders, ADHD was the most common co-occurring disorder
at age 9/12 (10.0%) whereas OCD and ASD were each comorbid
in 2.9% of the cases. However, no significant differences emerged
between the hoarding and the non-hoarding groups in terms of
comorbidity.
Heritability
In total, 1555 twin pairs were included in the model-fitting
analyses. The intraclass correlations for HRS-SR hoarding
symptoms are provided in Table 2. In MZ boys, the correlation
(0.44; 95% CI 0.33–54) was significantly higher than the DZ
correlation (0.17; 95% CI 0.06–0.29), indicating that genes had an
influence on hoarding among males. In contrast, we found no
significant difference in MZ (0.35; 95% CI 0.25–0.44) and DZ
(0.41; 95% CI 0.31–0.51) correlations among girls, suggesting that
familial similarity regarding could be explained by shared
environment rather than genes.
Table 3 provides model-fitting results. Compared to the initial
saturated model, the GSM did not provide a significantly worse fit
(p = 0.88). Similarly, testing the more parsimonious CESM did not
result in a worsening of fit compared to the GSM (p = 0.99),
suggesting no qualitative genetic/shared environmental sex
differences (i.e., the same genes/shared environments are impor-
tant for boys and girls). However, in comparison to the CESM the
NESM, in which genetic and environmental influences are
equated across sexes, resulted in a significant deterioration of the
fit (p = 0.02). Thus, the model with the best fit was the CESM,
indicating that the same genes/shared environments accounted for
the variation in hoarding symptoms in both adolescent males and
females, but that the magnitude of this influence varied across
sexes.
Table 4 summarizes the standardized parameter estimates of
the best-fitting model (i.e. the CESM). The figures indicated that
in boys, genes accounted for 32% (95% CI 13–44%) of the
Table 1. Characteristics of 15-year old twins in Sweden fulfilling criteria for clinically significant hoarding symptoms according to
the HRS-SR and those who did not.
Hoarding (N = 79) Non-hoarding (N = 3,895) t Wilcoxon’s Z x2
p
Female sex, n (%) 57 (72.2) 2112 (54.2) 10.04 ,0.01
Monozygotic, n (%) 22 (31.9) 1188 (35.3) 0.35 0.61
Living in urban area, n (%) 52 (74.3) (missing = 9) 2337 (69.3) (missing = 522) 0.81 0.43
Father’s highest education, n (%) 0.73 0.47
Primary school 13 (16.5) 554 (14.2)
High School 30 (38.0) 1852 (47.5)
University ,3 yrs 10 (12.7) 391 (10.0)
University $3 yrs 25 (31.7) 1022 (26.2)
PhD 1 (1.3) 72 (1.9) (missing = 4)
Mother’s highest education, n (%) 0.83 0.41
Primary school 5 (6.3) 145 (6.3)
High School 39 (49.4) 1768 (45.4)
University ,3 yrs 6 (7.6) 191 (4.9)
University $3 yrs 28 (35.4) 1661 (42.6)
PhD 1 (1.3) 28 (0.7) (missing = 4)
Mean annual income father, SEK (SD) 361,7 00 (541,700) 346,100 (351,400) –0.38 0.70
Mean annual income mother, SEK (SD) 245,000 (92,100) 262,400 (150,600) 1.02 0.31
Father born abroad, n (%) 7 (11.3) (missing = 17) 225 (7.5) (missing = 898) 1.24 0.23
Mother born abroad, n (%) 7 (10.3) (missing = 11) 304 (9.2) (missing = 572) 0.10 0.67
OCDa, n (%) 2 (2.9) (missing = 9) 49 (1.5) (missing = 517) 0.93 0.28
ADHDa, n (%) 7 (10.0) (missing = 9) 244 (7.2) (missing = 520) 0.78 0.38
ASDa, n (%) 2 (2.9) (missing = 9) 74 (2.2) 0.14 0.67
Note: SEK = Swedish Crowns, OCD = Obsessive Compulsive Disorder, ADHD = Attention Deficit Hyperactivity Disorder. ASD = Autism Spectrum Disorders. a) Determined
from parental reports at age 9/12 years.
doi:10.1371/journal.pone.0069140.t001
Table 2. Intraclass correlations for hoarding symptoms
according to the HRS-SR in Swedish twins at age 15 years.
N (pairs) ICC 95% CI
MZ males 231 0.44 0.33–0.54
DZ males 279 0.17 0.06–0.29
MZ females 336 0.35 0.25–0.44
DZ females 265 0.41 0.31–0.51
DZOS 444 0.16 0.07–0.25
Note: MZ = Monozygotic twins; DZ = Dizygotic same sex twins;
DZOS = Dizygotic opposite-sex twins.
doi:10.1371/journal.pone.0069140.t002
Hoarding Symptoms in Adolescence
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Page 4
phenotypic variance in hoarding symptoms whereas shared
environmental factors (4%; 95% CI 0–17%) only had a negligible
effect. Non-shared environmental effects and measurement error
(64%; 95% CI 55–75%) accounted for the largest proportion of
the variance. By contrast, genes only accounted for a non-
significant 2% (95% CI 0–24%) of the variance in girls, whereas
the shared environment (32%; 95% CI 14–41%) and the non-
shared environment plus measurement error (65%; 95% CI 58–
73%) accounted for most of the phenotypic variance.
Discussion
As proposed by retrospective studies of adults [8,9] and studies
of children with OCD exhibiting hoarding symptoms [13–15] our
study suggests that hoarding symptoms are relatively prevalent
(approximately 2%) among adolescents although somewhat less
prevalent than in similar adult studies [11,43]. Mean scores on
HRS-SR among young hoarders (mean = 19.7; sd = 4.9,
range = 12–40) in the current study were also similar to scores
reported in adults (mean = 21.1; sd = 3.9) [11]. However, a notable
difference between hoarding symptoms in adolescence and
adulthood is that they seem to affect females to a larger extent
in the younger age group, a finding that also has been reported
earlier [15]. An additional difference emerged when examining
the frequency of excessive acquisition amongst individuals classed
as having clinically significant hoarding difficulties. Approximately
30–40% of these individuals also reported at least moderate
problems with acquisition, indicating that excessive acquisition
may be less prominent in adolescents than it is in adults (about
85%; [44]). This lends further support to the inclusion of excessive
acquisition as a diagnostic specifier rather than a core criterion in
DSM25. It is possible that excessive acquisition difficulties
develop later in life when individuals with hoarding tendencies
become financially independent and also have more control over
their acquisitive behavior and space.
The obtained prevalence estimate of hoarding symptoms also
indicates that these are at least as common as OCD during
adolescence [45,46], a finding that contradicts the notion that
hoarding is merely is a subtype of OCD.
Given the lack of published data on the hoarding phenotype in
adolescence and the potential of familial effects on clutter we also
estimated a prevalence rate of 3.7% when excluding the
requirement to have significant clutter in the participant’s room.
It is still unknown whether the phenomenology of hoarding
changes across the lifespan and whether the proposed diagnostic
criteria for HD can be applied to adolescents without adaptation.
Further exploration of the phenomenology of hoarding during
adolescence involving face-to-face interviews and home visits will
be needed in order to determine which features of hoarding are
most prominent and problematic during this age period and
whether the diagnostic criteria require adapting for their use in
adolescents. Nevertheless, our estimates provide an important first
step towards estimating the possible prevalence of hoarding
difficulties in this age group.
Our findings also showed that OCD, to which HD has been
linked traditionally, co-occurred in only 2.9% of adolescents who
fulfilled hoarding criteria and at a similar rate among those who
did not. This finding from a non-clinical sample suggests that the
link between the two disorders might be especially tenuous during
adolescence. Previous findings of high comorbidity between HD
and ADHD in clinically ascertained samples of adults [12,47] and
youth [18] were not confirmed. We also found comparable rates of
ASD in the hoarding and non-hoarding groups. Similarly,
research in adults suggests that symptoms of autism are not more
prevalent in subjects with HD compared to psychiatric controls
[17]. Taken together, our findings suggest that in the majority of
cases at the population level, hoarding symptoms are frequently
present in the absence of other neurodevelopmental disorders,
lending further support to the notion that HD might be a distinct
nosological entity.
Finally, the twin analyses indicated that hoarding symptoms
were moderately heritable in adolescence, although the magnitude
of the genetic influence was much stronger in boys than in girls.
This somewhat unexpected finding hoarding symptoms are
clearly heritable in adult men and women [10,23] was related to
Table 3. Model-fitting results for hoarding symptoms in Swedish twins at age 15 years.
Model
2
2LL x2 D df
p
AIC Compared to model
1. Saturated Model 8182.713 2012.71
2. General Sex Limitation Model* 8192.436 9.72 16 0.88 1990.44 1
3. General Sex Limitation Model** 8192.436 9.72 16 0.88 1990.44 1
4. Common Effects Sex Limitation Model 8192.436 0 1 0.99 1988.44 2, 3
5. No Effects Sex Limitation Model 8201.754 9.318 3 0.02 1991.754 4
Note:
The General Sex Limitation Mod el tested for qualitative and quantitative sex differences.
*Testing for the presence of qualitative genetic effects across sexes.
**Testing for the presence of qualitative shared environmental effects across sexes.
The Common Effects Sex Limitation Model tested for quantitative sex differences and the No Effects Sex Limitation Model tested for no differences across sexes.
The best fitting model is bolded.
22LL = minus twice the log likelihood; x2 = differences in 22LL statistic between submodel and full model; D df = change in degrees of freedom between submodel
and full model; p=probability; AIC = Akaike Information Criterion.
doi:10.1371/journal.pone.0069140.t003
Table 4. Explained variance by additive genetic and
environmental factors to hoarding symptoms in Swedish
twins at age 15 years according to best fitting model.
A (95% CI) C (95% CI) E (95% CI)
Males 0.32 (.13–44) 0.04 (.00–17) 0.64 (.55–75)
Females 0.02 (.00–24) 0.32 (.14–41) 0.65 (.58–73)
Note: A = additive genetic effects; C = shared environmental effects; E = non-
shared environmental effects.
doi:10.1371/journal.pone.0069140.t004
Hoarding Symptoms in Adolescence
PLOS ONE | www.plosone.org 5 July 2013 | Volume 8 | Issue 7 | e69140
Page 5
considerable shared environmental influences on hoarding symp-
toms amongst girls. However, similar findings of sex differences
during adolescence have been reported previously regarding
genetic and environmental influences for OCD, [48,49] weight
[50], and pubertal development [51]. Furthermore, dynamic
developmental genetic effects from childhood to young adulthood,
expressed in genetic attenuation and innovation (i.e. the decline in
impact of certain genes and the activation of genes which
previously had no effect) in symptoms of anxiety and depression
are well documented [26]. It seems plausible that hoarding may
become progressively more heritable over time as the influence of
shared familial environment decreases when young people leave
their parents’ home and have stronger control over their own
living space. Longitudinal studies of the heritability of hoarding
symptoms in young adulthood and beyond are needed to elucidate
developmental trajectories of hoarding in both sexes.
The results should be interpreted considering several limita-
tions. First, we based our classification of clinically significant
hoarding symptoms on a measure not specifically validated in an
adolescent population. Thus, the possibility that it did not capture
hoarding symptoms equally well as in adults cannot be ruled out.
Hopefully, the modification of the clutter item increased its
relevance for this age group. Second, prevalence estimates should
be seen as indicative rather than definitive because we could not
conclusively rule out other medical or psychiatric conditions that
are known to lead to hoarding behavior [52,53]. Third, although
ADHD, ASD and OCD are relatively stable prevalence-wise in
the age span from 9/12 to 15 years, more precise estimates of their
co-occurrence with hoarding symptoms would have been obtained
had they been assessed at age 15 years and not at age 9/12; hence,
we cannot totally exclude an under- or possibly overestimation of
ADHD, ASD and OCD comorbidity. Fourth, albeit modeled
closely after DSM-IV-TR-criteria [39], comorbid OCD was not
determined using a validated measure, and was based solely on
parental report. Thus, the OCD comorbidity rate might have been
underestimated by parents and should therefore be interpreted
cautiously. Fifth, and finally, since ASD and ADHD were
significantly more common among non-responders, we cannot
rule out that the true comorbidity of hoarding symptoms and
neurodevelopmental disorders might be higher.
Conclusion
This study is the first to investigate the occurrence of hoarding
symptoms in a large population based sample of adolescents.
Hoarding symptoms were prevalent among adolescents and
usually appeared without co-occurring ADHD, ASD and OCD.
Furthermore, the same etiological factors seemed to influence
hoarding symptoms in both sexes although the genetic effect was
much stronger in boys. Longitudinal studies are required to
elucidate the developmental trajectories of hoarding symptoms
and their heritability from adolescence onto adulthood.
Acknowledgments
The authors would like to thank Camilla Palm at the Department of
Medical Epidemiology and Biostatistics, Karolinska Institutet for assistance
in data management and preparation.
Author Contributions
Conceived and designed the experiments: DMC PL HA ZC CHG SL NL
CR ES. Analyzed the data: VZI DMC PL ZC CR. Wrote the paper: VZI
DMC ES PL HA ZC CHG SL NL CR.
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  • Source
    • "To clarify the relationships between autism and hoarding further, future research should be conducted to investigate the relevant results in a clinical sample and a comparison group. Second, this study does not off er any explanation for the weak association between hoarding and autism symptoms ( Anholt, et al ., 2010 ; Ivanov, et al ., 2013 ). Further studies with more comprehensive models and meta-analysis are needed to explore the essential and detailed link between autism and hoarding; possibly other repetitive behaviors should be included. "
    [Show abstract] [Hide abstract] ABSTRACT: Researchers and clinical practitioners have found that hoarding appears in many autism patients and that most of these patients show high anxiety and depression. There is no consensus on the relationship between autistic traits and hoarding, and little research concerning the role of negative emotions. This study investigated the relationship between autistic traits and hoarding in a large non-clinical Chinese sample. Participants were 3,229 university students (M age = 20.5 yr., SD = 1.6; 1,839 men) who were recruited in classroom. They completed measures of hoarding, autistic symptomology, anxiety, and depression: specifically the Saving Inventory-Revised, the Autism-Spectrum Quotient, the Zung Self-Rating Anxiety Scale, and The Center for Epidemiological Studies Depression Scale. Mediating effects of anxiety and depression in the correlation between autistic traits and hoarding were also explored. There was a weak but significant correlation between autistic traits and hoarding. Significant mediating effects of anxiety and depression were observed. Hoarding in people with high autistic traits could be influenced by anxiety and depression.
    Full-text · Article · Feb 2015 · Psychological Reports
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    • "brain lesions in the anterior ventromedial prefrontal and cingulate cortices following injury) (Anderson et al. 2005 ). A distinction should be made between symptoms related to hoarding disorder, neurodevelopmental disorders (Ivanov et al. 2013 ), or neurodegenerative disorders like Alzheimer's disease. A diagnosis of hoarding disorder should not be made if the accumulation of items is due to delusions or symptoms related to schizophrenia spectrum or psychotic disorders (APA 2013 ). "
    [Show abstract] [Hide abstract] ABSTRACT: The obsessive-compulsive and related disorders (OCRDs) category in DSM-5 is comprised not only of OCD but also of body dysmorphic disorder (BDD), hoarding disorder, trichotillomania (hair-pulling disorder) (TTM), and skin picking (excoriation) disorder (SPD). A review of the literature on the phenomenology, psychobiology, pharmacotherapy, and psychotherapy of these OCRDs was undertaken with a specific focus on gender. OCRDs (e.g. BDD) may have a roughly equal gender ratio, may be more common in females (e.g. HPD) or may be more common in males (e.g. hoarding disorder). Comorbidity in OCRDs may also differ across gender; e.g. in SPD, females present with increased depressive symptomatology compared to males. The literature on treatment differences by gender in the OCRDs is, however, sparse. Thus, a range of questions arise for future research and for clinical practice.
    Preview · Article · Jan 2015
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    • "Frank et al. (2014) studied 68 children treated at a pediatric anxiety clinic (age range 4–10 years); compared to the non-hoarding patients, the hoarding group had an earlier age at the onset of their primary diagnosis, a greater prevalence of attention deficit/hyperactivity disorder (ADHD), and a greater prevalence of anxiety disorders (generalized anxiety, social anxiety, or separation anxiety disorders). The etiology of hoarding is complex, with evidence of involvement of genetic factors (Ivanov et al., 2013; Samuels et al., 2007b), adverse life experiences (Cromer, Schmidt, & Murphy, 2007; Landau, Iervolino, Pertusa, & Santo, 2011; Przeworski, Cain, & Dunbeck, 2014), and deficits in executive functions (Grisham, Norberg, Williams, Certoma, and Kadib, 2010; Mathews, Perez, Delucchi, & Mathalon, 2012; McGrath et al., 2014; Morein-Zamir et al., 2014). Moreover, there is an evidence for an association between hoarding behavior and autism. "
    [Show abstract] [Hide abstract] ABSTRACT: Compared to studies in adults, there have been few studies of hoarding in children and adolescents with obsessive–compulsive disorder (OCD). In the current study, we evaluated OCD clinical features, Axis I disorders, and social reciprocity scores in 641 children and adolescents with OCD, of whom 163 (25%) had hoarding compulsions and 478 did not. We found that, as a group, youth with hoarding had an earlier age at onset and more severe lifetime OCD symptoms, poorer insight, more difficulty making decisions and completing tasks, and more overall impairment. The hoarding group also had a greater lifetime prevalence of panic disorder, specific phobia, Tourette disorder, and tics. As measured with the Social Reciprocity Scale, the hoarding group had more severe deficits in parent-rated domains of social communication, social motivation, and restricted interests and repetitive behavior. In a multivariable model, the overall social reciprocity score, age at onset of OCD symptoms, symmetry obsessions, and indecision were independently related to hoarding in these children and adolescents with OCD. These features should be considered as candidate risk factors for the development of hoarding behavior in pediatric OCD.
    Full-text · Article · Oct 2014 · Journal of Obsessive-Compulsive and Related Disorders
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