Available via license: CC BY 4.0
Content may be subject to copyright.
March 2018 | Volume 9 | Article 1011
REVIEW
published: 27 March 2018
doi: 10.3389/fpsyt.2018.00101
Frontiers in Psychiatry | www.frontiersin.org
Edited by:
Marin Veldic,
Mayo Clinic, United States
Reviewed by:
Didem Oztop,
Erciyes University, Turkey
Katerina Maniadaki,
Technological Educational Institute of
Athens, Greece
Pratibha N. Reebye,
British Columbia Children’s Hospital,
Canada
*Correspondence:
Robert L. Hendren
robert.hendren@ucsf.edu
Specialty section:
This article was submitted to Child
and Adolescent Psychiatry,
a section of the journal
Frontiers in Psychiatry
Received: 18October2017
Accepted: 13March2018
Published: 27March2018
Citation:
HendrenRL, HaftSL, BlackJM,
WhiteNC and HoeftF (2018)
Recognizing Psychiatric Comorbidity
With Reading Disorders.
Front. Psychiatry 9:101.
doi: 10.3389/fpsyt.2018.00101
Recognizing Psychiatric
Comorbidity With Reading Disorders
Robert L. Hendren1,2*, Stephanie L. Haft1, Jessica M. Black3, Nancy Cushen White2,4 and
Fumiko Hoeft1,2,5,6,7
1 Division of Child and Adolescent Psychiatry, Department of Psychiatry, Weill Institute for Neurosciences, University of
California San Francisco, San Francisco, CA, United States, 2 Dyslexia Center, University of California San Francisco,
SanFrancisco, CA, United States, 3 School of Social Work, Boston College, Chestnut Hill, MA, United States,
4 Departmentof Pediatrics, University of California San Francisco, San Francisco, CA, United States, 5 University of California
Multi-Campus Precision Learning Center (PrecL), San Francisco, CA, United States, 6 Haskins Laboratories, New Haven, CT,
United States, 7 Department of Neuropsychiatry, Keio University School of Medicine, Tokyo, Japan
Reading disorder (RD), a specic learning disorder (SLD) of reading that includes impair-
ment in word reading, reading uency, and/or reading comprehension, is common in the
general population but often is not comprehensively understood or assessed in mental
health settings. In education settings, comorbid mental and associated disorders may
be inadequately integrated into intervention plans. Assessment and intervention for RD
may be delayed or absent in children with frequently co-occurring mental disorders not
fully responding to treatment in both school and mental health settings. To address
this oversight, this review summarizes current knowledge regarding RDs and common
comorbid or co-occurring disorders that are important for mental health and school set-
tings. We chose to highlight RD because it is the most common SLD, and connections
to other often comorbid disorders have been more thoroughly described in the literature.
Much of the literature we describe is on decoding-based RD (or developmental dyslexia)
as it is the most common form of RD. In addition to risk for academic struggle and
social, emotional, and behavioral problems, those with RD often show early evidence
of combined or intertwined Diagnostic and Statistical Manual of Mental Disorders, Fifth
Edition childhood disorders. These include attention decit hyperactivity disorder, anxiety
and depression, disruptive, impulse-control, and conduct disorders, autism spectrum
disorders, and other SLDs. The present review highlights issues and areas of controversy
within these comorbidities, as well as directions for future research. An interdisciplinary,
integrated approach between mental health professionals and educators can lead to
comprehensive and targeted treatments encompassing both academic and mental
health interventions. Such targeted treatments may contribute to improved educational
and health-related outcomes in vulnerable youth. While there is a growing research
literature on this association, more studies are needed of when to intervene and of the
early and long-term benets of comprehensive intervention.
Keywords: specic learning disorder, developmental dyslexia, comorbidity, mental health, neurodevelopmental
INTRODUCTION
Despite a strong reciprocal association between reading disorder (RD) and mental disorders in
young people (1), their co-occurrence is oen under-recognized and under-treated resulting in less
than optimal outcomes in all areas including emotional outcomes. Diculties with comorbidities
may continue into adulthood (2). Recognition of RD by health-care professionals is important—the
FIGURE 1 | Current issues, areas of investigation, and suggestions for future research in conditions commonly occurring with RD in children. RD, reading disorder;
ADHD, attention decit hyperactivity disorder; ASD, autism spectrum disorder; SLD, specic learning disorder; CD, conduct disorder; ODD, oppositional deant
disorder.
2
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
prevalence of dyslexia (decoding-based RD; the term RD is used
from hereon) is approximately 5–10% of all children depending
on the study across languages, cultures, and writing systems (3).
In an eort to bridge the recognition gap between RD and
associated mental disorders, we review RD along with other co-
occurring Diagnostic and Statistical Manual of Mental Disorders,
Fih Edition (DSM-5) mental disorders. We also review literature
that describes best practice interventions for children with RD and
comorbid disorders and identify areas where stronger research
is important (Figure1). Our overarching goal is to increase the
awareness of health professionals to disorders of reading that
overlap or are confused with mental conditions and disorders.
DSM-5 denes RD, within neurodevelopmental disorders, as
a type of specic learning disorder (SLD) with impairment in
reading that is characterized by problems with word reading
accuracy, reading uency, and reading comprehension that are
not the result of sensory impairments, neurological disorders,
intellectual disabilities, or inadequate educational instruction
(4). e impairments in word reading accuracy or reading u-
ency are also noted as developmental dyslexia in the literature.
RD is oen associated with diculties in phonological aware-
ness (awareness of sounds of a language, i.e., phonemes, to
process spoken and written language), lexical uency (i.e., rapid
naming of common items), letter (sound) knowledge, graph-
eme–phoneme association, which are predictive of later decod-
ing and word reading. Oral language, vocabulary, and executive
function on the other hand are generally more predictive of
reading comprehension. Diculties in reading comprehension
may be a result of reduced reading experience that can impede
growth of vocabulary and background knowledge in those with
decoding-based RD (5). However, it is possible for children with
specic reading comprehension decits to have intact decoding
skills (6).
METHODS
We used two electronic databases (PubMed and PsycInfo) in
order to review prevalence and characteristics of RD’s comorbid-
ity with other psychiatric disorders. Searching for relevant articles
from the past 20years (1997–2017), we used the keywords such
as “dyslexia,” “reading disability,” “reading disorder,” “learning
disability,” “learning disorder” along with “comorbid,” and/or
terms pertaining to other specic DSM-5 disorders [e.g., “autism
and Autism Spectrum Disorder (ASD),” “Attention Decit
3
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
Hyperactivity Disorder (ADHD),” “anxiety,” “depression,” “con-
duct disorder,” etc.]. We primarily selected articles with a focus
on child populations (individuals under the age of 18years) and
a specied diagnosis of RD.
Overview of RD
Etiology
Reading disorder results from a constellation of genetic and
environmental risk factors and their interactions and not a
single underlying cause. e estimated heritability rate of RD is
approximately 50–70% (7, 8). Several susceptibility genes have
been identied (8), though each explains only a small fraction
of variance, suggesting the involvement of other mechanisms
including polygenicity, epistasis, and epigenetics, in RD (9).
Neuroanatomical anomalies in both gray and white matters
shown to be causally related to RD (10) are observed in areas
and networks associated with phonological, orthographic, and
articulatory processing (11–13). Additionally, work in neural
oscillations as well as neurochemistry shows decits related to
sensory processing, particularly auditory discrimination, in
individuals with or at-risk for RD (14, 15). Within the context
of comorbidity, the pathophysiology oen overlaps between RD
and co-occurring mental disorders. For example, RD shares com-
mon risk genes with ADHD (16, 17). In ASD, links to language
impairment (LI) such as specic language impairment (SLI) have
been made (18), which in turn may be associated with RD risk
genes (19). Neuroimaging studies of RD comorbidity with mental
disorders are currently limited but hold promise for elucidating
shared versus dierential etiologies. For instance, one neuroim-
aging study found distinct neural biomarkers for children with
dyslexia, ADHD, and age-matched controls in auditory neuro-
anatomy, physiology, and behavior (20).
Early Characteristics
In those at-risk for developing decoding-based RD, decits in
pre-literacy skills (e.g., phonological awareness, letter identica-
tion and letter-sound knowledge, and rapid naming) are observed
(21). A growing body of research also implicates non-linguistic,
domain-general abilities in early literacy acquisition and RD, such
as visual attention (22) and executive functions (23). Decoding-
based RD is oen noticed initially in kindergarten or rst grade
when children are rst exposed to formal reading instruction and
may be diagnosed between 2nd and 4th grade, depending on the
educational system, parents, caregivers, and teachers. RD of read-
ing comprehension tends to be identied later as the demands
of reading increases from learning to read to reading to learn,
unless children are initially diagnosed in earlier years with SLI.
ough proles of specic comorbidities will be discussed in later
sections, the general pattern is that RD in combination with a
comorbid condition results in greater impairment.
Assessment and Diagnosis
In order to obtain a formal diagnosis of RD, a child must undergo
a battery of tests that are administered by a qualied professional
(diagnostician qualications vary by state). Careful considera-
tion of the potential for co-occurring disorders or impairments
and other interacting factors is critical for ensuring accurate
diagnoses to inform recommendations for intervention or treat-
ment—and for predicting prognosis. For example, it would be
important to determine whether a child presents with ADHD and
has a secondary diculty in reading or presents with RD that
results in inattention.
Prior to assessment, it is important to obtain the child’s fam-
ily, developmental, and educational history. Sensory issues (e.g.,
impairment in vision or hearing), home and school literacy
environment, native language (e.g., English learners who lack
English prociency) that may aect reading should be ruled out
as causes of diculty; at the same time, it must be kept in mind
that the presence of these issues do not necessarily preclude exist-
ence of RD. Parental self-report scales of reading and attention
diculties may be useful for identication of adults at-risk for
these diculties, since at-risk parents may confer risks on their
children for related problems (24).
COMORBID MENTAL DISORDERS
Neurodevelopmental Disorders
Attention Decit Hyperactivity Disorder
Attention decit hyperactivity disorder and RD are recognized
as frequently comorbid disorders (Ta bl e 1 ). ADHD involves an
unremitting pattern of inattention and/or hyperactivity–impul-
sivity that results in functional impairment (4). RD oen involves
attention diculties, sometimes representing overlooked and
undertreated ADHD (25), which can contribute to academic
underachievement (26). Subgroups of children with RD show
attention-related impairments (e.g., decits in alertness, covert
shi of attention, divided attention, exibility, and visual search)
(27). In experimental work, researchers have shown attention-
related decits in RD in both the auditory (attention shiing)
(28) and visual domains (which some argue is an independent
contributor to phonological decits) (29).
Approximately 20–40% of children with the inattentive sub-
type of ADHD have RD (50, 51) and 20–40% of those with RD
have ADHD (33). e relationship between ADHD symptoms
and reading is found to be predominantly in the inattentive type
(30, 31). Neuropsychological proles of RD and ADHD comor-
bid groups include decits in processing speed, verbal working
memory, phonological short-term memory, naming speed, and
central executive processes (32, 33). A strong explanation for this
comorbidity proposes that multiple predictors of each disorder
have shared or overlapping genetic (16, 17), as well as neural and
cognitive risk factors. A proposed subgroup of ADHD, “sluggish
cognitive tempo,” characterized by diculty sustaining attention,
daydreaming, lethargy, and physical underactivity, is thought by
some to represent a possible link to RD (52) using electrophysi-
ological (53) and pharmacological (54) evidence. Imaging stud-
ies, however, have generally found distinct patterns of structural
and functional abnormalities among RD and ADHD, most oen
examined separately (55).
e research on comorbidity between RD and ADHD is
extensive—for reviews, see Ref. (17, 33, 56). However, the com-
bined developmental progression of RD + ADHD is not well
studied. Further research is needed of the overlap or intertwined
TABLE 1 | An overview of comorbid conditions that commonly occur with reading disorder (RD) as well as their shared symptoms and risk mechanisms.
Comorbid condition Features of comorbid group Shared risk with RD
Attention decit hyperactivity disorder (ADHD) Inattention (30, 31) in auditory (28) and visual (29)
Decits in processing speed, verbal working
memory, phonological short-term memory, naming
speed, and central executive processes (32, 33)
Shared risk genes (KIAA0319 and DCDC2) (17)
Shared structural and functional neural abnormalities (33)
Environmental factors (smoke and miscarriage) (16)
Autism spectrum disorder Impaired reading comprehension (34) Shared risk genes (MRPL19) (19)
Comorbidity with language impairment (35)
Disruptive, impulse-control, and conduct
disorders
Externalizing behavior (36, 37) Shared cognitive risk in working memory decit (38)
Comorbidity with ADHD (39–41)
Decits in verbal processing/language skills (38, 42)
Anxiety and depressive disorders Poor self-esteem (43)
Internalizing psychopathology (44)
Negative academic/social experiences (45)
Shared familial risk factors (46)
Other specic learning disorders Internalizing psychopathology (47)
Handwriting decits (48)
Shared cognitive risk in working memory, semantic memory, and
verbal processing decits (49)
Decits in rhythmic organization (48)
4
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
nature of the two disorders and the inuence of this potential
co-contribution during the development of reading.
Autism Spectrum Disorder
ere are limited studies of ASD+RD children, and the preva-
lence of RD reported in ASD children ranges considerably from
6 (57) to 30% (58). One consideration in discussing co-occurring
ASD and RD is dierentiating between “true” comorbidity and
symptom overlap—a recurring issue in child psychopathology. In
both ASD and RD, there are documented impairments in read-
ing comprehension, language, and visual/auditory processing.
However, simply counting these overlaps in cognitive symptoms
in ASD and RD may lead to false recognition of comorbidity. On
the other hand, failure to recognize a comorbid RD could result
in inadequate treatment with negative academic consequences.
Reading disorder and ASD might not be considered “true” co-
occurring disorders because the reading diculty in ASD is not
a decoding or phonics problem. Numerous studies report reading
comprehension decits in children with ASD that are discrepantly
low with their intelligence [see Ref. (59) for meta-analysis], which
typically do not fall under decoding-based RD. In fact, though
reading comprehension impairment in ASD children is well-
documented (34), ASD children oen show intact and sometimes
even precocious abilities in word reading, non-word decoding,
and text reading accuracy (60). ese ndings suggest that the
reading decits observed in ASD are dierent than that of a child
with decoding-based RD, which are characterized by phonologi-
cal decits that may lead to impaired reading comprehension.
One way to further explore if ADHD+RD represent a “true”
comorbidity is to examine the possibility of shared etiological fac-
tors. One explanation for shared reading problems is co-occurring
LI. LI is prevalent in both ASD (61) and RD (62), and studies
suggest that the presence of reading comprehension decits in
children with ASD is mediated by language ability (35, 61). ese
behavioral results are supported by a study showing that genes
contributing to general language skills are shared among dyslexia,
ASD, and LI (19). However, LI is certainly not the sole contributor
to reading problems in ASD—some literature shows a correlation
between social abilities and reading comprehension in ASD
(60). In other words, the behavioral manifestation of reading
impairment in ASD and RD originates at least partly from dif-
ferent mechanisms; however, longitudinal and family studies are
needed to further explore how the disorders may be related. As
discussed in the treatment section, the underlying explanation for
the RD and ASD comorbidity has important implications for how
comorbid RD is treated in children with ASD, and further study is
needed to determine the most eective dierential interventions.
Other SLDs
Historically, the subtypes of SLDs have been viewed from an
academic-subject approach—for example, the DSM-4 had
distinct categories for RD, mathematics disorder (MD or dyscal-
culia), disorder of written expression (dysgraphia), and learning
disorder not otherwise specied. e DSM-5 moved away from
these categories in including RD, MD, and dysgraphia together
under the label of “Specic Learning Disorder” with speciers
for the area of impairment. ese areas of impairment can be
further broken down into component subskills in the areas of
reading (e.g., word reading accuracy, reading uency, and reading
comprehension), mathematics (e.g., number sense, calculation,
and math reasoning), and writing (e.g., spelling, grammar, and
written expression). In a move from a categorical to a dimensional
approach, research has sought to identify comorbidities among
the SLDs through the lens of shared versus unique cognitive
processes that might underlie them.
Reading disorder and MD have a comorbidity of approxi-
mately 40% (63), and this co-occurrence is associated with greater
impairment on measures of internalizing psychopathology and
academic functioning (47). Although RD and MD are generally
accepted to have unique neurocognitive proles, researchers
have pointed to shared cognitive processes in working memory,
semantic memory, and verbal processes that may explain the high
comorbidity (49). One recent paper applied a cluster analysis to
children with SLD to identify associations between cognitive clus-
ters and SLD subtypes. Results showed that impaired subskills of
each domain were associated with dierent clusters—for example,
5
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
math and text reading speed were most strongly associated with a
cluster involving cognitive processing, while text comprehension
was more linked to the verbal abilities cluster (64). is approach
is promising in recognizing the heterogeneity within RD and
MD themselves, as well as adopting a dimensional approach to
highlight shared cognitive decits.
Reading disorder has also been shown to co-occur with
dysgraphia. Comorbidity rates between RD and dysgraphia are
dicult to determine, yet the correlation of word reading and
writing performance is shown to be around 70% (65). Although
RD and dysgraphia are shown to have dierences in brain bases
for written language tasks (66), they exhibit shared behavioral
decits in rhythm, which is required for both reading and writing
(48). Most researchers have explained the overlap of dysgraphia
and dyslexia by highlighting learning to read and learning to spell
as “two sides of the same coin” (65). Phonological awareness,
visual attention, working memory, and auditory processing play
predictive roles in both reading and writing (67).
Further research is warranted on examining comorbidities
between RD and other SLDs from a process perspective. In par-
ticular, studies should examine trajectories of impairment in these
cognitive processes from before the onset of formal schooling to
adult years when “compensation” for decits may have occurred.
Disruptive, Impulse-Control, and Conduct
Disorders (CDs)
Children with RD can exhibit comorbidities in the disruptive,
impulse-control, and CD categories of the DSM-5 including CD
and oppositional deant disorder (ODD) (4). Most of the exist-
ing literature focuses on associations between RD and behavioral
problems or disorders in general, though specic links between
RD and diagnosed CD (68) have been established. It is not clear,
however, how much of the higher incidences of externalizing
behavior among children with RD precedes RD or is the emotional
result of it (36, 37). Although more recent studies have found that
reading diculties oen precede behavioral problems, results do
not necessarily support a direct causal pattern between the two
conditions. Instead, conduct and behavioral issues in RD children
are exhibited across both academic and non-academic settings
and appear more independent of reading problems (69, 70).
ese ndings are important in implying that interventions for
RD may not treat co-occurring behavioral problems—however,
such treatment studies have yet to be conducted and represent an
area of needed research.
One promising explanation for the co-occurrence of RD
and behavioral disorders is each conditions’ comorbidity with
ADHD—ADHD commonly occurs with RD, CD, and ODD
(71), and ADHD and RD are associated with higher delinquency
severity scores than for either one alone (72). Further support for
this explanation comes from studies showing that hyperactivity
mediates between reading problems and disruptive behaviors
in adolescent populations (39, 73). However, one study of adult
forensic patients with RD found a higher level of cognitive impul-
sivity than those without RD, regardless of ADHD diagnosis (74).
An additional explanation for the comorbidity of these condi-
tions with RD involves shared neurocognitive risk factors—for
example, children diagnosed with disruptive and CDs are shown
to have abnormal language processing (42) and working memory
decits (38), characteristics also shared by children with RD. Taken
together, these results suggest that the comorbidity of disruptive,
impulse-control, and CDs and RD are at least partially due to each
disorders’ co-occurrence with ADHD. Further study is needed
to determine how the co-occurrence of RD and CD/ODD may
dier with or without the presence of comorbid ADHD. is will
inform the most eective timing and nature of interventions to
improve outcomes for RD and intertwined behavioral disorders.
Anxiety Disorders
Children with RD report greater generalized anxiety than their
non-RD peers (44), and a meta-analysis has conrmed that LD
children and adolescents, including those with RD, have signi-
cantly higher scores on anxiety measures than non-LD students
(75). is higher rate of anxiety in RD children persists even
aer controlling for ADHD symptoms (76). In explaining this
comorbidity, researchers have proposed a model whereby anxiety
distracts from learning and interferes with cognitive processes
necessary for reading, leading to potential RD (77). However,
researchers have also proposed that reading problems associated
with RD can lead to anxiety as a result of the experience of school
failure (78). More neurodevelopmental longitudinal studies are
needed to investigate these processes, although current evidence
suggests that both models have merit, with a bi-directional rela-
tionship between anxiety and reading (79).
In order to investigate a potential genetic etiology for the
RD-anxiety comorbidity, researchers have studied siblings and
twin pairs. One study of monozygotic and dizygotic adult twins
found a strong link between anxiety and RD but with no shared
genetic cause (45). A separate study demonstrated that siblings of
children and adolescents with RD were more than twice as likely
to meet criteria for generalized anxiety disorder (GAD), suggest-
ing shared familial risk factors between the two disorders (46).
e study also showed marginally signicant dierences between
monozygotic and dizygotic twin pairs in RD cross-concordance
with GAD, indicating a small role for genetic risk in the comor-
bidity between RD and anxiety. Although more work is needed
on neural correlates of comorbidity, these genetic studies support
the model of a combination of genetic and environmental risk
factors in explaining co-occurrence of RD and anxiety.
One area of future research involves distinguishing between
comorbidity of RD and general anxiety versus anxiety specic
to reading (reading anxiety). Reading anxiety as a concept has
not been investigated in the literature, but over three decades of
research on math anxiety indicate that its neural and behavioral
characteristics are related but distinct from general anxiety [see
Ref. (80, 81) for reviews on math anxiety]. ere is no doubt that
RD is commonly comorbid with general anxiety, but investigating
the potential presence of reading anxiety could enable more tar-
geted interventions to address co-occurring emotional problems
children with RD. Unfortunately, there are currently no measures
to assess reading anxiety, representing an area of need in the eld.
Depressive Disorders
In addition to or potentially as a result of anxiety, children and
adolescents with RD exhibit higher rates of depression (44, 82),
6
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
with evidence for a correlation between more severe RD and
greater depressive symptoms in younger children (83). Similar
to the research on RD and anxiety association, the existence of
depression in RD does not appear to be dependent on comorbid-
ity with ADHD (84). Researchers have identied low self-esteem
as a symptom of depression in RD as well as a target for interven-
tion (85, 86)—in one study of adolescents with RD, self-esteem
predicted 23% of the variation in depression risk (87). Depression
and RD exhibit patterns of familial risk and marginally signicant
genetic contributions similar to that of RD and anxiety (46), sug-
gesting multiple risk factors. e higher incidence of bullying and
peer victimization faced by children and adolescents with RD
may be an environmental factor that partially explains comorbid-
ity with depression (88) but further study of neurodevelopmental
risk factors will likely provide targets for early interventions.
For example, a growing area of research suggests that emo-
tion processing may be impaired in children with RD (89).
is impairment has important implications for assessing for
comorbid depression and anxiety in RD (44), since decits in
understanding emotions, depressive and anxious symptoms may
go underreported. us, self-report measures may not be su-
cient to assess for comorbid depression and anxiety in RD youth.
Other Disorders and Conditions
Reading disorder can sometimes co-occur with other DSM-5
categories, though these appear to be less investigated than the
aforementioned conditions. Although RD is not listed as a com-
mon comorbid condition in the category of sleep-wake disorders
and vice versa, a recent exploratory study found a signicantly
greater frequency of sleep disorders in RD children compared to
controls (90). Given that a prior neurophysiological study showed
an association between sleep activity and reading abilities in RD
children (91), evaluation of sleep may be an important factor to
consider in RD treatment and management.
Reading disorder may also co-occur with disorders more
commonly appearing in adulthood. For instance, one study of
substance-related and addictive disorders showed that out of a sam-
ple of adults with addiction issues, 40% had RD (92). However, a
separate study reported signicantly lower substance use history
in RD versus non-RD university students (93). Future research
is therefore needed to draw conclusion about the comorbidity
of RD and substance abuse. Similarly, due to the rarity of early
onset schizophrenia, RD and schizophrenia have not been shown
to co-occur in children, but one study found that 70% of adult
patients with schizophrenia met criteria for RD (94). However,
this nding may be confounded in part by reduced educational
and occupational outcomes (94), as well as IQ changes that may
occur with progression of schizophrenia (95). Finally, a form of
RD can occur in patients with the neurocognitive disorder of
dementia (96) and may share susceptibility genes (97), though
this is only observed in adult populations.
TREATMENT
A challenge in treating comorbid conditions is whether to target
both conditions simultaneously or to treat one condition to see
if benet in the other condition results. However, there is a gap
in the literature of evidence-based strategies for treating RD with
comorbid conditions, likely because investigations of treatments
oen intentionally exclude individuals with comorbidities. is
is further complicated by the fragmented approach to treatment
a child with RD may receive. For example, an educator may focus
on treating one symptom (e.g., decoding) while a psychiatrist
may target another (e.g., anxiety). e majority of studies of
interventions for comorbid RD are with ADHD with few to no
studies of other comorbid conditions such as ASD, CD, anxiety,
or depression.
Reading Interventions
Phonics-based reading instruction is the most common and
most eective intervention for students with RD (98) and for
poor readers (99). Phonics instruction that is systematic and
explicit has the greatest evidence (100). Instruction designed
to explicitly teach adult students to assign selective attention to
grapheme–phoneme associations—as opposed to attempts to
memorize whole unfamiliar words—impacts brain circuitry that
can subsequently be recruited during reading (101). Reading
interventions are eective for students with and without RD
when administered by teachers or researchers (102). Although
music education has also been investigated as a way to improve
reading in children with RD, evidence does not currently support
its eectiveness (103).
Reading interventions in comorbid ADHD+RD are shown
to be eective regardless of adjunctive ADHD medications (104).
In a recent paper, ADHD treatment alone resulted in greater
reduction in ADHD symptoms than reading treatment alone,
and reading treatment led to greater improvements in reading
outcome (word reading and decoding) than ADHD treatment
only. e administration of both treatments simultaneously did
not result in a greater level of improvement of each outcome
(ADHD symptoms and reading skills). In other words, there was
no additive value to combining treatments. However, the com-
bined treatment enabled remediation of both ADHD and reading
symptoms in the comorbid group simultaneously, so would still
be recommended over treating each disorder in isolation (105). It
should be noted that this study involved predominantly African
American males and should be replicated with a diverse range of
demographics.
To be most eective, children with RD and comorbid condi-
tions may need reading interventions to be more specic or
combined with other interventions. For example, children with
RD+MD who received both reading intervention and number
combination intervention outperformed RD+MD students who
received reading intervention alone (106). Reading intervention
may also need to specically target the unique reading proles of
subjects with comorbidities. Children with ASD and comorbid
reading problems show a prole of intact decoding abilities, yet
low reading comprehension, and accordingly, reading interven-
tion specically targeting vocabulary skills is shown to be most
eective in this population (107, 108).
Socioemotional Health
Because children with RD may be exposed to signicant
stressors, and RD can co-occur with anxiety and depression,
7
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
treatments should address socioemotional health in addition
to reading. Protective factors that foster resilience for children
and adolescents with RD include self-advocacy tools, strength
identication, and social connections (109). However, research
on evidence-based treatments for depression and anxiety that
commonly occur with RD is inadequate and is a critically impor-
tant area for future work. Cognitive behavioral therapy (CBT),
a treatment that focuses on altering negative behavioral and
thought patterns, may reduce symptoms of comorbid anxiety
and depression in RD children. CBT is the standard for treat-
ing unidimensional cases of anxiety and depressive disorders
(110, 111) and is shown to be eective in treating psychiatric
comorbidities in other conditions that co-occur with RD, such
as ADHD (112) and ASD (113). More research is needed to
delineate unique modications that might be necessary for the
greatest eectiveness when the emotional condition is combined
with RD.
Mindfulness meditation shows increasing promise for benet
to socioemotional health in people with these combined dis-
orders. Mindfulness meditation is shown to reduce anxiety in
RD adolescents (114). It is also shown to improve attention and
lexical processing/word reading (but not non-word decoding)
in combined RD and ADHD in adults, more so than in those
with RD only (115). A mindfulness intervention incorporating
elements of CBT was shown to improve ODD and CD symp-
toms in RD+ ADHD adolescents, as well as reduce anxiety in
RD+anxiety adolescents. Academic performance is thought to
be improved through the reduction in anxiety as a result from
mindfulness meditation among youth with RD and comorbid
conditions (114).
Biomedical and Nutritional
Pharmacotherapy is increasingly investigated for combined RD
and comorbid conditions, although the most common treatment
for RD alone is reading interventions. e great majority of these
studies examined RD with comorbid ADHD. Results from these
studies are summarized in recent reviews (56, 116). In summary,
these studies have investigated the use of atomoxetine (ATX),
methylphenidate (MPH), and nutritional supplements such as
polyunsaturated fatty acids (117) on outcomes of reading, ADHD
symptoms, and executive functions in ADHD + RD groups.
Reviews reporting on treatment studies found that outcome
eect sizes range from small to medium [as low as 0.13 for ATX
and as high as 0.60 for MPH (56)], although eects on ADHD
symptoms are larger and more consistent than for executive
function or reading (56, 116). Future work in this area should
investigate the impact of these and other medications on RD with
other commonly co-occurring conditions, as well as examine the
neurophysiological mechanisms of these treatments in comorbid
groups.
Experimental Interventions
Initial research suggests that neurofeedback training to increase
attention processes (118, 119) may be eective in reducing
ADHD and RD symptoms, although investigations of these
brain-based interventions are too preliminary to be fully
endorsed as treatments for RD. Altering cortical excitability using
neuromodulation techniques, transcranial magnetic stimulation,
and transcranial direct current stimulation is shown to change
reading and reading-related abilities in typical and RD adults
and children, though parameters such as stimulation frequency
and location are not consistent in their benets (120, 121). ese
studies have not investigated neuromodulation with RD and
comorbid conditions and are still in experimental and proof-of-
concept stages.
CLINICAL IMPLICATIONS AND
SIGNIFICANCE
Knowledge and awareness of RD are highly relevant to health-
care professionals working with children, as mental disorders
may be comorbid or blended, and RD can be overlooked or
undertreated. Evidence for the co-occurring disorder may be
recognized before the RD is identied (e.g., ADHD and ASD),
may follow the RD (e.g., depression), or may be intertwined
with RD (e.g., anxiety and behavioral disorders). In all of these
co-morbidities, the mechanisms of the disorders may overlap,
and more research is needed to identify the mechanism of
the overlap, the sequencing of their developmental and neu-
rodevelopmental inuence, the most benecial targeting and
nature of interventions, and the economic burden of RD with
and without treated and untreated comorbid mental disorders.
Although one disorder may be identied as the primary target
for intervention, comprehensive interventions should address
both the RD and the comorbidity to produce optimal treatment
results.
AUTHOR CONTRIBUTIONS
RH designed the article and wrote the Sections “Introduction”
and “Treatment.” RH and SH cowrote the Comorbid Mental
Disorders sections—SH also constructed the table. JB wrote
the Section “Socioemotional Health.” NW wrote the Section
“Reading Interventions.” FH wrote the Section “Overview of RD”
and added to all sections. All the authors read and approved the
paper.
FUNDING
RH was supported by research grants from Curemark,
BioMarin, Roche, Shire, Sunovion, Autism Speaks, and
Vitamin D Council and is on the Advisory Board for Curemark,
BioMarin,Neuren, and Janssen. FH was supported by grants
from the Eunice Kennedy Shriver National Institute of Child
Health and Human Development (NICHD) R01HD078351,
R01HD086168, R01HD065794, P01HD001994, National
Science Foundation (NSF) NSF1540854,Oak Foundation Grant
ORIO-16-012, University of California Oce of the President
Multi-campus Research Program (MRP-17-454925), and the
Potter Family. JB was supported by an Ignite Award, Boston
College.
8
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
REFERENCES
1. Willcutt EG, Pennington BF. Psychiatric comorbidity in children and adoles-
cents with reading disability. J Child Psychol Psychiatry (2000) 41(8):1039–48.
doi:10.1111/1469-7610.00691
2. Ascherman LI, Shael J. Facilitating transition from high school and
special education to adult life: focus on youth with learning disorders,
attention- decit/hyperactivity disorder, and speech/language impairments.
Child Adolesc Psychiatr Clin N Am (2017) 26(2):311–27. doi:10.1016/j.
chc.2016.12.009
3. Siegel LS. Perspectives on dyslexia. Paediatr Child Health (2006) 11(9):581–7.
doi:10.1093/pch/11.9.581
4. American Psychiatric Association. Diagnostic and Statistical Manual
of Mental Disorders, Fih Edition (DSM-5). Arlington, VA: American
Psychiatric Publishing (2013).
5. Lyon GR, Shaywitz SE, Shaywitz BA. A denition of dyslexia. Ann Dyslexia
(2003) 53(1):1–14. doi:10.1007/s11881-003-0001-9
6. Cutting LE, Clements-Stephens A, Pugh KR, Burns S, Cao A, Pekar JJ, etal.
Not all reading disabilities are dyslexia: distinct neurobiology of specic
comprehension decits. Brain Connect (2013) 3(2):199–211. doi:10.1089/
brain.2012.0116
7. Hawke JL, Wadsworth SJ, DeFries JC. Genetic inuences on reading dicul-
ties in boys and girls: the Colorado twin study. Dyslexia (2006) 12(1):21–9.
doi:10.1002/dys.301
8. Peterson RL, Pennington BF. Developmental dyslexia. Annu Rev Clin Psychol
(2015) 11:283–307. doi:10.1146/annurev-clinpsy-032814-112842
9. Girirajan S. Missing heritability and where to nd it. Genome Biol (2017)
18(1):89. doi:10.1186/s13059-017-1227-x
10. Xia Z, Hancock R, Hoe F. Neurobiological bases of reading disorder part
I: etiological investigations. Lang Linguist Compass (2017) 11(4):e12239.
doi:10.1111/lnc3.12239
11. Richlan F, Kronbichler M, Wimmer H. Meta-analyzing brain dysfunc-
tions in dyslexic children and adults. Neuroimage (2011) 56(3):1735–42.
doi:10.1016/j.neuroimage.2011.02.040
12. Richlan F, Kronbichler M, Wimmer H. Structural abnormalities in the
dyslexic brain: a meta-analysis of voxel-based morphometry studies. Hum
Brain Mapp (2013) 34(11):3055–65. doi:10.1002/hbm.22127
13. Vandermosten M, Boets B, Wouters J, Ghesquiere P. A qualitative and
quantitative review of diusion tensor imaging studies in reading and
dyslexia. Neurosci Biobehav Rev (2012) 36(6):1532–52. doi:10.1016/j.
neubiorev.2012.04.002
14. De Vos A, Vanvooren S, Vanderauwera J, Ghesquière P, Wouters J. Atypical
neural synchronization to speech envelope modulations in dyslexia. Brain
Lang (2017) 164:106–17. doi:10.1016/j.bandl.2016.10.002
15. Hancock R, Pugh KR, Hoe F. Neural noise hypothesis of developmental
dyslexia. Trends Cogn Sci (2017) 21(6):434–48. doi:10.1016/j.tics.2017.08.003
16. Mascheretti S, Trezzi V, Giorda R, Boivin M, Plourde V, Vitaro F, et al.
Complex eects of dyslexia risk factors account for ADHD traits: evidence
from two independent samples. J Child Psychol Psychiatry (2017) 58(1):75–82.
doi:10.1111/jcpp.12612
17. Willcutt EG, Betjemann RS, McGrath LM, Chhabildas NA, Olson RK, DeFries
JC, et al. Etiology and neuropsychology of comorbidity between RD and
ADHD: the case for multiple-decit models. Cortex (2010) 46(10):1345–61.
doi:10.1016/j.cortex.2010.06.009
18. Bartlett CW, Hou L, Flax JF, Hare A, Cheong SY, Fermano Z, etal. A genome
scan for loci shared by autism spectrum disorder and language impairment.
Am J Psychiatry (2014) 171(1):72–81. doi:10.1176/appi.ajp.2013.12081103
19. Eicher JD, Gruen JR. Language impairment and dyslexia genes inuence
language skills in children with autism spectrum disorders. Autism Res
(2015) 8(2):229–34. doi:10.1002/aur.1436
20. Serrallach B, Groß C, Bernhofs V, Engelmann D, Benner J, Gündert N, etal.
Neural biomarkers for dyslexia, ADHD, and ADD in the auditory cortex of
children. Front Neurosci (2016) 10:324. doi:10.3389/fnins.2016.00324
21. Ozernov-Palchik O, Gaab N. Tackling the ‘dyslexia paradox’: reading brain
and behavior for early markers of developmental dyslexia. Wiley Interdiscip
Rev Cogn Sci (2016) 7(2):156–76. doi:10.1002/wcs.1383
22. Franceschini S, Gori S, Runo M, Pedrolli K, Facoetti A. A causal link
between visual spatial attention and reading acquisition. Curr Biol (2012)
22(9):814–9. doi:10.1016/j.cub.2012.03.013
23. Segers E, Damhuis CM, van de Sande E, Verhoeven L. Role of executive
functioning and home environment in early reading development. Learn
Individ Dier (2016) 49:251–9. doi:10.1016/j.lindif.2016.07.004
24. Pennington BF, Ley DL. Early reading development in children at family risk
for dyslexia. Child Dev (2001) 72(3):816–33. doi:10.1111/1467-8624.00317
25. Hong DS. Learning disorders and ADHD: are LDs getting the attention
they deserve? J Am Acad Child Adolesc Psychiatry (2014) 53(9):933–4.
doi:10.1016/j.jaac.2014.06.006
26. Voigt RG, Katusic SK, Colligan RC, Killian JM, Weaver AL, Barbaresi WJ.
Academic achievement in adults with a history of childhood attention-
decit/hyperactivity disorder: a population-based prospective study. J Dev
Behav Pediatr (2017) 38(1):1–11. doi:10.1097/DBP.0000000000000358
27. L ewandowska M, Milner R, Ganc M, Włodarczyk E, Skarżyński H. Attention
dysfunction subtypes of developmental dyslexia. Med Sci Monit (2014)
20:2256. doi:10.12659/MSM.890969
28. Jednorog K, Gawron N, Marchewka A, Heim S, Grabowska A. Cognitive sub-
types of dyslexia are characterized by distinct patterns of grey matter volume.
Brain Struct Funct (2014) 219(5):1697–707. doi:10.1007/s00429-013-0595-6
29. Zoubrinetzky R, Bielle F, Valdois S. New insights on developmental dys-
lexia subtypes: heterogeneity of mixed reading proles. PLoS One (2014)
9(6):e99337. doi:10.1371/journal.pone.0099337
30. Plourde V, Boivin M, Brendgen M, Vitaro F, Dionne G. Phenotypic and
genetic associations between reading and attention-decit/hyperactivity
disorder dimensions in adolescence. Dev Psychopathol (2017) 29(4):1215–26.
doi:10.1017/S0954579416001255
31. Schuchardt K, Fischbach A, Balke-Melcher C, Maehler C. e comorbidity
of learning diculties and ADHD symptoms in primary-school-age
children. Z Kinder Jugendpsychiatr Psychother (2015) 43(3):185–93.
doi:10.1024/1422-4917/a000352
32. Moura O, Pereira M, Alfaiate C, Fernandes E, Fernandes B, Nogueira S,
etal. Neurocognitive functioning in children with developmental dyslexia
and attention-decit/hyperactivity disorder: multiple decits and diagnostic
accuracy. J Clin Exp Neuropsychol (2017) 39(3):296–312. doi:10.1080/13803
395.2016.1225007
33. Germano E, Gagliano A, Curatolo P. Comorbidity of ADHD and dyslexia.
Dev Neuropsychol (2010) 35(5):475–93. doi:10.1080/87565641.2010.494748
34. Nation K, Clarke P, Wright B, Williams C. Patterns of reading ability in
children with autism spectrum disorder. J Autism Dev Disord (2006)
36(7):911–9. doi:10.1007/s10803-006-0130-1
35. McIntyre NS, Solari EJ, Gonzales JE, Solomon M, Lerro LE, Novotny S, etal.
e scope and nature of reading comprehension impairments in school-aged
children with higher-functioning autism spectrum disorder. J Autism Dev
Disord (2017) 47(9):2838–60. doi:10.1007/s10803-017-3209-y
36. Dahle AE, Knivsberg AM, Andreassen AB. Coexisting problem
behaviour in severe dyslexia. J Res Spec Educ Needs (2011) 11(3):162–70.
doi:10.1111/j.1471-3802.2010.01190.x
37. Heiervang E, Lund A, Stevenson J, Hugdahl K. Behaviour problems
in children with dyslexia. Nord J Psychiatry (2001) 55(4):251–6.
doi:10.1080/080394801681019101
38. Carpenter JL, Drabick DA. Co-occurrence of linguistic and behavioural dif-
culties in early childhood: a developmental psychopathology perspective.
Early Child Dev Care (2011) 181(8):1021–45. doi:10.1080/03004430.2010.5
09795
39. Simono E, Elander J, Holmshaw J, Pickles A, Murray R, Rutter M. Predictors
of antisocial personality. Br J Psychiatry (2004) 184(2):118–27. doi:10.1192/
bjp.184.2.118
40. Smart D, Sanson A, Prior M. Connections between reading disability and
behavior problems: testing temporal and causal hypotheses. J Abnorm Child
Psychol (1996) 24(3):363–83. doi:10.1007/BF01441636
41. Svensson I, Lundberg I, Jacobson C. e prevalence of reading and spelling
diculties among inmates of institutions for compulsory care of juvenile
delinquents. Dyslexia (2001) 7(2):62–76. doi:10.1002/dys.178
42. Pine DS, Bruder GE, Wasserman GA, Miller LS, Musabegovic A,
Watson JB. Verbal dichotic listening in boys at risk for behavior dis-
orders. J Am Acad Child Adolesc Psychiatry (1997) 36(10):1465–73.
doi:10.1097/00004583-199710000-00030
43. Nelson JM, Gregg N. Depression and anxiety among transitioning adolescents
and college students with ADHD, dyslexia, or comorbid ADHD/dyslexia.
J Atten Disord (2012) 16(3):244–54. doi:10.1177/1087054710385783
9
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
44. Mammarella IC, Ghisi M, Bomba M, Bottesi G, Caviola S, Broggi F, etal.
Anxiety and depression in children with nonverbal learning disabilities, read-
ing disabilities, or typical development. J Learn Disabil (2016) 49(2):130–9.
doi:10.1177/0022219414529336
45. Whitehouse AJO, Spector TD, Cherkas LF. No clear genetic inuences on the
association between dyslexia and anxiety in a population-based sample of
female twins. Dyslexia (2009) 15(4):282–90. doi:10.1002/dys.378
46. Willcutt EG. Behavioral genetic approaches to understand the etiology
of comorbidity. In: Rhee SH, Ronald A, editors. Behavior Genetics of
Psychopathology. New York, NY: Springer (2014). p. 231–52.
47. Willcutt EG, Petrill SA, Wu S, Boada R, Defries JC, Olson RK, et al.
Comorbidity between reading disability and math disability: concurrent psy-
chopathology, functional impairment, and neuropsychological functioning.
J Learn Disabil (2013) 46(6):500–16. doi:10.1177/0022219413477476
48. Pagliarini E, Guasti MT, Toneatto C, Granocchio E, Riva F, Sarti D,
et al. Dyslexic children fail to comply with the rhythmic constraints of
handwriting. Hum Mov Sci (2015) 42:161–82. doi:10.1016/j.humov.2015.
04.012
49. Ashkenazi S, Black JM, Abrams DA, Hoe F, Menon V. Neurobiological
underpinnings of math and reading learning disabilities. J Learn Disabil
(2013) 46(6):549–69. doi:10.1177/0022219413483174
50. S ciberras E, Mueller KL, Efron D, Bisset M, Anderson V, Schilpzand EJ, etal.
Language problems in children with ADHD: a community-based study.
Pediatrics (2014) 133(5):793–800. doi:10.1542/peds.2013-3355
51. Wadsworth SJ, DeFries JC, Willcutt EG, Pennington BF, Olson RK. e
Colorado longitudinal twin study of reading diculties and ADHD: etiologies
of comorbidity and stability. Twin Res Human Genet (2015) 18(06):755–61.
doi:10.1017/thg.2015.66
52. Willcutt EG, Pennington BF, Olson RK, Chhabildas N, Hulslander J.
Neuropsychological analyses of comorbidity between reading disability and
attention decit hyperactivity disorder: in search of the common decit. Dev
Neuropsychol (2005) 27(1):35–78. doi:10.1207/s15326942dn2701_3
53. Lallier M, Tainturier M-J, Dering B, Donnadieu S, Valdois S, ierry G.
Behavioral and ERP evidence for amodal sluggish attentional shiing
in developmental dyslexia. Neuropsychologia (2010) 48(14):4125–35.
doi:10.1016/j.neuropsychologia.2010.09.027
54. Wietecha L, Williams D, Shaywitz S, Shaywitz B, Hooper SR, Wigal SB,
et al. Atomoxetine improved attention in children and adolescents with
attention-decit/hyperactivity disorder and dyslexia in a 16 week, acute,
randomized, double-blind trial. J Child Adolesc Psychopharmacol (2013)
23(9):605–13. doi:10.1089/cap.2013.0054
55. E den GF, Vaidya CJ. ADHD and developmental dyslexia: two pathways lead-
ing to impaired learning. Ann N Y Acad Sci (2008) 1145:316–27. doi:10.1196/
annals.1416.022
56. Sexton CC, Gelhorn HL, Bell JA, Classi PM. e co-occurrence of
reading disorder and ADHD: epidemiology, treatment, psychosocial
impact, and economic burden. J Learn Disabil (2012) 45(6):538–64.
doi:10.1177/0022219411407772
57. Mayes SD, Calhoun SL. Frequency of reading, math, and writing disabilities
in children with clinical disorders. Learn Individ Dier (2006) 16(2):145–57.
doi:10.1016/j.lindif.2005.07.004
58. Åsberg J, Kopp S, Berg-Kelly K, Gillberg C. Reading comprehension,
word decoding and spelling in girls with autism spectrum disorders
(ASD) or attention-decit/hyperactivity disorder (AD/HD): perfor-
mance and predictors. Int J Lang Commun Disord (2010) 45(1):61–71.
doi:10.3109/13682820902745438
59. Brown HM, Oram-Cardy J, Johnson A. A meta-analysis of the reading
comprehension skills of individuals on the autism spectrum. J Autism Dev
Disord (2013) 43(4):932–55. doi:10.1007/s10803-012-1638-1
60. Fernandes FDM, de La Higuera Amato CA, Cardoso C, Navas AL, Molini-
Avejonas DR. Reading in autism spectrum disorders: a literature review. Folia
Phoniatr Logop (2015) 67(4):169–77. doi:10.1159/000442086
61. Bishop DV. Overlaps between autism and language impairment: phenom-
imicry or shared etiology? Behav Genet (2010) 40(5):618–29. doi:10.1007/
s10519-010-9381-x
62. Nash HM, Hulme C, Gooch D, Snowling MJ. Preschool language proles
of children at family risk of dyslexia: continuities with specic language
impairment. J Child Psychol Psychiatry (2013) 54(9):958–68. doi:10.1111/
jcpp.12091
63. Wilson AJ, Andrewes SG, Struthers H, Rowe VM, Bogdanovic R, Waldie KE.
Dyscalculia and dyslexia in adults: cognitive bases of comorbidity. Learn
Individ Dier (2015) 37:118–32. doi:10.1016/j.lindif.2014.11.017
64. Poletti M, Carretta E, Bonvicini L, Giorgi-Rossi P. Cognitive clusters
in specic learning disorder. J Learn Disabil (2018) 51(1):32–42.
doi:10.1177/0022219416678407
65. Ehri LC. Learning to read and learning to spell: two sides of a coin. Top Lang
Disord (2000) 20(3):19–36. doi:10.1097/00011363-200020030-00005
66. Richards T, Grabowski T, Boord P, Yagle K, Askren M, Mestre Z, et al.
Contrasting brain patterns of writing-related DTI parameters, fMRI connec-
tivity, and DTI–fMRI connectivity correlations in children with and without
dysgraphia or dyslexia. Neuroimage Clin (2015) 8:408–21. doi:10.1016/j.
nicl.2015.03.018
67. D öhla D, Heim S. Developmental dyslexia and dysgraphia: what can we learn
from the one about the other? Front Psychol (2016) 6:2045. doi:10.3389/
fpsyg.2015.02045
68. Burke JD, Loeber R, Birmaher B. Oppositional deant disorder and conduct
disorder: a review of the past 10 years, part II. J Am Acad Child Adolesc
Psychiatry (2002) 41(11):1275–93. doi:10.1097/00004583-200211000-00009
69. Kempe C, Gustafson S, Samuelsson S. A longitudinal study of early reading
diculties and subsequent problem behaviors. Scand J Psychol (2011)
52(3):242–50. doi:10.1111/j.1467-9450.2011.00870.x
70. Russell G, Ryder D, Norwich B, Ford T. Behavioural diculties that co-occur
with specic word reading diculties: a UK population-based cohort study.
Dyslexia (2015) 21(2):123–41. doi:10.1002/dys.1496
71. Levy F, Young DJ, Bennett KS, Martin NC, Hay DA. Comorbid ADHD and
mental health disorders: are these children more likely to develop reading
disorders? Atten Dec Hyperact Disord (2013) 5(1):21–8. doi:10.1007/
s12402-012-0093-3
72. Poon K, Ho CS-H. Contrasting decits on executive functions in Chinese
delinquent adolescents with attention decit and hyperactivity disorder
symptoms and/or reading disability. Res Dev Disabil (2014) 35(11):3046–56.
doi:10.1016/j.ridd.2014.07.046
73. Fergusson DM, Horwood LJ. Early disruptive behavior, IQ, and later school
achievement and delinquent behavior. J Abnorm Child Psychol (1995)
23(2):183–99. doi:10.1007/BF01447088
74. Dåderman AM, Meurling AW, Levander S. ‘Speedy action over goal orienta-
tion’: cognitive impulsivity in male forensic patients with dyslexia. Dyslexia
(2012) 18(4):226–35. doi:10.1002/dys.1444
75. Nelson JM, Harwood H. Learning disabilities and anxiety: a meta-analysis.
J Learn Disabil (2011) 44(1):3–17. doi:10.1177/0022219409359939
76. Goldston DB, Walsh A, Arnold EM, Reboussin B, Daniel SS, Erkanli A,
etal. Reading problems, psychiatric disorders, and functional impairment
from mid-to late adolescence. J Am Acad Child Adolesc Psychiatry (2007)
46(1):25–32. doi:10.1097/01.chi.0000242241.77302.f4
77. Bryan T, Burstein K, Ergul C. e social-emotional side of learning disabil-
ities: a science-based presentation of the state of the art. Learn Disabil Q
(2004) 27(1):45–51. doi:10.2307/1593631
78. Carroll JM, Iles JE. An assessment of anxiety levels in dyslexic students in
higher education. Br J Educ Psychol (2006) 76(3):651–62. doi:10.1348/0007
09905X66233
79. Grills-Taquechel AE, Fletcher JM, Vaughn SR, Stuebing KK. Anxiety and
reading diculties in early elementary school: evidence for unidirectional-or
bi-directional relations? Child Psychiatry Hum Dev (2012) 43(1):35–47.
doi:10.1007/s10578-011-0246-1
80. Artemenko C, Daroczy G, Nuerk H-C. Neural correlates of math anxiety—
an overview and implications. Front Psychol (2015) 6:1333. doi:10.3389/
fpsyg.2015.01333
81. Suárez-Pellicioni M, Núñez-Peña MI, Colomé À. Math anxiety: a review of its
cognitive consequences, psychophysiological correlates, and brain bases. Cogn
Aect Behav Neurosci (2016) 16(1):3–22. doi:10.3758/s13415-015-0370-7
82. Mugnaini D, Lassi S, La Malfa G, Albertini G. Internalizing correlates of dys-
lexia. World J Pediatr (2009) 5(4):255–64. doi:10.1007/s12519-009-0049-7
83. Maughan B, Rowe R, Loeber R, Stouthamer-Loeber M. Reading problems
and depressed mood. J Abnorm Child Psychol (2003) 31(2):219–29. doi:10.
1023/A:1022534527021
84. Carroll JM, Maughan B, Goodman R, Meltzer H. Literacy diculties and
psychiatric disorders: evidence for comorbidity. J Child Psychol Psychiatry
(2005) 46(5):524–32. doi:10.1111/j.1469-7610.2004.00366.x
10
Hendren et al. Psychiatric Comorbidity With RDs
Frontiers in Psychiatry | www.frontiersin.org March 2018 | Volume 9 | Article 101
85. Alexander-Passe N. How dyslexic teenagers cope: an investigation of self-
esteem, coping and depression. Dyslexia (2006) 12(4):256–75. doi:10.1002/
dys.318
86. Singer E. e strategies adopted by Dutch children with dyslexia to maintain
their self-esteem when teased at school. J Learn Disabil (2005) 38(5):411–23.
doi:10.1177/00222194050380050401
87. Yajai Sitthimongkol R, Apinuntavech S. Predicting factors for risk of
depression in adolescents with learning disorders. J Med Assoc ai (2012)
95(11):1480–4.
88. Baumeister AL, Storch EA, Geen GR. Peer victimization in children
with learning disabilities. Child Adolesc Soc Work J (2008) 25(1):11–23.
doi:10.1007/s10560-007-0109-6
89. G oulème N, Gerard CL, Bucci MP. Postural control in children with dyslexia:
eects of emotional stimuli in a dual-task environment. Dyslexia (2017)
23(3):283–95. doi:10.1002/dys.1559
90. Carotenuto M, Esposito M, Cortese S, Laino D, Verrotti A. Children with
developmental dyslexia showed greater sleep disturbances than controls,
including problems initiating and maintaining sleep. Acta Paediatr (2016)
105(9):1079–82. doi:10.1111/apa.13472
91. Bruni O, Ferri R, Novelli L, Terribili M, Troianiello M, Finotti E, etal. Sleep
spindle activity is correlated with reading abilities in developmental dyslexia.
Sleep (2009) 32(10):1333–40. doi:10.1093/sleep/32.10.1333
92. Yates R. Bad mouthing, bad habits and bad, bad, boys: an exploration of the
relationship between dyslexia and drug dependence. Ment Health Subst Use
(2013) 6(3):184–202. doi:10.1080/17523281.2012.699460
93. Wilcockson TD, Pothos EM, Fawcett AJ. Dyslexia and substance use in a
university undergraduate population. Subst Use Misuse (2016) 51(1):15–22.
doi:10.3109/10826084.2015.1073322
94. Revheim N, Corcoran CM, Dias E, Hellmann E, Martinez A, Butler PD,
et al. Reading decits in schizophrenia and individuals at high clinical
risk: relationship to sensory function, course of illness, and psychosocial
outcome. Am J Psychiatry (2014) 171(9):949–59. doi:10.1176/appi.ajp.2014.
13091196
95. Kubota M, van Haren NE, Haijma SV, Schnack HG, Cahn W, Pol HEH,
etal. Association of IQ changes and progressive brain changes in patients
with schizophrenia. JAMA Psychiatry (2015) 72(8):803–12. doi:10.1001/
jamapsychiatry.2015.0712
96. Wilson SM, Brambati SM, Henry RG, Handwerker DA, Agosta F, Miller BL,
etal. e neural basis of surface dyslexia in semantic dementia. Brain (2008)
132(1):71–86. doi:10.1093/brain/awn300
97. Paternicó D, Premi E, Alberici A, Archetti S, Bonomi E, Gualeni V, et al.
Dyslexiasusceptibility genes influence brain atrophy in frontotemporal
dementia. Neurol Genet (2015) 1(3):e24. doi:10.1212/NXG.0000000
000000024
98. Galuschka K, Ise E, Krick K, Schulte-Korne G. Eectiveness of treatment
approaches for children and adolescents with reading disabilities: a
meta-analysis of randomized controlled trials. PLoS One (2014) 9(2):e89900.
doi:10.1371/journal.pone.0089900
99. McArthur G, Eve P, Jones K, Banales E, Kohnen S, Anandakumar T, et al.
Phonics training for English-speaking poor readers. Cochrane Database Syst
Rev (2012) 12:CD009115. doi:10.1002/14651858.CD009115.pub2
100. Brady SA, Braze D, Fowler CA. Explaining Individual Dierences in Reading:
eory and Evidence. New York, NY: Psychology Press (2011).
101. Yoncheva YN, Wise J, McCandliss B. Hemispheric specialization for visual
words is shaped by attention to sublexical units during initial learning. Brain
Lang (2015) 145:23–33. doi:10.1016/j.bandl.2015.04.001
102. Scammacca NK, Roberts G, Vaughn S, Stuebing KK. A meta-analysis of
interventions for struggling readers in grades 4–12: 1980–2011. J Learn
Disabil (2015) 48(4):369–90. doi:10.1177/0022219413504995
103. C ogo-Moreira H, Andriolo RB, Yazigi L, Ploubidis GB, Brandão de Ávila CR,
Mari JJ. Music education for improving reading skills in children and
adolescents with dyslexia. Cochrane Database Syst Rev (2012) 8:CD009133.
doi:10.1002/14651858.CD009133.pub2
104. Tannock R, Frijters JC, Martinussen R, White EJ, Ickowicz A, Benson NJ,
etal. Combined modality intervention for ADHD with comorbid reading
disorders: a proof of concept study. J Learn Disabil (2018) 51(1):55–72.
doi:10.1177/0022219416678409
105. Tamm L, Denton CA, Epstein JN, Schatschneider C, Taylor H, Arnold LE,
et al. Comparing treatments for children with ADHD and word reading
diculties: a randomized clinical trial. J Consult Clin Psychol (2017) 85(5):
434. doi:10.1037/ccp0000170
106. Fuchs LS, Fuchs D, Compton DL. Intervention eects for students with comor-
bid forms of learning disability understanding the needs of nonresponders.
J Learn Disabil (2013) 46(6):534–48. doi:10.1177/0022219412468889
107. Davidson MM, Ellis Weismer S. Reading comprehension of ambiguous
sentences by school-age children with autism spectrum disorder. Autism Res
(2017) 10(12):2002–22. doi:10.1002/aur.1850
108. El Z ein F, Solis M, Vaughn S, McCulley L. Reading comprehension interven-
tions for students with autism spectrum disorders: a synthesis of research.
J Autism Dev Disord (2014) 44(6):1303–22. doi:10.1007/s10803-013-1989-2
109. Ha SL, Myers CA, Hoe F. Socio-emotional and cognitive resilience in
children with reading disabilities. Curr Opin Behav Sci (2016) 10:133–41.
doi:10.1016/j.cobeha.2016.06.005
110. Hofmann SG, Asnaani A, Vonk IJ, Sawyer AT, Fang A. e ecacy of cog-
nitive behavioral therapy: a review of meta-analyses. Cognit er Res (2012)
36(5):427–40. doi:10.1007/s10608-012-9476-1
111. Spirito A, Esposito-Smythers C, Wol J, Uhl K. Cognitive-behavioral therapy
for adolescent depression and suicidality. Child Adolesc Psychiatr Clin N Am
(2011) 20(2):191–204. doi:10.1016/j.chc.2011.01.012
112. Antshel KM, Olszewski AK. Cognitive behavioral therapy for adolescents
with ADHD. Child Adolesc Psychiatr Clin N Am (2014) 23(4):825–42.
doi:10.1016/j.chc.2014.05.001
113. Sukhodolsky DG, Bloch MH, Panza KE, Reichow B. Cognitive-behavioral
therapy for anxiety in children with high-functioning autism: a meta-analy-
sis. Pediatrics (2013) 132(5):e1341–50. doi:10.1542/peds.2013-1193
114. B eauchemin J, Hutchins TL, Patterson F. Mindfulness meditation may lessen
anxiety, promote social skills, and improve academic performance among
adolescents with learning disabilities. Complement Health Pract Rev (2008)
13(1):34–45. doi:10.1177/1533210107311624
115. Tarrasch R, Berman Z, Friedmann N. Mindful reading: mindfulness medita-
tion helps keep readers with dyslexia and ADHD on the lexical track. Front
Psychol (2016) 7:578. doi:10.3389/fpsyg.2016.00578
116. Gray C, Climie EA. Children with attention decit/hyperactivity disorder
and reading disability: a review of the ecacy of medication treatments.
Front Psychol (2016) 7:988. doi:10.3389/fpsyg.2016.00988
117. Tan ML, Ho JJ, Teh KH. Polyunsaturated fatty acids (PUFAs) for children with
specic learning disorders. Cochrane Database Syst Rev (2016) 9:CD009398.
doi:10.1002/14651858.CD009398.pub3
118. Breteler MH, Arns M, Peters S, Giepmans I, Verhoeven L. Improvements in
spelling aer QEEG-based neurofeedback in dyslexia: a randomized con-
trolled treatment study. Appl Psychophysiol Biofeedback (2010) 35(1):5–11.
doi:10.1007/s10484-009-9105-2
119. Van Doren J, Heinrich H, Bezold M, Reuter N, Kratz O, Horndasch S,
et al. eta/beta neurofeedback in children with ADHD: feasibility of a
short-term setting and plasticity eects. Int J Psychophysiol (2017) 112:80–8.
doi:10.1016/j.ijpsycho.2016.11.004
120. C ostanzo F, Menghini D, Caltagirone C, Oliveri M, Vicari S. How to improve
reading skills in dyslexics: the eect of high frequency rTMS. Neuropsychologia
(2013) 51(14):2953–9. doi:10.1016/j.neuropsychologia.2013.10.018
121. Costanzo F, Varuzza C, Rossi S, Sdoia S, Varvara P, Oliveri M, etal. Reading
changes in children and adolescents with dyslexia aer transcranial direct
current stimulation. Neuroreport (2016) 27(5):295–300. doi:10.1097/WNR.
0000000000000536
Conict of Interest Statement: Research was conducted in the absence of any
commercial or nancial relationships that could be construed as a potential conict
of interest.
Copyright © 2018 Hendren, Ha, Black, White and Hoe. is is an open-access
article distributed under the terms of the Creative Commons Attribution License (CC
BY). e use, distribution or reproduction in other forums is permitted, provided
the original author(s) and the copyright owner are credited and that the original
publication in this journal is cited, in accordance with accepted academic practice. No
use, distribution or reproduction is permitted which does not comply with these terms.