International Journal of Contemporary Pediatrics

Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

http://www.ijpediatrics.com pISSN 2349-3283 | eISSN 2349-3291

DOI: http://dx.doi.org/10.18203/2349-3291.ijcp20160836
Research Article

Neurodevelopmental comorbidity profile in specific learning disorders

Alpana Somale, Santosh V. Kondekar*, Surbhi Rathi, Nisha Iyer

Department of Pediatrics, T N Medical College, Mumbai-400008, INDIA

Received: 10 March 2016

Accepted: 18 March 2016

*Correspondence:
Dr. Santosh V. Kondekar,
E-mail: drkondekar@gmail.com

Copyright: © the author(s), publisher and licensee Medip Academy. This is an open-access article distributed under
the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial
use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

Background: Specific learning disorders (SLD) are the common reasons for referral of an otherwise healthy child
from a main stream school. Although children do have difficulties even in early learning years in pre-primary and
primary school; a significant number of preadolescent children from mainstream school do present with such
disabilities. Primary objective was to study the differential distribution of various comorbidities across SLD spectrum.
Secondary objective was to check for prevalence of abnormal neurological examination findings including soft signs.
Methods: After approval of institutional ethics committee, 100 consecutive case records of children presenting to the
center were studied. Diagnosis was confirmed as per DSM V criteria. The clinical, psychological and neurological
information was derived from notes of pediatrician, after SLD certification. Details about history, ADHD and
comorbidities if any were recorded from parents where documented information was not sufficient. The prevalence of
comorbidities was expressed as a percentage of total cases studied.
Results: ADD of combined type was the commonest comorbidity seen in 53% cases. Other occasional comorbidities
noted were epilepsy, autism, cerebral palsy, history of meningitis and febrile seizures. Speech and visuospatial skills
were affected 10% and 41% in children with SLD and all of these had ADD. Soft neurological signs like
astereognosis, graphesthesia, dysdiadochokinesia, dysmetria were seen in more than 20% cases. Abnormal antenatal
and perinatal history was more common in ADHD with SLD.
Conclusions: SLD children from mainstream schools usually have ADHD as commonest comorbidity. Often they
should be looked for various neurological comorbidites like autism, epilepsy, cerebral palsy. Soft signs and motor
delay need not be overlooked in view of comprehensive management. A large multicentric study is needed to look for
soft neurological signs; neuroimaging may be needed in SLD to understand the disorders in cognitive spectrum.

Keywords: Dyslexia, Specific learning disorder, Comorbidity, ADHD

INTRODUCTION Previously known as dyslexia or learning disability; now

as per DSM V classification it is labeled as Specific
Awareness of specific learning disorder (SLD) in India Learning Disorder (SLD).2 In 2013, DSM-5 defined a
existed two decades ago. Kulkarni M et al described Specific Learning Disorders (SLD) as “difficulties in
approach to learning disabilities and also stated that learning and using academic skills”. Alves LM had noted
dyslexia and its comorbidities affect true potential and that school children took longer time to conclude tasks
ability of an individual.1 Despite all facilities and when they had SLD or ADHD.3 Governments have
capabilities; few children in mainstream schools do have introduced special concessions or assistance to the
issues related to reading, writing, basic arithmetic skills certified children by making special legal provisions.
appropriate for the age. These children do present at These learning difficulties are likely to be innate and due
times in early learning years; or they present at age when to central nervous system dysfunction. They are not
complex learning issues are involved. better accounted for by intellectual disabilities,

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 Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

uncorrected visual or auditory acuity, other mental or Institutional Ethics Committee permission was taken
neurological disorders, psychosocial adversity, lack of prior to commencement of study.
proficiency in the language of academic instruction, or
inadequate educational instruction.2 Children from age 7-16 year referred from main stream
schools with or without neurological disorders and had a
The following describes the updated 2013 DSM-5 SLD certification from our institute were included. Non-
diagnostic subtypes of specific learning disorder:4 schooling children and children from special
rehabilitatory schools were excluded. Children with
1) Specific learning disorder with impairment in reading major psychiatric disorders like depression, psychosis,
includes possible deficits in: word reading accuracy, behavioural disturbances and adjustment disorders were
Reading rate or fluency, reading comprehension. 2) excluded.
Specific learning disorder with impairment in written
expression includes possible deficits in: spelling Consecutive 100 certified cases of SLD from mainstream
accuracy, grammar and punctuation accuracy, clarity or school certified by a team of pediatrician and
organization of written expression. 3) Specific learning psychologist were studied, after taking a written informed
disorder with impairment in mathematics includes consent from parents and assent from children above age
possible deficits in: number sense, memorization of 7 years. It was a convenient sampling as only 119 cases
arithmetic facts, accurate or fluent calculation, accurate were on record in the study year 2013 and 19 cases were
math reasoning. excluded due to referral from pre-primary school or
special school.
Changed spectrum of SLD as per new criteria, does
create challenges and generate need for revisions in The diagnosis of SLD was confirmed as per DSM V,
comparative research, clinical evaluations and from available structured age appropriate psychological
implementations of Individuals with disabilities assessment by certifying team of specialists.
education act (IDEA) in school settings.5 Neurodevelopmental morbidities and clinical signs,
symptoms were noted from notes of pediatrician.
Schulte-körne G described prevalence of these disorders Information regarding Birth history, family history and
as 5-15%.4 Sahoo et al quoted prevalence as 2-10%, in medical history was based on recall by parents. ADHD
school children with 30% these having neuropsychiatric diagnosis was confirmed as per DSM V criteria during
issues like ADHD, behavioural problems,anxiety, parent interview. The data was analysed using Microsoft
depression that may go unrecognised.6 excel and the prevalence was studied as percentage with
total number of study population as denominator.
The comorbidity profile apart from ADHD is least
studied; primarily because the DSM IV definition of RESULTS
dyslexia had excluded visual, hearing, intellectual and
motor disabilities. Many neurological comorbidities are In this study, out of 100 cases of SLD, 69% were boys
known to have SLD as association either due to disease and 31% were girls. Mean age of children was 12.2%;
or otherwise due to original insult. Epilepsy, autism, median age of children was 13.5 years, although there
Attention deficit hyperactivity disorder (ADHD), cerebral were 3 children between ages 7-9 years (Table 1).
palsy, genetic syndromes are few of the conditions in
which SLD is likely to exist. The neurodevelopmental Table 1: Age distribution of SLD children from
comorbidities appear to be overlooked. mainstream schools.

This study aims to know the prevalence of these neuro Age wise distribution of SLD
Age distribution
developmental comorbidities in SLD; so that a cases on record
comprehensive therapy plan can be targeted to cure. 7 to <9 years 3
9 to <11 years 22
METHODS
11 to <13 years 20
The study was aimed at understanding the prevalence of 13 to <15 years 33
neurological and developmental comorbidities in
15 to <16 years 22
mainstream school children being certified as SLD at our
institute. Primary objective was to study the differential Mean=12.2 year, Median 13.5 year
distribution of various comorbidities across SLD
spectrum. Secondary objective was to check for Eighty three percent of children had impairment in all
prevalence of abnormal neurological examination three domains of SLD; that is reading (dyslexia), writing
findings including soft signs. (dysgraphia) and arithmetic (dyscalculia). Impairment of
reading was seen in 94% cases; while impairment of
This study was conducted as a prospective observational writing was noted in 99% cases and impairment in
study at a tertiary care pediatric institute. calculations was seen in 86% cases of SLD as per DSM

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 Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

V, as assessed by psychologist with age appropriate short Commonest comorbidity noted was ADHD, in 53% cases
tests for reading writing and calculations of previous (n=100). Autism was noted in 3% cases (2 girls and 1
standard. boy) while epilepsy and cerebral palsy were noted in 2%
cases each. Three cases had history of meningitis and 8
As per Table 2, amongst total 100 cases, 39 children with cases had history of febrile seizures. Inattentive type
SLD had no comorbidities. Amongst total 83 cases with ADHD was also an overlapping additional comorbidity in
all three domains of SLD affected, 46.98% cases (29) had epilepsy, cerebral palsy and meningitis. Amongst 53
no neuro developmental comorbidity. cases of SLD with ADHD, 56% (30) cases were boys
with ADHD of combined type, 15.09% (8) cases were
Table 2: This study shows number boys and girls with boys of inattentive type ADHD while there were 8 girls
SLD across different comorbidities. with SLD and ADHD of combined type prevailing to
15.09%.
Sex distribution across comorbidities
Comorbidity There were two cases each of cerebral palsy and
distribution Boys with SLD Girls with SLD neurofibromatosis with all three domains affected.
(total cases)
None (39) 25 14 Table 3 shows perinatal aetiological events across
ADHD CT (38) 30 8 comorbidities. Twenty four percent children with SLD
ADHD had significant prenatal history. In most cases it was fever
8 7 and cough for three days, which included 14 cases of
Inattentive (15)
Autism (3) 1 2 SLD with ADHD. Seven cases of SLD also had history
Epilepsy(2) 1 1 of fever in second trimester antenatally.
Cerebral palsy
1 1 Total 15% cases had required resuscitation at birth. These
(2)
included 9 cases of ADHD, one each of epilepsy, cerebral
NF1 (2) 2 0
palsy, febrile seizure, meningitis and two cases with
Erbs palsy (1) 1 0
neurofibromatosis.
Feb seizures(8) 7 1
Meningitis(3) 2 1 Of the 39 cases of SLD without co-morbidities 18.4%
had significant antenatal history and 7.6% had neonatal
hospitalization.

Table 3: Antenatal and prerinatal probable factors across comorbidities.

NICU NICU
SLD Antenatal Birth Birth No
Antenatal Term Preterm stay stay
comorbidities risk resuscitation resuscitation NICU
no risk baby baby yes yes
(cases) present needed not needed stay
<7days >7 d
ADHD CT
8 30 8 30 31 7 2 4 30
(38)
ADHD I (15) 5 9 1 13 13 1 2 1 11
Autism (3) 1 2 0 3 3 0 3
Epilepsy (2) 0 2 1 1 2 0 0 1 1
Cerebral palsy
1 1 1 1 2 0 1 1 0
(2)
NF1(2) 0 2 0 2 2 0 0 0 2
Erbs palsy (1) 0 1 1 0 1 0 1 0 0
Feb seizures
1 7 2 6 7 1 1 1 6
(8)
Meningitis (3) 1 2 1 2 2 1 0 2 1
NO
comorbidity 7 31 1 38 36 2 1 2 35
(39)

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 Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

Parents of 31.5% cases with SLD with ADHD-combined Nocturnal Enuresis was noted in 10 cases out of 53 who
type had recalled a positive family history in father in the had SLD with ADHD.
form of early year learning difficulties. Also parents of
20% of SLD with inattention type had paternal history of More so, the higher functions like speech, gait, left-right
inattention in their primary school age. orientation, visual spatial skills and ability to tell time
were affected significantly in those SLD with ADHD
Amongst two kids who had SLD with Neurofibromatosis; (Table 4), but also in few SLD children without any
there was a family history of neurofibromatosis but not of comorbidity. Despite being main stream, 18% of ADHD
SLD. CT type had speech delay, 9.4% had gait issues, and
62.2% had poor directionality. Among the three students
Only three cases had microcephaly, two cerebral palsy with autism, all had abnormal speech and 2 had poor
cases and third one with history of meningitis. directionality and visual spatial skills. Amongst 39
children with no comorbidities, 12.5% had abnormal gait,
Fine motor and language milestones were delayed in SLD 25% had speech deficit and 37.5% had poor time
with epilepsy, cerebral palsy, and history of meningitis. orientation and 50% had poor directionality. Seventy five
Language milestones were delayed in all 3 cases of percent of SLD children without added comorbidities had
autism and 8 cases of ADHD. Fine motor milestones poor visual spatial skills.
were delayed in 49% of SLD with ADHD.
Table 4: Abnormal higher neurological functions in SLD children with comorbidities.

SLD Comorbidities (cases) Speech Gait L-R orientation Time orientation Visuospatial skills
ADHD CT (38) 10 4 24 17 31
ADHD I (15) 0 1 9 7 10
Autism (3) 3 0 2 1 2
Epilepsy (2) 1 0 2 2 2
Cerebral palsy (2) 2 1 2 1 1
NF1(2) 0 0 1 1 1
Erbs palsy (1) 0 0 0 0 1
Feb seizures (8) 2 1 4 3 6
Meningitis (3) 0 1 3 3 3
NO cormorbidity (39) 4 0 6 6 11

Table 5: Abnormal gross and soft neurological signs in SLD children.

Comorbidity Tone Power DTR Plantar Cerebellar signs Soft CNS signs
ADHD CT (38) 16 0 4 3 1 24
ADHD I (15) 3 0 0 0 0 7
Autism (3) 0 0 0 0 0 3
Epilepsy (2) 0 0 0 0 0 2
Cerebral palsy (2) 2 1 2 2 0 2
NF1(2) 0 0 0 0 0 1
Erb’s palsy (1) 1 1 1 0 0 1
Feb seizures (8) 3 0 2 2 0 6
Meningitis (3) 3 0 1 1 1 3
NO comorbidity (39) 3 0 0 0 1 13

Gross CNS examination abnormalities were very In cases of SLD without any comorbidity, 7.6% children
infrequent. In SLD with ADHD of combined type, 38.5% had minor tone abnormalities and 2.5% of these had
had tone issues as compared to 20% amongst inattention cerebellar signs.
type. Ten percent children had abnormal deep tendon
reflexes while extensor plantar and cerebellar signs were A high percentage of children with SLD had soft
seen in 7.8% and 2.6% children respectively. Minor tone neurological signs. Astereognosis was seen in 23% cases,
issues were noted in children who had obvious history or graphesthesia was affected in 28% cases while
CNS insult in the form of meningitis or cerebral palsy dysdiadochokinesia was present in 31% cases. Soft
(Table 5). neurological signs were present in 58.4% of SLD with
ADHD. All children with some or other neurological

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 Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

morbidity had at least one soft neurological sign. al in a large population based study (N=2586) noted that
Amongst SLD without added comorbidities, 33.3% (13) comorbidity rates of impairment in these domains were 4-
had soft neurological signs (Table 5). 5 times higher in those having at least one domain
affection, compared to normal population. Accordingly,
Asterognosis, dysdiadochokinesia, abnormal we had 83% SLD children with affection of all 3
graphesthesia, tandem walking, finger nose test domains.11
abnormalities and abnormal two point discrimination
were seen more in boys compared to girls. Sensory As per literature, ADHD is known to coexist as
extinction and dysdiadochokinesia coordination commonest comorbidity, accounting for 12-24% cases of
abnormalities were by far the commonest soft SLD.12 In our study, it was 53%. Margari et al in a recent
neurological sign amongst boys and girls with SLD study reported ADHD as 33% comorbidity in SLD. 13
(Figure 1). Mayes et al in 2000, reported SLD in 20% of ADHD
cases in a population of 119 children from age 8-16
years.14 A higher mean comorbidity was reported as
45.1% in a review of 17 studies from 2001-2011 by
Dupaul GJ et al.15 This data must be viewed as tentative
because of wide variations and difficulties defining
ADHD. The imbalanced nature of relationship suggests
that these two are likely to be independent syndromes.

Sex predisposition was striking with ADHD as co

morbidity in this study, having 55.07% (n=69) boys with
SLD and ADHD; 43% (30) were of ADHD combined
type. Amongst the girls (n-31%), 48% (15) had ADHD as
co morbidity, with 25% of ADHD combined type. Even
this association is not yet described in literature in
children with SLD. In general ADHD is more comorbid
in boys. LD and ADHD are considered by many as a
continuum, interrelated and are usual association.
Yoshimasu K, Barbaresi WJ followed 5718 children and
Figure 1: Sex distribution of various soft neurological found the cumulative incidence of SLD higher in children
signs amongst SpLD. with ADHD, than otherwise.16 The higher prevalence of
ADHD in our study does confirm the same and point
DISCUSSION towards a common etiology and therapy.

Individual conditions and their association with learning Although 39 cases had significant antenatal or perinatal
disabilities have been studied in great details but the history, more so in cases with ADHD as added morbidity,
spectrum of comorbidities that are associated with LD the previous studies reported significant perinatal history
aren’t really explored. in 30% of subjects.8

The male:female sex ratio was 2.2:1, 69% SLD children Positive family history suggestive of LD was noted in
were boys. A study in Taiwan had male:female ratio of 31.5% of combined type ADHD and 20% of inattentive
5.8:1.7 Our study correlated well with Indian study in type. In all other comorbidities no family history was
2004, with sex ratio of 2.3:1.8 In a study from Bikaner, noted except in case of neurofibromatosis. There is no
the sex ratio was 11.4% vs 7.4%.9 documentation available in literature with respect to
same.
In previous studies, median age of presentation was 11.4
years while our study had median age of 14 years, with In our study, 5% had delayed gross motor milestones,
youngest being 7 year old.8 Al-mamari et al found Mean 35% had delayed fine motor milestones. Language was
age of children with learning disorders in Omani children delayed in 43% cases.
was 8.5 years.10 A higher median age at diagnosis points
to delayed referral. Significantly abnormal antenatal history was 21% ADHD
of combined type, which was more (33.3%) than ADHD
Most common impairment in this study was in writing inattentive type. No past studies were available to
domain (dysgraphia), seen in 99% cases, impaired compare this.
reading(dyslexia) was in 94% cases while 86% cases had
issues in arithmetic.8 Globally the prevalence is near In this study, 5% children had delayed gross motor
about same with writing impairment in 96% of learning milestones and 35% cases had delayed fine motor
disability children, with dyscalculia in 74% cases. milestones. In past literature, delayed milestones were
Reading disability was noted in 60% cases. Landerl K et recorded in less than one third of cases.8 This difference

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 Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

may be attributed to memory bias of parents. Of the 39 There are no studies with concurrence of autism and LD;
children without comorbidities, 17.9% had fine motor we had three children with same. While special education
delay and 35.8% had gross motor delay. In this study, is required for both; more evidence is needed to
10% cases with SLD and ADHD as comorbidity had understand their association. In this study, 2 out of three
delayed gross motor milestones and 50% had delayed autism children with SLD were girls. Autism is known to
fine motor milestones. There are separate studies on be severe in girls but SLD concurrence with autism isn’t
milestone delay in LD or ADHD, but there is no data on studied yet.
delay in LD with ADHD.17,18
Cognitive impairment is a known long term sequel of
Language milestone was delayed in 43% children and bacterial and viral meningitis or encephalitis. There were
22% had history of nocturnal enuresis. three cases with past history of CNS infection. The
association is not studied in literature.
Amongst 39 SLD children without comorbidities 35.8%
had language delay and 17.9% had fine motor delay. No Structural brain imaging in LD was reported as showing
similar studies were on record. loss of grey mater volume and loss of asymmetry of left
planum temporal. In this study neuroimaging was
These things point out towards possible complex multiple available only in few symptomatic cases, of cerebral
neurodeficits independently or together resulting in SLD. palsy, meningitis and epilepsy. The findings were
correlating with primary insult in some while in others it
Soft neurological signs were present in 58.4% of children was normal.
with ADHD and 33.33% of kids without comorbidities.
Various soft neurological signs were noted by Karande et This study was limited by many factors despite good
al in 54% cases with LD.8 Some studies noted unusually sample size. The children were from main stream schools
high prevalence of soft neurological signs in LD. In that had bias making samples size population without
literature, no data was available with soft signs in intellectual disability. Most children were above age 10
presence of comorbidities. years, making age appropriate assessment tricky.
Children were enrolled after SLD certification, so those
Approximately a third to a fourth of patients with who had been referred but were not certified could not be
epilepsies have learning disability and conversely 6-24% studied. Also despite some good references we could not
of SLD may have seizure disorders.19 directly compare our results to them as all references had
cases defined as per DSM IV as dyslexia and this study
In our study, only 2% had idiopathic epilepsy. Both these had the latest broad spectrum definition while applying
children were well controlled on valproate therapy. same. This study had excluded psychiatric morbidities for
Dyslexia was a known morbidity in 19.4% of children technical reasons.
with rolandic epilepsy in a recent study by Oliveria et
al.20 CONCLUSION

Discrepancy between these and our results are likely to ADHD of combined type was most common morbidity
be due to small sample size and children from higher with SLD in children from main stream school. A good
middle class main stream school. SLD severity is number of these cases had abnormal antenatal or prenatal
expected to be more with early age of onset of seizures. history and soft neurological signs. Autism, Epilepsy and
As the sample size was from mainstream and involved CP were additional comorbidities that could not be
elder kids; cases of epilepsy with SLD with IQ deficits neglected. Soft neurological signs were likely to be
automatically got dropped. This may explain low abnormal in LD with or without ADHD.
incidence of seizure cases in our study. Our study, had 8
children with history of febrile seizures in past. Of these Fine motor and language delay was frequently associated
five were typical and three were atypical. These findings with LD. This study suggests the possibility of complex
confirm of no specific association of febrile seizure multiple neurodeficits independently or together resulting
history with SLD as concluded by Norgaard M et al. 21 in SLD.

Association between CP, epilepsy and SLD is known A large multicentric study is needed to look for soft
throughout literature. We had only 2% cases of CP in this neurological signs, neuroimaging and organic causes of
study. As the mean age was 12.5 years, it would have SLD, so as to help in therapy.
been unlikely for a cognitively abnormal child to study in
main stream. ACKNOWLEDGEMENTS

Similarly apart from motor deficit causing writing We thank Dean TNMC Mumbai for permission of
difficulty, we could not find any reason for the SLD in publication of this research paper.
the case of Erb’s palsy.

International Journal of Contemporary Pediatrics | April-May 2016 | Vol 3 | Issue 2 Page 360
 Somale A et al. Int J Contemp Pediatr. 2016 May;3(2):355-361

Funding: No funding sources 11. Landerl K, Moll K. Comorbidity of learning

Conflict of interest: None declared disorders: prevalence and familial transmission. J
Ethical approval: Ethical Approval from Institutional Child Psychol Psychiatry. 2010;51(3):287-94.
ethics committee 12. Karande S, Kulkarni M. Specific learning disability:
the invisible handicap. Indian Pediatr.
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Cite this article as: Somale A, Kondekar SV, Rathi S,
Iyer N. Neurodevelopmental comorbidity profile in
specific learning disorders. Int J Contemp Pediatr
2016;3:355-61.

International Journal of Contemporary Pediatrics | April-May 2016 | Vol 3 | Issue 2 Page 361