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201]

Saudi J Kidney Dis Transpl 2016;27(1):73-80

© 2016 Saudi Center for Organ Transplantation Saudi Journal
of Kidney Diseases
and Transplantation

Original Article

Attention Deficit Hyperactivity Disorder in Children with Primary

Monosymptomatic Nocturnal Enuresis: A Case–Control Study
Parsa Yousefichaijan1, Mojtaba Sharafkhah2, Bahman Salehi3, Mohammad Rafiei4
1
Department of Pediatrics, 2Students Research Committee, 3Department of Psychiatry,
4
Department of Biostatistics and Epidemiology, School of Medicine,
Arak University of Medical Sciences, Arak, Iran

ABSTRACT. Attention deficit hyperactivity disorder (ADHD) is one of the most common
childhood neurological disorders. The aim of this study was to investigate ADHD in children with
primary monosymptomatic nocturnal enuresis (PMNE) and compare it with healthy children. A
total of 100 five to 16-year-old children with PMNE and 100 healthy children without NE were
included in this case–control study as the cases and control groups, respectively. Subjects were
selected from children who were referred to the pediatric clinic of the Amir Kabir Hospital of
Arak, Iran, based on inclusion and exclusion criteria. ADHD was diagnosed by Conner’s Parent
Rating Scale–48 and the Diagnostic and Statistical Manual of Mental Disorders, fourth edition
criteria and was confirmed by consultation with a psychiatrist. Data were analyzed by binomial
test using SPSS18. ADHD inattentive type was observed in 16 cases (16%) with PMNE and five
controls (5%) (P = 0.01). Despite these significant differences in the case and control groups, 25
(25%) and 16 (16%) children were affected by ADHD hyperactive-impulsive type (P = 0.08) and
15 (15%) and 16 (16%) children were affected by ADHD mixed type (P = 0.84), respectively.
ADHD inattentive type in children with PMNE was significantly more common than that in
healthy children. The observed correlation between ADHD inattentive type and PMNE makes
psychological counseling mandatory in children with PMNE.

Introduction Diagnostic and Statistical Manual of Mental

Attention deficit hyperactivity disorder
(ADHD) is one of the most common neuro-
behavioral disorders of childhood. As per the
Correspondence to:
Dr. Mojtaba Sharafkhah
Students Research Committee,
School of Medicine, Arak University of
Medical Sciences, Arak, Iran
E-mail: sharafkhah@arakmu.ac.ir
Disorders, fourth edition (DSM-IV) criteria,
ADHD is classified as inattentive type, hyper-
active-impulsive type and combined type.1
ADHD affects 5–10% of children in school
age.2 The causes of ADHD in children are not
clearly known; however, some evidence recog-
nizes underlying genetic defect and central
nervous system dysfunction as its main cau-
ses.3 Based on the reported literature, ADHD
is associated with a variety of chronic di-
seases,4-6 depression,6 behavioral, emotional,
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74
language and hearing disorders7,8 and even
illnesses such as epilepsy4,5 and abnormal
electroencephalogram (EEG) in children.9
As the evidence suggests, in addition to the
aforementioned disorders, urinary and bowel
disorders can also be associated with ADHD
in children.10-13 In this regard, Burgu,11
McKeown12 and Duel13 showed that the preva-
lence of different types of urinary disorders
and constipation is significantly higher in
children with ADHD than in healthy control. It
is also found that urinary disorders such as
enuresis can be related to the onset and wor-
sening of symptoms in ADHD patients.14
Nocturnal enuresis (NE) is a common pro-
blem in children during the developmental
years with an estimated overall prevalence
ranging from 1.6% to 15%, and possible per-
sistence during adolescence.15-18 NE is the
involuntary loss of urine during the night in
children aged >5 years, and is distinguished in
primary and secondary forms.15-18 In primary
enuresis, children have never gained control
over urination (about 75% of cases), while in
secondary enuresis children have developed
incontinence after a period of at least six
months of urinary control (25% of cases).19,20
Moreover, NE could be classified as mono-
symptomatic nocturnal enuresis, in which there
are no daytime urinary symptoms, and non-
monosymptomatic nocturnal enuresis, which is
accompanied by daytime urinary symptoms.21
Similar to ADHD, NE can result in severe
mental disorders and academic failure and
undermine patients’ self-confidence.22 Consi-
dering the importance of ADHD and NE du-
ring childhood, experiencing ADHD and NE
simultaneously can have a bigger negative
impact on the clinical course and response to
treating either of the disorders.11,23 This study
was carried out with the aim to investigate
ADHD and its association in children with
primary monosymptomatic nocturnal enuresis
(PMNE) and compare it with healthy children.
Methods
This case–control study was performed on
200 children in the age group between five and
Yousefichaijan P, Sharafkhah M, Bahman Salehi B, et al
16 years who were referred to the pediatric
clinic of the Amir Kabir Hospital in Arak, Iran
in 2013. Of the 200 children under study, 100
children with PMNE as the case group and
100 healthy children without NE as the control
group were included in the study based on the
inclusion and exclusion criteria. As per
standard definitions, PMNE was classified and
grouped as follows: (1) NE, (2) primary enu-
resis and (3) monosymptomatic nocturnal enu-
resis.15-21
Clinical interviews were carried out with the
children and their parents to evaluate them as
per the inclusion/exclusion criteria. Our inclu-
sion criteria were: (1) children of both genders
in the age bracket of five to 16, (2) children
with PMNE according to its diagnostic criteria
and (3) written consent from patients’ parents
or guardians. Our exclusion criteria were: (1)
history of major depressive disorder (MDD),
anxiety disorders (ADs), schizophrenia, autis-
tic disorders (ASD), Tourette’s disorder,
ADHD (in the case group, before developing
NE) and other considerable psychiatric disor-
ders or nervous system disorders, (2) conge-
nital and chromosomal abnormalities such as
Down’s syndrome and fetal alcohol syndrome,
birth weight <1500 g or very low birth weight
(VLBW), (1 and 2 due to confounding factors
that - based on the studies - may contribute to
ADHD in children),1,24,25 (3) substance abuse,
mental retardation (MR) and history of sleep
apnea or other sleeping disorders that can
cause ADHD-like symptoms, (4) history of
considerable or chronic medical disorders such
as epilepsy, asthma, diabetes, immune defi-
ciency, malignancy, etc., (5) chronic medica-
tion use, low socio-economic status, parental
consanguinity and separation or death and (6)
family history of major psychiatric diseases
aiming first-degree relatives (parents and
siblings) such as ADs, schizophrenia, depres-
sion, ADHD, etc.
Schizophrenia, different types of ADs (post-
traumatic stress disorder [PTSD], panic attacks,
etc.), MDD, ASD, Tourette’s disorder and
other considerable psychiatric disorders were
defined according to the DSM-IV criteria by
the history of each.26-30 MR was defined as the
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Attention deficit hyperactivity disorder in children with enuresis
intelligence quotient (IQ) of ≤70,31,32 epilepsy
was defined as a history of recurrent seizures
for which no cause can be identified in clinical
studies5 and chronic drug use was defined as a
history of at least six months to one year of
continuous use of one or more types of medi-
cations. Moreover, the low socioeconomic
status was considered as monthly family
income <5,000,000 Rials, (the equivalent of
American $400) for a family of three to five
members and parental education lower than
diploma. Diagnostic evaluation (clinical,
laboratory and imaging studies) were carried
out on the children who were with PMNE
taking into consideration the clinical histories
of their parents and their medical records (if
available).
These diagnostic evaluation included (1) pa-
tient’s history (medical and surgical history,
history of polydipsia and frequent urination
and liquid intake at night, major trauma in the
genitalia area, invasive diagnostic and thera-
peutic procedures for kidneys, bladder, ureters,
external urinary tract, genitalia and perinea
and congenital diseases, especially in the kid-
neys and unitary tracts), (2) full physical
examination, (3) blood and urinary chemistry
tests and urine culture test and (4) sonograms
of kidneys, bladder and ureters.
Based on these findings, children who did not
have any underlying problems such as anato-
mical disorders in the genitalia area, impaired
kidney function (BUN/Cr), history of recurrent
urinary tract infections (UTIs), abnormal uri-
nalysis (U/A), kidney and urinary tract stones,
UTI (pyelonephritis, cystitis, asymptomatic
bacteriuria), urinary tract obstruction, vesico-
ureteric reflux, hydronephrosis, renal hypo-
plasia, ectopic kidney, neurogenic bladder and
any unilateral and bilateral renal and/or urinary
tract anomalies were recruited. Repeated UTI
was defined as a minimum of two UTIs in a
year33 and anatomical disorders of the genitalia
area were defined as any abnormality caused
by congenital reasons or trauma or surgery in
the genitalia area (such as labial adhesion).
Abnormality in urinalysis and the urine culture
test were defined as microscopic and/or mac-
roscopic hematuria, glucosoria, sterile pyuria
75
(more than five to eight white blood cells in
each high-power field without bacteria in
urine) and positive urine culture. More than
100,000 microbial colonies per milliliter of
clean-catch midstream urine sample obtained
by free voiding or 10,000 colonies plus UTI
symptoms were defined as positive UTI.34,35
According to the diagnostic workup and
PMNE definition, the children with PMNE
were entered into the study as the case group
and the control group members were selected
from children who were referred to the hos-
pital for common cold, etc. as an outpatient. A
matching method was used for selecting the
control group and children were matched in
two groups regarding age, gender, develop-
mental level, economic status, number of fa-
mily members and place of residence (in terms
of floor and area) with a standard deviation of
±2. After primary evaluation regarding the
exclusion/inclusion criteria and receipt of
informed consent from childrens’ parents for
participating in the study, basic information
(age, sex) was recorded.
ADHD was diagnosed by its DSM-IV criteria
and the Conner’s Parent Rating Scale–48
(CPRS-48). The ADHD DSM-IV criteria are
given in Tables 1 and 2. Based on A to E items
of these criteria, ADHD includes ADHD-
inattentive type, ADHD-hyperactive–impulsive
type and ADHD combined type (1). The
ADHD-inattentive type was defined if six (or
more) symptoms of inattention (but fewer than
six symptoms of hyperactivity–impulsivity)
have persisted for at least six months, the
ADHD hyperactive–impulsive type was defined
if six (or more) symptoms of hyperactivity–
impulsivity (but fewer than six of inattention)
have persisted for at least six months and the
ADHD combined Type was defined if six (or
more) symptoms of inattention and six (or
more) symptoms of hyperactivity–impulsivity
have persisted for at least six months.
The CPRS was standardized by Conners et al
in 1999. It has two 93-item and 48-item ver-
sions. The present research uses the 48-item
version. This version of the Conners Question-
naire evaluates five factors of conduct, psycho-
somatic–impulsivity, hyperactivity, anxiety and
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76 Yousefichaijan P, Sharafkhah M, Bahman Salehi B, et al

Table 1. Diagnostic criteria for the three subtypes of attention-deficit/hyperactivity disorder according to
the DSM-IV criteria.
A criteria
Persistent pattern of inattention and/or hyperactivity–impulsivity that is more frequently displayed and is
more severe than is typically observed in individuals at a comparable level of development. The
individual must meet the criteria for either (1) or (2)
1a 2b
Inattention Hyperactivity Impulsivity
(a) Often fails to give close attention to (a) Often fidgets with hands or (g) Often blurts out
details or makes careless mistakes in feet or squirms in seat answers before questions
schoolwork, work or other activities (b) Often leaves seat in class- have been completed
(b) Often has difficulty sustaining attention room or in other situations in (h) Often has difficulty
in tasks or play activities which the remaining seated is awaiting turn
(c) Often does not seem to listen when expected (i) Often interrupts or
spoken to directly (c) Often runs about or climbs intrudes on others (e.g.,
(d) Often does not follow through on excessively in situations in butts into conversations
instructions and fails to finish schoolwork, which it is inappropriate (in or games)
chores or duties in the workplace (not due adolescents or adults, may be
to oppositional behavior or failure to limited to subjective feelings
understand instructions) of restlessness)
(e) Often has difficulty organizing tasks (d) Often has difficulty playing
and activities or engaging in leisure acti-
(f) Often avoids, dislikes or is reluctant to vities quietly
engage in tasks that require sustained (e) Is often “on the go” or
mental effort (such as schoolwork or often acts as if “driven by a
homework) motor”
(g) Often loses things necessary for tasks (f) Often talks excessively
or activities (e.g., toys, school assign-
ments, pencils, books or tools)
(h) Is often easily distracted by extraneous
stimuli
(i) Is often forgetful in daily activities
a
Six (or more) of the following symptoms of inattention have persisted for at least 6 months to a degree
that is maladaptive and inconsistent with developmental level, bsix (or more) of the following symptoms
of hyperactivity–impulsivity have persisted for at least 6 months to a degree that is maladaptive and
inconsistent with developmental level.

Table 2. Diagnostic criteria for the three subtypes of attention-deficit/hyperactivity disorder according to
the DSM-IV criteria.
B to E criteria
B C D E
Some hyperactive– Some impairment from There must be clear The disturbance does not occur
impulsive or inatten- the symptoms is pre- evidence of interfe- exclusively during the course of
tive symptoms must sent in at least two rence with develop- a pervasive developmental dis-
have been present settings (e.g., at school mentally appropriate order, schizophrenia or other
before the age of 7 [or work] and at home) social, academic or psychotic disorders and is not
years occupational better accounted for by another
functioning mental disorder (e.g., mood dis-
order, anxiety disorder, disso-
ciative disorder or a personality
disorder)
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Attention deficit hyperactivity disorder in children with enuresis 77

Table 3. Frequency of children with any form of ADHD in the case and control groups.
ADHDa inattentive ADHD hyperactive–
ADHD mixed type
type impulsive type
P- P- P-
Caseb Controlc Case Control Case Control
valued value value
(n = 100) (n = 100) (n = 100) (n = 100) (n = 100) (n = 100)
N (%) N (%) N (%) N (%) N (%) N (%)
16 (16) 5 (5) 0.01 25 (25) 16 (16) 0.08 15 (15) 16 (16) 0.84
a
Attention deficit hyperactivity disorder, bchildren group with PMNE, chealthy children group, d,aP-
values <0.05 were considered significant.

learning problems and has four choices scored
from 0 (never) to 3 (very high). The score of
each article is converted into t-scores, with an
average of 50 and standard deviation of 10. If
the t-scores of 12 standard deviations are
higher than the average, the individual has a
problem.36 Abdekhodaie et al37 reported the
sensitivity and specificity of this form of
Conner Questionnaire for the diagnosis of
children with ADHD at 90.3% and 81.2%,
respectively.
After the CPRS-48 questionnaire was com-
pleted by the parents and the children were
identified with one or other form of ADHD,
the children were referred to an expert psy-
chiatrist (project administrator) in order to
confirm the diagnosis of ADHD.1 It should be
mentioned that for confirming the ADHD
diagnosis for children with this disorder, its
differential diagnoses such as hyperthyroidism
(by measuring TSH and FT4) and lead pois-
oning [blood lead level (BLL) >5–10 μg/dL]38
were also excluded.
The collected data were analyzed with SPSS
software (Statistical Package for the Social
Sciences, version 18.0; SPSS Inc., Chicago,
IL, USA) and descriptive statistics methods for
frequency determination. Moreover, the bino-
mial test was used for data analysis. P-values
<0.05 were considered significant. This study
was approved by the ethics committee of the
Arak University of Medical Sciences and in all
Table 4. Gender distribution of the children with ADHD inattentive type, ADHD hyperactive–impulsive
type and ADHD mixed type in both groups.
ADHD inattentive type ADHD hyperactive–impulsive
Gender
(n = 21), N (%)
Male 15 (71.4)
Female 6 (28.5)
P-value 0.08
stages of this study, the authors abided by the
Helsinki declaration principles. A written con-
sent was obtained from all participants and
they were free to exit the study at their will.
Results
The mean ages of children in the PMNE and
control groups were 7.9 ± 2.09 and 8.2 ± 1.23
years, respectively (P = 0.21). There were 49
(49%) boys and 51 (51%) girls in the case
group and 50 (50%) boys and 50 (50%) girls
in the control group (P >0.05).
Of the 200 (100%) children under study in
both groups, 21 (10.5%), 41 (20.5%) and 31
(15.5%) children were affected by ADHD in-
attentive type, ADHD hyperactive–impulsive
type and ADHD mixed type, respectively.
Between the prevalence of ADHD inattentive
type (P = 0.01), there were significant diffe-
rence between the two groups. However, there
were no significant differences in the preva-
lence of ADHD hyperactive–impulsive type (P
= 0.08) and ADHD mixed type (P = 0.84)
(Table 3).
The results showed that there is no significant
relationship between ADHD inattentive type
(P = 0.08), ADHD hyperactive–impulsive type
(P = 0.19) and ADHD mixed type (P = 0.18)
and gender distribution of the children under
study in both groups (Table 4).
ADHD mixed type
type (n = 41), N (%) (n = 31), N (%)
19 (46.3) 10 (32.2)
22 (53.6) 21 (67.7)
0.19 0.18
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78
Discussion
Based on our study, there were no significant
differences in the prevalence of ADHD
hyperactive–impulsive type and ADHD mixed
type between the PMNE children and healthy
group. However, the prevalence of ADHD
inattentive type in the children with PMNE
was significantly higher than those in the
control group.
The relationship between NE and ADHD was
investigated in the study by Baeyens et al14 on
120 children with ages ranging from six to 12
years. Based on the results, of all enuretic
children 15% were diagnosed with the full
syndrome of ADHD and 22.5% met the
criteria of the ADHD inattentive subtype. Data
revealed that the older the children (9 to 12
years), the higher prevalence of attention
deficit disorder or ADHD. In another study by
Okur et al39 in 2012, 64 children with NE were
investigated for ADHD and compared with 42
children without NE. The results indicated that
26.6% and 14.1% of the case group suffered
from ADHD inattentive type and ADHD
hyperactive–impulsive type, respectively.
In 2005, Baeyens40 studied 86 children with
enuresis and observed that a considerable
number of those with enuresis were also suf-
fering from ADHD. The author concluded that
ADHD could be considered as one of the
major risk factor of enuresis.
Shreeram41 and Yang42 mentioned onset of
ADHD in the children with enuresis and onset
of enuresis in the children with ADHD as
9.89% and 28.3%, respectively. Similar to
Shreeram, Elina43 obtained a comparable value
for onset of ADHD in children with enuresis.
In 2012, Kaye44 showed that among 75
children with ADHD and different urinary
disorders, 88% and 87% are with frequency
and enuresis, respectively.
Despite the results of most studies and our
study, Robson,45 who conducted a study in
1997 aiming at examining urinary disorders in
children with ADHD, did not observe any sig-
nificant difference between different types of
urinary disorders in children with ADHD and
healthy children.
Yousefichaijan P, Sharafkhah M, Bahman Salehi B, et al
According to the earlier studies, ADHD pre-
valence in male children is higher than in
female children.1,24,46 Based on our results, and
unlike other studies,1,24,46 ADHD was seen
more commonly in female children than in
male children; however, the difference bet-
ween genders was not statistically significant.
Based on the results of most studies concer-
ning the relationship between ADHD and NE,
it seems likely that NE is well associated with
ADHD in children, and, based on the earlier
studies39 and the present study, it seems likely
that there is a stronger relationship between
NE and the inattentive-type subgroup of
ADHD.
In conclusion, based on our findings and the
recommendations of the earlier studies – such
as the study of Shreeram et al,41 it is better to
study the children with NE for ADHD so that
a useful psychiatric therapeutic intervention
can be performed for this group of children if
necessary.
As there are limited studies concerning the
relationship between ADHD and the primary
monosymptomatic form of enuresis, the rela-
tionship between ADHD and enuresis may be
under the influence of different underlying
factors in each region, such as genetic factors
and onset level of either of these two dis-
orders. We suggest that further studies in this
field should be conducted in other treatment
centers in the future.
Finally, it should be mentioned that with the
limitations of our study, we should indicate the
non-cooperation of some parents to fill in the
ADHD questionnaire and the psychiatric exa-
mination of the child. Although this criterion
caused us to exclude some children who could
have been eligible for the study, we had
earnestly attempted to remove such limitations
by encouraging the parents by explaining the
possible usefulness of the study and helped
them fill in the said questionnaire.
Acknowledgments
The research team wish to thank the vice
chancellor of research, Arak University of
Medical Sciences, for their financial support
[Downloaded free from http://www.sjkdt.org on Wednesday, September 28, 2016, IP: 31.46.144.201]
Attention deficit hyperactivity disorder in children with enuresis
and also the children and their parents who
contributed in this research.
Conflict of interest: None declared.
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