|Year : 2016 | Volume
| Issue : 1 | Page : 73-80
|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, School of Medicine, Arak University of Medical Sciences, Arak, Iran
2 Students Research Committee, School of Medicine, Arak University of Medical Sciences, Arak, Iran
3 Department of Psychiatry, School of Medicine, Arak University of Medical Sciences, Arak, Iran
4 Department of Biostatistics and Epidemiology, School of Medicine, Arak University of Medical Sciences, Arak, Iran
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|Date of Web Publication||15-Jan-2016|
| 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.
|How to cite this article:|
Yousefichaijan P, Sharafkhah M, Salehi B, Rafiei M. Attention deficit hyperactivity disorder in children with primary monosymptomatic nocturnal enuresis: A case-control study. Saudi J Kidney Dis Transpl 2016;27:73-80
|How to cite this URL:|
Yousefichaijan P, Sharafkhah M, Salehi B, Rafiei M. Attention deficit hyperactivity disorder in children with primary monosymptomatic nocturnal enuresis: A case-control study. Saudi J Kidney Dis Transpl [serial online] 2016 [cited 2019 Nov 14];27:73-80. Available from: http://www.sjkdt.org/text.asp?2016/27/1/73/174077
| Introduction|| |
Attention deficit hyperactivity disorder (ADHD) is one of the most common neurobehavioral disorders of childhood. As per the Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV) criteria, ADHD is classified as inattentive type, hyperactive-impulsive type and combined type.  ADHD affects 5-10% of children in school age.  The causes of ADHD in children are not clearly known; however, some evidence recognizes underlying genetic defect and central nervous system dysfunction as its main causes.  Based on the reported literature, ADHD is associated with a variety of chronic diseases, ,, depression,  behavioral, emotional, language and hearing disorders , and even illnesses such as epilepsy , and abnormal electroencephalogram (EEG) in children. 
As the evidence suggests, in addition to the aforementioned disorders, urinary and bowel disorders can also be associated with ADHD in children. ,,, In this regard, Burgu,  McKeown  and Duel  showed that the prevalence 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 worsening of symptoms in ADHD patients. 
Nocturnal enuresis (NE) is a common problem in children during the developmental years with an estimated overall prevalence ranging from 1.6% to 15%, and possible persistence during adolescence. ,,, NE is the involuntary loss of urine during the night in children aged >5 years, and is distinguished in primary and secondary forms. ,,, 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). , Moreover, NE could be classified as monosymptomatic nocturnal enuresis, in which there are no daytime urinary symptoms, and nonmonosymptomatic nocturnal enuresis, which is accompanied by daytime urinary symptoms.  Similar to ADHD, NE can result in severe mental disorders and academic failure and undermine patients' self-confidence.  Considering the importance of ADHD and NE during childhood, experiencing ADHD and NE simultaneously can have a bigger negative impact on the clinical course and response to treating either of the disorders. , 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 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 enuresis and (3) monosymptomatic nocturnal enuresis. ,,,,,,
Clinical interviews were carried out with the children and their parents to evaluate them as per the inclusion/exclusion criteria. Our inclusion 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, autistic disorders (ASD), Tourette's disorder, ADHD (in the case group, before developing NE) and other considerable psychiatric disorders or nervous system disorders, (2) congenital 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), ,, (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 deficiency, malignancy, etc., (5) chronic medication 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, depression, 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. ,,,, MR was defined as the intelligence quotient (IQ) of ≤70, , epilepsy was defined as a history of recurrent seizures for which no cause can be identified in clinical studies  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 medications. 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) patient'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 therapeutic procedures for kidneys, bladder, ureters, external urinary tract, genitalia and perinea and congenital diseases, especially in the kidneys 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 anatomical disorders in the genitalia area, impaired kidney function (BUN/Cr), history of recurrent urinary tract infections (UTIs), abnormal urinalysis (U/A), kidney and urinary tract stones, UTI (pyelonephritis, cystitis, asymptomatic bacteriuria), urinary tract obstruction, vesicoureteric reflux, hydronephrosis, renal hypoplasia, 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 year  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 macroscopic hematuria, glucosoria, sterile pyuria (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. ,
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 hospital 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, developmental level, economic status, number of family 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 [Table 1] and [Table 2]. Based on A to E items of these criteria, ADHD includes ADHDinattentive 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.
|Table 1: Diagnostic criteria for the three subtypes of attention-deficit/hyperactivity disorder according to the DSM-IV criteria.|
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|Table 2: Diagnostic criteria for the three subtypes of attention-deficit/hyperactivity disorder according to the DSM-IV criteria.|
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The CPRS was standardized by Conners et al in 1999. It has two 93-item and 48-item versions. The present research uses the 48-item version. This version of the Conners Questionnaire evaluates five factors of conduct, psychosomatic-impulsivity, hyperactivity, anxiety and 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.  Abdekhodaie et al  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 completed by the parents and the children were identified with one or other form of ADHD, the children were referred to an expert psychiatrist (project administrator) in order to confirm the diagnosis of ADHD.  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 poisoning [blood lead level (BLL) >5-10 μg/dL  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 binomial 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 stages of this study, the authors abided by the Helsinki declaration principles. A written consent 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 inattentive type, ADHD hyperactive-impulsive type and ADHD mixed type, respectively.
Between the prevalence of ADHD inattentive type (P = 0.01), there were significant difference between the two groups. However, there were no significant differences in the prevalence of ADHD hyperactive-impulsive type (P= 0.08) and ADHD mixed type (P = 0.84) [Table 3].
|Table 3: Frequency of children with any form of ADHD in the case and control groups.|
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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].
|Table 4: Gender distribution of the children with ADHD inattentive type, ADHD hyperactive–impulsive type and ADHD mixed type in both groups.|
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| 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 al  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 al  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, Baeyens  studied 86 children with enuresis and observed that a considerable number of those with enuresis were also suffering from ADHD. The author concluded that ADHD could be considered as one of the major risk factor of enuresis.
Shreeram  and Yang  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, Elina  obtained a comparable value for onset of ADHD in children with enuresis. In 2012, Kaye  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,  who conducted a study in 1997 aiming at examining urinary disorders in children with ADHD, did not observe any significant difference between different types of urinary disorders in children with ADHD and healthy children.
According to the earlier studies, ADHD prevalence in male children is higher than in female children. ,, Based on our results, and unlike other studies, ,, ADHD was seen more commonly in female children than in male children; however, the difference between genders was not statistically significant. Based on the results of most studies concerning the relationship between ADHD and NE, it seems likely that NE is well associated with ADHD in children, and, based on the earlier studies  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,  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 relationship 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 disorders. 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 examination 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 and also the children and their parents who contributed in this research.
Conflict of Interest: None declared.
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Students Research Committee, School of Medicine, Arak University of Medical Sciences, Arak
[Table 1], [Table 2], [Table 3], [Table 4]
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