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April2014 Vol.51 Issue:      2 Table of Contents
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Neuropsychiatric Correlates of Nocturnal Enuresis in Adolescent and Young Adult Females

Salwa Mohamad Rabie1, Maha Ali Hassan1, Saber A. Mohamed2, Nermin Ali Hamdy1

Departments of Neurology and Psychiatry1, El-Minia University; Psychiatry2, Zagazig university; Egypt



ABSTRACT

Background: Nocturnal Enuresis (NE) is a common problem throughout the world. It has high prevalence in the preschool population and the prevalence gradually falls during childhood and adult life. NE in teenagers and adolescents is a different matter; it may be worrisome for parents and embarrassing for adolescents, and is considered a physical symptom of deeper troubles in a teenager or adolescent. Objective: To assess the neuropsychiatric correlates in adolescent and young adult female patients. Methods: The present study included 22 female patients with NE (their mean age was 15.81±2.57 years), and 22 -age matched control subjects. All were subjected to proper history taking, thorough neurological and psychiatric examination, urine analysis, lumbosacral spine plain X-ray, EEG, IQ and test for Soft Neurological Signs (SNS). Results: Ninety percent of patients have 1ry NE, 10 patients (45.4%) has family history of NE, only 12 patients (54.5%) of them sought medical advice.  EEG showed epileptiform changes in 9 (40.9%) cases. IQ was lower than in control subjects. Soft Neurological Signs (SNS) were significantly prevalent and negatively correlated with IQ. Patients had psychiatric abnormalities including low self-esteem. Conclusions: Adolescent and young adult females with NE have subtle neurological dysfunction, higher incidence of EEG changes, lower mean IQ, psychiatric abnormalities and delayed menarche, which might indicate a maturational deficit in the central nervous system in these cases. [Egypt J Neurol Psychiat Neurosurg.  2014; 51(2): 207-214]

Key Words: Nocturnal Enuresis, Adolescents, Soft Neurological Signs, Psychological impact

 Correspondence to Salwa Mohamad Rabie. Department of Neurology and Psychiatry, El-Minia University, Egypt.Tel.: +96547588108. Email: Salwarabie4@yahoo.com






INTRODUCTION

 

Nocturnal enuresis (NE) is defined as the involuntary loss of urine control at night when the individual is sleeping.1 While DSM-IV2 defines it as wetting at least twice a week,  the ICD-103 requires a frequency of 2/month (under 7 years ) or 1/month(over 7 years).

Bedwetting has a very high prevalence in the preschool population and the prevalence slowly falls during childhood.4,5 NE affects about 10-12% of six year olds, 2-3% of 12 year olds and 1% of adults.6 The ratio of the incidence of enuresis in boys versus girls is 2:1; at age of 5 years old. This ratio becomes 1:1 at adolescence.7 Enuresis is more common in lower socioeconomic groups.6

NE is classified into primary (PNE) where full urinary continence has never been achieved by age of five, and secondary (SNE) in which the person has had at least six months of dryness at night.1,8 

Three factors were presumed to participate in the pathogenesis of idiopathic NE.9 First, a disorder of sleep arousal when patients do not wake up to the sensation of a full or contracting bladder.10 Attention is being focused

 

on the locus coeruleus in the brain-stem which plays a key role in initiating cortical arousal to bladder distension, and plays a role in antidiuretic hormone (ADH) release.11  Second, nocturnal polyuria, which can be due to the evening and daytime fluid and solute intake, and the nocturnal secretion of antidiuretic hormone (ADH).9,12 Children with NE might have an abnormal circadian rhythm with increased water retention during the day and the reverse by nigh.13 Third, reduced nocturnal bladder capacity5, that can be attributed to cystitis and constipation.14

Soft Neurological Signs (SNS) refer to any neurological deviation- motor, sensory or integrative- that does not localize the site of a putative central nervous system lesion.15

The present study was planned to explore the neuropsychiatric correlates in adolescent and young adult female patients with NE.

 

SUBJECTS AND METHODS

 

Females with NE 12 years and older were recruited at Neurology and Psychiatry outpatient clinics, in El-Minia University Hospital. Consent from the patients and their families were taken. The exclusion criteria included patients aged under 12 years, clinical manifestation of epilepsy, mental retardation, acquired causes for nocturnal enuresis (cystitis, constipation, neurogenic bladder, urethral obstruction, diabetes insipidus, DM), pharmacologic treatment that may result in enuresis as a side effect and patients who did not agree to share in the study.

Twenty -two- age matched females were used as a control group and were collected from the normal females that accompany other patients attending the neurology and psychiatric- outpatient clinic, at El-Minia University Hospital.

Patients and the control group were subjected to specially designed form for the study was prepared by the researchers, including detailed history of NE (type, frequency, precipitating factors), psychosexual history, epilepsy, other neurological complaints and lifetime psychiatric disorders. Furthermore, they were subjected to thorough neurologic examination, urinalysis, (to exclude cystitis and diabetes mellitus), Lumbosacral spine plain X-ray (to exclude sacral agenesis or spinal dysraphism), digital Electroencephalography (EEG) (using 16 channel Nihon Kohden machine), assessment of IQ (using Stanford Binet Test) and test for soft neurological signs (SNS) that is composed  of three  groups; the first assesses some primitive reflexes, the second is concerned with repetitive sequential motor execution, and the third consists of tests related to integration of sensory information.16

 

Statistical Analysis

The advanced statistical package for social science (SPSS) for MS Windows (version 11.0) was used to perform the statistical analysis. Simple descriptive tests (Mean and Standard deviation) are used to describe the numerical values of the sample. To test the 2- tailed significance of differences in means, Student t-test for independent samples for 2 groups and one-way analysis of variance (ANOVA) test for comparison between more than 2 groups were used. Spearmen correlation test was used for correlations. A probability of (P) ≤ 0.05 is accepted as significant.

 

RESULTS

 

Due to the ‘taboo’ nature of the subject, we could recruit only 22 female patients over a two years period. Their ages ranged between 12 and 22 (15.81±2.57). All cases were right handed. Two cases were illiterate, 10 in preparatory School, 7 in Secondary School, 1 in faculty and 2 cases were graduated (Table 1).

All cases had normal delivery with no postpartum complications except for two patients (9.1%) who had low birth weight. All cases were breast fed except two (9.1%) were artificially fed. Three patients had developmental delay (13.6%) and one patient (4.54%) had early psychological traumatic event (Table 2).

               Twenty cases had primary NE (90%) while only 2 had secondary NE. The most common precipitating factors for bed-wetting were cold weather, presented in 27.3 % of cases, followed by drinking fluids in the evening in 22.7% of cases and psychological stressors in 13.7%.  Psychological reactions to enuresis were different among cases; 16 (72.7%) had social isolation, 13 (59%) fear of detection, 8 (36.3%) low self-esteem and only one had indifference (Table 3).

Five patients had chronic headache (22.7%), 3 (13.6%) had sleep talking, and 2 (9%) had somnambulism and nightmares. Nine cases (40.9%) had dark phobia which was not explained to be the cause of NE, one had agoraphobia and another one had animal phobia. 2 cases had significant neurotic traits in the form of thumb sucking and nail biting,  and 2 had behavioral disturbances during childhood (Table 4).

Age of menarche ranged between 11 and 17 years (13.36±1.64) which was significantly higher than controls (11.50±0.67). All have regular menstruation; the frequency of enuresis does not differ before and after menarche. Considering circumcision, sixteen (72.7%) cases had circumcision at an age ranged between 8 and 15, only one case had circumcision at 15years old. The onset of NE is not related to this event as most of cases had 1ry NE. 

Ten cases (45.4%) had family history of NE; none had family history of epilepsy.

All patients had normal neurological examination and lumbosacral plain X-ray. Urine analysis was normal in all cases except 2 had oxalate salts.

EEG was normal in 6 (27.2%) patients, showed non-significant changes in 7 (31.8%) cases and showed epileptiform changes in 9 (40.9%) cases.

IQ ranged between 78 and 128 (98.86±12.87), the IQ of three cases with history of developmental delay were 85, 98 and 100.

Soft Neurological Signs (SNS) score ranged between 2 and 7 (4.5±1.73) which was significantly higher than controls (table 5). IQ and SNS were negatively correlated (r= -0.36, p=0.09) not reaching statistical significance. They were not correlated with patient age, age at menarche, birth order or age of mother at time of delivery. In illiterate cases IQ was lower and SNS were higher however, the difference was insignificant. IQ was lower and SNS were significantly higher (p=0.024) among patients with EEG changes (Figure 1). The same was true among patients with headache but the difference was insignificant. Figure (2) shows that cases with high frequency of NE (≥ 3 times /week) had a statistically significant low mean IQ than cases with low frequency of NE (p= 0.01). Furthermore, a significant negative correlation was found between frequency of NE and IQ (R= -0.49, P=0.02) which means the higher frequency of NE is associated with lower IQ (Figure 3). However, no significant correlation was found between SNS and frequency of NE.


 

Table 1. Socio-demographic characteristics of the study patients.

 

Socio-demographic characteristics

Study group (n: 22)

Age

Range

Mean ±SD

12-22 years

15.81 ±2.57

Gender

Female

Male

22

0

Handedness

Right handed

Left handed

22(100%)

0

Education Level

Illiterate

Students in preparatory school

Students in secondary school

Students in faculty

Graduated

2 (9.1%)

10 (45.4%)

7 (31.8%)

1 (4.54%)

2 (9.1%)

 

Table 2. Abnormalities in the developmental history of the study patients.

 

 

n (%)

Post-partum complications

2(9.1%) (low birth weight)

Artificial-feeding

2(9.1%)

Developmental delay

3(13.6%)

Early psychological traumatic event

1(4.54%)

NE Nocturnal Enuresis

 

Table 3. Detailed Description of Nocturnal Enuresis (NE).

 

 

n (%)

Primary NE

Secondary NE

20(90.9%)

2(9.1%)

Precipitating factors:   

    Cold weather

    Drinking fluids in the evening

    Psychological stressors   

 

6(27.3 %)

5(22.7%)

3(13.7%)

Psychological reactions to enuresis;

     Social isolation

     Fear for detection

     Low self esteem

     Indifference

 

16(72.7%)

13(59%)

8(36.3%)

1(4.54%)

 

Table 4. Psychiatric and Neurological Co-morbidity.

 

 

n (%)

Chronic headache

5(22.7%)

Sleep talking

3(13.6%)

Somnambulism and night mares

2(9%)

Phobias:

  Dark phobia

 Animal phobia

  agoraphobia

 

9(40.9%)

1(4.54%)

1(4.54%)

Neurotic traits

2(9%)

Behavioral disturbance

2(9%)

Table 5. Comparison between patients and controls as regard  IQ and SNS.

 

 

Patients

Controls

P

IQ

98.86±12.87

103.27±10.33

0.217

SNS

4.5±1.73

0.63±.90

0.0001

IQ= Intelligence quotient, P value ≤ 0.05= significant, SNS= Soft Neurological Signs 

 

 

 

Figure 1. IQ and soft neurological signs (SNS) in relation to EEG changes.

 

 

 

Figure 2. Comparison between cases with low and high frequency nocturnal enuresis in the mean of IQ.

 

 

Figure 3. Correlation between frequency of nocturnal enuresis and IQ.

 

 


DISCUSSION

 

The present study included 22 female patients with NE. Their ages ranged between 12 and 22 years old.  Ninety percent(n=20) of patients had primary NE which approaches the results of Nappo and his colleagues17, who found that enuresis was primary in  74% and secondary in 26% of enuretic adolescent patients. Frequency of NE among our patients was severe, 70% had enuresis more than three nights per week, which is in agreement with Yeung7,18, who concluded that patients 16-40 years old with nocturnal enuresis are classified into 53% wetting more than three nights per week, and 26% wetting every night. Nappo and his colleagues17 also reported that the rate in 80% of adult enuretics was considered severe (≥ three nights/week).

Age of menarche in our cases ranged between 11 and 17 years (13.36±1.64) which was higher than controls (11.50 ±0.67).  It was noted that late sexual maturation has been associated with a higher prevalence of enuresis among adolescents.18-20 This finding may be part of an endocrinological maturational delay, which might play a part in the maturation of the CNS.

There is a clear genetic component to enuresis.  In our study, ten cases (45.4%) had family history of NE.  Other studies found 15% incidence of enuresis in children from non-enuretic families, 44% and 77% of children were enuretic when one or both parents, respectively, were themselves enuretic.20 A positive family history for enuresis was recorded in 82% of Nappo and his colleagues cases.17 It is believed that there are four responsible chromosomes; 13q13-13q14.2 (ENUR 1), 12q13 (ENUR 2), 8q and 22q11.21

Nine (40.9%) of our patients showed epileptiform changes in EEG. This is in agreement with Torso and colleagues22, who evaluated resting EEG changes in NE children. The frequency of EEG abnormalities was significantly higher in the enuresis group and in their dry siblings than in the control group. Additionally, as an indicator of cortical dysmaturity, an increased Hyperventilation (HV) response was observed more often in enuretic children and their dry siblings than in the control group, which confirm the genetic origin of nocturnal enuresis. Other EEG studies were performed during sleep, overnight EEG's were recorded on  subjects from 12–53 years of age found that Adult enuresis occurred during the synchronization phase of activated sleep (episodical appearance of alpha waves).23 Other sleep EEG studies proved an increased depth of sleep in enuretics.24 NE was classified according to changes in sleep EEG record into; (a) enuresis type I with cases showing a normal cystometrogram (CMG) with an awakening response on the EEG before enuresis, without awakening, (b) type IIa with cases showing a normal CMG without an awakening response on the EEG, and (c) enuresis type IIb with cases showing an abnormal CMG with no awakening response on the EEG.23,25 

Our cases had lower means of IQ which is in agreement with Joinson and colleagues26, who found NE to be associated with lower IQ scores. The decrease in intellectual capacities in NE patients may reflect maturational deficits of the CNS.

We reported significant negative correlation between IQ and SNS which is in agreement with Hertzig27 who found significant difference in mean full scale IQ between children and adolescents with positive SNS and those without.

A developmental delay in CNS control of bladder function might be a cause of NE.28 In our cases SNS were significantly present compared to controls, which is in agreement with other researches that found 30 to 40% of patients with NE have soft signs  of neurological dysfunction.29-31

A higher rate of SNS has been found in patients with NE who showed a slower motor performance than controls, particularly for repetitive hand and finger movements. The present study suggested a maturational deficit not only of the brainstem, but also of the motor cortex circuitry and related cortical areas.32

Feelings of embarrassment and anxiety; loss of self-esteem; and effects on interpersonal relationships, quality of life and school performance had been reported in NE patients.33 We found low self-esteem in our cases which is in agreement with other Studies.14,33,34 The present study found that high percent of the sample had significant pathological anxiety disorders especially dark phobia. Dark phobia is known to be one of the neurotic traits present in young children, which disappears with psychological maturity. Persistent dark phobia in enuretic females might be a psychological sign of maturational deficit in the CNS.

Psychopathology may be associated with NE. In PNE, psychological problems are usually the result and only rarely the cause. By contrast, with SNE, psychological problems are a possible cause. Secondary enuretics have experienced a stress, such as parental divorce, school trauma, or sexual abuse.19,20,34 However, we could not confirm this as our sample included only two cases with secondary NE.

Enuresis has been described in the psychiatric literature as a masturbatory equivalent, an expression of bisexuality, or the somatic expression of a defect in body image. It has also been reported to appear in previously dry children after sexual molestation. As circumcision is common in our culture, we proposed that circumcision might be perceived by females as a form of sexual abuse or humiliation. So, NE may be a regressive defense to the psychological trauma associated with that event. However, we could not find any relation between circumcision and the onset of NE or even the change of its frequency.

 

Conclusion

Adolescent and young adult females with NE have subtle neurological dysfunction, higher incidence of EEG changes, lower mean IQ and psychiatric abnormalities.  It is therefore important to identify the causes of nocturnal enuresis, risk factors, and associated neurological and psychiatric problems. With correct diagnosis of the problem, management strategies are likely to be highly effective. Further research for adolescent and young adult females with NE is highly recommended, including larger number of patients, with more detailed exploration of the neuro-psycho-endocrinal axis maturation and deficits. This might give more understanding of the possible mechanisms of NE and its management.  

 

[Disclosure: Authors report no conflict of interest]

 

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16.     Chen EY, Shapleske J, Luque R, McKenna PJ, Hodges JR, Calloway SP, et al. The Cambridge Neurological Inventory: A clinical instrument for assessment of soft neurological signs in psychiatric patients.  Psychiatry Res. 1995; 56:183-204.

17.     Nappo SR, Del Gado ML, Chiozza M, Biraghi P. Nocturnal enuresis in the adolescent: a neglected problem. BJU Int. 2002; 90(9):912-7.

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20.     Fritz G, Rockney R, Bernet W, Arnold V, Beitchman J, Benson RS, et al.  Practice parameter for the assessment and treatment of children and adolescents with enuresis.  J Am Acad Child Adolesc Psychiatry. 2004; 43(12):1540-50.

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24.     Hunsballe JM. Increased delta component in computerized sleep electroencephalographic analysis suggests abnormally deep sleep in primary monosymptomatic nocturnal enuresis. Scan J Urol Nephrol. 2000; 34:294-302.

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26.     Joinson C, Heron J, Butler R, Psycholb C, Gontard AV, Butler U, et al.  A United Kingdom Population-Based Study of Intellectual Capacities in Children with and Without Soiling, Daytime Wetting, and Bed-wetting. Pediatrics. 2007; 120:308-16

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الملخص العربي

 

المصاحبات العصبية والنفسية للتبول اللاإرادي في الفتيات المراهقات و البالغات

 

 

التبول اللاإرادي من المشكلات المعروفة بالعالم. و تعرف بأنها فقدان البول لاإراديا أثناء النوم. وتتواجد بكثرة في أطفال ما قبل المدرسة ويقل معدل انتشارها تدريجيا خلال مرحلة الطفولة والبلوغ. ويقسم التبول اللاإرادي الى نوعين: أولى و ثانوي. يعتبر التبول اللاإرادي في مرحلة المراهقة والبلوغ مشكلة مختلفة. قد تكون مقلقة للوالدين ومحبطة للمراهقات. وتعتبر عرض لمشكلات  أخرى عميقة.

كان الهدف من  هذه الدراسة البحث عن اضطرابات عصبية ونفسية دقيقة في هؤلاء المريضات.

اشتملت الدراسة اثنان وعشرين فتاه متوسط أعمارهن خمسة عشرة عاما مصابات بالتبول اللاإرادي, وعدد مماثل كعينة ضابطة من نفس المرحلة العمرية. تم أخذ تاريخ مرضى مفصل, فحص عصبي ونفسى, تحليل بول, أشعة عادية على الفقرات القطنية والعجزية, رسم مخ كهربي, قياس نسبة الذكاء وفحص العلامات العصبية الدقيقة للمجموعتين.

وجدنا تسعون بالمائة مصابات بتبول لاإرادي أولى و حوالى نصفهن لهن أقرباء يعانون من التبول اللاإرادي . نصف المريضات فقط سبق لهن اللجوء للمشورة الطبية.  ووجدنا تغيرات برسم المخ في تسع حالات. وكانت نسبة الذكاء أقل من العينة الضابطة. ووجدنا العلامات العصبية الدقيقة بنسبة ذات دلالة إحصائية و كانت تتناسب تناسبا عكسيا مع نسبة الذكاء. كما وجدنا تغيرات نفسية منها نقص الثقة بالذات و التي تحسنت بعد تلقى علاج للتبول اللاإرادي.

ونخلص من هذه الدراسة الى احتمال وجود خلل نموي بالجهاز العصبي المركزي في حالات التبول اللاإرادي.  و ربما هناك خلل نموي اشمل في المحور العصبي-النفسي- الغدي في هؤلاء المرضى. لذا نوصي بدراسات أوسع في هؤلاء المرضى من الجنسين لمحاولة معرفة الأسباب المختلفة وعلاجها  في مرضى التبول الليلي اللاإرادي.



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