The Prevalence of Bladder and Bowel Dysfunction in Children with Cerebral Palsy and its Association with Motor, Cognitive, and Autonomic Function

ABSTRACT

Purpose

To describe the prevalence of bladder and bowel dysfunction (BBD) in 8–10-year-old children with cerebral palsy and its association with motor, cognitive, and autonomic dysfunction.

Methods

A cross-sectional, random sample study of parents of 8–10-year-old children with cerebral palsy. Tools: The Enuresis/Urinary Incontinence Parental Questionnaire, the Functional Independence Measure children’s version, the autonomic signs questionnaire, and the Gross Motor Function Classification System.

Results

39 out of 59 parents consented to participate, whereas 25.64% reported complete continence. Of the 29 children with BBD, 21 (72.4%) had lower urinary tract symptoms and bowel problems. Only two of the children received conservative and noninvasive treatments. Lastly, motor, cognitive and autonomic impairments were associated with incontinence.

Conclusions

BBD is common in 8–10-year-old children with cerebral palsy at all levels of functioning. Most having both lower urinary tract symptoms and bowel problems.

KEYWORDS:

• Bladder dysfunction
• bowel dysfunction
• cerebral palsy
• prevalence

Introduction

Cerebral palsy (CP) is an umbrella term for a group of neurological disorders where the brain is damaged during its early stages of development. ¹ The incidence of CP is approximately 3.5 cases per 1000 births,² and is characterized according to anatomical distribution, the type of movement disorder, and functional limitation.¹ The motor impairments often combine with other impairments such as sensory, cognitive, and attention deficit disorders.^1,2

When looking at the CP population, there is a high incidence of bladder and bowel (BBD) dysfunction,³ with continence achieved later, compared to the general population.⁴ BBD includes daytime and nighttime enuresis, urinary urgency or frequency, encopresis (fecal soiling), chronic and functional constipation, and pain in the lower abdominal area and pelvis.⁵ In children with typical development, the incidence of daytime enuresis by 12 years old was between 2–19.2%.⁶ Additionally, nighttime enuresis was between 3–20% by ten years old.⁶ The incidence of constipation in children was 22.6%, and encopresis was 4.4%.⁵ In children with CP, the incidence of daytime enuresis ranges between 8.8–40.8% and nighttime enuresis between 6.5–25.5%.⁷ The incidence of fecal incontinence was 39.2–54%,^7,8 and constipation was 26–74%.⁹

Since most studies conducted in children with CP involve urinary incontinence,⁷ the primary objective of this study was to present the prevalence of BBD in children with CP.

Previous studies suggest several possible reasons for BBD in children, such as poor coordination and activity of the pelvic floor muscles during urination/defecation, neurogenic detrusor overactivity, problems with perceiving the visceral sensations from the bladder and the rectum, and cognitive and psychological elements.¹⁰ In children with CP, additional factors affecting BBD and age at toilet training have been identified, such as cognitive ability, motor function level, and impairment of the autonomic system.^7,8,11–13

The association between cognitive ability and sphincter control has been examined in several studies.^7,8,12 The median age for reaching daytime and nighttime continence among children with CP with age-appropriate cognitive levels is five years old, while only a third of children with severe cognitive difficulties will achieve complete continence by the time they are 17 years old.⁸ According to the Gross Motor Function Classification System (GMFCS), an association was found between motor function level and the age at which continence was achieved.^7,8,12,13 Children with motor function level I-II presented a median continence age under five years. In children with bilateral cerebral palsy, approximately 30% of children with a low motor function level (IV) achieved continence around the age of 14, and a combination of cognitive and motor impairment is associated with a high prevalence of BBD.^10”

In a literature review, Samijn et al. (2017)¹¹ indicated that abnormal bladder responses are common in children with CP during filling, and the pelvic floor muscles are hyperactive during voiding. These symptoms stem from delayed or incomplete development of the bladder and hyper-tonus of the pelvic floor muscles. Neurogenic detrusor overactivity (NDO) is found among 59% of children with CP.¹¹ This condition leads to a small bladder capacity relative to the age norm and involuntary bladder contractions resulting in urinary incontinence. Children with spasticity tend to present overactivity of the pelvic floor muscles. The lack of coordination between the contraction of the bladder and the relaxation of the pelvic floor muscles can lead to recurrent infections, urinary incontinence, and renal reflux.

BBD significantly affects the quality of life of a child and their family.¹⁴ In the general population, pelvic floor physiotherapy with urotherapy is an accepted method of achieving continence. Combined treatment of pelvic floor physiotherapy and standard treatment consisting of dietary advice, education for toileting behavior, and medication resolved constipation in 92.3% of the children, with only 63% being resolved with standard treatment alone.¹⁵

Pelvic floor physiotherapy is a noninvasive conservative treatment that includes training of proprioception, contraction and/or relaxation and/or correct use of the pelvic floor during urination and stool evacuation, passive treatments (massages, motility, different types of taping, and electricity), and exercising the pelvic floor muscles. Urotherapy relates to behavioral therapy, encouraging an active lifestyle, dietary changes, explanations and demonstrations of how various systems work.^10,16 Since treatment requires parents’ full cooperation, parents provide explanations and instructions. As such, parental questionnaires are a tool to help parents understand the scope of the problem and the various factors that may contribute to it.

Objectives

The study’s primary objective is to describe the prevalence of BBD in 8–10-year-old children with CP and examine at what age continence is reached. The choice of 8–10-year-old children is based on the findings of Singh et al.‘s study (2006)¹² that children with CP who were not toilet trained by the age of eight had lower odds of being toilet trained later. The third objective was to examine the association between BBD and characteristics associated with continence in this group of children. The last objective of this study was to examine the incidence of children with CP who were treated with pelvic floor physiotherapy and urotherapy to achieve sphincter control.

Research Methods

Study Type

A cross-sectional study using a retrospective data collection.

Participants

Parents of children with CP at all function levels according to the standard GMFCS I-V index. The patients were from the ALYN Pediatric and Adolescent Rehabilitation Hospital in Jerusalem, aged 8–10 years and lived at home. Hebrew and/or English-speaking parents. The hospital and the University’s ethics committees approved the study protocol.

Based on hospital records, 146 children and parents met these criteria. Figure 1 presents the selection process of the participants for the study.

Figure 1. Flow chart of the participants.

Tools

Background Questionnaire -The parents were asked to complete a simple questionnaire about the age at which their child was toilet trained and whether their child had been previously treated for BBD. The details of the treatment were asked of the children who had received previous treatments. Questions such as what treatment was given, when the treatment was given, and how long the treatment lasted.

Autonomic system function questionnaire in children with CP – questions relating to cold limbs, pain, sleep disorders, and constipation.¹⁷ The English version underwent a language and content validation processor for the Hebrew and Arabic -speaking population.¹⁸

Daily functional independence - Functional Independence Measure for Children (WeeFIM) – included questions about the degree of independence in motor and cognitive functions.¹⁹ The WeeFIM presents high construct validity (Spearman correlation coefficient of (-0.74) with the Manual Ability Classification System (MACS), and (-0.85) with the GMFCS. A high inter-rater agreement was found when WeeFIM was administered by direct observation and by interviewing a parent (intraclass correlation = 0.93).²⁰

BBD – the Enuresis/Urinary Incontinence Parental Questionnaire (PQ-EnU) - a questionnaire with 72 questions about daytime enuresis, nighttime enuresis, constipation, encopresis, toilet habits, and behavioral disorders.²¹ The PQ-EnU presents a high correlation with the International Children’s Continence Society and the ROME-III/ROME-IV guidelines and good to high Internal consistencies (Cronbach’s alpha>0.7).²¹ According to Loening-Baucke (2007), the following questions have content validity for BBD in children; “Does your child wet their clothes during the day?,” “Does your child wet the bed (the diaper) at night?,” “Does your child feel a sudden urge to go to the toilet?,” “How many times a day does your child empty their bladder (on average)?,” “Does your child generally suffer from constipation?,” “Does your child soil their underpants during the day?” Does your child soil their underpants at night?”

Before using the PQ-EnU questionnaire, the English version underwent a language and content validation processor for the Hebrew-speaking population (with the approval of the questionnaire’s author - Appendix). Ten participants answered the questionnaire twice – one to three weeks apart to examine reporting reliability. The questions that were identified by Loening-Baucke (2007)⁵ for BBD and found to be highly reliable include: “Does your child wet their clothes during the day?,” “Does your child wet the bed (the diaper) at night?” and “Does your child generally suffer from constipation?.” The answers were converted into a “number of BBD signs” (Bladder and bowel dysfunction index) (0–3).

Motor function - GMFCS²² - a tool to classify gross motor function in CP. The tool consists of five levels; at level one, the child’s mobility functions are without limitations/assistance; at level five, there is a severe limitation that requires transportation in a manual wheelchair. The interrater agreement was found to be high k = 0.84, p < .0001, and its association with other gross motor tests was>0.7.²³

Procedure

The contact details for the parents were obtained through the clinic records of the hospital. Clinic records were selected randomly from a list of 146 names. The first author Moriah Baram M.Sc, a physiotherapist specializing in pelvic floor training and urotherapy with ten years’ seniority, contacted the parents by telephone. The first author is not part of the hospital’s staff and has no previous acquaintance with the children or their parents. If the parents agreed, they were asked to give informed consent and respond to the questionnaires on the phone in the fixed order of- A few general questions, the autonomic signs questionnaire, and the WeeFIM. If BBD was indicated, the parents were asked to answer the PQ-EnU. The GMFCS classification was taken from the hospital file.

Statistical Analysis

The incidence of BBD was presented using descriptive statistics. Differences in the various motor, autonomic, and cognitive functions between children with continence vs. BBD, are shown by a Mann-Whitney U test. The associations between the BBD index and motor, autonomic, and cognitive characteristics are presented using the Spearman’s rank correlation and partial correlation coefficient. Data analysis was performed with the SPSS software version 25. A p-value<.05 was considered significant.

Results

Table 1 shows that about 70% of participants exhibited spastic tone, and 64.1% of the children had at least one autonomic sign. The most common signs were cold limbs and constipation (around 40%). While around 94% of all children experienced constipation and 40–50% sleep disorders and pain were treated, no children were treated for the cold limb sign.

Table 1. “Participants” demographic and impairments characteristics.

	N=39
Age (years) 8 9 10	4(10.3) 20(51.3) 15(38.5)
Gender male female	20(51.3) 19(48.7)
Classification Spastic diplegia hemiplegia quadriplegia Dyskinetic Ataxic Mixed	27 (69.2) 10 (25.6) 6 (15.4) 11 (28.2) 2 (5.4) 0 (0) 6 (15.4)
GMFCS I II III IV V	4(10.3) 5(12.8) 4(10.3) 8(20.5) 5(12.8)
WeeFIM ranking on items Dressing- lower extremities Transfer to toilet Communication- comprehension Communication- verbal Cognition- interaction Cognition- problem solving Cognition- memory	1[1–7] 2[1–7] 7[1–7] 7[1–7] 5[1–7] 5[1–7] 7[1–7]
Autonomic signs Cold extremities pain Sleeping disorders constipation	16(41.0) 11(28.2) 12(30.8) 17(43.6)
No. of autonomic signs per child 0 1 2 3 4	14(35.9) 7(17.9) 8(20.5) 7(17.9) 3(7.7)

Values are presented as number (percentage), median [min- max].

Twenty-one of the parents reported their child needed full assistance with dressing their lower body and 22 parents reported their child needed full assistance with stairs. In contrast, 25 parents stated that their child had full and independent memory capability (Table 1).

When investigating the age of toilet training, 20 parents reported a specific age for their child being toilet trained (Table 2); around half of the parents mentioned situations in which the child was not toilet trained. Seven out of 29 children with existing BBD (24%) were given treatment. Two were treated with pelvic floor physiotherapy and urotherapy. Daytime enuresis was the most common problem, while nighttime enuresis and daytime encopresis were the second most prevalent. Around half of the children (18/39) presented more than one sign of BBD.

Table 2. Bladder and Bowel dysfunction characteristics.

Answer to the question“The age in which your child was toilet trained … ”
Reported on being toilet trained	20(51.3)
Reported age at toilet training (in years)	3.5 [2–10]
Reported toilet training without reservation*	10(25.6)
Reported age at toilet training without accidents (in years)	4 [2–10]
Yes to “Has your child been treated for Baldder and Bowel Dysfunction?	7(17.9)
If so, what was the treatment Pediatric pelvic floor physiotherapy and urotherapy Incontinence clinic Urology Emotional Medication	2 2 1 1 1
Treatment for constipation taken from “Autonomic signs” questionaire Enema Polyethylene Glycol Magnesium Dietary changes Physical activity Combination treatment of the above	4 13 1 2 1 4
PQ-EnU- number of BBD signs	N=39
Daytime wetting Nighttime wetting Constipation Daytime soiling Nighttime soiling Urgency Frequency	24(61.5) 19(48.7) 13(33.3) 19(48.7) 7(17.9) 14(35.0) 4(11.4)
Baldder and bowel dysfunction Index (0–3) 0 1 2 3	10(25.6) 10(25.6) 11(28.2) 8(20.5)

*laughter/fatigue/physical stress.

Values are presented as number (percentage), median [min- max].

Ten parents reported continence, and 21 parents reported overall BBD. Seven parents reported urinary incontinence alone, and only one reported fecal incontinence alone. Children who were continent showed greater motor, cognitive and autonomic function than children with BBD (Table 3)

Table 3. Motor, cognitive and autonomic function by continence.

	Overall continence			Urinary continence			Fecal continence
The measure	Yes N = 10	No N = 29	p-value	Yes 11=N	No 28=N	p-value	yes 13=N	no 26=N	p-value
GMFCS	2.2[1–4]	4.0[1–5]	<0.01	2.2[1–4]	4.0[1–5]	<0.01	3.1[1–5]	4.2[3–5]	0.06
Dressing- lower extremities	4.4[1–7]	2.2[1–7]	0.04	4.6[1–7]	2.1[1–7]	<0.01	3.4[1–7]	1.6[1–7]	0.01
Transfer to toilet (1–7)	5.5[1–7]	2.9[1–7]	0.01	5.6[1–7]	2.8[1–7]	0.01	4.2[1–7]	2.3[1–7]	0.03
Cognition sum (5–35)	33.3[26–35]	20.3[5–35]	<0.01	33.2[26–35]	20.4[5–35]	0.01	28.4[5–35]	15.2[5–33]	<0.01
No. of autonomic signs (0–4)	0.4[0–2]	1.8[0–4]	<0.01	0.6[0–3]	1.8[0–4]	0.18	0.8[0–3]	2.7[1–4]	<0.01

Values are presented as median [min- max], p-value-Mann Whitney.

. For example, the median functional independence in transferring on/off the toilet in a continent child is 5.5 (sit down and stand up independently and safely but require supervision/cues/guidance/organization), while in a child with BBD the median score is 2.9 (perform less than half of the action, need at least one person’s assistance).

Moderately strong and inverse associations were found between FIM scores of dressing lower body and cognition and BBD index (r_s=-0.73, p < .01,r_s=-0.72, p < .01 accordingly). Additionally, a strong positive relationship was found between the number of autonomic signs and BBD index (rs = 0.74, p < .01), (Table 4). When nullifying the relationships between the motor function, cognitive ability, and autonomic function characteristics, it was found that the cognition characteristic explains a significant part of the association between the other characteristics (GMFCS classification, dressing lower body, transferring on/off the toilet, and the number of autonomic signs) and BBD index. It can also be seen that the GMFCS index explains the association between function, dressing, toilet transfers, and the number of BBD signs.

Table 4. Spearman’s rank correlation coefficients and partial coefficients between motor function, cognitive ability, and autonomic function characteristics, and BBD index.

		Partial correlation coefficients (discounting the character in the head of the column)
	Correlation	GMFCS	Dressing- lower extremities (WeeFIM)	Cognition (WeeFIM)	Number of autonomic signs
GMFCS	0.68**		0.39	0.36	0.62*
Dressing- lower extremities (WeeFIM)	-0.72**	-0.24		-0.41	-0.58*
(WeeFIM)Transfer to toilet	-0.60**	-0.05	0.59	-0.37	-0.56*
(WeeFIM)Cognition	-0.73**	-0.65**	-0.71**
Number of autonomic signs	0.74**	0.58*	0.60*	0.24

Values are presented spearman’s rank *p-value<.05, **p-value<.01.

Discussion

The findings of this study present a high incidence of BBD among children with CP. Previous studies showed that the incidence of daytime enuresis ranged between 8.8–40.8% and nighttime enuresis between 6.5–25.5%.⁶ This study found higher incidences, with: 61.5% of the subjects suffering from daytime enuresis and 48.7% from nighttime enuresis. This difference may stem from the fact that no exception was made for any functional level, model, or pattern of CP. Instead, we included all the children at the appropriate age who were at the list of outpatients clinic in the hospital where the study was conducted.

This study’s participants are children who were followed at a clinic for children with CP at the ALYN Pediatric and Adolescent Rehabilitation Hospital, which may not accurately represent children with CP, but rather a sub-group with more severe damage characteristics, whom the multi-team clinic aids at the hospital. The distribution of the GMFCS classification reinforces this hypothesis: 57% of the participants had an IV-V level, compared to the typical proportion reported in literature of 30–35% of all people with CP.²⁰ In light of the finding that there is an association between GMFCS level and continence, the bias in this study may be for a higher incidence than that found in this population of children. Since this study used various tools to ask questions about BBD, the findings may represent a more accurate reality explaining the higher incidence found. For example, 25% of the sample had urinary incontinence even though in a direct question to the parent, “Is your child toilet trained?,” the answer was “Yes, my child is toilet trained.”

When the parents were asked a question about toilet training or BBD, most parents referred only to urinary incontinence, as the parents do not associate constipation with BBD. Therefore, when asked about the treatment of BBD, no parent mentioned constipation. This may be since a different specialist treats each sphincter with urinary incontinence being treated by urologists⁶ and bowel problems by gastroenterologists.²¹ However, a direct question about constipation is clear to parents. If asked in several different ways, the parents respond consistently.

According to previous studies, bowel problems are high where 39.2–54% of children with CP suffer from encopresis and 26–74% from constipation.^6,8,11,20 In this study, the incidence of encopresis was 48.7%, and the incidence of constipation was 33.3%. This study found that all the children with diagnosed constipation were treated with different methods (medication, supplements, diet, and more). The study participants may represent a treated population; therefore, the incidence of constipation is closer to the lower values as present in the literature on this topic.^7–9,24,25

Despite the high incidence of BBD, only a quarter of the children were being treated, and only two were with pelvic floor physiotherapy and urotherapy. An additional two were treated at the sphincter clinic, despite the accessibility of these treatments at the hospital where the study was conducted. The treatment of physical components positively affects continence in children with CP. For example, passive treatments such as manipulation of connective tissues and Kinesio taping were found to affect the number of weekly bowel movements, consistency of the feces, sense of exertion as experienced by the child, and quality of life indices.²⁶ Movement and mobility, even when using a passive walker for children with severe CP, exhibited an effect on bowel activity.²⁷

Studies have found that the child’s cognitive ability is associated with achieving continence.^7,8,12 Indeed, cognition was found to be the most significant of the various indices examined in this study. Therefore, children with sufficient ability to comprehend active and behavioral treatment approaches must be identified to achieve some sphincter control. However, children with limited cognition can be helped by using various passive methods to improve their BBD.

Motor function is associated with achieving continence in general and in particular, which is compatible with the literature.^7,8,12,13 However, in this study, when disregarding the effect of autonomic signs and cognitive function, the association of motor function in achieving continence was not found to be significant. The tone component was not found to be associated with achieving continence.

The autonomic impairment component was associated with BBD but did not exhibit statistical significance when disregarding the cognition component. However, this study’s incidence of autonomic signs is high; cold limbs were reported in 41% of the children. Since the cause of this phenomenon is unclear, not examined in previous studies on continence, and is not treated in continuation, its origin should be examined in-depth.

Limitations

The study may be biased due to shame and unease in discussing the topic (Landgraf et al., 2004).²⁸ Another bias is associated with the term “toilet training,” which may create a diminishment bias for its true extent. In this study, and without further investigation, a diminished report of 25% of the children in the sample was exhibited.

In addition, at ages 8–10, most children spend a lot of time in educational settings outside the home. Parents are not always aware of their child’s symptoms associated with BBD leading to under-reporting.

Additionally, the PQ-EnU questionnaire was found stable in less than half of the questions. Therefore, its reliability and validity in the population of children with CP are questionable. The questions that were found to be unreliable were those that pertain to encopresis (four out of six), urinary frequency, and the duration of time the child was dry. Possibly with encopresis there is a reporting bias due to unwillingness or shame.

In addition, the sample size of the current study is small for a prevalence study. Moreover, possible selection bias associated with the fact that 35% of the parents that were approached did not respond or did not agree to participate in the study.

Summary and Recommendations

The incidence of BBD in children with CP, even after age-expected toilet training, is high. Despite the high incidence, most parents reported that their children do not receive physiotherapy-related or urotherapy treatment but are usually treated with medication mostly to treat constipation. The children in the study were under follow-up at a hospital clinic where medical professionals specialize in treating BBD.

When investigating why only two children received neither medication nor accessories as a treatment for their BBD, it was hypothesized that the parents and children did not voluntarily expose the problem to professionals.^28,29 Several parents who participated in this study asked if there was another treatment other than medication. On top of urotherapy interventions, various studies have presented physical treatment components like manual treatment,³⁰ daily therapeutic walking,²⁷ or manipulation of all connective tissues and Kinesiotaping with obvious benefits.²² These have all led to improvement in constipation problems in this population of children.

When investigating if there is an element of parental fatigue due to the prolonged treatment of the child’s various difficulties, numerous parents indicated that they were prepared to spend a lot of time in physical treatment with their child in order to solve the constipation problem. This study found that most of the children who were treated for the problem were in treatment within the past year. Since the study participants were children aged 8–10, parents and children seem to seek a solution to the continence issue long after the “normative” toilet training age.

BBD is a sensitive topic that most of the affected population find difficult to discuss.²⁸ However, it is important to educate healthcare professionals to ask the right questions and to explain various treatment methods to patients, as it is essential for the treatment of BBD to become an integral part of the treatment of these children.

A reliable and valid tool must be developed to identify children with BBD. A tool that will enable dialogue and present the full picture of the size and complexity of the problem. The topic must be discussed in clinics, among family doctors, physiotherapists, as well as among parents. The issue should be broached in a simple manner to assess the severity of the problem and present a solution for each child according to their needs and abilities.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

The author(s) reported there is no funding associated with the work featured in this article.

Appendix

Dear Mrs. Baram,

thank you for your email and your patience. The first German version of the Parental Questionnaire: Enuresis/urinary incontinence was indeed developed by Prof. Beetz and Prof Alexander von Gontard. The English translation of the questionnaire was done by Prof. von Gontard and you can find it in the IACAPAP textbook (http://iacapap.org/wp-content/uploads/C.4-ENURESIS-072012.pdf), see Appendix C.4.3).

This was also the basic questionnaire, of which we conducted the validation study.

I talked to Prof. von Gontard, who permits the translation of the questionnaire, which is sufficient for your work. Could you please send us the Hebrew version of the questionnaire when you have translated it?

If you have further questions, please contact me anytime.

Kind regards,

Justine Hussong