Keywords
bladder and bowel dysfunction - constipation - lower-urinary-tract symptoms - pediatric urology - pediatric nephrology - prevalence
Palabras clave
disfunción de la vejiga y del intestino - estreñimiento - síntomas del tracto urinario inferior - urología pediátrica - nefrología pediátrica - prevalencia
Introduction
The International Children's Continence Society (ICCS) defines bladder and bowel dysfunction (BBD) as the presence of functional alterations in these organs in children older than 5 years of age.[1]
[2] It occurs due to the anatomical contiguity and the shared irrigation and innervation of the bladder and the bowel: dysfunction in one organ affects the function of the other.[3]
[4] The symptoms include urinary incontinence, enuresis, nocturia and increased or decreased urinary frequency, constipation and encopresis.[3]
[5]
The presence of lower-urinary-tract symptoms (LUTSs) is a frequent reason for consultation in the pediatric urology and nephrology clinic, representing up to 40% of the cases.[4] Worldwide, the prevalence of urinary incontinence is between 6.3% and 9% at the age of 7 years, decreasing to between 1.2% and 3% in teenagers.[4] Likewise, constipation in the pediatric population has a prevalence of ∼ 0.3% to 8%[4] and of ∼ 4.2% to 32% when associated to voiding dysfunction.[6]
[7]
[8] However, these data are variable and inconclusive. The complications include vesicoureteral reflux, urinary-tract infections (UTIs), abdominal pain, and emotional and behavioral disorders.[4]
[5]
[9]
The diagnosis of BBD is based on the clinical history focused on habits and voiding and bowel technique, as well as the documentation of the voiding diary and, in some cases, the measurement of the postvoid residual (PVR) volume, uroflowmetry with electromyography, and videourodynamic study.[6]
[10]
[11] The physical examination should be aimed at ruling out pathologies such as obstruction of the lower urinary tract or neurological disorders.[10]
[11] The treatment is based on the management of intestinal symptoms, improving the LUTSs.[10]
[11]
The aim of the present study is to estimate the prevalence of BBD in the outpatient clinic of pediatric urology and nephrology.
Methods
A prospective cohort composed of 334 patients aged between 5 and 18 years who attended the outpatient clinic of pediatric urology and nephrology was prospectively evaluated between April 4th, 2018 and April 3rd, 2019. The sample included all kids that attended the outpatient clinic during this period. The study protocol was approved by the Institutional Ethics Committee at Hospital Universitario Fundación Santa Fe de Bogotá, Bogotá, DC, Colombia, under the tenets of the Declaration of Helsinki. Before the consultation, an informed consent form was signed by the parents or legal guardians of the kids. Kids older than 7 years of age were asked for assessment.
All patients were evaluated for medical history, including gender, age, height and weight, history of prematurity, history of neurological, psychological, urological and nephrological disorders, history of UTI admission, and history of enuresis in the parents. A total of 86 patients with past history of myelomeningocele, spina bifida, refractory epilepsy, lysosomal storage diseases, Down syndrome, nephrectomy, urothelial carcinoma, hypospadias, vesicoureteral reflux and acute and chronic kidney injury were excluded.
During the consultation, the caregivers and the patients filled the version of the Pediatric Lower Urinary Tract Symptom Score (PLUTSS) translated into Spanish and validated by Somoza-Argibay et al,[12] and the Bristol Stool Scale to assess the patients with constipation.
The PLUTSS questionnaire contains 15 questions that evaluate enuresis and incontinence, the subjective quantity of urine lost during the day and night, the LUTSs (storage and voiding), the habits to hold urination, the daily deposition, and the quality of life (QoL). A score higher than 8 was considered significant for LUTSs.
If needed, the patients were ruled out for UTIs with urinalysis and urine culture, and had their PVR volume evaluated by abdominal ultrasound, the uroflowmetry by electromyography, and a urodynamic study was also performed. The diagnosis of BBD was made after significant LUTSs measured by PLUTSS, history of UTI or PVR volume higher than 10% of the total bladder capacity, and constipation were observed.
The database was recorded using the Microsoft Excel for Mac (Microsoft Excel for MacOS, 2016, Microsoft Corp., Redmond, WA, US). The statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS for MacOS, IBM Corp., Armonk, NY, US) software, version 25.0. The first analysis included all patients (n = 334) for evaluation of the medical history and exclusion criteria. The qualitative data were evaluated as frequencies, and the quantitative data were tested for normality using the Kolmogorov-Smirnoff test. If the data had normal distribution, they were reported as mean ± standard deviation; otherwise, they were reported as median (interquartile range, IQR).
Out of de 334 patients surveyed, 86 did not meet the inclusion criteria. The remaining 248 patients were included in the second analysis. The data were described and then stratified by type of consultation (pediatric urology versus pediatric nephrology), and by diagnosis of BBD. All of the qualitative variables were compared using the Chi-squared test. The parametric quantitative data were compared using the Student t-test for independent samples, and the Mann-Whitney U test for the non-parametric variables.
Univariate and multivariate analyses were performed to determine the risk factors for BBD. The variables included relevant medical history (gender, history of prematurity, neurological and psychological disorders, urinary tract malformation, hydronephrosis and enuresis in the parents) and every question of the PLUTSS questionnaire. In the analyses, p-values < 0.05 were considered significant.
Results
The median age of the patients who attended the outpatient clinic was 9 years-old (IQR: 6–13), and median body surface area was 0.103 m2 (IQR: 0.085–0.143). In total, the sample was composed of 174 (52.1%) male patients and 160 (47.9%) female patients. Regarding the medical history, prematurity was found in 174 (52.1%) patients, neurologic disorders, in 28 (8.4%), psychological disorders, in 13 (5.9%), previous abdominal surgery, in 39 (11.7%), intestinal disorders, in 3 (0.9%), UTIs, in 103 (30.8%), hydronephrosis, in 20 (6%), anatomical malformation, in 22 (6.6%), and kidney transplantation, in 7 (2.1%) patients. A total of 86 (25.7%) patients were excluded. The overall data can be found in [Table 1].
Table 1
Characteristics of the patients who attended the clinic
|
Variable
|
n = 334
|
|
Age (years) ⇞
|
9 (6–13)
|
|
Gender ⌽
|
|
|
Female
|
160 (47.9)
|
|
Male
|
174 (52.1)
|
|
Body surface area (m2) ⇞
|
0.103 (0.085–0.143)
|
|
Weeks of gestation at birth ⇞
|
39 (36–40)
|
|
History of prematurity ⌽
|
62 (29.5)
|
|
Neurological disorders ⌽
|
|
|
Myelomeningocele
|
7 (2.1)
|
|
Hypotonia
|
1 (0.3)
|
|
Down syndrome
|
1 (0.3)
|
|
Arteriovenous malformation
|
1 (0.3)
|
|
Spina bifida
|
2 (0.6)
|
|
Epilepsy
|
10 (3)
|
|
Neurofibromatosis
|
3 (0.9)
|
|
Brain tumor
|
1 (0.3)
|
|
Lysosomal storage disease
|
1 (0.3)
|
|
Asperger syndrome
|
1 (0.3)
|
|
Psychological disorders ⌽
|
|
|
Attention deficit hyperactivity disorder
|
6 (1.8)
|
|
Traumatic event in the past
|
3 (0.9)
|
|
Anxiety and obsessive-compulsive disorder
|
2 (0.6)
|
|
History of urinary-tract infection ⌽
|
103 (30.8)
|
|
One episode
|
46 (14.7)
|
|
Two or more episodes
|
34 (10.7)
|
|
History of hydronephrosis ⌽
|
20 (6)
|
|
History of urinary malformation ⌽
|
22 (6.6)
|
|
History of vesicoureteral reflux ⌽
|
34 (10.2)
|
|
Enuresis in the parents ⌽
|
|
|
Father
|
1 (0.3)
|
|
Mother
|
2 (0.6)
|
|
Excluded patients ⌽
|
86 (25.7)
|
Notes: ⌽ Reported as n (%). ⇞ Reported as median (interquartile range).
When compared by type of consultation (pediatric urology versus pediatric nephrology), there were more males in the urology group (90.6% versus 44%;. p < 0.001). The week of gestation at birth was higher for the nephrology group (36.5 [IQR: 35–39] versus 40 [IQR: 36–40]; p = 0.005); however, there were no differences regarding the history of prematurity. Moreover, the history of psychological disorders (12.5 versus 0%; p < 0.001), abdominal surgery (17.2 versus 3.3; p = 0.001) and enuresis in the kid's parents (3.1 versus 0.5%; p = 0.047) were higher in the urology group, while the history of UTIs was lower (14.1 versus 32.6%; p = 0.004).
During the consultation, more patients in the nephrology group needed abdominal ultrasound (18.8 versus 44.6%; p < 0.001); however, less patients had a significant PVR volume (18.8 versus 6.5%; p = 0.004). As for the PLUTSS questionnaire, the diagnosis of constipation or fecal incontinence, and the diagnosis of BBD, there were no differences between the groups. The overall prevalence of BBD was of 27.8%. The prevalence in the pediatric urology clinic was of 26.6%, and in the pediatric nephrology clinic it was of 28.3%. All data stratified by type of consultation are in [Table 2].
Table 2
Evaluation of the included patients stratified by type of consultation
|
Pediatric urology
|
Pediatric nephrology
|
p-value
|
|
Variables
|
n = 64
|
n = 184
|
|
Relevant medical history
|
|
|
|
|
Age (years) ⇞
|
9 (6–14)
|
9 (6.75–13)
|
0.988
|
|
Gender ⌽
|
|
|
< 0.001
|
|
Female
|
6 (9.4)
|
103 (56)
|
|
|
Male
|
58 (90.6)
|
81 (44)
|
|
|
Body surface area (m2) ⇞
|
0.107 (0.083–0.149)
|
0.102 (0.086–0.142)
|
0.803
|
|
Weeks of gestation at birth ⇞
|
36.5 (35–39)
|
40 (36–40)
|
0.005
|
|
History of prematurity ⌽
|
16 (37.2)
|
32 (26.4)
|
0.183
|
|
Neurological disorders ⌽
|
6 (9.4)
|
7 (3.8)
|
0.192
|
|
Psychological disorders ⌽
|
8 (12.5)
|
0 (0)
|
< 0.001
|
|
History of UTI ⌽
|
9 (14.1)
|
60 (32.6)
|
0.004
|
|
One episode
|
4 (6.3)
|
30 (17.5)
|
0.245
|
|
Two or more episodes
|
5 (7.8)
|
17 (9.3)
|
|
History of hydronephrosis ⌽
|
5 (7.8)
|
11 (6)
|
0.288
|
|
History of urinary malformation ⌽
|
0 (0)
|
15 (8.2)
|
0.593
|
|
Enuresis in the parents ⌽
|
2 (3.1)
|
1 (0.5)
|
0.047
|
|
Evaluation of BBD
|
|
|
|
|
PLUTSS score ⇞
|
1 (0–5.75)
|
0 (0–4.75)
|
0.234
|
|
Incontinence ⌽
|
12 (18.7)
|
32 (17.4)
|
0.875
|
|
Enuresis ⌽
|
11 (17.2)
|
23 (12.5)
|
0.695
|
|
Frequency ⌽
|
7 (11.9)
|
21 (11.4)
|
0.700
|
|
Voiding symptoms ⌽
|
20 (7.8)
|
40 (5.43)
|
0.128
|
|
Urgency ⌽
|
12 (9.38)
|
39 (10.59)
|
0.640
|
|
Hold urination ⌽
|
14 (21.9)
|
35 (19)
|
0.621
|
|
Daily deposition ⌽
|
47 (73.4)
|
141 (76.6)
|
0.607
|
|
Affected quality of life ⌽
|
6 (9.4)
|
15 (8.1)
|
0.437
|
|
Diagnosis of significant LUTS ⌽
|
10 (15.6)
|
31 (16.8)
|
0.821
|
|
Bristol Stool Scale ⌽
|
|
|
0.014
|
|
1
|
1 (2.1)
|
22 (19.3)
|
|
|
2
|
7 (14.6)
|
24 (21.1)
|
|
|
3
|
15 (31.3)
|
25 (21.9)
|
|
|
4
|
25 (52.1)
|
43 (37.7)
|
|
|
Diagnosis of constipation ⌽
|
18 (28.1)
|
61 (33.2)
|
0.457
|
|
Encopresis ⌽
|
2 (3.1)
|
8 (4.3)
|
0.668
|
|
Additional laboratories or imaging studies
|
|
|
|
|
Infectious urinalysis ⌽
|
2 (11.8)
|
12 (9.3)
|
0.746
|
|
Positive urine culture ⌽
|
3 (33.3)
|
12 (27.9)
|
0.134
|
|
PVR volume (mL) ⇞
|
9.5 (2–14.75)
|
8.5 (0.975–8.5)
|
0.920
|
|
Significant PVR ⌽
|
12 (18.8)
|
12 (6.5)
|
0.004
|
|
Diagnosis of BBD
|
|
|
|
|
Global prevalence ⌽
|
69 (27.8)
|
|
Stratified prevalence ⌽
|
17 (26.6)
|
52 (28.3)
|
0.794
|
Abbreviations: BBD, bladder and bowel dysfunction; LUTS, lower-urinary-tract symptoms; PLUTSS, Pediatric Lower Urinary Tract Symptom Score; PVR, postvoid residual; UTI, urinary-tract infection.
Notes: ⌽ Reported as n (%). ⇞ Reported as median (interquartile range).
The children with diagnosis of BBD were younger (7 years [IQR: 5–8] versus 11 years [IQR: 7–14]; p < 0.001). Additionally, BBD was more frequent in females (37.6 versus 20.1%; p = 0.002) ([Table 3]). There were no differences between the groups regarding past medical history.
Table 3
Characteristics of the patients stratified by diagnosis of bladder and bowel dysfunction
|
Variable
|
Patient with bladder and bowel dysfunction
|
Healthy patient
|
p-value
|
|
n = 69
|
n = 179
|
|
Age (years) ⇞
|
11 (7–14)
|
7 (5–8)
|
< 0.001
|
|
Gender ⌽
|
|
|
0.002
|
|
Female
|
41 (59.4)
|
68 (38)
|
|
|
Male
|
28 (40.6)
|
111 (62)
|
|
|
Body surface area (m2) ⇞
|
0.120 (0.089–0.153)
|
0.092 (0.075–0.102)
|
< 0.001
|
|
Weeks of gestation at birth ⇞
|
39.5 (36–40)
|
38 (35.75–40)
|
0.182
|
|
History of prematurity ⌽
|
16 (34.8)
|
32 (27.1)
|
0.333
|
|
Neurological disorders ⌽
|
4 (5.8)
|
9 (5)
|
0.636
|
|
Psychological disorders ⌽
|
6 (8.7)
|
4 (2.2)
|
0.100
|
|
History of hydronephrosis ⌽
|
4 (5.8)
|
12 (6.7)
|
0.746
|
|
History of urinary malformation ⌽
|
13 (7.3)
|
2 (2.9)
|
0.939
|
|
Enuresis in parents ⌽
|
1 (1.4)
|
2 (1.2)
|
0.645
|
Notes: ⌽ Reported as n (%). ⇞ Reported as median (interquartile range).
In the univariate analysis, we found that being female (odds ratio [OR]: 2.47 [95% confidence interval (95%CI: 1.389–4.4)]; p = 0.002) and having psychological disorders (OR: 4.637 [95%CI: 1.224–17.558]; p = 0.024) like trauma, obsessive-compulsive disorder (OCD), anxiety and attention deficit hyperactivity disorder (ADHD) were a risk factors for BBD.
Moreover, the analysis of the questionnaire showed as risk factors incontinence (question 2; OR: 3.059 [95%CI: 1.067–8.776]; p = 0.038), enuresis (question 3; OR: 8.532 [95%CI: 2.7–26.96]; p < 0.001), intermittent flow (question 8; OR: 9.211 [2.011–42.196]; p = 0.004), frequency (question 9; OR: 6.73 [95%CI: 1.788–25.33]; p = 0.005) and constipation (question 13; OR: 34.46 [95%CI: 13.393–88.666]; p < 0.001). The summary of the regression analysis of the risk factors for BBD is in [Table 4].
Table 4
Regression analysis of the various risk factors for bladder and bowel dysfunction
|
Variable
|
Univariate analysis*
|
|
Multivariate analysis**
|
|
|
OR (95% CI
|
p-value
|
Adjusted OR (95%CI)
|
p-value
|
|
Baseline characteristics
|
|
|
|
|
|
Gender (female)
|
2.39 (1.355–4.216)
|
0.002
|
2.472 (1.389–4.4)
|
0.002
|
|
History of prematurity
|
1.433 (0.691–2.974)
|
0.333
|
1
|
N/A
|
|
Neurological disorders
|
1.162 (0.349–3.906)
|
0.808
|
1
|
N/A
|
|
Psychological disorders
|
4.167 (1.138–15.251)
|
0.020
|
4.637 (1.224–17.558)
|
0.024
|
|
History of hydronephrosis
|
0.856 (0.267–2.752)
|
0.794
|
1
|
N/A
|
|
History of urinary malformation
|
0.381 (0.084–1.735)
|
0.196
|
1
|
N/A
|
|
Enuresis in the parents
|
1.301 (0.116–14.588)
|
0.830
|
1
|
N/A
|
|
Questionnaire
|
|
|
|
|
|
Incontinence
|
9.066 (4.395–18.701)
|
< 0.001
|
1
|
N/A
|
|
Quantitative incontinence
|
10.09 (4.737–21.489)
|
< 0.001
|
3.059 (1.067–8.776)
|
0.038
|
|
Enuresis
|
5.587 (2.606–11.977)
|
< 0.001
|
8.532 (2.7–26.96)
|
< 0.001
|
|
Quantitative enuresis
|
5.587 (2.606–11.977)
|
< 0.001
|
1
|
N/A
|
|
Polaquiuria
|
3 (1.346–6.685)
|
0.005
|
1
|
N/A
|
|
Straining
|
4.94 (1.398–17.452)
|
0.007
|
1
|
N/A
|
|
Voiding pain
|
3.418 (0.89–13.127)
|
0.059
|
1
|
N/A
|
|
Intermittent flow
|
6.6 (2.201–19.79)
|
< 0.001
|
9.211 (2.011–42.196)
|
0.004
|
|
Frequency
|
10.176 (3.837–26.987)
|
< 0.001
|
6.73 (1.788–25.33)
|
0.005
|
|
Urgency
|
7.178 (3.057–16.852)
|
< 0.001
|
1
|
N/A
|
|
Holding
|
6.478 (3.305–12.695)
|
< 0.001
|
1
|
N/A
|
|
Wetting
|
5.938 (2.388–14.765)
|
< 0.001
|
1
|
N/A
|
|
Constipation
|
20.5 (9.933–42.307)
|
< 0.001
|
34.46 (13.393–88.666)
|
< 0.001
|
Abbreviations:95%CI, 95% confidence interval; N/A, not available; OR, odds ratio.
Notes: *Chi-squared test. **Logistic regression.
Discussion
The true incidence of BBD is unknown,[13] and the prevalence is inconclusive due to the lack of studies on the subject. Burgers et al[14] studied BBD in a cohort of 113 patients who attended the pediatric urology clinic due to LUTSs, and they found a prevalence of 47%. Vaz et al,[15] in a population of 739 schoolchildren, found a prevalence of symptoms of lower-urinary-tract dysfunction in 21.8% of the cases, and of constipation in 30.7%. In the present study, the prevalence of BBD in the pediatric urology consultation was of 26.6%; in the pediatric nephrology consultation, it was of 28.3%; and the overall prevalence was of 27.8%. These differences can be attributed to the different inclusion criteria of each study. We included all patients who attended the clinic, and only excluded kids with pathologies that could explain the LUTSs, the history of UTI, or the constipation.
In the present study, there were more male patients; however, the prevalence of BBD was higher in the female population (41 (59.4%) cases versus 28 (40.6%) cases; p = 0.002). Moreover, being of the female gender increased the risk of developing BBD, with a ratio of 2.5:1 in relation to the male gender. In the study by Vaz et al,[15] the authors found an association of lower-urinary-tract dysfunction and the female gender, with an OR: of 3.7 (95%CI: 2.5–5.7; p < 0.001). It is hypothesized that in women there are inappropriate activities of the pelvic floor muscles and/or the urethral sphincter during voiding, causing functional bladder outlet obstruction (BOO).[16]
The relevant medical history showed no differences between the populations with or without BBD; however, when the categories were stratified by the presence or not of the corresponding disorder, the psychological history increased the chance of developing BBD, with a ratio of 4.6:1 patient. The psychological diagnosis included trauma, OCD, anxiety and ADHD. Yang et al[17] evaluated 130 patients in the pediatric urology clinic and stratified the results by ADHD diagnosis. They stated that kids with ADHD presented more soaked underwear and urgency.[17] Additionally, Arlen et al[18] presented 25 patients with phantom urinary incontinence and concomitant LUTSs and constipation, and 70% of the kids had a diagnosis of OCD. And in a comparison of 38 kids with LUTSs versus 38 kids without LUTSs, Zhao et al[19] found an anxiety level score higher in the group with LUTSs (3.68 versus 0.97; p < 0.001).
On the other hand, the PLUTSS questionnaire showed a significant association between LUTSs and BBD when the score was higher than 8 points.[12] When evaluating the association of each question with the diagnosis of BBD, the risk was 3.06 times higher for incontinence, 8.53 times higher for enuresis, 9.21 times higher for intermittent flow, 6.73 times higher for frequency, and 34.46 times higher for constipation. We believe that reducing the PLUTSS questionnaire to only these five questions would speed up the consultation without resulting in the underdiagnosis of the patients with LUTSs.
Once the patient is diagnosed with BBD and other diagnosis are ruled out, it is important to focus the treatment in the urinary and bowel symptomatology at the same time. The constipation should be assessed and managed with a high amount of fluids and increased ingestion of dietary fiber, as well as stool softeners[20] concomitant with behavioral recommendations for micturition. Polyethylene glycol (PEG) is the most commonly used stool softener, and it should be administer to all patients with LUTSs.[20] In cases of recurrent UTIs, the antibacterial prophylaxis can be prescribed,[21]
[22] specifically for the patients with vesicoureteral reflux and changes in the renal cortex.[23] The misconception regarding antibiotic prophylaxis might increase bacterial resistance. Toska and Geitona[24] evaluated 301 doctors and nurses about the prescription of antibiotics in the pediatric population, and found irrational prescribing in 56% of the cases due to uncertainty regarding the diagnosis. Thus, the right diagnosis and evaluation, as well as the management with dietary and behavioral changes, are important to avoid the prescription of prophylactic or therapeutic antibiotics due to the complications of an undermanaged BBD.
Pediatric patients are up to 10 times more sensible to radiation than adults.[25] This vulnerability leads physicians to try to reduce the number of imaging procedures performed on them. In case the patient with BBD is resistant to therapy or a functional or anatomical dysfunction is suspected, the images must be taken according to the as low as reasonably achievable (ALARA) protocol.[25]
[26] In our cohort, 50% of the patients needed imaging evaluations, and they were first submitted to ultrasonography. Only 9.7% of the kids presented positive findings for high PVR volume, but we did not find patients with urological malformations.
The Center for Child Incontinence at the Aarhus University Hospital, in Denmark, has a multidisciplinary team (pediatric nephrology, urology, urotherapy, psychology, sleep disorders, genetics and constipation) that treats children with nocturnal enuresis, overactive bladder and BBD.[27] In a study[27] with 400 patients, they concluded that most of them could be treated in primary care, and that the specialized clinics should assess therapy-resistant patients and kids with underlying pathologies. The creation of an specialized clinic on BBD in our hospital would help us improve and speed up the diagnosis of BBD and the beginning of the non-antibacterial non-pharmacological management of the patients. Moreover, a multidisciplinary team involving pediatric gastroenterology, urotherapy and nursing under a protocol of recurrent UTIs or therapy-resistant BBD management might prioritize patients, reducing complications and the rate of admissions to the inpatient care facility, as well as the need for imaging or invasive procedures and antibacterial therapy, thus reducing the costs to the healthcare system.
The limitations of the present study include the missing data regarding the PVR volume, the urinalysis and the urine culture in some patients. However, we believe that assessing the prevalence in the pediatric urology and nephrology clinic would help physicians to prevent complications, hospitalizations, the management with antibiotics and invasive or imaging procedures.
Conclusion
The prevalence of BBD is of 27.8% in our outpatient clinic. Adequate evaluation, diagnosis and management are important to prevent the associated complications and the exposure to multiple antibiotic treatments and invasive and imaging procedures. With the creation of a standardized transdisciplinary BBD clinic, physicians would assess the patients easily and better, thus decreasing the costs to the healthcare system.
