What Is Known
- Co-occurrence of bladder and bowel problems is often reported, but the actual extent of the problem is unknown.
- The bladder and bowel share a common pathway, which might be the explanation of the frequent co-occurrence.
What Is New
- The reported prevalence of bladder symptoms in children with functional constipation varied greatly across studies.
- Urinary incontinence is the most studied bladder symptom in children with functional constipation.
- Children with functional constipation seem to be more likely to have bladder symptoms than children without functional constipation.
- There is a lot of clinical heterogeneity between studies in the definitions of bladder symptoms and functional constipation.
Functional constipation (FC) is common among children (1). Co-occurrence with bladder symptoms, such as lower urinary tract symptoms (LUTS) and urinary tract infection (UTI), is often reported (2–5). The international Children's Continence Society (ICCS) has introduced the term bladder and bowel dysfunction (BBD) to emphasize the frequent combination of bladder and bowel problems (6). Clinical experts have reported the prevalence of bladder symptoms as approximately 30% in children with FC (4,7), though figures range from 12% to 46% (8–11). Bladder and bowel problems, especially in combination, can lead to reduced psychosocial well-being and may have negative impact on bladder and renal function (12–15). Focusing on 1 condition may lead to inadequate diagnostic and therapeutic interventions.
The explanation of the frequent co-occurrence of bowel and bladder dysfunction is that they share a common pathway. The underlying pathophysiology of this common pathway is not completely understood, but 2 main pathways are assumed. First, there may be a mechanical problem, with the proximity of the bladder and bowel meaning that large volumes of feces in the rectum could place direct pressure on the posterior bladder wall, which in turn, may cause bladder emptying and storage problems (3,16). Second, there may be a neurogenic problem. The genitourinary tract and gastrointestinal system share the same embryologic origin in the hindgut. Given that normal functioning of the pelvic organ systems requires cross-sensitization between neural pathways, dysfunction of 1 of the 2 organ systems could lead to dysfunction of the other (17,18).
Little is known about the actual extent of bladder symptoms in children with FC. In this study, we therefore aimed to conduct a systematic review of studies on the prevalence of bladder symptoms in children with FC. The secondary aim was to compare this prevalence among children with and without FC.
A systematic literature search was conducted of the MEDLINE, EMBASE, PsycINFO, and Cochrane library electronic databases (from January 1990 to July 17, 2018), using Medical Subject Headings, Emtree terms, and free text words related to child, FC, and bladder symptoms (LUTS and UTI) (Supplemental Digital Content 1, http://links.lww.com/MPG/B480). In addition, experts were consulted, and a clinical librarian assisted in the literature search. No language restrictions were applied. The protocol of the systematic review has been published in the International Prospective Register of Systematic Reviews (number PROSPERO 2016:CRD42016045742).
The population of interest was children aged 4 to 17 years with FC, and we used the definitions of conditions applied by the authors of each article. Studies of children with underlying organic or metabolic causes of constipation, or with psychological or behavioral problems known to be related to either FC or LUTS or UTI, were excluded. The conditions of interest were bladder symptoms and UTI. Studies that reported on the prevalence of bladder symptoms or UTI in children with FC, or that provided enough information to allow us to calculate this prevalence, were eligible for inclusion. All clinical settings (contexts) were included (ie, community, primary care, and specialist care populations.
Two reviewers (J.V.S. and S.V.O.) independently screened the titles and abstracts of all identified articles, before assessing the full text of identified articles for potential inclusion. Disagreement was resolved through discussion with a third reviewer (J.D.). Also, the reference lists of selected full-text articles and review articles were hand-searched by the 2 authors.
The quality of the included studies was assessed using a critical appraisal checklist for prevalence studies (Supplemental Digital Content 2, http://links.lww.com/MPG/B481) (19). This instrument contained 9 items addressing the following: sample adequacy; sample frame bias; sample size adequacy (5% precision); appropriateness of study subjects and setting description; missing at random data; consistency of bladder symptoms descriptions with the ICCS terminology document (validity); assessment bias; prevalence with confidence intervals (CIs); and whether the response rate with refusals was described (20). We assessed each item as having risk of bias, no risk of bias, or unclear risk of bias. Quality assessment focused only on the study elements relevant to estimate the prevalence and was done by 2 reviewers independently (J.V.S. and G.H.), with any disagreement resolved through discussion with a third reviewer (M.B.).
Data extraction was performed independently by 2 researchers (J.V.S. and S.V.O.), using a structured data extraction form, with disagreement resolved through discussion with a third reviewer (J.D.). The following data were extracted: general study information, population characteristics (eg, number of participants with FC, age, gender, definition, and method of data collection for FC, and if specified, the number of control children without FC), condition characteristics (eg, definitions and method of data collection for bladder symptoms and UTI), and context characteristics (eg, setting, and recruitment of patients).
Data Synthesis and Analysis
Point or period prevalence rates were defined as the proportions of children with bladder symptoms and/or UTI in a population of children with (or without) FC at a specific point in time or within a defined period, respectively. The prevalence and corresponding 95% CIs were presented in a forest plot. If at least 4 suitable studies were available for analysis, we intended to perform a meta-analysis in homogeneous populations of children based on population characteristics (ie, definition of FC), condition characteristics (ie, definition of bladder symptoms or UTI), and setting. Forest plots were produced for prevalence using the “metaprop cinmethod(exact)” command in STATA/SE version 14 (Stata Corp, College station, TX) (21).
To evaluate the association between bladder symptoms and FC, we selected studies reporting the prevalence of bladder symptoms and UTI in children with and without FC. Relative risks (RRs) and corresponding 95% CIs were calculated with 2 × 2 tables and presented in a forest plot. Statistical significance was accepted when the 95% CI did not include 1. Forest plots of RRs were produced using Review Manager 5.3 (The Nordic Cochrane Center, Copenhagen, Denmark).
A flowchart of the screening and selection process of the studies is shown in Figure 1. We included 23 studies, among which 22 reported the prevalence of at least 1 bladder symptom (8–11,22–39) and 7 reported the prevalence of UTIs (8,11,28,32,34,35,40).
We evaluated the methodological quality of the studies as their ability to find valid and unbiased estimates of the prevalence of bladder symptoms and UTI. The quality of the selected studies was rated as poor to moderate (Table 1). Sample adequacy was addressed for bladder symptoms in 18 of 22 studies (8–11,23–27,30,33–39) and for UTI in 1 of 7 studies (8). In 15 of 23 studies (8–10,22–24,26,29,31,33,36–40), a random or consecutive sample of participants was recruited, and in 11 of 23 studies the response rate with refusals was adequate (>70%) or appeared to be unrelated to the outcome (9,22,24,25,27,29–31,36,40).
Description of Selected Study Populations
The characteristics of the included studies are summarized in Supplemental Digital Content 3 (http://links.lww.com/MPG/B482). The definition of FC was reported according to the Rome III criteria for FC in 5 studies (10,11,28,36,40), to another described definition in 12 studies (9,22–24,27,30,32–35,37,39), and to no described definition in six 6 studies (8,25,26,29,31,37). A validated or a modified version of the dysfunctional voiding symptom score (DVSS) was used in three studies (10,22,32). Urinary incontinence (UI) was measured in 20 studies: in 6 the frequency of urine leakage was at least once a week (8–10,27,29,36); in 4 the frequency of urine leakage was at least once a month (24–26,38); and in 10, the frequency of urine leakage was not reported (11,28,30–35,37,39). Finally, UTI was diagnosed by urinalysis and culture in 6 studies (8,11,32,34,35,40), and in 1 study, the authors did not describe how they diagnosed UTI (28). Ten studies were conducted in a community population (10,22–27,36–38), 1 in a primary care population (9), and 12 in specialist care (8,11,28–35,39,40).
The significant differences in populations (FC definition), conditions (definition of bladder symptoms), and settings meant that a meta-analysis of the reported prevalence and RRs would be inappropriate and meaningless (19).
Prevalence of Bladder Symptoms in Children With Functional Constipation
Four studies on UI reported the period prevalence (9,29,31,39), and all other studies reported point prevalence (Fig. 2). The prevalence of LUTS (based on the DVSS) was reported in 3 studies as 37% (95% CI 36%–38%) (22), 39% (95% CI 27%–52%) (10), and 64% (95% CI, 52%–74%) (32).
The prevalence for UI not otherwise defined ranged between 18% and 46% (9,25,27,29,31,33,36,41), for daytime UI between 3% and 29% (9,11,24,26,28,30,41), and for nighttime UI between 13% and 47% (Fig. 2a) (9–11,28,30,32,34,35,37–39,41). The prevalence of other bladder storage symptoms was as follows: overactive bladder, 19% (95%CI 11–31%) (23); decreased frequency of micturition, 20% (95% CI 12%–29%) (10); increased frequency of micturition, 13% (95% CI 7%–20%) (11); urgency, 25% (95% CI 17%–35%) in 1 study (10) and 27% (95% CI 12%–48%) in another (35); and urge UI, 19% (95% CI 7%–39%) (35). For bladder voiding symptoms, the prevalence was as follows: dysuria, 10% (95% CI 5%–18%) (10) and 17% (95% CI 10%–25%) (11); and straining, 2% (95% CI 0%–8%) (10). For other bladder symptoms, the prevalence of dribbling was 4% (95% CI 1%–6%) (11) and the prevalence of holding maneuvers was 49% (95% CI 39%–60%) (10).
Prevalence of Urinary Tract Infections in Children With Functional Constipation
No studies reported a period prevalence or incidence of UTI. The prevalence of UTI in children with FC was only measured once at enrollment in all studies, and ranged between 6% and 53% (Fig. 2B) (8,11,28,32,34,35,40).
Relative Risk for Bladder Symptoms and Urinary Tract Infection in Children With and Without Functional Constipation
In 12 of 23 studies, bladder symptoms were also observed in children without FC (Fig. 3A) (9,10,23–27,32,35–38). Children without FC were recruited in the same community (10 studies), in 1 study the control group consisted of children consulting the pediatrician with other than gastrointestinal or urological symptoms, and in 1 study the control group consisted of volunteers without gastrointestinal diseases in history. The RRs for LUTS were 4.54 (95% CI 3.08–6.71) (10) and 6.35 (95% CI 4.32–6.71) (32), and the results were statistically significant.
For UI not otherwise defined the RRs were between 2.61 and 6.03 (4 studies, 95% CI 1.70–9.66), and all RRs were statistically significant (9,25,27,36). The RRs for daytime UI were between 2.17 and 6.52 (3 studies, 95% CI 0.73–10.00) (9,24,26), but only 2 RRs were statistically significant (24,26). The RRs for nighttime UI were between 1.24 and 3.82 (4 studies, 95% CI 0.64–12.97) (9,10,35,38), but again, only 2 RRs were statistically significant (9,38). In a fifth study, we identified an unexplainable but very high RR of nighttime UI (38.58; 95% CI 28.67–51.90) (37). We decided to report this study as an outlier, and therefore, it was not included in the reporting on nighttime UI (Fig. 3A).
The RRs for bladder storage symptoms were as follows: overactive bladder, 1.46 (95% CI 0.76–2.79) (23); decreased micturition, 3.85 (95% CI 2.29–6.45) (10); and urgency, 6.73 (95% CI 0.89–50.84) (35) and 1.57 (95% CI 1.06–2.32) (10). The RRs for bladder voiding symptoms were 4.87 (95% CI 2.20–10.81) for dysuria (10) and 2.71 (95% CI 0.55–13.21) (10) for straining. For holding maneuvers the RR was 2.05 (95% CI 1.61–2.62) (10).
The prevalence of UTI was only reported for children without FC in 2 of the 7 studies covering UTI (Fig. 3B). The RRs were 2.18 (95% CI 0.97–4.89) (35) and 6.55 (95% CI 0.86–50.02) (34) for these studies, but neither was statistically significant.
To the best of our knowledge, this is the first systematic review of studies reporting the prevalence of bladder symptoms in children with FC. The prevalence of LUTS was 37% to 64% in 3 studies of children with FC, though the prevalence of single bladder symptoms ranged from 2% to 47% in the 22 studies. Among these, UI was the most evaluated bladder symptom (21 studies), with a reported prevalence of 3% to 47%. Clinical heterogeneity in the definitions of bladder symptoms and FC between studies meant that we could not statistically pool the prevalence.
Among the included studies, bladder symptoms occurred more frequently in children with FC than in children without FC, though the RR had wide ranges. The RRs for both studies of LUTS were statistically significant at 4.54 and 6.35, but the RRs for single bladder symptoms ranged from 1.24 to 6.73 among 18 studies, of which 6 were not significant. Therefore, our results indicate that children with FC are more likely to have bladder symptoms than children without FC, which supports the assumption of a common pathway for FC and LUTS (2–5). One study showed a very high RR (38.58; 95% CI 28.67–51.90) of nighttime UI in children with FC compared to children without FC (37). Characteristics like age, definition of FC and context cannot explain this outlier. One study not included in this systematic review investigated the co-occurrence of bladder symptoms and FC in consultations. In this Australian study, pediatricians have recorded all clinical problems for 4181 consultations in 2013. In 212 (5%) of the consultations FC was reported and among 52 (24.5%) of these consultations nighttime UI was reported (42).
By contrast, although 7 studies reported that prevalence of UTI in children with FC was 6% to 53%, only two small studies compared the prevalence of UTI between children with and without FC. This was insufficient to do any meaningful analysis on the association between FC and UTI.
Methodological Issues With the Prevalence Studies
For an accurate evaluation of prevalence, two methodological questions need to be answered: “1) How representative are the patients recruited in the included studies for the target population?” and “2) Are the outcome measures valid and reliable?’ ’(43), In our review, the target population was defined as children aged 4 to 17 years who had FC, and the outcome measures were bladder symptoms and UTI.
In 4 of the 22 studies measuring bladder symptoms the patients did not represented the target population exactly. These studies either included only boys (31), or excluded children belonging to our target population (ie, excluding children with earlier treatment for BBD) (22,28,29,31). In addition, not all studies included a random or consecutive sample of patients, or examined selective inclusion due to non-response. Therefore, care should be taken when extrapolating the prevalence of bladder symptoms, which certainly cannot be averaged.
The methods used to measure bladder symptoms and UTI varied between studies, thereby possibly affecting the prevalence. In 2006 (updated in 2016) the ICCS agreed criteria for diagnosing bladder symptoms (6,44). According to the ICCS, UI is defined as involuntary urine leakage on a regular basis in a child aged 5 years and older. The studies in this review used different frequencies of urine leakage (from at least weekly to at least monthly). Thus, studies that included involuntary urine leakage at least once per month might have overestimated the prevalence of UI in comparison with studies that included involuntary urine leakage as once a week.
No studies measured the period prevalence of UTI. Given that UTI can be recurrent, though mostly limited in time, the true prevalence will probably be underestimated when using point prevalence. In addition, 6 out of 7 studies measuring UTI included children under the age of 4 years and all studies were performed in specialist care. It is unknown whether the reported prevalence rates of UTI can be extrapolated to children aged 4 to 18 years with FC.
Finally, only 6 studies had sufficiently large sample sizes to calculate prevalence estimates with a 5% precision. Thus, the prevalence estimates of these studies lacked precision (45,46).
Strengths and Limitations
We applied a broad search strategy and also included studies in which the main aim was not to evaluate the prevalence of bladder symptoms in children with FC. An additional 2 studies were found via reference lists. Therefore, we are confident that we did not miss relevant studies. The prevalence of FC in children with bladder symptoms felt outside the scope of this study. When selecting eligible studies, we did not apply any restrictions to the definition of FC, instead aiming to include a representative sample of children with FC. An obvious drawback of this approach is that the heterogeneity of results increases. Only 5 studies used the advocated Rome criteria to define FC (10,11,28,36,40). Clinicians and researchers (especially in older studies) often use less well-defined criteria for diagnosis. In five studies FC was defined as encopresis or fecal incontinence (25,26,29,31,39). The definitions of FC and bladder symptoms were more in line with each other if they were performed in the same clinical setting. This makes a comparison between different clinical settings even more complicated. Due to the limited number of studies conducted in clinically homogeneous populations, according to setting, definition of FC and definition of bladder symptoms, we could not give pooled prevalence rates or pooled RRs.
FC appears to increase the risk of bladder symptoms in children aged 4 to 17 years. Despite expert reports that the prevalence of LUTS is approximately 30% in children with FC (4,7), our review indicates that this might underestimate the true prevalence. Indeed, we found that the prevalence of LUTS was 37% to 64%. The early diagnosis and treatment of bladder problems in children with FC is considered essential to preventing adverse effects on kidney function, bladder function, and psychosocial well-being (12,13). The propensity for clinicians to underdiagnose BBD was also highlighted in a study in which parents reported more concomitant bladder and bowel problems than clinicians did, regardless of the healthcare setting (47). Therefore, we recommend that clinicians be aware of concomitant bladder problems in children presenting with FC.
Constipation management is the first step of treatment in children with BBD, as relief of bowel dysfunction has been shown to reduce the frequency of UI (8,48). During evaluation of treatment, disappearance of both constipation symptoms and bladder symptoms have to be monitored. Children with FC and bladder symptoms can be treated in primary care or by a general pediatrician. Consider referral to a specialist when no or only partial response of adequate constipation management is achieved after 6 months (12).
Recommendations for Further Research
More research is needed in less clinically heterogeneous populations to clarify the true prevalence of bladder symptoms and UTI in children with FC. Future studies should use consistent diagnostic frameworks to further reduce heterogeneity and facilitate future meta-analysis. In addition, it would be interesting to investigate if the prevalence of bladder symptoms is influenced by the type of FC: functional fecal retention and slow-transit constipation or by behavioral or psychological comorbidity (49,50).
Secondly, future research should seek to unravel the association between FC and either bladder symptoms or UTI by age and the severity and duration of FC symptoms. Lastly, the common pathway theory suggests that we need to adopt a simultaneous approach to the treatment of bladder and bowel problems (3,7,16). Future research must investigate how interventions directed at both conditions affect prognosis (3,7,16).
Given the findings of this study, we cannot make any definitive statements on the prevalence of bladder symptoms in children with FC. This is hampered by the wide variation in prevalence, despite bladder symptoms clearly occurring with significant frequency in children with FC. Indeed, our review indicates that children with FC are more likely to have bladder symptoms than are children without FC. Until more robust data can be presented, it is important for clinicians to be alert for concomitant bladder symptoms in children consulting with FC. Early diagnosis and treatment are straightforward and can have marked beneficial effects on prognosis and psychosocial well-being.
The authors thank Sjoukje van der Werf (medical information specialist, central medical library, University Medical Center Groningen) for assisting with the literature search. The authors also thank Dr Robert Sykes (www.doctored.org.uk) for providing editorial services.
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