Introduction

Bladder and bowel dysfunction (BBD) is highly prevalent worldwide and is thought to result from the interplay of multiple factors that vary regionally. The coexistence of voiding dysfunction symptoms and functional constipation and/or faecal incontinence (FI) in children was previously termed ‘dysfunctional elimination syndrome’ (DES)1,2,3. However, there was no standardized definition of DES for children until 2013 when the International Children’s Continence Society (ICCS) suggested the term ‘bladder and bowel dysfunction’ instead of DES as a descriptive comprehensive term of a combined bladder and bowel disturbance that does not explain pathogenesis but rather encompasses this parallel dysfunction. Lower urinary tract(LUT) dysfunctions common to BBD include storage symptomps like urinary frequency, urgency, incontinence, nocturia, as well as voiding symptomps like hesitancy, dysuria and other issues like over active bladder and underactive bladder, meanwhile, defecation complaints accompanied by the LUT dysfunctions are like constipation, functional non-retentive faecal incontinence(FNRFI) and/or encopresis2,3. BBD can predispose children to urinary tract infection (UTI), urinary incontinence and other complications such as vesicoureteral reflux (VUR)4. Not only is it therefore a difficult and distressing problem for children and their families but can impose a sense of guilt and embarrassment amongst them with some children ending up as victims of bullying1,5.

In some children with neuropathic diseases, such as congenital spina bifida, neural tube defects and congenital megacolon, a clear common neurological basis is identifiable. A functional interaction between the bladder and bowel has been postulated, due to their close anatomical proximity, and both share innervation of the parasympathetic S2-S4 and sympathetic L1–L3 nerve roots2. However, no neurological basis for the combined dysfunction of the two organs has been obviously recognized.

Elimination communication (EC) is also known as ‘natural infant hygiene’ and sometimes referred to as ‘baby-led potty training’ or ‘assisted infant toilet training’. Elimination refers to the act of defecation or urination. Elimination communication is a two-way process in toilet training. When the child shows cues of elimination, such as crying, squirming, straining, wriggling, grimacing, fussing and vocalizing, the caregiver can coordinate this elimination process with audio cues (soft whistle or hum) whilst holding or sitting the child with thighs apart over the toilet to complete this process rather than to allow them to eliminate in their DDs5.

The timing of toilet training may vary somewhat between countries and cultures. It has been suggested that children less than two years old are not considered ready for toilet training because of immature bladder and bowel control as well as a lack in physical skills to go to a toilet and remove their own clothes by themselves. The American Academy of Pediatrics (AAP) had suggested that children should use DDs until they are considered ready for toilet training6. However, whether DDs should be used before and until the maturation of voiding and defecation skills remains debatable. Furthermore, whether early active defecation guidance and discontinued DD usage combined with commencement of EC and potty training can effectively decrease the occurrence of BBD in children remains to be answered.

Traditionally, in China, many families may just use a cloth or split-crotch pants (Fig. 1) instead of DD or after weaning off DDs. They also practice “Baniao” (a Chinese term) which describes lifting of the child in a semi-squatting position with their thighs apart over the toilet or potty (Fig. 2). Some of the intrinsic connection may should be discussed in more detail, particularly the internal relationship between DD use and delayed EC or delayed toilet training, as well as the relationship between BBD prevalence and EC start and end times. DD use cessation was the period of cessation of diaper use at the discretion of the caregiver proactively, from assisted infant toilet training gradually to the start of toilet training independently. Bladder control was considered achieved when the child is aware of the need to void, able to express the need with verbal and/or non-verbal communication, managed to stay dry and have no urinary retention7.

Figure 1
figure 1

With split-crotch pants, it is more convenient for parents to wean off diapers in a timely manner and to allow the children to control their own urination and defecation. (Photo taken and provided by the first author and the colleagues).

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Figure 2
figure 2

Caregivers can coordinate EC with holding out and separating the thighs (‘Baniao’ in Chinese). (Photo drawn and provided by the first author and the colleagues).

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Although the physiological mechanisms of BBD have been previously examined in a number of studies, no definite conclusions have been drawn. It has also been reported that excessive dependence on DDs and subsequent delayed EC may be associated with BBD symptoms, such as voiding frequency and/or urgency, an unstable bladder, incontinence and other defecation problems8. It is therefore worth exploring, whether voiding and defecation problems in young children may be related to prolonged usage of DD and delayed EC, particularly before the age of 2 years. Epidemiological surveys of BBD prevalence and its risk factors can help elucidate the pathogenesis.

This study used a questionnaire to investigate the voiding and defecation conditions of 11,285 children in different regions of mainland China. The purpose of this study was to determine the relationship between the prevalence of BBD, delayed EC and DD usage.

Methods

General information and methods

From March 2018 to June 2019, an epidemiological survey was performed in 12 cities with high population densities located throughout mainland China: Shenzhen (south), **amen (southeast), Zhengzhou (central), **'an (west) and Harbin (north). Nineteen kindergartens and 18 primary schools in total were selected by means of systematic sampling; classes were randomly chosen according to the children’s age distributions in the kindergartens/primary schools.

The investigation was approved by the Research Ethics Committee of the First Affiliated Hospital of Zhengzhou University and informed consent forms were obtained from all patients or legal guardian for participation in this study, including agreement of publication of identifying information or images in an online open-access publication without name,gender,age and other personal private information. Before the survey, medical staff engaged in questionnaire collection and guidance to fill in the questionnaires were trained to avoid the respondents’ misunderstanding and uncertain recall of the time of EC and DD use. As derived from parents or caregivers filling in the validated BBD questionnaire, the number of children surveyed per school was more than 200. The cross-sectional paper survey consisted of a self-administered anonymous questionnaire completed by the parents and/or caregivers. If some parents were unsure about some questions, taking the questionnaires home to complete them and returning them within one week was allowed. The procedure for filling out the questionnaires and the BBD diagnostic criteria were in accordance with the ICCS guidelines3.

The main contents of the questionnaire included the following: ① General information: sex, age, date of birth, height, weight, details of primary caregivers (including parents, grandparents and babysitters); ② DD usage (whether DDs were used; age when DD use was stopped; whether DDs were used during the day, at night, or all day; and adverse reactions); ③ the start time of EC and the onset of toilet independence; ④ the current voiding and defecation behaviours; ⑤ start time of urination training/bowel training, time of urination/defecation independence. The information and contents of the questionnaires were kept confidential and only known by medical staff participating in this study.

Inclusion, exclusion and diagnostic criteria

The inclusion criteria were as follows: children aged 4 to 10 years old with normal urinary anatomy and those who had not experienced surgery for the urinary system, pelvic organs, or nervous system. BBD was defined according to the 2013 ICCS guidelines, which describe a combination of functional bladder and bowel disturbances. Accordingly, any cases who meet this definition and conform with the information collected by questionnaires will be classified as BBD group. The specific types of voiding and defecation abnormalities associated with BBD were diagnosed according to the International Classification of Diseases 10th Revision (ICD-10) and Diagnostic and Statistical Manual of Mental Disorders 5 (DSM-V), and the functional defecation disorder part of BBD spectrum was based on the Rome III criteria2,3. In the kindergartens and primary schools we surveyed, all children have a routine physical examination once or twice a year, including routine urine, abdominal and urinary ultrasonography, so according to the results of a prior medical examination, the exclusion criteria were as follows: children who have organic diseases, taking medication for, or had surgery of the urinary, gastrointestinal and/or nervous system. Children with current UTIs were also excluded from the study because concurrent symptoms such as urgency, voiding frequency and urge incontinence may be related to the UTI, resulting in interference or false positives in our diagnosis of BBD.

Statistical analysis and processing

Statistical analysis was performed using the Statistical Package for Social Sciences (SPSS), version 11.0 for Windows (IBM Corp., Armonk, NY). The quantitative data with a normal distribution are expressed as the \({\overline{\text{x}}}\) ± s. Fisher’s exact tests and χ2 tests were used for group distribution comparisons, and the multigroup rates were compared using χ2 tests, trending χ2 tests and logistic regression.

Results

Questionnaire collection

A total of 11,050 questionnaires were distributed, and 10,166 valid questionnaires were included in the analysis, comprising 5118 (50.34%) males and 5048 (49.66%) females. The response rate for the questionnaires was 92% (10,166/11,050).

The prevalence of BBD and its associations with different genders and ages are shown in Table 1 and Fig. 3

Table 1 Prevalence of BBD in children of different ages from 4 to 10 years old.
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Figure 3
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The prevalence of BBD according to gender and age.

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As shown in Fig. 3, the prevalence of BBD decreased with age (P < 0.001). The average BBD prevalence was 3.73% (191/5,118) in boys and 4.32% (218/5,048) in girls. No significant difference in prevalence of BBD between boys and girls was noted (P > 0.05).

The prevalence of BBD was related to the length of DD usage and the EC starting time (Table 2)

Table 2 Relationship between the prevalence of BBD and DD usage and EC.
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Results showed: ① According to the Spearman correlation coefficient analysis (r = 0.236 and P < 0.001), with prolonged usage of DDs, there was a significant delay in starting EC and significantly increased the prevalence of BBD(P < 0.001). ② The prevalence of BBD was significantly lower amongst children who never used DDs (P < 0.001) as compared to those children who used DDs until 12 or 24 months of age. However, BBD prevalence was also significantly lower amongst children who stopped DD usage before 12 months when compared to those who used DD until after 24 months (P < 0.001). The BBD prevalence was also higher amongst children who used DDs during the daytime or for the entire day compared with those that never used DDs (P < 0.001). Moreover, children using DDs during the day are more likely to have BBD (P < 0.001) when compared with children who only use DDs at night. ③ With regards to the introduction of EC, prevalence of BBD was lower amongst children who started EC within 12 months of age compared with those who started EC after 12 or 24 months (P < 0.001).

Risk and protective factors for BBD prevalence

To screen out the main influencing factors affecting the prevalence of BBD, the following factors were simultaneously introduced into the logistic regression model for analysis (Table 3).

Table 3 Logistic regression analysis of factors influencing BBD prevalence.
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The results of logistic regression analysis(Table 3) showed: ① The continuous prolonged use of DDs (for over 12 and 24 months) and daytime usage of DDs are risk factors for BBD in children (OR > 1, P < 0.05); ② DD usage only at night seemed to be a protective factor against BBD (OR < 1, P < 0.05); and ③ starting EC within 12 or 24 months of age was a protective factor against BBD(OR < 1, P < 0.05).

Discussion

Disposable diapers are undoubtedly one of the greatest inventions of the twentieth century and is widely used around the world. In China, it has become increasingly popular over the past few decades. With their strong water absorption ability, children using DDs can sometimes go a whole day without needing to use the toilet. Based on this strong absorption ability and also disposable features, DDs are now also used for some Chinese medical workers who need to work long hours to combat COVID-19 and sometimes amongst astronauts.

It is well known that the prevalence of BBD gradually decreases with increasing age due to the natural maturation of the body. However, with the popularisation of DD usage, it is not known whether this has had any effect on the prevalence of BBD. To our knowledge, there is very limited literature addressing this and our study is one of very few studies involving such a large study population addressing issues of DD usage, EC and/or prevalence of BBD8,28. In order to facilitate the filling of the questionnaires and avoid recall bias as much as possible, the schools of the respondents we selected were mainly distributed in cities and towns, and therefore, it is unable to analyze the results between children in the schools of the urban and rural areas in this study. Meanwhile, the limitations like incorrect memory of the duration of the use of DD and the age the children start EC might occur in the present study, although we have tried our best to avoid recall bias during the survey and the later data analysis, which we will strive to improve in the future research. From our current study, EC can have a preventive role against BBD, and seems to have a role in reducing the progression of BBD even when introduced a little later in toilet training and may thus even have a therapeutic role in BBD management. The bladder and rectum are closely related in anatomy and function. Approximately 20–50% of children with bowel dysfunction have combined bladder symptoms, demonstrating that voiding and defecation function can affect each other. One study by Luise Borch analysed 73 children in Denmark and demonstrated that the standardized treatment regimen of BBD led to the resolution of functional defecation disorder in 70 of the 73 children (96%). Of the children with DUI, 68% had at least a 50% reduction in the number of daytime incontinence episodes attributable to the successful relief of bowel dysfunction, and 27% achieved complete continence during the daytime2,27. Another study found that while actively treating intestinal problems, 95% of the children experienced improved bowel function, and 68% of the children experienced simultaneous reduced urinary incontinence during the day, with some of the children's enuresis symptoms even disappearing. At the same time, the treatment of voiding dysfunction can also reduce the prevalence of constipation and FI among children13,29.

Conclusions

The prevalence of BBD has increased significantly during recent decades in mainland China, where DDs have exhibited a much increased utilization rate in recent years. The present study showed that prolonged DD usage (particularly during the daytime) and resulting delayed introduction of EC in toilet training, are significant risk factors for BBD in our population of children. Early introduction of EC and weaning of DD usage, is associated with a lower prevalence of BBD in children.