Original Article Functional constipation and bladder capacity and severity of enuresis in children: a correlation study
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Int J Clin Exp Med 2018;11(2):806-811 www.ijcem.com /ISSN:1940-5901/IJCEM0058710 Original Article Functional constipation and bladder capacity and severity of enuresis in children: a correlation study Yanli Ma1, Ying Shen1, Xiaomei Liu2 1 Department of Nephrology, Beijing Children’s Hospital, Capital Medical University, Beijing Key Laboratory of Chronic Kidney Disease and Blood Purification of Children, China; 2The General Ward, Beijing Children’s Hospital, Capital Medical University, No. 56, South Lishi Road, Xicheng District, Beijing, China Received June 2, 2017; Accepted November 26, 2017; Epub February 15, 2018; Published February 28, 2018 Abstract: Background: Primary nocturnal enuresis (PNE) is the most common voiding problem among pediatric patients. Enuresis has a complex etiology involving bladder function derangements, circadian rhythm, genetics, psy- chological factors, and the central nervous system. In this study, we studied the correlations among constipation, bladder capacity, and severity of PNE in children. Methods: The study was conducted in children and adolescents aged 5-15 years and diagnosed with PNE in Beijing Children’s Hospital, Capital Medical University. Severity of noc- turnal enuresis was classified as mild-moderate and severe according to the frequency of enuresis. In particular, more than six wet nights weekly was classified as severe and six or less as mild-moderate. Rome III questionnaire was used to determine whether a patient has constipation. Urinalysis and urinary ultrasound were performed for all participants. A logistic regression model was used to investigate the relationship between the severity of enuresis and possible predictive variables. Results: The mean age of the patients was 7.13 ± 2.45 years. A total of 92 pa- tients were male, and 72 were female. Sixty percent of the patients had constipation for more than 6 months, and a negative association was found between constipation and bladder capacity (P = 0.000, r = -0.656). Rome III score was an independent predictor of severity of enuresis (P < 0.05). Constipated children were 1.47 times more likely to have severe enuresis than those not constipated (P = 0.002, 95% CI: 1.147-1.877). However, no significant relation- ship was observed between constipation and bladder residual urine volume (P = 0.725). Conclusion: Constipation was correlated with the severity of enuresis and bladder capacity. We strongly recommend careful inspection of constipation in each patient with enuresis. Keywords: Constipation, enuresis, bladder capacity, correlation, Rome III score Introduction and above [6] and is the most common voiding problem in children. NE can be classified as pri- Functional constipation is characterized by mary or secondary. Primary nocturnal enuresis infrequent stool evacuation, passing of hard (PNE) is defined as enuresis since childhood stools, or painful defecation without fundamen- without at least 6 months of dryness. The tal organic causes [1]. No structural, endocrine, pathophysiology of enuresis is complex and or metabolic etiology is identified in childho- involves bladder function derangements, circa- od constipation, which is often categorized dian rhythm (e.g., sleep and diuresis), genetics, as “functional” [2, 3]. The worldwide preva- psychological factors, and the central nervous lence of childhood constipation ranges from system (e.g., several neurotransmitters and 0.3% to 28% [4]. Functional constipation is the receptors). second most common reason that a child is referred to a pediatric gastroenterologist, and Recently, Veiga et al. [7] demonstrated that such children account for up to 25% of all visits constipation is associated not only with dys- [3, 5]. functional urination but also with overac-tive bladder. Rectal distention is stimulatory in Nocturnal enuresis (NE) refers to urinary incon- humans, decreasing bladder capacity and in- tinence during sleep in children aged 5 years creasing contractility [8, 9]. Meanwhile, night-
Functional constipation and enuresis in children: a correlation study pulmonary, cardiovascular, endocrinological, or neurological disease that would interfere with evaluation; (2) received treatment for NE within the past 6 months; (3) unwillingness to sign informed consent. To evaluate the presence of constipation, we used the Rome III child questionnaire for pa- tients aged 4-18 years. All patients were en- couraged to complete the questionnaire by themselves. When the patients experienced any difficulty, they sought help from their par- ents. The questionnaires can be completed by parents if necessary (e.g., for those with read- ing difficulty, 5-8 years old). Participants who Figure 1. Spearman correlation between frequency of enuresis (FOE) and Rome III criteria (R2 = 0.097 responded positively to two of the six ques- Linear). tions were considered constipated [11]. The severity of NE was classified as mild-moderate and severe according to the frequency of en- time detrusor overactivity, which is associated uresis. More than six wet nights weekly was with constipation, plays an important role in classified as severe, whereas six or less as enuresis. mild-moderate. Urinalysis and urinary ultra- sound were performed in all the participants. The association between enuresis and con- The study was submitted to the ethics com- stipation is also well established and known. mittee of our institution and obtained approval Hogdes [10] showed that 80% of enuretic pa- for its implementation. Written consent was tients are also constipated and laxative therapy obtained from the parents. obtained significant resolution of their enuretic problem. However, this association remains un- Statistical analysis clear. To the best of our knowledge, there is a lack of studies that extensively assessed the The collected data were analyzed using SPSS association of constipation systems with blad- 20.0 (Statistical Package for the Social Sci- der capacity and severity of enuresis in enuret- ences, version 20.0, SPSS Inc., Chicago, Illinois, ic children. Thus, this study aims to discuss USA). Numerical variables, such as age, were these issues. expressed as mean and SD. Categorical vari- ables, such as the incidence of severe or mild- Materials and methods moderate enuresis, were compared using the chi-square test, where a P value of < 0.05 was The study was conducted in children and ado- considered significant. Nonparametric variabl- lescents aged 5-15 years and diagnosed with es of bladder capacity and Rome III scores PNE between September 2016 and February and frequency of enuresis were compared us- 2017 in Beijing Children’s Hospital, Capital Me- ing the Spearman correlation, where P < 0.05 dical University. The inclusion criteria were as was considered significant. A logistic regres- follows: (1) age of 5-15 years, PNE (i.e. two or sion model was used to investigate the rela- more wet nights per week and not dry for more tionship between the severity of enuresis and than 6 months); (2) no medication for PNE rec- possible predictive variables. eived during the last 6 months; (3) lack of cli- nical or laboratory signs suggestive of some Results underlying diseases other than NE (e.g., kidney diseases, endocrine diseases, and nervous Patient characteristics system diseases that may contribute to enure- sis); (4) voluntarily agreed to participate in this A total of 164 PNE patients aged between 5 study and signed the informed consent. The and 15 years fulfilled the inclusion criteria. Of exclusion criteria were as follows: (1) a pres- them, 92 patients (56.1%) were male and 72 ence or a history of organic urological, hepatic, (43.9%) were female. The mean age of the 807 Int J Clin Exp Med 2018;11(2):806-811
Functional constipation and enuresis in children: a correlation study Table 1. Incidence of severe and mild-moderate We also found that constipated children, ac- enuresis in constipated and not constipated cording to the Rome III criteria, had a higher patients with enuresis incidence of severe enuresis and lower inci- mild-moderate Severe dence of mild-moderate enuresis than those P value without constipation (68.7% versus 44.6%, enuresis enuresis Not constipated 36 (55.4%) 29 (44.6%) 0.003 31.3% versus 55.4%, P = 0.003, Table 1). Constipated 31 (31.3%) 68 (68.7%) Correlation between constipation and bladder Total 67 97 capacity A negative association was found between con- stipation (Rome III scores) and bladder capacity (Figure 2, P = 0.000, coefficient and correlation of -0.656). Correlation between constipation and bladder residual urine volume No significant relationship was observed be- tween constipation and bladder residual urine volume (Figure 3, P = 0.725, coefficient and correlation of 0.028). Figure 2. Spearman correlation between bladder ca- Multivariate analysis of predictive risk factors pacity and Rome III criteria (R2 = 0.474 Linear). of severe enuresis A logistic regression model was used to investi- gate the relationship between severity of enure- sis and possible predictive variables, including age, gender, family history of NE, residual urine volume, and Roman III score, which was the only independent predictor of severe enuresis (Table 2). Constipated children were 1.47 times more likely to have severe enuresis than those not constipated. Discussion Constipation is a common pediatric problem that remains underdiagnosed and poorly treat- ed and thus often lead to severe functional Figure 3. Spearman correlation between residual impairment [12]. It is a commonly unrecognized urine volume (RUV) and Rome III criteria (P = 0.725). etiologic factor in enuresis, and its treatment contributes to the resolution of enuresis [13]. The reported prevalence of constipation am- patients was 7.13 ± 2.45 years. A total of 99 ong enuretic children ranged from 7.06% in a patients (60.0%) had constipation for more Turkish population study [14] to 69.8% at a than 6 months, and 60.9% of them were male tertiary US pediatric voiding dysfunction clinic and 59.7% were female. [15]. The prevalence of constipation among Correlation between constipation and symp- enuretic children in this study (60.0%) was con- toms of enuresis sistent with findings of Robson [15]. Hodges [10] determined that 80% of enuretic children A positive correlation was found between con- are constipated, and their conditions can be stipation (Rome III scores) and frequency of improved through laxative therapy. Given the enuresis (Figure 1, P = 0.001, coefficient and high incidence of constipation in children with correlation of 0.267). enuresis, thoroughly assessing constipation in 808 Int J Clin Exp Med 2018;11(2):806-811
Functional constipation and enuresis in children: a correlation study Table 2. Multivariate analysis of severity of enuresis As previously stated, urinary Standard Wald 95% confidence interval and bowel dysfunction are Factors P OR associated because the blad- error value Lower limit Upper limit der, urethra, and rectum are Rome III scores 0.126 9.313 0.002 1.47 1.147 1.877 close in anatomical structure [20]. Rectal distension due to each enuretic patient is necessary. In the pres- fecal retention in chronic functional constipa- ent study, a positive correlation between con- tion causes bladder distortion and stimulation stipation (Rome III scores) and frequency of of detrusor stretch receptors, resulting in detru- enuresis was observed, although the correla- sor proneal dyssynergism [21]. Bladder func- tion coefficient was low, suggesting a weak tion derangements play an important role in the relationship between them. From another per- pathogenesis of enuresis [22]. One important spective, constipated children, according to finding in our study was that children with more the Rome III criteria, had a higher incidence of severe constipation symptoms had more re- severe enuresis and lower incidence of mild- duced bladder capacity (r = -0.656). According moderate enuresis than those without consti- to a study by Burgers [23], rectal distention sig- pation, and the differences had statistical sig- nificantly and at times markedly affects bladder nificance. Furthermore, Rome III score was the capacity, contractility, and sensation. Franco only independent predictor of severe enure- [24] also suggested that when the rectum is sis. Constipated children were 1.47 times more distended, it compresses the adjacent blad- likely to have severe enuresis than those not der and decreases functional bladder capacity. constipated. Previous research also supports Kim et al. [25] reported that overactive bladder this view. McGrath et al. [16] conducted a pro- symptoms that contribute to enuresis can be spective cross-sectional study and found that improved by treating constipation. Constipation the prevalence of constipation is high among induces bladder dysfunction when the rectum children with NE. The severity of bedwetting is filled with stool and stretch receptors are was higher in their cohort (95.3% wetted the stimulated and transmitted to the brain, induc- bed at least once per week) compared with ing temporary involuntary contraction of the 5.1% in a large Australian population study of external anal sphincter and the puborectalis school-aged children [17], supporting that the muscles [25]. In our study, we analyzed the re- severity of wetting may be associated with lationship between constipation and residual the presence of constipation. Thus, severe en- urine volume, but the difference was not statis- tically significant (P = 0.725), suggesting no cor- uresis often occurs concomitantly with consti- relation between the two. pation, and constipation should be identified and treated before managing enuresis if ne- Our study has several limitations. Restricted by cessary. objective reality condition, we did not evaluate constipation by digital rectal examination or by Nevertheless, the relationship between consti- rectal diameter on ultrasound. As this is a pation and enuresis remains controversial. Our cross-sectional study, we cannot establish any results are in contrast to those in previous stud- causal relationship because of the small sam- ies, indicating no association between noctur- ple size, and no participant responded positive- nal enuresis and constipation. Sampaio [18] ly to five or six of the six questions based on reported that 12.6% of children and adoles- Rome III criteria. Therefore, future research in cents had constipation in association with NE, this direction is necessary. although this association was nonsignificant (P = 0.483). Sureshkumar et al. [19] evaluated Conclusions potential risk factors for the presence and severity of nocturnal enuresis and found no sig- Constipation was negatively associated with nificant association between constipation and bladder capacity. Children with more severe severe nocturnal enuresis. These differences constipation exhibited more reduced bladder might be related to different definitions and capacity. Constipation was also correlated with severity of NE used in different studies, differ- the severity of enuresis. For enuretic patients ent scales for evaluating constipation [19], dif- with constipation, constipation should be eval- ferent age groups, different race, and sociocul- uated and treated to increase bladder capacity tural differences. and therefore relieve enuresis. 809 Int J Clin Exp Med 2018;11(2):806-811
Functional constipation and enuresis in children: a correlation study Acknowledgements [8] Panayi D, Khullar V, Spiteri M, Hendricken C and Fernando R. A pilot randomised study to The authors gratefully acknowledge the pa- determine if rectal distension alters urodynam- tients and clinical investigators who participat- ics. Meeting of the International-continence- ed in this trial and thank the support from the society 2008; 19: 636-636. research special project of capital health de- [9] De Wachter S and Wyndaele JJ. Impact of rec- tal distention on the results of evaluations velopment. This study was funded by research of lower urinary tract sensation. J Urol 2003; special project of capital health development 169: 1392-1394. (grant number 2016-1-2095). [10] Hodges SJ and Anthony EY. Occult megarec- tum-a commonly unrecognized cause of en- Disclosure of conflict of interest uresis. Urology 2012; 79: 421-424. [11] Rasquin A, Di Lorenzo C, Forbes D, Guiraldes None. E, Hyams JS, Staiano A and Walker LS. Child- hood functional gastrointestinal disorders: ch- Address correspondence to: Ying Shen, Department ild/adolescent. Gastroenterology 2006; 130: of Nephrology, Beijing Children’s Hospital, Capital 1527-1537. Medical University, Beijing Key Laboratory of Chronic [12] Culbert TP and Banez GA. Integrative ap- Kidney Disease and Blood Purification of Children, proaches to childhood constipation and en- China. Tel: 13370115116; E-mail: xdaspiwn@163. copresis. Pediatr Clin North Am 2007; 54: 927- com; Xiaomei Liu, The General Ward, Beijing 930. Children’s Hospital, Capital Medical University, No. [13] O’ Regan S, Yazbeck S, Hamberger B and 56, South Lishi Road, Xicheng District, Beijing, Schick E. Constipation a commonly unrecog- China. Tel: 13370115078; E-mail: xmliu16@163. nized cause of enuresis. Am J Dis Child 1986; 140: 260-261. com [14] Cayan S, Doruk E, Bozlu M, Nass Duce M, Ulu- References soy E and Akbay E. The assessment of consti- pation in monosymptomatic primary nocturnal [1] Voskuijl WP, Heijmans J, Heijmans HS, Tamin- enuresis. Int Urol Nephrol 2001; 33: 513-6. iau JA and Benninga MA. Use of Rome II crite- [15] Robson LM, Leung AK and Van Howe R. Pri- ria in childhood defecation disorders: applica- mary and secondary nocturnal enuresis: simi- bility in clinical and research practice. J Pediatr larities in presentation. Pediatrics 2005; 115: 2004; 145: 213-217. 956-9. [2] Biggs WS and Dery WH. Evaluation and treat- [16] McGrath KH, Caldwell PH and Jones MP. The ment of constipation in infants and children. frequency of constipation in children with noc- Am Fam Physicion 2006; 73: 469-477. turnal enuresis: a comparison with parental [3] Lewis G and Rudolph CD. Practical approach reporting. J Paediatr Child Health 2008; 44: to defecation disorder in children. Pediatr Ann 19-27. 1997; 26: 260-268. [17] Bower WF, Moore KH, Shepherd RB and Ad- [4] Dehghani SM, Basiratnia M, Matin M, Hamid- ams RD. The epidemiology of childhood enure- pour L, Haghighat M and Imanieh MH. Urinary sis in Australia. Br J Urol 1996; 78: 602-6. tract infection and enuresis in children with [18] Sampaio C, Sousa AS, Fraga LG, Veiga ML, chronic functional constipation. Iran J Kidney Bastos Netto JM and Barroso U Jr. Constipation Dis 2013; 7: 363-366. and lower urinary tract dysfunction in children [5] Youssef NN and Di Lorenzo C. Childhood con- and adolescents: a population-based study. stipation: evaluation and treatment. J Clin Front Pediatr 2016; 4: 101. Gastroenterol 2001; 33: 199-205. [19] Sureshkumar P, Jones M, Caldwell PH and [6] Austin PF, Bauer SB, Bower W, Chase J, Franco Craig JC. Risk factors for nocturnal enuresis in I, Hoebeke P, Rittig S, Vande Walle J, von Gon- school-age children. J Urol 2009; 182: 2893- tard A, Wright A, Yang SS and Nevéus T. The 2899. standardization of terminology of lower urinary [20] Burgers RE, Mugie SM, Chase J, Cooper CS, tract function in children and adolescents: up- von Gontard A, Rittig CS, Homsy Y, Bauer SB date report from the Standardization Commit- and Benninga MA. Management of functional tee of the International Children’s Continence constipation in children with lower urinary tract Society. J Urol 2014; 191: 1863-1865. symptoms: report from the Standardization [7] Veiga ML, Lordelo P, Farias T, Barroso C, Bon- Committee of the International Children’s Con- fim J and Barroso U Jr. Constipation in children tinence Society. J Urol 2013; 190: 29-36. with isolated overactive bladders. J Pediatr [21] Hyman PE and Fleisher D. Functional fecal re- Urol 2013; 6: 945-949. tention. Pract Gastroenterol 1992; 16: 29-37. 810 Int J Clin Exp Med 2018;11(2):806-811
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