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Dysfunction elimination syndrome: Is age at toilet training a determinant?

      Abstract

      Purpose

      To study the relationship between the age of completion of toilet training during daytime and the onset of dysfunctional elimination syndrome (DES).

      Methods

      The present study was designed as a case-control study. A total of 80 patients with DES were allocated to the case group and 80 patients age- and gender-matched without DES were allocated to the control group. The patients with DES were seen in a tertiary center and the control patients were seen in a primary care center. Early completion of toilet training was considered to be before 24 months.

      Results

      Patients were aged 3–17 years (mean: 7.55); 24 were male (30%) and 56 female (70%). The most frequent lower urinary tract symptoms were: urgency (77%), incontinence (75%), holding maneuvers (30%), high urinary frequency (61%) and low urinary frequency (16%). There was a history of urinary tract infection (UTI) in 62% of the DES group. The first UTI episode was before toilet training in 40%. The completion of toilet training was before the age of 2 years in 48% of DES patients and in 50% of the control group (p = 0.752) [odds ratio (OR) 0.91, 95% confidence interval (CI) 0.49–1.62].

      Conclusion

      The completion of toilet training before 24 months of age was not associated with DES. Some patients had DES symptoms such as UTI, infrequent voiding and constipation before toilet training. These findings suggest that DES may precede toilet training and this possibility should be confirmed in further studies.

      Keywords

      Introduction

      Dysfunctional elimination syndrome (DES) is the association of lower urinary tract and bowel dysfunction [
      • Koff S.A.
      • Wagner T.T.
      • Jayanthi V.R.
      The relationship among dysfunctional elimination syndromes, primary vesicoureteral reflux and urinary tract infections in children.
      ,
      • Feldman A.S.
      • Bauer S.B.
      Diagnosis and management of dysfunctional voiding.
      ]. The spectrum of urinary disorders includes urge syndrome, dysfunctional voiding with in coordination between the detrusor and urinary sphincter, and enuresis [
      • Feldman A.S.
      • Bauer S.B.
      Diagnosis and management of dysfunctional voiding.
      ]. Koff et al. reported the frequent association between DES, vesicoureteral reflux and urinary tract infection [
      • Koff S.A.
      • Wagner T.T.
      • Jayanthi V.R.
      The relationship among dysfunctional elimination syndromes, primary vesicoureteral reflux and urinary tract infections in children.
      ]. Urinary tract and bowel have the same embryologic origin, enervation and anatomic proximity, but the exact pathophysiologic mechanisms of DES are still not fully understood [
      • Hoebeke P.
      Twenty years of Urotherapy in children: what have We Learned?.
      ].
      Lower urinary tract dysfunction and constipation have been closely connected with incorrect or early toilet training, said to be caused by parental expectations that do not consider the child’s neurological development stage [
      • Mota D.M.
      • Barros A.J.
      Toilet training: methods, parental expectations, and associated dysfunctions.
      ]. However, the published studies to date are insufficient for a conclusive comparison between the different techniques for toilet training [
      • Vermandel A.
      • Van Kampen M.
      • Van Gorp C.
      • Wyndaele J.J.
      How to toilet train healthy children? A review of the literature.
      ].
      Studies suggest that although children are completing toilet training much later than in the preceding generation there has been an increase in DES prevalence [
      • Bakker E.
      • Wyndaele J.J.
      Changes in the toilet training of children during the last 60 years: the cause of an increase in lower urinary tract dysfunction?.
      ]. We do not know the exact mechanisms of these dysfunctions and their relation to diaper use [
      • Hoebeke P.
      Twenty years of Urotherapy in children: what have We Learned?.
      ]. Specific and evidence-based studies on this topic are few. Therefore, the objective of this paper was to study the relationship between the age of completion of toilet training during the daytime and the onset of DES.

      Materials and methods

      This study was designed as a case control, and was approved by the local ethics committee and conducted in a tertiary hospital and a primary care center, both located in the city of Rio de Janeiro, Brazil. The case group was composed of 80 children randomly selected out of a group of 435 DES patients seen at the Voiding Disturbance and Urodynamic Pediatric Clinic. Children with neurogenic bladder, urologic and orthopedic malformations were excluded from this study. The 80 patients for the control group were randomly selected among patients seen during routine visits or visits due to mild upper respiratory tract infection in a primary care center. Children with a medical history of urinary tract disorders, bowel dysfunction or malformations were excluded. All the control patients were daytime continent and showed no evidence of neurological development delay. This primary care center was chosen because it is an extension project of our Medical School in a low-income community. The two groups were matched by age and gender.
      In the case group, the patients were seen by a doctor (one of the authors) who after taking the medical history filled out a previously published questionnaire [
      • Fonseca E.G.
      • Bordallo A.P.
      • Garcia K.
      • Munhoz C.
      • Silva C.P.
      Lower urinary tract symptoms in enuretic and nonenuretic children.
      ]. In the control group, the mothers were asked about urinary tract disorders, lower urinary tract symptoms (LUTS; the ones mentioned in the questionnaire), urinary tract infection (UTI) and constipation, and all of these were considered exclusion criteria. When a child was eligible to be included in the control group, the mother was asked at what age the child completed toilet training during the daytime. The authors only filled out the questionnaire after they were sure that the parent had understood the questions. This methodology was chosen because the authors consider the medical history as the best way to collect information about sign and symptoms. In addition, the parents come from a low-income social class and have a poor educational background which could affect their comprehension of the questionnaire.
      The completion of toilet training during daytime was considered to be early when it occurred before 24 months. Lower urinary tract symptoms were defined according to the International Children’s Continence Society [
      • Nevéus T.
      • von Gontard A.
      • Hoebeke P.
      • et al.
      The Standardization of terminology of lower urinary tract function in children and adolescents: report from the standardization committee of the international children’s continence society.
      ]. For children aged 3–4 years the urinary frequency was defined as increased when it was consistently higher than 11 voids per 24 h and as decreased when it was consistently fewer than 5 voids per 24 h [
      • Jansson U.-B.
      • Hanson M.
      • Hanson E.
      • Hellstrom A.L.
      • Sillen U.
      Voiding pattern in healthy children 0–3 years old: a longitudinal study.
      ,
      • Goellner M.
      • Ziegler E.E.
      • Fomon S.J.
      Urination during during the first three years of life.
      ]. For infants, a history of a low number (less than 5) of wet diapers per day and long intervals between changes was considered indicative of decreased urinary frequency [
      • McLellan D.L.
      • Bauer S.B.
      Bladder dysfunction.
      ].
      Data were compiled and statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS). Chi-square statistics was used; p values of <0.05 were considered to be statistically significant. An odds ratio was estimated for presenting DES.

      Results

      The patients in both groups were aged 3 to 17 with a mean age of 7.55 years, with a gender distribution of 24 males (30%) to 56 females (70%). The case group DES complaints by order of prevalence were: urgency (77%), incontinence (75%), high urinary frequency (61%), holding maneuvers (30.4%), low urinary frequency (16%) and post-micturition dribble (12%). Ten out of the 80 DES patients were under 5 (4 were 3 years old and 6 were 4 years old). They were referred to this specialized clinic because of recurrent urinary infection. These patients were found to have constipation and lower urinary tract dysfunction with deficient emptying. History of UTI was present in 62% of patients of the case group and the first episode of UTI in 40% of these patients occurred prior to toilet training; 82% of the patients who had their first UTI before toilet training were female. In this group, constipation and infrequent voiding were present before the beginning of toilet training. A family history of enuresis, urinary incontinence or LUTS was present in 68 (85%) patients of the case group. The mean, median and mode ages of completion of toilet training during daytime were respectively: 2.3 years, 2.0 years and 2.5 years in the DES group and 1.8 years, 2.0 years and 2.0 years in the control group. The age of completion of toilet training during daytime was before 2 years in 48% of DES patients and 50% of the control group (p = 0.752) [odds ratio (OR) 0.91, 95% confidence interval (CI) 049–1.62]. Among the DES patients, 64% of parents pointed out long dry intervals as a reason for early toilet training.

      Discussion

      In this study, the completion of toilet training during daytime before 24 months of age was not associated with DES.
      This result is in accordance with the observations of other authors who did not find an association between early toilet training and DES [
      • Blum N.J.
      • Taubman B.
      • Nemeth N.
      During toilet training, constipation occurs before stool toileting refusal.
      ,
      • Blum N.J.
      • Taubman B.
      • Nemeth N.
      Relationship between age at initiation of toilet training and duration of training: a prospective study.
      ,
      • Chang S.J.
      • Yang S.S.D.
      The effects of the age initiating toilet training on urinary continence and voiding function in children.
      ]. Blum et al. studied 406 children between 17 and 19 months old and found that the following factors were associated with completion of toilet training at later ages: beginning toilet training at a later age, stool toileting refusal and constipation [
      • Blum N.J.
      • Taubman B.
      • Nemeth N.
      During toilet training, constipation occurs before stool toileting refusal.
      ]. The above-mentioned authors also reported that initiation of intensive training before 27 months does not correlate with earlier completion of toilet training [
      • Blum N.J.
      • Taubman B.
      • Nemeth N.
      Relationship between age at initiation of toilet training and duration of training: a prospective study.
      ]. Chang SJ and Yang SSD studied 235 healthy kindergarteners and found that children toilet trained early attained daytime and nighttime continence earlier and had normal voiding function and a lower dysfunctional voiding symptom score [
      • Chang S.J.
      • Yang S.S.D.
      The effects of the age initiating toilet training on urinary continence and voiding function in children.
      ].
      Another important finding in our study was that of the DES patients 40% had their first episode of UTI before toilet training and 16% were referred as presenting low urinary frequency. Constipation and infrequent voiding were present before the beginning of toilet training. This finding refutes the belief that DES starts exclusively as a consequence of early and inadequate toilet training. Constipation and infrequent voiding should be addressed because parents do not often complain about them as opposed to urinary incontinence which is usually a major concern for parents. Although clinical manifestation of inadequate bladder emptying is not so easy to diagnose, it is important to identify such patients as they are the ones who present more complications and poor outcome among those with non-neurologic lower urinary tract dysfunction [
      • Koff S.A.
      • Wagner T.T.
      • Jayanthi V.R.
      The relationship among dysfunctional elimination syndromes, primary vesicoureteral reflux and urinary tract infections in children.
      ,
      National Institute for Health and Clinical Excellence
      Urinary tract infection in children.
      ].
      Family history of enuresis, urinary incontinence and LUTS were present in a high percentage (85%) of patients of the case group. This finding is in accordance with previous studies, which showed that urge symptoms, repeated bladder infections, nighttime awakening and high micturition frequency are also common in the families of enuretics [
      • Néveus T.
      • Hetta J.
      • Cnattingius S.
      • Tuvemo T.
      • Lackgren G.
      • Olsson U.
      Depth of sleep and sleep habits among enuretic and incontinent children.
      ], and that families with bladder dysfunction had linkages to the same chromosomal regions as those with enuresis [
      • Loeys B.
      • Hoebecke P.
      • Raes A.
      • Messian L.
      • De Paepe A.
      • Vande Walle J.
      Does monosymptomatic enuresis exist? A molecular genetic exploration of 32 families with enuresis/incontinence.
      ,
      • von Gotard A.
      • Hollman E.
      • Eiberg H.
      • Benden B.
      • Rittig S.
      • Lehmkuhl G.
      Clinical enuresis phenotypes in familial nocturnal enuresis.
      ]. This finding suggests that an individual genetic predisposition to lower urinary tract dysfunction in this group may have hindered the toilet training. This is an important result and should be addressed in future studies.
      Not having information regarding the motivation for starting toilet training in the control group is a limitation of this initial study. This information may bring about important contributions to the understanding of the relationship between toilet training and DES, and should be researched in further studies.
      Proper bladder and bowel function rely on a complex integration of central and peripheral neural pathways. Infants’ voiding is controlled by pontine mesencephalic micturition with minimal cortical influence. An uncoordinated pattern of voiding may be demonstrated in 50% of the infants. This pattern matures into coordinated voiding between 1 and 3 years of age when the cortical inhibitory pathways to and from the pontine micturition center develop [
      • Jansson U.-B.
      • Hanson M.
      • Hanson E.
      • Hellstrom A.L.
      • Sillen U.
      Voiding pattern in healthy children 0–3 years old: a longitudinal study.
      ,
      • Yeung C.K.
      • Goodley M.I.
      • Ho C.K.W.
      • Ransley P.G.
      • Duffy P.G.
      • Chen C.N.
      • et al.
      Some new insights into bladder function in infancy.
      ].
      The effectiveness of potty training depends on a certain level of maturity and integrity of those structures and also of the child’s development [
      • Feldman A.S.
      • Bauer S.B.
      Diagnosis and management of dysfunctional voiding.
      ,
      • Rushton H.G.
      Wetting and functional voiding disorders.
      ]. Based on this, some changes in toilet-training techniques have occurred in the last few years. A marked tendency to postpone toilet training has been noticed [
      • Bakker E.
      • Wyndaele J.J.
      Changes in the toilet training of children during the last 60 years: the cause of an increase in lower urinary tract dysfunction?.
      ,
      • Choby B.A.
      • George S.
      Toilet training.
      ]. Those who defend this later toilet training believe that this strategy allows the child to begin this process more mature and prepared, decreasing the likelihood of problems in the lower urinary tract and bowel [
      • Mota D.M.
      • Barros A.J.
      Toilet training: methods, parental expectations, and associated dysfunctions.
      ]. The ‘child-oriented’ approach focuses on autonomous achievement of the tasks related to continence. It was pioneered by the American pediatrician T. Berry Brazelton whose concept ‘let children themselves decide when they are ready to use the pot’ was made popular [
      • Brazelton T.B.
      A child-oriented approach to toilet training.
      ].
      The results of this study indicate the possibility of wrong voiding mechanisms being caused by factors that precede toilet training such as slight structural anomalies or a maturation delay either in the lower urinary tract or in the nervous system [
      • Hoebeke P.
      Twenty years of Urotherapy in children: what have We Learned?.
      ]. A problem or delay in changing the voiding pattern from uncoordinated to a coordinated one may result in voiding dysfunction. This may explain the finding that not all cases of DES are caused by toilet training.

      Conclusion

      The completion of toilet training before 24 months of age was not associated with DES. In addition, some patients had DES symptoms such as UTI, infrequent voiding and constipation before toilet training. These findings suggest that DES may precede toilet training, and this possibility should be confirmed in further studies.

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