Abstract and Introduction
Abstract
Achievement of urinary continence is an important developmental step that most children attain with the assistance of their parents and caregivers. Debate continues as to the best time to toilet train; in some Asian and African cultures children are trained as infants, while training at age 2-3 years is more typical in Western cultures. Infant voiding is not merely a spinal reflex, as the sensation of bladder filling is relayed to the brain. However, the ability of the brain to inhibit bladder contractions, and to achieve coordinated bladder contraction with sphincter relaxation, matures over time. While there is a concern that later toilet training may be responsible for an increase in urinary incontinence in children, no controlled studies on early versus late toilet training exist to evaluate this hypothesis. A number of medical conditions such as spina bifida, posterior urethral valves, cerebral palsy and autism can cause incontinence and difficulties in toilet training. The decision to start toilet training a child should take into account both the parents' expectation of how independent the child will be in terms of toileting, and the child's developmental readiness, so that a realistic time course for toilet training can be implemented.
Introduction
Toilet training is an important step for both children and parents, because it transitions the child to a more independent stage of life. The great majority of children and parents accomplish this without significant input from physicians, relying on practices that may be culturally determined, discussed in parenting magazines and books, or available on the Internet. Parents faced with a child that does not successfully toilet train often seek guidance from their pediatrician or primary care physician on the readiness of the child to begin toilet training, and how best to accomplish this successfully. Recommendations in western medical literature commonly rely on guidelines published by the American Academy of Pediatrics (AAP) in 1999, outlining the roles of parents, clinicians, and day-care providers in the process of toilet training. Studies performed in the 2000s indicate that the prevalence of urinary incontinence in children is approximately 6-9%. If the primary care physician is unable to determine a neurologic or metabolic cause for urinary incontinence (such as tethered spinal cord or diabetes insipidus), the child is usually referred to a pediatric urologist.
Parents seeking advice on toilet training their infant or toddler are faced with multiple options. Do they take the 'infant toilet training' approach, and pay close attention to their infant, positioning the child over the toilet or sink when he or she makes the tell-tale sign or noise that they need to urinate or defecate? Do they put the child on the toilet for a few minutes after each meal? Do they go along with standard medical recommendations, and wait until their child is 2 or 3 years old, leaving the child in diapers until then? Much of this information is dependent on cultural norms. Grandparents from non-Western cultures might remind parents that they were themselves toilet trained at a young age, using a variation of the first technique. While the 'infant toilet training' approach has received increased media attention in the past 5 years, it is still infrequently practiced in the US, and is not discussed in published guidelines from medical societies. Such anecdotes raise the question of whether the current recommendation to delay toilet training, based on the AAP guidelines, is a cultural practice, or if it is supported by scientific evidence. Changes in childcare over the past 50 years have complicated the process of toilet training, as it now involves both parents and childcare providers, who may use different approaches to toilet training. Some day-care providers require that a child be toilet trained before starting, reflecting the fact that the staffing ratio of care providers to children does not allow the same number of diaper changes that would be carried out at home. Therefore, the economics of childcare can also affect when parents start to toilet train their children.
This Review will focus on the achievement of urinary continence in children. The optimum age for toilet training will be discussed, using examples of variations in method between Western and non-Western cultures. This Review will also provide an overview of bladder function and voiding mechanisms in the infant and young child, will discuss factors in dysfunctional voiding, reviewing the hypothesis that delaying the age of toilet training may paradoxically cause urinary incontinence in children, and will overview medical disorders that may cause difficulty in achieving urinary continence
Urinary Continence
The narrowest definition of urinary continence in a child would be merely the avoidance of unexpected voiding. From this viewpoint, an infant is capable of urinary continence if the caregiver is able to recognize when the infant needs to urinate. Some critics have called this "a reflex conditioning of the mother", a comment which reflects the reality that infant toilet training is time intensive and requires the continuous presence of a parent or caregiver. A broader definition, which is probably more in line with the expectations of parents and physicians, would include the ability of the child to sense when the bladder is full, inhibit the urge to urinate until a socially acceptable time and location, and independently use the toilet. This is the definition of urinary continence which will be used in this article. As this definition of continence requires that the child show significant communication, motor, and decision-making skills, toilet training to achieve these goals depends not only on the maturity of the central nervous system and bladder to store, detect and empty urine, but also on the child's overall development.
Toilet Training
Toilet training is the process of achieving both urinary and stool continence. Infant (less than 1 year old) or early toilet training is not directly comparable with late toilet training (children aged 18 months or over), since both the timing and expected outcome are different. In early toilet training, the goal is to learn when the child needs to void, so that he or she can be brought to the toilet, while the goal of late toilet training is for the child to be completely independent in the entire process of toileting. In the late 19th century, infant toilet training using mechanical stimulants such as soap or laxatives, or rectal stimulation, was popular in the US. The preference for late toilet training returned in the 1930s when concerns were raised about relapses back to incontinence following early toilet training. A 1962 paper by Brazleton and a 1974 book by Foxx and Azrin both emphasized the value of starting toilet training when the child was developmentally ready (known as the 'child-centered approach'), which laid the foundations for the current recommendation to wait until the child is at least 18 months old before starting toilet training, as by this age the child is able to relay the sensation of bladder fullness to their parent. The Foxx-Azrin approach is more intensive and structured than that of Brazleton, and begins with demonstration of toileting to the child using a doll, followed by increased fluid intake and scheduled toilet times. Correct behavior is reinforced with rewards such as food, hugs and toys, while accidents are over-corrected by verbal reprimand, loss of reinforcements, and additional practice sessions. The Brazleton approach begins by sitting the child on the potty clothed, followed by sitting without a diaper. Stool and urine are emptied into the potty, explaining to the child that this is where they go; the final stage is independent use of the potty by the child. Foxx and Azrin reported that continence can be achieved in 4 h in appropriately selected children, while children who are toilet trained using the Brazleton approach appear to take between 6 and 18 months to achieve urinary continence.
Retrospective questionnaires investigating age at toilet training are subject to significant recall bias; the best data from Western countries come from two longitudinal cohort studies performed in Switzerland in the late 1950s and the 1970s. In these studies, stool continence was achieved first at the age of 3 years in 97% of the group, followed by daytime urinary continence in 97% of the group by the age of 6 years, and finally night-time urinary continence. In total, 90% of boys and 94% of girls had achieved complete night-time urinary continence by the age of 6 years. Although toilet training was started at 6-12 months of age in the 1950s cohort, and 12-18 months of age in the 1970s cohort, daytime urinary continence was achieved in 90% of both groups by 4 years of age, and 97% of both groups by 6 years of age. These results were replicated in another longitudinal cohort of children born in 1952, from Baltimore in the USA, with exactly the same percentages seen at the same ages. Nowadays, completion of toilet training before starting kindergarten at approximately 5 years of age would be considered a normal age in children. A more recent prospective study using the child-centered approach in middle class families was conducted in 2003. Children were recruited between 17 and 19 months of age, and parents began toilet training them at a mean age of 29 months. Children who started toilet training before 27 months of age achieved urinary continence at the same time as those who started after 27 months; an average of 37 months.
Many Asian, African, and South American countries show a cultural preference for early toilet training of infants, but other than case reports, no data on age of completion of toilet training and urinary incontinence are available. The most quoted paper in this context describes the toilet training practices of the Digo people of Kenya. These practices are similar to infant toilet training, with the expectation of daytime and nighttime urinary continence by 6 months of age. The mother positions the child between her legs and makes a "shuus" sound that the child learns to link with urinating. Mothers are able to tell that their child is ready to urinate based on the sounds and movements made by the child. This approach combines a stimulus (sound) with the conditioned response (urination), assisted by the mother's perception of when the child needs to void. The authors note that cultural acceptance of public urination, uncumbersome clothes, and the ability of the mother to spend the entirety of the first 2 months of the child's life with her infant contribute to the success of this approach. A study from Vietnam suggests that infant toilet training results in a decreased postvoid residual volume by 9 months, which may indicate that infants can empty their bladders more efficiently if toilet training is undertaken. If this initial finding can be confirmed in other populations, it could indicate that early toilet training might be an important tool for children with anatomical abnormalities such as vesicoureteral reflux, which put them at higher risk for urinary tract infection. Longer-term follow-up on participants who undergo infant toilet training is not currently available.
If one considers the three-part definition of continence outlined earlier (sensing a full bladder; inhibiting the urge to urinate until socially acceptable; and independent use of the toilet or potty), a combination of developmental skills indicate when a child is ready to be toilet trained. Generally, not having bowel movements at night, noticing the urge to void or to pass stool, communicating the need to go to the toilet, being dry for periods of at least 2 h, and waking up dry from a nap, are prerequisites in a child-centered approach to toilet training. These skills are achieved at a median of 22 months in girls, and at 25 months in boys, when they become continent of stool at night. The AAP recommends that toilet training can be started when the child is aged 18 months, but children will reach these developmental milestones at different times; girls acquire almost all the developmental skills related to toilet training at an earlier age than boys.
The role of stress and behavior in toilet training was studied in a group of children aged 4 years or older, who were unsuccessful at toilet training for more than 6 months, or who refused to use the toilet. Although parenting styles (laxness, verbosity, over-reactivity) were not different between the difficult to train and control groups, children who were characterized as difficult personalities by behavioral questionnaire (less adaptable, negative mood, less persistent) were more likely to be difficult to toilet train. Parental stress (isolation, depression, spousal relationship issues) does not seem to influence the age of the child on toilet training, but refusal to stool in a toilet, constipation, and hiding when defecating are more frequent in children who toilet trained after 42 months of age
Bladder Function and Voiding Mechanisms
The natural history of infant bladder function was first systematically studied in the 1990s using free voiding studies and urodynamics. The human neonate initially voids small amounts, about once an hour. Bladder capacity increases in two growth spurts: the first at birth, the second at 3 years of age. Neonates were previously believed to urinate while sleeping as well as when awake, suggesting that a local sacral reflex was responsible for emptying the bladder. However, analysis of neonatal electroencephalography tracings suggests that most neonates experience some arousal before voiding, indicating that the brain is always involved when the bladder empties. Infants experience interrupted (or incomplete) voiding as a result of lack of coordination between the bladder and the external sphincter, which causes elevated voiding pressures until the child reaches the age of 18 months. At 1 week of age, boys void with mean detrusor pressures of 117 cm H2O, and girls with pressures of 75 cm H2O.The traditional belief that the urinary frequency seen in the infant bladder was due to overactivity was disproved by the rarity of overactive contractions observed during studies of infant urodynamics carried out in asymptomatic children.
The high bladder pressures and progressive control of the bladder by the brain in the human infant matches that of the neonatal rat, allowing a great degree of translation from experimental animal findings to humans. It is not ethically possible to obtain bladder tissue from healthy human infants or interfere with their neural maturation, therefore much of what we understand about the neonatal bladder is derived from experimental models. Neonatal cats, rats, and mice are unable to void spontaneously, and are dependent on their mother to lick the perigenital area to cause the bladder to empty. By 3 weeks of age, when they are weaned, neonatal rats are able to void spontaneously in response to bladder filling. At first glance, these findings suggest that the neonatal nervous system is not mature enough for animals to void spontaneously. As the perigenital-bladder reflex reemerges after spinal cord injury, however, and bladder emptying in response to filling can occur in neonatal rats if the forebrain is disconnected from the brainstem, the perigenital reflex actually inhibits the mature bladder emptying reflex. This inhibition is removed at the time of weaning, allowing the rat to void spontaneously. Experimental bladder distension similarly results in the onset of spontaneous voiding at 3 weeks, but prolongs the perigenital reflex for another 2 weeks. Surgical reduction of bladder volume causes the immediate onset of spontaneous voiding in neonatal rats, and results in a long-term increase in bladder capacity and lower voiding pressures. These findings suggest that coordination between the bladder and sphincter requires maturation of central neural control, and that peripheral nervous system connections are ready for use at birth.
While human infants do not exhibit the perigenital reflex, they will void in response to stroking of the paravertebral muscles until 2 months of age.Perhaps infant toilet training activates a primitive bladder emptying reflex via stimuli provided by the mother, while the mature bladder emptying reflex in response to filling requires control exerted by the child's forebrain. Previously, neonatal bladder emptying was thought to only involve an isolated sacral spinal cord reflex, but animal data suggest that bladder emptying in neonates involves descending control from the forebrain to the brainstem, all the way down to the bladder.
The other key finding from animal studies is that neonatal bladder smooth muscle functions differently to that in older juvenile animals and children. Animal study findings indicate that the neonatal bladder produces more pressure per gram of tissue, is more dependent on local calcium levels, and has large-amplitude spontaneous contractions, which become downregulated with maturation.The elevated voiding pressures seen in infants may therefore also represent immature smooth muscle function. The neonatal bladder empties well, but does not store well in both rats and humans. The spontaneous contractions observed in the neonatal rat bladder occur only when central regulation of the bladder is removed, suggesting that the brain exerts a tonic inhibition on the bladder. In children, a high-capacity bladder and small postvoid residual volume seem to predict earlier completion of toilet training, which likely means that central control of the bladder is more effective when the bladder demonstrates mature smooth muscle function
Urinary Incontinence
A comparison of different toilet training methods and timings has suggested that the modern trend for late toilet training may have caused an increase in the diagnosis of urinary incontinence. It is unclear whether we are diagnosing urinary incontinence more commonly because we are more aware of it, if urinary incontinence and late toilet training are both increasing but unrelated, or if late toilet training is a cause of urinary incontinence. In these studies, children with persistent daytime and night-time incontinence had begun toilet training at an older age (greater than 18-24 months) than the children who were dry. Limitations of these studies included retrospective design,and a varying definition of late toilet training (age greater than 18 months, or age greater than 24 months) between studies. A retrospective survey of schoolchildren at a mean age of 11.5 years found that children with daytime urinary incontinence tended to start toilet training 6 months later than those without, although the median age for starting toilet training in both groups was 18-24 months. A prospective study designed to investigate environmental effects on children's health was reanalyzed to evaluate the age that toilet training was initiated, which was then compared with the child's daytime continence at 9 years of age. 50% of parents in the study reported starting toilet training when their child was between 15 and 24 months of age. Only 2% had started by the time their child had reached the age of 6 months, and 14% started when their child was aged between 6 and 15 months; the outcomes in this group were no different to those in the 15-24 month group. Children who started toilet training after 24 months of age were more likely to have persistent daytime incontinence than those in the 15-24 month group. Since the study was not initially designed to evaluate this question, no data about toilet training at 18 months was available.An alternative conclusion from the last 2 studies might be that the parents of children with persistent incontinence had delayed toilet training because the children had not reached the appropriate developmental milestones.
Current understanding of dysfunctional voiding based on physiological principles proposes that the root cause is failure to relax the external urethral sphincter.Patients with dysfunctional voiding exhibit excessive urethral sphincter and pelvic floor activity, and it has been hypothesized that persistence of an immature stage of bladder and sphincter control is responsible.As lack of coordination between the bladder and sphincter is a normal developmental phase, the failure of a child to achieve normal coordination at 18 months of age has been proposed as a key point at which dysfunctional voiding (or non-neurogenic bladder dysfunction) could develop. A key factor in the acquisition of urinary continence that has not been studied is the age at which children gain the ability to voluntarily suppress the urge to void (the guarding reflex). This information will probably never be obtained, as children are gaining language skills at the same time that they are achieving this process so are unable to accurately communicate this. As the guarding reflex is capable of shutting off bladder contractions, dysfunctional voiding might arise because children over-learn the ability to contract the external urethral sphincter during toilet training, and never learn to relax their sphincter correctly, allowing the neonatal lack of coordination between bladder and sphincter to persist. A larger than normal bladder capacity could lead either to a high-capacity, compliant bladder with poor emptying, or a hypertrophied bladder with overactive contractions. Progressive loss of bladder sensation can occur with either of these disorders, making the child less likely to void at the proper time. No clinical studies have proved that early or late toilet training is more likely to cause urinary incontinence or dysfunctional voiding. While it is reasonable to assume that a sphincter which cannot completely relax, or a bladder that empties inefficiently are due to persistently immature sphincter and bladder function, the role that toilet training plays in this persistence remains unclear.
The persistence of childhood urinary incontinence as a cause of adult urinary incontinence has been suggested, based on retrospective surveys. As asking women with urinary incontinence to remember the severity of their childhood incontinence is subject to recall bias, prospective follow-up studies on children diagnosed with urinary incontinence into adult life would confirm this hypothesis and show if any spontaneous resolution of urinary incontinence occurs. If childhood treatment for urinary incontinence was found to prevent this morbidity in adults, it would provide additional incentive to treat during childhood.
Incontinence in Medical Disorders
A number of patient populations have difficulty achieving urinary continence as a consequence of a medical disorder or surgery. Treatment for these patients does not follow a one-size-fits-all approach, but should be specifically tailored to the individual.
Anticholinergic medications, such as oxybutynin, are commonly used to treat urinary incontinence due to bladder overactivity (cerebral palsy, posterior urethral valves) or hyperactivity (spina bifida). They act by relaxing the smooth muscle of the bladder, enabling it to store more urine at low pressures. Anticholinergic medications do not affect bladder sphincter coordination, nor do they relax the urethral sphincter. Spina Bifida
Patients with spina bifida have difficulty with bladder storage, bladder sensation, and toileting. Abnormal efferent innervation of the bladder leads to inadequate storage capacity or to high-pressure storage and emptying, which may lead to renal insufficiency and hypertension, and the abnormal afferent nerves have reduced ability to sense bladder fullness. Patients with spina bifida may also have difficulty with multistep tasks, such as intermittent catheterization for bladder emptying, or administration of an antegrade continence enema. Management of urinary continence in these patients focuses on turning the bladder into an appropriate storage organ by using anticholinergic medications, bypassing the sphincter with intermittent catheterization at safe volumes (pressures below 20 cm H2O), patient education, and continued monitoring of bowel and bladder management throughout adulthood. While there are varying degrees of urinary continence in patients with spina bifida, management of urinary incontinence is secondary to maintenance of normal renal function, and is dependent on the patient's level of function. High-functioning patients with spina bifida will likely choose surgical procedures to gain social urinary continence during adolescence so that they may achieve greater independence as adults Patients who are not able to reliably perform catheterization may remain incontinent so that their renal function is not threatened.
Posterior Urethral Valves
Posterior urethral valves (PUVs) affect boys, and are caused by an obstructing membrane in the prostatic urethra. They are often detected prenatally, but can also present as failure to toilet train in the older boy, as they prevent normal bladder emptying. Surgical management involves endoscopic ablation of the valves postnatally, and occasionally supravesical diversion. Patients with PUVs have variable bladder function after initial valve ablation, which might account for the universal delay in toilet training in these individuals. The obligate diuresis caused by poor renal concentrating ability and polyuria in patients with PUVs results in a bladder that does not appropriately signal fullness. Only 50% of patients with PUVs achieve urinary continence by 10 years of age, although there is a progressive improvement in continence as the patient reaches adulthood. Patients with an overactive bladder will require anticholinergic medication to reduce bladder pressures while maintaining adequate emptying, while patients with incomplete emptying initially use behavioral therapies such as timed voiding and double voiding to empty the bladder before additional stretch injury can occur. Patients with a flaccid bladder might need α-blockers or intermittent catheterization to overcome their inability to empty. The aim of these maneuvers is to improve the efficiency of bladder emptying, but if there is worsening hydronephrosis or an increase in serum creatinine, clean intermittent catheterization is usually started. Overnight catheter drainage is effective in improving hydronephrosis and renal function, if patient bladder control does not improve with initial behavioral therapy.
Cerebral Palsy
The main cause of urinary incontinence in children with cerebral palsy is lack of executive function, and inability to suppress the urge to void. The degree of urinary incontinence varies with cerebral palsy severity, partly due to the communication problems that exist for more severely affected patients. Approximately one-third of patients with cerebral palsy will require urologic evaluation. Medical treatment with anticholinergic medications can be successful in creating a larger functional bladder capacity. While patients with cerebral palsy can sense a full bladder, they might have difficulty expressing the sensation clearly to their caregivers. In an approach similar to that taken with infant toilet training, understanding how the child expresses his or her sensation of bladder fullness is important, so that they can get to a toilet in time. Limb weakness, spasticity, and tendon contractures can make it difficult for patients with cerebral palsy to toilet independently, and family members and caregivers should be given a realistic idea of what level of urinary continence the patient is capable of achieving. A child can sometimes be dry at home when the parents are able to rapidly get them to a toilet, but be wet at school because the number of children per caregiver is higher. Urinary incontinence may persist into adult life in some patients.
Autism
Children with autism are extremely challenging to toilet train. While their bladder storage and emptying function should be normal, their individual response to bladder filling is unpredictable. Some children have sensory issues, and find the sensation of bladder contraction unbearable; these patients might require anticholinergic medications to increase the interval between voiding. Others might completely ignore the signals from their bladder and wet themselves because their attention is focused elsewhere. The system of timed and double voiding that works well in patients with PUVs can be difficult to implement in a child with autism, if he or she finds the sounds and smells of the bathroom disturbing. Although the literature in this area is scant, the structured Foxx-Azrin child-centered approach to toilet training seems to be most successful in achieving urinary continence in children with autism. Success in achieving toilet training is variable in children with autism, and is dependent on both the severity and type.
Conclusions
The age at which children successfully achieve urinary continence can be affected by many factors, including parental expectations, developmental stage of the child, and medical disorders. The optimum age for toilet training is still uncertain. No trial has compared different methods of toilet training, nor have studies told us when the optimum time for toilet training should be. Longitudinal studies reflect the current practices of toilet training, rather than comparing different methods or timings. Early toilet training has obvious benefits, but requires an investment of time, along with cultural norms that do not require children to void in a toilet. The experience of early toilet training in non-Western cultures suggests that it can be done successfully, although long-term outcomes of urinary continence are not reported. Toilet training after 18 months of age in Western cultures minimizes the length of training by starting when a child has met certain developmental milestones, but is dependent on convenience factors, such as the availability of cheap, disposable diapers, or suitable washing facilities for soiled clothing and diapers.
A child's bladder and sphincter function show increased maturity at approximately 18 months of age, but whether toilet training should occur before or after this milestone remains unclear. Available data suggest that toilet training is easier to achieve when the bladder is more stable and the brain is capable of making the bladder and sphincter work in concert; the timing of voluntary control over voiding is also difficult to change.
As parents from all cultures find toilet training a challenge, our most appropriate approach as physicians might be to first identify the parents' expectations of toilet training and then discuss a toilet training regimen based on the available knowledge and methods that best fit the parents and child. Information on various toilet training methods can be provided to enable the parents to estimate how long the process will take, and what obstacles will be encountered. There is not enough available information to determine how long infant toilet training should take, aside from the expectation that it should be accomplished by the age of 6-12 months. No evidence exists that it is harmful to begin toilet training early, as long as the parents are willing to invest the time in doing so. If early toilet training is undertaken, the child will still need to learn the skills associated with independent toileting at the age of 2-3 years. If the parents prefer to wait until the child is older, and implement a method that allows the child to be completely independent in terms of toileting, then assessment of the child's developmental milestones and interest in toilet training is a good place to start. If the parents discover that their child is having significant difficulty with toilet training, then the ability of the parents to understand and implement their chosen method of toilet training should be evaluated, and the child should be examined to rule out the presence of any medical conditions that may delay toilet training.
Further investigation into the transition from immature to mature bladder function in neonatal animals may determine the mechanisms which delay the acquisition of urinary continence in children with medical disorders. Long-term evaluation of bladder function in children trained as infants, at 18 months, or later, will eventually prove or disprove the hypothesis that late toilet training is creating a generation of children with urinary incontinence. While it is tempting to attribute success in toilet training purely to the time and method chosen, the child's personality and physiological readiness to toilet train will also clearly affect how long the process will take.
Abstract
Achievement of urinary continence is an important developmental step that most children attain with the assistance of their parents and caregivers. Debate continues as to the best time to toilet train; in some Asian and African cultures children are trained as infants, while training at age 2-3 years is more typical in Western cultures. Infant voiding is not merely a spinal reflex, as the sensation of bladder filling is relayed to the brain. However, the ability of the brain to inhibit bladder contractions, and to achieve coordinated bladder contraction with sphincter relaxation, matures over time. While there is a concern that later toilet training may be responsible for an increase in urinary incontinence in children, no controlled studies on early versus late toilet training exist to evaluate this hypothesis. A number of medical conditions such as spina bifida, posterior urethral valves, cerebral palsy and autism can cause incontinence and difficulties in toilet training. The decision to start toilet training a child should take into account both the parents' expectation of how independent the child will be in terms of toileting, and the child's developmental readiness, so that a realistic time course for toilet training can be implemented.
Introduction
Toilet training is an important step for both children and parents, because it transitions the child to a more independent stage of life. The great majority of children and parents accomplish this without significant input from physicians, relying on practices that may be culturally determined, discussed in parenting magazines and books, or available on the Internet. Parents faced with a child that does not successfully toilet train often seek guidance from their pediatrician or primary care physician on the readiness of the child to begin toilet training, and how best to accomplish this successfully. Recommendations in western medical literature commonly rely on guidelines published by the American Academy of Pediatrics (AAP) in 1999, outlining the roles of parents, clinicians, and day-care providers in the process of toilet training. Studies performed in the 2000s indicate that the prevalence of urinary incontinence in children is approximately 6-9%. If the primary care physician is unable to determine a neurologic or metabolic cause for urinary incontinence (such as tethered spinal cord or diabetes insipidus), the child is usually referred to a pediatric urologist.
Parents seeking advice on toilet training their infant or toddler are faced with multiple options. Do they take the 'infant toilet training' approach, and pay close attention to their infant, positioning the child over the toilet or sink when he or she makes the tell-tale sign or noise that they need to urinate or defecate? Do they put the child on the toilet for a few minutes after each meal? Do they go along with standard medical recommendations, and wait until their child is 2 or 3 years old, leaving the child in diapers until then? Much of this information is dependent on cultural norms. Grandparents from non-Western cultures might remind parents that they were themselves toilet trained at a young age, using a variation of the first technique. While the 'infant toilet training' approach has received increased media attention in the past 5 years, it is still infrequently practiced in the US, and is not discussed in published guidelines from medical societies. Such anecdotes raise the question of whether the current recommendation to delay toilet training, based on the AAP guidelines, is a cultural practice, or if it is supported by scientific evidence. Changes in childcare over the past 50 years have complicated the process of toilet training, as it now involves both parents and childcare providers, who may use different approaches to toilet training. Some day-care providers require that a child be toilet trained before starting, reflecting the fact that the staffing ratio of care providers to children does not allow the same number of diaper changes that would be carried out at home. Therefore, the economics of childcare can also affect when parents start to toilet train their children.
This Review will focus on the achievement of urinary continence in children. The optimum age for toilet training will be discussed, using examples of variations in method between Western and non-Western cultures. This Review will also provide an overview of bladder function and voiding mechanisms in the infant and young child, will discuss factors in dysfunctional voiding, reviewing the hypothesis that delaying the age of toilet training may paradoxically cause urinary incontinence in children, and will overview medical disorders that may cause difficulty in achieving urinary continence
Urinary Continence
The narrowest definition of urinary continence in a child would be merely the avoidance of unexpected voiding. From this viewpoint, an infant is capable of urinary continence if the caregiver is able to recognize when the infant needs to urinate. Some critics have called this "a reflex conditioning of the mother", a comment which reflects the reality that infant toilet training is time intensive and requires the continuous presence of a parent or caregiver. A broader definition, which is probably more in line with the expectations of parents and physicians, would include the ability of the child to sense when the bladder is full, inhibit the urge to urinate until a socially acceptable time and location, and independently use the toilet. This is the definition of urinary continence which will be used in this article. As this definition of continence requires that the child show significant communication, motor, and decision-making skills, toilet training to achieve these goals depends not only on the maturity of the central nervous system and bladder to store, detect and empty urine, but also on the child's overall development.
Toilet Training
Toilet training is the process of achieving both urinary and stool continence. Infant (less than 1 year old) or early toilet training is not directly comparable with late toilet training (children aged 18 months or over), since both the timing and expected outcome are different. In early toilet training, the goal is to learn when the child needs to void, so that he or she can be brought to the toilet, while the goal of late toilet training is for the child to be completely independent in the entire process of toileting. In the late 19th century, infant toilet training using mechanical stimulants such as soap or laxatives, or rectal stimulation, was popular in the US. The preference for late toilet training returned in the 1930s when concerns were raised about relapses back to incontinence following early toilet training. A 1962 paper by Brazleton and a 1974 book by Foxx and Azrin both emphasized the value of starting toilet training when the child was developmentally ready (known as the 'child-centered approach'), which laid the foundations for the current recommendation to wait until the child is at least 18 months old before starting toilet training, as by this age the child is able to relay the sensation of bladder fullness to their parent. The Foxx-Azrin approach is more intensive and structured than that of Brazleton, and begins with demonstration of toileting to the child using a doll, followed by increased fluid intake and scheduled toilet times. Correct behavior is reinforced with rewards such as food, hugs and toys, while accidents are over-corrected by verbal reprimand, loss of reinforcements, and additional practice sessions. The Brazleton approach begins by sitting the child on the potty clothed, followed by sitting without a diaper. Stool and urine are emptied into the potty, explaining to the child that this is where they go; the final stage is independent use of the potty by the child. Foxx and Azrin reported that continence can be achieved in 4 h in appropriately selected children, while children who are toilet trained using the Brazleton approach appear to take between 6 and 18 months to achieve urinary continence.
Retrospective questionnaires investigating age at toilet training are subject to significant recall bias; the best data from Western countries come from two longitudinal cohort studies performed in Switzerland in the late 1950s and the 1970s. In these studies, stool continence was achieved first at the age of 3 years in 97% of the group, followed by daytime urinary continence in 97% of the group by the age of 6 years, and finally night-time urinary continence. In total, 90% of boys and 94% of girls had achieved complete night-time urinary continence by the age of 6 years. Although toilet training was started at 6-12 months of age in the 1950s cohort, and 12-18 months of age in the 1970s cohort, daytime urinary continence was achieved in 90% of both groups by 4 years of age, and 97% of both groups by 6 years of age. These results were replicated in another longitudinal cohort of children born in 1952, from Baltimore in the USA, with exactly the same percentages seen at the same ages. Nowadays, completion of toilet training before starting kindergarten at approximately 5 years of age would be considered a normal age in children. A more recent prospective study using the child-centered approach in middle class families was conducted in 2003. Children were recruited between 17 and 19 months of age, and parents began toilet training them at a mean age of 29 months. Children who started toilet training before 27 months of age achieved urinary continence at the same time as those who started after 27 months; an average of 37 months.
Many Asian, African, and South American countries show a cultural preference for early toilet training of infants, but other than case reports, no data on age of completion of toilet training and urinary incontinence are available. The most quoted paper in this context describes the toilet training practices of the Digo people of Kenya. These practices are similar to infant toilet training, with the expectation of daytime and nighttime urinary continence by 6 months of age. The mother positions the child between her legs and makes a "shuus" sound that the child learns to link with urinating. Mothers are able to tell that their child is ready to urinate based on the sounds and movements made by the child. This approach combines a stimulus (sound) with the conditioned response (urination), assisted by the mother's perception of when the child needs to void. The authors note that cultural acceptance of public urination, uncumbersome clothes, and the ability of the mother to spend the entirety of the first 2 months of the child's life with her infant contribute to the success of this approach. A study from Vietnam suggests that infant toilet training results in a decreased postvoid residual volume by 9 months, which may indicate that infants can empty their bladders more efficiently if toilet training is undertaken. If this initial finding can be confirmed in other populations, it could indicate that early toilet training might be an important tool for children with anatomical abnormalities such as vesicoureteral reflux, which put them at higher risk for urinary tract infection. Longer-term follow-up on participants who undergo infant toilet training is not currently available.
If one considers the three-part definition of continence outlined earlier (sensing a full bladder; inhibiting the urge to urinate until socially acceptable; and independent use of the toilet or potty), a combination of developmental skills indicate when a child is ready to be toilet trained. Generally, not having bowel movements at night, noticing the urge to void or to pass stool, communicating the need to go to the toilet, being dry for periods of at least 2 h, and waking up dry from a nap, are prerequisites in a child-centered approach to toilet training. These skills are achieved at a median of 22 months in girls, and at 25 months in boys, when they become continent of stool at night. The AAP recommends that toilet training can be started when the child is aged 18 months, but children will reach these developmental milestones at different times; girls acquire almost all the developmental skills related to toilet training at an earlier age than boys.
The role of stress and behavior in toilet training was studied in a group of children aged 4 years or older, who were unsuccessful at toilet training for more than 6 months, or who refused to use the toilet. Although parenting styles (laxness, verbosity, over-reactivity) were not different between the difficult to train and control groups, children who were characterized as difficult personalities by behavioral questionnaire (less adaptable, negative mood, less persistent) were more likely to be difficult to toilet train. Parental stress (isolation, depression, spousal relationship issues) does not seem to influence the age of the child on toilet training, but refusal to stool in a toilet, constipation, and hiding when defecating are more frequent in children who toilet trained after 42 months of age
Bladder Function and Voiding Mechanisms
The natural history of infant bladder function was first systematically studied in the 1990s using free voiding studies and urodynamics. The human neonate initially voids small amounts, about once an hour. Bladder capacity increases in two growth spurts: the first at birth, the second at 3 years of age. Neonates were previously believed to urinate while sleeping as well as when awake, suggesting that a local sacral reflex was responsible for emptying the bladder. However, analysis of neonatal electroencephalography tracings suggests that most neonates experience some arousal before voiding, indicating that the brain is always involved when the bladder empties. Infants experience interrupted (or incomplete) voiding as a result of lack of coordination between the bladder and the external sphincter, which causes elevated voiding pressures until the child reaches the age of 18 months. At 1 week of age, boys void with mean detrusor pressures of 117 cm H2O, and girls with pressures of 75 cm H2O.The traditional belief that the urinary frequency seen in the infant bladder was due to overactivity was disproved by the rarity of overactive contractions observed during studies of infant urodynamics carried out in asymptomatic children.
The high bladder pressures and progressive control of the bladder by the brain in the human infant matches that of the neonatal rat, allowing a great degree of translation from experimental animal findings to humans. It is not ethically possible to obtain bladder tissue from healthy human infants or interfere with their neural maturation, therefore much of what we understand about the neonatal bladder is derived from experimental models. Neonatal cats, rats, and mice are unable to void spontaneously, and are dependent on their mother to lick the perigenital area to cause the bladder to empty. By 3 weeks of age, when they are weaned, neonatal rats are able to void spontaneously in response to bladder filling. At first glance, these findings suggest that the neonatal nervous system is not mature enough for animals to void spontaneously. As the perigenital-bladder reflex reemerges after spinal cord injury, however, and bladder emptying in response to filling can occur in neonatal rats if the forebrain is disconnected from the brainstem, the perigenital reflex actually inhibits the mature bladder emptying reflex. This inhibition is removed at the time of weaning, allowing the rat to void spontaneously. Experimental bladder distension similarly results in the onset of spontaneous voiding at 3 weeks, but prolongs the perigenital reflex for another 2 weeks. Surgical reduction of bladder volume causes the immediate onset of spontaneous voiding in neonatal rats, and results in a long-term increase in bladder capacity and lower voiding pressures. These findings suggest that coordination between the bladder and sphincter requires maturation of central neural control, and that peripheral nervous system connections are ready for use at birth.
While human infants do not exhibit the perigenital reflex, they will void in response to stroking of the paravertebral muscles until 2 months of age.Perhaps infant toilet training activates a primitive bladder emptying reflex via stimuli provided by the mother, while the mature bladder emptying reflex in response to filling requires control exerted by the child's forebrain. Previously, neonatal bladder emptying was thought to only involve an isolated sacral spinal cord reflex, but animal data suggest that bladder emptying in neonates involves descending control from the forebrain to the brainstem, all the way down to the bladder.
The other key finding from animal studies is that neonatal bladder smooth muscle functions differently to that in older juvenile animals and children. Animal study findings indicate that the neonatal bladder produces more pressure per gram of tissue, is more dependent on local calcium levels, and has large-amplitude spontaneous contractions, which become downregulated with maturation.The elevated voiding pressures seen in infants may therefore also represent immature smooth muscle function. The neonatal bladder empties well, but does not store well in both rats and humans. The spontaneous contractions observed in the neonatal rat bladder occur only when central regulation of the bladder is removed, suggesting that the brain exerts a tonic inhibition on the bladder. In children, a high-capacity bladder and small postvoid residual volume seem to predict earlier completion of toilet training, which likely means that central control of the bladder is more effective when the bladder demonstrates mature smooth muscle function
Urinary Incontinence
A comparison of different toilet training methods and timings has suggested that the modern trend for late toilet training may have caused an increase in the diagnosis of urinary incontinence. It is unclear whether we are diagnosing urinary incontinence more commonly because we are more aware of it, if urinary incontinence and late toilet training are both increasing but unrelated, or if late toilet training is a cause of urinary incontinence. In these studies, children with persistent daytime and night-time incontinence had begun toilet training at an older age (greater than 18-24 months) than the children who were dry. Limitations of these studies included retrospective design,and a varying definition of late toilet training (age greater than 18 months, or age greater than 24 months) between studies. A retrospective survey of schoolchildren at a mean age of 11.5 years found that children with daytime urinary incontinence tended to start toilet training 6 months later than those without, although the median age for starting toilet training in both groups was 18-24 months. A prospective study designed to investigate environmental effects on children's health was reanalyzed to evaluate the age that toilet training was initiated, which was then compared with the child's daytime continence at 9 years of age. 50% of parents in the study reported starting toilet training when their child was between 15 and 24 months of age. Only 2% had started by the time their child had reached the age of 6 months, and 14% started when their child was aged between 6 and 15 months; the outcomes in this group were no different to those in the 15-24 month group. Children who started toilet training after 24 months of age were more likely to have persistent daytime incontinence than those in the 15-24 month group. Since the study was not initially designed to evaluate this question, no data about toilet training at 18 months was available.An alternative conclusion from the last 2 studies might be that the parents of children with persistent incontinence had delayed toilet training because the children had not reached the appropriate developmental milestones.
Current understanding of dysfunctional voiding based on physiological principles proposes that the root cause is failure to relax the external urethral sphincter.Patients with dysfunctional voiding exhibit excessive urethral sphincter and pelvic floor activity, and it has been hypothesized that persistence of an immature stage of bladder and sphincter control is responsible.As lack of coordination between the bladder and sphincter is a normal developmental phase, the failure of a child to achieve normal coordination at 18 months of age has been proposed as a key point at which dysfunctional voiding (or non-neurogenic bladder dysfunction) could develop. A key factor in the acquisition of urinary continence that has not been studied is the age at which children gain the ability to voluntarily suppress the urge to void (the guarding reflex). This information will probably never be obtained, as children are gaining language skills at the same time that they are achieving this process so are unable to accurately communicate this. As the guarding reflex is capable of shutting off bladder contractions, dysfunctional voiding might arise because children over-learn the ability to contract the external urethral sphincter during toilet training, and never learn to relax their sphincter correctly, allowing the neonatal lack of coordination between bladder and sphincter to persist. A larger than normal bladder capacity could lead either to a high-capacity, compliant bladder with poor emptying, or a hypertrophied bladder with overactive contractions. Progressive loss of bladder sensation can occur with either of these disorders, making the child less likely to void at the proper time. No clinical studies have proved that early or late toilet training is more likely to cause urinary incontinence or dysfunctional voiding. While it is reasonable to assume that a sphincter which cannot completely relax, or a bladder that empties inefficiently are due to persistently immature sphincter and bladder function, the role that toilet training plays in this persistence remains unclear.
The persistence of childhood urinary incontinence as a cause of adult urinary incontinence has been suggested, based on retrospective surveys. As asking women with urinary incontinence to remember the severity of their childhood incontinence is subject to recall bias, prospective follow-up studies on children diagnosed with urinary incontinence into adult life would confirm this hypothesis and show if any spontaneous resolution of urinary incontinence occurs. If childhood treatment for urinary incontinence was found to prevent this morbidity in adults, it would provide additional incentive to treat during childhood.
Incontinence in Medical Disorders
A number of patient populations have difficulty achieving urinary continence as a consequence of a medical disorder or surgery. Treatment for these patients does not follow a one-size-fits-all approach, but should be specifically tailored to the individual.
Anticholinergic medications, such as oxybutynin, are commonly used to treat urinary incontinence due to bladder overactivity (cerebral palsy, posterior urethral valves) or hyperactivity (spina bifida). They act by relaxing the smooth muscle of the bladder, enabling it to store more urine at low pressures. Anticholinergic medications do not affect bladder sphincter coordination, nor do they relax the urethral sphincter. Spina Bifida
Patients with spina bifida have difficulty with bladder storage, bladder sensation, and toileting. Abnormal efferent innervation of the bladder leads to inadequate storage capacity or to high-pressure storage and emptying, which may lead to renal insufficiency and hypertension, and the abnormal afferent nerves have reduced ability to sense bladder fullness. Patients with spina bifida may also have difficulty with multistep tasks, such as intermittent catheterization for bladder emptying, or administration of an antegrade continence enema. Management of urinary continence in these patients focuses on turning the bladder into an appropriate storage organ by using anticholinergic medications, bypassing the sphincter with intermittent catheterization at safe volumes (pressures below 20 cm H2O), patient education, and continued monitoring of bowel and bladder management throughout adulthood. While there are varying degrees of urinary continence in patients with spina bifida, management of urinary incontinence is secondary to maintenance of normal renal function, and is dependent on the patient's level of function. High-functioning patients with spina bifida will likely choose surgical procedures to gain social urinary continence during adolescence so that they may achieve greater independence as adults Patients who are not able to reliably perform catheterization may remain incontinent so that their renal function is not threatened.
Posterior Urethral Valves
Posterior urethral valves (PUVs) affect boys, and are caused by an obstructing membrane in the prostatic urethra. They are often detected prenatally, but can also present as failure to toilet train in the older boy, as they prevent normal bladder emptying. Surgical management involves endoscopic ablation of the valves postnatally, and occasionally supravesical diversion. Patients with PUVs have variable bladder function after initial valve ablation, which might account for the universal delay in toilet training in these individuals. The obligate diuresis caused by poor renal concentrating ability and polyuria in patients with PUVs results in a bladder that does not appropriately signal fullness. Only 50% of patients with PUVs achieve urinary continence by 10 years of age, although there is a progressive improvement in continence as the patient reaches adulthood. Patients with an overactive bladder will require anticholinergic medication to reduce bladder pressures while maintaining adequate emptying, while patients with incomplete emptying initially use behavioral therapies such as timed voiding and double voiding to empty the bladder before additional stretch injury can occur. Patients with a flaccid bladder might need α-blockers or intermittent catheterization to overcome their inability to empty. The aim of these maneuvers is to improve the efficiency of bladder emptying, but if there is worsening hydronephrosis or an increase in serum creatinine, clean intermittent catheterization is usually started. Overnight catheter drainage is effective in improving hydronephrosis and renal function, if patient bladder control does not improve with initial behavioral therapy.
Cerebral Palsy
The main cause of urinary incontinence in children with cerebral palsy is lack of executive function, and inability to suppress the urge to void. The degree of urinary incontinence varies with cerebral palsy severity, partly due to the communication problems that exist for more severely affected patients. Approximately one-third of patients with cerebral palsy will require urologic evaluation. Medical treatment with anticholinergic medications can be successful in creating a larger functional bladder capacity. While patients with cerebral palsy can sense a full bladder, they might have difficulty expressing the sensation clearly to their caregivers. In an approach similar to that taken with infant toilet training, understanding how the child expresses his or her sensation of bladder fullness is important, so that they can get to a toilet in time. Limb weakness, spasticity, and tendon contractures can make it difficult for patients with cerebral palsy to toilet independently, and family members and caregivers should be given a realistic idea of what level of urinary continence the patient is capable of achieving. A child can sometimes be dry at home when the parents are able to rapidly get them to a toilet, but be wet at school because the number of children per caregiver is higher. Urinary incontinence may persist into adult life in some patients.
Autism
Children with autism are extremely challenging to toilet train. While their bladder storage and emptying function should be normal, their individual response to bladder filling is unpredictable. Some children have sensory issues, and find the sensation of bladder contraction unbearable; these patients might require anticholinergic medications to increase the interval between voiding. Others might completely ignore the signals from their bladder and wet themselves because their attention is focused elsewhere. The system of timed and double voiding that works well in patients with PUVs can be difficult to implement in a child with autism, if he or she finds the sounds and smells of the bathroom disturbing. Although the literature in this area is scant, the structured Foxx-Azrin child-centered approach to toilet training seems to be most successful in achieving urinary continence in children with autism. Success in achieving toilet training is variable in children with autism, and is dependent on both the severity and type.
Conclusions
The age at which children successfully achieve urinary continence can be affected by many factors, including parental expectations, developmental stage of the child, and medical disorders. The optimum age for toilet training is still uncertain. No trial has compared different methods of toilet training, nor have studies told us when the optimum time for toilet training should be. Longitudinal studies reflect the current practices of toilet training, rather than comparing different methods or timings. Early toilet training has obvious benefits, but requires an investment of time, along with cultural norms that do not require children to void in a toilet. The experience of early toilet training in non-Western cultures suggests that it can be done successfully, although long-term outcomes of urinary continence are not reported. Toilet training after 18 months of age in Western cultures minimizes the length of training by starting when a child has met certain developmental milestones, but is dependent on convenience factors, such as the availability of cheap, disposable diapers, or suitable washing facilities for soiled clothing and diapers.
A child's bladder and sphincter function show increased maturity at approximately 18 months of age, but whether toilet training should occur before or after this milestone remains unclear. Available data suggest that toilet training is easier to achieve when the bladder is more stable and the brain is capable of making the bladder and sphincter work in concert; the timing of voluntary control over voiding is also difficult to change.
As parents from all cultures find toilet training a challenge, our most appropriate approach as physicians might be to first identify the parents' expectations of toilet training and then discuss a toilet training regimen based on the available knowledge and methods that best fit the parents and child. Information on various toilet training methods can be provided to enable the parents to estimate how long the process will take, and what obstacles will be encountered. There is not enough available information to determine how long infant toilet training should take, aside from the expectation that it should be accomplished by the age of 6-12 months. No evidence exists that it is harmful to begin toilet training early, as long as the parents are willing to invest the time in doing so. If early toilet training is undertaken, the child will still need to learn the skills associated with independent toileting at the age of 2-3 years. If the parents prefer to wait until the child is older, and implement a method that allows the child to be completely independent in terms of toileting, then assessment of the child's developmental milestones and interest in toilet training is a good place to start. If the parents discover that their child is having significant difficulty with toilet training, then the ability of the parents to understand and implement their chosen method of toilet training should be evaluated, and the child should be examined to rule out the presence of any medical conditions that may delay toilet training.
Further investigation into the transition from immature to mature bladder function in neonatal animals may determine the mechanisms which delay the acquisition of urinary continence in children with medical disorders. Long-term evaluation of bladder function in children trained as infants, at 18 months, or later, will eventually prove or disprove the hypothesis that late toilet training is creating a generation of children with urinary incontinence. While it is tempting to attribute success in toilet training purely to the time and method chosen, the child's personality and physiological readiness to toilet train will also clearly affect how long the process will take.
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