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PEDIATRIC UROLOGY

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DEVELOPMENT OF NOCTURNAL URINARY CONTROL INCHINESE CHILDREN YOUNGER THAN 8 YEARS OLD

JIAN GUO WEN, QING WEI WANG, JIAN JUN WEN, JING SU, YUE CHEN,KUI LIU, AND HE YING YANG

ABSTRACTbjectives. To estimate the development of nocturnal urinary control (NUC) with age in Chinese childrenounger than 8 years of age using cross-sectional and retrospective surveys.ethods. We used a cross-sectional survey of 4754 children (1 to 8 years old), a retrospective investigation

f 2745 children younger than 9 years old, and an anonymous questionnaire of 8222 children 9 to 18 yearsld . The children without NUC were subdivided into infant (1 to 3 years old), preschool age (4 to 6 years old),nd primary school (7 to 8 years old) groups.esults. The response rate to the cross-sectional and retrospective surveys was 90% and 89%, respec-

ively. In the cross-sectional survey, the prevalence of children attaining NUC was 52% for those youngerhan 2 years of age, 76% for those aged 2 to 3 years, and 93% at age 8. Girls were more likely than boyso acquire NUC earlier. In the retrospective survey, the prevalence of children attaining NUC before age 2as 17% and was 72% for those aged 2 to 3 years, and 98% by age 8. The proportion of nonmonosymp-

omatic bedwettings in children without NUC was 14%. Arousal difficulty and a positive family history wereound in 67% and 11% of children with nocturnal wetting, respectively. The severity of bedwetting androusal difficulty was significantly greater in infants than in preschool and school-age children.onclusions. The results from the cross-sectional and retrospective surveys showed that the most impor-ant period of attaining NUC is 2 to 3 years of age. Nearly 90% of children attained NUC by the age of. UROLOGY 68: 1103–1108, 2006. © 2006 Elsevier Inc.

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octurnal bedwetting is one of the most com-mon developmental disorders among chil-

ren, and attaining nocturnal urinary controlNUC) is a social milestone in a child’s develop-ent. A delay in attaining NUC often causes sec-

ndary emotional and social problems such asdolescent suicidal behavior.1–3 However, fewpidemiologic studies have been done on the rela-ionship between age and NUC in young children,

his study was supported by the Innovation and Talent Researchoundation of Henan Province China (grant 022-100-2000),enan Innovation Project for University Prominent Researchalents (grant 2001KYCX004), and National Natural Scienceoundation of China (grant 30571931).From the Department of Pediatric Surgery, Pediatric Urody-

amic Centre, First Affiliated Hospital of Zhengzhou University,hengzhou City, Henan, China; and Institute of Clinical Medicalesearch, Henan University, Zhengzhou City, Henan, ChinaReprint requests: Jian Guo Wen, M.D., Ph.D., Pediatric Urody-

amic Centre and Clinical Medical Research Institute, First Af-liated Hospital of Zhengzhou University, Zhengzhou, 450052,hina. E-mail: jgwen@zzu.edu.cnSubmitted: November 4, 2005, accepted (with revisions): June

t5, 2006

2006 ELSEVIER INC.LL RIGHTS RESERVED

specially during the most important stage, beforeyears of age. Extensive studies on the types and

everity of nocturnal wetting are limited. Further-ore, because bedwetting is generally considered

mbarrassing, children who wet the bed (andometimes their parents) are often too shy to tellhe truth during a survey, making it difficult to getccurate information. It is possible that a retro-pective survey could overcome such disadvan-ages and provide more accurate information onhe prevalence of nocturnal bedwetting.4

Differences in toilet training in the early agesetween China and Western countries have beenoted.5 For example, in China, young children of-en sleep with their parents; the mother immedi-tely wakes up the child to void when the childhows dysphoria because of bladder fullness. Also,diaper is often not used after children begin toalk on their own when it is feasible to void inublic areas. These factors, different from those ofestern countries, may play a role in the early

raining of voiding. Therefore, we believed it

0090-4295/06/$32.00doi:10.1016/j.urology.2006.06.030 1103

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ould be valuable to compare the data from Chinaith the data from a Western country.The present study was designed to estimate the

evelopment of NUC by investigating the relation-hip between the attainment of NUC and age inhinese children younger than 8 years old and toiscriminate the factors influencing the attainmentf NUC using cross-sectional and retrospectiveurveys and an anonymous questionnaire. Weoped this would provide valuable insights intohe mechanism of the normal development of NUCn Chinese children.

MATERIAL AND METHODS

From July 2003 to December 2004, an epidemiologic surveyn the attainment of NUC was performed throughout Henanrovince in China. The procedures used in this study were theame as in our previous studies.6 In brief, seven districts cov-ring 13 primary schools, 10 junior high schools, and 9 seniorigh schools were randomly sampled. A self-administerednonymous questionnaire was used that consisted of threeections. The first section was used to document the back-round data. The second section asked about the rate of noc-urnal continence. A sample question was “Has your childttained NUC (with no bedwetting) during the past month?”f the answer to this question was “Yes,” the parents weresked to write down the date at which their child ceased wet-ing the bed at night (a dry period of at least 1 month up to thenvestigation period without relapse was defined as the attain-

ent of NUC). If the answer was “No,” the parents were in-tructed to answer the third section, which included five ques-ions: the frequency of nocturnal bedwetting; whether thehild had nonmonosymptomatic bedwetting (bedwetting as-ociated with multiple daytime lower urinary tract symptoms,ncluding frequency, urgency, and incontinence); arousal dif-culty (ie, the child could not wake up during or after wettinghe bed at night); management strategy; and family history ofocturnal bedwetting.The questionnaire was distributed with an explanation let-

er by the investigators (medical doctor and medical postgrad-ates) who had been trained to administer medical epidemio-

ogic surveys. The explanation letter informed the parents ofhe purpose of the survey and the meaning of terms on theuestionnaire and offered an opportunity for a free consulta-ion on NUC. All questionnaires were answered by the parentsnd returned to the investigator. Because the questionnaireas given anonymously, it protected the privacy of the chil-ren and families who might face societal pressures becausef a failure to attain NUC. Thus, it minimized the possibletigma/embarrassment to those children and their families.

The obtainment of NUC was defined as the child crying oruddenly moving a leg, arm, or the body during sound sleepust before the voiding and the parents waking up and helpinghe child to void. In contrast, nonobtainment of NUC wasefined as the child who continued to sleep during and afteroiding.

A cross-sectional survey was performed by distributing theurvey to 4754 children aged 1 to 8 years. The response rateas 90% (4279 of 4754). Also, 2745 children younger than 9ears old and 8222 children aged 9 to 18 years old who hadttained NUC were investigated retrospectively. The responseate for the latter was 89% (7318 of 8222). Therefore, retro-pective investigation data were obtained from surveys distrib-ted to 10,967 (2745 plus 8222) children aged 1 to 18 yearsho had attained NUC.

The children younger than 8 years old in the cross-sectional a

104

urvey were further subdivided into three groups according tohe different educational stages of children in China: infantroup (1 to 3 years old, generally stayed home with parents orrandparents or babysitter), preschool/kindergarten group (4o 6 years old), and primary school group (7 to 8 years old).his grouping strategy made it easier to determine the rela-

ionship between the development of NUC and the social lifef the children.Statistical analyses were done using the Statistical Package

or Social Sciences, version 11.0, for Windows (SPSS, Chicago,ll). The chi-square test was used to determine the factorsnfluencing the attainment of NUC. The Cochran-Armitagerend test was used to evaluate the trend between the attain-ent of NUC and age. P values less than 0.05 were considered

tatistically significant. The incidence of NUC attainment inhe cross-sectional and retrospective surveys was calculatedeparately.

RESULTS

The prevalence of the children attaining NUC inhe cross-sectional and retrospective surveys ishown in Tables I and II, respectively. The datahowed that the prevalence of NUC in the cross-ectional survey was greater before age 4 and lowerfter age 5 than that in the retrospective investiga-ion. In the cross-sectional survey, a significantrend was noted for an increasing attainment ofUC between 1 and 8 years of age (chi-square �06.687, P �0.05 for boys and chi-square �12.424, P �0.05 for girls). The influencing fac-ors of the children without NUC attainment arehown in Table III.

COMMENT

The ability to attain NUC increases with age, es-ecially for those younger than 8 years old.7 Fee-an et al.8 reported in 1990 on 1139 children born

n the same year in Dunedin and found an im-rovement in 92% of them followed up for 6 yearsnd that bedwetting usually resolved with age at aate of around 15% annually. Another studyhowed that bedwetting resolved, on average, by.5 to 3.5 years of age.9 The present study has dem-nstrated results similar to those from studies fromther Asian countries, but the prevalence of NUCttainment was greater than that in studies from

estern countries. The fastest development of uri-ary control was found between the ages of 2 and 3ears, and most children had attained NUC by age. The overall prevalence among girls was signifi-antly greater than that among boys, indicatinghat growth development is faster in girls than inoys.Because bedwetting is embarrassing for the child

nd family, the cross-sectional survey was subjecto bias because of the subjectiveness (dishonesty)f the parents when they answered the question-aire. To overcome this disadvantage, we used an

nonymous questionnaire. Even so, our cross-sec-

UROLOGY 68 (5), 2006

TABLE I. Prevalence of children attaining NUC on cross-sectional survey

Group(Age [yr])

Boys* Girls† Total

Chi-square P Value‡Responded

(n)AttainedNUC (n) % (95% CI)

Responded(n)

AttainedNUC (n) % (95% CI)

Responded(n)

AttainedNUC (n) % (95% CI)

Infants1 74 40 54.05 (42.70–65.41) 70 35 50.00 (38.29–61.71) 144 75 52.08 (43.92–60.24) 0.237 0.6262 147 105 71.43 (64.13–78.74) 128 89 69.53 (61.56–77.51) 275 194 70.55 (65.16–75.93) 0.119 0.7313 295 215 72.88 (67.81–77.95) 266 210 78.95 (74.05–83.85) 561 425 75.76 (72.21–79.30) 2.802 0.094

Preschool4 318 266 83.65 (79.58–87.71) 378 330 87.30 (83.95–90.66) 696 596 85.63 (83.03–88.24) 1.874 0.1715 313 270 86.26 (82.45–90.08) 287 259 90.24 (86.81–93.68) 600 529 88.17 (85.58–90.75) 2.275 0.1316 421 375 89.01 (86.09–92.05) 371 337 90.84 (87.90–93.77) 792 712 89.90 (87.80–92.00) 0.674 0.412

Primaryschool7 278 256 92.08 (88.91–95.26) 280 255 91.07 (87.73–94.41) 558 511 91.58 (89.27–93.88) 0.186 0.6668 311 284 91.32 (88.19–94.45) 342 323 94.44 (92.02–96.87) 653 607 92.96 (90.99–94.92) 2.431 0.119

Total 2157 1811 83.96 (82.41–85.51) 2122 1838 86.62 (85.17–88.07) 4279 3649 85.28 (84.22–86.34) 6.015 0.014

KEY: NUC � nocturnal urinary control.* P � 0.001 with Cochran-Armitage trend test (chi-square � 106.687) on prevalence of Chinese boys with NUC attainment in different age groups.† P � 0.001 with Cochran-Armitage trend test (chi-square � 112.424) on prevalence of Chinese girls with NUC attainment in the different age groups.‡ Significance with chi-square test on prevalence of bedwetting between boys and girls in different age groups.

TABLE II. Prevalence of children attaining NUC on retrospective investigation

Age (yr)

Boys Girls Total

Responded(n) Percentage

AccumulativePercentage

Responded(n) Percentage

AccumulativePercentage

Responded(n) Percentage

AccumulativePercentage

1 879 15.88 15.88 1000 18.41 18.41 1879 17.13 17.132 1434 25.91 41.79 1777 32.71 51.12 3211 29.28 46.413 1356 24.50 66.29 1425 26.23 77.36 2781 25.35 71.774 728 13.15 79.44 639 11.76 89.13 1367 12.46 84.235 500 9.03 88.47 300 5.52 94.64 800 7.29 91.536 244 4.41 92.88 152 2.80 97.44 396 3.61 95.147 177 3.20 96.08 56 1.03 98.47 233 2.12 97.268 85 1.54 97.62 24 0.44 98.91 109 0.99 98.26Total 5403 97.62 5373 98.91 10776 98.26

KEY: NUC � nocturnal urinary control.

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ional survey seemed more likely to get positivenswers from parents even if their children weretill bedwetting. Also, although the retrospectiveurvey might avoid such a disadvantage, it couldesult in a recall bias because the family might notemember the exact time of NUC attainment, espe-ially for older children. Therefore, these two dif-erent surveys were used in the present study in anffort to decrease the bias regarding the prevalencef the attainment of NUC in children. A retrospec-ive study was performed in 3600 Chinese childrenged 6 through 16 years and revealed results simi-ar to those of present study.4

The absence of NUC attainment might be asso-iated with a simultaneous failure of consciousrousal in response to the sensation of bladder full-ess.10 Until today, it has been a widely held beliefhat the children who wet their beds at night areeep sleepers.11,12 In a survey of 1390 school chil-ren, difficult arousal from sleep was noted in 43%f those with bedwetting versus 23% of those with-

TABLE III. Influencing factors o

actorInfants(1–3 yr)

Pres(4–

enderMale 156 1Female 130 1

requency of nocturnal bed wetting*†

�1/p night 411/p night 544–6/p wk 212–3/p wk 491/p wk 28�1/p wk 92 1

ssociated daytime symptoms*†

Yes 28No 258 2

nhabitationRural 164 1Urban 122 1

rousal dysfunction*†

Yes 217 1No 69 1

amily history*†

Yes 18No 268 2

reatment of the children without NUCWait for maturity 145 1Fluid restriction 3Waking to void 120Fluid restriction combined withwaking to void

12

Professional management 6

EY: NUC � nocturnal urinary control.P � 0.05, chi-square test between infant group and preschool group.P � 0.05, chi-square test between infant group and primary school group.P � 0.05, chi-square test among 3 groups.

ut bedwetting.13 In the present study, arousal dif- t

106

culty after nocturnal bedwetting occurred in6.8% of children without NUC, with fewer chil-ren in the preschool and primary school groupshan in the infant group, suggesting that a problemith arousal in children is still an important factor

or young children not attaining NUC.Genetic factors may play a role in the delay ofUC attainment.14 A family history of nocturnal

nuresis proved to be the strongest predictor forhe age of attaining dryness in a study by Feehan etl.8 The present study showed that the prevalencef a positive family history tended to increase withge for the children who had not attained NUC.It is well known that quite a percentage of 1 to

-year-old children do not attain NUC. Accordingo the International Children Continence SocietyICCS), the 1 to 3 year-old children who had notttained NUC could not be treated as if they hadnuresis. Thus, the prevalence of a positive familyistory in these young children is not comparableith the data of enuresis in published reports.14 In

ildren without NUC attainmentol)

Primary School(7–8 yr) Total (%)

Chisquare

PValue

0.363 0.83449 346 (54.92)44 284 (45.08)

53.488 0.000‡

4 60 (9.52)15 97 (15.40)4 37 (5.87)8 81 (12.86)5 60 (9.52)

57 294 (46.83)7.683 0.02‡

17 88 (13.97)76 542 (86.03)

0.075 0.96353 358 (56.83)40 272 (43.17)

19.433 0.000‡

54 421 (66.83)39 209 (33.17)

10.863 0.004‡

15 67 (10.63)78 563 (89.37)

41.886 0.000‡

47 299 (47.46)11 42 (6.67)20 231 (36.67)11 43 (6.83)

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ot attaining NUC was relatively larger than thosef the older age groups, which might be one of theeasons for the relatively lower incidence of a pos-tive family history in the 1 to 3-year old children.owever, research regarding the incidence of aositive family history in very young children is

imited in published reports.In the older age group, especially the school age

roup, however, the incidence of a positive familyistory did increase with age, reaching 17% in thelder age group, very close to the rate reported inublished reports,14 in which the greater incidenceas shown to be relevant to the older age of chil-ren.Bedwetting occurring weekly has been reported

n 3.4% to 40% of 5 to 7-year-old children.15 In005, Butler et al.16 found that 15.5% of children.5 years old wet the bed, and only 17.1% of themet the bed at least twice a week and 8.2% everyight. In our study, approximately 40% of 1 to-year-old children without NUC wet the bedore than twice a week. The episodic severity of

octurnal bedwetting in the infant group was sig-ificantly greater than that of the preschool andrimary school groups, indicating that bedwettingould remit and resolve with age. Furthermore, weound that 13.97% of 1 to 8-year-old children with-ut NUC were nonmonosymptomatic bedwetters.espite extensive reports of treatment for childrenith nonattainment of NUC, our study showed

hat Chinese parents of the 1 to 8-year-old childrenithout attainment of NUC were more likely to

ake the measure of “wait and see” than to seekrofessional help. This is in accordance with thendings of the Korean study.17

The retrospective group had a lower rate of NUCttainment than the cross-sectional group of chil-ren before age 4 and a greater rate after age 5 inhe present study. This difference might have re-ulted from the subjectiveness of the parents whenhey answered the questionnaires in the cross-sec-ional survey. It is understandable that parentsould overestimate before age 4 and underesti-ate after age 5 their child’s ability in attainingUC, because parents know from experience thatchild may acquire NUC with age and it is not

ecessary to seek medical help at a very youngtage, but after age 5, it is totally different. Thearents become worried about delayed NUC at-ainment of their children after 5 years of age, be-ause they believe the sequelae might be more se-ious than the social stigma of not attaining NUC.lso, the difference might be related to poor mem-ry. Some parents might forget the exact date athich their children attained NUC, especially inlder children. Therefore, it was helpful for us toet the true prevalence of NUC attainment with

ncreased age by the combined analysis of two dif- J

ROLOGY 68 (5), 2006

erent epidemiologic investigations. We believe therevalence of attaining NUC is 15% to 50% beforeyears of age, about 90% by age 5, and more than5% by age 8.The data presented in this study have come fromsurvey, not “direct,” but subjective, using infor-ation supplied anonymously by families because

f the possible stigma/embarrassment due to theedwetting their children experience. Therefore,he information collected might not be 100% cor-ect, which could have led to bias. However, thenonymous questionnaire and rather large sampleumbers of the present study should have de-reased the bias.

CONCLUSIONS

Both the cross-sectional and retrospective sur-eys showed that the most important period of at-aining NUC is 2 to 3 years of age. Nearly 90% ofhildren will have attained NUC by 5 years of age.

ACKNOWLEDGMENT. To Professors J. C. Djurhuus and T. M.orgensen, Clinical Institute and Department of Pediatricrology, Aarhus University, Denmark, for their good sugges-

ions in creating the research protocol and revising the manu-cript; and especially to Professor Barry A. Kogan, Depart-ents of Urology and Pediatrics, Albany Medical College,lbany, New York, for his revisions to the manuscript.

REFERENCES1. Morison MJ, Tappin D, and Staines H: “You feel help-

ess, that’s exactly it”: parents’ and young people’s beliefsbout bed-wetting and the implications for practice. J Advurs 31: 1216–1227, 2000.

2. Redsell SA, and Collier J: Bedwetting, behaviour andelf-esteem: a review of the literature. Child Care Health Dev7: 149–162, 2001.

3. Liu X, and Sun Z: Age of attaining nocturnal bladderontrol and adolescent suicidal behavior. J Affect Disord 87:81–289, 2005.

4. Liu X, Sun Z, Uchiyama M, et al: Attaining NUC, noc-urnal enuresis, and behavioral problems in Chinese childrenged 6 through 16 years. J Am Acad Child Adolesc Psychiatry9: 1557–1564, 2000.

5. Hellstrom AL: Influence of potty training habits on dys-unctional bladder in children. Lancet 357: 1292–1293, 2001.

6. Wen JG, Wang QW, Chen Y, et al: An epidemiologicaltudy of primary nocturnal enuresis in Chinese children anddolescents. Eur Urol 49: 1107–1113, 2006.

7. Hjalmas K, Arnold T, Bower W, et al: Nocturnal enure-is: an international evidence based management strategy.Urol 171(6 Pt 2): 2545–2561, 2004.

8. Feehan M, McGee R, Stanton W, et al: A 6 year fol-ow-up of childhood enuresis: prevalence in adolescence andonsequences for mental health. J Paediatr Child Health 26:5–79, 1990.

9. Kawauchi A, Tanaka Y, Yamao Y, et al: Follow-up studyf bedwetting from 3 to 5 years of age. Urology 58: 772–776,001.10. Yeung CK: Nocturnal enuresis (bedwetting). Currpin Urol 13: 337–343, 2003.11. Wolfish NM: Sleep/arousal and enuresis subtypes.

Urol 166: 2444–2447, 2001.

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12. Chandra M, Saharia R, Hill V, et al: Prevalence of diur-al voiding symptoms and difficult arousal from sleep in chil-ren with nocturnal enuresis. J Urol 172: 311–316, 2004.13. Neveus T, Hetta J, Cnattingius S, et al: Depth of sleep

nd sleep habits among enuretic and incontinent children.cta Paediatr 88: 748–752, 1999.14. von Gontard A, Schaumburg H, Hollmann E, et al: The

enetics of enuresis: a review. J Urol 166: 2438–2443, 2001.15. Cochat P, Cochat N, Collet J, et al: Nocturnal enuresis:

ocial aspects and treatment perspectives in France. ScandUrol Nephrol Suppl 163: 15–19, 1994.16. Butler RJ, Golding J, Northstone K, for the ALSPAC

tudy Team: Nocturnal enuresis at 7.5 years old: prevalencend analysis of clinical signs. BJU Int 96: 404–410, 2005.

17. Lee SD, Sohn DW, Lee JZ, et al: An epidemiological studyf enuresis in Korean children. BJU Int 85: 869–873, 2000.

EDITORIAL COMMENTThe authors should be congratulated on completing thisonumental questionnaire review using information con-

erning the attainment of nocturnal urinary control in morehan 14,000 Chinese children surveyed.

It appears that most Chinese children attain nocturnal con-inence when they are 2 to 3 years old, a time at which mostarents in the Western world are happy just to have theirhildren dry during the day. The review also showed that 90%f Chinese children are dry at night by 5 years old when otherecent studies1 found that as many as 15% of children weretill having bedwetting episodes at 7.5 years of age. Further-ore, only 4% of parents seek “professional management” of

heir 7 to 8-year old children’s bedwetting—a point at whichany Western parents are seeking medical evaluation and

reatment for ongoing nocturnal enuresis.Certainly, cultural and societal differences in child rearing

xist in China, with many of these children sleeping witharents as a potential “bedwetting alarm” system, more soci-tal pressures on children and their parents in obtaining or, ateast reporting, early achievement of nocturnal continencend possibly, less access to medical management because ofnancial or geographic constraints (rural versus city environ-ent) compared with the West and other more establishedsian economies.However, using anonymous, parental questionnaire assess-ents to study the attainment of nocturnal continence ob-

ains, at best, subjective evidence about when most childrenecome dry but more likely represents when most parentsish or remember when they think their children have

chieved nocturnal dryness.

108

REFERENCE1. Butler RJ, Golding J, Northstone K, for the ALSPAC

tudy Team: Nocturnal enuresis at 75 years old: prevalencend analysis of clinical signs. BJU Int 96: 404–410, 2005.

Irene McAleer, M.D.Department of Surgery

Division of UrologyUniversity of Connecticut, School of Medicine

Hartford, Connecticut

doi:10.1016/j.urology.2006.08.1104© 2006 ELSEVIER INC.

ALL RIGHTS RESERVED

REPLY BY THE AUTHORSI agree with the comment on our study. The differences in

ultural background may contribute significantly to the differ-nces in the prevalence of bedwetting in children youngerhan 8 years old between China and Western countries. Thathinese children sleep with their parents allows the children

o receive earlier bladder training during the night comparedith children in Western countries. This may play a role in

stablishing the voiding reflex during the night early for Chi-ese children and contribute to the 90% rate of Chinese chil-ren who were dry at night by 5 years of age.To overcome the bias of the investigation, this study was

erformed using both cross-sectional and retrospective sur-eys. Because bedwetting is regarded as shameful, the cross-ectional survey might have resulted in bias owing to the dis-onesty of the parents if their child had not attained NUC. Inontrast, by using the retrospective survey, we hoped to avoiduch social stigma bias because all children had attained NUCt investigation.

Jian Guo Wen, M.D., Ph.D.Pediatric Urodynamic Centre

First Teaching Hospital of Zhengzhou UniversityZhengzhou, Henan, China

doi:10.1016/j.urology.2006.09.022© 2006 ELSEVIER INC.

ALL RIGHTS RESERVED

UROLOGY 68 (5), 2006