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ORIGINAL PAPER
Dieter Baeyens Æ Herbert Roeyers Æ Johan Vande Walle
Piet Hoebeke
Behavioural problems and attention-deficit hyperactivity disorderin children with enuresis: a literature review
Received: 15 November 2004 / Accepted: 29 April 2005 / Published online: 12 July 2005� Springer-Verlag 2005
Abstract Nearly all studies on the co-morbidity betweenenuresis and psychopathology in children suggest anincreased prevalence of behavioural disorders in generaland of attention-deficit hyperactivity disorder (ADHD)in particular. Depending strongly on characteristics ofthe study design, the extent to which this prevalence isincreased fluctuates heavily. In the current literaturereview we found a lack of standardization in the defi-nitions of both enuresis and psychopathology, whichmakes comparison of research findings difficult. A seriesof confounding factors that possibly bias study results isalso covered. Psychopathology in enuresis seems to beassociated with older age, male gender, low socio-eco-nomic status and admission to specialized (university)paediatric clinics. Research that fails to report or tocontrol for these factors will not be able to make gen-eralizations to the total population of enuretic children.It is highly important for paediatricians to be aware ofthe effect of these methodological factors in order toread critically and appreciate the co-morbidity studieson the one hand and to understand better the associa-tion between enuresis and psychopathology on the otherhand. Future research would benefit from diagnosesbased on international diagnostic classification systemsmade within a well-defined sample.
Keywords Enuresis Æ ADHD Æ Behavioural Æ review
Introduction
The relationship between enuresis and behaviouralproblems has been researched extensively for several
decades. Results have been reported that range fromwell-adjusted enuretic children without marked emo-tional, social, or behavioural problems [34] to childrenwith a 4.3-times increase in psychological difficultiescompared with their non-enuretic peers [21]. This varia-tion can be explained by the diversity in conceptualisa-tion of the disorder and in the difference inmethodological design of these studies. In order forstudies and their findings to be assessed at their truevalue, these effects on study results need to be clarified.The aim of this literature review is to determine the rel-evant confounding factors in these studies and to inves-tigate their relative impact in enuresis research focusingon behavioural problems in general and on attention-deficit hyperactivity disorder (ADHD) in particular.
Literature review
In what follows we present a survey of recent studiesthat focus on the relationship between enuresis and bothADHD and other behavioural problems. Epidemiolog-ical studies (Table 1) and clinical studies (Tables 2 and3) are presented separately, since their respective aimsvary considerably. The various variables in these tablesare further discussed.
Diagnosis of enuresis
First of all, the conceptualisation of enuresis is takeninto account. In international diagnostic classificationsystems, such as the international statistical classifica-tion of diseases and related health problems (ICD)-10[35] and diagnostic and statistical manual of mentaldisorders (DSM)-IV-TR [2], enuresis is defined as theinvoluntary voiding of urine in a child of 5 years orolder in whom organic causes are excluded. Bothclassification systems do not agree on the frequency atwhich the wetting problem should be present; a
D. Baeyens (&) Æ H. RoeyersDepartment of Psychology, Developmental Disorders,Faculty of Psychology and Educational Sciences,Ghent University, Henri Dunantlaan 2,9000 Ghent, Belgium
D. Baeyens Æ J. Vande Walle Æ P. HoebekePaediatric Uro-nephrological Centre,Ghent University Hospital, Ghent, Belgium
Eur J Pediatr (2005) 164: 665–672DOI 10.1007/s00431-005-1712-1
Table
1Epidem
iologicalstudiesonenuresisandADHD/behaviouralproblems(N
Enocturnalenuresis,PEprimary
enuresis,SEsecondary
enuresis,PNEprimary
nocturnalenuresis,
HShyperkinetic
syndrome,
extern.externalizingproblems)
Study
Sample
Diagnostics
Instruments
and
inform
ants
Controlenuresis
variables
Control
dem
ographic
variables
Results
Relativerisk
Byrd
etal.,1996[8]
n=10,960
NE:questions
Questionnaire
NE
Age
NE:16.5%
behavioural
problems
Age:
5–17years
Behavioural
problems
Parent
Gender
CuredNE:10.2%
behaviouralproblems
1.62
SES
Feehanet
al.,1990[13]
n=
1,037
Enuresis:DSM-III
Interview,
questionnaire
PE/SE
Age
ADHD:dry
at13years
andenuresisat
11years
>noenuresis
at11years
or13years
–
Age:
3,5,11,13years
ADHD:DSM-III
Parent,child
Gender
ADHD:SE>
PE
Fergussonand
Horw
ood,1994[14]
n=
1,265
Enuresis:questions
Interview,
questionnaire
PE/SE
Age
Enuresisatage11years
and13years:no
increase
inADHD
–
Age:
4months,annual
year1–15
ADHD:DSM-III
Parent,
teacher,child
Gender
Enuresisatage15years:
increase
inADHD
SES
Hirasinget
al.,
1997[17]
n=1,652
NE:questions
Questionnaire
PE/SE
Age
At8–9years:23%
overallproblems
2.3
Age:
8–9and9–10years
Behavioural
problems
Parent
NE
Gender
Atage9–10years:17%
overallproblems
1.7
Norm
group:1%
overallproblems
Liu
etal.,2000[21]
n=
3,344
Enuresis:one
question
Questionnaire
–Age
Enuresis:29.3%
extern.
(parent)
Age:
6–16years
Behavioural
problems
Parent,teacher
Gender
Non-enuretic:
9.3%
extern.
(parent)
3.57
SES
Enuresis:25.5%
extern.
(teacher)
Non-enuretic:
11.1%
extern.
(teacher)
3.28
Moilanen
etal.,
1998[23]
n=
5,603
Enuresis:one
question
Questions
––
Antisocial:never
episode
<sometim
es<weekly
–
Age:
8years
Behavioural
problems
Parent,teacher
Hyperactive:
never
episode
<sometim
es<weekly
666
Table
2Clinicalstudieswithbetween-subject
andwithin-subject
designontheprevalence
ofADHD/behaviouralproblemsin
enureticchildren(D
Ediurnalenuresis,NE
nocturnal
enuresis,PEprimary
enuresis,SEsecondary
enuresis,PNEprimary
nocturnalenuresis,VPvoidingpostponem
ent,UIurgeincontinence,UTIurinary
tract
infection,HShyperkinetic
syndrome,
extern.externalizingproblems)
Study
Sample
Diagnostics
Instruments
and
inform
ants
Setting
Control
enuresis
variables
Control
dem
ographic
variables
Results
Relative
risk
Between-subject
Changet
al.,2002[9]
PNE,n=
93
Enuresis:
‡three
episodes/w
eek
Questionnaire
Paediatric
clinic
PNE
Age
PNE:28%
extern.
Control,n=
131
Behaviouralproblems
Parent,expert
Gender
Control:8%
extern.
3.52
Age:
7–15years
Frimanet
al.,1998[15]
PNE,n=
92
Enuresis:
‡one
episode/week,
over
6months
Questionnaire
Paediatric
clinic
PNE
Age
PNE:32%
behaviour
problem
Clinical,n=
92
Behaviouralproblems
Parent
Gender
Clinic:61%
behaviour
problem
0.52
Control,n=
92
Control:17%
behaviour
problem
1.88
Age:
5–13years
Rey
andHensley,
1995[26]
Clinical,n=
2,325
Enuresis:tw
oquestions
Questionnaire
Mentalhealth
service
community
DE/N
EGender
Hyperactivity
associatedwith
bedwetting
1.66
Control,n=
528
Behaviouralproblems
Parent
Age
Age:
12–16years
SteinhausenandGobel,
1989[28]
Enuresis,n=386
Enuresis:DSM-III-R
ICD
schem
ePsychiatric
clinic
––
Enuresis:4%
HS
Clinical,n=
2,404
HS:IC
D-9
Expert
Clinical:7%
HS
0.61
Age:
6to
‡14years
VanHoeckeet
al.,
2003[30]
Enuresis,n=
154
Enuresis:notspecified
Questionnaire
Paediatric
clinic
-Age
Enuresis:17%
extern.
Control,n=
153
Behaviouralproblems
Parent
Gender
Control:9%
extern.
1.89
Age:
6–12years
SES
Enuresis:11%
inattention
Control:9%
inattention
1.22
Enuresis;14%
hyperactivity
Control:6%
hyperactivity
2.33
Wille
andAnveden,
1995[34]
PNE,n=
14
Enuresis:
‡three
episodes/w
eek
32questions
Paediatric
clinic
PNE
Age
PNE:
median
„antisocial
CuredPNE,n=
15
Behaviouralproblems
Parent
Gender
CuredPNE:
median
„antisocial
1
Control,n=
15
Control:
median
„antisocial
1
Age:
notspecified
Within-subject
Baeyenset
al.,2004[3]
Enuresis,n=
120
Enuresis:nephro-/
urologists
Interview,
questionnaire
Paediatric
clinic
PE/SE
Age
Interview:
ADHD-IA
22.5%
,ADHD-H
YP2.5%
,ADHD-C
OM
15%
–
Age:
6–12years
ADHD:DSM-IV
Parent,teacher
DE/N
EGender
Questionnaire:
36%
extern.(parent),21%
extern.(teacher)
Behaviouralproblems
SES
667
frequency of twice a month under the age of 7 yearsand once a month over the age of 7 years is requiredfor research purposes by ICD-10 [35] and twice a weekby DSM-IV-TR [2]. There is consensus on a minimumduration of at least 3 months for the respective fre-quencies.
These criteria can be criticized, since they fail to dif-ferentiate between phenotypes of enuresis with andwithout lower urinary tract dysfunctions. According tothe terminology of the International Children’s Conti-nence Society (ICCS), enuresis refers to wetting withnormal micturition and without bladder dysfunction butat a socially unacceptable place and time, whereas uri-nary incontinence/wetting usually results from bladderdysfunction such as urge incontinence or dysfunctionalvoiding [18, 24]. Since this classification requires veryspecific data on patient characteristics, very few studieson the relationship between enuresis and psychologicalproblems adopt the ICCS standardization. Nevertheless,available reports suggest that more complex phenotypesof enuresis are associated with a higher prevalence ofICD-10 behavioural disorders than enuresis withoutlower urinary tract dysfunctions [32]. Since the debateon the definition of enuresis and its subtypes is stillongoing, and only DSM and ICD diagnoses are wide-spread in the relevant literature, the term ‘‘enuresis’’ inits broadest sense will be used throughout this review.
Apart from the (pertinent) addition to the interna-tional classification systems made by ICCS criteria, aseries of studies on the relationship between enuresis andbehavioural disorders even fail to meet the non-committal ICD-10 and DSM-IV criteria. As shown inTable 1, in epidemiologic and cohort studies, durationand frequency of signs are ignored, and the presence orabsence of involuntary voiding of urine is not ques-tioned. The assessment of enuresis is solely based onsome questions that are part of an existing question-naire, such as item 108 ‘‘wets the bed’’ of the childbehaviour checklist (CBCL) [1, 26]. Others use a self-constructed questionnaire that retrospectively assessesenuresis among other disorders [8].
These inconsistencies in questioning result in highlyvarying percentages of clinically increased problemscores on parental reports measuring behaviouralproblems; percentages range from 16.5% [8] to 29.0%[21]. In (ADHD) co-morbidity studies, with a cross-sectional design (Tables 2 and 3), the same shortcomingsare observed, seen in the strong diversity in the defini-tion of enuresis that results in a co-occurrence rangebetween 28.6% and 40% [3, 4, 5, 25]. The lack ofstandardization hampers the comparison and interpre-tation of research findings.
Diagnosis of ADHD and other externalizing problems
The same limitations are encountered in studies assess-ing psychological problems and psychiatric disordersassociated with enuresis.T
able
2(C
ontd.)
Study
Sample
Diagnostics
Instruments
and
inform
ants
Setting
Control
enuresis
variables
Control
dem
ographic
variables
Results
Relative
risk
Kodman-Jones
etal.,
2001[19]
Enuresis,n=54
Enuresis:notspecified
Questionnaire
Urologicalclinic
DE/N
E-
ADHD:NE22%,
DEwithoutUTI21%
,DEwithUTI0%
–Age:
8–15years
ADHD:notre-evaluated
Parent
Lettgen
etal.,2002[20]
DE,n=94
Enuresis:IC
CS
Questionnaire
Paediatric
clinic
VP/U
IGender
VP:31%
extern.
–Age:
5–10years
Behaviouralproblems
Parent
Psychiatric
clinic
UI:8%
extern.
VonGontard
etal.,
1998[31]
DE,n=94
Enuresis:IC
CS
Questionnaire
Paediatric
clinic
VP/U
I-
Extern.:VP31%,UI8%
–Age:
5–10years
Expansivedisorders:
ICD-10
Parent,expert
Psychiatric
clinic
Expansive:
VP31%
,UI5%
Behaviouralproblems
VonGontard
etal.,
1999[32]
Enuresis:n=
167
Enuresis:
‡1
episode/week
Questionnaire
Paediatric
clinic
PE/SE
-DE:29%
extern,28%
expansive
–
Age:
5–10years
Expansivedisorders:
ICD-10
Parent,expert
DE/N
ENE:19%
extern,17%
expansive
Behaviouralproblems
VP/U
IPNE:16%
extern,12%
expansive
SNE:25%
extern,32%
expansive
VP:37%
extern,39%
expansive
UI:19%
extern,14%
expansive
Wagner
etal.,1988[33]
Enuresis,n=
134
Enuresis:
‡3episodes/w
eek
Questionnaire
Paediatric
clinic
DE/N
E-
Delinquency:day/night>night
–Age:
5–16years
Behaviouralproblems
Parent
Familypractice
668
The diagnosis of psychiatric disorders follows criteriaset by the international classification systems. Consid-ering ADHD, the DSM-IV-TR [2] demands that thesymptoms of inattention, hyperactivity and impulsivitybe present in at least two different settings (e.g. at homeand at school), the so-called pervasiveness criterion. Thebest way to obtain a valid diagnosis is by using a multi-method (e.g. rating scales as well as diagnostic interview)multi-informant (e.g. parents as well as teachers)assessment of ADHD [16, 29]. Most studies on therelationship between enuresis and ADHD recruitedsubjects from a population of children with ADHD(Table 3). Although the use of DSM criteria is reportedin these studies, the description of instruments andinformants was not mentioned [4, 27].
In spite of this, the co-occurrence of ADHD andenuresis is consistently reported in approximately 30%of patients [4, 5]. Robson et al. [27] worked out that a 6-year-old child with ADHD has 2.7-times more chance ofsuffering co-morbid nocturnal enuresis than its peersand 4.5-times more chance of suffering diurnal enuresis.As far as we know, we were the first to take ADHDsubtypes into account in this area of research [3]. Wereported that the DSM-IV criteria for inattention weremet significantly more than for hyperactivity/impulsivityin children with enuresis.
Contrary to ADHD co-morbidity research, theprevalence of externalizing problems in subjects re-cruited from an enuretic population is relatively welldocumented. Externalizing problems, such as aggres-siveness and disobedience, are strongly associated withADHD symptomatology [12]. The diagnostic criteria forthe description of these psychological problems are notdeveloped. Information gathered from more generalquestionnaires should be sufficient to guarantee a rep-resentative description. Most studies prefer to comparethe number of clinical cases (i.e. cases that cross theclinical cut-off score) between the study groups ratherthan the average group scores [8, 21, 32], which are lessinformative. Nearly all epidemiological (Table 1) andclinical (Tables 2 and 3) studies reveal an increasedprevalence of clinical behavioural problems in enureticchildren, with the relative risk often being up to three-times as high as for non-enuretic controls [9, 21].
Study designs
Prior to the recruitment of subjects, a researcher shouldtake several factors into account that might possiblyinfluence the study results if not controlled for. Theseconfounding factors can be biases by the recruitmentsetting, ignorance of enuresis subtyping, boys-versus-girls ratio, age range and socio-economic status.
Setting
As shown in Tables 2 and 3, most co-morbidity studiesrecruit their subjects from paediatric clinics rather than T
able
3Clinicalstudieswithbetween-subject
designontheprevalence
ofenuresisin
childrenwithADHD
(DE
diurnalenuresis,
NE
nocturnalenuresis,
PE
primary
enuresis,
SE
secondary
enuresis,PNE
primary
nocturnalenuresis,DVSSdysfunctionalvoidingsymptom
survey)
Study
Sample
Diagnostics
Instruments
and
inform
ants
Setting
Controlenuresis
variables
Controldem
ographic
variables
Results
Relative
risk
Bhatiaet
al.,1991[4]
ADHD,n=
112
Enuresis:notmentioned
Questionnaire
Paediatric
clinic
–Age
ADHD:28.6%
enuresis
Controls,n=
112
ADHD:DSM-III
Parent
Gender
Control:5.2%
enuresis
5.5
Age:
3–12years
SES
Biedermanet
al.,
1995[5]
ADHD,n=
140
Enuresis:DSM-III-R
Interview
Paediatric
clinic
PE/SE
Age
ADHD:32%
enuresis
Control,n=
120
ADHD:DSM-III-R
Parent,expert
Psychiatric
clinic
DE/N
EGender
Control:14%
enuresis
2.29
Age:
6–17years
SES
Duel
etal.,2003[11]
ADHD,n=
28
Enuresis:DVSS
questionnaire
Notspecified
Development
centre
DE/N
EGender
Voidingsymptoms:
ADHD
>control
–
Control,n=
22
ADHD:notspecified
Parent,child
Paediatric
clinic
Age:
6–12years
Robsonet
al.,
1997[27]
ADHD,n=
153
Enuresis:3item
questionnaire
Expert
Paediatric
clinic
DE/N
EAge
Atage6:
Control,n=142
ADHD:DSM-III-R
Gender
NE:ADHD
20.9%,
control7.8%
2.7
Age:
6–14years
DE:ADHD
6.5%
,control2.1%
4.5
669
from a primary care sample. This could hamper thegeneralization of the study results to the total popula-tion. In many countries health care consists of severalhierarchically organized departments. Primary care willdeal with a spectrum of common problems that can berecognized and treated rather easily. However, when thesituation is complex to such an extent that it requiresadditional expertise concerning diagnosis or treatment,referral to a more specialized, often university,paediatric or psychiatric, clinic will be appropriate.Consequently, these specialized centres often attracttherapy-resistant patients with increased rates ofco-morbid disorders and problems [31]. In order to givean adequate interpretation to research findings, oneshould always be alert for the kind of setting.
Subtyping of enuresis
Tables 1, 2 and 3 reveal that subtypes of enuresis are notsufficiently taken into account. Enuresis is defined by twocomplementary classification categories. According thedevelopmental path, primary (i.e. at least one wettingepisode in every 6 months) and secondary enuresis (i.e.relapse after 6 months without wetting episodes) can bedistinguished.Depending on the time atwhich thewettingepisodes occur, a child can be diagnosed with nocturnal,diurnal, or combined enuresis. A number of studies sug-gest that these categories should be taken into account.
Concerning the developmental path of enuresis, VonGontard et al. [32] revealed that 32.1% of the childrenwith secondary nocturnal enuresis also meet the criteriaof a co-morbid ICD-10 diagnosis of behaviouraldisorders, compared to only 12.2% of the children withprimary nocturnal enuresis. This significant groupdifference could not be reconfirmed in studies onexternalizing problems on the CBCL [1]. The prevalencerates are 16.3% and 25% for primary and secondarynocturnal enuresis, respectively [32]. As opposed toemotional disorders, behavioural problems are not moreprevalent in diurnal enuresis than in nocturnal enuresis[32].
Gender
Enuresis is more prevalent in boys than in girls, i.e. oddsratio of 1.5 to 2:1 [7, 10], as are behavioural disorderssuch as ADHD, i.e. odds ratio of 4 to 9:1 [2]. Thus, thechance for enuretic boys to have increased problemscores on behavioural rating scales is twice as high as forenuretic girls [8, 15]. Therefore, most published studiescontrol for gender (e.g. [5, 15, 21, 27]).
Age
Most studies in the literature control for age (e.g. [5, 15,21, 27]) since evidence suggests that the older the age at
which the child attains urinary control, the more clini-cally increased the problem scores on rating scales willbe observed, starting from 12.1% in the age range 5–8years, over 22.5% in the age range 9-12 years, to 30.1%in the age range of 13–17 years [8]. Fergusson andHorwood [14] refine this finding by revealing that afterthe age of 10 years, bedwetting is associated with limitedincrease in risk for conduct problems, attention deficit,and anxiety in early adolescence.
Socio-economic status
Enuresis is strongly associated with social disadvantage[28, 29], as is psychopathology such as ADHD [6].Although only a few studies actually control for socio-economic status, it has been postulated that socio-economic status (SES) is a common underlying factor bywhich behavioural problems and enuresis emergesimultaneously [29].
Associations
As the exact nature of the relationship betweenbehavioural problems and enuresis cannot be deter-mined on the basis of the applied research designs,defining associations between conditions is better thanlooking for causal relationships. Nevertheless, moststudies seem to adopt such causal relationships implic-itly, since they refer to effects. By stating that the in-creased prevalence of enuresis in children with ADHD isbest explained by the inhibition deficits of this neuro-developmental disorder, Kodman-Jones et al. [19] stressthat psychological problems have an effect on enuresis.However, Bhatia et al. [4] adopt the reverse effect bysuggesting that ADHD symptomatology could be anexpression of the underlying emotional problems due tofrustration and failure. A second argument for consid-ering psychopathology to be reactive to enuresis is thedecrease in attention problems and externalizing prob-lems once the child has been treated for enuresis [22].Nevertheless, it is not unthinkable that psychiatricsymptoms and enuresis are influenced by a common riskfactor. The studies on male gender and lower SES stressthis option [4, 30]. Maturational delay is another com-mon underlying factor that has previously been sug-gested [14]. Finally, the relationship betweenpsychopathology and enuresis could be based on chance,an option that is not taken into account in researchfindings.
Conclusions
Despite the extensive criticism of conceptualisation andresearch methods, nearly all studies, either epidemio-logical or clinical, consistently reveal an increasedchance of co-morbid behavioural problems and
670
disorders such as ADHD in enuretic children. The lackof standardization of study design and the concisereporting of the study methods makes comparison ofresearch findings difficult. The research topic of thecurrently reviewed studies could best be referred to as(bed)wetting, since most research does not follow thespecific ICCS criteria of enuresis, which require veryspecific data on patients’ characteristics. However, sincethis would be incompatible with the (more broadly de-fined) DSM and ICD diagnosis of enuresis, we used theterm enuresis, in its broadest sense, throughout this re-view. Although the debate on an adequate definition ofenuresis is still fierce and, to date, hardly observable instudy designs on the relationship with psychopathology,there is evidence that more complex phenotypes ofenuresis are associated with a higher prevalence ofADHD and externalizing problems.
In this literature review we have covered a series ofconfounding factors that possibly bias the study resultsand of which nephrologists, urologists, and paediatri-cians should be aware in order to read critically andappreciate the co-morbidity studies. Moreover, it ishighly important to note that most co-morbidity studiesare able to look at only the association between enuresisand behavioural disorders rather than at their (causal)relationship. Longitudinal research and outcome effectstudies could help determine whether there is a causalrelationship between psychopathology and enuresis or ifthe association between both concepts is merely basedon a common risk factor. Either way, future researchwould benefit from diagnoses based on internationaldiagnostic classification systems made within a well-de-fined sample.
Acknowledgements This paper was prepared with the support of adoctoral fellowship awarded to Dieter Baeyens by the Fund forScientific Research, Flanders.
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